|
|
|
Heterogeneity of the tumor immune microenvironment and clinical interventions |
Zheng Jin1,2,3,4, Qin Zhou1,2,5, Jia-Nan Cheng1,2( ), Qingzhu Jia1,2(), Bo Zhu1,2() |
1. Department of Oncology, Xinqiao Hospital, Army Medical University, Chongqing 400037, China
2. Key Laboratory of Tumor Immunotherapy, Chongqing 400037, China
3. Research Institute, GloriousMed Clinical Laboratory (Shanghai) Co. Ltd., Shanghai 201318, China
4. Institute of Life Sciences, Chongqing Medical University, Chongqing 400016, China
5. School of Pharmacy and Bioengineering, Chongqing University of Technology, Chongqing 400054, China |
|
|
|
|
Abstract The tumor immune microenvironment (TIME) is broadly composed of various immune cells, and its heterogeneity is characterized by both immune cells and stromal cells. During the course of tumor formation and progression and anti-tumor treatment, the composition of the TIME becomes heterogeneous. Such immunological heterogeneity is not only present between populations but also exists on temporal and spatial scales. Owing to the existence of TIME, clinical outcomes can differ when a similar treatment strategy is provided to patients. Therefore, a comprehensive assessment of TIME heterogeneity is essential for developing precise and effective therapies. Facilitated by advanced technologies, it is possible to understand the complexity and diversity of the TIME and its influence on therapy responses. In this review, we discuss the potential reasons for TIME heterogeneity and the current approaches used to explore it. We also summarize clinical intervention strategies based on associated mechanisms or targets to control immunological heterogeneity.
|
| Keywords
tumor immune heterogeneity
clinical intervention
tumor microenvironment
|
|
Corresponding Author(s):
Jia-Nan Cheng,Qingzhu Jia,Bo Zhu
|
|
Just Accepted Date: 08 August 2023
Online First Date: 13 September 2023
Issue Date: 12 October 2023
|
|
| 1 |
M Binnewies, EW Roberts, K Kersten, V Chan, DF Fearon, M Merad, LM Coussens, DI Gabrilovich, S Ostrand-Rosenberg, CC Hedrick, RH Vonderheide, MJ Pittet, RK Jain, W Zou, TK Howcroft, EC Woodhouse, RA Weinberg, MF Krummel. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med 2018; 24(5): 541–550
https://doi.org/10.1038/s41591-018-0014-x
|
| 2 |
F Galli, JV Aguilera, B Palermo, SN Markovic, P Nisticò, A Signore. Relevance of immune cell and tumor microenvironment imaging in the new era of immunotherapy. J Exp Clin Cancer Res 2020; 39(1): 89
https://doi.org/10.1186/s13046-020-01586-y
|
| 3 |
M Yarchoan, A Hopkins, EM Jaffee. Tumor mutational burden and response rate to PD-1 inhibition. N Engl J Med 2017; 377(25): 2500–2501
https://doi.org/10.1056/NEJMc1713444
|
| 4 |
M Yarchoan, LA Albacker, AC Hopkins, M Montesion, K Murugesan, TT Vithayathil, N Zaidi, NS Azad, DA Laheru, GM Frampton, EM Jaffee. PD-L1 expression and tumor mutational burden are independent biomarkers in most cancers. JCI Insight 2019; 4(6): e126908
https://doi.org/10.1172/jci.insight.126908
|
| 5 |
X Ren, L Zhang, Y Zhang, Z Li, N Siemers, Z Zhang. Insights gained from single-cell analysis of immune cells in the tumor microenvironment. Annu Rev Immunol 2021; 39(1): 583–609
https://doi.org/10.1146/annurev-immunol-110519-071134
|
| 6 |
TF Gajewski, H Schreiber, YX Fu. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013; 14(10): 1014–1022
https://doi.org/10.1038/ni.2703
|
| 7 |
Q Jia, H Chu, Z Jin, H Long, B Zhu. High-throughput single-сell sequencing in cancer research. Signal Transduct Target Ther 2022; 7(1): 145
https://doi.org/10.1038/s41392-022-00990-4
|
| 8 |
I Dagogo-Jack, AT Shaw. Tumour heterogeneity and resistance to cancer therapies. Nat Rev Clin Oncol 2018; 15(2): 81–94
https://doi.org/10.1038/nrclinonc.2017.166
|
| 9 |
K Isomoto, K Haratani, H Hayashi, S Shimizu, S Tomida, T Niwa, T Yokoyama, Y Fukuda, Y Chiba, R Kato, J Tanizaki, K Tanaka, M Takeda, T Ogura, T Ishida, A Ito, K Nakagawa. Impact of EGFR-TKI treatment on the tumor immune microenvironment in EGFR mutation-positive non-small cell lung cancer. Clin Cancer Res 2020; 26(8): 2037–2046
https://doi.org/10.1158/1078-0432.CCR-19-2027
|
| 10 |
M Wang, J Zhao, L Zhang, F Wei, Y Lian, Y Wu, Z Gong, S Zhang, J Zhou, K Cao, X Li, W Xiong, G Li, Z Zeng, C Guo. Role of tumor microenvironment in tumorigenesis. J Cancer 2017; 8(5): 761–773
https://doi.org/10.7150/jca.17648
|
| 11 |
Z Lamplugh, Y Fan. Vascular microenvironment, tumor immunity and immunotherapy. Front Immunol 2021; 12: 811485
https://doi.org/10.3389/fimmu.2021.811485
|
| 12 |
SP Shah, A Roth, R Goya, A Oloumi, G Ha, Y Zhao, G Turashvili, J Ding, K Tse, G Haffari, A Bashashati, LM Prentice, J Khattra, A Burleigh, D Yap, V Bernard, A McPherson, K Shumansky, A Crisan, R Giuliany, A Heravi-Moussavi, J Rosner, D Lai, I Birol, R Varhol, A Tam, N Dhalla, T Zeng, K Ma, SK Chan, M Griffith, A Moradian, SW Cheng, GB Morin, P Watson, K Gelmon, S Chia, SF Chin, C Curtis, OM Rueda, PD Pharoah, S Damaraju, J Mackey, K Hoon, T Harkins, V Tadigotla, M Sigaroudinia, P Gascard, T Tlsty, JF Costello, IM Meyer, CJ Eaves, WW Wasserman, S Jones, D Huntsman, M Hirst, C Caldas, MA Marra, S Aparicio. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012; 486(7403): 395–399
https://doi.org/10.1038/nature10933
|
| 13 |
D Shibata. Cancer. Heterogeneity and tumor history. Science 2012; 336(6079): 304–305
https://doi.org/10.1126/science.1222361
|
| 14 |
D Buob, H Fauvel, MP Buisine, S Truant, C Mariette, N Porchet, A Wacrenier, MC Copin, E Leteurtre. The complex intratumoral heterogeneity of colon cancer highlighted by laser microdissection. Dig Dis Sci 2012; 57(5): 1271–1280
https://doi.org/10.1007/s10620-011-2023-1
|
| 15 |
M Gerlinger, AJ Rowan, S Horswell, M Math, J Larkin, D Endesfelder, E Gronroos, P Martinez, N Matthews, A Stewart, P Tarpey, I Varela, B Phillimore, S Begum, NQ McDonald, A Butler, D Jones, K Raine, C Latimer, CR Santos, M Nohadani, AC Eklund, B Spencer-Dene, G Clark, L Pickering, G Stamp, M Gore, Z Szallasi, J Downward, PA Futreal, C Swanton. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012; 366(10): 883–892
https://doi.org/10.1056/NEJMoa1113205
|
| 16 |
N McGranahan, C Swanton. Clonal heterogeneity and tumor evolution: past, present, and the future. Cell 2017; 168(4): 613–628
https://doi.org/10.1016/j.cell.2017.01.018
|
| 17 |
RA Burrell, N McGranahan, J Bartek, C Swanton. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 2013; 501(7467): 338–345
https://doi.org/10.1038/nature12625
|
| 18 |
Q Jia, A Wang, Y Yuan, B Zhu, H Long. Heterogeneity of the tumor immune microenvironment and its clinical relevance. Exp Hematol Oncol 2022; 11(1): 24
https://doi.org/10.1186/s40164-022-00277-y
|
| 19 |
BS Shastry. SNPs: impact on gene function and phenotype. Methods Mol Biol 2009; 578: 3–22
https://doi.org/10.1007/978-1-60327-411-1_1
|
| 20 |
T Lifsted, T Le Voyer, M Williams, W Muller, A Klein-Szanto, KH Buetow, KW Hunter. Identification of inbred mouse strains harboring genetic modifiers of mammary tumor age of onset and metastatic progression. Int J Cancer 1998; 77(4): 640–644
https://doi.org/10.1002/(SICI)1097-0215(19980812)77:4<640::AID-IJC26>3.0.CO;2-8
|
| 21 |
SM Hsieh, NA Lintell, KW Hunter. Germline polymorphisms are potential metastasis risk and prognosis markers in breast cancer. Breast Dis 2007; 26(1): 157–162
https://doi.org/10.3233/BD-2007-26114
|
| 22 |
SM Hsieh, MP Look, AM Sieuwerts, JA Foekens, KW Hunter. Distinct inherited metastasis susceptibility exists for different breast cancer subtypes: a prognosis study. Breast Cancer Res 2009; 11(5): R75
https://doi.org/10.1186/bcr2412
|
| 23 |
J Peng, BF Sun, CY Chen, JY Zhou, YS Chen, H Chen, L Liu, D Huang, J Jiang, GS Cui, Y Yang, W Wang, D Guo, M Dai, J Guo, T Zhang, Q Liao, Y Liu, YL Zhao, DL Han, Y Zhao, YG Yang, W Wu. Single-cell RNA-seq highlights intra-tumoral heterogeneity and malignant progression in pancreatic ductal adenocarcinoma. Cell Res 2019; 29(9): 725–738
https://doi.org/10.1038/s41422-019-0195-y
|
| 24 |
R Rosenthal, EL Cadieux, R Salgado, MA Bakir, DA Moore, CT Hiley, T Lund, M Tanić, JL Reading, K Joshi, JY Henry, E Ghorani, GA Wilson, NJ Birkbak, M Jamal-Hanjani, S Veeriah, Z Szallasi, S Loi, MD Hellmann, A Feber, B Chain, J Herrero, SA Quezada, J Demeulemeester, Loo P Van, S Beck, N McGranahan, C; TRACERx consortium Swanton. Neoantigen-directed immune escape in lung cancer evolution. Nature 2019; 567(7749): 479–485
https://doi.org/10.1038/s41586-019-1032-7
|
| 25 |
MJ Aryee, W Liu, JC Engelmann, P Nuhn, M Gurel, MC Haffner, D Esopi, RA Irizarry, RH Getzenberg, WG Nelson, J Luo, J Xu, WB Isaacs, GS Bova, S Yegnasubramanian. DNA methylation alterations exhibit intraindividual stability and interindividual heterogeneity in prostate cancer metastases. Sci Transl Med 2013; 5(169): 169ra10
https://doi.org/10.1126/scitranslmed.3005211
|
| 26 |
T Mazor, A Pankov, BE Johnson, C Hong, EG Hamilton, RJA Bell, IV Smirnov, GF Reis, JJ Phillips, MJ Barnes, A Idbaih, A Alentorn, JJ Kloezeman, MLM Lamfers, AW Bollen, BS Taylor, AM Molinaro, AB Olshen, SM Chang, JS Song, JF Costello. DNA methylation and somatic mutations converge on the cell cycle and define similar evolutionary histories in brain tumors. Cancer Cell 2015; 28(3): 307–317
https://doi.org/10.1016/j.ccell.2015.07.012
|
| 27 |
JJ Hao, DC Lin, HQ Dinh, A Mayakonda, YY Jiang, C Chang, Y Jiang, CC Lu, ZZ Shi, X Xu, Y Zhang, Y Cai, JW Wang, QM Zhan, WQ Wei, BP Berman, MR Wang, HP Koeffler. Spatial intratumoral heterogeneity and temporal clonal evolution in esophageal squamous cell carcinoma. Nat Genet 2016; 48(12): 1500–1507
https://doi.org/10.1038/ng.3683
|
| 28 |
WA Flavahan, E Gaskell, BE Bernstein. Epigenetic plasticity and the hallmarks of cancer. Science 2017; 357(6348): eaal2380
https://doi.org/10.1126/science.aal2380
|
| 29 |
AG Deshwar, S Vembu, CK Yung, GH Jang, L Stein, Q Morris. PhyloWGS: reconstructing subclonal composition and evolution from whole-genome sequencing of tumors. Genome Biol 2015; 16(1): 35
https://doi.org/10.1186/s13059-015-0602-8
|
| 30 |
DK Patten, G Corleone, B Győrffy, Y Perone, N Slaven, I Barozzi, E Erdős, A Saiakhova, K Goddard, A Vingiani, S Shousha, LS Pongor, DJ Hadjiminas, G Schiavon, P Barry, C Palmieri, RC Coombes, P Scacheri, G Pruneri, L Magnani. Enhancer mapping uncovers phenotypic heterogeneity and evolution in patients with luminal breast cancer. Nat Med 2018; 24(9): 1469–1480
https://doi.org/10.1038/s41591-018-0091-x
|
| 31 |
Z Yang, B Zhang, D Li, M Lv, C Huang, GX Shen, B Huang. Mast cells mobilize myeloid-derived suppressor cells and Treg cells in tumor microenvironment via IL-17 pathway in murine hepatocarcinoma model. PLoS One 2010; 5(1): e8922
https://doi.org/10.1371/journal.pone.0008922
|
| 32 |
S Ostrand-Rosenberg, P Sinha, DW Beury, VK Clements. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol 2012; 22(4): 275–281
https://doi.org/10.1016/j.semcancer.2012.01.011
|
| 33 |
JL Yu, JW Rak, P Carmeliet, A Nagy, RS Kerbel, BL Coomber. Heterogeneous vascular dependence of tumor cell populations. Am J Pathol 2001; 158(4): 1325–1334
https://doi.org/10.1016/S0002-9440(10)64083-7
|
| 34 |
E Ullrich, M Bonmort, G Mignot, G Kroemer, L Zitvogel. Tumor stress, cell death and the ensuing immune response. Cell Death Differ 2008; 15(1): 21–28
https://doi.org/10.1038/sj.cdd.4402266
|
| 35 |
