Please wait a minute...
Shopping Cart Email List Chinese
Advanced Search Fig/Tab
Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Featured Articles  |  Most Downloaded  |  Most Reading
Online Submission Subscribe to Our RSS Content Feed
Front. Med.    2021, Vol. 15 Issue (4) : 551-561    https://doi.org/10.1007/s11684-020-0760-2
REVIEW
Intratumor heterogeneity, microenvironment, and mechanisms of drug resistance in glioma recurrence and evolution
Zhaoshi Bao1,2,5, Yongzhi Wang1,2, Qiangwei Wang1, Shengyu Fang1, Xia Shan1,7, Jiguang Wang3, Tao Jiang1,2,4,6()
1. Beijing Neurosurgical Institute, Capital Medical University, Beijing 100050, China
2. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100050, China
3. Divison of Life Science, Department of Chemical and Biological Engineering, Center for Systems Biology and Human Health, and State Key Laboratory of Molecular Neuroscience, The Hong Kong University of Science and Technology, Hong Kong, China
4. China National Clinical Research Center for Neurological Diseases, Beijing 100050, China
5. Division of Life Science, Hong Kong University of Science and Technology, Hong Kong, China
6. Center of Brain Tumor, Beijing Institute for Brain Disorders, Beijing 100069, China
7. Department of Radiotherapy, Beijing Tiantan Hospital, Capital Medical University, Beijing 100050, China
 Download: PDF(487 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Glioma is the most common lethal tumor of the human brain. The median survival of patients with primary World Health Organization grade IV glioma is only 14.6 months. The World Health Organization classification of tumors of the central nervous system categorized gliomas into lower-grade gliomas and glioblastomas. Unlike primary glioblastoma that usually develop de novo in the elderly, secondary glioblastoma enriched with an isocitrate dehydrogenase mutant typically progresses from lower-grade glioma within 5–10 years from the time of diagnosis. Based on various evolutional trajectories brought on by clonal and subclonal alterations, the evolution patterns of glioma vary according to different theories. Some important features distinguish the normal brain from other tissues, e.g., the composition of the microenvironment around the tumor cells, the presence of the blood-brain barrier, and others. The underlying mechanism of glioma recurrence and evolution patterns of glioma are different from those of other types of cancer. Several studies correlated tumor recurrence with tumor heterogeneity and the immune microenvironment. However, the detailed reasons for the progression and recurrence of glioma remain controversial. In this review, we introduce the different mechanisms involved in glioma progression, including tumor heterogeneity, the tumor microenvironment and drug resistance, and their pre-clinical implements in clinical trials. This review aimed to provide new insights into further clinical strategies for the treatment of patients with recurrent and secondary glioma.
Keywords glioma      evolution mechanism      strategies      tumor heterogeneity      secondary glioma     
Corresponding Author(s): Tao Jiang   
Just Accepted Date: 13 January 2021   Online First Date: 22 April 2021    Issue Date: 23 September 2021
 Cite this article:   
Zhaoshi Bao,Yongzhi Wang,Qiangwei Wang, et al. Intratumor heterogeneity, microenvironment, and mechanisms of drug resistance in glioma recurrence and evolution[J]. Front. Med., 2021, 15(4): 551-561.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-020-0760-2
https://academic.hep.com.cn/fmd/EN/Y2021/V15/I4/551
Fig.1  Mechanisms of glioma progression. (A) Patterns of glioma evolution. Model I: both samples are monophyletic (“branching evolution”) due to founder clonal genetic alterations. Model II: recurrence monophyletic, nested within tumors owing to the subclonal genetic alterations. Red circles indicate the founder clone, whereas multicolor circles indicate subclones. Circles indicate the time point of diagnosis of primary and recurrent glioma. (B) Heterogeneity in glioma. (C) Microenvironment of glioma. (D) Drug resistance in glioma. All cell types are listed at the bottom of the figure.
