Perspectives for applying Alphaviruses in antitumor therapy

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Oncolytic viral therapy is a promising approach for treating tumors. Oncolytic viruses can directly lyse tumor cells and indirectly activate antitumor immunity. Alphaviruses, as oncolytic viruses, are particularly promising agents because they can selectively infect and lyse tumor cells, modulate microtumor environment, elicit immune-mediated lysis of tumor cells, and serve as a platform for transgene delivery. To ensure safety, attenuated strains of Alphaviruses are typically used for genetic engineering, and immunogenic tumor-associated antigens or cytokines are commonly chosen as transgenes. Studies evaluating both in vitro and in vivo oncolytic and immunomodulatory effects of Alphaviruses and vectors based on them have been growing exponentially. Animal models of various tumor types were used to examine the effectiveness of Alphaviruses, including Sindbis, Semliki Forest virus, Geta (strain M1), Venezuelan equine encephalitis virus, and vectors based on them. Additionally, Alphaviruses revealed enhanced antitumor activity while used in combination therapies with other oncolytic viruses. Alphavirus-like replicon particles based on attenuated Venezuelan equine encephalitis virus may serve for transgene delivery to express heterologous proteins at high levels, and induce both humoral and cellular immune responses. An alphaviral vector-based vaccine, encoding the HER2 extracellular and transmembrane domains, has demonstrated safety and efficacy in preclinical mouse models, as well as in phase I clinical trials for advanced breast cancer patients with HER2 overexpression. This vaccine is known to be safe, effective, and capable of inducing T-cell immunity. In this review, we discuss the current progress in preclinical and clinical investigations, as well as the future potential of Alphaviruses for oncolytic virotherapy.

作者简介

Alina Nazarenko

M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute)

编辑信件的主要联系方式.
Email: nazarenko_as@chumakovs.su
SPIN 代码: 8733-3345

Researcher, Laboratory of Tick-Borne Encephalitis and Other Viral Encephalitides

俄罗斯联邦, 108819, Moscow, Settlement “Moskovskiy”, Village of Institute of Poliomyelitis, Premises 8, build. 1

Yulia Biryukova

M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute)

Email: biriukova-ula@mail.ru
ORCID iD: 0000-0002-5804-4001
SPIN 代码: 7940-9531
Scopus 作者 ID: 36028326200
Researcher ID: D-8577-2014

PhD (Biology), Senior Researcher, Laboratory of Tick-Borne Encephalitis and Other Viral Encephalitides, Chumakov Federal Scientific Center for Research and Development

俄罗斯联邦, 108819, Moscow, Settlement “Moskovskiy”, Village of Institute of Poliomyelitis, Premises 8, build. 1

Nadezhda Kolyasnikova

M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute)

Email: kolyasnikova_nm@chumakovs.su

PhD (Medicine), Leading Researcher, Head of Laboratory of Tick-Borne Encephalitis and Other Viral Encephalitides

俄罗斯联邦, 108819, Moscow, Settlement “Moskovskiy”, Village of Institute of Poliomyelitis, Premises 8, build. 1

Mikhail Vorovich

M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute); Institute of Translational Medicine and Biotechnology, I.M. Sechenov First Moscow State Medical University of the Ministry of Health of Russian Federation (Sechenov University)

Email: vorovich_mf@chumakovs.su

PhD (Biology), Leading Researcher, Laboratory of Tick-Borne Encephalitis and Other Viral Encephalitides, Chumakov Federal Scientific Center for Research and Development, Associate Professor, Department of Organization and Research of Immunobiological Technologies

俄罗斯联邦, 108819, Moscow, Settlement “Moskovskiy”, Village of Institute of Poliomyelitis, Premises 8, build. 1; 119991, Moscow, st Trubetskaya 8/2

Nikolai Pestov

M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute)

Email: pestov_nb@chumakovs.su

PhD (Chemistry), Leading Researcher, Laboratory of Tick-Borne Encephalitis and Other Viral Encephalitides

俄罗斯联邦, 108819, Moscow, Settlement “Moskovskiy”, Village of Institute of Poliomyelitis, Premises 8, build. 1

Aidar Ishmukhametov

M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute); Institute of Translational Medicine and Biotechnology, I.M. Sechenov First Moscow State Medical University of the Ministry of Health of Russian Federation (Sechenov University)

Email: ishmukhametov@chumakovs.su
SPIN 代码: 2971-8228
Scopus 作者 ID: 57195034442

RAS Full Member, DSc (Medicine), Professor, General Director, Head of the Department of Organization and Research of Immunobiological Technologies

 

俄罗斯联邦, 108819, Moscow, Settlement “Moskovskiy”, Village of Institute of Poliomyelitis, Premises 8, build. 1; 119991, Moscow, st Trubetskaya 8/2

参考

  1. Alberts P., Tilgase A., Rasa A., Bandere K., Venskus D. The advent of oncolytic virotherapy in oncology: The Rigvir® story. Eur. J. Pharmacol., 2018, vol. 837, pp. 117–126. doi: 10.1016/j.ejphar.2018.08.042
  2. Al-Saleh W., Delvenne P., Brule F.A., Menard S., Boniver J., Castronovo V. Expression of the 67 KD laminin receptor in human cervical preneoplastic and neoplastic squamous epithelial lesions: an immunohistochemical study. J. Pathol. Clin. Res., 1997, vol. 181, pp. 287–293. doi: 10.1002/(SICI)1096-9896(199703)181:3<287::AID-PATH762>3.0.CO;2-W
  3. Bradish C.J., Allner K., Maber H.B. The virulence of original and derived strains of Semliki Forest virus for mice, guinea-pigs and rabbits. J. Gen. Virol., 1971, vol. 12, pp. 141–160. doi: 10.1099/0022-1317-12-2-141
  4. Cassetti M.C., McElhiney S.P., Shahabi V., Pullen J.K., Le Poole I.C., Eiben G.L., Smith L.R., Kast W.M. Antitumor efficacy of Venezuelan equine encephalitis virus replicon particles encoding mutated HPV16 E6 and E7 genes. Vaccine, 2004, vol. 22, pp. 520–527. doi: 10.1016/j.vaccine.2003.07.003
  5. Crosby E.J., Gwin W., Blackwell K., Marcom P.K., Chang S., Maecker H.T., Broadwater G., Hyslop T., Kim S., Rogatko A., Lubkov V., Snyder J.C., Osada T., Hobeika A.C., Morse M.A., Lyerly H.K., Hartman Z.C. Vaccine-induced memory CD8+ T cells provide clinical benefit in HER2 expressing breast cancer: a mouse to human translational study. Clin. Cancer Res., 2019, vol. 25, pp. 2725–2736. doi: 10.1158/1078-0432.CCR-18-3102
  6. Frampton J.E. Teserpaturev/G47Δ: first approval. BioDrugs, 2022, vol. 36, pp. 667–672. doi: 10.1007/s40259-022-00553-7
  7. Fukunaga Y., Kumanomido T., Kamada M. Getah virus as an equine pathogen. Vet. Clin. North Am. Equine Pract., 2000, vol. 16, pp. 605–617. doi: 10.1016/s0749-0739(17)30099-8
  8. Gnjatic S., Nishikawa H., Jungbluth A.A., Güre A.O., Ritter G., Jäger E., Knuth A., Chen Y.-T., Old L.J. NY-ESO-1: review of an immunogenic tumor antigen. Adv. Cancer Res., 2006, vol. 95, pp. 1–30. doi: 10.1016/S0065-230X(06)95001-5
  9. Granot T., Venticinque L., Tseng J.-C., Meruelo D. Activation of cytotoxic and regulatory functions of NK cells by Sindbis viral vectors. PLoS One, 2011, vol. 6: e20598. doi: 10.1371/journal.pone.0020598
  10. Granot T., Yamanashi Y., Meruelo D. Sindbis viral vectors transiently deliver tumor-associated antigens to lymph nodes and elicit diversified antitumor CD8+ T-cell immunity. Mol. Ther., 2014, vol. 22, pp. 112–122. doi: 10.1038/mt.2013.215
  11. Hasanzadeh M., Shadjou N., Lin Y., de la Guardia M. Nanomaterials for use in immunosensing of carcinoembryonic antigen (CEA): recent advances. Trends Analyt. Chem., 2017, vol. 86, pp. 185–205. doi: 10.1016/j.trac.2016.11.003
  12. Heikkilä J.E., Vähä-Koskela M.J.V., Ruotsalainen J.J., Martikainen M.W., Stanford M.M., McCart J.A., Bell J.C., Hinkkanen A.E. Intravenously administered Alphavirus vector VA7 eradicates orthotopic human glioma xenografts in nude mice. PLoS One, 2010, vol. 5: e8603. doi: 10.1371/journal.pone.0008603
  13. Hu J., Cai X.F., Yan G. Alphavirus M1 induces apoptosis of malignant glioma cells via downregulation and nucleolar translocation of p21WAF1/CIP1 protein. Cell Cycle, 2009, vol. 8, pp. 3328–3339. doi: 10.4161/cc.8.20.9832
  14. Huang P.Y., Guo J.H., Hwang L.H. Oncolytic Sindbis virus targets tumors defective in the interferon response and induces significant bystander antitumor immunity in vivo. Mol. Ther., 2012, vol. 20, pp. 298–305. doi: 10.1038/mt.2011.245
  15. Kaufman H.L., Kohlhapp F.J., Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov., 2015, vol. 14, pp. 642–662. doi: 10.1038/nrd4663
  16. Kaufman H.L., Shalhout S.Z., Iodice G. Talimogene laherparepvec: moving from first-in-class to best-in-class. Front. Mol. Biosci., 2022, vol. 9: 834841. doi: 10.3389/fmolb.2022.834841
  17. Kelly E., Russell S.J. History of oncolytic viruses: genesis to genetic engineering. Mol. Ther., 2007, vol. 15, pp. 651–659. doi: 10.1038/sj.mt.6300108
  18. Ketola A., Hinkkanen A., Yongabi F., Furu P., Määttä A.M., Liimatainen T., Pirinen R., Björn M., Hakkarainen T., Mäkinen K., Wahlfors J., Pellinen R. Oncolytic Semliki Forest virus vector as a novel candidate against unresectable osteosarcoma. Cancer Res., 2008, vol. 68, pp. 8342–8350. doi: 10.1158/0008-5472.CAN-08-0251
  19. Klimstra W.B., Nangle E.M., Smith M.S., Yurochko A.D., Ryman K.D. DC-SIGN and L-SIGN can act as attachment receptors for Alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J. Virol., 2003, vol. 77, pp. 12022–12032. doi: 10.1128/jvi.77.22.12022-12032.2003
  20. Laine M., Luukkainen R., Toivanen A. Sindbis viruses and other Alphaviruses as cause of human arthritic disease. J. Int. Med., 2004, vol. 256, pp. 457–471. doi: 10.1111/j.1365-2796.2004.01413.x
  21. Leung J.Y.-S., Ng M.M.-L., Chu J.J.-H. Replication of Alphaviruses: a review on the entry process of Alphaviruses into cells. Adv. Virol., 2011, vol. 2011: e249640. doi: 10.1155/2011/249640
  22. Liang M. Oncorine, the world first oncolytic virus medicine and its update in China. Curr. Cancer Drug Targets, 2018, vol. 18, pp. 171–176. doi: 10.2174/1568009618666171129221503
  23. Lin Y., Zhang H., Liang J., Li K., Zhu W., Fu L., Wang F., Zheng X., Shi H., Wu S., Xiao X., Chen L., Tang L., Yan M., Yang X., Tan Y., Qiu P., Huang Y., Yin W., Su X., Hu H., Hu J., Yan G. Identification and characterization of Alphavirus M1 as a selective oncolytic virus targeting ZAP-defective human cancers. Proc. Natl Acad. Sci. USA, 2014, vol. 111, pp. e4504–e4512. doi: 10.1073/pnas.1408759111
  24. Määttä A.-M., Liimatainen T., Wahlfors T., Wirth T., Vähä-Koskela M., Jansson L., Valonen P., Häkkinen K., Rautsi O., Pellinen R., Mäkinen K., Hakumäki J., Hinkkanen A., Wahlfors J. Evaluation of cancer virotherapy with attenuated replicative Semliki Forest virus in different rodent tumor models. Int. J. Cancer, 2007, vol. 121, pp. 863–870. doi: 10.1002/ijc.22758
  25. Määttä A.-M., Mäkinen K., Ketola A., Liimatainen T., Yongabi F.N., Vähä-Koskela M., Pirinen R., Rautsi O., Pellinen R., Hinkkanen A., Wahlfors J. Replication competent Semliki Forest virus prolongs survival in experimental lung cancer. Int. J. Cancer, 2008, vol. 123, pp. 1704–1711. doi: 10.1002/ijc.23646
  26. Malfitano A.M., Di Somma S., Iannuzzi C.A., Pentimalli F., Portella G. Virotherapy: from single agents to combinatorial treatments. Biochem. Pharmacol., 2020, vol. 177: e113986. doi: 10.1016/j.bcp.2020.113986
  27. Markoff L. Alphaviruses (Chikungunya, Eastern Equine Encephalitis). In: Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases. Elsevier, Inc., 2020. Chapter 151: 1997-2006.e4
  28. Martikainen M., Niittykoski M., von und zu Fraunberg M., Immonen A., Koponen S., van Geenen M., Vähä-Koskela M., Ylösmäki E., Jääskeläinen J.E., Saksela K., Hinkkanen A. MicroRNA-attenuated clone of virulent Semliki Forest virus overcomes antiviral type I interferon in resistant mouse CT-2A glioma. J. Virol., 2015, vol. 89, pp. 10637–10647. doi: 10.1128/JVI.01868-15
  29. Martikainen M., Ramachandran M., Lugano R., Ma J., Martikainen M.-M., Dimberg A., Yu D., Merits A., Essand M. IFN-I-tolerant oncolytic Semliki Forest virus in combination with anti-PD1 enhances T cell response against mouse glioma. Mol. Ther. Oncolytics, 2021, vol. 21, pp. 37–46. doi: 10.1016/j.omto.2021.03.008
  30. Martikainen M., Ruotsalainen J., Tuomela J., Härkönen P., Essand M., Heikkilä J., Hinkkanen A. Oncolytic Alphavirus SFV-VA7 efficiently eradicates subcutaneous and orthotopic human prostate tumours in mice. Br. J. Cancer, 2017, vol. 117, pp. 51–55. doi: 10.1038/bjc.2017.151
  31. Morse M.A., Hobeika A., Gwin W., Osada T., Gelles J., Rushing C., Niedzwiecki D., Lyerly H.K. Phase I study of alphaviral vector (AVX701) in colorectal cancer patients: comparison of immune responses in stage III and stage IV patients. J. Immunother. Cancer, 2015, vol. 3: 444. doi: 10.1186/2051-1426-3-S2-P444
  32. Osada T., Berglund P., Morse M.A., Hubby B., Lewis W., Niedzwiecki D., Yang X.Y., Hobeika A., Burnett B., Devi G.R., Clay T.M., Smith J., Kim Lyerly H. Co-delivery of antigen and IL-12 by Venezuelan equine encephalitis virus replicon particles enhances antigen-specific immune responses and antitumor effects. Cancer Immunol. Immunother., 2012, vol. 61, pp. 1941–1951. doi: 10.1007/s00262-012-1248-y
  33. Quetglas J.I., Fioravanti J., Ardaiz N., Medina-Echeverz J., Baraibar I., Prieto J., Smerdou C., Berraondo P. A Semliki Forest virus vector engineered to express IFNα induces efficient elimination of established tumors. Gene Ther., 2012, vol. 19, pp. 271–278. doi: 10.1038/gt.2011.99
  34. Ramsey J., Mukhopadhyay S. Disentangling the frames, the state of research on the Alphavirus 6K and TF proteins. Viruses, 2017, vol. 9: 228. doi: 10.3390/v9080228
  35. Roche F.P., Sheahan B.J., O’Mara S.M., Atkins G.J. Semliki Forest virus-mediated gene therapy of the RG2 rat glioma. Neuropathol. Appl. Neurobiol., 2010, vol. 36, pp. 648–660. doi: 10.1111/j.1365-2990.2010.01110.x
  36. Rodriguez-Madoz J.R., Liu K.H., Quetglas J.I., Ruiz-Guillen M., Otano I., Crettaz J., Butler S.D., Bellezza C.A., Dykes N.L., Tennant B.C., Prieto J., González-Aseguinolaza G., Smerdou C., Menne S. Semliki Forest virus expressing interleukin-12 induces antiviral and antitumoral responses in woodchucks with chronic viral hepatitis and hepatocellular carcinoma. J. Virol., 2009, vol. 83, pp. 12266–12278. doi: 10.1128/JVI.01597-09
  37. Samuel C.E. Antiviral actions of interferons. Clin. Microbiol. Rev., 2001, vol. 14, pp. 778–809. doi: 10.1128/CMR.14.4.778-809.2001
  38. Scherwitzl I., Hurtado A., Pierce C.M., Vogt S., Pampeno C., Meruelo D. Systemically administered sindbis virus in combination with immune checkpoint blockade induces curative anti-tumor immunity. Mol. Ther. Oncolytics., 2018, vol. 9, pp. 51–63. doi: 10.1016/j.omto.2018.04.004
  39. Scherwitzl I., Opp S., Hurtado A.M., Pampeno C., Loomis C., Kannan K., Yu M., Meruelo D. Sindbis virus with anti-OX40 overcomes the immunosuppressive tumor microenvironment of low-immunogenic tumors. Mol. Ther. Oncolytics., 2020, vol. 17, pp. 431–447. doi: 10.1016/j.omto.2020.04.012
  40. Skidmore A.M., Bradfute S.B. The life cycle of the Alphaviruses: from an antiviral perspective. Antiviral Res., 2023, vol. 209: e105476. doi: 10.1016/j.antiviral.2022.105476
  41. Smit J.M., Waarts B.-L., Kimata K., Klimstra W.B., Bittman R., Wilschut J. Adaptation of Alphaviruses to heparan sulfate: interaction of Sindbis and Semliki Forest viruses with liposomes containing lipid-conjugated heparin. J. Virol., 2002, vol. 76, pp. 10128–10137. doi: 10.1128/jvi.76.20.10128-10137.2002
  42. Strauss J.H., Strauss E.G. The Alphaviruses: gene expression, replication, and evolution. Microbiol. Rev., 1994, vol. 58, pp. 491–562. doi: 10.1128/mr.58.3.491-562.1994
  43. Strauss J.H., Strauss E.G. Virus evolution: how does an enveloped virus make a regular structure? Cell, 2001, vol. 105, pp. 5–8. doi: 10.1016/s0092-8674(01)00291-4
  44. Sun S., Liu Y., He C., Hu W., Liu W., Huang X., Wu J., Xie F., Chen C., Wang J., Lin Y., Zhu W., Yan G., Cai J., Li S. Combining NanoKnife with M1 oncolytic virus enhances anticancer activity in pancreatic cancer. Cancer Lett., 2021, vol. 502, pp. 9–24. doi: 10.1016/j.canlet.2020.12.018
  45. Suomalainen M., Liljeström P., Garoff H. Spike protein-nucleocapsid interactions drive the budding of Alphaviruses. J. Virol., 1992, vol. 66, pp. 4737–4747. doi: 10.1128/JVI.66.8.4737-4747.1992
  46. Takenouchi A., Saito K., Saito E., Saito T., Hishiki T., Matsunaga T., Isegawa N., Yoshida H., Ohnuma N., Shirasawa H. Oncolytic viral therapy for neuroblastoma cells with Sindbis virus AR339 strain. Pediatr. Surg. Int., 2015, vol. 31, pp. 1151–1159. doi: 10.1007/s00383-015-3784-y
  47. Tian Y., Xie D., Yang L. Engineering strategies to enhance oncolytic viruses in cancer immunotherapy. Signal Transduct. Target Ther., 2022, vol. 7: 117. doi: 10.1038/s41392-022-00951-x
  48. Tseng J.-C., Hurtado A., Yee H., Levin B., Boivin C., Benet M., Blank S.V., Pellicer A., Meruelo D. Using sindbis viral vectors for specific detection and suppression of advanced ovarian cancer in animal models. Cancer Res., 2004, vol. 64, pp. 6684–6692. doi: 10.1158/0008-5472.CAN-04-1924
  49. Tseng J.-C., Levin B., Hirano T., Yee H., Pampeno C., Meruelo D. In vivo antitumor activity of sindbis viral vectors. J. Natl Cancer Inst., 2002, vol. 94, pp. 1790–1802. doi: 10.1093/jnci/94.23.1790
  50. Tseng J.-C., Levin B., Hurtado A., Yee H., de Castro I.P., Jimenez M., Shamamian P., Jin R., Novick R.P., Pellicer A., Meruelo D. Systemic tumor targeting and killing by Sindbis viral vectors. Nat. Biotechnol., 2004, vol. 22, pp. 70–77. doi: 10.1038/nbt917
  51. Unno Y., Shino Y., Kondo F., Igarashi N., Wang G., Shimura R., Yamaguchi T., Asano T., Saisho H., Sekiya S., Shirasawa H. Oncolytic viral therapy for cervical and ovarian cancer cells by Sindbis virus AR339 strain. Clin. Cancer Res., 2005, vol. 11, pp. 4553–4560. doi: 10.1158/1078-0432.CCR-04-2610
  52. Vähä-Koskela M.J.V., Kallio J.P., Jansson L.C., Heikkilä J.E., Zakhartchenko V.A., Kallajoki M.A. Kähäri V.-M., Hinkkanen A.E. Oncolytic capacity of attenuated replicative semliki forest virus in human melanoma xenografts in severe combined immunodeficient mice. Cancer Res., 2006, vol. 66, pp. 7185–7194. doi: 10.1158/0008-5472.CAN-05-2214
  53. Vähä-Koskela M.J.V., Le Boeuf F., Lemay C., De Silva N., Diallo J.-S., Cox J., Becker M., Choi Y., Ananth A., Sellers C., Breton S., Roy D., Falls T., Brun J., Hemminki A., Hinkkanen A., Bell J.C. Resistance to two heterologous neurotropic oncolytic viruses, Semliki Forest virus and vaccinia virus, in experimental glioma. J. Virol., 2013, vol. 87, pp. 2363–2366. doi: 10.1128/JVI.01609-12
  54. Van den Brûle F.A., Castronovo V., Ménard S., Giavazzi R., Marzola M., Belotti D., Taraboletti G. Expression of the 67 kD laminin receptor in human ovarian carcinomas as defined by a monoclonal antibody, MLuC5. Eur. J. Cancer, 1996, vol. 32, no. 9, pp. 1598–1602. doi: 10.1016/0959-8049(96)00119-0
  55. Wang K.S., Kuhn R.J., Strauss E.G., Ou S., Strauss J.H. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J. Virol., 1992, vol. 66, pp. 4992–5001. doi: 10.1128/JVI.66.8.4992-5001.1992
  56. Wen J.-S., Zhao W.-Z., Liu J.-W., Zhou H., Tao J.-P., Yan H.-J., Liang Y., Zhou J.-J., Jiang L.-F. Genomic analysis of a Chinese isolate of Getah-like virus and its phylogenetic relationship with other Alphaviruses. Virus Genes, 2007, vol. 35, pp. 597–603. doi: 10.1007/s11262-007-0110-3
  57. Wollmann G., Tattersall P., van den Pol A.N. Targeting human glioblastoma cells: comparison of nine viruses with oncolytic potential. J. Virol., 2005, vol. 79, pp. 6005–6022. doi: 10.1128/JVI.79.10.6005-6022.2005
  58. Yu M., Scherwitzl I., Opp S., Tsirigos A., Meruelo D. Molecular and metabolic pathways mediating curative treatment of a non-Hodgkin B cell lymphoma by Sindbis viral vectors and anti-4-1BB monoclonal antibody. J. Immunother. Cancer, 2019, vol. 7, no. 1: 185. doi: 10.1186/s40425-019-0664-3
  59. Zhang H., Lin Y., Li K., Liang J., Xiao X., Cai J., Tan Y., Xing F., Mai J., Li Y., Chen W., Sheng L., Gu J., Zhu W., Yin W., Qiu P., Su X., Lu B., Tian X., Liu J., Lu W., Dou Y., Huang Y., Hu B., Kang Z., Gao G., Mao Z., Cheng S.-Y., Lu L., Bai X.-T., Gong S., Yan G., Hu J. Naturally existing oncolytic virus M1 is nonpathogenic for the nonhuman primates after multiple rounds of repeated intravenous injections. Human Gene Ther., 2016, vol. 27, no. 9, pp. 700–711. doi: 10.1089/hum.2016.038
  60. Zhang J., Liu Y., Tan J., Zhang Y., Wong C.-W., Lin Z., Liu X., Sander M., Yang X., Liang L., Song D., Dan J., Zhou Y., Cai J., Lin Y., Liang J., Hu J., Yan G., Zhu W. Necroptotic virotherapy of oncolytic Alphavirus M1 cooperated with Doxorubicin displays promising therapeutic efficacy in TNBC. Oncogene, 2021, vol. 40, no. 29, pp. 4783–4795. doi: 10.1038/s41388-021-01869-4
  61. Zhang S., Rabkin S.D. The discovery and development of oncolytic viruses: are they the future of cancer immunotherapy? Expert Opin. Drug Discov., 2021, vol. 16, no. 4, pp. 391–410. doi: 10.1080/17460441.2021.1850689
  62. Zhang Y.-Q., Tsai Y.-C., Monie A., Wu T.-C., Hung C.-F. Enhancing the therapeutic effect against ovarian cancer through a combination of viral oncolysis and antigen-specific immunotherapy. Mol. Ther., 2010, vol. 18, pp. 692–699. doi: 10.1038/mt.2009.318
  63. Zhao H., Garoff H. Role of cell surface spikes in Alphavirus budding. J. Virol., 1992, vol. 66, pp. 7089–7095. doi: 10.1128/JVI.66.12.7089-7095.1992
  64. Zimmerman O., Holmes A.C., Kafai N.M., Adams L.J., Diamond M.S. Entry receptors — the gateway to Alphavirus infection. J. Clin. Invest., 2023, vol. 133, no. 2: e165307. doi: 10.1172/JCI165307

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Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

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2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».