Y Bian, W Li, DM Kremer, P Sajjakulnukit, S Li, J Crespo, ZC Nwosu, L Zhang, A Czerwonka, A Pawłowska, H Xia, J Li, P Liao, J Yu, L Vatan, W Szeliga, S Wei, S Grove, JR Liu, K McLean, M Cieslik, AM Chinnaiyan, W Zgodziński, G Wallner, I Wertel, K Okła, I Kryczek, CA Lyssiotis, W Zou. Cancer SLC43A2 alters T cell methionine metabolism and histone methylation. Nature 2020; 585(7824): 277–282
https://doi.org/10.1038/s41586-020-2682-1
|
| 36 |
KE Yost, AT Satpathy, DK Wells, Y Qi, C Wang, R Kageyama, KL McNamara, JM Granja, KY Sarin, RA Brown, RK Gupta, C Curtis, SL Bucktrout, MM Davis, ALS Chang, HY Chang. Clonal replacement of tumor-specific T cells following PD-1 blockade. Nat Med 2019; 25(8): 1251–1259
https://doi.org/10.1038/s41591-019-0522-3
|
| 37 |
L Peng, Y Xiong, R Wang, L Xiang, H Zhou, H Gu. Identification of a subpopulation of long-term tumor-initiating cells in colon cancer. Biosci Rep 2020; 40(8): BSR20200437
https://doi.org/10.1042/BSR20200437
|
| 38 |
Y Hüsemann, JB Geigl, F Schubert, P Musiani, M Meyer, E Burghart, G Forni, R Eils, T Fehm, G Riethmüller, CA Klein. Systemic spread is an early step in breast cancer. Cancer Cell 2008; 13(1): 58–68
https://doi.org/10.1016/j.ccr.2007.12.003
|
| 39 |
V Bernard, A Semaan, J Huang, FA San Lucas, FC Mulu, BM Stephens, PA Guerrero, Y Huang, J Zhao, N Kamyabi, S Sen, PA Scheet, CM Taniguchi, MP Kim, CW Tzeng, MH Katz, AD Singhi, A Maitra, HA Alvarez. Single-cell transcriptomics of pancreatic cancer precursors demonstrates epithelial and microenvironmental heterogeneity as an early event in neoplastic progression. Clin Cancer Res 2019; 25(7): 2194–2205
https://doi.org/10.1158/1078-0432.CCR-18-1955
|
| 40 |
X Wu, PA Northcott, A Dubuc, AJ Dupuy, DJ Shih, H Witt, S Croul, E Bouffet, DW Fults, CG Eberhart, L Garzia, T Van Meter, D Zagzag, N Jabado, J Schwartzentruber, J Majewski, TE Scheetz, SM Pfister, A Korshunov, XN Li, SW Scherer, YJ Cho, K Akagi, TJ MacDonald, J Koster, MG McCabe, AL Sarver, VP Collins, WA Weiss, DA Largaespada, LS Collier, MD Taylor. Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature 2012; 482(7386): 529–533
https://doi.org/10.1038/nature10825
|
| 41 |
S Yachida, S Jones, I Bozic, T Antal, R Leary, B Fu, M Kamiyama, RH Hruban, JR Eshleman, MA Nowak, VE Velculescu, KW Kinzler, B Vogelstein, CA Iacobuzio-Donahue. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010; 467(7319): 1114–1117
https://doi.org/10.1038/nature09515
|
| 42 |
W Liu, S Laitinen, S Khan, M Vihinen, J Kowalski, G Yu, L Chen, CM Ewing, MA Eisenberger, MA Carducci, WG Nelson, S Yegnasubramanian, J Luo, Y Wang, J Xu, WB Isaacs, T Visakorpi, GS Bova. Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat Med 2009; 15(5): 559–565
https://doi.org/10.1038/nm.1944
|
| 43 |
L Zhang, X Yu, L Zheng, Y Zhang, Y Li, Q Fang, R Gao, B Kang, Q Zhang, JY Huang, H Konno, X Guo, Y Ye, S Gao, S Wang, X Hu, X Ren, Z Shen, W Ouyang, Z Zhang. Lineage tracking reveals dynamic relationships of T cells in colorectal cancer. Nature 2018; 564(7735): 268–272
https://doi.org/10.1038/s41586-018-0694-x
|
| 44 |
B Izar, I Tirosh, EH Stover, I Wakiro, MS Cuoco, I Alter, C Rodman, R Leeson, MJ Su, P Shah, M Iwanicki, SR Walker, A Kanodia, JC Melms, S Mei, JR Lin, CBM Porter, M Slyper, J Waldman, L Jerby-Arnon, O Ashenberg, TJ Brinker, C Mills, M Rogava, S Vigneau, PK Sorger, LA Garraway, PA Konstantinopoulos, JF Liu, U Matulonis, BE Johnson, O Rozenblatt-Rosen, A Rotem, A Regev. A single-cell landscape of high-grade serous ovarian cancer. Nat Med 2020; 26(8): 1271–1279
https://doi.org/10.1038/s41591-020-0926-0
|
| 45 |
B Winterhoff, S Talukdar, Z Chang, J Wang, TK Starr. Single-cell sequencing in ovarian cancer: a new frontier in precision medicine. Curr Opin Obstet Gynecol 2019; 31(1): 49–55
https://doi.org/10.1097/GCO.0000000000000516
|
| 46 |
MC Asselin, JP O’Connor, R Boellaard, NA Thacker, A Jackson. Quantifying heterogeneity in human tumours using MRI and PET. Eur J Cancer 2012; 48(4): 447–455
https://doi.org/10.1016/j.ejca.2011.12.025
|
| 47 |
E Berglund, J Maaskola, N Schultz, S Friedrich, M Marklund, J Bergenstråhle, F Tarish, A Tanoglidi, S Vickovic, L Larsson, F Salmén, C Ogris, K Wallenborg, J Lagergren, P Ståhl, E Sonnhammer, T Helleday, J Lundeberg. Spatial maps of prostate cancer transcriptomes reveal an unexplored landscape of heterogeneity. Nat Commun 2018; 9(1): 2419
https://doi.org/10.1038/s41467-018-04724-5
|
| 48 |
R Moncada, D Barkley, F Wagner, M Chiodin, JC Devlin, M Baron, CH Hajdu, DM Simeone, I Yanai. Integrating microarray-based spatial transcriptomics and single-cell RNA-seq reveals tissue architecture in pancreatic ductal adenocarcinomas. Nat Biotechnol 2020; 38(3): 333–342
https://doi.org/10.1038/s41587-019-0392-8
|
| 49 |
AR Brannon, E Vakiani, BE Sylvester, SN Scott, G McDermott, RH Shah, K Kania, A Viale, DM Oschwald, V Vacic, AK Emde, A Cercek, R Yaeger, NE Kemeny, LB Saltz, J Shia, MI D’Angelica, MR Weiser, DB Solit, MF Berger. Comparative sequencing analysis reveals high genomic concordance between matched primary and metastatic colorectal cancer lesions. Genome Biol 2014; 15(8): 454
https://doi.org/10.1186/s13059-014-0454-7
|
| 50 |
J Galon, A Costes, F Sanchez-Cabo, A Kirilovsky, B Mlecnik, C Lagorce-Pagès, M Tosolini, M Camus, A Berger, P Wind, F Zinzindohoué, P Bruneval, PH Cugnenc, Z Trajanoski, WH Fridman, F Pagès. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313(5795): 1960–1964
https://doi.org/10.1126/science.1129139
|
| 51 |
AL Ji, AJ Rubin, K Thrane, S Jiang, DL Reynolds, RM Meyers, MG Guo, BM George, A Mollbrink, J Bergenstråhle, L Larsson, Y Bai, B Zhu, A Bhaduri, JM Meyers, X Rovira-Clavé, ST Hollmig, SZ Aasi, GP Nolan, J Lundeberg, PA Khavari. Multimodal analysis of composition and spatial architecture in human squamous cell carcinoma. Cell 2020; 182(2): 497–514.e22
https://doi.org/10.1016/j.cell.2020.05.039
|
| 52 |
L Zhang, Y Zhao, Y Dai, JN Cheng, Z Gong, Y Feng, C Sun, Q Jia, B Zhu. Immune landscape of colorectal cancer tumor microenvironment from different primary tumor location. Front Immunol 2018; 9: 1578
https://doi.org/10.3389/fimmu.2018.01578
|
| 53 |
DA Barbie, P Tamayo, JS Boehm, SY Kim, SE Moody, IF Dunn, AC Schinzel, P Sandy, E Meylan, C Scholl, S Fröhling, EM Chan, ML Sos, K Michel, C Mermel, SJ Silver, BA Weir, JH Reiling, Q Sheng, PB Gupta, RC Wadlow, H Le, S Hoersch, BS Wittner, S Ramaswamy, DM Livingston, DM Sabatini, M Meyerson, RK Thomas, ES Lander, JP Mesirov, DE Root, DG Gilliland, T Jacks, WC Hahn. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 2009; 462(7269): 108–112
https://doi.org/10.1038/nature08460
|
| 54 |
M Angelova, P Charoentong, H Hackl, ML Fischer, R Snajder, AM Krogsdam, MJ Waldner, G Bindea, B Mlecnik, J Galon, Z Trajanoski. Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy. Genome Biol 2015; 16(1): 64
https://doi.org/10.1186/s13059-015-0620-6
|
| 55 |
R Govindan, L Ding, M Griffith, J Subramanian, ND Dees, KL Kanchi, CA Maher, R Fulton, L Fulton, J Wallis, K Chen, J Walker, S McDonald, R Bose, D Ornitz, D Xiong, M You, DJ Dooling, M Watson, ER Mardis, RK Wilson. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 2012; 150(6): 1121–1134
https://doi.org/10.1016/j.cell.2012.08.024
|
| 56 |
S Ogino, JA Nowak, T Hamada, AI Phipps, U Peters, DA Jr Milner, EL Giovannucci, R Nishihara, M Giannakis, WS Garrett, M Song. Integrative analysis of exogenous, endogenous, tumour and immune factors for precision medicine. Gut 2018; 67(6): 1168–1180
https://doi.org/10.1136/gutjnl-2017-315537
|
| 57 |
K Inamura, T Hamada, S Bullman, T Ugai, S Yachida, S Ogino. Cancer as microenvironmental, systemic and environmental diseases: opportunity for transdisciplinary microbiomics science. Gut 2022; 71: 2107–2122
https://doi.org/10.1136/gutjnl-2022-327209
|
| 58 |
Y Cao, R Nishihara, ZR Qian, M Song, K Mima, K Inamura, JA Nowak, DA Drew, P Lochhead, K Nosho, T Morikawa, X Zhang, K Wu, M Wang, WS Garrett, EL Giovannucci, CS Fuchs, AT Chan, S Ogino. Regular aspirin use associates with lower risk of colorectal cancers with low numbers of tumor-infiltrating lymphocytes. Gastroenterology 2016; 151(5): 879–892.e4
https://doi.org/10.1053/j.gastro.2016.07.030
|
| 59 |
A Hanyuda, S Ogino, ZR Qian, R Nishihara, M Song, K Mima, K Inamura, Y Masugi, K Wu, JA Meyerhardt, AT Chan, CS Fuchs, EL Giovannucci, Y Cao. Body mass index and risk of colorectal cancer according to tumor lymphocytic infiltrate. Int J Cancer 2016; 139(4): 854–868
https://doi.org/10.1002/ijc.30122
|
| 60 |
S Ogino, JA Nowak, T Hamada, DA Jr Milner, R Nishihara. Insights into pathogenic interactions among environment, host, and tumor at the crossroads of molecular pathology and epidemiology. Annu Rev Pathol 2019; 14(1): 83–103
https://doi.org/10.1146/annurev-pathmechdis-012418-012818
|
| 61 |
N Akimoto, T Ugai, R Zhong, T Hamada, K Fujiyoshi, M Giannakis, K Wu, Y Cao, K Ng, S Ogino. Rising incidence of early-onset colorectal cancer—a call to action. Nat Rev Clin Oncol 2021; 18(4): 230–243
https://doi.org/10.1038/s41571-020-00445-1
|
| 62 |
S Ogino, AT Chan, CS Fuchs, E Giovannucci. Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut 2011; 60(3): 397–411
https://doi.org/10.1136/gut.2010.217182
|
| 63 |
T Ugai, L Liu, FK Tabung, T Hamada, BW Langworthy, N Akimoto, K Haruki, Y Takashima, K Okadome, H Kawamura, M Zhao, SMM Kahaki, JN Glickman, JK Lennerz, X Zhang, AT Chan, CS Fuchs, M Song, M Wang, KH Yu, M Giannakis, JA Nowak, JA Meyerhardt, K Wu, S Ogino, EL Giovannucci. Prognostic role of inflammatory diets in colorectal cancer overall and in strata of tumor-infiltrating lymphocyte levels. Clin Transl Med 2022; 12(11): e1114
https://doi.org/10.1002/ctm2.1114
|
| 64 |
F Wang, T Ugai, K Haruki, Y Wan, N Akimoto, K Arima, R Zhong, TS Twombly, K Wu, K Yin, AT Chan, M Giannakis, JA Nowak, JA Meyerhardt, L Liang, M Song, SA Smith-Warner, X Zhang, EL Giovannucci, WC Willett, S Ogino. Healthy and unhealthy plant-based diets in relation to the incidence of colorectal cancer overall and by molecular subtypes. Clin Transl Med 2022; 12(8): e893
https://doi.org/10.1002/ctm2.893
|
| 65 |
B Lee, J Lee, MY Woo, MJ Lee, HJ Shin, K Kim, S Park. Modulation of the gut microbiota alters the tumour-suppressive efficacy of Tim-3 pathway blockade in a bacterial species- and host factor-dependent manner. Microorganisms 2020; 8(9): 1395
https://doi.org/10.3390/microorganisms8091395
|
| 66 |
EN Baruch, I Youngster, G Ben-Betzalel, R Ortenberg, A Lahat, L Katz, K Adler, D Dick-Necula, S Raskin, N Bloch, D Rotin, L Anafi, C Avivi, J Melnichenko, Y Steinberg-Silman, R Mamtani, H Harati, N Asher, R Shapira-Frommer, T Brosh-Nissimov, Y Eshet, S Ben-Simon, O Ziv, MAW Khan, M Amit, NJ Ajami, I Barshack, J Schachter, JA Wargo, O Koren, G Markel, B Boursi. Fecal microbiota transplant promotes response in immunotherapy-refractory melanoma patients. Science 2021; 371(6529): 602–609
https://doi.org/10.1126/science.abb5920
|
| 67 |
D Davar, AK Dzutsev, JA McCulloch, RR Rodrigues, JM Chauvin, RM Morrison, RN Deblasio, C Menna, Q Ding, O Pagliano, B Zidi, S Zhang, JH Badger, M Vetizou, AM Cole, MR Fernandes, S Prescott, RGF Costa, AK Balaji, A Morgun, I Vujkovic-Cvijin, H Wang, AA Borhani, MB Schwartz, HM Dubner, SJ Ernst, A Rose, YG Najjar, Y Belkaid, JM Kirkwood, G Trinchieri, HM Zarour. Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science 2021; 371(6529): 595–602
https://doi.org/10.1126/science.abf3363
|
| 68 |
AH Cheung, C Chow, KF To. Latest development of liquid biopsy. J Thorac Dis 2018; 10(S14 Suppl 14): S1645–S1651
https://doi.org/10.21037/jtd.2018.04.68
|
| 69 |
L Giannopoulou, M Zavridou, S Kasimir-Bauer, ES Lianidou. Liquid biopsy in ovarian cancer: the potential of circulating miRNAs and exosomes. Transl Res 2019; 205: 77–91
https://doi.org/10.1016/j.trsl.2018.10.003
|
| 70 |
E Crowley, F Di Nicolantonio, F Loupakis, A Bardelli. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol 2013; 10(8): 472–484
https://doi.org/10.1038/nrclinonc.2013.110
|
| 71 |
HT Chan, S Nagayama, M Otaki, YM Chin, Y Fukunaga, M Ueno, Y Nakamura, SK Low. Tumor-informed or tumor-agnostic circulating tumor DNA as a biomarker for risk of recurrence in resected colorectal cancer patients. Front Oncol 2023; 12: 1055968
https://doi.org/10.3389/fonc.2022.1055968
|
| 72 |
AP Liu, PA Northcott, GW Robinson, A Gajjar. Circulating tumor DNA profiling for childhood brain tumors: technical challenges and evidence for utility. Lab Invest 2022; 102(2): 134–142
https://doi.org/10.1038/s41374-021-00719-x
|
| 73 |
K Pantel, C Alix-Panabières. Real-time liquid biopsy in cancer patients: fact or fiction?. Cancer Res 2013; 73(21): 6384–6388
https://doi.org/10.1158/0008-5472.CAN-13-2030
|
| 74 |
M Elazezy, SA Joosse. Techniques of using circulating tumor DNA as a liquid biopsy component in cancer management. Comput Struct Biotechnol J 2018; 16: 370–378
https://doi.org/10.1016/j.csbj.2018.10.002
|
| 75 |
CP Paweletz, AG Sacher, CK Raymond, RS Alden, A O’Connell, SL Mach, Y Kuang, L Gandhi, P Kirschmeier, JM English, LP Lim, PA Jänne, GR Oxnard. Bias-corrected targeted next-generation sequencing for rapid, multiplexed detection of actionable alterations in cell-free DNA from advanced lung cancer patients. Clin Cancer Res 2016; 22(4): 915–922
https://doi.org/10.1158/1078-0432.CCR-15-1627-T
|
| 76 |
J Rodríguez, J Avila, C Rolfo, A Ruíz-Patiño, A Russo, L Ricaurte, C Ordóñez-Reyes, O Arrieta, ZL Zatarain-Barrón, G Recondo, AF Cardona. When tissue is an issue the liquid biopsy is nonissue: a review. Oncol Ther 2021; 9(1): 89–110
https://doi.org/10.1007/s40487-021-00144-6
|
| 77 |
SQ Wong, A Fellowes, K Doig, J Ellul, TJ Bosma, D Irwin, R Vedururu, AY Tan, J Weiss, KS Chan, M Lucas, DM Thomas, A Dobrovic, JP Parisot, SB Fox. Assessing the clinical value of targeted massively parallel sequencing in a longitudinal, prospective population-based study of cancer patients. Br J Cancer 2015; 112(8): 1411–1420
https://doi.org/10.1038/bjc.2015.80
|
| 78 |
DK Dang, BH Park. Circulating tumor DNA: current challenges for clinical utility. J Clin Invest 2022; 132(12): e154941
https://doi.org/10.1172/JCI154941
|
| 79 |
J Uchida, K Kato, Y Kukita, T Kumagai, K Nishino, H Daga, I Nagatomo, T Inoue, M Kimura, S Oba, Y Ito, K Takeda, F Imamura. Diagnostic accuracy of noninvasive genotyping of EGFR in lung cancer patients by deep sequencing of plasma cell-free DNA. Clin Chem 2015; 61(9): 1191–1196
https://doi.org/10.1373/clinchem.2015.241414
|
| 80 |
C Alix-Panabières, K Pantel. Liquid biopsy: from discovery to clinical application. Cancer Discov 2021; 11(4): 858–873
https://doi.org/10.1158/2159-8290.CD-20-1311
|
| 81 |
C Alix-Panabières, K Pantel. Clinical applications of circulating tumor cells and circulating tumor dna as liquid biopsy. Cancer Discov 2016; 6(5): 479–491
https://doi.org/10.1158/2159-8290.CD-15-1483
|
| 82 |
Q Jia, L Chiu, S Wu, J Bai, L Peng, L Zheng, R Zang, X Li, B Yuan, Y Gao, D Wu, X Li, L Wu, J Sun, J He, BWS Robinson, B Zhu. Tracking neoantigens by personalized circulating tumor DNA sequencing during checkpoint blockade immunotherapy in non-small cell lung cancer. Adv Sci (Weinh) 2020; 7(9): 1903410
https://doi.org/10.1002/advs.201903410
|
| 83 |
D Chu, C Paoletti, C Gersch, DA VanDenBerg, DJ Zabransky, RL Cochran, HY Wong, PV Toro, J Cidado, S Croessmann, B Erlanger, K Cravero, K Kyker-Snowman, B Button, HA Parsons, WB Dalton, R Gillani, A Medford, K Aung, N Tokudome, AM Chinnaiyan, A Schott, D Robinson, KS Jacks, J Lauring, PJ Hurley, DF Hayes, JM Rae, BH Park. ESR1 mutations in circulating plasma tumor DNA from metastatic breast cancer patients. Clin Cancer Res 2016; 22(4): 993–999
https://doi.org/10.1158/1078-0432.CCR-15-0943
|
| 84 |
Y Zhang, Y Yao, Y Xu, L Li, Y Gong, K Zhang, M Zhang, Y Guan, L Chang, X Xia, L Li, S Jia, Q Zeng. Pan-cancer circulating tumor DNA detection in over 10,000 Chinese patients. Nat Commun 2021; 12(1): 11
https://doi.org/10.1038/s41467-020-20162-8
|
| 85 |
E Hedlund, Q Deng. Single-cell RNA sequencing: technical advancements and biological applications. Mol Aspects Med 2018; 59: 36–46
https://doi.org/10.1016/j.mam.2017.07.003
|
| 86 |
MD Luecken, FJ Theis. Current best practices in single-cell RNA-seq analysis: a tutorial. Mol Syst Biol 2019; 15(6): e8746
https://doi.org/10.15252/msb.20188746
|
| 87 |
MJT Stubbington, T Lönnberg, V Proserpio, S Clare, AO Speak, G Dougan, SA Teichmann. T cell fate and clonality inference from single-cell transcriptomes. Nat Methods 2016; 13(4): 329–332
https://doi.org/10.1038/nmeth.3800
|
| 88 |
AM Klein, L Mazutis, I Akartuna, N Tallapragada, A Veres, V Li, L Peshkin, DA Weitz, MW Kirschner. Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell 2015; 161(5): 1187–1201
https://doi.org/10.1016/j.cell.2015.04.044
|
| 89 |
EZ Macosko, A Basu, R Satija, J Nemesh, K Shekhar, M Goldman, I Tirosh, AR Bialas, N Kamitaki, EM Martersteck, JJ Trombetta, DA Weitz, JR Sanes, AK Shalek, A Regev, SA McCarroll. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 2015; 161(5): 1202–1214
https://doi.org/10.1016/j.cell.2015.05.002
|
| 90 |
X Guo, Y Zhang, L Zheng, C Zheng, J Song, Q Zhang, B Kang, Z Liu, L Jin, R Xing, R Gao, L Zhang, M Dong, X Hu, X Ren, D Kirchhoff, HG Roider, T Yan, Z Zhang. Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing. Nat Med 2018; 24(7): 978–985
https://doi.org/10.1038/s41591-018-0045-3
|
| 91 |
L Zheng, S Qin, W Si, A Wang, B Xing, R Gao, X Ren, L Wang, X Wu, J Zhang, N Wu, N Zhang, H Zheng, H Ouyang, K Chen, Z Bu, X Hu, J Ji, Z Zhang. Pan-cancer single-cell landscape of tumor-infiltrating T cells. Science 2021; 374(6574): abe6474
https://doi.org/10.1126/science.abe6474
|
| 92 |
Y Liu, Q Zhang, B Xing, N Luo, R Gao, K Yu, X Hu, Z Bu, J Peng, X Ren, Z Zhang. Immune phenotypic linkage between colorectal cancer and liver metastasis. Cancer Cell 2022; 40(4): 424–437.e5
https://doi.org/10.1016/j.ccell.2022.02.013
|
| 93 |
R Xue, Q Zhang, Q Cao, R Kong, X Xiang, H Liu, M Feng, F Wang, J Cheng, Z Li, Q Zhan, M Deng, J Zhu, Z Zhang, N Zhang. Liver tumour immune microenvironment subtypes and neutrophil heterogeneity. Nature 2022; 612(7938): 141–147
https://doi.org/10.1038/s41586-022-05400-x
|
| 94 |
SM Lewis, ML Asselin-Labat, Q Nguyen, J Berthelet, X Tan, VC Wimmer, D Merino, KL Rogers, SH Naik. Spatial omics and multiplexed imaging to explore cancer biology. Nat Methods 2021; 18(9): 997–1012
https://doi.org/10.1038/s41592-021-01203-6
|
| 95 |
A Rao, D Barkley, GS França, I Yanai. Exploring tissue architecture using spatial transcriptomics. Nature 2021; 596(7871): 211–220
https://doi.org/10.1038/s41586-021-03634-9
|
| 96 |
R Ke, M Mignardi, A Pacureanu, J Svedlund, J Botling, C Wählby, M Nilsson. In situ sequencing for RNA analysis in preserved tissue and cells. Nat Methods 2013; 10(9): 857–860
https://doi.org/10.1038/nmeth.2563
|
| 97 |
PL Ståhl, F Salmén, S Vickovic, A Lundmark, JF Navarro, J Magnusson, S Giacomello, M Asp, JO Westholm, M Huss, A Mollbrink, S Linnarsson, S Codeluppi, Å Borg, F Pontén, PI Costea, P Sahlén, J Mulder, O Bergmann, J Lundeberg, J Frisén. Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 2016; 353(6294): 78–82
https://doi.org/10.1126/science.aaf2403
|
| 98 |
SG Rodriques, RR Stickels, A Goeva, CA Martin, E Murray, CR Vanderburg, J Welch, LM Chen, F Chen, EZ Macosko. Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 2019; 363(6434): 1463–1467
https://doi.org/10.1126/science.aaw1219
|
| 99 |
SZ Wu, G Al-Eryani, DL Roden, S Junankar, K Harvey, A Andersson, A Thennavan, C Wang, JR Torpy, N Bartonicek, T Wang, L Larsson, D Kaczorowski, NI Weisenfeld, CR Uytingco, JG Chew, ZW Bent, CL Chan, V Gnanasambandapillai, CA Dutertre, L Gluch, MN Hui, J Beith, A Parker, E Robbins, D Segara, C Cooper, C Mak, B Chan, S Warrier, F Ginhoux, E Millar, JE Powell, SR Williams, XS Liu, S O’Toole, E Lim, J Lundeberg, CM Perou, A Swarbrick. A single-cell and spatially resolved atlas of human breast cancers. Nat Genet 2021; 53(9): 1334–1347
https://doi.org/10.1038/s41588-021-00911-1
|
| 100 |
Y Wu, S Yang, J Ma, Z Chen, G Song, D Rao, Y Cheng, S Huang, Y Liu, S Jiang, J Liu, X Huang, X Wang, S Qiu, J Xu, R Xi, F Bai, J Zhou, J Fan, X Zhang, Q Gao. Spatiotemporal immune landscape of colorectal cancer liver metastasis at single-cell level. Cancer Discov 2022; 12(1): 134–153
https://doi.org/10.1158/2159-8290.CD-21-0316
|
| 101 |
C Giesen, HA Wang, D Schapiro, N Zivanovic, A Jacobs, B Hattendorf, PJ Schüffler, D Grolimund, JM Buhmann, S Brandt, Z Varga, PJ Wild, D Günther, B Bodenmiller. Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat Methods 2014; 11(4): 417–422
https://doi.org/10.1038/nmeth.2869
|
| 102 |
Q Chang, OI Ornatsky, I Siddiqui, A Loboda, VI Baranov, DW Hedley. Imaging mass cytometry. Cytometry A 2017; 91(2): 160–169
https://doi.org/10.1002/cyto.a.23053
|
| 103 |
H Baharlou, NP Canete, AL Cunningham, AN Harman, E Patrick. Mass cytometry imaging for the study of human diseases-applications and data analysis strategies. Front Immunol 2019; 10: 2657
https://doi.org/10.3389/fimmu.2019.02657
|
| 104 |
B Bodenmiller. Multiplexed epitope-based tissue imaging for discovery and healthcare applications. Cell Syst 2016; 2(4): 225–238
https://doi.org/10.1016/j.cels.2016.03.008
|
| 105 |
D Moldoveanu, L Ramsay, M Lajoie, L Anderson-Trocme, M Lingrand, D Berry, LJM Perus, Y Wei, C Moraes, R Alkallas, S Rajkumar, D Zuo, M Dankner, EH Xu, NR Bertos, HS Najafabadi, S Gravel, S Costantino, MJ Richer, AW Lund, Rincon SV Del, A Spatz, WH Jr Miller, R Jamal, R Lapointe, AM Mes-Masson, S Turcotte, K Petrecca, S Dumitra, AN Meguerditchian, K Richardson, F Tremblay, B Wang, M Chergui, MC Guiot, K Watters, J Stagg, DF Quail, C Mihalcioiu, S Meterissian, IR Watson. Spatially mapping the immune landscape of melanoma using imaging mass cytometry. Sci Immunol 2022; 7(70): eabi5072
https://doi.org/10.1126/sciimmunol.abi5072
|
| 106 |
S Martinez-Morilla, F Villarroel-Espindola, PF Wong, MI Toki, TN Aung, V Pelekanou, B Bourke-Martin, KA Schalper, HM Kluger, DL Rimm. Biomarker discovery in patients with immunotherapy-treated melanoma with imaging mass cytometry. Clin Cancer Res 2021; 27(7): 1987–1996
https://doi.org/10.1158/1078-0432.CCR-20-3340
|
| 107 |
HJ Jang, HS Lee, W Yu, M Ramineni, CY Truong, D Ramos, T Splawn, JM Choi, SY Jung, JS Lee, DY Wang, JM Sederstrom, M Pietropaolo, F Kheradmand, CI Amos, TM Wheeler, RT Ripley, BM Burt. Therapeutic targeting of macrophage plasticity remodels the tumor-immune microenvironment. Cancer Res 2022; 82(14): 2593–2609
https://doi.org/10.1158/0008-5472.CAN-21-3506
|
| 108 |
MD Zarella, D Bowman, F Aeffner, N Farahani, A Xthona, SF Absar, A Parwani, M Bui, DJ Hartman. A Practical Guide to Whole Slide Imaging: A White Paper from the Digital Pathology Association. Arch Pathol Lab Med 2019; 143(2): 222–234
https://doi.org/10.5858/arpa.2018-0343-RA
|
| 109 |
AJ Gifford, AJ Colebatch, S Litkouhi, F Hersch, W Warzecha, K Snook, M Sywak, AJ Gill. Remote frozen section examination of breast sentinel lymph nodes by telepathology. ANZ J Surg 2012; 82(11): 803–808
https://doi.org/10.1111/j.1445-2197.2012.06191.x
|
| 110 |
L Pantanowitz. Digital images and the future of digital pathology. J Pathol Inform 2010; 1: 15
https://doi.org/10.4103/2153-3539.63821
|
| 111 |
V Baxi, R Edwards, M Montalto, S Saha. Digital pathology and artificial intelligence in translational medicine and clinical practice. Mod Pathol 2022; 35(1): 23–32
https://doi.org/10.1038/s41379-021-00919-2
|
| 112 |
M Indu, R Rathy, MP Binu. “Slide less pathology”: fairy tale or reality?. J Oral Maxillofac Pathol 2016; 20(2): 284–288
https://doi.org/10.4103/0973-029X.185921
|
| 113 |
F Ghaznavi, A Evans, A Madabhushi, M Feldman. Digital imaging in pathology: whole-slide imaging and beyond. Annu Rev Pathol 2013; 8(1): 331–359
https://doi.org/10.1146/annurev-pathol-011811-120902
|
| 114 |
Z Feng, S Puri, T Moudgil, W Wood, CC Hoyt, C Wang, WJ Urba, BD Curti, CB Bifulco, BA Fox. Multispectral imaging of formalin-fixed tissue predicts ability to generate tumor-infiltrating lymphocytes from melanoma. J Immunother Cancer 2015; 3(1): 47
https://doi.org/10.1186/s40425-015-0091-z
|
| 115 |
K Bera, KA Schalper, DL Rimm, V Velcheti, A Madabhushi. Artificial intelligence in digital pathologynew tools for diagnosis and precision oncology. Nat Rev Clin Oncol 2019; 16(11): 703–715
https://doi.org/10.1038/s41571-019-0252-y
|
| 116 |
PC Tumeh, MD Hellmann, O Hamid, KK Tsai, KL Loo, MA Gubens, M Rosenblum, CL Harview, JM Taube, N Handley, N Khurana, A Nosrati, MF Krummel, A Tucker, EV Sosa, PJ Sanchez, N Banayan, JC Osorio, DL Nguyen-Kim, J Chang, IP Shintaku, PD Boasberg, EJ Taylor, PN Munster, AP Algazi, B Chmielowski, R Dummer, TR Grogan, D Elashoff, J Hwang, SM Goldinger, EB Garon, RH Pierce, A Daud. Liver metastasis and treatment outcome with anti-PD-1 monoclonal antibody in patients with melanoma and NSCLC. Cancer Immunol Res 2017; 5(5): 417–424
https://doi.org/10.1158/2326-6066.CIR-16-0325
|
| 117 |
JM Taube, G Akturk, M Angelo, EL Engle, S Gnjatic, S Greenbaum, NF Greenwald, CV Hedvat, TJ Hollmann, J Juco, ER Parra, MC Rebelatto, DL Rimm, J Rodriguez-Canales, KA Schalper, EC Stack, CS Ferreira, K Korski, A Lako, SJ Rodig, E Schenck, KE Steele, MJ Surace, MT Tetzlaff, Loga K von, II Wistuba, CB; Society for Immunotherapy of Cancer (SITC) Pathology Task Force Bifulco. The Society for Immunotherapy of Cancer statement on best practices for multiplex immunohistochemistry (IHC) and immunofluorescence (IF) staining and validation. J Immunother Cancer 2020; 8(1): e000155
https://doi.org/10.1136/jitc-2019-000155
|
| 118 |
JL Carstens, P Correa de Sampaio, D Yang, S Barua, H Wang, A Rao, JP Allison, VS LeBleu, R Kalluri. Spatial computation of intratumoral T cells correlates with survival of patients with pancreatic cancer. Nat Commun 2017; 8(1): 15095
https://doi.org/10.1038/ncomms15095
|
| 119 |
N Coudray, PS Ocampo, T Sakellaropoulos, N Narula, M Snuderl, D Fenyö, AL Moreira, N Razavian, A Tsirigos. Classification and mutation prediction from non-small cell lung cancer histopathology images using deep learning. Nat Med 2018; 24(10): 1559–1567
https://doi.org/10.1038/s41591-018-0177-5
|
| 120 |
JN Kather, AT Pearson, N Halama, D Jäger, J Krause, SH Loosen, A Marx, P Boor, F Tacke, UP Neumann, HI Grabsch, T Yoshikawa, H Brenner, J Chang-Claude, M Hoffmeister, C Trautwein, T Luedde. Deep learning can predict microsatellite instability directly from histology in gastrointestinal cancer. Nat Med 2019; 25(7): 1054–1056
https://doi.org/10.1038/s41591-019-0462-y
|
| 121 |
S Park, CY Ock, H Kim, S Pereira, S Park, M Ma, S Choi, S Kim, S Shin, BJ Aum, K Paeng, D Yoo, H Cha, S Park, KJ Suh, HA Jung, SH Kim, YJ Kim, JM Sun, JH Chung, JS Ahn, MJ Ahn, JS Lee, K Park, SY Song, YJ Bang, YL Choi, TS Mok, SH Lee. Artificial intelligence-powered spatial analysis of tumor-infiltrating lymphocytes as complementary biomarker for immune checkpoint inhibition in non-small-cell lung cancer. J Clin Oncol 2022; 40(17): 1916–1928
https://doi.org/10.1200/JCO.21.02010
|
| 122 |
C Saillard, B Schmauch, O Laifa, M Moarii, S Toldo, M Zaslavskiy, E Pronier, A Laurent, G Amaddeo, H Regnault, D Sommacale, M Ziol, JM Pawlotsky, S Mulé, A Luciani, G Wainrib, T Clozel, P Courtiol, J Calderaro. Predicting survival after hepatocellular carcinoma resection using deep learning on histological slides. Hepatology 2020; 72(6): 2000–2013
https://doi.org/10.1002/hep.31207
|
| 123 |
B Schmauch, A Romagnoni, E Pronier, C Saillard, P Maillé, J Calderaro, A Kamoun, M Sefta, S Toldo, M Zaslavskiy, T Clozel, M Moarii, P Courtiol, G Wainrib. A deep learning model to predict RNA-Seq expression of tumours from whole slide images. Nat Commun 2020; 11(1): 3877
https://doi.org/10.1038/s41467-020-17678-4
|
| 124 |
R Sun, EJ Limkin, M Vakalopoulou, L Dercle, S Champiat, SR Han, L Verlingue, D Brandao, A Lancia, S Ammari, A Hollebecque, JY Scoazec, A Marabelle, C Massard, JC Soria, C Robert, N Paragios, E Deutsch, C Ferté. A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: an imaging biomarker, retrospective multicohort study. Lancet Oncol 2018; 19(9): 1180–1191
https://doi.org/10.1016/S1470-2045(18)30413-3
|
| 125 |
R Turkki, D Byckhov, M Lundin, J Isola, S Nordling, PE Kovanen, C Verrill, K von Smitten, H Joensuu, J Lundin, N Linder. Breast cancer outcome prediction with tumour tissue images and machine learning. Breast Cancer Res Treat 2019; 177(1): 41–52
https://doi.org/10.1007/s10549-019-05281-1
|
| 126 |
RS Vanguri, J Luo, AT Aukerman, JV Egger, CJ Fong, N Horvat, A Pagano, JAB Araujo-Filho, L Geneslaw, H Rizvi, R Sosa, KM Boehm, SR Yang, FM Bodd, K Ventura, TJ Hollmann, MS Ginsberg, J; MSK MIND Consortium; Hellmann MD Gao, JL Sauter, SP Shah. Multimodal integration of radiology, pathology and genomics for prediction of response to PD-(L)1 blockade in patients with non-small cell lung cancer. Nat Can 2022; 3(10): 1151–1164
https://doi.org/10.1038/s43018-022-00416-8
|
| 127 |
J Vamathevan, D Clark, P Czodrowski, I Dunham, E Ferran, G Lee, B Li, A Madabhushi, P Shah, M Spitzer, S Zhao. Applications of machine learning in drug discovery and development. Nat Rev Drug Discov 2019; 18(6): 463–477
https://doi.org/10.1038/s41573-019-0024-5
|
| 128 |
A Janowczyk, A Madabhushi. Deep learning for digital pathology image analysis: a comprehensive tutorial with selected use cases. J Pathol Inform 2016; 7(1): 29
https://doi.org/10.4103/2153-3539.186902
|
| 129 |
T Araújo, G Aresta, E Castro, J Rouco, P Aguiar, C Eloy, A Polónia, A Campilho. Classification of breast cancer histology images using Convolutional Neural Networks. PLoS One 2017; 12(6): e0177544
https://doi.org/10.1371/journal.pone.0177544
|
| 130 |
B Ehteshami Bejnordi, M Mullooly, RM Pfeiffer, S Fan, PM Vacek, DL Weaver, S Herschorn, LA Brinton, B van Ginneken, N Karssemeijer, AH Beck, GL Gierach, JAWM van der Laak, ME Sherman. Using deep convolutional neural networks to identify and classify tumor-associated stroma in diagnostic breast biopsies. Mod Pathol 2018; 31(10): 1502–1512
https://doi.org/10.1038/s41379-018-0073-z
|
| 131 |
N Pavillon, AJ Hobro, S Akira, NI Smith. Noninvasive detection of macrophage activation with single-cell resolution through machine learning. Proc Natl Acad Sci USA 2018; 115(12): E2676–E2685
https://doi.org/10.1073/pnas.1711872115
|
| 132 |
H Liu, WD Xu, ZH Shang, XD Wang, HY Zhou, KW Ma, H Zhou, JL Qi, JR Jiang, LL Tan, HM Zeng, HJ Cai, KS Wang, YL Qian. Breast cancer molecular subtype prediction on pathological images with discriminative patch selection and multi-instance learning. Front Oncol 2022; 12: 858453
https://doi.org/10.3389/fonc.2022.858453
|
| 133 |
HR Tizhoosh, L Pantanowitz. Artificial intelligence and digital pathology: challenges and opportunities. J Pathol Inform 2018; 9(1): 38
https://doi.org/10.4103/jpi.jpi_53_18
|
| 134 |
WCC Tan, SN Nerurkar, HY Cai, HHM Ng, D Wu, YTF Wee, JCT Lim, J Yeong, TKH Lim. Overview of multiplex immunohistochemistry/immunofluorescence techniques in the era of cancer immunotherapy. Cancer Commun (Lond) 2020; 40(4): 135–153
https://doi.org/10.1002/cac2.12023
|
| 135 |
Y Van Herck, A Antoranz, MD Andhari, G Milli, O Bechter, F De Smet, FM Bosisio. Multiplexed immunohistochemistry and digital pathology as the foundation for next-generation pathology in melanoma: methodological comparison and future clinical applications. Front Oncol 2021; 11: 636681
https://doi.org/10.3389/fonc.2021.636681
|
| 136 |
A Serag, A Ion-Margineanu, H Qureshi, R McMillan, Martin MJ Saint, J Diamond, P O’Reilly, P Hamilton. Translational AI and deep learning in diagnostic pathology. Front Med (Lausanne) 2019; 6: 185
https://doi.org/10.3389/fmed.2019.00185
|
| 137 |
H Farmer, N McCabe, CJ Lord, AN Tutt, DA Johnson, TB Richardson, M Santarosa, KJ Dillon, I Hickson, C Knights, NM Martin, SP Jackson, GC Smith, A Ashworth. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005; 434(7035): 917–921
https://doi.org/10.1038/nature03445
|
| 138 |
HE Bryant, N Schultz, HD Thomas, KM Parker, D Flower, E Lopez, S Kyle, M Meuth, NJ Curtin, T Helleday. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005; 434(7035): 913–917
https://doi.org/10.1038/nature03443
|
| 139 |
MP Dias, SC Moser, S Ganesan, J Jonkers. Understanding and overcoming resistance to PARP inhibitors in cancer therapy. Nat Rev Clin Oncol 2021; 18(12): 773–791
https://doi.org/10.1038/s41571-021-00532-x
|
| 140 |
L Ding, HJ Kim, Q Wang, M Kearns, T Jiang, CE Ohlson, BB Li, S Xie, JF Liu, EH Stover, BE Howitt, RT Bronson, S Lazo, TM Roberts, GJ Freeman, PA Konstantinopoulos, UA Matulonis, JJ Zhao. PARP inhibition elicits STING-dependent antitumor immunity in Brca1-deficient ovarian cancer. Cell Rep 2018; 25(11): 2972–2980.e5
https://doi.org/10.1016/j.celrep.2018.11.054
|
| 141 |
J Meng, J Peng, J Feng, J Maurer, X Li, Y Li, S Yao, R Chu, X Pan, J Li, T Zhang, L Liu, Q Zhang, Z Yuan, H Bu, K Song, B Kong. Niraparib exhibits a synergistic anti-tumor effect with PD-L1 blockade by inducing an immune response in ovarian cancer. J Transl Med 2021; 19(1): 415
https://doi.org/10.1186/s12967-021-03073-0
|
| 142 |
L Wang, D Wang, O Sonzogni, S Ke, Q Wang, A Thavamani, F Batalini, SA Stopka, MS Regan, S Vandal, S Tian, J Pinto, AM Cyr, VC Bret-Mounet, G Baquer, HP Eikesdal, M Yuan, JM Asara, YJ Heng, P Bai, NYR Agar, GM Wulf. PARP-inhibition reprograms macrophages toward an anti-tumor phenotype. Cell Rep 2022; 41(2): 111462
https://doi.org/10.1016/j.celrep.2022.111462
|
| 143 |
B Kaufman, R Shapira-Frommer, RK Schmutzler, MW Audeh, M Friedlander, J Balmaña, G Mitchell, G Fried, SM Stemmer, A Hubert, O Rosengarten, M Steiner, N Loman, K Bowen, A Fielding, SM Domchek. Olaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutation. J Clin Oncol 2015; 33(3): 244–250
https://doi.org/10.1200/JCO.2014.56.2728
|
| 144 |
M Robson, SA Im, E Senkus, B Xu, SM Domchek, N Masuda, S Delaloge, W Li, N Tung, A Armstrong, W Wu, C Goessl, S Runswick, P Conte. Olaparib for metastatic breast cancer in patients with a germline BRCA mutation. N Engl J Med 2017; 377(6): 523–533
https://doi.org/10.1056/NEJMoa1706450
|
| 145 |