NCT number Title Conditions Interventions
NCT00271609 Bevacizumab for recurrent malignant glioma Recurrent high-grade gliomas/malignant gliomas Drug: bevacizumab
NCT01738646 Ph II SAHA and bevacizumab for recurrent malignant glioma patients Recurrent glioblastoma multiforme/malignant glioma/adult brain tumor Drug: vorinostat/drug: bevacizumab
NCT00619112 Temozolomide in treating patients with recurrent high-grade glioma Recurrent central nervous system neoplasm Drug: temozolomide
NCT00597493 Ph. 2 sorafenib+ protracted temozolomide in recurrent GBM Recurrent glioblastoma multiforme Drug: sorafenib and temozolomide
NCT00575146 Ketogenic diet for recurrent glioblastoma Recurrent glioblastoma Dietary supplement: TAVARLIN
NCT00777153 Cediranib in combination with lomustine
chemotherapy in recurrent glioblastoma		 Recurrent Glioblastoma Drug: cediranib/drug: lomustine
chemotherapy/drug: placebo cediranib
Tab.1  Completed clinical trials for recurrent glioma
1 Y Wang, T Jiang. Understanding high grade glioma: molecular mechanism, therapy and comprehensive management. Cancer Lett 2013; 331(2): 139–146
https://doi.org/10.1016/j.canlet.2012.12.024 pmid: 23340179
2 DN Louis, H Ohgaki, OD Wiestler, WK Cavenee, PC Burger, A Jouvet, BW Scheithauer, P Kleihues. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007; 114(2): 97–109
https://doi.org/10.1007/s00401-007-0243-4 pmid: 17618441
3 D Schiff, M van den Bent, MA Vogelbaum, W Wick, CR Miller, M Taphoorn, W Pope, PD Brown, M Platten, R Jalali, T Armstrong, PY Wen. Recent developments and future directions in adult lower-grade gliomas: Society for Neuro-Oncology (SNO) and European Association of Neuro-Oncology (EANO) Consensus. Neuro Oncol 2019; 21(7):837–853
https://doi.org/10.1093/neuonc/noz033 pmid: 30753579
4 H Ohgaki, P Kleihues. Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci 2009; 100(12): 2235–2241
https://doi.org/10.1111/j.1349-7006.2009.01308.x pmid: 19737147
5 WK Cavenee, FB Furnari, M Nagane. Diffusely infiltrating astrocytomas. In: Kleihues P, Cavenee WK. Pathology and Genetics of Tumors of the Nervous System. WHO Classification of Tumors. Lyon: IARC press, 2000: 10–21
6 H Kim, S Zheng, SS Amini, SM Virk, T Mikkelsen, DJ Brat, J Grimsby, C Sougnez, F Muller, J Hu, AE Sloan, ML Cohen, EG Van Meir, L Scarpace, PW Laird, JN Weinstein, ES Lander, S Gabriel, G Getz, M Meyerson, L Chin, JS Barnholtz-Sloan, RG Verhaak. Whole-genome and multisector exome sequencing of primary and post-treatment glioblastoma reveals patterns of tumor evolution. Genome Res 2015; 25(3): 316–327
https://doi.org/10.1101/gr.180612.114 pmid: 25650244
7 J Kim, IH Lee, HJ Cho, CK Park, YS Jung, Y Kim, SH Nam, BS Kim, MD Johnson, DS Kong, HJ Seol, JI Lee, KM Joo, Y Yoon, WY Park, J Lee, PJ Park, DH Nam. Spatiotemporal evolution of the primary glioblastoma genome. Cancer Cell 2015; 28(3): 318–328
https://doi.org/10.1016/j.ccell.2015.07.013 pmid: 26373279
8 M Ceccarelli, FP Barthel, TM Malta, TS Sabedot, SR Salama, BA Murray, O Morozova, Y Newton, A Radenbaugh, SM Pagnotta, S Anjum, J Wang, G Manyam, P Zoppoli, S Ling, AA Rao, M Grifford, AD Cherniack, H Zhang, L Poisson, CG Carlotti Jr, DP Tirapelli, A Rao, T Mikkelsen, CC Lau, WK Yung, R Rabadan, J Huse, DJ Brat, NL Lehman, JS Barnholtz-Sloan, S Zheng, K Hess, G Rao, M Meyerson, R Beroukhim, L Cooper, R Akbani, M Wrensch, D Haussler, KD Aldape, PW Laird, DH Gutmann; TCGA Research Network, Noushmehr H, Iavarone A, Verhaak RG. Molecular profiling reveals biologically discrete subsets and pathways of progression in diffuse glioma. Cell 2016; 164(3): 550–563
https://doi.org/10.1016/j.cell.2015.12.028 pmid: 26824661
9 BE Johnson, T Mazor, C Hong, M Barnes, K Aihara, CY McLean, SD Fouse, S Yamamoto, H Ueda, K Tatsuno, S Asthana, LE Jalbert, SJ Nelson, AW Bollen, WC Gustafson, E Charron, WA Weiss, IV Smirnov, JS Song, AB Olshen, S Cha, Y Zhao, RA Moore, AJ Mungall, SJM Jones, M Hirst, MA Marra, N Saito, H Aburatani, A Mukasa, MS Berger, SM Chang, BS Taylor, JF Costello. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 2014; 343(6167): 189–193
https://doi.org/10.1126/science.1239947 pmid: 24336570
