Semliki forest virus expressing interleukin-12 induces antiviral and antitumoral responses in woodchucks with chronic viral hepatitis and hepatocellular carcinoma

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12266-12278

  Rodriguez Madoz, Juan R ^a   Liu, Katherine H ^b   Quetglas, Jose I ^a   Ruiz Guillen, Marta ^a   Otano, Itziar ^a   Crettaz, Julien ^a   Butler, Scott D ^b   Bellezza, Christine A ^b   Dykes, Nathan L ^b   Tennant, Bud C ^b   Prieto, Jesus ^a   González Aseguinolaza, Gloria ^a   Smerdou, Cristian ^a   Menne, Stephan ^b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; LUCIFERASE; SFV ENHIL 12 VIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; CANCER TRANSPLANTATION; CHRONIC HEPATITIS; CONTROLLED STUDY; CYTOKINE RELEASE; ECHOGRAPHY; FEMALE; HEPATITIS B VIRUS; HEPATITIS VIRUS; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; LIVER CELL CARCINOMA; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REPORTER GENE; SEMLIKI FOREST ALPHAVIRUS; T LYMPHOCYTE; TREATMENT DURATION; TREATMENT RESPONSE; TUMOR GROWTH; TUMOR REGRESSION; TUMOR VOLUME; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIREMIA; WOODCHUCK;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEPATITIS B VACCINES; HEPATITIS B VIRUS, WOODCHUCK; HEPATITIS B, CHRONIC; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-12; LIVER; MALE; MARMOTA; SEMLIKI FOREST VIRUS; TUMOR NECROSIS FACTOR-ALPHA;

HEPATITIS B VIRUS; MARMOTA MONAX; RABBIT FIBROMA VIRUS; RODENTIA; SEMLIKI FOREST VIRUS; WOODCHUCK HEPATITIS VIRUS;

EID: 70450193052     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01597-09     Document Type: Article

References (54)

1. Albert, M. L., B. Sauter, and N. Bhardwaj. 1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392:86-89.
2. Asselin-Paturel, C., N. Lassau, J. M. Guinebretiere, J. Zhang, F. Gay, F. Bex, S. Hallez, J. Leclere, P. Peronneau, F. Mami-Chouaib, and S. Chouaib. 1999. Transfer of the murine interleukin-12 gene in vivo by a Semliki Forest virus vector induces B16 tumor regression through inhibition of tumor blood vessel formation monitored by Doppler ultrasonography. Gene Ther. 6:606-615. (Pubitemid 29192669)
3. Barajas, M., G. Mazzolini, G. Genove, R. Bilbao, I. Narvaiza, V. Schmitz, B. Sangro, I. Melero, C. Qian, and J. Prieto. 2001. Gene therapy of orthotopic hepatocellular carcinoma in rats using adenovirus coding for interleukin 12. Hepatology 33:52-61. (Pubitemid 32016887)
4. Bilbao, R., R. Gerolami, M. P. Bralet, C. Qian, P. L. Tran, B. Tennant, J. Prieto, and C. Brechot. 2000. Transduction efficacy, antitumoral effect, and toxicity of adenovirus-mediated herpes simplex virus thymidine kinase/ganciclovir therapy of hepatocellular carcinoma: the woodchuck animal model. Cancer Gene Ther. 7:657-662. (Pubitemid 30314049)
5. Blondon, H., L. Fritsch, and D. Cherqui. 2004. Two cases of spontaneous regression of multicentric hepatocellular carcinoma after intraperitoneal rupture: possible role of immune mechanisms. Eur. J. Gastroenterol. Hepatol. 16:1355-1359.
6. Casales, E., J. R. Rodriguez-Madoz, M. Ruiz-Guillen, N. Razquin, Y. Cuevas, J. Prieto, and C. Smerdou. 2008. Development of a new noncytopathic Semliki Forest virus vector providing high expression levels and stability. Virology 376:242-251.
7. Chang, C. Y., J. Lee, E. Y. Kim, H. J. Park, C. H. Kwon, J. W. Joh, and S. J. Kim. 2007. Intratumoral delivery of IL-18 naked DNA induces T-cell activation and Th1 response in a mouse hepatic cancer model. BMC Cancer 7:87.
8. Chang, G. C., H. C. Lan, S. H. Juang, Y. C. Wu, H. C. Lee, Y. M. Hung, H. Y. Yang, J. Whang-Peng, and K. J. Liu. 2005. A pilot clinical trial of vaccination with dendritic cells pulsed with autologous tumor cells derived from malignant pleural effusion in patients with late-stage lung carcinoma. Cancer 103:763-771.
9. Chikkanna-Gowda, C. P., B. J. Sheahan, M. N. Fleeton, and G. J. Atkins. 2005. Regression of mouse tumours and inhibition of metastases following administration of a Semliki Forest virus vector with enhanced expression of IL-12. Gene Ther. 12:1253-1263.
10. Colmenero, P., M. Chen, E. Castanos-Velez, P. Liljestrom, and M. Jondal. 2002. Immunotherapy with recombinant SFV-replicons expressing the P815A tumor antigen or IL-12 induces tumor regression. Int. J. Cancer 98:554-560. (Pubitemid 34208556)
11. Cote, P. J., B. E. Korba, R. H. Miller, J. R. Jacob, B. H. Baldwin, W. E. Hornbuckle, R. H. Purcell, B. C. Tennant, and J. L. Gerin. 2000. Effects of age and viral determinants on chronicity as an outcome of experimental woodchuck hepatitis virus infection. Hepatology 31:190-200.
12. Cote, P. J., C. Roneker, K. Cass, F. Schodel, D. Peterson, B. Tennant, F. De Noronha, and J. Gerin. 1993. New enzyme immunoassays for the serologic detection of woodchuck hepatitis virus infection. Viral Immunol. 6:161-169.
13. Crettaz, J., I. Otano, L. Ochoa, A. Benito, A. Paneda, I. Aurrekoetxea, P. Berraondo, J. R. Rodriguez-Madoz, A. Astudillo, F. Kreppel, S. Kochanek, J. Ruiz, S. Menne, J. Prieto, and G. Gonzalez-Aseguinolaza. 2009. Treatment of chronic viral hepatitis in woodchucks by prolonged intrahepatic expression of interleukin-12. J. Virol. 83:2663-2674.
14. Drozdzik, M., C. Qian, X. Xie, D. Peng, R. Bilbao, G. Mazzolini, and J. Prieto. 2000. Combined gene therapy with suicide gene and interleukin-12 is more efficient than therapy with one gene alone in a murine model of hepatocellular carcinoma. J. Hepatol. 32:279-286. (Pubitemid 30093907)
15. Fleeton, M. N., B. J. Sheahan, E. A. Gould, G. J. Atkins, and P. Liljestrom. 1999. Recombinant Semliki Forest virus particles encoding the prME or NS1 proteins of louping ill virus protect mice from lethal challenge. J. Gen. Virol. 80:1189-1198.
16. Guan, M., J. R. Rodriguez-Madoz, P. Alzuguren, C. Gomar, M. G. Kramer, S. Kochanek, J. Prieto, C. Smerdou, and C. Qian. 2006. Increased efficacy and safety in the treatment of experimental liver cancer with a novel adenovirus-alphavirus hybrid vector. Cancer Res. 66:1620-1629. (Pubitemid 43259946)
17. Hashemi, S. M., Z. M. Hassan, S. Soudi, and S. Shahabi. 2008. The effect of vaccination with the lysate of heat-shocked tumor cells on nitric oxide production in BALB/c mice with fibrosarcoma tumor. Cell Biol. Int. 32:835-840.
18. Haussinger, D., and F. Schliess. 2008. Pathogenetic mechanisms of hepatic encephalopathy. Gut 57:1156-1165.
19. Hwang, K. S., W. K. Cho, J. Yoo, Y. R. Seong, B. K. Kim, S. Kim, and D. S. Im. 2004. Adenovirus-mediated interleukin-18 mutant in vivo gene transfer inhibits tumor growth through the induction of T cell immunity and activation of natural killer cell cytotoxicity. Cancer Gene Ther. 11:397-407.
20. Kobayashi, H., S. Dubois, N. Sato, H. Sabzevari, Y. Sakai, T. A. Waldmann, and Y. Tagaya. 2005. Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance. Blood 105:721-727. (Pubitemid 40070758)
21. Lau, W. Y., and E. C. Lai. 2008. Hepatocellular carcinoma: current management and recent advances. Hepatobiliary Pancreat. Dis. Int. 7:237-257.
22. Li, Y., H. Hacker, A. Kopp-Schneider, U. Protzer, and P. Bannasch. 2002. Woodchuck hepatitis virus replication and antigen expression gradually decrease in preneoplastic hepatocellular lineages. J. Hepatol. 37:478-485.
23. Liljestrom, P., and H. Garoff. 1994. Expression of proteins using Semliki Forest virus vectors, p. 16.20.11-16.20.16. In F. M. Ausubel et al. (ed.), Current protocols in molecular biology. Greene Publishing Associates and Wiley Interscience, New York, NY.
