Oncolytic virotherapy as a personalized cancer vaccine

International Journal of Cancer

Volumn 123, Issue 3, 2008, Pages 493-499

  Li, Qi Xiang ^a   Liu, Guohong ^a   Wong Staal, Flossie ^a  

^a iTherX Pharmaceuticals Inc   (United States)

Author keywords

Adaptive anticancer immunity; Antiviral innate immunity; Cancer immunotherapy; Combination therapy; Cyclophosphamide; Oncolytic virus; Personalized medicine

Indexed keywords

CANCER VACCINE; CYCLOPHOSPHAMIDE; HEAT SHOCK PROTEIN; IMMUNOMODULATING AGENT; ONCOLYTIC VIRUS;

ADAPTIVE IMMUNITY; CANCER IMMUNOTHERAPY; CELL THERAPY; CYTOKINE PRODUCTION; CYTOREDUCTIVE SURGERY; DRUG SAFETY; GENE DELETION; GENE INSERTION; HUMAN; INNATE IMMUNITY; NEOPLASM; NONHUMAN; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; SHORT SURVEY; SINGLE DRUG DOSE; TRANSGENE; TUMOR IMMUNITY; VIRUS REPLICATION;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CANCER VACCINES; CELL TRANSPLANTATION; CYCLOPHOSPHAMIDE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; GENETIC ENGINEERING; GENETIC VECTORS; HEAT-SHOCK PROTEINS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; TRANSGENES; UP-REGULATION;

EID: 46049101017     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23692     Document Type: Short Survey

References (74)

1. Xue SA, Stauss HJ. Enhancing immune responses for cancer therapy. Cell Mol Immunol 2007;4:173-84.
2. Koyama AH, Fukumori T, Fujita M, Irie H, Adachi A. Physiological significance of apoptosis in animal virus infection. Microbes Infect 2000;2:1111-17.
3. Fu X, Tao L, Jin A, Vile R, Brenner MK, Zhang X. Expression of a fusogenic membrane glycoprotein by an oncolytic herpes simplex virus potentiates the viral antitumor effect. Mol Ther 2003;7:748-54.
4. Simpson GR, Han Z, Liu B, Wang Y, Campbell G, Coffin RS. Combination of a fusogenic glycoprotein, prodrug activation, and oncolytic herpes simplex virus for enhanced local tumor control. Cancer Res 2006;66:4835-42.
5. Harrop R, Carroll MW. Viral vectors for cancer immunotherapy. Front Biosci 2006;11:804-17.
6. Arlen PM, Skarupa L, Pazdur M, Seetharam M, Tsang KY, Grosenbach DW, Feldman J, Poole DJ, Litzinger M, Steinberg SM, Jones E, Chen C, et al. Clinical safety of a viral vector based prostate cancer vaccine strategy. J Urol 2007;178:1515-20.
7. Adamina M, Daetwiler S, Rosenthal R, Zajac P. Clinical applications of recombinant virus-based cancer immunotherapy. Expert Opin Biol Ther 2005;5:1211-24.
8. Jugovic P, Hill AM, Tomazin R, Ploegh H, Johnson DC. Inhibition of major histocompatibility complex class I antigen presentation in pig and primate cells by herpes simplex virus type 1 and 2 ICP47. J Virol 1998;72:5076-84.
9. Gyotoku T, Ono F, Aurelian L. Development of HSV-specific CD4+ Th1 responses and CD8+ cytotoxic T lymphocytes with antiviral activity by vaccination with the HSV-2 mutant ICP10DeltaPK. Vaccine 2002;20:2796-807.
10. Li H, Dutuor A, Tao L, Fu X, Zhang X. Virotherapy with a type 2 herpes simplex virus-derived oncolytic virus induces potent antitumor immunity against neuroblastoma. Clin Cancer Res 2007;13:316-22.
11. Shen Y, Nemunaitis J. Fighting cancer with vaccinia virus: teaching new tricks to an old dog. Mol Ther 2005;11:180-95.
12. Liu BL, Robinson M, Han ZQ, Branston RH, English C, Reay P, McGrath Y, Thomas SK, Thornton M, Bullock P, Love CA, Coffin RS. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther 2003;10: 292-303.
13. Hu JC, Coffin RS, Davis CJ, Graham NJ, Groves N, Guest PJ, Harrington KJ, James ND, Love CA, McNeish I, Medley LC, Michael A, et al. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res 2006;12:6737-47.
14. Kim JH, Oh JY, Park BH, Lee DE, Kim JS, Park HE, Roh MS, Je JE, Yoon JH, Thorne SH, Kirn D, Hwang TH. Systemic armed oncolytic and immunologic therapy for cancer with JX-594, a targeted poxvirus expressing GM-CSF. Mol Ther 2006;14:361-70.
15. Post DE, Sandberg EM, Kyle MM, Devi NS, Brat DJ, Xu Z, Tighiouart M, Van Meir EG. Targeted cancer gene therapy using a hypoxia inducible factor dependent oncolytic adenovirus armed with interleukin-4. Cancer Res 2007;67:6872-81.
16. Todo T, Martuza RL, Dallman MJ, Rabkin SD. In situ expression of soluble B7-1 in the context of oncolytic herpes simplex virus induces potent antitumor immunity. Cancer Res 2001;61:153-61.
17. Choi KJ, Kim JH, Lee YS, Kim J, Suh BS, Kim H, Cho S, Sohn JH, Kim GE, Yun CO. Concurrent delivery of GM-CSF and B7-1 using an oncolytic adenovirus elicits potent antitumor effect. Gene Ther 2006;13:1010-20.
18. Ino Y, Saeki Y, Fukuhara H, Todo T. Triple combination of oncolytic herpes simplex virus-1 vectors armed with interleukin-12, interleukin-18, or soluble B7-1 results in enhanced antitumor efficacy. Clin Cancer Res 2006;12:643-52.
19. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood SK. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000;6:435-42.
20. Multhoff G, Mizzen L, Winchester CC, Milner CM, Wenk S, Eissner G, Kampinga HH, Laumbacher B, Johnson J. Heat shock protein 70 (Hsp70) stimulates proliferation and cytolytic activity of natural killer cells. Exp Hematol 1999;27:1627-36.
21. Huang XF, Ren W, Rollins L, Pittman P, Shah M, Shen L, Gu Q, Strube R, Hu F, Chen SY. A broadly applicable, personalized heat shock protein-mediated oncolytic tumor vaccine. Cancer Res 2003; 63:7321-9.
22. Liu H. 10th Annual Meeting of American Gene Therapy Society, Seattle, WA, 2007.
23. Di Paolo NC, Tuve S, Ni S, Hellstrom KE, Hellstrom I, Lieber A. Effect of adenovirus-mediated heat shock protein expression and oncolysis in combination with low-dose cyclophosphamide treatment on antitumor immune responses. Cancer Res 2006;66:960-9.
24. Bateman AR, Harrington KJ, Kottke T, Ahmed A, Melcher AA, Gough MJ, Linardakis E, Riddle D, Dietz A, Lohse CM, Strome S, Peterson T, et al. Viral fusogenic membrane glycoproteins kill solid tumor cells by nonapoptotic mechanisms that promote cross presentation of tumor antigens by dendritic cells. Cancer Res 2002;62:6566-78.
25. Errington F, Bateman A, Kottke T, Thompson J, Harrington K, Merrick A, Hatfield P, Selby P, Vile R, Melcher A. Allogeneic tumor cells expressing fusogenic membrane glycoproteins as a platform for clinical cancer immunotherapy. Clin Cancer Res 2006;12:1333-41.
26. Errington F, Jones J, Merrick A, Bateman A, Harrington K, Gough M, O'Donnell D, Selby P, Vile R, Melcher A. Fusogenic membrane glycoprotein- mediated tumour cell fusion activates human dendritic cells for enhanced IL-12 production and T-cell priming. Gene Ther 2006; 13:138-49.
27. Li H, Dutuor A, Fu X, Zhang X. Induction of strong antitumor immunity by an HSV-2-based oncolytic virus in a murine mammary tumor model. J Gene Med 2007;9:161-9.
28. Li H, Zeng Z, Fu X, Zhang X. Coadministration of a herpes simplex virus-2 based oncolytic virus and cyclophosphamide produces a synergistic antitumor effect and enhances tumor-specific immune responses. Cancer Res 2007;67:7850-5.
29. Nakamori M, Fu X, Rousseau R, Chen SY, Zhang X. Destruction of nonimmunogenic mammary tumor cells by a fusogenic oncolytic herpes simplex virus induces potent antitumor immunity. Mol Ther 2004;9:658-65.
30. Hoffmann D, