1. State Key Laboratory of Vaccines for Infectious Diseases, Xiang An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University, Xiamen 361102, China 2. National Institute of Diagnostics and Vaccine Development in Infectious Diseases, State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, Xiamen University, Xiamen 361102, China
Oncolytic virus (OV)-based immunotherapy has emerged as a promising strategy for cancer treatment, offering a unique potential to selectively target malignant cells while sparing normal tissues. However, the immunosuppressive nature of tumor microenvironment (TME) poses a substantial hurdle to the development of OVs as effective immunotherapeutic agents, as it restricts the activation and recruitment of immune cells. This review elucidates the potential of OV-based immunotherapy in modulating the immune landscape within the TME to overcome immune resistance and enhance antitumor immune responses. We examine the role of OVs in targeting specific immune cell populations, including dendritic cells, T cells, natural killer cells, and macrophages, and their ability to alter the TME by inhibiting angiogenesis and reducing tumor fibrosis. Additionally, we explore strategies to optimize OV-based drug delivery and improve the efficiency of OV-mediated immunotherapy. In conclusion, this review offers a concise and comprehensive synopsis of the current status and future prospects of OV-based immunotherapy, underscoring its remarkable potential as an effective immunotherapeutic agent for cancer treatment.
Non-small cell lung cancer/triple-negative breast cancer
NCT03004183
Phase II; not yet recruiting
HSV
R130
Anti-CD3 scFv/ CD86/PD1/HSV2-US11
/
Solid tumors
NCT05961111
Phase I; recruiting
OH2
GM-CSF
Anti-PD-1/axitinib
Melanoma stage IV
NCT05070221
Phase I; not yet recruiting
HF10
/
Ipilimumab
Melanoma stage III/IV
NCT03153085
Phase II; completed
T-VEC
GM-CSF
Pembrolizumab
Sarcoma/cutaneous angiosarcoma
NCT03069378
Phase II; completed
Vaccinia virus
VV-GMCSF-Lact
GM-CSF/Lactaptin
/
Metastatic breast cancer
NCT05376527
Phase I; recruiting
RGV004
Anti-CD19/CD3 bispecific antibody
/
B cell lymphoma
NCT04887025
Phase I; recruiting
hV01
IL-21
/
Advanced solid tumors
NCT05914376
Phase I; recruiting
Reovirus
PeLareorEp
/
Paclitaxel/avelumab
Breast cancer metastatic
NCT04215146
Phase II; not yet recruiting
Poliovirus
PVSRIPO
/
/
Glioblastoma
NCT01491893
Phase I; completed
Newcastle disease virus
MEDI9253
IL-12
Durvalumab
Solid tumors
NCT04613492
Phase I; not yet recruiting
Tab.1
1
PF Ferrucci, L Pala, F Conforti, E Cocorocchio. Talimogene laherparepvec (T-VEC): an intralesional cancer immunotherapy for advanced melanoma. Cancers (Basel) 2021; 13(6): 1383 https://doi.org/10.3390/cancers13061383
2
T Todo, H Ito, Y Ino, H Ohtsu, Y Ota, J Shibahara, M Tanaka. Intratumoral oncolytic herpes virus G47∆ for residual or recurrent glioblastoma: a phase 2 trial. Nat Med 2022; 28(8): 1630–1639 https://doi.org/10.1038/s41591-022-01897-x
3
Q Qiao, M Song, C Song, Y Zhang, X Wang, Q Huang, B Wang, P Yang, S Zhao, Y Li, Z Wang, J Zhao. Single-dose vaccination of recombinant chimeric newcastle disease virus (NDV) LaSota vaccine strain expressing infectious bursal disease virus (IBDV) VP2 gene provides full protection against genotype VII NDV and IBDV challenge. Vaccines (Basel) 2021; 9(12): 1483 https://doi.org/10.3390/vaccines9121483
4
G Vijayakumar, P Palese, PH Goff. Oncolytic Newcastle disease virus expressing a checkpoint inhibitor as a radioenhancing agent for murine melanoma. EBioMedicine 2019; 49: 96–105 https://doi.org/10.1016/j.ebiom.2019.10.032
5
Z Huang, M Liu, Y Huang. Oncolytic therapy and gene therapy for cancer: recent advances in antitumor effects of Newcastle disease virus. Discov Med 2020; 30(159): 39–48
6
M Keshavarz, ASM Nejad, M Esghaei, F Bokharaei-Salim, H Dianat-Moghadam, H Keyvani, A Ghaemi. Oncolytic Newcastle disease virus reduces growth of cervical cancer cell by inducing apoptosis. Saudi J Biol Sci 2020; 27(1): 47–52 https://doi.org/10.1016/j.sjbs.2019.04.015
7
J Jiffry, T Thavornwatanayong, D Rao, EJ Fogel, D Saytoo, R Nahata, H Guzik, I Chaudhary, T Augustine, S Goel, R Maitra. Oncolytic reovirus (pelareorep) induces autophagy in KRAS-mutated colorectal cancer. Clin Cancer Res 2021; 27(3): 865–876 https://doi.org/10.1158/1078-0432.CCR-20-2385
8
BE Kennedy, JP Murphy, DR Clements, P Konda, N Holay, Y Kim, GP Pathak, MA Giacomantonio, YE Hiani, S Gujar. Inhibition of pyruvate dehydrogenase kinase enhances the antitumor efficacy of oncolytic reovirus. Cancer Res 2019; 79(15): 3824–3836 https://doi.org/10.1158/0008-5472.CAN-18-2414
9
S Gebremeskel, A Nelson, B Walker, T Oliphant, L Lobert, D Mahoney, B Johnston. Natural killer T cell immunotherapy combined with oncolytic vesicular stomatitis virus or reovirus treatments differentially increases survival in mouse models of ovarian and breast cancer metastasis. J Immunother Cancer 2021; 9(3): e002096 https://doi.org/10.1136/jitc-2020-002096
10
M Abudoureyimu, Y Lai, C Tian, T Wang, R Wang, X Chu. Oncolytic adenovirus—a Nova for gene-targeted oncolytic viral therapy in HCC. Front Oncol 2019; 9: 1182 https://doi.org/10.3389/fonc.2019.01182
11
KJ Mahasa, L de Pillis, R Ouifki, A Eladdadi, P Maini, AR Yoon, CO Yun. Mesenchymal stem cells used as carrier cells of oncolytic adenovirus results in enhanced oncolytic virotherapy. Sci Rep 2020; 10(1): 425 https://doi.org/10.1038/s41598-019-57240-x
12
M Sato-Dahlman, CJ LaRocca, C Yanagiba, M Yamamoto. Adenovirus and immunotherapy: advancing cancer treatment by combination. Cancers (Basel) 2020; 12(5): 1295 https://doi.org/10.3390/cancers12051295
13
W Matsunaga, A Gotoh. Adenovirus as a vector and oncolytic virus. Curr Issues Mol Biol 2023; 45(6): 4826–4840 https://doi.org/10.3390/cimb45060307
14
Y Zhao, Z Liu, L Li, J Wu, H Zhang, H Zhang, T Lei, B Xu. Oncolytic adenovirus: prospects for cancer immunotherapy. Front Microbiol 2021; 12: 707290 https://doi.org/10.3389/fmicb.2021.707290
J Cook, KW Peng, TE Witzig, SM Broski, JC Villasboas, J Paludo, M Patnaik, V Rajkumar, A Dispenzieri, N Leung, F Buadi, N Bennani, SM Ansell, L Zhang, N Packiriswamy, B Balakrishnan, B Brunton, M Giers, B Ginos, AC Dueck, S Geyer, MA Gertz, R Warsame, RS Go, SR Hayman, D Dingli, S Kumar, L Bergsagel, JL Munoz, W Gonsalves, T Kourelis, E Muchtar, P Kapoor, RA Kyle, Y Lin, M Siddiqui, A Fonder, M Hobbs, L Hwa, S Naik, SJ Russell, MQ Lacy. Clinical activity of single-dose systemic oncolytic VSV virotherapy in patients with relapsed refractory T-cell lymphoma. Blood Adv 2022; 6(11): 3268–3279 https://doi.org/10.1182/bloodadvances.2021006631
17
E Hastie, VZ Grdzelishvili. Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J Gen Virol 2012; 93(Pt 12): 2529–2545 https://doi.org/10.1099/vir.0.046672-0