J Ettl, RGW Quek, KH Lee, HS Rugo, S Hurvitz, A Gonçalves, L Fehrenbacher, R Yerushalmi, LA Mina, M Martin, H Roché, YH Im, D Markova, H Bhattacharyya, AL Hannah, W Eiermann, JL Blum, JK Litton. Quality of life with talazoparib versus physician’s choice of chemotherapy in patients with advanced breast cancer and germline BRCA1/2 mutation: patient-reported outcomes from the EMBRACA phase III trial. Ann Oncol 2018; 29(9): 1939–1947
https://doi.org/10.1093/annonc/mdy257
|
| 146 |
KN Moore, AA Secord, MA Geller, DS Miller, N Cloven, GF Fleming, AE Wahner Hendrickson, M Azodi, P DiSilvestro, AM Oza, M Cristea, JS Berek, JK Chan, BJ Rimel, DE Matei, Y Li, K Sun, K Luptakova, UA Matulonis, BJ Monk. Niraparib monotherapy for late-line treatment of ovarian cancer (QUADRA): a multicentre, open-label, single-arm, phase 2 trial. Lancet Oncol 2019; 20(5): 636–648
https://doi.org/10.1016/S1470-2045(19)30029-4
|
| 147 |
RL Coleman, AM Oza, D Lorusso, C Aghajanian, A Oaknin, A Dean, N Colombo, JI Weberpals, A Clamp, G Scambia, A Leary, RW Holloway, MA Gancedo, PC Fong, JC Goh, DM O'Malley, DK Armstrong, J Garcia-Donas, EM Swisher, A Floquet, GE Konecny, IA McNeish, CL Scott, T Cameron, L Maloney, J Isaacson, S Goble, C Grace, TC Harding, M Raponi, J Sun, KK Lin, H Giordano, JA; ARIEL3 investigators Ledermann. Rucaparib maintenance treatment for recurrent ovarian carcinoma after response to platinum therapy (ARIEL3): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 2017; 390(10106): 1949–1961
https://doi.org/10.1016/S0140-6736(17)32440-6
|
| 148 |
AS Zimmer, E Nichols, A Cimino-Mathews, C Peer, L Cao, MJ Lee, EC Kohn, CM Annunziata, S Lipkowitz, JB Trepel, R Sharma, L Mikkilineni, M Gatti-Mays, WD Figg, ND Houston, JM Lee. A phase I study of the PD-L1 inhibitor, durvalumab, in combination with a PARP inhibitor, olaparib, and a VEGFR1-3 inhibitor, cediranib, in recurrent women’s cancers with biomarker analyses. J Immunother Cancer 2019; 7(1): 197
https://doi.org/10.1186/s40425-019-0680-3
|
| 149 |
CL Gerard, J Delyon, A Wicky, K Homicsko, MA Cuendet, O Michielin. Turning tumors from cold to inflamed to improve immunotherapy response. Cancer Treat Rev 2021; 101: 102227
https://doi.org/10.1016/j.ctrv.2021.102227
|
| 150 |
MJ Topper, M Vaz, KB Chiappinelli, CE DeStefano Shields, N Niknafs, RC Yen, A Wenzel, J Hicks, M Ballew, M Stone, PT Tran, CA Zahnow, MD Hellmann, V Anagnostou, PL Strissel, R Strick, VE Velculescu, SB Baylin. Epigenetic therapy ties MYC depletion to reversing immune evasion and treating lung cancer. Cell 2017; 171(6): 1284–1300.e21
https://doi.org/10.1016/j.cell.2017.10.022
|
| 151 |
AR Abbas, D Baldwin, Y Ma, W Ouyang, A Gurney, F Martin, S Fong, M van Lookeren Campagne, P Godowski, PM Williams, AC Chan, HF Clark. Immune response in silico (IRIS): immune-specific genes identified from a compendium of microarray expression data. Genes Immun 2005; 6(4): 319–331
https://doi.org/10.1038/sj.gene.6364173
|
| 152 |
SG Pai, BA Carneiro, JM Mota, R Costa, CA Leite, R Barroso-Sousa, JB Kaplan, YK Chae, FJ Giles. Wnt/beta-catenin pathway: modulating anticancer immune response. J Hematol Oncol 2017; 10(1): 101
https://doi.org/10.1186/s13045-017-0471-6
|
| 153 |
L Yang, Y Pang, HL Moses. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 2010; 31(6): 220–227
https://doi.org/10.1016/j.it.2010.04.002
|
| 154 |
JG Paez, PA Jänne, JC Lee, S Tracy, H Greulich, S Gabriel, P Herman, FJ Kaye, N Lindeman, TJ Boggon, K Naoki, H Sasaki, Y Fujii, MJ Eck, WR Sellers, BE Johnson, M Meyerson. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304(5676): 1497–1500
https://doi.org/10.1126/science.1099314
|
| 155 |
S Gross, R Rahal, N Stransky, C Lengauer, KP Hoeflich. Targeting cancer with kinase inhibitors. J Clin Invest 2015; 125(5): 1780–1789
https://doi.org/10.1172/JCI76094
|
| 156 |
HY Tan, N Wang, W Lam, W Guo, Y Feng, YC Cheng. Targeting tumour microenvironment by tyrosine kinase inhibitor. Mol Cancer 2018; 17(1): 43
https://doi.org/10.1186/s12943-018-0800-6
|
| 157 |
Y Shi, JS Au, S Thongprasert, S Srinivasan, CM Tsai, MT Khoa, K Heeroma, Y Itoh, G Cornelio, PC Yang. A prospective, molecular epidemiology study of EGFR mutations in Asian patients with advanced non-small-cell lung cancer of adenocarcinoma histology (PIONEER). J Thorac Oncol 2014; 9(2): 154–162
https://doi.org/10.1097/JTO.0000000000000033
|
| 158 |
R Sordella, DW Bell, DA Haber, J Settleman. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004; 305(5687): 1163–1167
https://doi.org/10.1126/science.1101637
|
| 159 |
TJ Lynch, DW Bell, R Sordella, S Gurubhagavatula, RA Okimoto, BW Brannigan, PL Harris, SM Haserlat, JG Supko, FG Haluska, DN Louis, DC Christiani, J Settleman, DA Haber. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350(21): 2129–2139
https://doi.org/10.1056/NEJMoa040938
|
| 160 |
C Dominguez, KY Tsang, C Palena. Short-term EGFR blockade enhances immune-mediated cytotoxicity of EGFR mutant lung cancer cells: rationale for combination therapies. Cell Death Dis 2016; 7(9): e2380
https://doi.org/10.1038/cddis.2016.297
|
| 161 |
C Selenz, A Compes, M Nill, S Borchmann, M Odenthal, A Florin, J Brägelmann, R Büttner, L Meder, RT Ullrich. EGFR inhibition strongly modulates the tumour immune microenvironment in EGFR-driven non-small-cell lung cancer. Cancers (Basel) 2022; 14(16): 3943
https://doi.org/10.3390/cancers14163943
|
| 162 |
KH Hsu, YH Huang, JS Tseng, KC Chen, WH Ku, KY Su, JJW Chen, HW Chen, SL Yu, TY Yang, GC Chang. High PD-L1 expression correlates with primary resistance to EGFR-TKIs in treatment naïve advanced EGFR-mutant lung adenocarcinoma patients. Lung Cancer 2019; 127: 37–43
https://doi.org/10.1016/j.lungcan.2018.11.021
|
| 163 |
Y Oshima, T Tanimoto, K Yuji, A Tojo. EGFR-TKI-associated interstitial pneumonitis in nivolumab-treated patients with non-small cell lung cancer. JAMA Oncol 2018; 4(8): 1112–1115
https://doi.org/10.1001/jamaoncol.2017.4526
|
| 164 |
S Kato, A Goodman, V Walavalkar, DA Barkauskas, A Sharabi, R Kurzrock. Hyperprogressors after immunotherapy: analysis of genomic alterations associated with accelerated growth rate. Clin Cancer Res 2017; 23(15): 4242–4250
https://doi.org/10.1158/1078-0432.CCR-16-3133
|
| 165 |
T Tian, M Yu, J Li, M Jiang, D Ma, S Tang, Z Lin, L Chen, Y Gong, J Zhu, Q Zhou, M Huang, Y Lu. Front-line ICI-based combination therapy post-TKI resistance may improve survival in NSCLC patients with EGFR mutation. Front Oncol 2021; 11: 739090
https://doi.org/10.3389/fonc.2021.739090
|
| 166 |
C Gridelli, S Peters, A Sgambato, F Casaluce, AA Adjei, F Ciardiello. ALK inhibitors in the treatment of advanced NSCLC. Cancer Treat Rev 2014; 40(2): 300–306
https://doi.org/10.1016/j.ctrv.2013.07.002
|
| 167 |
KC Arbour, GJ Riely. Diagnosis and treatment of anaplastic lymphoma kinase-positive non-small cell lung cancer. Hematol Oncol Clin North Am 2017; 31(1): 101–111
https://doi.org/10.1016/j.hoc.2016.08.012
|
| 168 |
Y Fang, Y Wang, D Zeng, S Zhi, T Shu, N Huang, S Zheng, J Wu, Y Liu, G Huang, Y Xue, J Bin, Y Liao, M Shi, W Liao. Comprehensive analyses reveal TKI-induced remodeling of the tumor immune microenvironment in EGFR/ALK-positive non-small-cell lung cancer. OncoImmunology 2021; 10(1): 1951019
https://doi.org/10.1080/2162402X.2021.1951019
|
| 169 |
DR Spigel, C Reynolds, D Waterhouse, EB Garon, J Chandler, S Babu, P Thurmes, A Spira, R Jotte, J Zhu, WH Lin, G Jr Blumenschein. Phase 1/2 study of the safety and tolerability of nivolumab plus crizotinib for the first-line treatment of anaplastic lymphoma kinase translocation—positive advanced non-small cell lung cancer (CheckMate 370). J Thorac Oncol 2018; 13(5): 682–688
https://doi.org/10.1016/j.jtho.2018.02.022
|
| 170 |
R Dummer, P Queirolo, AM Abajo Guijarro, Y Hu, D Wang, SJ de Azevedo, C Robert, PA Ascierto, V Chiarion-Sileni, P Pronzato, F Spagnolo, K Mujika Eizmendi, G Liszkay, L de la Cruz Merino, H Tawbi. Atezolizumab, vemurafenib, and cobimetinib in patients with melanoma with CNS metastases (TRICOTEL): a multicentre, open-label, single-arm, phase 2 study. Lancet Oncol 2022; 23(9): 1145–1155
https://doi.org/10.1016/S1470-2045(22)00452-1
|
| 171 |
RJ Sullivan, O Hamid, R Gonzalez, JR Infante, MR Patel, FS Hodi, KD Lewis, HA Tawbi, G Hernandez, MJ Wongchenko, Y Chang, L Roberts, M Ballinger, Y Yan, E Cha, P Hwu. Atezolizumab plus cobimetinib and vemurafenib in BRAF-mutated melanoma patients. Nat Med 2019; 25(6): 929–935
https://doi.org/10.1038/s41591-019-0474-7
|
| 172 |
A Ribas, D Lawrence, V Atkinson, S Agarwal, WH Jr Miller, MS Carlino, R Fisher, GV Long, FS Hodi, J Tsoi, CS Grasso, B Mookerjee, Q Zhao, R Ghori, BH Moreno, N Ibrahim, O Hamid. Combined BRAF and MEK inhibition with PD-1 blockade immunotherapy in BRAF-mutant melanoma. Nat Med 2019; 25(6): 936–940
https://doi.org/10.1038/s41591-019-0476-5
|
| 173 |
PA Ascierto, D Stroyakovskiy, H Gogas, C Robert, K Lewis, S Protsenko, RP Pereira, T Eigentler, P Rutkowski, L Demidov, N Zhukova, J Schachter, Y Yan, I Caro, C Hertig, C Xue, L Kusters, GA McArthur, R Gutzmer. Overall survival with first-line atezolizumab in combination with vemurafenib and cobimetinib in BRAFV600 mutation-positive advanced melanoma (IMspire150): second interim analysis of a multicentre, randomised, phase 3 study. Lancet Oncol 2023; 24(1): 33–44
https://doi.org/10.1016/S1470-2045(22)00687-8
|
| 174 |
DS Chen, I Mellman. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013; 39(1): 1–10
https://doi.org/10.1016/j.immuni.2013.07.012
|
| 175 |
X Liu, Y Pu, K Cron, L Deng, J Kline, WA Frazier, H Xu, H Peng, YX Fu, MM Xu. CD47 blockade triggers T cell-mediated destruction of immunogenic tumors. Nat Med 2015; 21(10): 1209–1215
https://doi.org/10.1038/nm.3931
|
| 176 |
H Wang, S Hu, X Chen, H Shi, C Chen, L Sun, ZJ Chen. cGAS is essential for the antitumor effect of immune checkpoint blockade. Proc Natl Acad Sci USA 2017; 114(7): 1637–1642
https://doi.org/10.1073/pnas.1621363114
|
| 177 |
T Li, H Cheng, H Yuan, Q Xu, C Shu, Y Zhang, P Xu, J Tan, Y Rui, P Li, X Tan. Antitumor activity of cGAMP via stimulation of cGAS-cGAMP-STING-IRF3 mediated innate immune response. Sci Rep 2016; 6(1): 19049
https://doi.org/10.1038/srep19049
|
| 178 |
L Deng, H Liang, M Xu, X Yang, B Burnette, A Arina, XD Li, H Mauceri, M Beckett, T Darga, X Huang, TF Gajewski, ZJ Chen, YX Fu, RR Weichselbaum. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity 2014; 41(5): 843–852
https://doi.org/10.1016/j.immuni.2014.10.019
|
| 179 |
MS Diamond, M Kinder, H Matsushita, M Mashayekhi, GP Dunn, JM Archambault, H Lee, CD Arthur, JM White, U Kalinke, KM Murphy, RD Schreiber. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011; 208(10): 1989–2003
https://doi.org/10.1084/jem.20101158
|
| 180 |
KE Sivick, AL Desbien, LH Glickman, GL Reiner, L Corrales, NH Surh, TE Hudson, UT Vu, BJ Francica, T Banda, GE Katibah, DB Kanne, JJ Leong, K Metchette, JR Bruml, CO Ndubaku, JM McKenna, Y Feng, L Zheng, SL Bender, CY Cho, ML Leong, Elsas A van, TW Jr Dubensky, SM McWhirter. Magnitude of therapeutic STING activation determines CD8+ T cell-mediated anti-tumor immunity. Cell Rep 2019; 29(3): 785–789
https://doi.org/10.1016/j.celrep.2019.09.089
|
| 181 |
T Kawasaki, T Kawai. Toll-like receptor signaling pathways. Front Immunol 2014; 5: 461
https://doi.org/10.3389/fimmu.2014.00461
|
| 182 |
C Wang, Y Zhuang, Y Zhang, Z Luo, N Gao, P Li, H Pan, L Cai, Y Ma. Toll-like receptor 3 agonist complexed with cationic liposome augments vaccine-elicited antitumor immunity by enhancing TLR3-IRF3 signaling and type I interferons in dendritic cells. Vaccine 2012; 30(32): 4790–4799
https://doi.org/10.1016/j.vaccine.2012.05.027
|
| 183 |
AM Krieg. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 2006; 5(6): 471–484
https://doi.org/10.1038/nrd2059
|
| 184 |
J Koh, S Kim, SN Lee, SY Kim, JE Kim, KY Lee, MS Kim, JY Heo, YM Park, BM Ku, JM Sun, SH Lee, JS Ahn, K Park, S Yang, SJ Ha, YT Lim, MJ Ahn. Therapeutic efficacy of cancer vaccine adjuvanted with nanoemulsion loaded with TLR7/8 agonist in lung cancer model. Nanomedicine 2021; 37: 102415
https://doi.org/10.1016/j.nano.2021.102415
|
| 185 |
A Ribas, T Medina, S Kummar, A Amin, A Kalbasi, JJ Drabick, M Barve, GA Daniels, DJ Wong, EV Schmidt, AF Candia, RL Coffman, ACF Leung, RS Janssen. SD-101 in combination with pembrolizumab in advanced melanoma: results of a phase Ib, multicenter Study. Cancer Discov 2018; 8(10): 1250–1257
https://doi.org/10.1158/2159-8290.CD-18-0280
|
| 186 |
RH Vonderheide. CD40 agonist antibodies in cancer immunotherapy. Annu Rev Med 2020; 71(1): 47–58
https://doi.org/10.1146/annurev-med-062518-045435
|
| 187 |
SM Mangsbo, S Broos, E Fletcher, N Veitonmäki, C Furebring, E Dahlén, P Norlén, M Lindstedt, TH Tötterman, P Ellmark. The human agonistic CD40 antibody ADC-1013 eradicates bladder tumors and generates T-cell-dependent tumor immunity. Clin Cancer Res 2015; 21(5): 1115–1126
https://doi.org/10.1158/1078-0432.CCR-14-0913
|
| 188 |
P Johnson, R Challis, F Chowdhury, Y Gao, M Harvey, T Geldart, P Kerr, C Chan, A Smith, N Steven, C Edwards, M Ashton-Key, E Hodges, A Tutt, C Ottensmeier, M Glennie, A Williams. Clinical and biological effects of an agonist anti-CD40 antibody: a Cancer Research UK phase I study. Clin Cancer Res 2015; 21(6): 1321–1328
https://doi.org/10.1158/1078-0432.CCR-14-2355
|
| 189 |
J Rüter, SJ Antonia, HA Burris, RD Huhn, RH Vonderheide. Immune modulation with weekly dosing of an agonist CD40 antibody in a phase I study of patients with advanced solid tumors. Cancer Biol Ther 2010; 10(10): 983–993
https://doi.org/10.4161/cbt.10.10.13251
|
| 190 |
RH Vonderheide, KT Flaherty, M Khalil, MS Stumacher, DL Bajor, NA Hutnick, P Sullivan, JJ Mahany, M Gallagher, A Kramer, SJ Green, PJ O’Dwyer, KL Running, RD Huhn, SJ Antonia. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007; 25(7): 876–883
https://doi.org/10.1200/JCO.2006.08.3311
|
| 191 |
DL Bajor, X Xu, DA Torigian, R Mick, LR Garcia, LP Richman, C Desmarais, KL Nathanson, LM Schuchter, M Kalos, RH Vonderheide. Immune activation and a 9-year ongoing complete remission following CD40 antibody therapy and metastasectomy in a patient with metastatic melanoma. Cancer Immunol Res 2014; 2(11): 1051–1058
https://doi.org/10.1158/2326-6066.CIR-14-0154
|
| 192 |
DL Bajor, R Mick, MJ Riese, AC Huang, B Sullivan, LP Richman, DA Torigian, SM George, E Stelekati, F Chen, JJ Melenhorst, SF Lacey, X Xu, EJ Wherry, TC Gangadhar, RK Amaravadi, LM Schuchter, RH Vonderheide. Long-term outcomes of a phase I study of agonist CD40 antibody and CTLA-4 blockade in patients with metastatic melanoma. OncoImmunology 2018; 7(10): e1468956
https://doi.org/10.1080/2162402X.2018.1468956
|
| 193 |
L Russell, KW Peng, SJ Russell, RM Diaz. Oncolytic viruses: priming time for cancer immunotherapy. BioDrugs 2019; 33(5): 485–501
https://doi.org/10.1007/s40259-019-00367-0
|
| 194 |
S Gujar, JG Pol, Y Kim, PW Lee, G Kroemer. Antitumor benefits of antiviral immunity: an underappreciated aspect of oncolytic virotherapies. Trends Immunol 2018; 39(3): 209–221
https://doi.org/10.1016/j.it.2017.11.006
|
| 195 |
A Lemos de Matos, LS Franco, G McFadden. Oncolytic viruses and the immune system: the dynamic duo. Mol Ther Methods Clin Dev 2020; 17: 349–358
https://doi.org/10.1016/j.omtm.2020.01.001
|
| 196 |
RH Andtbacka, HL Kaufman, F Collichio, T Amatruda, N Senzer, J Chesney, KA Delman, LE Spitler, I Puzanov, SS Agarwala, M Milhem, L Cranmer, B Curti, K Lewis, M Ross, T Guthrie, GP Linette, GA Daniels, K Harrington, MR Middleton, WH Jr Miller, JS Zager, Y Ye, B Yao, A Li, S Doleman, A VanderWalde, J Gansert, RS Coffin. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol 2015; 33(25): 2780–2788
https://doi.org/10.1200/JCO.2014.58.3377
|
| 197 |
A Ribas, R Dummer, I Puzanov, A VanderWalde, RHI Andtbacka, O Michielin, AJ Olszanski, J Malvehy, J Cebon, E Fernandez, JM Kirkwood, TF Gajewski, L Chen, KS Gorski, AA Anderson, SJ Diede, ME Lassman, J Gansert, FS Hodi, GV Long. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell 2017; 170(6): 1109–1119.e10
https://doi.org/10.1016/j.cell.2017.08.027
|
| 198 |
Y Zhang, Z Zhang. The history and advances in cancer immunotherapy: understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell Mol Immunol 2020; 17(8): 807–821
https://doi.org/10.1038/s41423-020-0488-6
|
| 199 |
C Ogi, A Aruga. Immunological monitoring of anticancer vaccines in clinical trials. OncoImmunology 2013; 2(8): e26012
https://doi.org/10.4161/onci.26012
|
| 200 |
CL Lorentzen, JB Haanen, Ö Met, IM Svane. Clinical advances and ongoing trials on mRNA vaccines for cancer treatment. Lancet Oncol 2022; 23(10): e450–e458
https://doi.org/10.1016/S1470-2045(22)00372-2
|
| 201 |
MJ Lin, J Svensson-Arvelund, GS Lubitz, A Marabelle, I Melero, BD Brown, JD Brody. Cancer vaccines: the next immunotherapy frontier. Nat Can 2022; 3(8): 911–926
https://doi.org/10.1038/s43018-022-00418-6
|
| 202 |
Q Song, CD Zhang, XH Wu. Therapeutic cancer vaccines: from initial findings to prospects. Immunol Lett 2018; 196: 11–21
https://doi.org/10.1016/j.imlet.2018.01.011
|
| 203 |
BJ Coventry. Therapeutic vaccination immunomodulation: forming the basis of all cancer immunotherapy. Ther Adv Vaccines Immunother 2019; 7: 2515135519862234
https://doi.org/10.1177/2515135519862234
|
| 204 |
J Zhang, Z Shi, X Xu, Z Yu, J Mi. The influence of microenvironment on tumor immunotherapy. FEBS J 2019; 286(21): 4160–4175
https://doi.org/10.1111/febs.15028
|
| 205 |
CS Shemesh, JC Hsu, I Hosseini, BQ Shen, A Rotte, P Twomey, S Girish, B Wu. Personalized cancer vaccines: clinical landscape, challenges, and opportunities. Mol Ther 2021; 29(2): 555–570
https://doi.org/10.1016/j.ymthe.2020.09.038
|
| 206 |
SW Tsao, G Tramoutanis, CW Dawson, AK Lo, DP Huang. The significance of LMP1 expression in nasopharyngeal carcinoma. Semin Cancer Biol 2002; 12(6): 473–487
https://doi.org/10.1016/S1044579X02000901
|
| 207 |
MC Lin, YC Lin, ST Chen, TH Young, PJ Lou. Therapeutic vaccine targeting Epstein-Barr virus latent protein, LMP1, suppresses LMP1-expressing tumor growth and metastasis in vivo. BMC Cancer 2017; 17(1): 18
https://doi.org/10.1186/s12885-016-3027-1
|
| 208 |
GS Taylor, H Jia, K Harrington, LW Lee, J Turner, K Ladell, DA Price, M Tanday, J Matthews, C Roberts, C Edwards, L McGuigan, A Hartley, S Wilson, EP Hui, AT Chan, AB Rickinson, NM Steven. A recombinant modified vaccinia ankara vaccine encoding Epstein–Barr virus (EBV) target antigens: a phase I trial in UK patients with EBV-positive cancer. Clin Cancer Res 2014; 20(19): 5009–5022
https://doi.org/10.1158/1078-0432.CCR-14-1122-T
|
| 209 |
GG Kenter, MJ Welters, AR Valentijn, MJ Lowik, DM Berends-van der Meer, AP Vloon, F Essahsah, LM Fathers, R Offringa, JW Drijfhout, AR Wafelman, J Oostendorp, GJ Fleuren, SH van der Burg, CJ Melief. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 2009; 361(19): 1838–1847
https://doi.org/10.1056/NEJMoa0810097
|
| 210 |
Y Oka, A Tsuboi, Y Oji, I Kawase, H Sugiyama. WT1 peptide vaccine for the treatment of cancer. Curr Opin Immunol 2008; 20(2): 211–220
https://doi.org/10.1016/j.coi.2008.04.009
|
| 211 |
W Zhang, X Lu, P Cui, C Piao, M Xiao, X Liu, Y Wang, X Wu, J Liu, L Yang. Phase I/II clinical trial of a Wilms’ tumor 1-targeted dendritic cell vaccination-based immunotherapy in patients with advanced cancer. Cancer Immunol Immunother 2019; 68(1): 121–130
https://doi.org/10.1007/s00262-018-2257-2
|
| 212 |
I Moeller, GC Spagnoli, J Finke, H Veelken, L Houet. Uptake routes of tumor-antigen MAGE-A3 by dendritic cells determine priming of naïve T-cell subtypes. Cancer Immunol Immunother 2012; 61(11): 2079–2090
https://doi.org/10.1007/s00262-012-1272-y
|
| 213 |
M Schnurr, M Orban, NC Robson, A Shin, H Braley, D Airey, J Cebon, E Maraskovsky, S Endres. ISCOMATRIX adjuvant induces efficient cross-presentation of tumor antigen by dendritic cells via rapid cytosolic antigen delivery and processing via tripeptidyl peptidase II. J Immunol 2009; 182(3): 1253–1259
https://doi.org/10.4049/jimmunol.182.3.1253
|
| 214 |
B Dreno, JF Thompson, BM Smithers, M Santinami, T Jouary, R Gutzmer, E Levchenko, P Rutkowski, JJ Grob, S Korovin, K Drucis, F Grange, L Machet, P Hersey, I Krajsova, A Testori, R Conry, B Guillot, WHJ Kruit, L Demidov, JA Thompson, I Bondarenko, J Jaroszek, S Puig, G Cinat, A Hauschild, JJ Goeman, HC van Houwelingen, F Ulloa-Montoya, A Callegaro, B Dizier, B Spiessens, M Debois, VG Brichard, J Louahed, P Therasse, C Debruyne, JM Kirkwood. MAGE-A3 immunotherapeutic as adjuvant therapy for patients with resected, MAGE-A3-positive, stage III melanoma (DERMA): a double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol 2018; 19(7): 916–929
https://doi.org/10.1016/S1470-2045(18)30254-7
|
| 215 |
JF Vansteenkiste, BC Cho, T Vanakesa, T De Pas, M Zielinski, MS Kim, J Jassem, M Yoshimura, J Dahabreh, H Nakayama, L Havel, H Kondo, T Mitsudomi, K Zarogoulidis, OA Gladkov, K Udud, H Tada, H Hoffman, A Bugge, P Taylor, EE Gonzalez, ML Liao, J He, JL Pujol, J Louahed, M Debois, V Brichard, C Debruyne, P Therasse, N Altorki. Efficacy of the MAGE-A3 cancer immunotherapeutic as adjuvant therapy in patients with resected MAGE-A3-positive non-small-cell lung cancer (MAGRIT): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol 2016; 17(6): 822–835
https://doi.org/10.1016/S1470-2045(16)00099-1
|
| 216 |
EA Mittendorf, B Lu, M Melisko, J Price Hiller, I Bondarenko, AM Brunt, G Sergii, K Petrakova, GE Peoples. Efficacy and safety analysis of Nelipepimut-S vaccine to prevent breast cancer recurrence: a randomized, multicenter, phase III clinical trial. Clin Cancer Res 2019; 25(14): 4248–4254
https://doi.org/10.1158/1078-0432.CCR-18-2867
|
| 217 |
FS Hodi, SJ O’Day, DF McDermott, RW Weber, JA Sosman, JB Haanen, R Gonzalez, C Robert, D Schadendorf, JC Hassel, W Akerley, den Eertwegh AJ van, J Lutzky, P Lorigan, JM Vaubel, GP Linette, D Hogg, CH Ottensmeier, C Lebbé, C Peschel, I Quirt, JI Clark, JD Wolchok, JS Weber, J Tian, MJ Yellin, GM Nichol, A Hoos, WJ Urba. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363(8): 711–723
https://doi.org/10.1056/NEJMoa1003466
|
| 218 |
CL Slingluff, KD Lewis, R Andtbacka, J Hyngstrom, M Milhem, SN Markovic, T Bowles, O Hamid, L Hernandez-Aya, J Claveau, S Jang, P Philips, SG Holtan, MF Shaheen, B Curti, W Schmidt, MO Butler, J Paramo, J Lutzky, A Padmanabhan, S Thomas, D Milton, A Pecora, T Sato, E Hsueh, S Badarinath, J Keech, S Kalmadi, P Kumar, R Weber, E Levine, A Berger, A Bar, JT Beck, JB Travers, C Mihalcioiu, B Gastman, P Beitsch, S Rapisuwon, J Glaspy, EC McCarron, V Gupta, D Behl, B Blumenstein, JJ Peterkin. Multicenter, double-blind, placebo-controlled trial of seviprotimut-L polyvalent melanoma vaccine in patients with post-resection melanoma at high risk of recurrence. J Immunother Cancer 2021; 9(10): e003272
https://doi.org/10.1136/jitc-2021-003272
|
| 219 |
PK Srivastava. Neoepitopes of cancers: looking back, looking ahead. Cancer Immunol Res 2015; 3(9): 969–977
https://doi.org/10.1158/2326-6066.CIR-15-0134
|
| 220 |
Z Hu, DE Leet, RL Allesøe, G Oliveira, S Li, AM Luoma, J Liu, J Forman, T Huang, JB Iorgulescu, R Holden, S Sarkizova, SH Gohil, RA Redd, J Sun, L Elagina, A Giobbie-Hurder, W Zhang, L Peter, Z Ciantra, S Rodig, O Olive, K Shetty, J Pyrdol, M Uduman, PC Lee, P Bachireddy, EI Buchbinder, CH Yoon, D Neuberg, BL Pentelute, N Hacohen, KJ Livak, SA Shukla, LR Olsen, DH Barouch, KW Wucherpfennig, EF Fritsch, DB Keskin, CJ Wu, PA Ott. Personal neoantigen vaccines induce persistent memory T cell responses and epitope spreading in patients with melanoma. Nat Med 2021; 27(3): 515–525
https://doi.org/10.1038/s41591-020-01206-4
|
| 221 |
H Chen, Z Li, L Qiu, X Dong, G Chen, Y Shi, L Cai, W Liu, H Ye, Y Zhou, J Ouyang, Z Cai, X Liu. Personalized neoantigen vaccine combined with PD-1 blockade increases CD8+ tissue-resident memory T-cell infiltration in preclinical hepatocellular carcinoma models. J Immunother Cancer 2022; 10(9): e004389
https://doi.org/10.1136/jitc-2021-004389
|
| 222 |
PA Ott, Z Hu, DB Keskin, SA Shukla, J Sun, DJ Bozym, W Zhang, A Luoma, A Giobbie-Hurder, L Peter, C Chen, O Olive, TA Carter, S Li, DJ Lieb, T Eisenhaure, E Gjini, J Stevens, WJ Lane, I Javeri, K Nellaiappan, AM Salazar, H Daley, M Seaman, EI Buchbinder, CH Yoon, M Harden, N Lennon, S Gabriel, SJ Rodig, DH Barouch, JC Aster, G Getz, K Wucherpfennig, D Neuberg, J Ritz, ES Lander, EF Fritsch, N Hacohen, CJ Wu. An immunogenic personal neoantigen vaccine for patients with melanoma. Nature 2017; 547(7662): 217–221
https://doi.org/10.1038/nature22991
|
| 223 |
CY Slaney, MH Kershaw, PK Darcy. Trafficking of T cells into tumors. Cancer Res 2014; 74(24): 7168–7174
https://doi.org/10.1158/0008-5472.CAN-14-2458
|
| 224 |
M Huang, Y Lin, C Wang, L Deng, M Chen, YG Assaraf, ZS Chen, W Ye, D Zhang. New insights into antiangiogenic therapy resistance in cancer: mechanisms and therapeutic aspects. Drug Resist Updat 2022; 64: 100849
https://doi.org/10.1016/j.drup.2022.100849
|
| 225 |
A Palazón, J Aragonés, A Morales-Kastresana, Landázuri MO de, I Melero. Molecular pathways: hypoxia response in immune cells fighting or promoting cancer. Clin Cancer Res 2012; 18(5): 1207–1213
https://doi.org/10.1158/1078-0432.CCR-11-1591
|
| 226 |
M Bellone, A Calcinotto. Ways to enhance lymphocyte trafficking into tumors and fitness of tumor infiltrating lymphocytes. Front Oncol 2013; 3: 231
https://doi.org/10.3389/fonc.2013.00231
|
| 227 |
WS Lee, H Yang, HJ Chon, C Kim. Combination of anti-angiogenic therapy and immune checkpoint blockade normalizes vascular-immune crosstalk to potentiate cancer immunity. Exp Mol Med 2020; 52(9): 1475–1485
https://doi.org/10.1038/s12276-020-00500-y
|
| 228 |
K Shigeta, M Datta, T Hato, S Kitahara, IX Chen, A Matsui, H Kikuchi, E Mamessier, S Aoki, RR Ramjiawan, H Ochiai, N Bardeesy, P Huang, M Cobbold, AX Zhu, RK Jain, DG Duda. Dual programmed death receptor-1 and vascular endothelial growth factor receptor-2 blockade promotes vascular normalization and enhances antitumor immune responses in hepatocellular carcinoma. Hepatology 2020; 71(4): 1247–1261
https://doi.org/10.1002/hep.30889
|
| 229 |
CG Kim, M Jang, Y Kim, G Leem, KH Kim, H Lee, TS Kim, SJ Choi, HD Kim, JW Han, M Kwon, JH Kim, AJ Lee, SK Nam, SJ Bae, SB Lee, SJ Shin, SH Park, JB Ahn, I Jung, KY Lee, SH Park, H Kim, BS Min, EC Shin. VEGF-A drives TOX-dependent T cell exhaustion in anti-PD-1-resistant microsatellite stable colorectal cancers. Sci Immunol 2019; 4(41): eaay0555
https://doi.org/10.1126/sciimmunol.aay0555
|
| 230 |
BI Rini, ER Plimack, V Stus, R Gafanov, R Hawkins, D Nosov, F Pouliot, B Alekseev, D Soulières, B Melichar, I Vynnychenko, A Kryzhanivska, I Bondarenko, SJ Azevedo, D Borchiellini, C Szczylik, M Markus, RS McDermott, J Bedke, S Tartas, YH Chang, S Tamada, Q Shou, RF Perini, M Chen, MB Atkins, T; KEYNOTE-426 Investigators Powles. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N Engl J Med 2019; 380(12): 1116–1127
https://doi.org/10.1056/NEJMoa1816714
|
| 231 |
BI Rini, T Powles, MB Atkins, B Escudier, DF McDermott, C Suarez, S Bracarda, WM Stadler, F Donskov, JL Lee, R Hawkins, A Ravaud, B Alekseev, M Staehler, M Uemura, Giorgi U De, B Mellado, C Porta, B Melichar, H Gurney, J Bedke, TK Choueiri, F Parnis, T Khaznadar, A Thobhani, S Li, E Piault-Louis, G Frantz, M Huseni, C Schiff, MC Green, RJ; IMmotion151 Study Group Motzer. Atezolizumab plus bevacizumab versus sunitinib in patients with previously untreated metastatic renal cell carcinoma (IMmotion151): a multicentre, open-label, phase 3, randomised controlled trial. Lancet 2019; 393(10189): 2404–2415
https://doi.org/10.1016/S0140-6736(19)30723-8
|
| 232 |
RJ Motzer, T Powles, MB Atkins, B Escudier, DF McDermott, BY Alekseev, JL Lee, C Suarez, D Stroyakovskiy, U De Giorgi, F Donskov, B Mellado, R Banchereau, H Hamidi, O Khan, V Craine, M Huseni, N Flinn, S Dubey, BI Rini. Final overall survival and molecular analysis in IMmotion151, a phase 3 trial comparing atezolizumab plus bevacizumab vs sunitinib in patients with previously untreated metastatic renal cell carcinoma. JAMA Oncol 2022; 8(2): 275–280
https://doi.org/10.1001/jamaoncol.2021.5981
|
| 233 |
S Rafiq, CS Hackett, RJ Brentjens. Engineering strategies to overcome the current roadblocks in CAR T cell therapy. Nat Rev Clin Oncol 2020; 17(3): 147–167
https://doi.org/10.1038/s41571-019-0297-y
|
| 234 |
L Miao, Z Zhang, Z Ren, F Tang, Y Li. Obstacles and coping strategies of CAR-T cell immunotherapy in solid tumors. Front Immunol 2021; 12: 687822
https://doi.org/10.3389/fimmu.2021.687822
|
| 235 |
DL Porter, BL Levine, M Kalos, A Bagg, CH June. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011; 365(8): 725–733
https://doi.org/10.1056/NEJMoa1103849
|
| 236 |
SL Maude, N Frey, PA Shaw, R Aplenc, DM Barrett, NJ Bunin, A Chew, VE Gonzalez, Z Zheng, SF Lacey, YD Mahnke, JJ Melenhorst, SR Rheingold, A Shen, DT Teachey, BL Levine, CH June, DL Porter, SA Grupp. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med 2014; 371(16): 1507–1517
https://doi.org/10.1056/NEJMoa1407222
|
| 237 |
RJ Brentjens, I Rivière, JH Park, ML Davila, X Wang, J Stefanski, C Taylor, R Yeh, S Bartido, O Borquez-Ojeda, M Olszewska, Y Bernal, H Pegram, M Przybylowski, D Hollyman, Y Usachenko, D Pirraglia, J Hosey, E Santos, E Halton, P Maslak, D Scheinberg, J Jurcic, M Heaney, G Heller, M Frattini, M Sadelain. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood 2011; 118(18): 4817–4828
https://doi.org/10.1182/blood-2011-04-348540
|
| 238 |
F Marofi, R Motavalli, VA Safonov, L Thangavelu, AV Yumashev, M Alexander, N Shomali, MS Chartrand, Y Pathak, M Jarahian, S Izadi, A Hassanzadeh, N Shirafkan, S Tahmasebi, FM Khiavi. CAR T cells in solid tumors: challenges and opportunities. Stem Cell Res Ther 2021; 12(1): 81
https://doi.org/10.1186/s13287-020-02128-1
|
| 239 |
SJ Bagley, DM O’Rourke. Clinical investigation of CAR T cells for solid tumors: lessons learned and future directions. Pharmacol Ther 2020; 205: 107419
https://doi.org/10.1016/j.pharmthera.2019.107419
|
| 240 |
M Hegde, M Mukherjee, Z Grada, A Pignata, D Landi, SA Navai, A Wakefield, K Fousek, K Bielamowicz, KK Chow, VS Brawley, TT Byrd, S Krebs, S Gottschalk, WS Wels, ML Baker, G Dotti, M Mamonkin, MK Brenner, JS Orange, N Ahmed. Tandem CAR T cells targeting HER2 and IL13Rα2 mitigate tumor antigen escape. J Clin Invest 2016; 126(8): 3036–3052
https://doi.org/10.1172/JCI83416
|
| 241 |
BD Choi, X Yu, AP Castano, AA Bouffard, A Schmidts, RC Larson, SR Bailey, AC Boroughs, MJ Frigault, MB Leick, I Scarfò, CL Cetrulo, S Demehri, BV Nahed, DP Cahill, H Wakimoto, WT Curry, BS Carter, MV Maus. CAR-T cells secreting BiTEs circumvent antigen escape without detectable toxicity. Nat Biotechnol 2019; 37(9): 1049–1058
https://doi.org/10.1038/s41587-019-0192-1
|
| 242 |
R Xu, S Du, J Zhu, F Meng, B Liu. Neoantigen-targeted TCR-T cell therapy for solid tumors: how far from clinical application. Cancer Lett 2022; 546: 215840
https://doi.org/10.1016/j.canlet.2022.215840
|
| 243 |
RA Morgan, ME Dudley, JR Wunderlich, MS Hughes, JC Yang, RM Sherry, RE Royal, SL Topalian, US Kammula, NP Restifo, Z Zheng, A Nahvi, CR de Vries, LJ Rogers-Freezer, SA Mavroukakis, SA Rosenberg. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006; 314(5796): 126–129
https://doi.org/10.1126/science.1129003
|
| 244 |
SWL Lee, G Adriani, E Ceccarello, A Pavesi, AT Tan, A Bertoletti, RD Kamm, SC Wong. Characterizing the role of monocytes in T cell cancer immunotherapy using a 3D microfluidic model. Front Immunol 2018; 9: 416
https://doi.org/10.3389/fimmu.2018.00416
|
| 245 |
A Pavesi, AT Tan, S Koh, A Chia, M Colombo, E Antonecchia, C Miccolis, E Ceccarello, G Adriani, MT Raimondi, RD Kamm, A Bertoletti. A 3D microfluidic model for preclinical evaluation of TCR-engineered T cells against solid tumors. JCI Insight 2017; 2(12): e89762
https://doi.org/10.1172/jci.insight.89762
|
| 246 |
SA Rosenberg, BS Packard, PM Aebersold, D Solomon, SL Topalian, ST Toy, P Simon, MT Lotze, JC Yang, CA Seipp, C Simpson, C Carter, S Bock, D Schwartzentruber, JP Wei, DE White. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med 1988; 319(25): 1676–1680
https://doi.org/10.1056/NEJM198812223192527
|
| 247 |
ME Dudley, JC Yang, R Sherry, MS Hughes, R Royal, U Kammula, PF Robbins, J Huang, DE Citrin, SF Leitman, J Wunderlich, NP Restifo, A Thomasian, SG Downey, FO Smith, J Klapper, K Morton, C Laurencot, DE White, SA Rosenberg. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008; 26(32): 5233–5239
https://doi.org/10.1200/JCO.2008.16.5449
|
| 248 |
P Kvistborg, CJ Shu, B Heemskerk, M Fankhauser, CA Thrue, M Toebes, N van Rooij, C Linnemann, MM van Buuren, JH Urbanus, JB Beltman, P Thor Straten, YF Li, PF Robbins, MJ Besser, J Schachter, GG Kenter, ME Dudley, SA Rosenberg, JB Haanen, SR Hadrup, TN Schumacher. TIL therapy broadens the tumor-reactive CD8+ T cell compartment in melanoma patients. OncoImmunology 2012; 1(4): 409–418
https://doi.org/10.4161/onci.18851
|
| 249 |
TN Schumacher, RD Schreiber. Neoantigens in cancer immunotherapy. Science 2015; 348(6230): 69–74
https://doi.org/10.1126/science.aaa4971
|
| 250 |
Y Zhao, J Deng, S Rao, S Guo, J Shen, F Du, X Wu, Y Chen, M Li, M Chen, X Li, W Li, L Gu, Y Sun, Z Zhang, Q Wen, Z Xiao, J Li. Tumor infiltrating lymphocyte (TIL) therapy for solid tumor treatment: progressions and challenges. Cancers (Basel) 2022; 14(17): 4160
https://doi.org/10.3390/cancers14174160
|
| 251 |
E Tran, PF Robbins, YC Lu, TD Prickett, JJ Gartner, L Jia, A Pasetto, Z Zheng, S Ray, EM Groh, IR Kriley, SA Rosenberg. T-cell transfer therapy targeting mutant kras in cancer. N Engl J Med 2016; 375(23): 2255–2262
https://doi.org/10.1056/NEJMoa1609279
|
| 252 |
BC Creelan, C Wang, JK Teer, EM Toloza, J Yao, S Kim, AM Landin, JE Mullinax, JJ Saller, AN Saltos, DR Noyes, LB Montoya, W Curry, SA Pilon-Thomas, AA Chiappori, T Tanvetyanon, FJ Kaye, ZJ Thompson, SJ Yoder, B Fang, JM Koomen, AA Sarnaik, DT Chen, JR Conejo-Garcia, EB Haura, SJ Antonia. Tumor-infiltrating lymphocyte treatment for anti-PD-1-resistant metastatic lung cancer: a phase 1 trial. Nat Med 2021; 27(8): 1410–1418
https://doi.org/10.1038/s41591-021-01462-y
|
| 253 |
RC Augustin, RD Leone, A Naing, L Fong, R Bao, JJ Luke. Next steps for clinical translation of adenosine pathway inhibition in cancer immunotherapy. J Immunother Cancer 2022; 10(2): e004089
https://doi.org/10.1136/jitc-2021-004089
|
| 254 |
RD Leone, LA Emens. Targeting adenosine for cancer immunotherapy. J Immunother Cancer 2018; 6(1): 57
https://doi.org/10.1186/s40425-018-0360-8
|
| 255 |
S Apasov, M Koshiba, F Redegeld, MV Sitkovsky. Role of extracellular ATP and P1 and P2 classes of purinergic receptors in T-cell development and cytotoxic T lymphocyte effector functions. Immunol Rev 1995; 146(1): 5–19
https://doi.org/10.1111/j.1600-065X.1995.tb00680.x
|
| 256 |
SG Apasov, M Koshiba, TM Chused, MV Sitkovsky. Effects of extracellular ATP and adenosine on different thymocyte subsets: possible role of ATP-gated channels and G protein-coupled purinergic receptor. J Immunol 1997; 158(11): 5095–5105
https://doi.org/10.4049/jimmunol.158.11.5095
|
| 257 |
A Filippini, RE Taffs, T Agui, MV Sitkovsky. Ecto-ATPase activity in cytolytic T-lymphocytes. Protection from the cytolytic effects of extracellular ATP. J Biol Chem 1990; 265(1): 334–340
https://doi.org/10.1016/S0021-9258(19)40234-2
|
| 258 |
A Ohta, E Gorelik, SJ Prasad, F Ronchese, D Lukashev, MK Wong, X Huang, S Caldwell, K Liu, P Smith, JF Chen, EK Jackson, S Apasov, S Abrams, M Sitkovsky. A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci USA 2006; 103(35): 13132–13137
https://doi.org/10.1073/pnas.0605251103
|
| 259 |
R Iannone, L Miele, P Maiolino, A Pinto, S Morello. Adenosine limits the therapeutic effectiveness of anti-CTLA4 mAb in a mouse melanoma model. Am J Cancer Res 2014; 4(2): 172–181
|
| 260 |
D Mittal, A Young, K Stannard, M Yong, MW Teng, B Allard, J Stagg, MJ Smyth. Antimetastatic effects of blocking PD-1 and the adenosine A2A receptor. Cancer Res 2014; 74(14): 3652–3658
https://doi.org/10.1158/0008-5472.CAN-14-0957
|
| 261 |
PA Beavis, MA Henderson, L Giuffrida, JK Mills, K Sek, RS Cross, AJ Davenport, LB John, S Mardiana, CY Slaney, RW Johnstone, JA Trapani, J Stagg, S Loi, L Kats, D Gyorki, MH Kershaw, PK Darcy. Targeting the adenosine 2A receptor enhances chimeric antigen receptor T cell efficacy. J Clin Invest 2017; 127(3): 929–941
https://doi.org/10.1172/JCI89455
|
| 262 |
MV Sitkovsky. Lessons from the A2A adenosine receptor antagonist-enabled tumor regression and survival in patients with treatment-refractory renal cell cancer. Cancer Discov 2020; 10(1): 16–19
https://doi.org/10.1158/2159-8290.CD-19-1280
|
| 263 |
J Stagg, U Divisekera, N McLaughlin, J Sharkey, S Pommey, D Denoyer, KM Dwyer, MJ Smyth. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci USA 2010; 107(4): 1547–1552
https://doi.org/10.1073/pnas.0908801107
|
| 264 |
J Stagg, PA Beavis, U Divisekera, MC Liu, A Möller, PK Darcy, MJ Smyth. CD73-deficient mice are resistant to carcinogenesis. Cancer Res 2012; 72(9): 2190–2196
https://doi.org/10.1158/0008-5472.CAN-12-0420
|
| 265 |
MG Terp, KA Olesen, EC Arnspang, RR Lund, BC Lagerholm, HJ Ditzel, R Leth-Larsen. Anti-human CD73 monoclonal antibody inhibits metastasis formation in human breast cancer by inducing clustering and internalization of CD73 expressed on the surface of cancer cells. J Immunol 2013; 191(8): 4165–4173
https://doi.org/10.4049/jimmunol.1301274
|
| 266 |
BG Leclerc, R Charlebois, G Chouinard, B Allard, S Pommey, F Saad, J Stagg. CD73 expression is an independent prognostic factor in prostate cancer. Clin Cancer Res 2016; 22(1): 158–166
https://doi.org/10.1158/1078-0432.CCR-15-1181
|
| 267 |
S Loi, S Pommey, B Haibe-Kains, PA Beavis, PK Darcy, MJ Smyth, J Stagg. CD73 promotes anthracycline resistance and poor prognosis in triple negative breast cancer. Proc Natl Acad Sci USA 2013; 110(27): 11091–11096
https://doi.org/10.1073/pnas.1222251110
|
| 268 |
PO Gaudreau, B Allard, M Turcotte, J Stagg. CD73-adenosine reduces immune responses and survival in ovarian cancer patients. OncoImmunology 2016; 5(5): e1127496
https://doi.org/10.1080/2162402X.2015.1127496
|
| 269 |
XR Wu, XS He, YF Chen, RX Yuan, Y Zeng, L Lian, YF Zou, N Lan, XJ Wu, P Lan. High expression of CD73 as a poor prognostic biomarker in human colorectal cancer. J Surg Oncol 2012; 106(2): 130–137
https://doi.org/10.1002/jso.23056
|
| 270 |
S Morello, M Capone, C Sorrentino, D Giannarelli, G Madonna, D Mallardo, AM Grimaldi, A Pinto, PA Ascierto. Soluble CD73 as biomarker in patients with metastatic melanoma patients treated with nivolumab. J Transl Med 2017; 15(1): 244
https://doi.org/10.1186/s12967-017-1348-8
|
| 271 |
RS Herbst, M Majem, F Barlesi, E Carcereny, Q Chu, I Monnet, A Sanchez-Hernandez, S Dakhil, DR Camidge, L Winzer, Y Soo-Hoo, ZA Cooper, R Kumar, J Bothos, C Aggarwal, A Martinez-Marti. COAST: an open-label, phase II, multidrug platform study of durvalumab alone or in combination with oleclumab or monalizumab in patients with unresectable, stage III non-small-cell lung cancer. J Clin Oncol 2022; 40(29): 3383–3393
https://doi.org/10.1200/JCO.22.00227
|
| 272 |
A Ohta. A Metabolic immune checkpoint: adenosine in tumor microenvironment. Front Immunol 2016; 7: 109
https://doi.org/10.3389/fimmu.2016.00109
|
| 273 |
N Bonnefoy, J Bastid, G Alberici, A Bensussan, JF Eliaou. CD39: a complementary target to immune checkpoints to counteract tumor-mediated immunosuppression. OncoImmunology 2015; 4(5): e1003015
https://doi.org/10.1080/2162402X.2014.1003015
|
| 274 |
S Deaglio, KM Dwyer, W Gao, D Friedman, A Usheva, A Erat, JF Chen, K Enjyoji, J Linden, M Oukka, VK Kuchroo, TB Strom, SC Robson. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204(6): 1257–1265
https://doi.org/10.1084/jem.20062512
|
| 275 |
X Sun, Y Wu, W Gao, K Enjyoji, E Csizmadia, CE Müller, T Murakami, SC Robson. CD39/ENTPD1 expression by CD4+Foxp3+ regulatory T cells promotes hepatic metastatic tumor growth in mice. Gastroenterology 2010; 139(3): 1030–1040
https://doi.org/10.1053/j.gastro.2010.05.007
|
| 276 |
M Michaud, I Martins, AQ Sukkurwala, S Adjemian, Y Ma, P Pellegatti, S Shen, O Kepp, M Scoazec, G Mignot, S Rello-Varona, M Tailler, L Menger, E Vacchelli, L Galluzzi, F Ghiringhelli, F di Virgilio, L Zitvogel, G Kroemer. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011; 334(6062): 1573–1577
https://doi.org/10.1126/science.1208347
|
| 277 |
XY Cai, XC Ni, Y Yi, HW He, JX Wang, YP Fu, J Sun, J Zhou, YF Cheng, JJ Jin, J Fan, SJ Qiu. Overexpression of CD39 in hepatocellular carcinoma is an independent indicator of poor outcome after radical resection. Medicine (Baltimore) 2016; 95(40): e4989
https://doi.org/10.1097/MD.0000000000004989
|
| 278 |
XY Cai, XF Wang, J Li, JN Dong, JQ Liu, NP Li, B Yun, RL Xia, J Qin, YH Sun. High expression of CD39 in gastric cancer reduces patient outcome following radical resection. Oncol Lett 2016; 12(5): 4080–4086
https://doi.org/10.3892/ol.2016.5189
|
| 279 |
C Perry, I Hazan-Halevy, S Kay, M Cipok, D Grisaru, V Deutsch, A Polliack, E Naparstek, Y Herishanu. Increased CD39 expression on CD4+ T lymphocytes has clinical and prognostic significance in chronic lymphocytic leukemia. Ann Hematol 2012; 91(8): 1271–1279
https://doi.org/10.1007/s00277-012-1425-2
|
| 280 |
S Colak, P Ten Dijke. Targeting TGF-β signaling in cancer. Trends Cancer 2017; 3(1): 56–71
https://doi.org/10.1016/j.trecan.2016.11.008
|
| 281 |
DVF Tauriello, S Palomo-Ponce, D Stork, A Berenguer-Llergo, J Badia-Ramentol, M Iglesias, M Sevillano, S Ibiza, A Cañellas, X Hernando-Momblona, D Byrom, JA Matarin, A Calon, EI Rivas, AR Nebreda, A Riera, CS Attolini, E Batlle. TGFβ drives immune evasion in genetically reconstituted colon cancer metastasis. Nature 2018; 554(7693): 538–543
https://doi.org/10.1038/nature25492
|
| 282 |
CY Huang, CL Chung, TH Hu, JJ Chen, PF Liu, CL Chen. Recent progress in TGF-β inhibitors for cancer therapy. Biomed Pharmacother 2021; 134: 111046
https://doi.org/10.1016/j.biopha.2020.111046
|
| 283 |
C Fang, J Lin, T Zhang, J Luo, D Nie, M Li, X Hu, Y Zheng, X Huang, Z Xiao. Metastatic colorectal cancer patient with microsatellite stability and BRAFV600E mutation showed a complete metabolic response to PD-1 blockade and bevacizumab: a case report. Front Oncol 2021; 11: 652394
https://doi.org/10.3389/fonc.2021.652394
|
| 284 |
KM Knudson, KC Hicks, X Luo, JQ Chen, J Schlom, SR Gameiro. M7824, a novel bifunctional anti-PD-L1/TGFβ Trap fusion protein, promotes anti-tumor efficacy as monotherapy and in combination with vaccine. OncoImmunology 2018; 7(5): e1426519
https://doi.org/10.1080/2162402X.2018.1426519
|
| 285 |
B Tan, A Khattak, E Felip, K Kelly, P Rich, D Wang, C Helwig, I Dussault, LS Ojalvo, N Isambert. Bintrafusp Alfa, a bifunctional fusion protein targeting TGF-β and PD-L1, in patients with esophageal adenocarcinoma: results from a phase 1 cohort. Target Oncol 2021; 16(4): 435–446
https://doi.org/10.1007/s11523-021-00809-2
|
| 286 |
M Zamanakou, AE Germenis, V Karanikas. Tumor immune escape mediated by indoleamine 2,3-dioxygenase. Immunol Lett 2007; 111(2): 69–75
https://doi.org/10.1016/j.imlet.2007.06.001
|
| 287 |
MMT Zhu, AR Dancsok, TO Nielsen. Indoleamine dioxygenase inhibitors: clinical rationale and current development. Curr Oncol Rep 2019; 21(1): 2
https://doi.org/10.1007/s11912-019-0750-1
|
| 288 |
S Tang, Q Ning, L Yang, Z Mo, S Tang. Mechanisms of immune escape in the cancer immune cycle. Int Immunopharmacol 2020; 86: 106700
https://doi.org/10.1016/j.intimp.2020.106700
|
| 289 |
RB Holmgaard, D Zamarin, Y Li, B Gasmi, DH Munn, JP Allison, T Merghoub, JD Wolchok. Tumor-expressed IDO recruits and activates MDSCs in a Treg-dependent manner. Cell Rep 2015; 13(2): 412–424
https://doi.org/10.1016/j.celrep.2015.08.077
|
| 290 |
AB Blair, J Kleponis, DL 2nd Thomas, ST Muth, AG Murphy, V Kim, L Zheng. IDO1 inhibition potentiates vaccine-induced immunity against pancreatic adenocarcinoma. J Clin Invest 2019; 129(4): 1742–1755
https://doi.org/10.1172/JCI124077
|
| 291 |
RB Holmgaard, D Zamarin, DH Munn, JD Wolchok, JP Allison. Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4. J Exp Med 2013; 210(7): 1389–1402
https://doi.org/10.1084/jem.20130066
|
| 292 |
AJ Muller, JB DuHadaway, PS Donover, E Sutanto-Ward, GC Prendergast. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med 2005; 11(3): 312–319
https://doi.org/10.1038/nm1196
|
| 293 |
S Spranger, HK Koblish, B Horton, PA Scherle, R Newton, TF Gajewski. Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8+ T cells directly within the tumor microenvironment. J Immunother Cancer 2014; 2(1): 3
https://doi.org/10.1186/2051-1426-2-3
|
| 294 |
C Uyttenhove, L Pilotte, I Théate, V Stroobant, D Colau, N Parmentier, T Boon, den Eynde BJ Van. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 2003; 9(10): 1269–1274
https://doi.org/10.1038/nm934
|
| 295 |
GV Long, R Dummer, O Hamid, TF Gajewski, C Caglevic, S Dalle, A Arance, MS Carlino, JJ Grob, TM Kim, L Demidov, C Robert, J Larkin, JR Anderson, J Maleski, M Jones, SJ Diede, TC Mitchell. Epacadostat plus pembrolizumab versus placebo plus pembrolizumab in patients with unresectable or metastatic melanoma (ECHO-301/KEYNOTE-252): a phase 3, randomised, double-blind study. Lancet Oncol 2019; 20(8): 1083–1097
https://doi.org/10.1016/S1470-2045(19)30274-8
|
| 296 |
G Stanta, S Bonin. Overview on clinical relevance of intra-tumor heterogeneity. Front Med (Lausanne) 2018; 5: 85
https://doi.org/10.3389/fmed.2018.00085
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