10 T Mazor, C Chesnelong, A Pankov, LE Jalbert, C Hong, J Hayes, IV Smirnov, R Marshall, CF Souza, Y Shen, P Viswanath, H Noushmehr, SM Ronen, SJM Jones, MA Marra, JG Cairncross, A Perry, SJ Nelson, SM Chang, AW Bollen, AM Molinaro, H Bengtsson, AB Olshen, S Weiss, JJ Phillips, HA Luchman, JF Costello. Clonal expansion and epigenetic reprogramming following deletion or amplification of mutant IDH1. Proc Natl Acad Sci USA 2017; 114(40): 10743–10748
https://doi.org/10.1073/pnas.1708914114 pmid: 28916733
11 J Wang, E Cazzato, E Ladewig, V Frattini, DI Rosenbloom, S Zairis, F Abate, Z Liu, O Elliott, YJ Shin, JK Lee, IH Lee, WY Park, M Eoli, AJ Blumberg, A Lasorella, DH Nam, G Finocchiaro, A Iavarone, R Rabadan. Clonal evolution of glioblastoma under therapy. Nat Genet 2016; 48(7): 768–776
https://doi.org/10.1038/ng.3590 pmid: 27270107
12 FP Barthel, KC Johnson, FS Varn, AD Moskalik, G Tanner, E Kocakavuk, KJ Anderson, O Abiola, K Aldape, KD Alfaro, D Alpar, SB Amin, DM Ashley, P Bandopadhayay, JS Barnholtz-Sloan, R Beroukhim, C Bock, PK Brastianos, DJ Brat, AR Brodbelt, AF Bruns, KR Bulsara, A Chakrabarty, A Chakravarti, JH Chuang, EB Claus, EJ Cochran, J Connelly, JF Costello, G Finocchiaro, MN Fletcher, PJ French, HK Gan, MR Gilbert, PV Gould, MR Grimmer, A Iavarone, A Ismail, MD Jenkinson, M Khasraw, H Kim, MCM Kouwenhoven, PS LaViolette, M Li, P Lichter, KL Ligon, AK Lowman, TM Malta, T Mazor, KL McDonald, AM Molinaro, DH Nam, N Nayyar, HK Ng, CY Ngan, SP Niclou, JM Niers, H Noushmehr, J Noorbakhsh, DR Ormond, CK Park, LM Poisson, R Rabadan, B Radlwimmer, G Rao, G Reifenberger, JK Sa, M Schuster, BL Shaw, SC Short, PAS Smitt, AE Sloan, M Smits, H Suzuki, G Tabatabai, EG Van Meir, C Watts, M Weller, P Wesseling, BA Westerman, G Widhalm, A Woehrer, WKA Yung, G Zadeh, JT Huse, JF De Groot, LF Stead, RGW Verhaak; GLASS Consortium. Longitudinal molecular trajectories of diffuse glioma in adults. Nature 2019; 576(7785): 112–120
https://doi.org/10.1038/s41586-019-1775-1 pmid: 31748746
13 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 pmid: 28187284
14 LB Alexandrov, PH Jones, DC Wedge, JE Sale, PJ Campbell, S Nik-Zainal, MR Stratton. Clock-like mutational processes in human somatic cells. Nat Genet 2015; 47(12): 1402–1407
https://doi.org/10.1038/ng.3441 pmid: 26551669
15 A Sottoriva, H Kang, Z Ma, TA Graham, MP Salomon, J Zhao, P Marjoram, K Siegmund, MF Press, D Shibata, C Curtis. A Big Bang model of human colorectal tumor growth. Nat Genet 2015; 47(3): 209–216
https://doi.org/10.1038/ng.3214 pmid: 25665006
16 PJ Campbell, S Yachida, LJ Mudie, PJ Stephens, ED Pleasance, LA Stebbings, LA Morsberger, C Latimer, S McLaren, ML Lin, DJ McBride, I Varela, SA Nik-Zainal, C Leroy, M Jia, A Menzies, AP Butler, JW Teague, CA Griffin, J Burton, H Swerdlow, MA Quail, MR Stratton, C Iacobuzio-Donahue, PA Futreal. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010; 467(7319): 1109–1113
https://doi.org/10.1038/nature09460 pmid: 20981101
17 DA Landau, SL Carter, P Stojanov, A McKenna, K Stevenson, MS Lawrence, C Sougnez, C Stewart, A Sivachenko, L Wang, Y Wan, W Zhang, SA Shukla, A Vartanov, SM Fernandes, G Saksena, K Cibulskis, B Tesar, S Gabriel, N Hacohen, M Meyerson, ES Lander, D Neuberg, JR Brown, G Getz, CJ Wu. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 2013; 152(4): 714–726
https://doi.org/10.1016/j.cell.2013.01.019 pmid: 23415222
18 Y Xue, L Martelotto, T Baslan, A Vides, M Solomon, TT Mai, N Chaudhary, GJ Riely, BT Li, K Scott, F Cechhi, U Stierner, K Chadalavada, E de Stanchina, S Schwartz, T Hembrough, G Nanjangud, MF Berger, J Nilsson, SW Lowe, JS Reis-Filho, N Rosen, P Lito. An approach to suppress the evolution of resistance in BRAFV600E-mutant cancer. Nat Med 2017; 23(8): 929–937
https://doi.org/10.1038/nm.4369 pmid: 28714990
19 JK Lee, J Wang, JK Sa, E Ladewig, HO Lee, IH Lee, HJ Kang, DS Rosenbloom, PG Camara, Z Liu, P van Nieuwenhuizen, SW Jung, SW Choi, J Kim, A Chen, KT Kim, S Shin, YJ Seo, JM Oh, YJ Shin, CK Park, DS Kong, HJ Seol, A Blumberg, JI Lee, A Iavarone, WY Park, R Rabadan, DH Nam. Spatiotemporal genomic architecture informs precision oncology in glioblastoma. Nat Genet 2017; 49(4): 594–599
https://doi.org/10.1038/ng.3806 pmid: 28263318
