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Volume 98, Issue 12

Recent advances in vesicular stomatitis virus-based oncolytic virotherapy: a 5-year update Free

Abstract

Oncolytic virus (OV) therapy is an anti-cancer approach that uses viruses that preferentially infect, replicate in and kill cancer cells. Vesicular stomatitis virus (VSV, a rhabdovirus) is an OV that is currently being tested in the USA in several phase I clinical trials against different malignancies. Several factors make VSV a promising OV: lack of pre-existing human immunity against VSV, a small and easy to manipulate genome, cytoplasmic replication without risk of host cell transformation, independence of cell cycle and rapid growth to high titres in a broad range of cell lines facilitating large-scale virus production. While significant advances have been made in VSV-based OV therapy, room for improvement remains. Here we review recent studies (published in the last 5 years) that address ‘old’ and ‘new’ challenges of VSV-based OV therapy. These studies focused on improving VSV safety, oncoselectivity and oncotoxicity; breaking resistance of some cancers to VSV; preventing premature clearance of VSV; and stimulating tumour-specific immunity. Many of these approaches were based on combining VSV with other therapeutics. This review also discusses another rhabdovirus closely related to VSV, Maraba virus, which is currently being tested in Canada in phase I/II clinical trials.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Maraba virus , oncolytic , rhabdovirus , vesicular stomatitis virus , virotherapy and VSV
© 2017 The Authors
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2017-12-01
2024-04-20
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References

  1. Breitbach CJ, Lichty BD, Bell JC. Oncolytic viruses: therapeutics with an identity crisis. EBioMedicine 2016; 9:31–36 [View Article][PubMed]
     [Google Scholar]
  2. Russell SJ, Peng KW. Oncolytic virotherapy: a contest between apples and oranges. Mol Ther 2017; 25:1107–1116 [View Article][PubMed]
     [Google Scholar]
  3. Rehman H, Silk AW, Kane MP, Kaufman HL. Into the clinic: talimogene laherparepvec (T-VEC), a first-in-class intratumoral oncolytic viral therapy. J Immunother Cancer 2016; 4:53 [View Article][PubMed]
     [Google Scholar]
  4. Doniņa S, Strēle I, Proboka G, Auziņš J, Alberts P et al. Adapted ECHO-7 virus Rigvir immunotherapy (oncolytic virotherapy) prolongs survival in melanoma patients after surgical excision of the tumour in a retrospective study. Melanoma Res 2015; 25:421–426 [View Article][PubMed]
     [Google Scholar]
  5. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst 2006; 98:298–300 [View Article][PubMed]
     [Google Scholar]
  6. Lyles DS, Rupprecht CE. Rhabdoviridae. In Knipe DM. (editor) Fields Virology Philadelphia, PA: Lippincott Williams & Wilkins; 2007 pp. 1363–1408
     [Google Scholar]
  7. Quiroz E, Moreno N, Peralta PH, Tesh RB. A human case of encephalitis associated with vesicular stomatitis virus (Indiana serotype) infection. Am J Trop Med Hyg 1988; 39:312–314 [View Article][PubMed]
     [Google Scholar]
  8. Hastie E, Grdzelishvili VZ. Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J Gen Virol 2012; 93:2529–2545 [View Article][PubMed]
     [Google Scholar]
  9. Hastie E, Cataldi M, Marriott I, Grdzelishvili VZ. Understanding and altering cell tropism of vesicular stomatitis virus. Virus Res 2013; 176:16–32 [View Article][PubMed]
     [Google Scholar]
  10. Pearson AS, Koch PE, Atkinson N, Xiong M, Finberg RW et al. Factors limiting adenovirus-mediated gene transfer into human lung and pancreatic cancer cell lines. Clin Cancer Res 1999; 5:4208–4213[PubMed]
     [Google Scholar]
  11. Stojdl DF, Lichty BD, tenOever BR, Paterson JM, Power AT et al. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 2003; 4:263–275 [View Article][PubMed]
     [Google Scholar]
  12. Wang BX, Rahbar R, Fish EN. Interferon: current status and future prospects in cancer therapy. J Interferon Cytokine Res 2011; 31:545–552 [View Article][PubMed]
     [Google Scholar]
  13. Petersen JM, Her LS, Varvel V, Lund E, Dahlberg JE. The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol Cell Biol 2000; 20:8590–8601 [View Article][PubMed]
     [Google Scholar]
  14. dal Canto MC, Rabinowitz SG, Johnson TC. Status spongiousus resulting from intracerebral infection of mice with temperature-sensitive mutants of vesicular stomatitis virus. Br J Exp Pathol 1976; 57:321–330[PubMed]
     [Google Scholar]
  15. Clarke DK, Nasar F, Lee M, Johnson JE, Wright K et al. Synergistic attenuation of vesicular stomatitis virus by combination of specific G gene truncations and N gene translocations. J Virol 2007; 81:2056–2064 [View Article][PubMed]
     [Google Scholar]
  16. Plakhov IV, Arlund EE, Aoki C, Reiss CS. The earliest events in vesicular stomatitis virus infection of the murine olfactory neuroepithelium and entry of the central nervous system. Virology 1995; 209:257–262 [View Article][PubMed]
     [Google Scholar]
  17. Shinozaki K, Ebert O, Suriawinata A, Thung SN, Woo SL. Prophylactic alpha interferon treatment increases the therapeutic index of oncolytic vesicular stomatitis virus virotherapy for advanced hepatocellular carcinoma in immune-competent rats. J Virol 2005; 79:13705–13713 [View Article][PubMed]
     [Google Scholar]
  18. Schellekens H, Smiers-de Vreede E, de Reus A, Dijkema R. Antiviral activity of interferon in rats and the effect of immune suppression. J Gen Virol 1984; 65:391–396 [View Article][PubMed]
     [Google Scholar]
  19. Johnson JE, Nasar F, Coleman JW, Price RE, Javadian A et al. Neurovirulence properties of recombinant vesicular stomatitis virus vectors in non-human primates. Virology 2007; 360:36–49 [View Article][PubMed]
     [Google Scholar]
  20. Coulon P, Deutsch V, Lafay F, Martinet-Edelist C, Wyers F et al. Genetic evidence for multiple functions of the matrix protein of vesicular stomatitis virus. J Gen Virol 1990; 71:991–996 [View Article][PubMed]
     [Google Scholar]
  21. Black BL, Rhodes RB, McKenzie M, Lyles DS. The role of vesicular stomatitis virus matrix protein in inhibition of host-directed gene expression is genetically separable from its function in virus assembly. J Virol 1993; 67:4814–4821[PubMed]
     [Google Scholar]
  22. Jenks N, Myers R, Greiner SM, Thompson J, Mader EK et al. Safety studies on intrahepatic or intratumoral injection of oncolytic vesicular stomatitis virus expressing interferon-beta in rodents and nonhuman primates. Hum Gene Ther 2010; 21:451–462 [View Article][PubMed]
     [Google Scholar]
  23. Obuchi M, Fernandez M, Barber GN. Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J Virol 2003; 77:8843–8856 [View Article][PubMed]
     [Google Scholar]
  24. Patel MR, Jacobson BA, Ji Y, Drees J, Tang S et al. Vesicular stomatitis virus expressing interferon-β is oncolytic and promotes antitumor immune responses in a syngeneic murine model of non-small cell lung cancer. Oncotarget 2015; 6:33165–33177 [View Article][PubMed]
     [Google Scholar]
  25. Barber GN. Vesicular stomatitis virus as an oncolytic vector. Viral Immunol 2004; 17:516–527 [View Article][PubMed]
     [Google Scholar]
  26. Lichty BD, Power AT, Stojdl DF, Bell JC. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 2004; 10:210–216 [View Article][PubMed]
     [Google Scholar]
  27. Kurisetty VV, Heiber J, Myers R, Pereira GS, Goodwin JW et al. Preclinical safety and activity of recombinant VSV-IFN-β in an immunocompetent model of squamous cell carcinoma of the head and neck. Head Neck 2014; 36:1619–1627 [View Article][PubMed]
     [Google Scholar]
  28. Zhang L, Steele MB, Jenks N, Grell J, Suksanpaisan L et al. Safety studies in tumor and non-tumor-bearing mice in support of clinical trials using oncolytic VSV-IFNβ-NIS. Hum Gene Ther Clin Dev 2016; 27:111–122 [View Article][PubMed]
     [Google Scholar]
  29. Leblanc AK, Naik S, Galyon GD, Jenks N, Steele M et al. Safety studies on intravenous administration of oncolytic recombinant vesicular stomatitis virus in purpose-bred beagle dogs. Hum Gene Ther Clin Dev 2013; 24:174–181 [View Article][PubMed]
     [Google Scholar]
  30. Naik S, Nace R, Barber GN, Russell SJ. Potent systemic therapy of multiple myeloma utilizing oncolytic vesicular stomatitis virus coding for interferon-β. Cancer Gene Ther 2012; 19:443–450 [View Article][PubMed]
     [Google Scholar]
  31. Naik S, Nace R, Federspiel MJ, Barber GN, Peng KW et al. Curative one-shot systemic virotherapy in murine myeloma. Leukemia 2012; 26:1870–1878 [View Article][PubMed]
     [Google Scholar]
  32. Westcott MM, Liu J, Rajani K, D'Agostino R, Lyles DS et al. Interferon beta and interferon alpha 2a differentially protect head and neck cancer cells from vesicular stomatitis virus-induced oncolysis. J Virol 2015; 89:7944–7954 [View Article][PubMed]
     [Google Scholar]
  33. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J et al. Type III IFN interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immune-competent mouse models of cancer. Cancer Res 2010; 70:4539–4549 [View Article][PubMed]
     [Google Scholar]
  34. Guayasamin RC, Reynolds TD, Wei X, Fujiwara M, Robek MD. Type III interferon attenuates a vesicular stomatitis virus-based vaccine vector. J Virol 2014; 88:10909–10917 [View Article][PubMed]
     [Google Scholar]
  35. Wollmann G, Rogulin V, Simon I, Rose JK, van den Pol AN. Some attenuated variants of vesicular stomatitis virus show enhanced oncolytic activity against human glioblastoma cells relative to normal brain cells. J Virol 2010; 84:1563–1573 [View Article][PubMed]
     [Google Scholar]
  36. van den Pol AN, Davis JN. Highly attenuated recombinant vesicular stomatitis virus VSV-12'GFP displays immunogenic and oncolytic activity. J Virol 2013; 87:1019–1034 [View Article][PubMed]
     [Google Scholar]
  37. Ammayappan A, Peng KW, Russell SJ. Characteristics of oncolytic vesicular stomatitis virus displaying tumor-targeting ligands. J Virol 2013; 87:13543–13555 [View Article][PubMed]
     [Google Scholar]
  38. Russell SJ, Peng KW. Measles virus for cancer therapy. Curr Top Microbiol Immunol 2009; 330:213–241[PubMed]
     [Google Scholar]
  39. Ayala-Breton C, Russell LO, Russell SJ, Peng KW. Faster replication and higher expression levels of viral glycoproteins give the vesicular stomatitis virus/measles virus hybrid VSV-FH a growth advantage over measles virus. J Virol 2014; 88:8332–8339 [View Article][PubMed]
     [Google Scholar]
  40. Ayala-Breton C, Suksanpaisan L, Mader EK, Russell SJ, Peng KW. Amalgamating oncolytic viruses to enhance their safety, consolidate their killing mechanisms, and accelerate their spread. Mol Ther 2013; 21:1930–1937 [View Article][PubMed]
     [Google Scholar]
  41. Ayala-Breton C, Barber GN, Russell SJ, Peng KW. Retargeting vesicular stomatitis virus using measles virus envelope glycoproteins. Hum Gene Ther 2012; 23:484–491 [View Article][PubMed]
     [Google Scholar]
  42. Ayala Breton C, Wikan N, Abbuhl A, Smith DR, Russell SJ et al. Oncolytic potency of HER-2 retargeted VSV-FH hybrid viruses: the role of receptor ligand affinity. Mol Ther Oncolytics 2015; 2:15012 [View Article][PubMed]
     [Google Scholar]
  43. Kleinlützum D, Hanauer JDS, Muik A, Hanschmann KM, Kays SK et al. Enhancing the Oncolytic activity of CD133-Targeted Measles Virus: receptor extension or chimerism with Vesicular Stomatitis Virus are Most effective. Front Oncol 2017; 7:127 [View Article][PubMed]
     [Google Scholar]
  44. Liu YP, Russell SP, Ayala-Breton C, Russell SJ, Peng KW. Ablation of nectin4 binding compromises CD46 usage by a hybrid vesicular stomatitis virus/measles virus. J Virol 2014; 88:2195–2204 [View Article][PubMed]
     [Google Scholar]
  45. Muik A, Kneiske I, Werbizki M, Wilflingseder D, Giroglou T et al. Pseudotyping vesicular stomatitis virus with lymphocytic choriomeningitis virus glycoproteins enhances infectivity for glioma cells and minimizes neurotropism. J Virol 2011; 85:5679–5684 [View Article][PubMed]
     [Google Scholar]
  46. Muik A, Stubbert LJ, Jahedi RZ, Geiβ Y, Kimpel J et al. Re-engineering vesicular stomatitis virus to abrogate neurotoxicity, circumvent humoral immunity, and enhance oncolytic potency. Cancer Res 2014; 74:3567–3578 [View Article][PubMed]
     [Google Scholar]
  47. Betancourt D, Ramos JC, Barber GN. Retargeting oncolytic vesicular stomatitis virus to human T-cell lymphotropic virus type 1-associated adult T-cell leukemia. J Virol 2015; 89:11786–11800 [View Article][PubMed]
     [Google Scholar]
  48. Wollmann G, Drokhlyansky E, Davis JN, Cepko C, van den Pol AN. Lassa-vesicular stomatitis chimeric virus safely destroys brain tumors. J Virol 2015; 89:6711–6724 [View Article][PubMed]
     [Google Scholar]
  49. van den Pol AN, Mao G, Chattopadhyay A, Rose JK, Davis JN. Chikungunya, Influenza, Nipah, and Semliki Forest Chimeric Viruses with Vesicular Stomatitis Virus: Actions in the Brain. J Virol 2017; 91:e02154-16 [View Article][PubMed]
     [Google Scholar]
  50. Garijo R, Hernández-Alonso P, Rivas C, Diallo JS, Sanjuán R. Experimental evolution of an oncolytic vesicular stomatitis virus with increased selectivity for p53-deficient cells. PLoS One 2014; 9:e102365 [View Article][PubMed]
     [Google Scholar]
  51. Garijo R, Cuevas JM, Briz Á, Sanjuán R. Constrained evolvability of interferon suppression in an RNA virus. Sci Rep 2016; 6:24722 [View Article][PubMed]
     [Google Scholar]
  52. Muik A, Dold C, Geiß Y, Volk A, Werbizki M et al. Semireplication-competent vesicular stomatitis virus as a novel platform for oncolytic virotherapy. J Mol Med 2012; 90:959–970 [View Article][PubMed]
     [Google Scholar]
  53. Batenchuk C, Le Boeuf F, Stubbert L, Falls T, Atkins HL et al. Non-replicating rhabdovirus-derived particles (NRRPs) eradicate acute leukemia by direct cytolysis and induction of antitumor immunity. Blood Cancer J 2013; 3:e123 [View Article][PubMed]
     [Google Scholar]
  54. Hastie E, Besmer DM, Shah NR, Murphy AM, Moerdyk-Schauwecker M et al. Oncolytic vesicular stomatitis virus in an immunocompetent model of MUC1-positive or MUC1-null pancreatic ductal adenocarcinoma. J Virol 2013; 87:10283–10294 [View Article][PubMed]
     [Google Scholar]
  55. Ammayappan A, Nace R, Peng KW, Russell SJ. Neuroattenuation of vesicular stomatitis virus through picornaviral internal ribosome entry sites. J Virol 2013; 87:3217–3228 [View Article][PubMed]
     [Google Scholar]
  56. Wollmann G, Paglino JC, Maloney PR, Ahmadi SA, van den Pol AN. Attenuation of vesicular stomatitis virus infection of brain using antiviral drugs and an adeno-associated virus-interferon vector. Virology 2015; 475:1–14 [View Article][PubMed]
     [Google Scholar]
  57. Marozin S, Altomonte J, Muñoz-Álvarez KA, Rizzani A, de Toni EN et al. STAT3 inhibition reduces toxicity of oncolytic VSV and provides a potentially synergistic combination therapy for hepatocellular carcinoma. Cancer Gene Ther 2015; 22:317–325 [View Article][PubMed]
     [Google Scholar]
  58. Yu H, Lee H, Herrmann A, Buettner R, Jove R. Revisiting STAT3 signalling in cancer: new and unexpected biological functions. Nat Rev Cancer 2014; 14:736–746 [View Article][PubMed]
     [Google Scholar]
  59. Athearn K, Sample CJ, Barefoot BE, Williams KL, Ramsburg EA. Acute reactogenicity after intramuscular immunization with recombinant vesicular stomatitis virus is linked to production of IL-1β. PLoS One 2012; 7:e46516 [View Article][PubMed]
     [Google Scholar]
  60. Yarde DN, Naik S, Nace RA, Peng KW, Federspiel MJ et al. Meningeal myeloma deposits adversely impact the therapeutic index of an oncolytic VSV. Cancer Gene Ther 2013; 20:616–621 [View Article][PubMed]
     [Google Scholar]
  61. Lun X, Senger DL, Alain T, Oprea A, Parato K et al. Effects of intravenously administered recombinant vesicular stomatitis virus (VSV(deltaM51)) on multifocal and invasive gliomas. J Natl Cancer Inst 2006; 98:1546–1557 [View Article][PubMed]
     [Google Scholar]
  62. Blackham AU, Northrup SA, Willingham M, D'Agostino RB, Lyles DS et al. Variation in susceptibility of human malignant melanomas to oncolytic vesicular stomatitis virus. Surgery 2013; 153:333–343 [View Article][PubMed]
     [Google Scholar]
  63. Blackham AU, Northrup SA, Willingham M, Sirintrapun J, Russell GB et al. Molecular determinants of susceptibility to oncolytic vesicular stomatitis virus in pancreatic adenocarcinoma. J Surg Res 2014; 187:412–426 [View Article][PubMed]
     [Google Scholar]
  64. Moerdyk-Schauwecker M, Shah NR, Murphy AM, Hastie E, Mukherjee P et al. Resistance of pancreatic cancer cells to oncolytic vesicular stomatitis virus: role of type I interferon signaling. Virology 2013; 436:221–234 [View Article][PubMed]
     [Google Scholar]
  65. Murphy AM, Besmer DM, Moerdyk-Schauwecker M, Moestl N, Ornelles DA et al. Vesicular stomatitis virus as an oncolytic agent against pancreatic ductal adenocarcinoma. J Virol 2012; 86:3073–3087 [View Article][PubMed]
     [Google Scholar]
  66. Cataldi M, Shah NR, Felt SA, Grdzelishvili VZ. Breaking resistance of pancreatic cancer cells to an attenuated vesicular stomatitis virus through a novel activity of IKK inhibitor TPCA-1. Virology 2015; 485:340–354 [View Article][PubMed]
     [Google Scholar]
  67. Hastie E, Cataldi M, Moerdyk-Schauwecker MJ, Felt SA, Steuerwald N et al. Novel biomarkers of resistance of pancreatic cancer cells to oncolytic vesicular stomatitis virus. Oncotarget 2016; 7:61601–61618 [View Article][PubMed]
     [Google Scholar]
  68. Escobar-Zarate D, Liu YP, Suksanpaisan L, Russell SJ, Peng KW. Overcoming cancer cell resistance to VSV oncolysis with JAK1/2 inhibitors. Cancer Gene Ther 2013; 20:582–589 [View Article][PubMed]
     [Google Scholar]
  69. Dold C, Rodriguez Urbiola C, Wollmann G, Egerer L, Muik A et al. Application of interferon modulators to overcome partial resistance of human ovarian cancers to VSV-GP oncolytic viral therapy. Mol Ther Oncolytics 2016; 3:16021 [View Article][PubMed]
     [Google Scholar]
  70. du Z, Wei L, Murti A, Pfeffer SR, Fan M et al. Non-conventional signal transduction by type 1 interferons: the NF-kappaB pathway. J Cell Biochem 2007; 102:1087–1094 [View Article][PubMed]
     [Google Scholar]
  71. du Z, Whitt MA, Baumann J, Garner JM, Morton CL et al. Inhibition of type I interferon-mediated antiviral action in human glioma cells by the IKK inhibitors BMS-345541 and TPCA-1. J Interferon Cytokine Res 2012; 32:368–377 [View Article][PubMed]
     [Google Scholar]
  72. Yarde DN, Nace RA, Russell SJ. Oncolytic vesicular stomatitis virus and bortezomib are antagonistic against myeloma cells in vitro but have additive anti-myeloma activity in vivo. Exp Hematol 2013; 41:1038–1049 [View Article][PubMed]
     [Google Scholar]
  73. Shulak L, Beljanski V, Chiang C, Dutta SM, van Grevenynghe J et al. Histone deacetylase inhibitors potentiate vesicular stomatitis virus oncolysis in prostate cancer cells by modulating NF-κB-dependent autophagy. J Virol 2014; 88:2927–2940 [View Article][PubMed]
     [Google Scholar]
  74. Nguyên TL, Abdelbary H, Arguello M, Breitbach C, Leveille S et al. Chemical targeting of the innate antiviral response by histone deacetylase inhibitors renders refractory cancers sensitive to viral oncolysis. Proc Natl Acad Sci USA 2008; 105:14981–14986 [View Article][PubMed]
     [Google Scholar]
  75. Fehl DJ, Ahmed M. Curcumin promotes the oncoltyic capacity of vesicular stomatitis virus for the treatment of prostate cancers. Virus Res 2017; 228:14–23 [View Article][PubMed]
     [Google Scholar]
  76. Ben Yebdri F, van Grevenynghe J, Tang VA, Goulet ML, Wu JH et al. Triptolide-mediated inhibition of interferon signaling enhances vesicular stomatitis virus-based oncolysis. Mol Ther 2013; 21:2043–2053 [View Article][PubMed]
     [Google Scholar]
  77. Arulanandam R, Batenchuk C, Varette O, Zakaria C, Garcia V et al. Microtubule disruption synergizes with oncolytic virotherapy by inhibiting interferon translation and potentiating bystander killing. Nat Commun 2015; 6:6410 [View Article][PubMed]
     [Google Scholar]
  78. Corredor JC, Redding N, Bloté K, Robbins SM, Senger DL et al. N-Myc expression enhances the oncolytic effects of vesicular stomatitis virus in human neuroblastoma cells. Mol Ther Oncolytics 2016; 3:16005 [View Article][PubMed]
     [Google Scholar]
  79. Komatsu Y, Christian SL, Ho N, Pongnopparat T, Licursi M et al. Oncogenic Ras inhibits IRF1 to promote viral oncolysis. Oncogene 2015; 34:3985–3993 [View Article][PubMed]
     [Google Scholar]
  80. Wollmann G, Davis JN, Bosenberg MW, van den Pol AN. Vesicular stomatitis virus variants selectively infect and kill human melanomas but not normal melanocytes. J Virol 2013; 87:6644–6659 [View Article][PubMed]
     [Google Scholar]
  81. Yu N, Puckett S, Antinozzi PA, Cramer SD, Lyles DS. Changes in susceptibility to oncolytic vesicular stomatitis virus during progression of prostate cancer. J Virol 2015; 89:5250–5263 [View Article][PubMed]
     [Google Scholar]
  82. Champion BR, Fisher K, Seymour L. A PTENtial cause for the selectivity of oncolytic viruses?. Nat Immunol 2016; 17:225–226 [View Article][PubMed]
     [Google Scholar]
  83. Le Boeuf F, Niknejad N, Wang J, Auer R, Weberpals JI et al. Sensitivity of cervical carcinoma cells to vesicular stomatitis virus-induced oncolysis: potential role of human papilloma virus infection. Int J Cancer 2012; 131:E204E215 [View Article][PubMed]
     [Google Scholar]
  84. Moon J, Kaowinn S, Cho IR, Min DS, Myung H et al. Hepatitis C virus core protein enhances hepatocellular carcinoma cells to be susceptible to oncolytic vesicular stomatitis virus through down-regulation of HDAC4. Biochem Biophys Res Commun 2016; 474:428–434 [View Article][PubMed]
     [Google Scholar]
  85. Felt SA, Droby GN, Grdzelishvili VZ. Ruxolitinib and polycation combination treatment overcomes multiple mechanisms of resistance of pancreatic cancer cells to oncolytic vesicular stomatitis virus. J Virol 2017; 91:e00461-17 [View Article][PubMed]
     [Google Scholar]
  86. Felt SA, Moerdyk-Schauwecker MJ, Grdzelishvili VZ. Induction of apoptosis in pancreatic cancer cells by vesicular stomatitis virus. Virology 2015; 474:163–173 [View Article][PubMed]
     [Google Scholar]
  87. Schache P, Gürlevik E, Strüver N, Woller N, Malek N et al. VSV virotherapy improves chemotherapy by triggering apoptosis due to proteasomal degradation of Mcl-1. Gene Ther 2009; 16:849–861 [View Article][PubMed]
     [Google Scholar]
  88. Samuel S, Tumilasci VF, Oliere S, Nguyên TL, Shamy A et al. VSV oncolysis in combination with the BCL-2 inhibitor obatoclax overcomes apoptosis resistance in chronic lymphocytic leukemia. Mol Ther 2010; 18:2094–2103 [View Article][PubMed]
     [Google Scholar]
  89. Samuel S, Beljanski V, van Grevenynghe J, Richards S, Ben Yebdri F et al. BCL-2 inhibitors sensitize therapy-resistant chronic lymphocytic leukemia cells to VSV oncolysis. Mol Ther 2013; 21:1413–1423 [View Article][PubMed]
     [Google Scholar]
  90. Dobson CC, Naing T, Beug ST, Faye MD, Chabot J et al. Oncolytic virus synergizes with Smac mimetic compounds to induce rhabdomyosarcoma cell death in a syngeneic murine model. Oncotarget 2017; 8:3495–3508 [View Article][PubMed]
     [Google Scholar]
  91. Malilas W, Koh SS, Kim S, Srisuttee R, Cho IR et al. Cancer upregulated gene 2, a novel oncogene, enhances migration and drug resistance of colon cancer cells via STAT1 activation. Int J Oncol 2013; 43:1111–1116 [View Article][PubMed]
     [Google Scholar]
  92. Malilas W, Koh SS, Srisuttee R, Boonying W, Cho IR et al. Cancer upregulated gene 2, a novel oncogene, confers resistance to oncolytic vesicular stomatitis virus through STAT1-OASL2 signaling. Cancer Gene Ther 2013; 20:125–132 [View Article][PubMed]
     [Google Scholar]
  93. Malilas W, Koh SS, Lee S, Srisuttee R, Cho IR et al. Suppression of autophagic genes sensitizes CUG2-overexpressing A549 human lung cancer cells to oncolytic vesicular stomatitis virus-induced apoptosis. Int J Oncol 2014; 44:1177–1184 [View Article][PubMed]
     [Google Scholar]
  94. Liu GH, Wang WL, Wang C, Li CL, Zhang XL et al. Livin modulates the apoptotic effects of vesicular stomatotitis virus in lung adenocarcinoma. Int J Oncol 2015; 47:1775–1782 [View Article][PubMed]
     [Google Scholar]
  95. Olagnier D, Lababidi RR, Hadj SB, Sze A, Liu Y et al. Activation of Nrf2 signaling augments vesicular stomatitis virus oncolysis via autophagy-driven suppression of antiviral immunity. Mol Ther 2017; 25:1900–1916 [View Article][PubMed]
     [Google Scholar]
  96. Bressy C, Hastie E, Grdzelishvili VZ. Combining oncolytic virotherapy with p53 tumor suppressor gene therapy. Mol Ther Oncolytics 2017; 5:20–40 [View Article][PubMed]
     [Google Scholar]
  97. Heiber JF, Barber GN. Vesicular stomatitis virus expressing tumor suppressor p53 is a highly attenuated, potent oncolytic agent. J Virol 2011; 85:10440–10450 [View Article][PubMed]
     [Google Scholar]
  98. Hastie E, Cataldi M, Steuerwald N, Grdzelishvili VZ. An unexpected inhibition of antiviral signaling by virus-encoded tumor suppressor p53 in pancreatic cancer cells. Virology 2015; 483:126–140 [View Article][PubMed]
     [Google Scholar]
  99. Alajez NM, Mocanu JD, Krushel T, Bell JC, Liu FF. Enhanced vesicular stomatitis virus (VSVΔ51) targeting of head and neck cancer in combination with radiation therapy or ZD6126 vascular disrupting agent. Cancer Cell Int 2012; 12:27 [View Article][PubMed]
     [Google Scholar]
  100. Altomonte J, Braren R, Schulz S, Marozin S, Rummeny EJ et al. Synergistic antitumor effects of transarterial viroembolization for multifocal hepatocellular carcinoma in rats. Hepatology 2008; 48:1864–1873 [View Article][PubMed]
     [Google Scholar]
  101. Miller A, Nace R, Ayala-Breton C C, Steele M, Bailey K et al. Perfusion pressure is a critical determinant of the intratumoral extravasation of oncolytic viruses. Mol Ther 2016; 24:306–317 [View Article][PubMed]
     [Google Scholar]
  102. Jha BK, Dong B, Nguyen CT, Polyakova I, Silverman RH. Suppression of antiviral innate immunity by sunitinib enhances oncolytic virotherapy. Mol Ther 2013; 21:1749–1757 [View Article][PubMed]
     [Google Scholar]
  103. Le Boeuf F, Diallo JS, Mccart JA, Thorne S, Falls T et al. Synergistic interaction between oncolytic viruses augments tumor killing. Mol Ther 2010; 18:888–895 [View Article][PubMed]
     [Google Scholar]
  104. Cronin M, Le Boeuf F, Murphy C, Roy DG, Falls T et al. Bacterial-mediated knockdown of tumor resistance to an oncolytic virus enhances therapy. Mol Ther 2014; 22:1188–1197 [View Article][PubMed]
     [Google Scholar]
  105. Zhang L, Steele MB, Jenks N, Grell J, Behrens M et al. Robust oncolytic virotherapy induces tumor lysis syndrome and associated toxicities in the MPC-11 plasmacytoma model. Mol Ther 2016; 24:2109–2117 [View Article][PubMed]
     [Google Scholar]
  106. Muharemagic D, Zamay A, Ghobadloo SM, Evgin L, Savitskaya A et al. Aptamer-facilitated protection of oncolytic virus from neutralizing antibodies. Mol Ther Nucleic Acids 2014; 3:e167 [View Article][PubMed]
     [Google Scholar]
  107. Muharemagic D, Labib M, Ghobadloo SM, Zamay AS, Bell JC et al. Anti-Fab aptamers for shielding virus from neutralizing antibodies. J Am Chem Soc 2012; 134:17168–17177 [View Article][PubMed]
     [Google Scholar]
  108. Labib M, Zamay AS, Muharemagic D, Chechik A, Bell JC et al. Electrochemical sensing of aptamer-facilitated virus immunoshielding. Anal Chem 2012; 84:1677–1686 [View Article][PubMed]
     [Google Scholar]
  109. Tesfay MZ, Kirk AC, Hadac EM, Griesmann GE, Federspiel MJ et al. PEGylation of vesicular stomatitis virus extends virus persistence in blood circulation of passively immunized mice. J Virol 2013; 87:3752–3759 [View Article][PubMed]
     [Google Scholar]
  110. Liang M, Yan M, Lu Y, Chen IS. Retargeting vesicular stomatitis virus glycoprotein pseudotyped lentiviral vectors with enhanced stability by in situ synthesized polymer shell. Hum Gene Ther Methods 2013; 24:11–18 [View Article][PubMed]
     [Google Scholar]
  111. Hwang BY, Schaffer DV. Engineering a serum-resistant and thermostable vesicular stomatitis virus G glycoprotein for pseudotyping retroviral and lentiviral vectors. Gene Ther 2013; 20:807–815 [View Article][PubMed]
     [Google Scholar]
  112. Tesfay MZ, Ammayappan A, Federspiel MJ, Barber GN, Stojdl D et al. Vesiculovirus neutralization by natural IgM and complement. J Virol 2014; 88:6148–6157 [View Article][PubMed]
     [Google Scholar]
  113. Simovic B, Walsh SR, Wan Y. Mechanistic insights into the oncolytic activity of vesicular stomatitis virus in cancer immunotherapy. Oncolytic Virother 2015; 4:157–167 [View Article][PubMed]
     [Google Scholar]
  114. Bridle BW, Clouthier D, Zhang L, Pol J, Chen L et al. Oncolytic vesicular stomatitis virus quantitatively and qualitatively improves primary CD8+ T-cell responses to anticancer vaccines. Oncoimmunology 2013; 2:e26013 [View Article][PubMed]
     [Google Scholar]
  115. Janelle V, Langlois MP, Lapierre P, Charpentier T, Poliquin L et al. The strength of the T cell response against a surrogate tumor antigen induced by oncolytic VSV therapy does not correlate with tumor control. Mol Ther 2014; 22:1198–1210 [View Article][PubMed]
     [Google Scholar]
  116. Bourgeois-Daigneault MC, Roy DG, Falls T, Twumasi-Boateng K, St-Germain LE et al. Oncolytic vesicular stomatitis virus expressing interferon-γ has enhanced therapeutic activity. Mol Ther Oncolytics 2016; 3:16001 [View Article][PubMed]
     [Google Scholar]
  117. Pulido J, Kottke T, Thompson J, Galivo F, Wongthida P et al. Using virally expressed melanoma cDNA libraries to identify tumor-associated antigens that cure melanoma. Nat Biotechnol 2012; 30:337–343 [View Article][PubMed]
     [Google Scholar]
  118. Cockle JV, Rajani K, Zaidi S, Kottke T, Thompson J et al. Combination viroimmunotherapy with checkpoint inhibition to treat glioma, based on location-specific tumor profiling. Neuro Oncol 2016; 18:518–527 [View Article][PubMed]
     [Google Scholar]
  119. Blanchard M, Shim KG, Grams MP, Rajani K, Diaz RM et al. Definitive management of oligometastatic melanoma in a murine model using combined ablative radiation therapy and viral immunotherapy. Int J Radiat Oncol Biol Phys 2015; 93:577–587 [View Article][PubMed]
     [Google Scholar]
  120. Rommelfanger DM, Wongthida P, Diaz RM, Kaluza KM, Thompson JM et al. Systemic combination virotherapy for melanoma with tumor antigen-expressing vesicular stomatitis virus and adoptive T-cell transfer. Cancer Res 2012; 72:4753–4764 [View Article][PubMed]
     [Google Scholar]
  121. Rommelfanger DM, Compte M, Grau MC, Diaz RM, Ilett E et al. The efficacy versus toxicity profile of combination virotherapy and TLR immunotherapy highlights the danger of administering TLR agonists to oncolytic virus-treated mice. Mol Ther 2013; 21:348–357 [View Article][PubMed]
     [Google Scholar]
  122. Mahoney KM, Freeman GJ, McDermott DF. The next immune-checkpoint inhibitors: PD-1/PD-L1 blockade in melanoma. Clin Ther 2015; 37:764–782 [View Article][PubMed]
     [Google Scholar]
  123. Shen W, Patnaik MM, Ruiz A, Russell SJ, Peng KW. Immunovirotherapy with vesicular stomatitis virus and PD-L1 blockade enhances therapeutic outcome in murine acute myeloid leukemia. Blood 2016; 127:1449–1458 [View Article][PubMed]
     [Google Scholar]
  124. Durham NM, Mulgrew K, McGlinchey K, Monks NR, Ji H et al. Oncolytic VSV primes differential responses to immuno-oncology therapy. Mol Ther 2017; 25:1917–1932 [View Article][PubMed]
     [Google Scholar]
  125. Ilett E, Kottke T, Thompson J, Rajani K, Zaidi S et al. Prime-boost using separate oncolytic viruses in combination with checkpoint blockade improves anti-tumour therapy. Gene Ther 2017; 24:21–30 [View Article][PubMed]
     [Google Scholar]
  126. Shim KG, Zaidi S, Thompson J, Kottke T, Evgin L et al. Inhibitory receptors induced by VSV viroimmunotherapy are not necessarily targets for improving treatment efficacy. Mol Ther 2017; 25:962–975 [View Article][PubMed]
     [Google Scholar]
  127. Brun J, McManus D, Lefebvre C, Hu K, Falls T et al. Identification of genetically modified Maraba virus as an oncolytic rhabdovirus. Mol Ther 2010; 18:1440–1449 [View Article][PubMed]
     [Google Scholar]
  128. Zhang J, Tai LH, Ilkow CS, Alkayyal AA, Ananth AA et al. Maraba MG1 virus enhances natural killer cell function via conventional dendritic cells to reduce postoperative metastatic disease. Mol Ther 2014; 22:1320–1332 [View Article][PubMed]
     [Google Scholar]
  129. Tong JG, Valdes YR, Barrett JW, Bell JC, Stojdl D et al. Evidence for differential viral oncolytic efficacy in an in vitro model of epithelial ovarian cancer metastasis. Mol Ther Oncolytics 2015; 2:15013 [View Article][PubMed]
     [Google Scholar]
  130. Le Boeuf F, Selman M, Son HH, Bergeron A, Chen A et al. Oncolytic Maraba virus MG1 as a treatment for Sarcoma. Int J Cancer 2017; 141:1257–1264 [View Article][PubMed]
     [Google Scholar]
  131. Bourgeois-Daigneault MC, St-Germain LE, Roy DG, Pelin A, Aitken AS et al. Combination of Paclitaxel and MG1 oncolytic virus as a successful strategy for breast cancer treatment. Breast Cancer Res 2016; 18:83 [View Article][PubMed]
     [Google Scholar]
  132. Alkayyal AA, Tai LH, Kennedy MA, de Souza CT, Zhang J et al. NK-cell recruitment is necessary for eradication of peritoneal carcinomatosis with an IL12-expressing Maraba virus cellular vaccine. Cancer Immunol Res 2017; 5:211–221 [View Article][PubMed]
     [Google Scholar]
  133. Evgin L, Ilkow CS, Bourgeois-Daigneault MC, de Souza CT, Stubbert L et al. Complement inhibition enables tumor delivery of LCMV glycoprotein pseudotyped viruses in the presence of antiviral antibodies. Mol Ther Oncolytics 2016; 3:16027 [View Article][PubMed]
     [Google Scholar]
  134. Pol JG, Zhang L, Bridle BW, Stephenson KB, Rességuier J et al. Maraba virus as a potent oncolytic vaccine vector. Mol Ther 2014; 22:420–429 [View Article][PubMed]
     [Google Scholar]
  135. Liu YP, Steele MB, Suksanpaisan L, Federspiel MJ, Russell SJ et al. Oncolytic measles and vesicular stomatitis virotherapy for endometrial cancer. Gynecol Oncol 2014; 132:194–202 [View Article][PubMed]
     [Google Scholar]
  136. Yamaki M, Shinozaki K, Sakaguchi T, Meseck M, Ebert O et al. The potential of recombinant vesicular stomatitis virus-mediated virotherapy against metastatic colon cancer. Int J Mol Med 2013; 31:299–306 [View Article][PubMed]
     [Google Scholar]
  137. Randle RW, Northrup SA, Sirintrapun SJ, Lyles DS, Stewart JH, Jht S. Oncolytic vesicular stomatitis virus as a treatment for neuroendocrine tumors. Surgery 2013; 154:1323–1330 discussion 1329-1330 [View Article][PubMed]
     [Google Scholar]
  138. Gamwell LF, Gambaro K, Merziotis M, Crane C, Arcand SL et al. Small cell ovarian carcinoma: genomic stability and responsiveness to therapeutics. Orphanet J Rare Dis 2013; 8:33 [View Article][PubMed]
     [Google Scholar]
  139. Abdelbary H, Brown CW, Werier J, Bell J. Using targeted virotherapy to treat a resistant Ewing sarcoma model: from the bedside to the bench and back. ScientificWorldJournal 2014; 2014:1–11 [View Article][PubMed]
     [Google Scholar]
  140. Zhou Y, Wen F, Zhang P, Tang R, Li Q. Vesicular stomatitis virus is a potent agent for the treatment of malignant ascites. Oncol Rep 2016; 35:1573–1581 [View Article][PubMed]
     [Google Scholar]
  141. Altomonte J, Marozin S, de Toni EN, Rizzani A, Esposito I et al. Antifibrotic properties of transarterial oncolytic VSV therapy for hepatocellular carcinoma in rats with thioacetamide-induced liver fibrosis. Mol Ther 2013; 21:2032–2042 [View Article][PubMed]
     [Google Scholar]
  142. Nath S, Mukherjee P. MUC1: a multifaceted oncoprotein with a key role in cancer progression. Trends Mol Med 2014; 20:332–342 [View Article][PubMed]
     [Google Scholar]
  143. Falls T, Roy DG, Bell JC, Bourgeois-Daigneault MC. Murine tumor models for oncolytic rhabdo-virotherapy. Ilar J 2016; 57:73–85 [View Article][PubMed]
     [Google Scholar]
  144. Muñoz-Álvarez KA, Altomonte J, Laitinen I, Ziegler S, Steiger K et al. PET imaging of oncolytic VSV expressing the mutant HSV-1 thymidine kinase transgene in a preclinical HCC rat model. Mol Ther 2015; 23:728–736 [View Article][PubMed]
     [Google Scholar]
  145. Miller A, Suksanpaisan L, Naik S, Nace R, Federspiel M et al. Reporter gene imaging identifies intratumoral infection voids as a critical barrier to systemic oncolytic virus efficacy. Mol Ther Oncolytics 2014; 1:14005 [View Article][PubMed]
     [Google Scholar]
  146. Eisenstein S, Coakley BA, Briley-Saebo K, Ma G, Chen HM et al. Myeloid-derived suppressor cells as a vehicle for tumor-specific oncolytic viral therapy. Cancer Res 2013; 73:5003–5015 [View Article][PubMed]
     [Google Scholar]
  147. Rommelfanger DM, Offord CP, Dev J, Bajzer Z, Vile RG et al. Dynamics of melanoma tumor therapy with vesicular stomatitis virus: explaining the variability in outcomes using mathematical modeling. Gene Ther 2012; 19:543–549 [View Article][PubMed]
     [Google Scholar]
  148. Le Bœuf F, Batenchuk C, Vähä-Koskela M, Breton S, Roy D et al. Model-based rational design of an oncolytic virus with improved therapeutic potential. Nat Commun 2013; 4:4 [View Article][PubMed]
     [Google Scholar]
  149. de Rioja VL, Isern N, Fort J. A mathematical approach to virus therapy of glioblastomas. Biol Direct 2016; 11:1 [View Article][PubMed]
     [Google Scholar]
  150. Velazquez-Salinas L, Naik S, Pauszek SJ, Peng KW, Russell SJ et al. Oncolytic Recombinant Vesicular Stomatitis Virus (VSV) is nonpathogenic and nontransmissible in pigs, a natural host of VSV. Hum Gene Ther Clin Dev 2017; 28:108–115 [View Article][PubMed]
     [Google Scholar]
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Recent advances in vesicular stomatitis virus-based oncolytic virotherapy: a 5-year update
J. Gen. Virol. 98, 2895 (2017); https://doi.org/10.1099/jgv.0.000980
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