Vesicular stomatitis virus as an oncolytic agent against pancreatic ductal adenocarcinoma

Journal of Virology

Volumn 86, Issue 6, 2012, Pages 3073-3087

  Murphy, Andrea M ^a   Besmer, Dahlia M ^a   Moerdyk Schauwecker, Megan ^a   Moestl, Natascha ^a   Ornelles, David A ^b   Mukherjee, Pinku ^a   Grdzelishvili, Valery Z ^a  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; ONCOLYTIC VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER CELL DESTRUCTION; CANCER INHIBITION; CANCER RESISTANCE; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; HUMAN; HUMAN ADENOVIRUS; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; OPEN READING FRAME; PANCREAS CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SENDAI VIRUS; VESICULAR STOMATITIS VIRUS; VIRUS REPLICATION;

ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; HUMANS; INTERFERON TYPE I; MALE; MICE; MICE, NUDE; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; PANCREATIC NEOPLASMS; VESICULAR STOMATITIS INDIANA VIRUS;

MUS; RESPIRATORY SYNCYTIAL VIRUS; SENDAI VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 84857966784     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05640-11     Document Type: Article

References (76)

1. Ahmed M, Cramer SD, Lyles DS. 2004. Sensitivity of prostate tumors to wild type and M protein mutant vesicular stomatitis viruses. Virology 330:34-49.
2. Ahmed M, Marino TR, Puckett S, Kock ND, Lyles DS. 2008. Immune response in the absence of neurovirulence in mice infected withMprotein mutant vesicular stomatitis virus. J. Virol. 82:9273-9277.
3. Ahmed M, Puckett S, Lyles DS. 2010. Susceptibility of breast cancer cells to an oncolytic matrix (M) protein mutant of vesicular stomatitis virus. Cancer Gene Ther. 17:883- 892.
4. Altomonte J, et al. 2009. Enhanced oncolytic potency of vesicular stomatitis virus through vector-mediated inhibition of NK and NKT cells. Cancer Gene Ther. 16:266 -278.
5. Ausubel LJ, et al. 2011. Current good manufacturing practice production of an oncolytic recombinant vesicular stomatitis viral vector for cancer treatment. Hum. Gene Ther. 22:489-497.
6. Barber GN. 2004. Vesicular stomatitis virus as an oncolytic vector. Viral Immunol. 17:516 -527.
7. Barber GN. 2005. VSV-tumor selective replication and protein translation. Oncogene 24:7710 -7719.
8. Bischoff JR, et al. 1996. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274:373-376.
9. Breitbach CJ, Reid T, Burke J, Bell JC, Kirn DH. 2010. Navigating the clinical development landscape for oncolytic viruses and other cancer therapeutics: no shortcuts on the road to approval. Cytokine Growth Factor Rev. 21:85- 89.
10. Cary ZD, Willingham MC, Lyles DS. 2011. Oncolytic vesicular stomatitis virus induces apoptosis in U87 glioblastoma cells by a type II death receptor mechanism and induces cell death and tumor clearance in vivo. J. Virol. 85:5708 -5717.
11. Chang G, et al. 2010. Enhanced oncolytic activity of vesicular stomatitis virus encoding SV5-F protein against prostate cancer. J. Urol. 183:1611- 1618.
12. Crompton AM, Kirn DH. 2007. From ONYX-015 to armed vaccinia viruses: the education and evolution of oncolytic virus development. Curr. Cancer Drug Targets 7:133-139.
13. Ebert O, Harbaran S, Shinozaki K, Woo SL. 2005. Systemic therapy of experimental breast cancer metastases by mutant vesicular stomatitis virus in immune-competent mice. Cancer Gene Ther. 12:350 -358.
14. Echchgadda I, et al. 2011. Oncolytic targeting of androgen-sensitive prostate tumor by the respiratory syncytial virus (RSV): consequences of deficient interferon-dependent antiviral defense. BMC Cancer 28:43.
15. Echchgadda I, et al. 2009. Anticancer oncolytic activity of respiratory syncytial virus. Cancer Gene Ther. 16:923-935.
16. Edge RE, et al. 2008. A let-7 MicroRNA-sensitive vesicular stomatitis virus demonstrates tumor-specific replication. Mol. Ther. 16:1437-1443.
17. Eisenberg DP, et al. 2010. Hyperthermia potentiates oncolytic herpes viral killing of pancreatic cancer through a heat shock protein pathway. Surgery 148:325-334.
18. Etoh T, et al. 2003. Oncolytic viral therapy for human pancreatic cancer cells by reovirus. Clin. Cancer Res. 9:1218 -1223.
19. Farrow B, Albo D, Berger DH. 2008. The role of the tumor microenvironment in the progression of pancreatic cancer. J. Surg. Res. 149:319- 328.
20. 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.
21. Furukawa T, et al. 1996. Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am. J. Pathol. 148:1763-1770.
22. Gaddy DF, Lyles DS. 2007. Oncolytic vesicular stomatitis virus induces apoptosis via signaling through PKR, Fas, and Daxx. J. Virol. 81:2792- 2804.
23. Gaddy DF, Lyles DS. 2005. Vesicular stomatitis viruses expressing wildtype or mutantMproteins activate apoptosis through distinct pathways. J. Virol. 79:4170-4179.
24. Galivo F, et al. 2010. Interference of CD40L-mediated tumor immunotherapy by oncolytic VSV. Hum. Gene Ther. 21:439-450.
25. Goel A, et al. 2007. Radioiodide imaging and radiovirotherapy of multiple myeloma using VSV(Delta51)-NIS, an attenuated vesicular stomatitis virus encoding the sodium iodide symporter gene. Blood 110:2342-2350.
26. Hallak LK, Collins PL, Knudson W, Peeples ME. 2000. Iduronic acidcontaining glycosaminoglycans on target cells are required for efficient respiratory syncytial virus infection. Virology 271:264 -275.
27. Hamacher R, Schmid RM, Saur D, Schneider G. 2008. Apoptotic pathways in pancreatic ductal adenocarcinoma. Mol. Cancer 7:64.
28. He X, et al. 2009. E1B-55kD-deleted oncolytic adenovirus armed with canstatin gene yields an enhanced anti-tumor efficacy on pancreatic cancer. Cancer Lett. 285:89 -98.
29. Himeno Y, et al. 2005. Efficacy of oncolytic reovirus against liver metastasis from pancreatic cancer in immunocompetent models. Int. J. Oncol. 27:901-906.
30. Hirano S, et al. 2009. Reovirus inhibits the peritoneal dissemination of pancreatic cancer cells in an immunocompetent animal model. Oncol. Rep. 21:1381-1384.
31. Huang TG, Savontaus MJ, Shinozaki K, Sauter BV, Woo SL. 2003. Telomerase-dependent oncolytic adenovirus for cancer treatment. Gene Ther. 10:1241-1247.
32. Huang TG, Ebert O, Shinozaki K, Garcia-Sastre A, Woo SL. 2003. Oncolysis of hepatic metastasis of colorectal cancer by recombinant vesicular stomatitis virus in immune-competent mice. Mol. Ther. 8:434-440.
33. Huch M, José GAA, González JR, Alemany R, Fillat C. 2009. Urokinasetype plasminogen activator receptor transcriptionally controlled adenoviruses eradicate pancreatic tumors and liver metastasis in mouse models. Neoplasia 11:518 -528.
34. Iwamura T, Katsuki T, Ide K. 1987. Establishment and characterization of a human pancreatic cancer cell line (SUIT-2) producing carcinoembryonic antigen and carbohydrate antigen 19-9. Jpn. J. Cancer Res. 78:54-62.
35. Kasuya H, Takeda S, Nomoto S, Nakao A. 2005. The potential of oncolytic virus therapy for pancreatic cancer. Cancer Gene Ther. 12:725- 736.
36. Kasuya H, et al. 2007. Suitability of a US3-inactivated HSV mutant (L1BR1) as an oncolytic virus for pancreatic cancer therapy. Cancer Gene Ther. 14:533-542.
37. Kelly EJ, Nace R, Barber GN, Russell SJ. 2010. Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J. Virol. 84: 1550-1562.
38. Kinoh H, Inoue M. 2008. New cancer therapy using geneticallyengineered oncolytic Sendai virus vector. Front. Biosci. 13:2327-2334.
39. Kinoh H, et al. 2004. Generation of a recombinant Sendai virus that is selectively activated and lyses human tumor cells expressing matrix metalloproteinases. Gene Ther. 11:1137-1145.
40. Komaru A, et al. 2009. Sustained and NK/CD4+ T cell-dependent efficient prevention of lung metastasis induced by dendritic cells harboring recombinant Sendai virus. J. Immunol. 183:4211- 4219.
41. Kuhlmann KF, Gouma DJ, Wesseling JG. 2008. Adenoviral gene therapy for pancreatic cancer: where do we stand? Dig. Surg. 25:278 -292.
42. 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.
43. Le Boeuf F, et al. 2010. Synergistic interaction between oncolytic viruses augments tumor killing. Mol. Ther. 18:888-895.
44. Lichty BD, Power AT, Stojdl DF, Bell JC. 2004. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol. Med. 10:210 -216.
45. Lindsay TH, et al. 2005. Pancreatic cancer pain and its correlation with changes in tumor vasculature, macrophage infiltration, neuronal innervation, body weight and disease progression. Pain 119:233-246.
46. Linge C, Gewert D, Rossmann C, Bishop JA, Crowe JS. 1995. Interferon system defects in human malignant melanoma. Cancer Res. 55:4099- 4104.
47. Lyles D, Rupprecht CE. 2007. Rhabdoviridae, p 1363-1408. In Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
48. Matin SF, et al. 2001. Impaired alpha-interferon signaling in transitional cell carcinoma: lack of p48 expression in 5637 cells. Cancer Res. 61:2261- 2266.
49. Moussavi M, et al. 2010. Oncolysis of prostate cancers induced by vesicular stomatitis virus in PTEN knockout mice. Cancer Res. 70:1367-1376.
50. Moyer SA, Baker SC, Lessard JL. 1986. Tubulin: a factor necessary for the synthesis of both Sendai virus and vesicular stomatitis virus RNAs. Proc. Natl. Acad. Sci. U. S. A. 83:5405-5409.
51. Naik S, Russell SJ. 2009. Engineering oncolytic viruses to exploit tumor specific defects in innate immune signaling pathways. Expert Opin. Biol. Ther. 9:1163-1176.
52. Nakao A, et al. 2007. Clinical experiment of mutant herpes simplex virus HF10 therapy for cancer. Curr. Cancer Drug Targets 7:169 -174.
53. 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.
54. Okabe T, Yamaguchi N, Ohsawa N. 1983. Establishment and characterization of a carcinoembryonic antigen (CEA)-producing cell line from a human carcinoma of the exocrine pancreas. Cancer 51:662- 668.
55. Ottolino-Perry K, Diallo JS, Lichty BD, Bell JC, McCart JA. 2010. Intelligent design: combination therapy with oncolytic viruses. Mol. Ther. 18:251-263.
56. 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.
57. Pfeffer LM, et al. 1996. Human renal cancers resistant to IFN=s antiproliferative action exhibit sensitivity to IFN=s gene-inducing and antiviral actions. J. Urol. 156:1867-1871.
58. Quiroz E, Moreno N, Peralta PH, Tesh RB. 1988. A human case of encephalitis associated with vesicular stomatitis virus (Indiana serotype) infection. Am. J. Trop. Med. Hyg. 39:312-314.
59. Russell SJ, Peng KW. 2007. Viruses as anticancer drugs. Trends Pharmacol. Sci. 28:326 -333.
60. Saloura V, et al. 2010. Evaluation of an attenuated vesicular stomatitis virus vector expressing interferon-beta for use in malignant pleural mesothelioma: heterogeneity in interferon responsiveness defines potential efficacy. Hum. Gene Ther. 21:51- 64.
61. Sarinella F, Calistri A, Sette P, Palu G, Parolin C. 2006. Oncolysis of pancreatic tumour cells by a gamma 34.5-deleted HSV-1 does not rely upon Ras-activation, but on the PI 3-kinase pathway. Gene Ther. 13: 1080-1087.
62. Sharif-Askari E, et al. 2007. Bax-dependent mitochondrial membrane permeabilization enhances IRF3-mediated innate immune response during VSV infection. Virology 365:20 -33.
63. Shi W, et al. 2009. Antitumor and antimetastatic activities of vesicular stomatitis virus matrix protein in a murine model of breast cancer. J. Mol. Med. 87:493-506.
64. Shinozaki K, Ebert O, Woo SL. 2005. Treatment of multi-focal colorectal carcinoma metastatic to the liver of immune-competent and syngeneic rats by hepatic artery infusion of oncolytic vesicular stomatitis virus. Int. J. Cancer 114:659-664.
65. Stathis A, Moore MJ. 2010. Advanced pancreatic carcinoma: current treatment and future challenges. Nat. Rev. Clin. Oncol. 7:163-172.
66. Stojdl DF, et al. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821- 825.
67. Stojdl DF, et al. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
68. Sun WH, et al. 1998. Interferon-alpha resistance in a cutaneous T-cell lymphoma cell line is associated with lack of STAT1 expression. Blood 91:570 -576.
69. Vähä-Koskela MJ, Heikkilä JE, Hinkkanen AE. 2007. Oncolytic viruses in cancer therapy. Cancer Lett. 254:178 -216.
70. von Messling V, Cattaneo R. 2004. Toward novel vaccines and therapies based on negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:281-312.
71. Watanabe I, et al. 2008. Effects of tumor selective replication-competent herpes viruses in combination with gemcitabine on pancreatic cancer. Cancer Chemother. Pharmacol. 61:875- 882.
72. Wiegand MA, Bossow S, Schlecht S, Neubert WJ. 2007. De novo synthesis of N and P proteins as a key step in Sendai virus gene expression. J. Virol. 81:13835-13844.
73. Wollmann G, Simon RVI, 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.
74. Wong LH, et al. 1997. Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3gamma. J. Biol. Chem. 272:28779 -28785.
75. Wu L, et al. 2008. rVSV(M Delta 51)-M3 is an effective and safe oncolytic virus for cancer therapy. Hum. Gene Ther. 19:635- 647.
76. Yonemitsu Y, Kinoh UYH, Hasegawa M. 2008. Immunostimulatory virotherapy using recombinant Sendai virus as a new cancer therapeutic regimen. Front. Biosci. 13:4953- 4959.