Current status and research progress of oncolytic virus

Yingyu Chen , Mengyuan Tao , Xuwei Wu , Zheng Tang , Yinfu Zhu , Kunxiang Gong , Yinger Huang , Wenbo Hao

Pharmaceutical Science Advances ›› 2024, Vol. 2 ›› Issue (1) : 100037

PDF (1340KB)
Pharmaceutical Science Advances ›› 2024, Vol. 2 ›› Issue (1) : 100037 DOI: 10.1016/j.pscia.2024.100037
Review Article
research-article

Current status and research progress of oncolytic virus

Author information +
History +
PDF (1340KB)

Abstract

Oncolytic viruses (OVs) are natural or genetically recombinant viruses that selectively infect and kill tumor cells without affecting normal cell growth. As a novel type of immunotherapy, OVs have been shown to activate antitumor immune responses, regulate the tumor microenvironment, and enhance the efficacy of immune checkpoint inhibitors. In this review article, we discuss the latest research on the characteristics, antitumor mechanisms, and status of OV research. In terms of mechanism of action, after targeting tumor cells, OVs not only directly lyse tumor cells but also exert antitumor effects through indirect approaches. As an emerging cancer treatment, OVs face challenges that need to be overcome. Finally, we summarize the challenges and prospects for the future application of OVs.

Keywords

Oncolytic virus / Malignant tumor / Immunotherapy / Genetic modification / Tumor microenvironment / Systemic administration

Cite this article

Download citation ▾
Yingyu Chen, Mengyuan Tao, Xuwei Wu, Zheng Tang, Yinfu Zhu, Kunxiang Gong, Yinger Huang, Wenbo Hao. Current status and research progress of oncolytic virus. Pharmaceutical Science Advances, 2024, 2(1): 100037 DOI:10.1016/j.pscia.2024.100037

登录浏览全文

4963

注册一个新账户 忘记密码

Author contributions

Yingyu Chen and Mengyuan Tao drafted the manuscript. Yinger Huang and Wenbo Hao obtained funding and designed, conceived, and supervised the study. Xuwei Wu, Zheng Tang, Yinfu Zhu, and Kunxiang Gong searched for and reviewed previous studies. Fig. 1, Fig. 2, Fig. 3 were original created by Xuwei Wu and Fig. 4 was created by Mengyuan Tao. All elements involved in the figures were designed using Adobe Illustrator 2020 and Procreate. All the authors have read and approved the final version of the manuscript.

Ethics approval

Not applicable.

Funding information

This work was supported by the China Innovation and Entrepreneurship Training Project for College Students (S202212121159), China Postdoctoral Science Foundation (No. 2023M731574), and National Natural Science Foundation of China (Nos. 82304781 and 31672536).

Data availability

Not applicable.

Declaration of competing interest

All authors declare no conflicts of interest regarding the present work and have no involvement that might raise the question of bias in the work reported or in the conclusions, implications, or opinions stated.

Acknowledgements

Not applicable.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.pscia.2024.100037.

References

[1]

N.G. Zaorsky, T.M. Churilla, B.L. Egleston, S.G. Fisher, J.A. Ridge, E.M. Horwitz, J.E. Meyer, Causes of death among cancer patients, Ann. Oncol. 28 (2017) 400-407. https://doi.org/10.1093/annonc/mdw604.

[2]

Y. Luo, S. Yin, J. Lu, S. Zhou, Y. Shao, X. Bao, T. Wang, Y. Qiu, H. Yu, Tumor microenvironment: a prospective target of natural alkaloids for cancer treatment, Cancer Cell Int. 21 (2021) 386. https://doi.org/10.1186/s12935-021-02085-6.

[3]

G.L. Szeto, S.D. Finley, Integrative approaches to cancer immunotherapy, Trends Cancer. 5 (2019) 400-410. https://doi.org/10.1016/j.trecan.2019.05.010.

[4]

J.H. Cha, L.C. Chan, M.S. Song, M.C. Hung, New approaches on cancer immunotherapy, Cold Spring Harb Perspect Med. 10 (2020) a036863. https://doi.org/10.1101/cshperspect.a036863.

[5]

N. Lorig-Roach, N.M. Harpell, R.M. DuBois, Structural basis for the activity and specificity of the immune checkpoint inhibitor lirilumab, Sci. Rep. 14 (2024) 742. https://doi.org/10.1038/s41598-023-50262-6.

[6]

M.P. Jogalekar, R.L. Rajendran, F. Khan, C. Dmello, P. Gangadaran, B.C. Ahn, CAR T-cell-based gene therapy for cancers: new perspectives, challenges, and clinical developments, Front. Immunol. 13 (2022) 925985. https://doi.org/10.3389/fimmu.2022.925985.

[7]

S.C. Wei, C.R. Duffy, J.P. Allison, Fundamental mechanisms of immune checkpoint blockade therapy, Cancer Discov. 8 (2018) 1069-1086. https://doi.org/10.1158/2159-8290.CD-18-0367.

[8]

D.S. Chen, I. Mellman, Oncology meets immunology: the cancer-immunity cycle, Immunity. 39 (2013) 1-10. http://dx.doi.org/10.1016/j.immuni.2013.07.012.

[9]

S.T. Workenhe, M.L. Verschoor, K.L. Mossman, The role of oncolytic virus immunotherapies to subvert cancer immune evasion, Future Oncol. 11 (2015) 675-689. https://doi.org/10.2217/fon.14.254.

[10]

S.R. Jhawar, A. Thandoni, P.K. Bommareddy, S. Hassan, F.J. Kohlhapp, S. Goyal, J.M. Schenkel, A.W. Silk, A. Zloza, Oncolytic viruses-natural and genetically engineered cancer immunotherapies, Front. Oncol. 7 (2017) 202. https://doi.o rg/10.3389/fonc.2017.00202.

[11]

J.P. van Vloten, S.T. Workenhe, S.K. Wootton, K.L. Mossman, B.W. Bridle, Critical interactions between immunogenic cancer cell death, oncolytic viruses, and the immune system define the rational design of combination immunotherapies, J. Immunol (2018) 450-458. https://doi.org/10.4049/jimmunol.1701021.

[12]

A.M. Henao-Restrepo, A. Camacho, I.M. Longini, C.H. Watson, W.J. Edmunds, M. Egger, M.W. Carroll, N.E. Dean, I. Diatta, M. Doumbia, B. Draguez, Efficacy and effectiveness of an rVSV-vectored vaccine in preventing Ebola virus disease: final results from the Guinea ring vaccination, open-label, cluster-randomised trial (Ebola Ca Suffit!), Lancet. 389 (2017) 505-518. https://doi.org/10.1016/S0140-6736(16)32621-6.

[13]

A. Kloos, N. Woller, R. Gerardy-Schahn, F. Kuhnel, Retargeted oncolytic viruses provoke tumor-directed T-cell responses, OncoImmunology. 4 (2015) e1052933. https://doi.org/10.1080/2162402x.2015.1052933.

[14]

S.K. Green, M.C. Karlsson, J.V. Ravetch, R.S. Kerbel, Disruption of cell-cell adhesion enhances antibody-dependent cellular cytotoxicity: implications for antibody-based therapeutics of cancer, Cancer Res. 62 (2002) 6891-6900.

[15]

J.T. Mullen, K.K. Tanabe, Viral oncolysis, Oncol. 7 (2002) 106-119. https://doi.org/10.1634/theoncologist.7-2-106.

[16]

X.Y. Ma, B.D. Hill, T. Hoang, F. Wen, Virus-inspired strategies for cancer therapy, Semin. Cancer Biol. 86 (2022) 1143-1157. https://doi.org/10.1016/j.semcancer.2021.06.021.

[17]

M. Watanabe, Y. Nishikawaji, H. Kawakami, K.I. Kosai, Adenovirus biology, recombinant adenovirus, and adenovirus usage in gene therapy, Viruses. 13 (2021) 2502. https://doi.org/10.3390/v13122502.

[18]

P.L. Triozzi, E.C. Borden, VB-111 for cancer, Expet Opin. Biol. Ther. 11 (2011) 1669-1676. https://doi.org/10.1517/14712598.2011.618122.

[19]

R.C. Arend, B.J. Monk, T.J. Herzog, K.N. Moore, R. Shapira-Frommer, J.A. Ledermann, K.S. Tewari, A.A. Secord, T. Rachmilewitz Minei, L.S. Freedman, A. Miller, S.F. Shmueli, M. Lavi, R.T. Penson, Utilizing an interim futility analysis of the OVAL study (VB-111-701/GOG 3018) for potential reduction of risk: a phase III, double blind, randomized controlled trial of ofranergene obadenovec (VB-111) and weekly paclitaxel in patients with platinum resistant ovarian cancer, Gynecol. Oncol. 161 (2021) 496-501. https://doi.org/10.1016/j.ygyno.2021.02.014.

[20]

F.F. Lang, C. Conrad, C. Gomez-Manzano, W.K.A. Yung, R. Sawaya, J.S. Weinberg, S.S. Prabhu, G. Rao, G.N. Fuller, K.D. Aldape, J. Gumin, L.M. Vence, I. Wistuba, J. Rodriguez-Canales, P.A. Villalobos, C.M.F. Dirven, S. Tejada, R.D. Valle, M.M. Alonso, B. Ewald, J.J. Peterkin, F. Tufaro, J. Fueyo, Phase I study of DNX- 2401 (Delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma, J. Clin. Oncol. 36 (2018) 1419-1427. https://doi.org/10.1200/JCO.2017.75.8219.

[21]

P.H. Cheng, S.L. Wechman, K.M. McMasters, H.S. Zhou, Oncolytic replication of E1b-deleted adenoviruses, Viruses. 7 (2015) 5767-5779. https://doi.org/10.3390/v7112905.

[22]

N. Ramesh, Y. Ge, D.L. Ennist, M. Zhu, M. Mina, S. Ganesh, P.S. Reddy, D.C. Yu, CG0070, a conditionally replicating granulocyte macrophage colony-stimulating factor-armed oncolytic adenovirus for the treatment of bladder cancer, Clin. Cancer Res. 12 (2006) 305-313. https://doi.org/10.1158/1078-0432.CCR-05-1059.

[23]

I. Mori, Y. Nishiyama, Herpes simplex virus and varicella-zoster virus: why do these human alphaherpesviruses behave so differently from one another? Rev. Med. Virol. 15 (2005) 393-406. https://doi.org/10.1002/rmv.478.

[24]

Y. Ma, H. Jin, T. Valyi-Nagy, Y. Cao, Z. Yan, B. He, Inhibition of TANK binding kinase 1 by herpes simplex virus 1 facilitates productive infection, J. Virol. 86 (2012) 2188-2196. https://doi.org/10.1128/jvi.05376-11.

[25]

E.I. Tognarelli, T.F. Palomino, N. Corrales, S.M. Bueno, A.M. Kalergis, P.A. González, Herpes simplex virus evasion of early host antiviral responses, Front. Cell. Infect. Microbiol. 9 (2019) 127. https://doi.org/10.3389/fcimb.2019.00127.

[26]

F. Lassalle, M.A. Beale, T. Bharucha, C.A. Williams, R.J. Williams, J. Cudini, R. Goldstein, T. Haque, D.P. Depledge, J. Breuer, Whole genome sequencing of Herpes Simplex Virus 1 directly from human cerebrospinal fluid reveals selective constraints in neurotropic viruses, Virus Evol. 6 (2020) veaa012, https://doi.org/10.1093/ve/veaa012.

[27]

I. Mori, Y. Nishiyama, Accessory genes define the relationship between the herpes simplex virus and its host, Microb. Infect. 8 (2006) 2556-2562. https://doi.org/10.1016/j.micinf.2006.05.007.

[28]

A. Pourchet, S.R. Fuhrmann, K.A. Pilones, S. Demaria, A.B. Frey, M. Mulvey, I. Mohr, CD8(þ) T-cell Immune evasion enables oncolytic virus immunotherapy, EBioMedicine. 5 (2016) 59-67. https://doi.org/10.1016/j.ebiom.2016.01.022.

[29]

M.K. Aghi, E.A. Chiocca, Phase ib trial of oncolytic herpes virus G207 shows safety of multiple injections and documents viral replication, Mol. Ther. 17 (2009) 8-9. https://doi.org/10.1038/mt.2008.275.