24. Liljestrom, P., and H. Garoff. 1991. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Bio/Technology 9:1356-1361.
25. Liu, T. C., T. Hwang, B. H. Park, J. Bell, and D. H. Kirn. 2008. The targeted oncolytic poxvirus JX-594 demonstrates antitumoral, antivascular, and anti-HBV activities in patients with hepatocellular carcinoma. Mol. Ther. 16:1637-1642.
26. Maschke, J., S. Menne, J. R. Jacob, E. Kreuzfelder, B. C. Tennant, M. Roggendorf, and H. Grosse-Wilde. 2001. Thymidine utilization abnormality in proliferating lymphocytes and hepatocytes of the woodchuck. Vet. Immunol. Immunopathol. 78:279-296.
27. Mason, W. S., A. R. Jilbert, and J. Summers. 2005. Clonal expansion of hepatocytes during chronic woodchuck hepatitis virus infection. Proc. Natl. Acad. Sci. USA 102:1139-1144.
28. Menne, S., S. D. Butler, A. L. George, I. A. Tochkov, Y. Zhu, S. Xiong, J. L. Gerin, P. J. Cote, and B. C. Tennant. 2008. Antiviral effect of lamivudine, emtricitabine, adefovir dipivoxil, and tenofovir disoproxil fumarate, adminstered orally alone and in combination, to woodchucks with chronic woodchuck hepatitis virus infection. Antimicrob. Agents Chemother. 52:3617-3632.
29. Menne, S., and P. J. Cote. 2007. The woodchuck as an animal model for pathogenesis and therapy of chronic hepatitis B virus infection. World J. Gastroenterol. 13:104-124.
30. Menne, S., P. J. Cote, S. D. Butler, I. A. Toshkov, J. L. Gerin, and B. C. Tennant. 2007. Immunosuppression reactivates viral replication long after resolution of woodchuck hepatitis virus infection. Hepatology 45:614-622. (Pubitemid 46450612)
31. Menne, S., C. A. Roneker, M. Roggendorf, J. L. Gerin, P. J. Cote, and B. C. Tennant. 2002. Deficiencies in the acute-phase cell-mediated immune response to viral antigens are associated with development of chronic woodchuck hepatitis virus infection following neonatal inoculation. J. Virol. 76:1769-1780. (Pubitemid 34094624)
32. Menne, S., B. C. Tennant, J. L. Gerin, and P. J. Cote. 2007. Chemoimmunotherapy of chronic hepatitis B virus infection in the woodchuck model overcomes immunologic tolerance and restores T-cell responses to pre-S and S regions of the viral envelope protein. J. Virol. 81:10614-10624. (Pubitemid 47463335)
33. Murphy, A. M., M. M. Morris-Downes, B. J. Sheahan, and G. J. Atkins. 2000. Inhibition of human lung carcinoma cell growth by apoptosis induction using Semliki Forest virus recombinant particles. Gene Ther. 7:1477-1482.
34. Popper, H., L. Roth, R. H. Purcell, B. C. Tennant, and J. L. Gerin. 1987. Hepatocarcinogenicity of the woodchuck hepatitis virus. Proc. Natl. Acad. Sci. USA 84:866-870.
35. Putzer, B. M., T. Stiewe, F. Rodicker, O. Schildgen, S. Ruhm, O. Dirsch, M. Fiedler, U. Damen, B. Tennant, C. Scherer, F. L. Graham, and M. Roggendorf. 2001. Large nontransplanted hepatocellular carcinoma in woodchucks: treatment with adenovirus-mediated delivery of interleukin 12/B7.1 genes. J. Natl. Cancer Inst. 93:472-479.
36. Radaeva, S., Y. Li, H. J. Hacker, V. Burger, A. Kopp-Schneider, and P. Bannasch. 2000. Hepadnaviral hepatocarcinogenesis: in situ visualization of viral antigens, cytoplasmic compartmentation, enzymic patterns, and cellular proliferation in preneoplastic hepatocellular lineages in woodchucks. J. Hepatol. 33:580-600. (Pubitemid 30736070)
37. Rodriguez, M. M., S. M. Ryu, C. Qian, M. Geissler, C. Grimm, J. Prieto, H. E. Blum, and L. Mohr. 2008. Immunotherapy of murine hepatocellular carcinoma by alpha-fetoprotein DNA vaccination combined with adenovirus-mediated chemokine and cytokine expression. Hum. Gene Ther. 19:753-759.
38. Rodriguez-Madoz, J. R., J. Prieto, and C. Smerdou. 2007. Biodistribution and tumor infectivity of Semliki Forest virus vectors in mice: effects of re-administration. Mol. Ther. 15:2164-2171.
39. Rodriguez-Madoz, J. R., J. Prieto, and C. Smerdou. 2005. Semliki forest virus vectors engineered to express higher IL-12 levels induce efficient elimination of murine colon adenocarcinomas. Mol. Ther. 12:153-163.
40. Salminen, A., J. M. Wahlberg, M. Lobigs, P. Liljestrom, and H. Garoff. 1992. Membrane fusion process of Semliki Forest virus. II. Cleavage-dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol. 116:349-357.
41. Sangro, B., G. Mazzolini, J. Ruiz, M. Herraiz, J. Quiroga, I. Herrero, A. Benito, J. Larrache, J. Pueyo, J. C. Subtil, C. Olague, J. Sola, B. Sadaba, C. Lacasa, I. Melero, C. Qian, and J. Prieto. 2004. Phase I trial of intratumoral injection of an adenovirus encoding interleukin-12 for advanced digestive tumors. J. Clin. Oncol. 22:1389-1397.
42. Schott, M., J. Feldkamp, D. Schattenberg, T. Krueger, C. Dotzenrath, J. Seissler, and W. A. Scherbaum. 2000. Induction of cellular immunity in a parathyroid carcinoma treated with tumor lysate-pulsed dendritic cells. Eur. J. Endocrinol. 142:300-306.
43. Smerdou, C., and P. Liljestrom. 1999. Two-helper RNA system for production of recombinant Semliki forest virus particles. J. Virol. 73:1092-1098. (Pubitemid 29036760)
44. Smyth, J. W., M. N. Fleeton, B. J. Sheahan, and G. J. Atkins. 2005. Treatment of rapidly growing K-BALB and CT26 mouse tumours using Semliki Forest virus and its derived vector. Gene Ther. 12:147-159.
45. Subleski, J. J., V. L. Hall, T. C. Back, J. R. Ortaldo, and R. H. Wiltrout. 2006. Enhanced antitumor response by divergent modulation of natural killer and natural killer T cells in the liver. Cancer Res. 66:11005-11012.
46. Tang, F., L. T. Zhao, Y. Jiang, N. Ba de, L. X. Cui, and W. He. 2008. Activity of recombinant human interleukin-15 against tumor recurrence and metastasis in mice. Cell Mol. Immunol. 5:189-196.
47. Tennant, B. C., I. A. Toshkov, S. F. Peek, J. R. Jacob, S. Menne, W. E. Hornbuckle, R. D. Schinazi, B. E. Korba, P. J. Cote, and J. L. Gerin. 2004. Hepatocellular carcinoma in the woodchuck model of hepatitis B virus infection. Gastroenterology 127:S283-S293. (Pubitemid 39423398)
48. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133-146.
49. Unitt, E., A. Marshall, W. Gelson, S. M. Rushbrook, S. Davies, S. L. Vowler, L. S. Morris, N. Coleman, and G. J. Alexander. 2006. Tumour lymphocytic infiltrate and recurrence of hepatocellular carcinoma following liver transplantation. J. Hepatol. 45:246-253.
50. Voest, E. E., B. M. Kenyon, M. S. O'Reilly, G. Truitt, R. J. D'Amato, and J. Folkman. 1995. Inhibition of angiogenesis in vivo by interleukin 12. J. Natl. Cancer Inst. 87:581-586.
51. Xu, C., T. Yamamoto, T. Zhou, C. E. Aldrich, K. Frank, J. M. Cullen, A. R. Jilbert, and W. S. Mason. 2007. The liver of woodchucks chronically infected with the woodchuck hepatitis virus contains foci of virus core antigen-negative hepatocytes with both altered and normal morphology. Virology 359:283-294. (Pubitemid 46274865)
52. Yajima, T., H. Nishimura, W. Wajjwalku, M. Harada, H. Kuwano, and Y. Yoshikai. 2002. Overexpression of interleukin-15 in vivo enhances antitumor activity against MHC class I-negative and -positive malignant melanoma through augmented NK activity and cytotoxic T-cell response. Int. J. Cancer 99:573-578. (Pubitemid 34461611)
53. Yamanaka, R. 2004. Alphavirus vectors for cancer gene therapy. Int. J. Oncol. 24:919-923.
54. Ying, H., T. Z. Zaks, R. F. Wang, K. R. Irvine, U. S. Kammula, F. M. Marincola, W. W. Leitner, and N. P. Restifo. 1999. Cancer therapy using a self-replicating RNA vaccine. Nat. Med. 5:823-827.