20 ZS Bao, HM Chen, MY Yang, CB Zhang, K Yu, WL Ye, BQ Hu, W Yan, W Zhang, J Akers, V Ramakrishnan, J Li, B Carter, YW Liu, HM Hu, Z Wang, MY Li, K Yao, XG Qiu, CS Kang, YP You, XL Fan, WS Song, RQ Li, XD Su, CC Chen, T Jiang. RNA-seq of 272 gliomas revealed a novel, recurrent PTPRZ1-MET fusion transcript in secondary glioblastomas. Genome Res 2014; 24(11): 1765–1773
https://doi.org/10.1101/gr.165126.113 pmid: 25135958
21 H Hu, Q Mu, Z Bao, Y Chen, Y Liu, J Chen, K Wang, Z Wang, Y Nam, B Jiang, JK Sa, HJ Cho, NG Her, C Zhang, Z Zhao, Y Zhang, F Zeng, F Wu, X Kang, Y Liu, Z Qian, Z Wang, R Huang, Q Wang, W Zhang, X Qiu, W Li, DH Nam, X Fan, J Wang, T Jiang. Mutational landscape of secondary glioblastoma guides MET-targeted trial in brain tumor. Cell 2018; 175(6): 1665–1678.e18
https://doi.org/10.1016/j.cell.2018.09.038 pmid: 30343896
22 K Abou-El-Ardat, M Seifert, K Becker, S Eisenreich, M Lehmann, K Hackmann, A Rump, G Meijer, B Carvalho, A Temme, G Schackert, E Schröck, D Krex, B Klink. Comprehensive molecular characterization of multifocal glioblastoma proves its monoclonal origin and reveals novel insights into clonal evolution and heterogeneity of glioblastomas. Neuro-oncol 2017; 19(4): 546–557
https://doi.org/10.1093/neuonc/now231 pmid: 28201779
23 M Baysan, K Woolard, MC Cam, W Zhang, H Song, S Kotliarova, D Balamatsias, A Linkous, S Ahn, J Walling, GI Belova, HA Fine. Detailed longitudinal sampling of glioma stem cells in situ reveals Chr7 gain and Chr10 loss as repeated events in primary tumor formation and recurrence. Int J Cancer 2017; 141(10): 2002–2013
https://doi.org/10.1002/ijc.30887 pmid: 28710771
24 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 pmid: 26373278
25 D Hanahan, RA Weinberg. Hallmarks of cancer: the next generation. Cell 2011; 144(5): 646–674
https://doi.org/10.1016/j.cell.2011.02.013 pmid: 21376230
26 S Alcantara Llaguno, J Chen, CH Kwon, EL Jackson, Y Li, DK Burns, A Alvarez-Buylla, LF Parada. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 2009; 15(1): 45–56
https://doi.org/10.1016/j.ccr.2008.12.006 pmid: 19111880
27 H Yan, DW Parsons, G Jin, R McLendon, BA Rasheed, W Yuan, I Kos, I Batinic-Haberle, S Jones, GJ Riggins, H Friedman, A Friedman, D Reardon, J Herndon, KW Kinzler, VE Velculescu, B Vogelstein, DD Bigner. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009; 360(8): 765–773
https://doi.org/10.1056/NEJMoa0808710 pmid: 19228619
28 Y Jiao, PJ Killela, ZJ Reitman, AB Rasheed, CM Heaphy, RF de Wilde, FJ Rodriguez, S Rosemberg, SM Oba-Shinjo, SK Nagahashi Marie, C Bettegowda, N Agrawal, E Lipp, C Pirozzi, G Lopez, Y He, H Friedman, AH Friedman, GJ Riggins, M Holdhoff, P Burger, R McLendon, DD Bigner, B Vogelstein, AK Meeker, KW Kinzler, N Papadopoulos, LA Diaz, H Yan. Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 2012; 3(7): 709–722
https://doi.org/10.18632/oncotarget.588 pmid: 22869205
29 P Yang, J Cai, W Yan, W Zhang, Y Wang, B Chen, G Li, S Li, C Wu, K Yao, W Li, X Peng, Y You, L Chen, C Jiang, X Qiu, T; CGGA project. Jiang Classification based on mutations of TERT promoter and IDH characterizes subtypes in grade II/III gliomas. Neuro-oncol 2016; 18(8): 1099–1108
https://doi.org/10.1093/neuonc/now021 pmid: 26957363
30 TM Brown, E Fee. Rudolf Carl Virchow: medical scientist, social reformer, role model. Am J Public Health 2006; 96(12): 2104–2105
https://doi.org/10.2105/AJPH.2005.078436 pmid: 17077410
31 GH Heppner, BE Miller. Tumor heterogeneity: biological implications and therapeutic consequences. Cancer Metastasis Rev 1983; 2(1): 5–23
https://doi.org/10.1007/BF00046903 pmid: 6616442
32 IJ Fidler. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res 1978; 38(9): 2651–2660
pmid: 354778
33 M Wu, JC Pastor-Pareja, T Xu. Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature 2010; 463(7280): 545–548
https://doi.org/10.1038/nature08702 pmid: 20072127
34 AS Cleary, TL Leonard, SA Gestl, EJ Gunther. Tumour cell heterogeneity maintained by cooperating subclones in Wnt-driven mammary cancers. Nature 2014; 508(7494): 113–117
https://doi.org/10.1038/nature13187 pmid: 24695311
35 CX Dominguez, S Muller, S Keerthivasan, H Koeppen, J Hung, S Gierke, B Breart, O Foreman, TW Bainbridge, A Castiglioni, Y Senbabaoglu, Z Madrusan, Y Liang, MR Junttila, C Klijn, R Bourgon, SJ Turley. Single-cell RNA sequencing reveals stromal evolution into LRRC15+ myofibroblasts as a determinant of patient response to cancer immunotherapy. Cancer Discov 2020; 10(2): 232–253
pmid: 31699795
36 C Neftel, J Laffy, MG Filbin, T Hara, ME Shore, GJ Rahme, AR Richman, D Silverbush, ML Shaw, CM Hebert, J Dewitt, S Gritsch, EM Perez, LN Gonzalez Castro, X Lan, N Druck, C Rodman, D Dionne, A Kaplan, MS Bertalan, J Small, K Pelton, S Becker, D Bonal, QD Nguyen, RL Servis, JM Fung, R Mylvaganam, L Mayr, J Gojo, C Haberler, R Geyeregger, T Czech, I Slavc, BV Nahed, WT Curry, BS Carter, H Wakimoto, PK Brastianos, TT Batchelor, A Stemmer-Rachamimov, M Martinez-Lage, MP Frosch, I Stamenkovic, N Riggi, E Rheinbay, M Monje, O Rozenblatt-Rosen, DP Cahill, AP Patel, T Hunter, IM Verma, KL Ligon, DN Louis, A Regev, BE Bernstein, I Tirosh, ML Suva. An integrative model of cellular states, plasticity, and genetics for glioblastoma. Cell 2019; 178(4): 835–849.e21
https://doi.org/10.1016/j.cell.2019.06.024 pmid: 31327527
37 F Favero, N McGranahan, M Salm, NJ Birkbak, JZ Sanborn, SC Benz, J Becq, JF Peden, Z Kingsbury, RJ Grocok, S Humphray, D Bentley, B Spencer-Dene, A Gutteridge, M Brada, S Roger, PY Dietrich, T Forshew, M Gerlinger, A Rowan, G Stamp, AC Eklund, Z Szallasi, C Swanton. Glioblastoma adaptation traced through decline of an IDH1 clonal driver and macro-evolution of a double-minute chromosome. Ann Oncol 2015; 26(5): 880–887
https://doi.org/10.1093/annonc/mdv127 pmid: 25732040
38 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 pmid: 20981102
39 TF Eleveld, DA Oldridge, V Bernard, J Koster, L Colmet Daage, SJ Diskin, L Schild, NB Bentahar, A Bellini, M Chicard, E Lapouble, V Combaret, P Legoix-Né, J Michon, TJ Pugh, LS Hart, J Rader, EF Attiyeh, JS Wei, S Zhang, A Naranjo, JM Gastier-Foster, MD Hogarty, S Asgharzadeh, MA Smith, JM Guidry Auvil, TB Watkins, DA Zwijnenburg, ME Ebus, P van Sluis, A Hakkert, E van Wezel, CE van der Schoot, EM Westerhout, JH Schulte, GA Tytgat, ME Dolman, I Janoueix-Lerosey, DS Gerhard, HN Caron, O Delattre, J Khan, R Versteeg, G Schleiermacher, JJ Molenaar, JM Maris. Relapsed neuroblastomas show frequent RAS-MAPK pathway mutations. Nat Genet 2015; 47(8): 864–871
https://doi.org/10.1038/ng.3333 pmid: 26121087
40 H Nikbakht, E Panditharatna, LG Mikael, R Li, T Gayden, M Osmond, CY Ho, M Kambhampati, EI Hwang, D Faury, A Siu, S Papillon-Cavanagh, D Bechet, KL Ligon, B Ellezam, WJ Ingram, C Stinson, AS Moore, KE Warren, J Karamchandani, RJ Packer, N Jabado, J Majewski, J Nazarian. Spatial and temporal homogeneity of driver mutations in diffuse intrinsic pontine glioma. Nat Commun 2016; 7(1): 11185
https://doi.org/10.1038/ncomms11185 pmid: 27048880
41 PY Wen, S Kesari. Malignant gliomas in adults. N Engl J Med 2008; 359(5): 492–507
https://doi.org/10.1056/NEJMra0708126 pmid: 18669428
42 EC Holland. Glioblastoma multiforme: the terminator. Proc Natl Acad Sci USA 2000; 97(12): 6242–6244
https://doi.org/10.1073/pnas.97.12.6242 pmid: 10841526
43 M Snuderl, L Fazlollahi, LP Le, M Nitta, BH Zhelyazkova, CJ Davidson, S Akhavanfard, DP Cahill, KD Aldape, RA Betensky, DN Louis, AJ Iafrate. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 2011; 20(6): 810–817
https://doi.org/10.1016/j.ccr.2011.11.005 pmid: 22137795
44 A Sottoriva, I Spiteri, SG Piccirillo, A Touloumis, VP Collins, JC Marioni, C Curtis, C Watts, S Tavaré. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 2013; 110(10): 4009–4014
https://doi.org/10.1073/pnas.1219747110 pmid: 23412337
45 JM Francis, CZ Zhang, CL Maire, J Jung, VE Manzo, VA Adalsteinsson, H Homer, S Haidar, B Blumenstiel, CS Pedamallu, AH Ligon, JC Love, M Meyerson, KL Ligon. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. Cancer Discov 2014; 4(8): 956–971
https://doi.org/10.1158/2159-8290.CD-13-0879 pmid: 24893890
46 AP Patel, I Tirosh, JJ Trombetta, AK Shalek, SM Gillespie, H Wakimoto, DP Cahill, BV Nahed, WT Curry, RL Martuza, DN Louis, O Rozenblatt-Rosen, ML Suvà, A Regev, BE Bernstein. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014; 344(6190): 1396–1401
https://doi.org/10.1126/science.1254257 pmid: 24925914