[30]

J. Fueyo, R. Alemany, C. Gomez-Manzano, G.N. Fuller, A. Khan, C.A. Conrad, T.J. Liu, H. Jiang, M.G. Lemoine, K. Suzuki, R. Sawaya, D.T. Curiel, W.K. Yung, F.F. Lang, Preclinical characterization of the antiglioma activity of a tropismenhanced adenovirus targeted to the retinoblastoma pathway, J. Natl. Cancer Inst. 95 (2003) 652-660. https://doi.org/10.1093/jnci/95.9.652.

[31]

T. Todo, Y. Ino, H. Ohtsu, J. Shibahara, M. Tanaka, A phase I/II study of triplemutated oncolytic herpes virus G47Δ in patients with progressive glioblastoma, Nat. Commun. 13 (2022) 4119. https://doi.org/10.1038/s41467-022-31262-y.

[32]

C. Grigg, Z. Blake, R. Gartrell, A. Sacher, B. Taback, Y. Saenger, Talimogene laherparepvec (T-Vec) for the treatment of melanoma and other cancers, Semin. Oncol. 43 (2016) 638-646. https://doi.org/10.1053/j.seminoncol.2016.10.005.

[33]

P.F. Ferrucci, L. Pala, F. Conforti, E. Cocorocchio, Talimogene laherparepvec (TVEC): an intralesional cancer immunotherapy for advanced melanoma, Cancers. 13 (2021) 1383. https://doi.org/10.3390/cancers13061383.

[34]

D.V. Chouljenko, J. Ding, I.F. Lee, Y.M. Murad, X. Bu, G. Liu, Z. Delwar, Y. Sun, S. Yu, I. Samudio, R. Zhao, Induction of durable antitumor response by a novel oncolytic herpesvirus expressing multiple immunomodulatory transgenes, Biomedicines. 8 (2020) 484. https://doi.org/10.3390/biomedicines8110484.

[35]

D.V. Chouljenko, Y.M. Murad, I.F. Lee, Z. Delwar, J. Ding, G. Liu, X. Liu, X. Bu, Y. Sun, I. Samudio, W.W.G. Jia,Targeting carcinoembryonic antigen-expressing tumors using a novel transcriptional and translational dual-regulated oncolytic herpes simplex virus type 1, Mol Ther Oncolytics. 28 (2023) 334-348. https://doi.org/10.1016/j.omto.2023.02.003.

[36]

Z.S. Guo, B. Lu, Z. Guo, E. Giehl, M. Feist, E. Dai, W. Liu, W.J. Storkus, Y. He, Z. Liu, D.L. Bartlett, Vaccinia virus-mediated cancer immunotherapy: cancer vaccines and oncolytics, J Immunother Cancer. 7 (2019) 6. https://doi.org/10.1186/s40425-018-0495-7.

[37]

N. Lee, Y.H. Jeon, J. Yoo, S.K. Shin, S. Lee, M.J. Park, B.J. Jung, Y.K. Hong, D.S. Lee, K. Oh, Generation of novel oncolytic vaccinia virus with improved intravenous efficacy through protection against complement-mediated lysis and evasion of neutralization by vaccinia virus-specific antibodies, J Immunother Cancer. 11 (2023) e006024. https://doi.org/10.1136/jitc-2022-006024.

[38]

L.E. Torres-Domínguez, G. McFadden G, Poxvirus oncolytic virotherapy, Expet Opin. Biol. Ther. 19 (2019) 561-573. https://doi.org/10.1080/14712598.2019.1600669.

[39]

Y. Woo, Z. Zhang, A. Yang, S. Chaurasiya, A.K. Park, J. Lu, S.I. Kim, S.G. Warner, D. Von Hoff, Y. Fong, Novel chimeric immuno-oncolytic virus CF33-hNISantiPDL1 for the treatment of pancreatic cancer, J. Am. Coll. Surg. 230 (2020) 709-717. https://doi.org/10.1016/j.jamcollsurg.2019.12.027.

[40]

S.G. Warner, S.I. Kim, S. Chaurasiya, M.P. O’Leary, J. Lu, V. Sivanandam, Y. Woo, N.G. Chen, Y. Fong, A novel chimeric poxvirus encoding hNIS is tumor-tropic, imageable, and synergistic with radioiodine to sustain colon cancer regression, Mol Ther Oncolytics. 13 (2019) 82-92. https://doi.org/10.1016/j.omto.2019.04.001.

[41]

T. Ferreira, A. Kulkarni, C. Bretscher, P.V. Nazarov, J.A. Hossain, L.A.R. Ystaas, H. Miletic, R. Röth, B. Niesler, A. Marchini, Oncolytic H-1 parvovirus hijacks galectin-1 to enter cancer cells, Viruses. 14 (2022) 1018. https://doi.org/10.3390/v14051018.

[42]

A. Marchini, L. Daeffler, V.I. Pozdeev, A. Angelova, J. Rommelaere, Immune conversion of tumor microenvironment by oncolytic viruses: the protoparvovirus H-1PV case study, Front. Immunol. 10 (2019) 1848. https://doi.org/10.3389/fimmu.2019.01848.

[43]

J. Fakhiri, D. Grimm, Best of most possible worlds: hybrid gene therapy vectors based on parvoviruses and heterologous viruses, Mol. Ther. 29 (2021) 3359-3382. https://doi.org/10.1016/j.ymthe.2021.04.005.

[44]

D. Masemann, Y. Boergeling, S. Ludwig, Employing RNA viruses to fight cancer: novel insights into oncolytic virotherapy, Biol. Chem. 398 (2017) 891-909. https://doi.org/10.1515/hsz-2017-0103.

[45]

R. Sanjuán, P. Domingo-Calap, Mechanisms of viral mutation, Cell. Mol. Life Sci. 73 (2016) 4433-4448. https://doi.org/10.1007/s00018-016-2299-6.

[46]

K. Lundstrom, Therapeutic applications for oncolytic self-replicating RNA viruses, Int. J. Mol. Sci. 23 (2022) 15622. https://doi.org/10.3390/ijms232415622.

[47]

V. Schirrmacher, Molecular mechanisms of anti-neoplastic and immune stimulatory properties of oncolytic Newcastle disease virus, Biomedicines. 10 (2022) 562. https://doi.org/10.3390/biomedicines10030562.

[48]

X. Cheng, W. Wang, Q. Xu, J. Harper, D. Carroll, M.S. Galinski, J. Suzich, H. Jin, Genetic modification of oncolytic Newcastle disease virus for cancer therapy, J. Virol. 90 (2016) 5343-5352. https://doi.org/10.1128/jvi.00136-16.

[49]

Y. Yanagi, M. Takeda, S. Ohno, Measles virus: cellular receptors, tropism and pathogenesis, J. Gen. Virol. 87 (2006) 2767-2779. https://doi.org/10.1099/vir.0.82221-0.

[50]

G. Lal, M.S. Rajala, Combination of oncolytic measles virus armed with BNiP3, a pro-apoptotic gene and paclitaxel induces breast cancer cell death, Front. Oncol. 8 (2019) 676. https://doi.org/10.3389/fonc.2018.00676.

[51]

B. Thompson, Oncolytics Biotech Inc, REOLYSIN for melanoma therapy, Melanoma. Manag. 2 (2015) 105-107. https://doi.org/10.2217/mmt.15.13.

[52]

D. Mahalingam, C. Fountzilas, J. Moseley, N. Noronha, H. Tran, R. Chakrabarty, G. Selvaggi, M. Coffey, B. Thompson, J. Sarantopoulos, A phase II study of REOLYSIN((R)) (pelareorep) in combination with carboplatin and paclitaxel for patients with advanced malignant melanoma, Cancer Chemother. Pharmacol. 79 (2017) 697-703. https://doi.org/10.1007/s00280-017-3260-6.

[53]

C. DeAntoneo, P. Danthi, S. Balachandran, Reovirus activated cell death pathways, Cells. 11 (2022) 1757. https://doi.org/10.3390/cells11111757.

[54]

P. Alberts, A. Tilgase, A. Rasa, K. Bandere, D. Venskus D, The advent of oncolytic virotherapy in oncology: the Rigvir(R) story, Eur. J. Pharmacol. 837 (2018) 117-126. https://doi.org/10.1016/j.ejphar.2018.08.042.

[55]

A. Tilgase, L. Patetko, I. Bláķ e, A. Ramata-Stunda, M. Boroduśķ is, P. Alberts, Effect of the oncolytic ECHO-7 virus Rigvir® on the viability of cell lines of human origin in vitro, J. Cancer. 9 (2018) 1033-1049. https://doi.org/10.7150/jca.23242.

[56]

S. Bradley, A.D. Jakes, K. Harrington, H. Pandha, A. Melcher, F. Errington-Mais, Applications of coxsackievirus A21 in oncology, Oncolytic Virotherapy. 3 (2014) 47-55. https://doi.org/10.2147/OV.S56322.

[57]

M. Sam, M. Selman, W. Zhao, J. Jung, A. Willingham, U. Phan, G.C. Starling, Q. Gao, Engineering oncolytic coxsackievirus A21 with small transgenes and enabling cell-mediated virus delivery by integrating viral cDNA into the genome, J. Virol. 97 (2023) e0030923. https://doi.org/10.1128/jvi.00309-23.

[58]

D. Lin, Y. Shen, T. Liang, Oncolytic virotherapy: basic principles, recent advances and future directions, Signal Transduct, Targeted Ther. 8 (2023) 156. https://doi.org/10.1038/s41392-023-01407-6.

[59]

J.R. Bischoff, D.H. Kirn, A. Williams, C. Heise, S. Horn, M. Muna, L. Ng, J.A. Nye, A. Sampson-Johannes, A. Fattaey, F. McCormick, An adenovirus mutant that replicates selectively in p53-deficient human tumor cells, Science. 5286 (1996) 373-376. https://doi.org/10.1126/science.274.5286.373.

[60]

R.E. Tamura, I.V. de Luna, M.G. Lana, B.E. Strauss, Improving adenoviral vectors and strategies for prostate cancer gene therapy, Clinics. 73 (2018) e476s. https://doi.org/10.6061/clinics/2018/e476s.

[61]

E. Yue, G. Yang, Y. Yao, G. Wang, A. Mohanty, F. Fan, L. Zhao, Y. Zhang, T. Mirzapoiazova, T.C. Walser, L. Rodriguez-Rodriguez, Y. Fong, R. Salgia, E.W. Wang, Targeting CA-125 transcription by development of a conditionally replicative adenovirus for ovarian cancer treatment, Cancers. 13 (2021) 4265. https://doi.org/10.3390/cancers13174265.

[62]

A. Geisler, A. Hazini, L. Heimann, J. Kurreck, H. Fechner, Coxsackievirus B3-Its potential as an oncolytic virus, Viruses. 13 (2021) 718. https://doi.org/10.3390/v13050718.

[63]

D.E. Post, E.G. Van Meir, A novel hypoxia-inducible factor (HIF) activated oncolytic adenovirus for cancer therapy, Oncogene. 22 (2003) 2065-2072. https://doi.org/10.1038/sj.onc.1206464.

[64]

K.B. Parker, Y. Shimizu, M. Andreeff, F.F. Lang, Mesenchymal stromal cells for the delivery of oncolytic viruses in gliomas, Cytotherapy. 19 (2017) 445-457. https://doi.org/10.1016/j.jcyt.2017.02.002.

[65]

A.S. Novozhilov, F.S. Berezovskaya, E.V. Koonin, G.P. Karev, Mathematical modeling of tumor therapy with oncolytic viruses: regimes with complete tumor elimination within the framework of deterministic models, Biol. Direct. 1 (2006) 6. https://doi.org/10.1186/1745-6150-1-6.

[66]

N. Martinez-Velez, V. Laspidea, M. Zalacain, M. Labiano S, García-Moure, M. Puigdelloses, L. Marrodan, M. Gonzalez-Huarriz, G. Herrador, D. de la Nava, I. Ausejo-Mauleon, J. Fueyo, C. Gomez-Manzano, A.A. Patiño-García, M.M. Alonso, Local treatment of a pediatric osteosarcoma model with a 4-1 BBL armed oncolytic adenovirus results in an antitumor effect and leads to immune memory, Mol. Cancer Therapeut. 3 (2022) 471-480. https://doi.org/10.1158/1535-7163.MCT-21-0565.

[67]

L. Yang, X. Gu, J. Yu, S. Ge, X. Fan, Oncolytic virotherapy: from bench to bedside, Front. Cell Dev. Biol. 9 (2021) 790150. https://doi.org/10.3389/fcell.2021.790150.

[68]

C.D. Zhang, L.H. Jiang, X. Zhou, Y.P. He, Y. Liu, D.M. Zhou, Y. Lv, B.Q. Wu, Z.Y. Zhao, Synergistic antitumor efficacy of rMV-Hu191 and olaparib in pancreatic cancer by generating oxidative DNA damage and ROS-dependent apoptosis, Transl Oncol. 39 (2023) 101812. https://doi.org/10.1016/j.tranon.2023.101812.

[69]

C.H. Liu, C.J. Tai, Y.T. Kuo, S.S. Chang, L.T. Lin, Combination of oncolytic measles virus and ursolic acid synergistically induces oncolysis of hepatocellular carcinoma cells, Viruses. 15 (2023) 1294. https://doi.org/10.3390/v15061294.

[70]

F. Li, Y. Yuan, Y. Dai, T. Cheng, H. Cao, D. Yan, Y. Li, Q. Sun, X. Huang, Q. Gao, M11: a tropism-modified oncolytic adenovirus arming with a tumor-homing peptide for advanced ovarian cancer therapies, Hum. Gene Ther. 33 (2022) 262-274. https://doi.org/10.1089/hum.2021.247.

[71]

T. Xiao, J.K. Fan, H.L. Huang, J.F. Gu, L.Y. Li, X.Y. Liu, VEGI-armed oncolytic adenovirus inhibits tumor neovascularization and directly induces mitochondriamediated cancer cell apoptosis, Cell Res. 20 (2010) 367-378. https://doi.org/10.1038/cr.2009.126.

[72]

P. Hersey, X.D. Zhang, Overcoming resistance of cancer cells to apoptosis, J. Cell. Physiol. 196 (2003) 9-18. https://doi.org/10.1002/jcp.10256.

[73]

H. Deng, B. Xiao, Y. Huang, K. Weng, J. Chen, K. Li, H. Wu, S. Luo, W. Hao, The combined use of Orf virus and PAK4 inhibitor exerts anti-tumor effect in breast cancer, Front. Microbiol. 13 (2022) 845259. https://doi.org/10.3389/fmicb.2022.845259.

[74]

S. Elankumaran, D. Rockemann, S.K. Samal, Newcastle disease virus exerts oncolysis by both intrinsic and extrinsic caspase-dependent pathways of cell death, J. Virol. 15 (2006) 7522-7534. https://doi.org/10.1128/jvi.00241-06.

[75]

J. Kalyanasundram, A. Hamid, K. Yusoff, S.L. Chia, Newcastle disease virus strain AF2240 as an oncolytic virus: a review, Acta Trop. 183 (2018) 126-133. https://doi.org/10.1016/j.actatropica.2018.04.007.

[76]

J. Hu, H. Wang, J. Gu, X. Liu, X. Zhou, Trail armed oncolytic poxvirus suppresses lung cancer cell by inducing apoptosis, Acta Biochim. Biophys. Sin. 50 (2018) 1018-1027. https://doi.org/10.1093/abbs/gmy096.

[77]

W. Zhu, H. Zhang, Y. Shi, M. Song, B. Zhu, L. Wei, Oncolytic adenovirus encoding tumor necrosis factor-related apoptosis inducing ligand (TRAIL) inhibits the growth and metastasis of triple-negative breast cancer, Cancer Biol. Ther. 14 (2013) 1016-1023. https://doi.org/10.4161/cbt.26043.

[78]

X. Yang, Y. Wang, Q. Li, Y. Zhong, L. Chen, Y. Du, J. He, L. Liao, K. Xiong, C.X. Yi, J. Yan, The main molecular mechanisms underlying methamphetamine- induced neurotoxicity and implications for pharmacological treatment, Front. Mol. Neurosci. 11 (2018) 186. https://doi.org/10.3389/fnmol.2018.00186.

[79]

X. Jia, Y. Chen, X. Zhao, C. Lv, J. Yan, Oncolytic vaccinia virus inhibits human hepatocellular carcinoma MHCC97-H cell proliferation via endoplasmic reticulum stress, autophagy and Wnt pathways, Gen. Med. 18 (2016) 211-219. https://doi.org/10.1002/jgm.2893.

[80]

Z. Wang, W. Liu, L. Wang, P. Gao, Z. Li, J. Wu, H. Zhang, H. Wu, W. Kong, B. Yu, X. Yu, Enhancing the antitumor activity of an engineered TRAIL-coated oncolytic adenovirus for treating acute myeloid leukemia, Signal Transduct. Targeted Ther. 5 (2020) 40. https://doi.org/10.1038/s41392-020-0135-9.

[81]

R. Reddy, S.C. Yan, Z. Hasanpour Segherlou, M.R. Hosseini-Siyanaki, J. Poe, C. Perez-Vega, E.A. Chiocca, B. Lucke-Wold, Oncolytic viral therapy: a review and promising future directions, J. Neurosurg. 140 (2023) 319-327. https://doi.org/10.3171/2023.6.JNS23243.

[82]

H.L. Kaufman, F.J. Kohlhapp, A. Zloza, Oncolytic viruses: a new class of immunotherapy drugs, Nat. Rev. Drug Discov. 14 (2015) 642-662. https://doi.org/10.1038/nrd4663.

[83]

H. Li, S. Zhao, L. Shen, P. Wang, S. Liu, Y. Ma, Z. Liang, G. Wang, J. Lv, W. Qiu, E2F 2 inhibition induces autophagy via the PI3K/Akt/mTOR pathway in gastric cancer, Aging. 10 (2021) 13626-13643. https://doi.org/10.18632/aging.202891.

[84]

J. Zhang, W. Lai, Q. Li, Y. Yu, J. Jin, W. Guo, X. Zhou, X. Liu, Y. Wang, A novel oncolytic adenovirus targeting Wnt signaling effectively inhibits cancer-stem like cell growth via metastasis, apoptosis and autophagy in HCC models, Biochem. Biophys. Res. Commun. 491 (2017) 469-477. https://doi.org/10.1016/j.bbrc.2017.07.041.

[85]

F. Eckerdt, L.C. Platanias, Emerging role of glioma stem cells in mechanisms of therapy resistance, Cancers 15 (2023) 3458, https://doi.org/10.3390/cancers15133458.

[86]

H. Jiang, E.J. White, C. Gomez-Manzano, J. Fueyo, Adenovirus’s last trick: you say lysis, we say autophagy, Autophagy. 4 (2008) 118-120. https://doi.org/10.4161/auto.5260.

[87]

Y. Huang, Y. Huang, K. Gong, J. Chen, H. Deng, K. Weng, H. Wu, K. Li, B. Xiao, S. Luo, W. Hao, Preclinical efficacy and involvement of mTOR signaling in the mechanism of Orf virus against nasopharyngeal carcinoma cells, Life Sci. 291 (2022) 120297. https://doi.org/10.1016/j.lfs.2021.120297.

[88]

Y.Y. Wu, T.K. Sun, M.S. Chen, M. Munir, H.J. Liu, Oncolytic viruses-modulated immunogenic cell death, apoptosis and autophagy linking to virotherapy and cancer immune response, Front. Cell. Infect. Microbiol. 13 (2023) 1142172. https://doi.org/10.3389/fcimb.2023.1142172.

[89]

M. Horii, T. Matsushita T, Regulatory B cells and T cell regulation in cancer, J. Mol. Biol. 433 (2021) 166685. https://doi.org/10.1016/j.jmb.2020.10.019.

[90]

A. Tiwari, R. Trivedi, S.Y. Lin, Tumor microenvironment: barrier or opportunity towards effective cancer therapy, J. Biomed. Sci. 29 (2022) 83. https://doi.o rg/10.1186/s12929-022-00866-3.

[91]

M.Z. Jin, W.L. Jin, The updated landscape of tumor microenvironment and drug repurposing, Signal Transduct, Targeted Ther. 5 (2020) 166. https://doi.o rg/10.1038/s41392-020-00280-x.

[92]

M. Nakatake, N. Kuwano, E. Kaitsurumaru, H. Kurosaki, T. Nakamura, Fusogenic oncolytic vaccinia virus enhances systemic antitumor immune response by modulating the tumor microenvironment, Mol. Ther. 29 (2021) 1782-1793. https://doi.org/10.1016/j.ymthe.2020.12.024.

[93]

N.H. Goradel, A.T. Baker, A. Arashkia, N. Ebrahimi, S. Ghorghanlu, B. Negahdari, Oncolytic virotherapy: challenges and solutions, Curr. Probl. Cancer. 45 (2021) 100639. https://doi.org/10.1016/j.currproblcancer.2020.100639.

[94]

Y. Zhang, Y. Li, K. Chen, L. Qian, P. Wang, Oncolytic virotherapy reverses the immunosuppressive tumor microenvironment and its potential in combination with immunotherapy, Cancer Cell Int. 21 (2021) 262. https://doi.org/10.1186/s12935-021-01972-2.

[95]

Y. Zhang, Y. Li, K. Chen, L. Qian, P. Wang P, Oncolytic virotherapy against the tumor microenvironment and its potential in pancreatic cancer, J. Cancer Res. Therapeut. 18 (2022) 1247-1255, https://doi.org/10.4103/jcrt.jcrt_91_21.

[96]

Y. Liu, J. Cai, W. Liu, Y. Lin, L. Guo, X. Liu, Z. Qin, C. Xu, Y. Zhang, X. Su, K. Deng, G. Yan, J. Liang, Intravenous injection of the oncolytic virus M1 awakens antitumor T cells and overcomes resistance to checkpoint blockade, Cell Death Dis. 11 (2020) 1062. https://doi.org/10.1038/s41419-020-03285-0.

[97]

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. 535 (2022) 215661. https://doi.org/10.1016/j.canlet.2022.215661.

[98]

L. Wang, D.L. Chard, Z. Cheng, Y. Wang, Remodeling the tumor microenvironment by oncolytic viruses: beyond oncolysis of tumor cells for cancer treatment, J Immunother Cancer. 10 (2022) e004167. https://doi.org/10.1136/jitc-2021-004167.

[99]

H.J. Chon, W.S. Lee, H. Yang, S.J. Kong, N.K. Lee, E.S. Moon, J. Choi, E.C. Han, J.H. Kim, J.B. Ahn, J.H. Kim, C. Kim, Tumor microenvironment remodeling by intratumoral oncolytic vaccinia virus enhances the efficacy of immune-checkpoint blockade, Clin. Cancer Res. 25 (2019) 1612-1623. https://doi.org/10.1158/1078-0432.CCR-18-1932.

[100]

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. 8 (2020) 632-647. https://doi.org/10.1158/2326-6066.CIR-19-0628.

[101]

J. Ahmed, L.S. Chard, M. Yuan, J. Wang, A. Howells, Y. Li, H. Li, Z. Zhang, S. Lu, D. Gao, P. Wang, Y. Chu, C. Al Yaghchi, J. Schwartz, G. Alusi, N. Lemoine, Y. Wang, A new oncolytic Vacciniavirus augments antitumor immune responses to prevent tumor recurrence and metastasis after surgery, J Immunother Cancer. 8 (2020) e000415. https://doi.org/10.1136/jitc-2019-000415.

[102]

S. Spranger, D. Dai, B. Horton, T.F. Gajewski, Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy, Cancer Cell. 31 (2017) 711-723.e4. https://doi.org/10.1016/j.ccell.2017.04.003.

[103]

P.K. Bommareddy, M. Shettigar, H.L. Kaufman, Integrating oncolytic viruses in combination cancer immunotherapy, Nat. Rev. Immunol. 18 (2018) 498-513. https://doi.org/10.1038/s41577-018-0014-6.

[104]

S. Zhang, Q. Xu, J. Yang, Q. Li, Y. Sun, X. Li, Y. Wang, X. Niu, X. Qu, J. Chen, E. Zhang, [Expression of NDV HN protein in rice and development of a semiquantitative rapid method for detection of antibodies], Sheng Wu Gong Cheng Xue Bao/Chin, J. Biotechnol. 38 (2022) 1981-1993. https://doi.org/10.13345/j.cjb.210629.

[105]

D.M. Sutherland, P. Aravamudhan, T.S. Dermody, An orchestra of reovirus receptors: still searching for the conductor, Adv. Virus Res. 100 (2018) 223-246. https://doi.org/10.1016/bs.aivir.2017.10.005.

[106]

S.M. Weis, D.A. Cheresh, Tumor angiogenesis: molecular pathways and therapeutic targets, Nat. Med. 17 (2011) 1359-1370. https://doi.org/10.1038/nm.2537.

[107]

Q. Zhang, S. Lu, T. Li, L. Yu, Y. Zhang, H. Zeng, X. Qian, J. Bi, Y. Lin, ACE 2 inhibits breast cancer angiogenesis via suppressing the VEGFa/VEGFR2/ERK pathway, J. Exp. Clin. Cancer Res. 38 (2019) 173. https://doi.org/10.1186/s13046-019-1156-5.

[108]

J. Tu, H. Liang, C. Li, Y. Huang, Z. Wang, X. Chen, X. Yuan, The application and research progress of anti-angiogenesis therapy in tumor immunotherapy, Front. Immunol. 14 (2023) 1198972. https://doi.org/10.3389/fimmu.2023.1198972.

[109]

Y. Tian, D. Xie, L. Yang, Engineering strategies to enhance oncolytic viruses in cancer immunotherapy, Signal Transduct. Targeted Ther. 7 (2022) 117. https://doi.org/10.1038/s41392-022-00951-x.

[110]

Y. Bykov, D. Zamarin, Virus, vessel, victory: a novel approach to tumor killing, Clin. Cancer Res. 25 (2019) 1446-1448. https://doi.org/10.1158/1078-0432.CCR-18-3441.

[111]

C.J. Breitbach, N.S. De Silva, T.J. Falls, U. Aladl, L. Evgin, J. Paterson, Y.Y. Sun, D.G. Roy, J.L. Rintoul, M. Daneshmand, K. Parato, M.M. Stanford, B.D. Lichty, A. Fenster, D. Kirn, H. Atkins, J.C. Bell, Targeting tumor vasculature with an oncolytic virus, Mol. Ther. 19 (2011) 886-894. https://doi.org/10.1038/mt.2011.26.

[112]

Z. Raykov, L. Savelyeva, G. Balboni, T. Giese, J. Rommelaere, N.A. Giese, B 1 lymphocytes and myeloid dendritic cells in lymphoid organs are preferential extratumoral sites of parvovirus minute virus of mice prototype strain expression, J. Virol. 79 (2005) 3517-3524. https://doi.org/10.1128/jvi.79.6.3517-3524.2005.

[113]

H. Tazawa, J. Hasei, S. Yano, S. Kagawa, T. Ozaki, T. Fujiwara, Bone and softtissue sarcoma: a new target for telomerase-specific oncolytic virotherapy, Cancers. 12 (2020) 478. https://doi.org/10.3390/cancers12020478.

[114]

V.M. Srinivasan, J. Gumin, K.M. Camstra, D.E. Collins, M.M. Chen, E.J. Shpall, B.C. Parker Kerrigan, J.N. Johnson, S.R. Chen, J. Fueyo, C. Gomez-Manzano, F.F. Lang, P. Kan, Endovascular selective intra-arterial infusion of mesenchymal stem cells loaded with delta-24 in a canine model, Neurosurgery (Baltim.). 88 (2020) E102-E113. https://doi.org/10.1093/neuros/nyaa470.

[115]

A.U. Ahmed, B. Thaci, N.G. Alexiades, Y. Han, S. Qian, F. Liu, I.V. Balyasnikova, I.Y. Ulasov, K.S. Aboody, M.S. Lesniak, Neural stem cell-based cell carriers enhance therapeutic efficacy of an oncolytic adenovirus in an orthotopic mouse model of human glioblastoma, Mol. Ther. 19 (2011) 1714-1726. https://doi.org/10.1038/mt.2011.100.

[116]

A.U. Ahmed, M.A. Tyler, B. Thaci, N.G. Alexiades, Y. Han, I.V. Ulasov, M.S. Lesniak, A comparative study of neural and mesenchymal stem cell-based carriers for oncolytic adenovirus in a model of malignant glioma, Mol. Pharm. 8 (2011) 1559-1572. https://doi.org/10.1021/mp200161f.

[117]

N.H. Goradel, A.T. Baker, A. Arashkia, N. Ebrahimi, S. Ghorghanlu, B. Negahdari, Oncolytic virotherapy: challenges and solutions. Oncolytic virotherapy: challenges and solutions, Curr. Probl. Cancer. 45 (2021) 100639. https://doi.org/10.1016/j.currproblcancer.2020.100639.

[118]

J. Stockis, R. Roychoudhuri, T. Halim, Regulation of regulatory T cells in cancer, Immunol. 157 (2019) 219-231. https://doi.org/10.1111/imm.13064.

[119]

A.S. Syed Khaja, S.M. Toor, H. El Salhat, B.R. Ali, E. Elkord, Intratumoral FoxP3( þ) Helios(þ) regulatory T cells upregulating immunosuppressive molecules are expanded in human colorectal cancer, Front. Immunol. 8 (2017) 619. https://doi.org/10.3389/fimmu.2017.00619.

[120]

X. Zhu, C. Fan, Z. Xiong, M. Chen, Z. Li, T. Tao, X. Liu, Development and application of oncolytic viruses as the nemesis of tumor cells, Front. Microbiol. 14 (2023) 1188526. https://doi.org/10.3389/fmicb.2023.1188526.

[121]

H. Jiang H, C. Gomez-Manzano, Y. Rivera-Molina, F.F. Lang, C.A. Conrad, J. Fueyo, Oncolytic adenovirus research evolution: from cell-cycle checkpoints to immune checkpoints, Curr Opin Virol. 13 (2015) 33-39. https://doi.org/10.1016/j.coviro.2015.03.009.

[122]

P.A. Netti, D.A. Berk, M.A. Swartz, A.J. Grodzinsky, R.K. Jain, Role of extracellular matrix assembly in interstitial transport in solid tumors, Cancer Res. 60 (2000) 2497-2503.

[123]

M. Xia, G. Meng, A. Jiang, A. Chen, M. Dahlhaus, P. Gonzalez, C. Beltinger, J. Wei, Mitophagy switches cell death from apoptosis to necrosis in NSCLC cells treated with oncolytic measles virus, Oncotarget. 5 (2014) 3907-3918. https://doi.org/10.18632/oncotarget.2028.

[124]

C. Li, G. Meng, L. Su, A. Chen, M. Xia, C. Xu, D. Yu, A. Jiang, J. Wei, Dichloroacetate blocks aerobic glycolytic adaptation to attenuated measles virus and promotes viral replication leading to enhanced oncolysis in glioblastoma, Oncotarget. 6 (2015) 1544-1555. https://doi.org/10.18632/oncotarget.2838.

[125]

V.M. Ngwa, D.N. Edwards, M. Philip, J. Chen, Microenvironmental metabolism regulates antitumor immunity, Cancer Res. 79 (2019) 4003-4008. https://doi.org/10.1158/0008-5472.CAN-19-0617.

[126]

Z. Liu, R. Ravindranathan, P. Kalinski, Z.S. Guo, D.L. Bartlett, Rational combination of oncolytic vaccinia virus and PD-L1 blockade works synergistically to enhance therapeutic efficacy, Nat. Commun. 8 (2017) 14754. https://doi.org/10.1038/ncomms14754.

[127]

S.L. Topalian, G.G. Drake, D.M. Pardoll, Immune checkpoint blockade: a common denominator approach to cancer therapy, Cancer Cell. 27 (2015) 450-461. http://dx.doi.org/10.1016/j.ccell.2015.03.001.

[128]

D.S. Chen, I. Mellman, Elements of cancer immunity and the cancer-immune set point, Nature. 541 (2017) 321-330. https://doi.org/10.1038/nature21349.

[129]

Z. Blake, D.K. Marks, R.D. Gartrell, T. Hart, P. Horton, S.K. Cheng, B. Taback, B.A. Horst, Y.M. Saenger, Complete intracranial response to talimogene laherparepvec (T-Vec), pembrolizumab and whole brain radiotherapy in a patient with melanoma brain metastases refractory to dual checkpoint-inhibition, J Immunother Cancer. 6 (2018) 25. https://doi.org/10.1186/s40425-018-0338-6.

[130]

A. Ribas, R. Dummer, I. Puzanov, A. VanderWalde, R.H.I. Andtbacka, O. Michielin, A.J. Olszanski, J. Malvehy, J. Cebon, E. Fernandez, J.M. Kirkwood, T.F. Gajewski, L. Chen, K.S. Gorski, A.A. Anderson, S.J. Diede, M.E. Lassman, J. Gansert, F.S. Hodi, G.V. Long, Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy, Cell. 170 (2017) 1109-1119.e10. https://doi.org/10.1016/j.cell.2017.08.027.

[131]

A.K. Park, Y. Fong, S.I. Kim, J. Yang, J.P. Murad, L. Lu, B. Jeang, W.C. Chang, N.G. Chen, S.H. Thomas, S.J. Forman, S.J. Priceman,Effective combination immunotherapy using oncolytic viruses to deliver CAR targets to solid tumors, Sci. Transl. Med. 12 (2020) eaaz1863, https://doi.org/10.1126/scitranslmed.aaz1863.

[132]

F.R. Khuri, J. Nemunaitis, I. Ganly, J. Arseneau, I.F. Tannock, L. Romel, M. Gore, J. Ironside, R.H. MacDougall, C. Heise, B. Randlev, A.M. Gillenwater, P. Bruso, S.M. Kaye, W.K. Hong, D.M. Kirn DH, A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5- fluorouracil in patients with recurrent head and neck cancer, Nat. Med. 6 (2000) 879-885. https://doi.org/10.1038/78638.

[133]

C.C. Hwang, M. Igase, M. Sakurai, T. Haraguchi, K. Tani, K. Itamoto, T. Shimokawa, M. Nakaichi, Y. Nemoto, S. Noguchi, M. Coffey, M. Okuda, T. Mizuno, Oncolytic reovirus therapy: pilot study in dogs with spontaneously occurring tumours, Vet. Comp. Oncol. 16 (2018) 229-238. https://doi.org/10.1111/vco.12361.

[134]

D. Mok, K.R. Chan, The effects of pre-existing antibodies on live-attenuated viral vaccines, Viruses. 12 (2020) 520. https://doi.org/10.3390/v12050520.

[135]

S.J. Russell, K.W. Peng, J.C. Bell, Oncolytic virotherapy, Nat. Biotechnol. 30 (2012) 658-670. https://doi.org/10.1038/nbt.2287.

[136]

W. Ban, J. Guan, H. Huang, Z. He, M. Sun, F. Liu, J. Sun, Emerging systemic delivery strategies of oncolytic viruses: a key step toward cancer immunotherapy, Nano Res. 15 (2022) 4137-4153. https://doi.org/10.1007/s12274-021-4031-6.

[137]

N. Mendez, V. Herrera, L. Zhang, F. Hedjran, R. Feuer, S.L. Blair, W.C. Trogler, T.R. Reid, A.C. Kummel, Encapsulation of adenovirus serotype 5 in anionic lecithin liposomes using a bead-based immunoprecipitation technique enhances transfection efficiency, Biomaterials. 35 (2014) 9554-9561. https://doi.org/10.1016/j.biomaterials.2014.08.010.

[138]

L.A. Rojas, G.N. Condezo, R. Moreno, C.A. Fajardo, M. Arias-Badia, C. San Martín, R. Alemany, Albumin-binding adenoviruses circumvent pre-existing neutralizing antibodies upon systemic delivery, J. Contr. Release. 237 (2016) 78-88. https://doi.org/10.1016/j.jconrel.2016.07.004.

[139]

P.A. Ott, F.S. Hodi, Talimogene laherparepvec for the treatment of advanced melanoma, Clin. Cancer Res. 22 (2016) 3127-3131. https://doi.org/10.1158/1078-0432.CCR-15-2709.

[140]

D. Song, X. Jia, X. Liu, L. Hu, K. Lin, T. Xiao, Y. Qiao, J. Zhang, J. Dan, C. Wong, C. Hu, K. Sai, S. Gong, M. Sander, R. Shen, X. Chen, X. Xiao, J. Chen, Y. Zhang, C. Wei, X. Xiao, J. Liang, Q. Zhang, J. Hu, W. Zhu, G. Yan, Y. Lin, J. Cai, Identification of the receptor of oncolytic virus M1 as a therapeutic predictor for multiple solid tumors, Signal Transduct. Targeted Ther. 7 (2022) 100. https://doi.org/10.1038/s41392-022-00921-3.

AI Summary AI Mindmap
PDF (1340KB)

591

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/