Vesicular stomatitis virus variants selectively infect and kill human melanomas but not normal melanocytes

Journal of Virology

Volumn 87, Issue 12, 2013, Pages 6644-6659

  Wollmann, Guido ^a   Davis, John N ^a   Bosenberg, Marcus W ^a   van den Pol, Anthony N ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; B RAF KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; ONCOLYTIC VIRUS; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAF GENE; CDKN2A GENE; CELL FUNCTION; CODON; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG EFFECT; DRUG RESPONSE; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERFERON STIMULATED GENE; MALIGNANT TRANSFORMATION; MELANOCYTE; MELANOMA; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NRAS GENE; NUCLEOTIDE SEQUENCE; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PTEN GENE; RNA SEQUENCE; SEQUENCE ANALYSIS; VESICULAR STOMATITIS VIRUS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS INFECTION; VIRUS MUTATION; VIRUS RECOMBINANT; VIRUS REPLICATION;

ANIMALS; CELL LINE, TUMOR; HUMANS; MELANOCYTES; MELANOMA; MICE; MICE, SCID; MUTATION; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PROTO-ONCOGENE PROTEINS B-RAF; TRANSPLANTATION, HETEROLOGOUS; VESICULAR STOMATITIS INDIANA VIRUS; VIRUS REPLICATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS; VESICULAR STOMATITIS VIRUS;

EID: 84878607022     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03311-12     Document Type: Article

References (68)

1. Mocellin S, Pasquali S, Rossi CR, Nitti D. 2010. Interferon alpha adjuvant therapy in patients with high-risk melanoma: a systematic review and meta-analysis. J. Natl. Cancer Inst. 102:493-501.
2. Lee B, Mukhi N, Liu D. 2012. Current management and novel agents for malignant melanoma. J. Hematol. Oncol. 5:3. doi:10.1186/1756-8722-5-3.
3. Carlino MS, Fogarty GB, Long GV. 2012. Treatment of melanoma brain metastases: a new paradigm. Cancer J. 18:208-212.
4. Sloan AE, Nock CJ, Einstein DB. 2009. Diagnosis and treatment of melanoma brain metastasis: a literature review. Cancer Control 16:248-255.
5. Trinh VA, Hwu WJ. 2012. Ipilimumab in the treatment of melanoma. Expert Opin. Biol. Ther. 12:773-782.
6. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O'Dwyer PJ, Lee RJ, Grippo JF, Nolop K, Chapman PB. 2010. Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med. 363:809-819.
7. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363:711-723.
8. Dummer R, Flaherty KT. 2012. Resistance patterns with tyrosine kinase inhibitors in melanoma: new insights. Curr. Opin. Oncol. 24:150-154.
9. Flaherty KT, Hodi FS, Fisher DE. 2012. From genes to drugs: targeted strategies for melanoma. Nat. Rev. Cancer 12:349-361.
10. Swick JM, Maize JC, Sr. 2012. Molecular biology of melanoma. J. Am. Acad. Dermatol. 67:1049-1054.
11. Au GG, Beagley LG, Haley ES, Barry RD, Shafren DR. 2011. Oncolysis of malignant human melanoma tumors by Coxsackieviruses A13, A15 and A18. Virol. J. 8:22.
12. Donnelly OG, Errington-Mais F, Steele L, Hadac E, Jennings V, Scott K, Peach H, Phillips RM, Bond J, Pandha H, Harrington K, Vile R, Russell S, Selby P, Melcher AA. 2013. Measles virus causes immunogenic cell death in human melanoma. Gene Ther. 20:7-15.
13. Eberle J, Fecker LF, Hossini AM, Kurbanov BM, Fechner H. 2008. Apoptosis pathways and oncolytic adenoviral vectors: promising targets and tools to overcome therapy resistance of malignant melanoma. Exp. Dermatol. 17:1-11.
14. Hwang TH, Moon A, Burke J, Ribas A, Stephenson J, Breitbach CJ, Daneshmand M, De Silva N, Parato K, Diallo JS, Lee YS, Liu TC, Bell JC, Kirn DH. 2011. A mechanistic proof-of-concept clinical trial with JX-594, a targeted multi-mechanistic oncolytic poxvirus, in patients with metastatic melanoma. Mol. Ther. 19:1913-1922.
15. MacKie RM, Stewart B, Brown SM. 2001. Intralesional injection of herpes simplex virus 1716 in metastatic melanoma. Lancet 357:525-526.
16. Moehler M, Sieben M, Roth S, Springsguth F, Leuchs B, Zeidler M, Dinsart C, Rommelaere J, Galle PR. 2011. Activation of the human immune system by chemotherapeutic or targeted agents combined with the oncolytic parvovirus H-1. BMC Cancer 11:464. doi:10.1186/1471-2407-11-464.
17. Muster T, Rajtarova J, Sachet M, Unger H, Fleischhacker R, Romirer I, Grassauer A, Url A, Garcia-Sastre A, Wolff K, Pehamberger H, Bergmann M. 2004. Interferon resistance promotes oncolysis by influenza virus NS1-deletion mutants. Int. J. Cancer 110:15-21.
18. Nettelbeck DM, Rivera AA, Balague C, Alemany R, Curiel DT. 2002. Novel oncolytic adenoviruses targeted to melanoma: specific viral replication and cytolysis by expression of E1A mutants from the tyrosinase enhancer/ promoter. Cancer Res. 62:4663-4670.
19. Shmulevitz M, Gujar SA, Ahn DG, Mohamed A, Lee PW. 2012. Reovirus variants with mutations in S1 and L2 genome segments exhibit enhanced virion infectivity and superior oncolysis. J. Virol. 86:7403-7413.
20. Thomas DL, Doty R, Tosic V, Liu J, Kranz DM, McFadden G, Macneill AL, Roy EJ. 2011. Myxoma virus combined with rapamycin treatment enhances adoptive T cell therapy for murine melanoma brain tumors. Cancer Immunol. Immunother. 60:1461-1472.
21. Zamarin D, Vigil A, Kelly K, Garcia-Sastre A, Fong Y. 2009. Genetically engineered Newcastle disease virus for malignant melanoma therapy. Gene Ther. 16:796-804.
22. Stojdl DF, Lichty BD, BRtenOever Paterson JM, Power AT, Knowles S, Marius R, Reynard J, Poliquin L, Atkins H, Brown EG, Durbin RK, Durbin JE, Hiscott J, Bell JC. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
23. Bridle BW, Stephenson KB, Boudreau JE, Koshy S, Kazdhan N, Pullenayegum E, Brunelliere J, Bramson JL, Lichty BD, Wan Y. 2010. Potentiating cancer immunotherapy using an oncolytic virus. Mol. Ther. 18:1430-1439.
24. Leveille S, Samuel S, Goulet ML, Hiscott J. 2011. Enhancing VSV oncolytic activity with an improved cytosine deaminase suicide gene strategy. Cancer Gene Ther. 18:435-443.
25. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J, Melcher A, Vile R. 2011. VSV oncolytic virotherapy in the B16 model depends upon intact MyD88 signaling. Mol. Ther. 19:150-158.
26. Leveille S, Goulet ML, Lichty BD, Hiscott J. 2011. Vesicular stomatitis virus oncolytic treatment interferes with tumor-associated dendritic cell functions and abrogates tumor antigen presentation. J. Virol. 85:12160-12169.
27. Ozduman K, Wollmann G, Piepmeier JM, van den Pol AN. 2008. Systemic vesicular stomatitis virus selectively destroys multifocal glioma and metastatic carcinoma in brain. J. Neurosci. 28:1882-1893.
28. Balachandran S, Barber GN. 2000. Vesicular stomatitis virus (VSV) therapy of tumors. IUBMB Life 50:135-138.
29. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N, Bell JC. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821-825.
30. Wong LH, Krauer KG, Hatzinisiriou I, Estcourt MJ, Hersey P, Tam ND, Edmondson S, Devenish RJ, Ralph SJ. 1997. Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3gamma. J. Biol. Chem. 272:28779-28785.
31. Clarke DK, Nasar F, Lee M, Johnson JE, Wright K, Calderon P, Guo M, Natuk R, Cooper D, Hendry RM, Udem SA. 2007. Synergistic attenuation of vesicular stomatitis virus by combination of specific G gene truncations and N gene translocations. J. Virol. 81:2056-2064.
32. Johnson JE, Nasar F, Coleman JW, Price RE, Javadian A, Draper K, Lee M, Reilly PA, Clarke DK, Hendry RM, Udem SA. 2007. Neurovirulence properties of recombinant vesicular stomatitis virus vectors in nonhuman primates. Virology 360:36-49.
33. van den Pol AN, Davis JN. 2013. Highly attenuated recombinant vesicular stomatitis virus VSV-12=GFP displays immunogenic and oncolytic activity. J. Virol. 87:1019-1034.
34. Wollmann G, Rogulin V, Simon I, Rose JK, van den Pol AN. 2010. Some attenuated variants of vesicular stomatitis virus show enhanced oncolytic activity against human glioblastoma cells relative to normal brain cells. J. Virol. 84:1563-1573.
35. Wollmann G, Tattersall P, van den Pol AN. 2005. Targeting human glioblastoma cells: comparison of nine viruses with oncolytic potential. J. Virol. 79:6005-6022.
36. Paglino JC, van den Pol AN. 2011. Vesicular stomatitis virus has extensive oncolytic activity against human sarcomas: rare resistance is overcome by blocking interferon pathways. J. Virol. 85:9346-9358.
37. Cheng E, Trombetta SE, Kovacs D, Beech RD, Ariyan S, Reyes-Mugica M, McNiff JM, Narayan D, Kluger HM, Picardo M, Halaban R. 2006. Rab33A: characterization, expression, and suppression by epigenetic modification. J. Invest. Dermatol. 126:2257-2271.
38. Tworkoski K, Singhal G, Szpakowski S, Zito CI, Bacchiocchi A, Muthusamy V, Bosenberg M, Krauthammer M, Halaban R, Stern DF. 2011. Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol. Cancer Res. 9:801-812.
39. Damsky WE, Curley DP, Santhanakrishnan M, Rosenbaum LE, Platt JT, Gould Rothberg BE, Taketo MM, Dankort D, Rimm DL, McMahon M, Bosenberg M. 2011. beta-catenin signaling controls metastasis in Brafactivated Pten-deficient melanomas. Cancer Cell 20:741-754.
40. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE, Jr, You MJ, DePinho RA, McMahon M, Bosenberg M. 2009. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 41:544-552.
41. Held MA, Curley DP, Dankort D, McMahon M, Muthusamy V, Bosenberg MW. 2010. Characterization of melanoma cells capable of propagating tumors from a single cell. Cancer Res. 70:388-397.
42. Publicover J, Ramsburg E, Robek M, Rose JK. 2006. Rapid pathogenesis induced by a vesicular stomatitis virus matrix protein mutant: viral pathogenesis is linked to induction of tumor necrosis factor alpha. J. Virol. 80:7028-7036.
43. Schnell MJ, Buonocore L, Whitt MA, Rose JK. 1996. The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. J. Virol. 70:2318-2323.
44. Dalton KP, Rose JK. 2001. Vesicular stomatitis virus glycoprotein containing the entire green fluorescent protein on its cytoplasmic domain is incorporated efficiently into virus particles. Virology 279:414-421.
45. Lawson ND, Stillman EA, Whitt MA, Rose JK. 1995. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. U. S. A. 92:4477-4481.
46. Whitt MA. 2010. Generation of VSV pseudotypes using recombinant DeltaG-VSV for studies on virus entry, identification of entry inhibitors, and immune responses to vaccines. J. Virol. Methods 169:365-374.
47. Wollmann G, Robek MD, van den Pol AN. 2007. Variable deficiencies in the interferon response enhance susceptibility to vesicular stomatitis virus oncolytic actions in glioblastoma cells but not in normal human glial cells. J. Virol. 81:1479-1491.
48. Kirkwood JM, Manola J, Ibrahim J, Sondak V, Ernstoff MS, Rao U. 2004. A pooled analysis of eastern cooperative oncology group and intergroup trials of adjuvant high-dose interferon for melanoma. Clin. Cancer Res. 10:1670-1677.
49. Haller O, Kochs G, Weber F. 2007. Interferon, Mx, and viral countermeasures. Cytokine Growth Factor Rev. 18:425-433.
50. Staeheli P, Pavlovic J. 1991. Inhibition of vesicular stomatitis virus mRNA synthesis by human MxA protein. J. Virol. 65:4498-4501.
51. Diaz RM, Galivo F, Kottke T, Wongthida P, Qiao J, Thompson J, Valdes M, Barber G, Vile RG. 2007. Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res. 67:2840-2848.
52. Obuchi M, Fernandez M, Barber GN. 2003. Development of recombinant vesicular stomatitis viruses that exploit defects in host defense to augment specific oncolytic activity. J. Virol. 77:8843-8856.
53. Fernandez M, Porosnicu M, Markovic D, Barber GN. 2002. Genetically engineered vesicular stomatitis virus in gene therapy: application for treatment of malignant disease. J. Virol. 76:895-904.
54. Galivo F, Diaz RM, Wongthida P, Thompson J, Kottke T, Barber G, Melcher A, Vile R. 2010. Single-cycle viral gene expression, rather than progressive replication and oncolysis, is required for VSV therapy of B16 melanoma. Gene Ther. 17:158-170.
55. Wongthida P, Diaz RM, Galivo F, Kottke T, Thompson J, Pulido J, Pavelko K, Pease L, Melcher A, Vile R. 2010. Type III IFN interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immunecompetent mouse models of cancer. Cancer Res. 70:4539-4549.
56. Blackham AU, Northrup SA, Willingham M, D'Agostino RB, Jr, Lyles DS, Stewart JH, 4th. 2013. Variation in susceptibility of human malignant melanomas to oncolytic vesicular stomatitis virus. Surgery 153:333-343.
57. Gaddy DF, Lyles DS. 2005. Vesicular stomatitis viruses expressing wildtype or mutant M proteins activate apoptosis through distinct pathways. J. Virol. 79:4170-4179.
58. Barber GN. 2005. VSV-tumor selective replication and protein translation. Oncogene 24:7710-7719.
59. Ferrantini M, Capone I, Belardelli F. 2007. Interferon-alpha and cancer: mechanisms of action and new perspectives of clinical use. Biochimie 89:884-893.
60. Kalvakolanu DV. 2004. The GRIMs: a new interface between cell death regulation and interferon/retinoid induced growth suppression. Cytokine Growth Factor Rev. 15:169-194.
61. Davar D, Tarhini AA, Kirkwood JM. 2012. Adjuvant therapy for melanoma. Cancer J. 18:192-202.
62. Conzelmann KK. 2005. Transcriptional activation of alpha/beta interferon genes: interference by nonsegmented negative-strand RNA viruses. J. Virol. 79:5241-5248.
63. Ebert O, Shinozaki K, Huang TG, Savontaus MJ, Garcia-Sastre A, Woo SL. 2003. Oncolytic vesicular stomatitis virus for treatment of orthotopic hepatocellular carcinoma in immune-competent rats. Cancer Res. 63:3605-3611.
64. Rose JK, Whitt MA. 2001. Rhabdoviridae: the viruses and their replication, p 1221-1244. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 4th ed. Lippincott, Williams and Wilkins, Philadelphia, PA.
65. Banerjee AK, Barik S. 1992. Gene expression of vesicular stomatitis virus genome RNA. Virology 188:417-428.
66. Rommelfanger DM, Wongthida P, Diaz RM, Kaluza KM, Thompson JM, Kottke TJ, Vile RG. 2012. Systemic combination virotherapy for melanoma with tumor antigen-expressing vesicular stomatitis virus and adoptive T-cell transfer. Cancer Res. 72:4753-4764.
67. Lun X, Senger DL, Alain T, Oprea A, Parato K, Stojdl D, Lichty B, Power A, Johnston RN, Hamilton M, Parney I, Bell JC, Forsyth PA. 2006. Effects of intravenously administered recombinant vesicular stomatitis virus (VSV(deltaM51)) on multifocal and invasive gliomas. J. Natl. Cancer Inst. 98:1546-1557.
68. Ozduman K, Wollmann G, Ahmadi SA, van den Pol AN. 2009. Peripheral immunization blocks lethal actions of vesicular stomatitis virus within the brain. J. Virol. 83:11540-11549.