18
SA Felt, VZ Grdzelishvili. Recent advances in vesicular stomatitis virus-based oncolytic virotherapy: a 5-year update. J Gen Virol 2017; 98(12): 2895–2911 https://doi.org/10.1099/jgv.0.000980
RM Diaz, F Galivo, T Kottke, P Wongthida, J Qiao, J Thompson, M Valdes, G Barber, RG Vile. Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res 2007; 67(6): 2840–2848 https://doi.org/10.1158/0008-5472.CAN-06-3974
21
HL Kaufman, FJ Kohlhapp, A Zloza. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov 2016; 15(9): 660 https://doi.org/10.1038/nrd.2016.178
22
S Taguchi, H Fukuhara, T Todo. Oncolytic virus therapy in Japan: progress in clinical trials and future perspectives. Jpn J Clin Oncol 2019; 49(3): 201–209 https://doi.org/10.1093/jjco/hyy170
23
L Guo, C Hu, Y Liu, X Chen, D Song, R Shen, Z Liu, X Jia, Q Zhang, Y Gao, Z Deng, T Zuo, J Hu, W Zhu, J Cai, G Yan, J Liang, Y Lin. Directed natural evolution generates a next-generation oncolytic virus with a high potency and safety profile. Nat Commun 2023; 14(1): 3410 https://doi.org/10.1038/s41467-023-39156-3
24
G Takano, S Esaki, F Goshima, A Enomoto, Y Hatano, H Ozaki, T Watanabe, Y Sato, D Kawakita, S Murakami, T Murata, Y Nishiyama, S Iwasaki, H Kimura. Oncolytic activity of naturally attenuated herpes-simplex virus HF10 against an immunocompetent model of oral carcinoma. Mol Ther Oncolytics 2020; 20: 220–227 https://doi.org/10.1016/j.omto.2020.12.007
25
GA Garmaroudi, F Karimi, LG Naeini, P Kokabian, N Givtaj. Therapeutic efficacy of oncolytic viruses in fighting cancer: recent advances and perspective. Oxid Med Cell Longev 2022; 2022: 3142306 https://doi.org/10.1155/2022/3142306
26
E Robilotti, NC Zeitouni, M Orloff. Biosafety and biohazard considerations of HSV-1-based oncolytic viral immunotherapy. Front Mol Biosci 2023; 10: 1178382 https://doi.org/10.3389/fmolb.2023.1178382
27
H Liu, H Luo. Development of group B coxsackievirus as an oncolytic virus: opportunities and challenges. Viruses 2021; 13(6): 1082 https://doi.org/10.3390/v13061082
28
N Jayawardena, JT Poirier, LN Burga, M Bostina. Virus-receptor interactions and virus neutralization: insights for oncolytic virus development. Oncolytic Virother 2020; 9: 1–15 https://doi.org/10.2147/OV.S186337
Y Tian, D Xie, L Yang. Engineering strategies to enhance oncolytic viruses in cancer immunotherapy. Signal Transduct Target Ther 2022; 7(1): 117 https://doi.org/10.1038/s41392-022-00951-x
31
SN Jeong, SY Yoo. Novel oncolytic virus armed with cancer suicide gene and normal vasculogenic gene for improved anti-tumor activity. Cancers (Basel) 2020; 12(5): 1070 https://doi.org/10.3390/cancers12051070
J Gong, E Sachdev, AC Mita, MM Mita. Clinical development of reovirus for cancer therapy: an oncolytic virus with immune-mediated antitumor activity. World J Methodol 2016; 6(1): 25–42 https://doi.org/10.5662/wjm.v6.i1.25
34
A Howells, G Marelli, NR Lemoine, Y Wang. Oncolytic viruses-interaction of virus and tumor cells in the battle to eliminate cancer. Front Oncol 2017; 7: 195 https://doi.org/10.3389/fonc.2017.00195
35
Z Herceg, P Hainaut. Genetic and epigenetic alterations as biomarkers for cancer detection, diagnosis and prognosis. Mol Oncol 2007; 1(1): 26–41 https://doi.org/10.1016/j.molonc.2007.01.004
36
K Martin, J Schreiner, A Zippelius. Modulation of APC function and anti-tumor immunity by anti-cancer drugs. Front Immunol 2015; 6: 501 https://doi.org/10.3389/fimmu.2015.00501
37
S Jeong, SH Park. Co-stimulatory receptors in cancers and their implications for cancer immunotherapy. Immune Netw 2020; 20(1): e3 https://doi.org/10.4110/in.2020.20.e3
38
V Huber, C Camisaschi, A Berzi, S Ferro, L Lugini, T Triulzi, A Tuccitto, E Tagliabue, C Castelli, L Rivoltini. Cancer acidity: an ultimate frontier of tumor immune escape and a novel target of immunomodulation. Semin Cancer Biol 2017; 43: 74–89 https://doi.org/10.1016/j.semcancer.2017.03.001
39
A Emami Nejad, S Najafgholian, A Rostami, A Sistani, S Shojaeifar, M Esparvarinha, R Nedaeinia, S Haghjooy Javanmard, M Taherian, M Ahmadlou, R Salehi, B Sadeghi, M Manian. The role of hypoxia in the tumor microenvironment and development of cancer stem cell: a novel approach to developing treatment. Cancer Cell Int 2021; 21(1): 62 https://doi.org/10.1186/s12935-020-01719-5
40
T Tang, X Huang, G Zhang, Z Hong, X Bai, T Liang. Advantages of targeting the tumor immune microenvironment over blocking immune checkpoint in cancer immunotherapy. Signal Transduct Target Ther 2021; 6(1): 72 https://doi.org/10.1038/s41392-020-00449-4
41
Y Tie, F Tang, YQ Wei, XW Wei. Immunosuppressive cells in cancer: mechanisms and potential therapeutic targets. J Hematol Oncol 2022; 15(1): 61 https://doi.org/10.1186/s13045-022-01282-8
42
MZ Jin, WL Jin. The updated landscape of tumor microenvironment and drug repurposing. Signal Transduct Target Ther 2020; 5(1): 166 https://doi.org/10.1038/s41392-020-00280-x
43
S Prasad, P Saha, B Chatterjee, AA Chaudhary, R Lall, AK Srivastava. Complexity of tumor microenvironment: therapeutic role of curcumin and its metabolites. Nutr Cancer 2023; 75(1): 1–13 https://doi.org/10.1080/01635581.2022.2096909
A Labani-Motlagh, M Ashja-Mahdavi, A Loskog. The tumor microenvironment: a milieu hindering and obstructing antitumor immune responses. Front Immunol 2020; 11: 940 https://doi.org/10.3389/fimmu.2020.00940
46
NA Giraldo, R Sanchez-Salas, JD Peske, Y Vano, E Becht, F Petitprez, P Validire, A Ingels, X Cathelineau, WH Fridman, C Sautès-Fridman. The clinical role of the TME in solid cancer. Br J Cancer 2019; 120(1): 45–53 https://doi.org/10.1038/s41416-018-0327-z
47
K Dhatchinamoorthy, JD Colbert, KL Rock. Cancer immune evasion through loss of MHC class I antigen presentation. Front Immunol 2021; 12: 636568 https://doi.org/10.3389/fimmu.2021.636568
48
JD Klement, PS Redd, C Lu, AD Merting, DB Poschel, D Yang, NM Savage, G Zhou, DH Munn, PG Fallon, K Liu. Tumor PD-L1 engages myeloid PD-1 to suppress type I interferon to impair cytotoxic T lymphocyte recruitment. Cancer Cell 2023; 41(3): 620–636.e9 https://doi.org/10.1016/j.ccell.2023.02.005
Y Ban, J Mai, X Li, M Mitchell-Flack, T Zhang, L Zhang, L Chouchane, M Ferrari, H Shen, X Ma. Targeting autocrine CCL5-CCR5 axis reprograms immunosuppressive myeloid cells and reinvigorates antitumor immunity. Cancer Res 2017; 77(11): 2857–2868 https://doi.org/10.1158/0008-5472.CAN-16-2913
51
ES Melese, E Franks, RA Cederberg, BT Harbourne, R Shi, BJ Wadsworth, JL Collier, EC Halvorsen, F Johnson, J Luu, MH Oh, V Lam, G Krystal, SB Hoover, M Raffeld, RM Simpson, AM Unni, WL Lam, S Lam, N Abraham, KL Bennewith, WW Lockwood. CCL5 production in lung cancer cells leads to an altered immune microenvironment and promotes tumor development. OncoImmunology 2021; 11(1): 2010905 https://doi.org/10.1080/2162402X.2021.2010905