47 M Jamal-Hanjani, GA Wilson, N McGranahan, NJ Birkbak, TBK Watkins, S Veeriah, S Shafi, DH Johnson, R Mitter, R Rosenthal, M Salm, S Horswell, M Escudero, N Matthews, A Rowan, T Chambers, DA Moore, S Turajlic, H Xu, SM Lee, MD Forster, T Ahmad, CT Hiley, C Abbosh, M Falzon, E Borg, T Marafioti, D Lawrence, M Hayward, S Kolvekar, N Panagiotopoulos, SM Janes, R Thakrar, A Ahmed, F Blackhall, Y Summers, R Shah, L Joseph, AM Quinn, PA Crosbie, B Naidu, G Middleton, G Langman, S Trotter, M Nicolson, H Remmen, K Kerr, M Chetty, L Gomersall, DA Fennell, A Nakas, S Rathinam, G Anand, S Khan, P Russell, V Ezhil, B Ismail, M Irvin-Sellers, V Prakash, JF Lester, M Kornaszewska, R Attanoos, H Adams, H Davies, S Dentro, P Taniere, B O’Sullivan, HL Lowe, JA Hartley, N Iles, H Bell, Y Ngai, JA Shaw, J Herrero, Z Szallasi, RF Schwarz, A Stewart, SA Quezada, J Le Quesne, P Van Loo, C Dive, A Hackshaw, C Swanton; TRACERx Consortium. Tracking the evolution of non-small-cell lung cancer. N Engl J Med 2017; 376(22): 2109–2121
https://doi.org/10.1056/NEJMoa1616288 pmid: 28445112
48 S Osuka, EG Van Meir. Overcoming therapeutic resistance in glioblastoma: the way forward. J Clin Invest 2017; 127(2): 415–426
https://doi.org/10.1172/JCI89587 pmid: 28145904
49 ML Suvà, E Rheinbay, SM Gillespie, AP Patel, H Wakimoto, SD Rabkin, N Riggi, AS Chi, DP Cahill, BV Nahed, WT Curry, RL Martuza, MN Rivera, N Rossetti, S Kasif, S Beik, S Kadri, I Tirosh, I Wortman, AK Shalek, O Rozenblatt-Rosen, A Regev, DN Louis, BE Bernstein. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 2014; 157(3): 580–594
https://doi.org/10.1016/j.cell.2014.02.030 pmid: 24726434
50 E Bouffet, V Larouche, BB Campbell, D Merico, R de Borja, M Aronson, C Durno, J Krueger, V Cabric, V Ramaswamy, N Zhukova, G Mason, R Farah, S Afzal, M Yalon, G Rechavi, V Magimairajan, MF Walsh, S Constantini, R Dvir, R Elhasid, A Reddy, M Osborn, M Sullivan, J Hansford, A Dodgshun, N Klauber-Demore, L Peterson, S Patel, S Lindhorst, J Atkinson, Z Cohen, R Laframboise, P Dirks, M Taylor, D Malkin, S Albrecht, RW Dudley, N Jabado, CE Hawkins, A Shlien, U Tabori. Immune checkpoint inhibition for hypermutant glioblastoma multiforme resulting from germline biallelic mismatch repair deficiency. J Clin Oncol 2016; 34(19): 2206–2211
https://doi.org/10.1200/JCO.2016.66.6552 pmid: 27001570
51 DF Quail, JA Joyce. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013; 19(11): 1423–1437
https://doi.org/10.1038/nm.3394 pmid: 24202395
52 A Naba, KR Clauser, S Hoersch, H Liu, SA Carr, RO Hynes. The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol Cell Proteomics 2012; 11(4): M111.014647
https://doi.org/10.1074/mcp.M111.014647 pmid: 22159717
53 J Folkman. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285(21): 1182–1186
https://doi.org/10.1056/NEJM197111182852108 pmid: 4938153
54 WH Fridman, F Pagès, C Sautès-Fridman, J Galon. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012; 12(4): 298–306
https://doi.org/10.1038/nrc3245 pmid: 22419253
55 SM Weis, DA Cheresh. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med 2011; 17(11): 1359–1370
https://doi.org/10.1038/nm.2537 pmid: 22064426
56 R Du, KV Lu, C Petritsch, P Liu, R Ganss, E Passegué, H Song, S Vandenberg, RS Johnson, Z Werb, G Bergers. HIF1α induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008; 13(3): 206–220
https://doi.org/10.1016/j.ccr.2008.01.034 pmid: 18328425
57 GL Semenza. Cancer-stromal cell interactions mediated by hypoxia-inducible factors promote angiogenesis, lymphangiogenesis, and metastasis. Oncogene 2013; 32(35): 4057–4063
https://doi.org/10.1038/onc.2012.578 pmid: 23222717
58 J Trylcova, P Busek, K Smetana Jr, E Balaziova, B Dvorankova, A Mifkova, A Sedo. Effect of cancer-associated fibroblasts on the migration of glioma cells in vitro. Tumour Biol 2015; 36(8): 5873–5879
https://doi.org/10.1007/s13277-015-3259-8 pmid: 25712375
59 JM Lemée, A Clavreul, P Menei. Intratumoral heterogeneity in glioblastoma: don’t forget the peritumoral brain zone. Neuro-oncol 2015; 17(10): 1322–1332
https://doi.org/10.1093/neuonc/nov119 pmid: 26203067
60 Q Wang, B Hu, X Hu, H Kim, M Squatrito, L Scarpace, AC deCarvalho, S Lyu, P Li, Y Li, F Barthel, HJ Cho, YH Lin, N Satani, E Martinez-Ledesma, S Zheng, E Chang, CG Sauve, A Olar, ZD Lan, G Finocchiaro, JJ Phillips, MS Berger, KR Gabrusiewicz, G Wang, E Eskilsson, J Hu, T Mikkelsen, RA DePinho, F Muller, AB Heimberger, EP Sulman, DH Nam, RGW Verhaak. Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell 2017; 32(1): 42–56.e6
https://doi.org/10.1016/j.ccell.2017.06.003 pmid: 28697342
61 SM Pyonteck, L Akkari, AJ Schuhmacher, RL Bowman, L Sevenich, DF Quail, OC Olson, ML Quick, JT Huse, V Teijeiro, M Setty, CS Leslie, Y Oei, A Pedraza, J Zhang, CW Brennan, JC Sutton, EC Holland, D Daniel, JA Joyce. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 2013; 19(10): 1264–1272
https://doi.org/10.1038/nm.3337 pmid: 24056773
62 CE Brown, D Alizadeh, R Starr, L Weng, JR Wagner, A Naranjo, JR Ostberg, MS Blanchard, J Kilpatrick, J Simpson, A Kurien, SJ Priceman, X Wang, TL Harshbarger, M D’Apuzzo, JA Ressler, MC Jensen, ME Barish, M Chen, J Portnow, SJ Forman, B Badie. Regression of glioblastoma after chimeric antigen receptor T-cell therapy. N Engl J Med 2016; 375(26): 2561–2569
https://doi.org/10.1056/NEJMoa1610497 pmid: 28029927
63 N Shafee, CR Smith, S Wei, Y Kim, GB Mills, GN Hortobagyi, EJ Stanbridge, EY Lee. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Cancer Res 2008; 68(9): 3243–3250
https://doi.org/10.1158/0008-5472.CAN-07-5480 pmid: 18451150
64 X Li, MT Lewis, J Huang, C Gutierrez, CK Osborne, MF Wu, SG Hilsenbeck, A Pavlick, X Zhang, GC Chamness, H Wong, J Rosen, JC Chang. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008; 100(9): 672–679
https://doi.org/10.1093/jnci/djn123 pmid: 18445819
65 D Raha, TR Wilson, J Peng, D Peterson, P Yue, M Evangelista, C Wilson, M Merchant, J Settleman. The cancer stem cell marker aldehyde dehydrogenase is required to maintain a drug-tolerant tumor cell subpopulation. Cancer Res 2014; 74(13): 3579–3590
https://doi.org/10.1158/0008-5472.CAN-13-3456 pmid: 24812274
66 R Haq, J Shoag, P Andreu-Perez, S Yokoyama, H Edelman, GC Rowe, DT Frederick, AD Hurley, A Nellore, AL Kung, JA Wargo, JS Song, DE Fisher, Z Arany, HR Widlund. Oncogenic BRAF regulates oxidative metabolism via PGC1α and MITF. Cancer Cell 2013; 23(3): 302–315
https://doi.org/10.1016/j.ccr.2013.02.003 pmid: 23477830
67 TG Bivona, RC Doebele. A framework for understanding and targeting residual disease in oncogene-driven solid cancers. Nat Med 2016; 22(5): 472–478
https://doi.org/10.1038/nm.4091 pmid: 27149220
68 M Ramirez, S Rajaram, RJ Steininger, D Osipchuk, MA Roth, LS Morinishi, L Evans, W Ji, CH Hsu, K Thurley, S Wei, A Zhou, PR Koduru, BA Posner, LF Wu, SJ Altschuler. Diverse drug-resistance mechanisms can emerge from drug-tolerant cancer persister cells. Nat Commun 2016; 7(1): 10690
https://doi.org/10.1038/ncomms10690 pmid: 26891683
69 AN Hata, MJ Niederst, HL Archibald, M Gomez-Caraballo, FM Siddiqui, HE Mulvey, YE Maruvka, F Ji, HE Bhang, V Krishnamurthy Radhakrishna, G Siravegna, H Hu, S Raoof, E Lockerman, A Kalsy, D Lee, CL Keating, DA Ruddy, LJ Damon, AS Crystal, C Costa, Z Piotrowska, A Bardelli, AJ Iafrate, RI Sadreyev, F Stegmeier, G Getz, LV Sequist, AC Faber, JA Engelman. Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition. Nat Med 2016; 22(3): 262–269
https://doi.org/10.1038/nm.4040 pmid: 26828195
70 AT Shaw, L Friboulet, I Leshchiner, JF Gainor, S Bergqvist, A Brooun, BJ Burke, YL Deng, W Liu, L Dardaei, RL Frias, KR Schultz, J Logan, LP James, T Smeal, S Timofeevski, R Katayama, AJ Iafrate, L Le, M McTigue, G Getz, TW Johnson, JA Engelman. Resensitization to crizotinib by the lorlatinib ALK resistance mutation L1198F. N Engl J Med 2016; 374(1): 54–61
https://doi.org/10.1056/NEJMoa1508887 pmid: 26698910
71 HA Yu, ME Arcila, MD Hellmann, MG Kris, M Ladanyi, GJ Riely. Poor response to erlotinib in patients with tumors containing baseline EGFR T790M mutations found by routine clinical molecular testing. Ann Oncol 2014; 25(2): 423–428
https://doi.org/10.1093/annonc/mdt573 pmid: 24478319
72 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 pmid: 29115304
73 C Blanpain, E Fuchs. Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration. Science 2014; 344(6189): 1242281
https://doi.org/10.1126/science.1242281 pmid: 24926024
74 A Wang, L Qu, L Wang. At the crossroads of cancer stem cells and targeted therapy resistance. Cancer Lett 2017; 385: 87–96
https://doi.org/10.1016/j.canlet.2016.10.039 pmid: 27816488
75 J Chen, Y Li, TS Yu, RM McKay, DK Burns, SG Kernie, LF Parada. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488(7412): 522–526
https://doi.org/10.1038/nature11287 pmid: 22854781
76 D Nassar, C Blanpain. Cancer stem cells: basic concepts and therapeutic implications. Annu Rev Pathol 2016; 11(1): 47–76
https://doi.org/10.1146/annurev-pathol-012615-044438 pmid: 27193450
77 S Bao, Q Wu, RE McLendon, Y Hao, Q Shi, AB Hjelmeland, MW Dewhirst, DD Bigner, JN Rich. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444(7120): 756–760
https://doi.org/10.1038/nature05236 pmid: 17051156
78 P Hamerlik, JD Lathia, R Rasmussen, Q Wu, J Bartkova, M Lee, P Moudry, J Bartek Jr, W Fischer, J Lukas, JN Rich, J Bartek. Autocrine VEGF-VEGFR2-Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth. J Exp Med 2012; 209(3): 507–520
https://doi.org/10.1084/jem.20111424 pmid: 22393126
79 B Auffinger, AL Tobias, Y Han, G Lee, D Guo, M Dey, MS Lesniak, AU Ahmed. Conversion of differentiated cancer cells into cancer stem-like cells in a glioblastoma model after primary chemotherapy. Cell Death Differ 2014; 21(7): 1119–1131
https://doi.org/10.1038/cdd.2014.31 pmid: 24608791
80 HE Barker, JT Paget, AA Khan, KJ Harrington. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat Rev Cancer 2015; 15(7): 409–425
https://doi.org/10.1038/nrc3958 pmid: 26105538
81 Y Jeong, NT Hoang, A Lovejoy, H Stehr, AM Newman, AJ Gentles, W Kong, D Truong, S Martin, A Chaudhuri, D Heiser, L Zhou, C Say, JN Carter, SM Hiniker, BW Loo Jr, RB West, P Beachy, AA Alizadeh, M Diehn. Role of KEAP1/NRF2 and TP53 mutations in lung squamous cell carcinoma development and radiation resistance. Cancer Discov 2017; 7(1): 86–101
https://doi.org/10.1158/2159-8290.CD-16-0127 pmid: 27663899
82 MG Vander Heiden, LC Cantley, CB Thompson. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324(5930): 1029–1033
https://doi.org/10.1126/science.1160809 pmid: 19460998
83 JA Menendez. Metabolic control of cancer cell stemness: lessons from iPS cells. Cell Cycle 2015; 14(24): 3801–3811
https://doi.org/10.1080/15384101.2015.1022697 pmid: 25738999
84 WA Flavahan, Q Wu, M Hitomi, N Rahim, Y Kim, AE Sloan, RJ Weil, I Nakano, JN Sarkaria, BW Stringer, BW Day, M Li, JD Lathia, JN Rich, AB Hjelmeland. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat Neurosci 2013; 16(10): 1373–1382
https://doi.org/10.1038/nn.3510 pmid: 23995067
85 M Morfouace, L Lalier, M Bahut, V Bonnamain, P Naveilhan, C Guette, L Oliver, N Gueguen, P Reynier, FM Vallette. Comparison of spheroids formed by rat glioma stem cells and neural stem cells reveals differences in glucose metabolism and promising therapeutic applications. J Biol Chem 2012; 287(40): 33664–33674
https://doi.org/10.1074/jbc.M111.320028 pmid: 22782899
86 AM Molinaro, JW Taylor, JK Wiencke, MR Wrensch. Genetic and molecular epidemiology of adult diffuse glioma. Nat Rev Neurol 2019; 15(7): 405–417
https://doi.org/10.1038/s41582-019-0220-2 pmid: 31227792
87 X Ding, M He, AWH Chan, QX Song, SC Sze, H Chen, MKH Man, K Man, SL Chan, PBS Lai, X Wang, N Wong. Genomic and epigenomic features of primary and recurrent hepatocellular carcinomas. Gastroenterology 2019; 157(6): 1630–1645.e6
https://doi.org/10.1053/j.gastro.2019.09.005 pmid: 31560893
[1] Guangbiao Zhou, Saijuan Chen, Zhu Chen. Advances in COVID-19: the virus, the pathogenesis, and evidence-based control and therapeutic strategies[J]. Front. Med., 2020, 14(2): 117-125.
[2] Chuanbao Zhang, Zhaoshi Bao, Wei Zhang, Tao Jiang. Progress on molecular biomarkers and classification of malignant gliomas[J]. Front Med, 2013, 7(2): 150-156.
[3] Jin Gao, Ben Panizza, Newell W. Johnson, Scott Coman, Alan R. Clough. Basic consideration of research strategies for head and neck cancer[J]. Front Med, 2012, 6(4): 339-353.
[4] Zhiyuan Zhang. Bone regeneration by stem cell and tissue engineering in oral and maxillofacial region[J]. Front Med, 2011, 5(4): 401-413.
[5] TIAN Yongji, LI Guilin, GAO Jun, WANG Renzhi, KONG Yanguo, ZHANG Zhenxing, LI Shifang, TIAN Shiqiang, DOU Wanchen, ZHANG Bo. Construction of 6HRE-GFAP-Baxα system specific for glioma gene therapy[J]. Front. Med., 2007, 1(1): 49-53.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed