Oncolytic viruses and cancer treatment

Czech version

Authors: H. Španielová ^1,2; R. Brdička ³
Authors‘ workplace: Ústav organické chemie a bio chemie AV ČR, Praha ¹; Katedra genetiky a mikrobio logie, Přírodovědecká fakulta, UK, Praha ²; Biogen Praha, s. r. o. ³
Published in: Klin Onkol 2023; 36(1): 12-27
Category: Review
doi: https://doi.org/10.48095/ccko202312

Overview

Background: The fundamental difference between tumor and normal tissue growth is the emergence of the microenvironment with diminished or extinguished immunogenicity. One of the main functions of oncolytic viruses is the formation of such a microenvironment, which leads to a revival of immunological processes and loss of viability of cancer cells. Oncolytic viruses are being continuously improved and should be considered as a possible adjuvant immunomodulatory cancer treatment. A key requirement for the success of this cancer therapy is the specificity of the oncolytic viruses, which replicate only in tumor cells but do not affect normal cells. In this review, optimization strategies to achieve cancer specificity with increased efficacy are discussed and the most interesting results from preclinical and clinical trials are presented. Purpose: This review provides information on the current status of the development and use of oncolytic viruses as part of the biological treatment of cancer.

Keywords:

immunotherapy – neoplasms – molecular targeted therapy – tumor microenvironment – oncolytic virotherapy

Sources

1. Quaresma M, Coleman MP, Rachet B. 40-year trends in an index of survival for all cancers combined and survival adjusted for age and sex for each cancer in England and Wales, 1971–2011: a population-based study. Lancet 2015; 385 (9974): 1206–1218. doi: 10.1016/S0140-6736 (14) 61396-9.

2. De Angelis R, Sant M, Coleman MP et al. Cancer survival in Europe 1999–2007 by country and age: results of EUROCARE-5 – a population-based study. Lancet Oncol 2014; 15 (1): 23–34. doi: 10.1016/S1470-2045 (13) 70546-1.

3. Španielová H. Viry, které uzdravují. Vesmír 2010; 89 (3): 181–183.

4. Mozaffari Nejad AS, Noor T, Munim ZH et al. A bibliometric review of oncolytic virus research as a novel approach for cancer therapy. Virol J 2021; 18 (1): 98. doi: 10.1186/s12985-021-01571-7.

5. Kuryk L, Vassilev L, Ranki T et al. Toxicological and bio-distribution profile of a GM-CSF-expressing, double-targeted, chimeric oncolytic adenovirus ONCOS-102 – support for clinical studies on advanced cancer treatment. PloS One 2017; 12 (8): e0182715. doi: 10.1371/journal.pone.0182715.

6. Santry LA, van Vloten JP, Knapp JP et al. Tumour vasculature: friend or foe of oncolytic viruses? Cytokine Growth Factor Rev 2020; 56: 69–82. doi: 10.1016/j.cytogfr.2020.07.007.

7. Rahman MM, McFadden G. Oncolytic viruses: newest frontier for cancer immunotherapy. Cancers 2021; 13 (21): 5452. doi: 10.3390/cancers13215452.

8. Humeau J, Le Naour J, Galluzzi L et al. Trial watch: intratumoral immunotherapy. Oncoimmunology 2021; 10 (1): 1984677. doi: 10.1080/2162402X.2021.1984677.

9. Roy DG, Geoffroy K, Marguerie M et al. Adjuvant oncolytic virotherapy for personalized anti-cancer vaccination. Nat Commun 2021; 12 (1): 2626. doi: 10.1038/s41467-021-22929-z.

10. Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov 2015; 14 (9): 642–662. doi: 10.1038/nrd4663.

11. Elvington M, Liszewski MK, Atkinson JP. CD46 and oncologic interactions: friendly fire against cancer. Antibodies 2020; 9 (4): 59. doi: 10.3390/antib9040059.

12. Fernandes J. Oncogenes: the passport for viral oncolysis through PKR inhibition. Biomark Cancer 2016; 8: 101–110. doi: 10.4137/BIC.S33378.

13. Jhawar SR, Thandoni A, Bommareddy PK et al. Oncolytic viruses – natural and genetically engineered cancer immunotherapies. Front Oncol 2017; 7: 202. doi: 10.3389/fonc.2017.00202.

14. Verheije MH, Rottier PJM. Retargeting of viruses to generate oncolytic agents. Adv Virol 2012; 2012: 798526. doi: 10.1155/2012/798526.

15. O’Shea C, Miyake-Stoner SJ, Powers CJ et al. Highly selective and potent p16-CDK-RB-E2F targeted oncolytic virus therapies. J Clin Oncol 2021; 39 (Suppl 15): e14543–e14543. doi: 10.1200/JCO.2021.39.15_suppl.e14543.

16. Pascual-Pasto G, Bazan-Peregrino M, Olaciregui NG et al. Therapeutic targeting of the RB1 pathway in retinoblastoma with the oncolytic adenovirus VCN-01. Sci Transl Med 2019; 11 (476): eaat9321. doi: 10.1126/scitranslmed.aat9321.

17. Kawashima T, Kagawa S, Kobayashi N et al. Telomerase-specific replication-selective virotherapy for human cancer. Clin Cancer Res 2004; 10 (1): 285–292. doi: 10.1158/1078-0432.CCR-1075-3.

18. Chaurasiya S, Fong Y, Warner SG. Optimizing oncolytic viral design to enhance antitumor efficacy: progress and challenges. Cancers 2020; 12 (6): 1699. doi: 10.3390/cancers12061699.

19. Pol JG, Workenhe ST, Konda P et al. Cytokines in oncolytic virotherapy. Cytokine Growth Factor Rev 2020; 56: 4–27. doi: 10.1016/j.cytogfr.2020.10.007.

20. Heidbuechel JPW, Engeland CE. Oncolytic viruses encoding bispecific T cell engagers: a blueprint for emerging immunovirotherapies. J Hematol Oncol 2021; 14 (1): 63. doi: 10.1186/s13045-021-01075-5.

21. Kontermann RE, Ungerechts G, Nettelbeck DM. Viro-antibody therapy: engineering oncolytic viruses for genetic delivery of diverse antibody-based biotherapeutics. MAbs 2021; 13 (1): 1982447. doi: 10.1080/19420862.2021.1982447.

22. Freedman JD, Duffy MR, Lei-Rossmann J et al. An oncolytic virus expressing a T-cell engager simultaneously targets cancer and immunosuppressive stromal cells. Cancer Res 2018; 78 (24): 6852–6865. doi: 10.1158/0008-5472.CAN-18-1750.

23. Bořilová S, Grell P, Bílek O et al. Biomarkers for predicting response to immunotherapy with immune checkpoint inhibitors. Onkologie 2020; 14 (5): 205–212. doi: 10.36290/xon.2020.075.

24. McGray AJR, Huang R-Y, Battaglia S et al. 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. doi: 10.1186/s40425-019-0641-x.

25. Mihályová J, Jelínek T, Kaščák M et al. Practical aspects of CAR-T cell therapy. Klin Onkol 2022; 35 (1): 44–54. doi: 10.48095/ccko202244.

26. Aalipour A, Le Boeuf F, Tang M et al. Viral delivery of CAR targets to solid tumors enables effective cell therapy. Mol Ther Oncolytics 2020; 17: 232–240. doi: 10.1016/j.omto.2020.03.018.

27. Ferguson MS, Lemoine NR, Wang Y. Systemic delivery of oncolytic viruses: hopes and hurdles. Adv Virol 2012; 2012: e805629. doi: 10.1155/2012/805629.

28. Xu W, Atkinson VG, Menzies AM. Intratumoural immunotherapies in oncology. Eur J Cancer 2020; 127: 1–11. doi: 10.1016/j.ejca.2019.12.007.

29. Koski A, Bramante S, Kipar A et al. Biodistribution analysis of oncolytic adenoviruses in patient autopsy samples reveals vascular transduction of noninjected tumors and tissues. Mol Ther 2015; 23 (10): 1641–1652. doi: 10.1038/mt.2015.125.

30. Dal Corso A, Pignataro L, Belvisi L et al. Innovative linker strategies for tumor-targeted drug conjugates. Chemistry 2019; 25 (65): 14740–14757. doi: 10.1002/chem.201903127.

31. Garofalo M, Bellato F, Magliocca S et al. Polymer coated oncolytic adenovirus to selectively target hepatocellular carcinoma cells. Pharmaceutics 2021; 13 (7): 949. doi: 10.3390/pharmaceutics13070949.

32. Sewald X, Motamedi N, Mothes W. Viruses exploit the tissue physiology of the host to spread in vivo. Curr Opin Cell Biol 2016; 41: 81–90. doi: 10.1016/j.ceb.2016.04.008.

33. Reale A, Calistri A, Altomonte J. Giving oncolytic viruses a free ride: carrier cells for oncolytic virotherapy. Pharmaceutics 2021; 13 (12): 2192. doi: 10.3390/pharmaceutics13122192.

34. Aldrak N, Alsaab S, Algethami A et al. Oncolytic herpes simplex virus-based therapies for cancer. Cells 2021; 10 (6): 1541. doi: 10.3390/cells10061541.

35. Cunliffe TG, Bates EA, Parker AL. Hitting the target but missing the point: recent progress towards adenovirus-based precision virotherapies. Cancers 2020; 12 (11): 3327. doi: 10.3390/cancers12113327.

36. Chan WM, McFadden G. Oncolytic poxviruses. Annu Rev Virol 2014; 1 (1): 119–141. doi: 10.1146/annurev-virology-031413-085442.

37. Alberts P, Tilgase A, Rasa A et al. The advent of oncolytic virotherapy in oncology: the Rigvir^® story. Eur J Pharmacol 2018; 837: 117–126. doi: 10.1016/j.ejphar.2018.08.042.

38. Alberts P. Comment on McCarthy, C.; et al. Developing picornaviruses for cancer therapy. Cancers 2019, 11, 685. Cancers 2020; 12 (7): 1775. doi: 10.3390/cancers12071775.

39. State Agency of Medicines Republic of Latvia. Rigvir marketing authorisation suspended; information for current patients. [online]. Available from: https: //www.zva.gov.lv/en/news-and-publications/news/rigvir-marketing-authorisation-suspended-information-current-patients.

40. Liang M. Oncorine, the world first oncolytic virus medicine and its update in China. Curr Cancer Drug Targets 2018; 18 (2): 171–176. doi: 10.2174/1568009618666171129221503.

41. Ferrucci PF, Pala L, Conforti F et al. Talimogene laherparepvec (T-VEC): an intralesional cancer immunotherapy for advanced melanoma. Cancers 2021; 13 (6): 1383. doi: 10.3390/cancers13061383.

42. Shen Y, Nemunaitis J. Herpes simplex virus 1 (HSV-1) for cancer treatment. Cancer Gene Ther 2006; 13 (11): 975–992. doi: 10.1038/sj.cgt.7700946.

43. Sugawara K, Iwai M, Ito H et al. Oncolytic herpes virus G47D works synergistically with CTLA-4 inhibition via dynamic intratumoral immune modulation. Mol Ther Oncolytics 2021; 22: 129–142. doi: 10.1016/j.omto.2021.05.004.

44. Taguchi S, Fukuhara H, Todo T. Oncolytic virus therapy in Japan: progress in clinical trials and future perspectives. Jpn J Clin Oncol 2019; 49 (3): 201–209. doi: 10.1093/jjco/hyy170.

45. Ferlay J, Soerjomataram I, Dikshit R et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015; 136 (5): E359–E386. doi: 10.1002/ijc.29210.

46. Lawler SE, Speranza M-C, Cho C-F et al. Oncolytic viruses in cancer treatment: a review. JAMA Oncol 2017; 3 (6): 841–849. doi: 10.1001/jamaoncol.2016.2064.

47. Chaurasiya S, Fong Y. Viroimmunotherapy for breast cancer: promises, problems and future directions. Cancer Gene Ther 2021; 28 (7–8): 757–768. doi: 10.1038/s41417-020-00265-6.

48. Zhang H, Xie W, Zhang Y et al. Oncolytic adenoviruses synergistically enhance anti-PD-L1 and anti-CTLA-4 immunotherapy by modulating the tumour microenvironment in a 4T1 orthotopic mouse model. Cancer Gene Ther 2021; 29 (5): 1–10. doi: 10.1038/s41417-021-00389-3.

49. Xie R, Bi X, Shang B et al. Efficacy and safety of oncolytic viruses in advanced or metastatic cancer: a network meta-analysis. Virol J 2021; 18 (1): 158. doi: 10.1186/s12985-021-01630-z.

50. Carter ME, Koch A, Lauer UM et al. Clinical trials of oncolytic viruses in breast cancer. Front Oncol 2021; 11: 803050. doi: 10.3389/fonc.2021.803050.

51. Bernstein V, Ellard SL, Dent SF et al. A randomized phase II study of weekly paclitaxel with or without pelareorep in patients with metastatic breast cancer: final analysis of Canadian Cancer Trials Group IND.213. Breast Cancer Res Treat 2018; 167 (2): 485–493. doi: 10.1007/s10549-017-4538-4.

52. Hall BL, Leronni D, Miyagawa Y et al. Generation of an oncolytic herpes simplex viral vector completely retargeted to the GDNF receptor GFRα1 for specific infection of breast cancer cells. Int J Mol Sci 2020; 21 (22): 8815. doi: 10.3390/ijms21228815.

53. Annels NE, Simpson GR, Denyer M et al. Oncolytic reovirus-mediated recruitment of early innate immune responses reverses immunotherapy resistance in prostate tumors. Mol Ther Oncolytics 2021; 20: 434–446. doi: 10.1016/j.omto.2020.09.010.

54. Boettcher AN, Usman A, Morgans A et al. Past, current, and future of immunotherapies for prostate cancer. Front Oncol 2019; 9: 884. doi: 10.3389/fonc.2019.00884.

55. Dhatchinamoorthy K, Colbert JD, Rock KL. Cancer immune evasion through loss of MHC class I antigen presentation. Front Immunol 2021; 12: 636568. doi: 10.3389/fimmu.2021.636568.

56. Liu Y-T, Sun Z-J. Turning cold tumors into hot tumors by improving T-cell infiltration. Theranostics 2021; 11 (11): 5365–5386. doi: 10.7150/thno.58390.

57. Zhao H, Wu L, Yan G et al. Inflammation and tumor progression: signaling pathways and targeted intervention. Signal Transduct Target Ther 2021; 6 (1): 1–46. doi: 10.1038/s41392-021-00658-5.

58. Patel D, McKay R, Parsons JK. Immunotherapy for localized prostate cancer: the next frontier? Urol Clin North Am 2020; 47 (4): 443–456. doi: 10.1016/j.ucl.2020.07.008.

59. Adamaki M, Zoumpourlis V. Immunotherapy as a precision medicine tool for the treatment of prostate cancer. Cancers 2021; 13 (2): 173. doi: 10.3390/cancers13020173.

60. Cheng H, Wang Y, Liu C et al. Development and verification of a prostate cancer prognostic signature based on an immunogenomic landscape analysis. Front Oncol 2021; 11: 711258. doi: 10.3389/fonc.2021.711258.

61. Eigl BJ, Chi K, Tu D et al. A randomized phase II study of pelareorep and docetaxel or docetaxel alone in men with metastatic castration resistant prostate cancer: CCTG study IND 209. Oncotarget 2018; 9 (8): 8155–8164. doi: 10.18632/oncotarget.24263.

62. Singh P, Pal SK, Alex A et al. Development of PROSTVAC immunotherapy in prostate cancer. Future Oncol 2015; 11 (15): 2137–2148. doi: 10.2217/fon.15.120.

63. Gulley JL, Borre M, Vogelzang NJ et al. Phase III trial of PROSTVAC in asymptomatic or minimally symptomatic metastatic castration-resistant prostate cancer. J Clin Oncol 2019; 37 (13): 1051–1061. doi: 10.1200/JCO.18.02031.

64. Zhu H, Liu X. Advances of tumorigenesis, diagnosis at early stage, and cellular immunotherapy in gastrointestinal malignancies. Front Oncol 2021; 11: 666340. doi: 10.3389/fonc.2021.666340.

65. Russo M, Sogari A, Bardelli A. Adaptive evolution: how bacteria and cancer cells survive stressful conditions and drug treatment. Cancer Discov 2021; 11 (8): 1886–1895. doi: 10.1158/2159-8290.CD-20-1588.

66. Russo M, Crisafulli G, Sogari A et al. Adaptive mutability of colorectal cancers in response to targeted therapies. Science 2019; 366 (6472): 1473–1480. doi: 10.1126/science.aav4474.

67. Kim CW, Chon HJ, Kim C. Combination immunotherapies to overcome intrinsic resistance to checkpoint blockade in microsatellite stable colorectal cancer. Cancers 2021; 13 (19): 4906. doi: 10.3390/cancers13194906.

68. Geevarghese SK, Geller DA, de Haan HA et al. Phase I/II study of oncolytic herpes simplex virus NV1020 in patients with extensively pretreated refractory colorectal cancer metastatic to the liver. Hum Gene Ther 2010; 21 (9): 1119–1128. doi: 10.1089/hum.2010.020.

69. Hu J, Lu R, Zhang Y et al. β-adrenergic receptor inhibition enhances oncolytic herpes virus propagation through STAT3 activation in gastric cancer. Cell Biosci 2021; 11 (1): 174. doi: 10.1186/s13578-021-00687-1.

70. Ilyas FZ, Beane JD, Pawlik TM. The state of immunotherapy in hepatobiliary cancers. Cells 2021; 10 (8): 2096. doi: 10.3390/cells10082096.