52
A O’Garra, PL Vieira, P Vieira, AE Goldfeld. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J Clin Invest 2004; 114(10): 1372–1378 https://doi.org/10.1172/JCI23215
53
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
54
N Ma, Q Liu, L Hou, Y Wang, Z Liu. MDSCs are involved in the protumorigenic potentials of GM-CSF in colitis-associated cancer. Int J Immunopathol Pharmacol 2017; 30(2): 152–162 https://doi.org/10.1177/0394632017711055
MJ Polanczyk, E Walker, D Haley, BS Guerrouahen, ET Akporiaye. Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4+CD25+Foxp3+ and CD4+CD25-Foxp3+ T cells. J Transl Med 2019; 17(1): 219 https://doi.org/10.1186/s12967-019-1967-3
57
SK Kim, SW Cho. The evasion mechanisms of cancer immunity and drug intervention in the tumor microenvironment. Front Pharmacol 2022; 13: 868695 https://doi.org/10.3389/fphar.2022.868695
58
J Chen, D Zhao, L Zhang, J Zhang, Y Xiao, Q Wu, Y Wang, Q Zhan. Tumor-associated macrophage (TAM)-derived CCL22 induces FAK addiction in esophageal squamous cell carcinoma (ESCC). Cell Mol Immunol 2022; 19(9): 1054–1066 https://doi.org/10.1038/s41423-022-00903-z
59
M Rapp, MWM Wintergerst, WG Kunz, VK Vetter, MML Knott, D Lisowski, S Haubner, S Moder, R Thaler, S Eiber, B Meyer, N Röhrle, I Piseddu, S Grassmann, P Layritz, B Kühnemuth, S Stutte, C Bourquin, Andrian UH von, S Endres, D Anz. CCL22 controls immunity by promoting regulatory T cell communication with dendritic cells in lymph nodes. J Exp Med 2019; 216(5): 1170–1181 https://doi.org/10.1084/jem.20170277
60
E Balta, GH Wabnitz, Y Samstag. Hijacked immune cells in the tumor microenvironment: molecular mechanisms of immunosuppression and cues to improve T cell-based immunotherapy of solid tumors. Int J Mol Sci 2021; 22(11): 5736 https://doi.org/10.3390/ijms22115736
61
AD Waldman, JM Fritz, MJ Lenardo. A guide to cancer immunotherapy: from T cell basic science to clinical practice. Nat Rev Immunol 2020; 20(11): 651–668 https://doi.org/10.1038/s41577-020-0306-5
62
AER Kartikasari, MD Prakash, M Cox, K Wilson, JC Boer, JA Cauchi, M Plebanski. Therapeutic cancer vaccines—T cell responses and epigenetic modulation. Front Immunol 2019; 9: 3109 https://doi.org/10.3389/fimmu.2018.03109
V To, VJ Evtimov, G Jenkin, A Pupovac, AO Trounson, RL Boyd. CAR-T cell development for cutaneous T cell lymphoma: current limitations and potential treatment strategies. Front Immunol 2022; 13: 968395 https://doi.org/10.3389/fimmu.2022.968395
66
P Shafer, LM Kelly, V Hoyos. Cancer therapy with TCR-engineered T cells: current strategies, challenges, and prospects. Front Immunol 2022; 13: 835762 https://doi.org/10.3389/fimmu.2022.835762
67
E Baulu, C Gardet, N Chuvin, S Depil. TCR-engineered T cell therapy in solid tumors: state of the art and perspectives. Sci Adv 2023; 9(7): eadf3700 https://doi.org/10.1126/sciadv.adf3700
68
R Zappasodi, T Merghoub, JD Wolchok. Emerging concepts for immune checkpoint blockade-based combination therapies. Cancer Cell 2018; 33(4): 581–598 https://doi.org/10.1016/j.ccell.2018.03.005
69
S Samnani, F Sachedina, M Gupta, E Guo, V Navani. Mechanisms and clinical implications in renal carcinoma resistance: narrative review of immune checkpoint inhibitors. Cancer Drug Resist 2023; 6(2): 416–429 https://doi.org/10.20517/cdr.2023.02
70
DR Wang, XL Wu, YL Sun. Therapeutic targets and biomarkers of tumor immunotherapy: response versus non-response. Signal Transduct Target Ther 2022; 7(1): 331 https://doi.org/10.1038/s41392-022-01136-2
71
Z Zhou, C Tao, J Li, JC Tang, AS Chan, Y Zhou. Chimeric antigen receptor T cells applied to solid tumors. Front Immunol 2022; 13: 984864 https://doi.org/10.3389/fimmu.2022.984864
72
B Farhood, M Najafi, K Mortezaee. CD8+ cytotoxic T lymphocytes in cancer immunotherapy: a review. J Cell Physiol 2019; 234(6): 8509–8521 https://doi.org/10.1002/jcp.27782
73
YT Liu, ZJ Sun. Turning cold tumors into hot tumors by improving T-cell infiltration. Theranostics 2021; 11(11): 5365–5386 https://doi.org/10.7150/thno.58390
74
P Bonaventura, T Shekarian, V Alcazer, J Valladeau-Guilemond, S Valsesia-Wittmann, S Amigorena, C Caux, S Depil. Cold tumors: a therapeutic challenge for immunotherapy. Front Immunol 2019; 10: 168 https://doi.org/10.3389/fimmu.2019.00168
75
J Galon, D Bruni. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat Rev Drug Discov 2019; 18(3): 197–218 https://doi.org/10.1038/s41573-018-0007-y
Y Wang, Y Liang, H Xu, X Zhang, T Mao, J Cui, J Yao, Y Wang, F Jiao, X Xiao, J Hu, Q Xia, X Zhang, X Wang, Y Sun, D Fu, L Shen, X Xu, J Xue, L Wang. Single-cell analysis of pancreatic ductal adenocarcinoma identifies a novel fibroblast subtype associated with poor prognosis but better immunotherapy response. Cell Discov 2021; 7(1): 36 https://doi.org/10.1038/s41421-021-00271-4
79
Z Zheng, T Wieder, B Mauerer, L Schäfer, R Kesselring, H Braumüller. T cells in colorectal cancer: unravelling the function of different T cell subsets in the tumor microenvironment. Int J Mol Sci 2023; 24(14): 11673 https://doi.org/10.3390/ijms241411673
80
S Narayanan, S Vicent, M Ponz-Sarvisé. PDAC as an immune evasive disease: can 3D model systems aid to tackle this clinical problem?. Front Cell Dev Biol 2021; 9: 787249 https://doi.org/10.3389/fcell.2021.787249
81
R Dutta, R Khalil, K Mayilsamy, R Green, M Howell, S Bharadwaj, SS Mohapatra, S Mohapatra. Combination therapy of mithramycin A and immune checkpoint inhibitor for the treatment of colorectal cancer in an orthotopic murine model. Front Immunol 2021; 12: 706133 https://doi.org/10.3389/fimmu.2021.706133
82
KY Jeong. Challenges to addressing the unmet medical needs for immunotherapy targeting cold colorectal cancer. World J Gastrointest Oncol 2023; 15(2): 215–224 https://doi.org/10.4251/wjgo.v15.i2.215
83
JL Liu, M Yang, JG Bai, Z Liu, XS Wang. “Cold” colorectal cancer faces a bottleneck in immunotherapy. World J Gastrointest Oncol 2023; 15(2): 240–250 https://doi.org/10.4251/wjgo.v15.i2.240
84
KP Fabian, B Wolfson, JW Hodge. From immunogenic cell death to immunogenic modulation: select chemotherapy regimens induce a spectrum of immune-enhancing activities in the tumor microenvironment. Front Oncol 2021; 11: 728018 https://doi.org/10.3389/fonc.2021.728018
85
S Mihm. Danger-associated molecular patterns (DAMPs): molecular triggers for sterile inflammation in the liver. Int J Mol Sci 2018; 19(10): 3104 https://doi.org/10.3390/ijms19103104
86
J Fucikova, O Kepp, L Kasikova, G Petroni, T Yamazaki, P Liu, L Zhao, R Spisek, G Kroemer, L Galluzzi. Detection of immunogenic cell death and its relevance for cancer therapy. Cell Death Dis 2020; 11(11): 1013 https://doi.org/10.1038/s41419-020-03221-2
87
ZS Guo, Z Liu, DL Bartlett. Oncolytic immunotherapy: dying the right way is a key to eliciting potent antitumor immunity. Front Oncol 2014; 4: 74 https://doi.org/10.3389/fonc.2014.00074
88
AD Garg, P Agostinis. Cell death and immunity in cancer: from danger signals to mimicry of pathogen defense responses. Immunol Rev 2017; 280(1): 126–148 https://doi.org/10.1111/imr.12574
89
Z Asadzadeh, E Safarzadeh, S Safaei, A Baradaran, A Mohammadi, K Hajiasgharzadeh, A Derakhshani, A Argentiero, N Silvestris, B Baradaran. Current approaches for combination therapy of cancer: the role of immunogenic cell death. Cancers (Basel) 2020; 12(4): 1047 https://doi.org/10.3390/cancers12041047
90
A Ramírez-Labrada, C Pesini, L Santiago, S Hidalgo, A Calvo-Pérez, C Oñate, A Andrés-Tovar, M Garzón-Tituaña, I Uranga-Murillo, MA Arias, EM Galvez, J Pardo. All about (NK cell-mediated) death in two acts and an unexpected encore: initiation, execution and activation of adaptive immunity. Front Immunol 2022; 13: 896228 https://doi.org/10.3389/fimmu.2022.896228
91
J Zhu, X Huang, Y Yang. A critical role for type I IFN-dependent NK cell activation in innate immune elimination of adenoviral vectors in vivo. Mol Ther 2008; 16(7): 1300–1307 https://doi.org/10.1038/mt.2008.88
92
TL Aaes, A Kaczmarek, T Delvaeye, B De Craene, S De Koker, L Heyndrickx, I Delrue, J Taminau, B Wiernicki, P De Groote, AD Garg, L Leybaert, J Grooten, MJ Bertrand, P Agostinis, G Berx, W Declercq, P Vandenabeele, DV Krysko. Vaccination with necroptotic cancer cells induces efficient anti-tumor immunity. Cell Rep 2016; 15(2): 274–287 https://doi.org/10.1016/j.celrep.2016.03.037
93
ST Workenhe, KL Mossman. Oncolytic virotherapy and immunogenic cancer cell death: sharpening the sword for improved cancer treatment strategies. Mol Ther 2014; 22(2): 251–256 https://doi.org/10.1038/mt.2013.220
94
MJF Crupi, Z Taha, TJA Janssen, J Petryk, S Boulton, N Alluqmani, A Jirovec, O Kassas, ST Khan, S Vallati, E Lee, BZ Huang, M Huh, L Pikor, X He, R Marius, B Austin, J Duong, A Pelin, S Neault, T Azad, CJ Breitbach, DF Stojdl, MF Burgess, S McComb, R Auer, JS Diallo, CS Ilkow, JC Bell. Oncolytic virus driven T-cell-based combination immunotherapy platform for colorectal cancer. Front Immunol 2022; 13: 1029269 https://doi.org/10.3389/fimmu.2022.1029269
95
K Ye, F Li, R Wang, T Cen, S Liu, Z Zhao, R Li, L Xu, G Zhang, Z Xu, L Deng, L Li, W Wang, A Stepanov, Y Wan, Y Guo, Y Li, Y Wang, Y Tian, AG Gabibov, Y Yan, H Zhang. An armed oncolytic virus enhances the efficacy of tumor-infiltrating lymphocyte therapy by converting tumors to artificial antigen-presenting cells in situ. Mol Ther 2022; 30(12): 3658–3676 https://doi.org/10.1016/j.ymthe.2022.06.010
96
G Wang, X Kang, KS Chen, T Jehng, L Jones, J Chen, XF Huang, SY Chen. An engineered oncolytic virus expressing PD-L1 inhibitors activates tumor neoantigen-specific T cell responses. Nat Commun 2020; 11(1): 1395 https://doi.org/10.1038/s41467-020-15229-5
97
N Packiriswamy, D Upreti, Y Zhou, R Khan, A Miller, RM Diaz, CM Rooney, A Dispenzieri, KW Peng, SJ Russell. Oncolytic measles virus therapy enhances tumor antigen-specific T-cell responses in patients with multiple myeloma. Leukemia 2020; 34(12): 3310–3322 https://doi.org/10.1038/s41375-020-0828-7
98
J Ma, M Ramachandran, C Jin, C Quijano-Rubio, M Martikainen, D Yu, M Essand. Characterization of virus-mediated immunogenic cancer cell death and the consequences for oncolytic virus-based immunotherapy of cancer. Cell Death Dis 2020; 11(1): 48 https://doi.org/10.1038/s41419-020-2236-3
99
R Ma, Z Li, EA Chiocca, MA Caligiuri, J Yu. The emerging field of oncolytic virus-based cancer immunotherapy. Trends Cancer 2023; 9(2): 122–139 https://doi.org/10.1016/j.trecan.2022.10.003
100
SR Niavarani, C Lawson, M Boudaud, C Simard, LH Tai. Oncolytic vesicular stomatitis virus-based cellular vaccine improves triple-negative breast cancer outcome by enhancing natural killer and CD8+ T-cell functionality. J Immunother Cancer 2020; 8(1): e000465 https://doi.org/10.1136/jitc-2019-000465
M Sadeghzadeh, S Bornehdeli, H Mohahammadrezakhani, M Abolghasemi, E Poursaei, M Asadi, V Zafari, L Aghebati-Maleki, D Shanehbandi. Dendritic cell therapy in cancer treatment; the state-of-the-art. Life Sci 2020; 254: 117580 https://doi.org/10.1016/j.lfs.2020.117580
103
SP Bak, MS Barnkob, A Bai, EM Higham, KD Wittrup, J Chen. Differential requirement for CD70 and CD80/CD86 in dendritic cell-mediated activation of tumor-tolerized CD8 T cells. J Immunol 2012; 189(4): 1708–1716 https://doi.org/10.4049/jimmunol.1201271
104
N Ke, A Su, W Huang, P Szatmary, Z Zhang. Regulating the expression of CD80/CD86 on dendritic cells to induce immune tolerance after xeno-islet transplantation. Immunobiology 2016; 221(7): 803–812 https://doi.org/10.1016/j.imbio.2016.02.002
105
HW Kim, SI Cho, S Bae, H Kim, Y Kim, YI Hwang, JS Kang, WJ Lee, C Vitamin. Vitamin C up-regulates expression of CD80, CD86 and MHC class II on dendritic cell line, DC-1 via the activation of p38 MAPK. Immune Netw 2012; 12(6): 277–283 https://doi.org/10.4110/in.2012.12.6.277
106
J Calmeiro, MA Carrascal, AR Tavares, DA Ferreira, C Gomes, A Falcão, MT Cruz, BM Neves. Dendritic cell vaccines for cancer immunotherapy: the role of human conventional type 1 dendritic cells. Pharmaceutics 2020; 12(2): 158 https://doi.org/10.3390/pharmaceutics12020158
107
AE Marciscano, N Anandasabapathy. The role of dendritic cells in cancer and anti-tumor immunity. Semin Immunol 2021; 52: 101481 https://doi.org/10.1016/j.smim.2021.101481
Z Ding, Q Li, R Zhang, L Xie, Y Shu, S Gao, P Wang, X Su, Y Qin, Y Wang, J Fang, Z Zhu, X Xia, G Wei, H Wang, H Qian, X Guo, Z Gao, Y Wang, Y Wei, Q Xu, H Xu, L Yang. Personalized neoantigen pulsed dendritic cell vaccine for advanced lung cancer. Signal Transduct Target Ther 2021; 6(1): 26 https://doi.org/10.1038/s41392-020-00448-5
Y Ma, M Chen, H Jin, BS Prabhakar, T Valyi-Nagy, B He. An engineered herpesvirus activates dendritic cells and induces protective immunity. Sci Rep 2017; 7(1): 41461 https://doi.org/10.1038/srep41461
W Liu, X Wang, X Feng, J Yu, X Liu, X Jia, H Zhang, H Wu, C Wang, J Wu, B Yu, X Yu. Oncolytic adenovirus-mediated intratumoral expression of TRAIL and CD40L enhances immunotherapy by modulating the tumor microenvironment in immunocompetent mouse models. Cancer Lett 2022; 535: 215661 https://doi.org/10.1016/j.canlet.2022.215661
C Rangsitratkul, C Lawson, F Bernier-Godon, SR Niavarani, M Boudaud, S Rouleau, AO Gladu-Corbin, A Surendran, N Ekindi-Ndongo, M Koti, CS Ilkow, PO Richard, LH Tai. Intravesical immunotherapy with a GM-CSF armed oncolytic vesicular stomatitis virus improves outcome in bladder cancer. Mol Ther Oncolytics 2022; 24: 507–521 https://doi.org/10.1016/j.omto.2022.01.009
116
HL Kaufman, SZ Shalhout, G Iodice. Talimogene laherparepvec: moving from first-in-class to best-in-class. Front Mol Biosci 2022; 9: 834841 https://doi.org/10.3389/fmolb.2022.834841
117
SM Ghouse, HM Nguyen, PK Bommareddy, K Guz-Montgomery, D Saha. Oncolytic herpes simplex virus encoding IL12 controls triple-negative breast cancer growth and metastasis. Front Oncol 2020; 10: 384 https://doi.org/10.3389/fonc.2020.00384
118
N Haghighi-Najafabadi, F Roohvand, MS Shams Nosrati, L Teimoori-Toolabi, K Azadmanesh. Oncolytic herpes simplex virus type-1 expressing IL-12 efficiently replicates and kills human colorectal cancer cells. Microb Pathog 2021; 160: 105164 https://doi.org/10.1016/j.micpath.2021.105164
119
S Zafar, S Sorsa, M Siurala, O Hemminki, R Havunen, V Cervera-Carrascon, JM Santos, H Wang, A Lieber, T De Gruijl, A Kanerva, A Hemminki. CD40L coding oncolytic adenovirus allows long-term survival of humanized mice receiving dendritic cell therapy. OncoImmunology 2018; 7(10): e1490856 https://doi.org/10.1080/2162402X.2018.1490856
120
R Wang, J Chen, W Wang, Z Zhao, H Wang, S Liu, F Li, Y Wan, J Yin, R Wang, Y Li, C Zhang, H Zhang, Y Cao. CD40L-armed oncolytic herpes simplex virus suppresses pancreatic ductal adenocarcinoma by facilitating the tumor microenvironment favorable to cytotoxic T cell response in the syngeneic mouse model. J Immunother Cancer 2022; 10(1): e003809 https://doi.org/10.1136/jitc-2021-003809
121
PK Bommareddy, S Aspromonte, A Zloza, SD Rabkin, HL Kaufman. MEK inhibition enhances oncolytic virus immunotherapy through increased tumor cell killing and T cell activation. Sci Transl Med 2018; 10(471): eaau0417 https://doi.org/10.1126/scitranslmed.aau0417
122
S Gettinger, J Choi, K Hastings, A Truini, I Datar, R Sowell, A Wurtz, W Dong, G Cai, MA Melnick, VY Du, J Schlessinger, SB Goldberg, A Chiang, MF Sanmamed, I Melero, J Agorreta, LM Montuenga, R Lifton, S Ferrone, P Kavathas, DL Rimm, SM Kaech, K Schalper, RS Herbst, K Politi. Impaired HLA class I antigen processing and presentation as a mechanism of acquired resistance to immune checkpoint inhibitors in lung cancer. Cancer Discov 2017; 7(12): 1420–1435 https://doi.org/10.1158/2159-8290.CD-17-0593
123
AM D’Alise, G Leoni, G Cotugno, F Troise, F Langone, I Fichera, Lucia M De, L Avalle, R Vitale, A Leuzzi, V Bignone, Matteo E Di, FG Tucci, V Poli, A Lahm, MT Catanese, A Folgori, S Colloca, A Nicosia, E Scarselli. Adenoviral vaccine targeting multiple neoantigens as strategy to eradicate large tumors combined with checkpoint blockade. Nat Commun 2019; 10(1): 2688 https://doi.org/10.1038/s41467-019-10594-2
124
K Das, E Belnoue, M Rossi, T Hofer, S Danklmaier, T Nolden, LM Schreiber, K Angerer, J Kimpel, S Hoegler, B Spiesschaert, L Kenner, D von Laer, K Elbers, M Derouazi, G Wollmann. A modular self-adjuvanting cancer vaccine combined with an oncolytic vaccine induces potent antitumor immunity. Nat Commun 2021; 12(1): 5195 https://doi.org/10.1038/s41467-021-25506-6
S Spranger, D Dai, B Horton, TF Gajewski. Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell 2017; 31(5): 711–723.e4 https://doi.org/10.1016/j.ccell.2017.04.003
127
JP van Vloten, K Matuszewska, MAA Minow, JA Minott, LA Santry, M Pereira, AA Stegelmeier, TM McAusland, EM Klafuric, K Karimi, J Colasanti, DG McFadden, JJ Petrik, BW Bridle, SK Wootton. Oncolytic Orf virus licenses NK cells via cDC1 to activate innate and adaptive antitumor mechanisms and extends survival in a murine model of late-stage ovarian cancer. J Immunother Cancer 2022; 10(3): e004335 https://doi.org/10.1136/jitc-2021-004335
128
V Cervera-Carrascon, DCA Quixabeira, JM Santos, R Havunen, S Zafar, O Hemminki, C Heiniö, E Munaro, M Siurala, S Sorsa, T Mirtti, P Järvinen, M Mildh, H Nisen, A Rannikko, M Anttila, A Kanerva, A Hemminki. Tumor microenvironment remodeling by an engineered oncolytic adenovirus results in improved outcome from PD-L1 inhibition. OncoImmunology 2020; 9(1): 1761229 https://doi.org/10.1080/2162402X.2020.1761229
129
EC Eckert, RA Nace, JM Tonne, L Evgin, RG Vile, SJ Russell. Generation of a tumor-specific chemokine gradient using oncolytic vesicular stomatitis virus encoding CXCL9. Mol Ther Oncolytics 2019; 16: 63–74 https://doi.org/10.1016/j.omto.2019.12.003
130
JH Lee, E Shklovskaya, SY Lim, MS Carlino, AM Menzies, A Stewart, B Pedersen, M Irvine, S Alavi, JYH Yang, D Strbenac, RPM Saw, JF Thompson, JS Wilmott, RA Scolyer, GV Long, RF Kefford, H Rizos. Transcriptional downregulation of MHC class I and melanoma de-differentiation in resistance to PD-1 inhibition. Nat Commun 2020; 11(1): 1897 https://doi.org/10.1038/s41467-020-15726-7
131
P Jugovic, AM Hill, R Tomazin, H Ploegh, DC Johnson. Inhibition of major histocompatibility complex class I antigen presentation in pig and primate cells by herpes simplex virus type 1 and 2 ICP47. J Virol 1998; 72(6): 5076–5084 https://doi.org/10.1128/JVI.72.6.5076-5084.1998
132
SA Gujar, DA Pan, P Marcato, KA Garant, PW Lee. Oncolytic virus-initiated protective immunity against prostate cancer. Mol Ther 2011; 19(4): 797–804 https://doi.org/10.1038/mt.2010.297
133
S Paul, G Lal. The molecular mechanism of natural killer cells function and its importance in cancer immunotherapy. Front Immunol 2017; 8: 1124 https://doi.org/10.3389/fimmu.2017.01124
A Shemesh, H Pickering, KT Roybal, LL Lanier. Differential IL-12 signaling induces human natural killer cell activating receptor-mediated ligand-specific expansion. J Exp Med 2022; 219(8): e20212434 https://doi.org/10.1084/jem.20212434
136
F Souza-Fonseca-Guimaraes, A Young, D Mittal, L Martinet, C Bruedigam, K Takeda, CE Andoniou, MA Degli-Esposti, GR Hill, MJ Smyth. NK cells require IL-28R for optimal in vivo activity. Proc Natl Acad Sci USA 2015; 112(18): E2376–E2384 https://doi.org/10.1073/pnas.1424241112
137
F Hamdan, E Ylösmäki, J Chiaro, Y Giannoula, M Long, M Fusciello, S Feola, B Martins, M Feodoroff, G Antignani, S Russo, O Kari, M Lee, P Järvinen, H Nisen, A Kreutzman, J Leusen, S Mustjoki, TG McWilliams, M Grönholm, V Cerullo. Novel oncolytic adenovirus expressing enhanced cross-hybrid IgGA Fc PD-L1 inhibitor activates multiple immune effector populations leading to enhanced tumor killing in vitro, in vivo and with patient-derived tumor organoids. J Immunother Cancer 2021; 9(8): e003000 https://doi.org/10.1136/jitc-2021-003000
138
B Xu, L Tian, J Chen, J Wang, R Ma, W Dong, A Li, J Zhang, E Antonio Chiocca, B Kaur, M Feng, MA Caligiuri, J Yu. An oncolytic virus expressing a full-length antibody enhances antitumor innate immune response to glioblastoma. Nat Commun 2021; 12(1): 5908 https://doi.org/10.1038/s41467-021-26003-6
139
J Niemann, N Woller, J Brooks, B Fleischmann-Mundt, NT Martin, A Kloos, S Knocke, AM Ernst, MP Manns, S Kubicka, TC Wirth, R Gerardy-Schahn, F Kühnel. Molecular retargeting of antibodies converts immune defense against oncolytic viruses into cancer immunotherapy. Nat Commun 2019; 10(1): 3236 https://doi.org/10.1038/s41467-019-11137-5
