Expressing human interleukin-15 from oncolytic vesicular stomatitis virus improves survival in a murine metastatic colon adenocarcinoma model through the enhancement of anti-tumor immunity

Cancer Gene Therapy

Volumn 19, Issue 4, 2012, Pages 238-246

  Stephenson, K B ^a   Barra, N G ^a   Davies, E ^a   Ashkar, A A ^a   Lichty, B D ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

colon cancer; IL 15; oncolytic virus; VSV

Indexed keywords

INTERLEUKIN 15; ONCOLYTIC VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; CANCER SURVIVAL; COLON ADENOCARCINOMA; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TRANSGENE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VESICULAR STOMATITIS VIRUS;

ADENOCARCINOMA; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; COLONIC NEOPLASMS; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GENE ORDER; GENE THERAPY; GENETIC VECTORS; HUMANS; INTERLEUKIN-15; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; NEOPLASM METASTASIS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; TRANSDUCTION, GENETIC; VESICULAR STOMATITIS INDIANA VIRUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE; VESICULAR STOMATITIS VIRUS;

EID: 84858702868     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2011.81     Document Type: Article

References (38)

1. Cattaneo R, Miest T, Shashkova EV, Barry MA. Reprogrammed viruses as cancer therapeutics: targeted, armed and shielded. Nat Rev Microbiol 2008; 6: 529-540. (Pubitemid 351850977)
2. Breitbach CJ, Reid T, Burke J, Bell JC, Kirn DH. Navigating the clinical development landscape for oncolytic viruses and other cancer therapeutics: no shortcuts on the road to approval. Cytokine Growth Factor Rev 2010; 21: 85-89.
3. Parato KA, Senger D, Forsyth PAJ, Bell JC. Recent progress in the battle between oncolytic viruses and tumours. Nat Rev Cancer 2005; 5: 965-976. (Pubitemid 41766784)
4. Prestwich RJ, Harrington KJ, Pandha HS, Vile RG, Melcher AA, Errington F. Oncolytic viruses: a novel form of immunotherapy. Expert Rev Anticancer Ther 2008; 8: 1581-1588.
5. Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N et al. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med 2000; 6: 821-825. (Pubitemid 30469434)
6. Stojdl D, Lichty B, tenOever B, Paterson J, Power A, Knowles S 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. (Pubitemid 37329791)
7. Lichty B, Power A, Stojdl D, Bell J. Vesicular stomatitis virus: re-inventing the bullet. Trends Mol Med 2004; 10: 210-216.
8. von Kobbe C, van Deursen J, Rodrigues J, Sitterlin D, Bachi A, Wu X et al. Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol Cell 2000; 6: 1243-1252.
9. Galivo F, Diaz RM, Thanarajasingam U, Jevremovic D, Wongthida P, Thompson J et al. Interference of CD40L-mediated tumor immunotherapy by oncolytic vesicular stomatitis virus. Hum Gene Ther 2010; 21: 439-450.
10. Lun X, Senger DL, Alain T, Oprea A, Parato K, Stojdl D 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. (Pubitemid 44680906)
11. Ebert O, Harbaran S, Shinozaki K, Woo S. Systemic therapy of experimental breast cancer metastases by mutant vesicular stomatitis virus in immune-competent mice. Cancer Gene Ther 2005; 12: 350-358. (Pubitemid 40411194)
12. Waldmann TA, Tagaya Y. The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu Rev Immunol 1999; 17: 19-49. (Pubitemid 29241118)
13. Carson WE, Giri JG, Lindemann MJ, Linett ML, Ahdieh M, Paxton R et al. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med 1994; 180: 1395-1403. (Pubitemid 24289613)
14. Ohteki T. Critical role for IL-15 in innate immunity. Curr Mol Med 2002; 2: 371-380. (Pubitemid 35452885)
15. Kokaji AI, Hockley DL, Kane KP. IL-15 transpresentation augments CD8+ T cell activation and is required for optimal recall responses by central memory CD8+ T cells. J Immunol 2008; 180: 4391-4401.
16. Teague RM, Sather BD, Sacks JA, Huang MZ, Dossett ML, Morimoto J et al. Interleukin-15 rescues tolerant CD8+ T cells for use in adoptive immunotherapy of established tumors. Nat Med 2006; 12: 335-341. (Pubitemid 43355083)
17. Ugen KE, Kutzler MA, Marrero B, Westover J, Coppola D, Weiner DB et al. Regression of subcutaneous B16 melanoma tumors after intratumoral delivery of an IL-15-expressing plasmid followed by in vivo electroporation. Cancer Gene Ther 2006; 13: 969-974. (Pubitemid 44373797)
18. Dubois S, Patel HJ, Zhang M, Waldmann TA, Müller JR. Preassociation of IL-15 with IL-15R alpha-IgG1-Fc enhances its activity on proliferation of NK and CD8+/ CD44high T cells and its antitumor action. J Immunol 2008; 180: 2099-2106.
19. Wu Z, Xu Y. IL-15R alpha-IgG1-Fc enhances IL-2 and IL-15 anti-tumor action through NK and CD8+ T cells proliferation and activation. J Mol Cell Biol 2010; 2: 217-222.
20. Yiang G-T, Harn H-J, Yu Y-L, Hu S-C, Hung Y-T, Hsieh C-J et al. Immunotherapy: rAAV2 expressing interleukin-15 inhibits HeLa cell tumor growth in mice. J Biomed Sci 2009; 16: 47.
21. Liu J, Wennier S, Reinhard M, Roy E, MacNeill A, McFadden G. Myxoma virus expressing interleukin-15 fails to cause lethal myxomatosis in European rabbits. J Virol 2009; 83: 5933-5938.
22. Marks-Konczalik J, Dubois S, Losi JM, Sabzevari H, Yamada N, Feigenbaum L et al. IL-2-induced activationinduced cell death is inhibited in IL-15 transgenic mice. Proc Natl Acad Sci USA 2000; 97: 11445-11450.
23. Davies E, Reid S, Medina MF, Lichty B, Ashkar AA. IL-15 has innate anti-tumor activity independent of NK and CD8 T cells. J Leukoc Biol 2010; 88: 529-536.
24. Lawson N, Stillman E, Whitt M, Rose J. Recombinant vesicular stomatitis viruses from DNA. Proc Natl Acad Sci USA 1995; 92: 4477-4481.
25. Araki A, Hazama S, Yoshimura K, Yoshino S, Iizuka N, Oka M. Tumor secreting high levels of IL-15 induces specific immunity to low immunogenic colon adenocarcinoma via CD8+ T cells. Int J Mol Med 2004; 14: 571-576.
26. Casares N, Lasarte JJ, de Cerio AL, Sarobe P, Ruiz M, Melero I et al. Immunization with a tumor-associated CTL epitope plus a tumor-related or unrelated Th1 helper peptide elicits protective CTL immunity. Eur J Immunol 2001; 31: 1780-1789. (Pubitemid 32547341)
27. Ramsburg EA, Publicover JM, Coppock D, Rose JK. Requirement for CD4 T cell help in maintenance of memory CD8 T cell responses is epitope dependent. J Immunol 2007; 178: 6350-6358. (Pubitemid 46717419)
28. Bessard A, Solé V, Bouchaud G, Quéméner A, Jacques Y. High antitumor activity of RLI, an interleukin-15 (IL-15)-IL-15 receptor alpha fusion protein, in metastatic melanoma and colorectal cancer. Mol Cancer Therap 2009; 8: 2736-2745.
29. Stoklasek TA, Schluns KS, Lefrançois L. Combined IL-15/IL-15Ralpha immunotherapy maximizes IL-15 activity in vivo. J Immunol 2006; 177: 6072-6080. (Pubitemid 44628822)
30. Smith E, Breznik J, Lichty B. Strategies to enhance viral penetration of solid tumors. Hum Gene Ther 2011; 22: 1053-1060.
31. Miller JM, Bidula SM, Jensen TM, Reiss CS. Vesicular stomatitis virus modified with single chain IL-23 exhibits oncolytic activity against tumor cells in vitro and in vivo. Int J Infereron Cytokine Mediat Res 2010; 2010: 63-72.
32. Shin E, Wanna G, Choi B, Aguila D, Ebert O, Genden E et al. Interleukin-12 expression enhances vesicular stomatitis virus oncolytic therapy in murine squamous cell carcinoma. Laryngoscope 2007; 117: 210-214. (Pubitemid 46207874)
33. Fernandez M, Porosnicu M, Markovic D, Barber GN. Genetically engineered vesicular stomatitis virus in gene therapy: application for treatment of malignant disease. J Virol 2002; 76: 895-904. (Pubitemid 34033386)
34. Willmon CL, Saloura V, Fridlender ZG, Wongthida P, Diaz RM, Thompson J et al. Expression of IFN-beta enhances both efficacy and safety of oncolytic vesicular stomatitis virus for therapy of mesothelioma. Cancer Res 2009; 69: 7713-7720.
35. Sato N, Patel HJ, Waldmann TA, Tagaya Y. The IL-15/IL-15Ralpha on cell surfaces enables sustained IL-15 activity and contributes to the long survival of CD8 memory T cells. Proc Natl Acad Sci USA 2007; 104: 588-593. (Pubitemid 46123069)
36. Tasaki K, Yoshida Y, Miyauchi M, Maeda T, Takenaga K, Kouzu T et al. Transduction of murine colon carcinoma cells with interleukin-15 gene induces antitumor effects in immunocompetent and immunocompromised hosts. Cancer Gene Ther 2000; 7: 255-261. (Pubitemid 30194560)
37. Breitbach CJ, De Silva NS, Falls TJ, Aladl U, Evgin L, Paterson J et al. Targeting tumor vasculature with an oncolytic virus. Mol Ther 2011; 19: 886-894.
38. Breitbach C, Paterson J, Lemay C, Falls T, McGuire A, Parato K et al. Targeted inflammation during oncolytic virus therapy severely compromises tumor blood flow. Mol Ther 2007; 15: 1686-1693. (Pubitemid 47289013)