140
Q Yang, N Guo, Y Zhou, J Chen, Q Wei, M Han. The role of tumor-associated macrophages (TAMs) in tumor progression and relevant advance in targeted therapy. Acta Pharm Sin B 2020; 10(11): 2156–2170 https://doi.org/10.1016/j.apsb.2020.04.004
141
S Zhu, M Yi, Y Wu, B Dong, K Wu. Roles of tumor-associated macrophages in tumor progression: implications on therapeutic strategies. Exp Hematol Oncol 2021; 10(1): 60 https://doi.org/10.1186/s40164-021-00252-z
142
J Wang, D Li, H Cang, B Guo. Crosstalk between cancer and immune cells: role of tumor-associated macrophages in the tumor microenvironment. Cancer Med 2019; 8(10): 4709–4721 https://doi.org/10.1002/cam4.2327
143
AR Muñoz-Rojas, I Kelsey, JL Pappalardo, M Chen, K Miller-Jensen. Co-stimulation with opposing macrophage polarization cues leads to orthogonal secretion programs in individual cells. Nat Commun 2021; 12(1): 301 https://doi.org/10.1038/s41467-020-20540-2
144
E Müller, PF Christopoulos, S Halder, A Lunde, K Beraki, M Speth, I Øynebråten, A Corthay. Toll-like receptor ligands and interferon-γ synergize for induction of antitumor M1 macrophages. Front Immunol 2017; 8: 1383 https://doi.org/10.3389/fimmu.2017.01383
C Lin, W Ren, Y Luo, S Li, Y Chang, L Li, D Xiong, X Huang, Z Xu, Z Yu, Y Wang, J Zhang, C Huang, N Xia. Intratumoral delivery of a PD-1-blocking scFv encoded in oncolytic HSV-1 promotes antitumor immunity and synergizes with TIGIT blockade. Cancer Immunol Res 2020; 8(5): 632–647 https://doi.org/10.1158/2326-6066.CIR-19-0628
147
F Cao, P Nguyen, B Hong, C DeRenzo, NC Rainusso, T Rodriguez Cruz, MF Wu, H Liu, XT Song, M Suzuki, LL Wang, JT Yustein, S Gottschalk. Engineering oncolytic vaccinia virus to redirect macrophages to tumor cells. Adv Cell Gene Ther 2021; 4(2): e99 https://doi.org/10.1002/acg2.99
148
A Bruno, L Mortara, D Baci, DM Noonan, A Albini. Myeloid derived suppressor cells interactions with natural killer cells and pro-angiogenic activities: roles in tumor progression. Front Immunol 2019; 10: 771 https://doi.org/10.3389/fimmu.2019.00771
149
JN Cheng, YX Yuan, B Zhu, Q Jia. Myeloid-derived suppressor cells: a multifaceted accomplice in tumor progression. Front Cell Dev Biol 2021; 9: 740827 https://doi.org/10.3389/fcell.2021.740827
150
H Wu, SS Li, M Zhou, AN Jiang, Y He, S Wang, W Yang, H Liu. Palliative radiofrequency ablation accelerates the residual tumor progression through increasing tumor-infiltrating MDSCs and reducing T-cell-mediated anti-tumor immune responses in animal model. Front Oncol 2020; 10: 1308 https://doi.org/10.3389/fonc.2020.01308
151
Y Chen, Y Xu, H Zhao, Y Zhou, J Zhang, J Lei, L Wu, M Zhou, J Wang, S Yang, X Zhang, G Yan, Y Li. Myeloid-derived suppressor cells deficient in cholesterol biosynthesis promote tumor immune evasion. Cancer Lett 2023; 564: 216208 https://doi.org/10.1016/j.canlet.2023.216208
152
K Li, H Shi, B Zhang, X Ou, Q Ma, Y Chen, P Shu, D Li, Y Wang. Myeloid-derived suppressor cells as immunosuppressive regulators and therapeutic targets in cancer. Signal Transduct Target Ther 2021; 6(1): 362 https://doi.org/10.1038/s41392-021-00670-9
153
S Tomić, B Joksimović, M Bekić, M Vasiljević, M Milanović, M Čolić, D Vučević. Prostaglanin-E2 potentiates the suppressive functions of human mononuclear myeloid-derived suppressor cells and increases their capacity to expand IL-10-producing regulatory T cell subsets. Front Immunol 2019; 10: 475 https://doi.org/10.3389/fimmu.2019.00475
154
Z Tan, L Liu, MS Chiu, KW Cheung, CW Yan, Z Yu, BK Lee, W Liu, K Man, Z Chen. Virotherapy-recruited PMN-MDSC infiltration of mesothelioma blocks antitumor CTL by IL-10-mediated dendritic cell suppression. OncoImmunology 2018; 8(1): e1518672 https://doi.org/10.1080/2162402X.2018.1518672
155
Y Otani, JY Yoo, CT Lewis, S Chao, J Swanner, T Shimizu, JM Kang, SA Murphy, K Rivera-Caraballo, B Hong, JC Glorioso, H Nakashima, SE Lawler, Y Banasavadi-Siddegowda, JD Heiss, Y Yan, G Pei, MA Caligiuri, Z Zhao, EA Chiocca, J Yu, B Kaur. NOTCH-induced MDSC recruitment after oHSV virotherapy in CNS cancer models modulates antitumor immunotherapy. Clin Cancer Res 2022; 28(7): 1460–1473 https://doi.org/10.1158/1078-0432.CCR-21-2347
156
W Hou, P Sampath, JJ Rojas, SH Thorne. Oncolytic virus-mediated targeting of PGE2 in the tumor alters the immune status and sensitizes established and resistant tumors to immunotherapy. Cancer Cell 2016; 30(1): 108–119 https://doi.org/10.1016/j.ccell.2016.05.012
157
L Rocamora-Reverte, FL Melzer, R Würzner, B Weinberger. The complex role of regulatory T cells in immunity and aging. Front Immunol 2021; 11: 616949 https://doi.org/10.3389/fimmu.2020.616949
158
H Yano, LP Andrews, CJ Workman, DAA Vignali. Intratumoral regulatory T cells: markers, subsets and their impact on anti-tumor immunity. Immunology 2019; 157(3): 232–247 https://doi.org/10.1111/imm.13067
JM González-Navajas, DD Fan, S Yang, FM Yang, B Lozano-Ruiz, L Shen, J Lee. The impact of Tregs on the anticancer immunity and the efficacy of immune checkpoint inhibitor therapies. Front Immunol 2021; 12: 625783 https://doi.org/10.3389/fimmu.2021.625783
161
F Zammarchi, K Havenith, F Bertelli, B Vijayakrishnan, S Chivers, PH van Berkel. CD25-targeted antibody-drug conjugate depletes regulatory T cells and eliminates established syngeneic tumors via antitumor immunity. J Immunother Cancer 2020; 8(2): e000860 https://doi.org/10.1136/jitc-2020-000860
162
I Solomon, M Amann, A Goubier, Vargas F Arce, D Zervas, C Qing, JY Henry, E Ghorani, AU Akarca, T Marafioti, A Śledzińska, Sunderland M Werner, Demane D Franz, JR Clancy, A Georgiou, J Salimu, P Merchiers, MA Brown, R Flury, J Eckmann, C Murgia, J Sam, B Jacobsen, E Marrer-Berger, C Boetsch, S Belli, L Leibrock, J Benz, H Koll, R Sutmuller, KS Peggs, SA Quezada. CD25-Treg-depleting antibodies preserving IL-2 signaling on effector T cells enhance effector activation and antitumor immunity. Nat Cancer 2020; 1(12): 1153–1166 https://doi.org/10.1038/s43018-020-00133-0
163
K Sugawara, M Iwai, H Ito, M Tanaka, Y Seto, T Todo. Oncolytic herpes virus G47Δ works synergistically with CTLA-4 inhibition via dynamic intratumoral immune modulation. Mol Ther Oncolytics 2021; 22: 129–142 https://doi.org/10.1016/j.omto.2021.05.004
164
LD Moon, RA Asher, JW Fawcett. Limited growth of severed CNS axons after treatment of adult rat brain with hyaluronidase. J Neurosci Res 2003; 71(1): 23–37 https://doi.org/10.1002/jnr.10449
165
S Ramanujan, A Pluen, TD McKee, EB Brown, Y Boucher, RK Jain. Diffusion and convection in collagen gels: implications for transport in the tumor interstitium. Biophys J 2002; 83(3): 1650–1660 https://doi.org/10.1016/S0006-3495(02)73933-7
166
A Pires, A Greenshields-Watson, E Jones, K Smart, SN Lauder, M Somerville, S Milutinovic, H Kendrick, JP Hindley, R French, MJ Smalley, WJ Watkins, R Andrews, A Godkin, A Gallimore. Immune remodeling of the extracellular matrix drives loss of cancer stem cells and tumor rejection. Cancer Immunol Res 2020; 8(12): 1520–1531 https://doi.org/10.1158/2326-6066.CIR-20-0070
167
MA Pibuel, D Poodts, M Díaz, SE Hajos, SL Lompardía. The scrambled story between hyaluronan and glioblastoma. J Biol Chem 2021; 296: 100549 https://doi.org/10.1016/j.jbc.2021.100549
168
J Kiyokawa, Y Kawamura, SM Ghouse, S Acar, E Barçın, J Martínez-Quintanilla, RL Martuza, R Alemany, SD Rabkin, K Shah, H Wakimoto. Modification of extracellular matrix enhances oncolytic adenovirus immunotherapy in glioblastoma. Clin Cancer Res 2021; 27(3): 889–902 https://doi.org/10.1158/1078-0432.CCR-20-2400
169
JH Kim, YS Lee, H Kim, JH Huang, AR Yoon, CO Yun. Relaxin expression from tumor-targeting adenoviruses and its intratumoral spread, apoptosis induction, and efficacy. J Natl Cancer Inst 2006; 98(20): 1482–1493 https://doi.org/10.1093/jnci/djj397
170
BK Jung, HY Ko, H Kang, J Hong, HM Ahn, Y Na, H Kim, JS Kim, CO Yun. Relaxin-expressing oncolytic adenovirus induces remodeling of physical and immunological aspects of cold tumor to potentiate PD-1 blockade. J Immunother Cancer 2020; 8(2): e000763 https://doi.org/10.1136/jitc-2020-000763
171
S Quintero-Fabián, R Arreola, E Becerril-Villanueva, JC Torres-Romero, V Arana-Argáez, J Lara-Riegos, MA Ramírez-Camacho, ME Alvarez-Sánchez. Role of matrix metalloproteinases in angiogenesis and cancer. Front Oncol 2019; 9: 1370 https://doi.org/10.3389/fonc.2019.01370
172
A Page-McCaw, AJ Ewald, Z Werb. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007; 8(3): 221–233 https://doi.org/10.1038/nrm2125
173
E Gobin, K Bagwell, J Wagner, D Mysona, S Sandirasegarane, N Smith, S Bai, A Sharma, R Schleifer, JX She. A pan-cancer perspective of matrix metalloproteases (MMP) gene expression profile and their diagnostic/prognostic potential. BMC Cancer 2019; 19(1): 581 https://doi.org/10.1186/s12885-019-5768-0
174
JF Huang, WX Du, JJ Chen. Elevated expression of matrix metalloproteinase-3 in human osteosarcoma and its association with tumor metastasis. J BUON 2016; 21(5): 1279–1286
175
C Mehner, E Miller, A Nassar, WR Bamlet, ES Radisky, DC Radisky. Tumor cell expression of MMP3 as a prognostic factor for poor survival in pancreatic, pulmonary, and mammary carcinoma. Genes Cancer 2015; 6(11–12): 480–489 https://doi.org/10.18632/genesandcancer.90
176
M Liang, J Wang, C Wu, M Wu, J Hu, J Dai, H Ruan, S Xiong, C Dong. Targeting matrix metalloproteinase MMP3 greatly enhances oncolytic virus mediated tumor therapy. Transl Oncol 2021; 14(12): 101221 https://doi.org/10.1016/j.tranon.2021.101221
177
W Mok, Y Boucher, RK Jain. Matrix metalloproteinases-1 and -8 improve the distribution and efficacy of an oncolytic virus. Cancer Res 2007; 67(22): 10664–10668 https://doi.org/10.1158/0008-5472.CAN-07-3107
178
CS Hong, W Fellows, A Niranjan, S Alber, S Watkins, JB Cohen, JC Glorioso, P Grandi. Ectopic matrix metalloproteinase-9 expression in human brain tumor cells enhances oncolytic HSV vector infection. Gene Ther 2010; 17(10): 1200–1205 https://doi.org/10.1038/gt.2010.66
179
H Choi, A Moon. Crosstalk between cancer cells and endothelial cells: implications for tumor progression and intervention. Arch Pharm Res 2018; 41(7): 711–724 https://doi.org/10.1007/s12272-018-1051-1
180
CJ Breitbach, NS De Silva, TJ Falls, U Aladl, L Evgin, J Paterson, YY Sun, DG Roy, JL Rintoul, M Daneshmand, K Parato, MM Stanford, BD Lichty, A Fenster, D Kirn, H Atkins, JC Bell. Targeting tumor vasculature with an oncolytic virus. Mol Ther 2011; 19(5): 886–894 https://doi.org/10.1038/mt.2011.26
181
W Hou, H Chen, J Rojas, P Sampath, SH Thorne. Oncolytic vaccinia virus demonstrates antiangiogenic effects mediated by targeting of VEGF. Int J Cancer 2014; 135(5): 1238–1246 https://doi.org/10.1002/ijc.28747
182
K Matuszewska, LA Santry, JP van Vloten, AWK AuYeung, PP Major, J Lawler, SK Wootton, BW Bridle, J Petrik. Combining vascular normalization with an oncolytic virus enhances immunotherapy in a preclinical model of advanced-stage ovarian cancer. Clin Cancer Res 2019; 25(5): 1624–1638 https://doi.org/10.1158/1078-0432.CCR-18-0220
183
DCA Quixabeira, S Zafar, JM Santos, V Cervera-Carrascon, R Havunen, TV Kudling, S Basnet, M Anttila, A Kanerva, A Hemminki. Oncolytic adenovirus coding for a variant interleukin 2 (vIL-2) cytokine re-programs the tumor microenvironment and confers enhanced tumor control. Front Immunol 2021; 12: 674400 https://doi.org/10.3389/fimmu.2021.674400
184
C Heiniö, R Havunen, J Santos, Lint K de, V Cervera-Carrascon, A Kanerva, A Hemminki. TNFa and IL2 encoding oncolytic adenovirus activates pathogen and danger-associated immunological signaling. Cells 2020; 9(4): 798 https://doi.org/10.3390/cells9040798
185
CN Ekeke, KL Russell, P Murthy, ZS Guo, AC Soloff, D Weber, W Pan, MT Lotze, R Dhupar. Intrapleural interleukin-2-expressing oncolytic virotherapy enhances acute antitumor effects and T-cell receptor diversity in malignant pleural disease. J Thorac Cardiovasc Surg 2022; 163(4): e313–e328 https://doi.org/10.1016/j.jtcvs.2020.11.160
186
Y Ge, H Wang, J Ren, W Liu, L Chen, H Chen, J Ye, E Dai, C Ma, S Ju, ZS Guo, Z Liu, DL Bartlett. Oncolytic vaccinia virus delivering tethered IL-12 enhances antitumor effects with improved safety. J Immunother Cancer 2020; 8(1): e000710 https://doi.org/10.1136/jitc-2020-000710
187
S Nakao, Y Arai, M Tasaki, M Yamashita, R Murakami, T Kawase, N Amino, M Nakatake, H Kurosaki, M Mori, M Takeuchi, T Nakamura. Intratumoral expression of IL-7 and IL-12 using an oncolytic virus increases systemic sensitivity to immune checkpoint blockade. Sci Transl Med 2020; 12(526): eaax7992 https://doi.org/10.1126/scitranslmed.aax7992
188
N Nishio, G Dotti. Oncolytic virus expressing RANTES and IL-15 enhances function of CAR-modified T cells in solid tumors. OncoImmunology 2015; 4(2): e988098 https://doi.org/10.4161/21505594.2014.988098
189
D Liu, J Ma, B Ding, H Zhou. Oncolytic vaccinia virus expressing CD40L (CD40L-VV) inhibits colorectal cancer cell growth and enhances anti-tumor activity of T cells in tumor-bearing mice. Chin J Cell Mol Imm (Xibao Yu Fenzi MianYiXue ZaZhi) 2021; 37(7): 602–607 (in Chinese)
190
M Hinterberger, R Giessel, G Fiore, F Graebnitz, B Bathke, S Wennier, P Chaplin, I Melero, M Suter, H Lauterbach, P Berraondo, H Hochrein, J Medina-Echeverz. Intratumoral virotherapy with 4-1BBL armed modified vaccinia Ankara eradicates solid tumors and promotes protective immune memory. J Immunother Cancer 2021; 9(2): e001586 https://doi.org/10.1136/jitc-2020-001586
191
F Ju, Y Luo, C Lin, X Jia, Z Xu, R Tian, Y Lin, M Zhao, Y Chang, X Huang, S Li, W Ren, Y Qin, M Yu, J Jia, J Han, W Luo, J Zhang, G Fu, X Ye, C Huang, N Xia. Oncolytic virus expressing PD-1 inhibitors activates a collaborative intratumoral immune response to control tumor and synergizes with CTLA-4 or TIM-3 blockade. J Immunother Cancer 2022; 10(6): e004762 https://doi.org/10.1136/jitc-2022-004762
192
S Zuo, M Wei, B He, A Chen, S Wang, L Kong, Y Zhang, G Meng, T Xu, J Wu, F Yang, H Zhang, S Wang, C Guo, J Wu, J Dong, J Wei. Enhanced antitumor efficacy of a novel oncolytic vaccinia virus encoding a fully monoclonal antibody against T-cell immunoglobulin and ITIM domain (TIGIT). EBioMedicine 2021; 64: 103240 https://doi.org/10.1016/j.ebiom.2021.103240
193
CM Arnone, VA Polito, A Mastronuzzi, A Carai, FC Diomedi, L Antonucci, LL Petrilli, M Vinci, F Ferrari, E Salviato, M Scarsella, C De Stefanis, G Weber, C Quintarelli, B De Angelis, MK Brenner, S Gottschalk, V Hoyos, F Locatelli, I Caruana, F Del Bufalo. Oncolytic adenovirus and gene therapy with EphA2-BiTE for the treatment of pediatric high-grade gliomas. J Immunother Cancer 2021; 9(5): e001930 https://doi.org/10.1136/jitc-2020-001930
194
J de Sostoa, CA Fajardo, R Moreno, MD Ramos, M Farrera-Sal, R Alemany. Targeting the tumor stroma with an oncolytic adenovirus secreting a fibroblast activation protein-targeted bispecific T-cell engager. J Immunother Cancer 2019; 7(1): 19 https://doi.org/10.1186/s40425-019-0505-4
195
P Barlabé, J Sostoa, CA Fajardo, R Alemany, R Moreno. Enhanced antitumor efficacy of an oncolytic adenovirus armed with an EGFR-targeted BiTE using menstrual blood-derived mesenchymal stem cells as carriers. Cancer Gene Ther 2020; 27(5): 383–388 https://doi.org/10.1038/s41417-019-0110-1
196
H Khalique, R Baugh, A Dyer, EM Scott, S Frost, S Larkin, J Lei-Rossmann, LW Seymour. Oncolytic herpesvirus expressing PD-L1 BiTE for cancer therapy: exploiting tumor immune suppression as an opportunity for targeted immunotherapy. J Immunother Cancer 2021; 9(4): e001292 https://doi.org/10.1136/jitc-2020-001292
197
W Lei, Q Ye, Y Hao, J Chen, Y Huang, L Yang, S Wang, W Qian. CD19-targeted BiTE expression by an oncolytic vaccinia virus significantly augments therapeutic efficacy against B-cell lymphoma. Blood Cancer J 2022; 12(2): 35 https://doi.org/10.1038/s41408-022-00634-4
198
F Yu, X Wang, ZS Guo, DL Bartlett, SM Gottschalk, XT Song. T-cell engager-armed oncolytic vaccinia virus significantly enhances antitumor therapy. Mol Ther 2014; 22(1): 102–111 https://doi.org/10.1038/mt.2013.240
199
DE Cohn, MW Sill, JL Walker, D O’Malley, CI Nagel, TL Rutledge, W Bradley, DL Richardson, KM Moxley, C Aghajanian. Randomized phase IIB evaluation of weekly paclitaxel versus weekly paclitaxel with oncolytic reovirus (Reolysin®) in recurrent ovarian, tubal, or peritoneal cancer: an NRG oncology/gynecologic oncology group study. Gynecol Oncol 2017; 146(3): 477–483 https://doi.org/10.1016/j.ygyno.2017.07.135
200
E Galanis, LC Hartmann, WA Cliby, HJ Long, PP Peethambaram, BA Barrette, JS Kaur, PJ Jr Haluska, I Aderca, PJ Zollman, JA Sloan, G Keeney, PJ Atherton, KC Podratz, SC Dowdy, CR Stanhope, TO Wilson, MJ Federspiel, KW Peng, SJ Russell. Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res 2010; 70(3): 875–882 https://doi.org/10.1158/0008-5472.CAN-09-2762
201
AJR McGray, RY Huang, S Battaglia, C Eppolito, A Miliotto, KB Stephenson, AA Lugade, G Webster, BD Lichty, M Seshadri, D Kozbor, K Odunsi. Oncolytic Maraba virus armed with tumor antigen boosts vaccine priming and reveals diverse therapeutic response patterns when combined with checkpoint blockade in ovarian cancer. J Immunother Cancer 2019; 7(1): 189 https://doi.org/10.1186/s40425-019-0641-x
202
JA Chesney, I Puzanov, FA Collichio, P Singh, MM Milhem, J Glaspy, O Hamid, M Ross, P Friedlander, C Garbe, T Logan, A Hauschild, C Lebbé, H Joshi, W Snyder, JM Mehnert. Talimogene laherparepvec in combination with ipilimumab versus ipilimumab alone for advanced melanoma: 5-year final analysis of a multicenter, randomized, open-label, phase II trial. J Immunother Cancer 2023; 11(5): e006270 https://doi.org/10.1136/jitc-2022-006270
N El-Sayes, A Vito, K Mossman. Tumor heterogeneity: a great barrier in the age of cancer immunotherapy. cancers (Basel) 2021; 13(4): 806 https://doi.org/10.3390/cancers13040806
205
T Suzuki, H Uchida, T Shibata, Y Sasaki, H Ikeda, M Hamada-Uematsu, R Hamasaki, K Okuda, S Yanagi, H Tahara. Potent anti-tumor effects of receptor-retargeted syncytial oncolytic herpes simplex virus. Mol Ther Oncolytics 2021; 22: 265–276 https://doi.org/10.1016/j.omto.2021.08.002
206
EA van Erp, LN Kaliberova, SA Kaliberov, DT Curiel. Retargeted oncolytic adenovirus displaying a single variable domain of camelid heavy-chain-only antibody in a fiber protein. Mol Ther Oncolytics 2015; 2: 15001 https://doi.org/10.1038/mto.2015.1
207
L Evgin, T Kottke, J Tonne, J Thompson, AL Huff, J van Vloten, M Moore, J Michael, C Driscoll, J Pulido, E Swanson, R Kennedy, M Coffey, H Loghmani, L Sanchez-Perez, G Olivier, K Harrington, H Pandha, A Melcher, RM Diaz, RG Vile. Oncolytic virus-mediated expansion of dual-specific CAR T cells improves efficacy against solid tumors in mice. Sci Transl Med 2022; 14(640): eabn2231 https://doi.org/10.1126/scitranslmed.abn2231
208
R Rezaei, H Esmaeili Gouvarchin Ghaleh, M Farzanehpour, R Dorostkar, R Ranjbar, M Bolandian, M Mirzaei Nodooshan, A Ghorbani Alvanegh. Combination therapy with CAR T cells and oncolytic viruses: a new era in cancer immunotherapy. Cancer Gene Ther 2022; 29(6): 647–660 https://doi.org/10.1038/s41417-021-00359-9
209
V Schirrmacher. Cancer vaccines and oncolytic viruses exert profoundly lower side effects in cancer patients than other systemic therapies: a comparative analysis. Biomedicines 2020; 8(3): 61 https://doi.org/10.3390/biomedicines8030061
210
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 2018; 174(4): 1031–1032 https://doi.org/10.1016/j.cell.2018.07.035
211
W Liu, Y Liu, C Hu, C Xu, J Chen, Y Chen, J Cai, G Yan, W Zhu. Cytotoxic T lymphocyte-associated protein 4 antibody aggrandizes antitumor immune response of oncolytic virus M1 via targeting regulatory T cells. Int J Cancer 2021; 149(6): 1369–1384 https://doi.org/10.1002/ijc.33703
212
B Zhang, P Cheng. Improving antitumor efficacy via combinatorial regimens of oncolytic virotherapy. Mol Cancer 2020; 19(1): 158 https://doi.org/10.1186/s12943-020-01275-6
213
Z Zhu, AJR McGray, W Jiang, B Lu, P Kalinski, ZS Guo. Improving cancer immunotherapy by rationally combining oncolytic virus with modulators targeting key signaling pathways. Mol Cancer 2022; 21(1): 196 https://doi.org/10.1186/s12943-022-01664-z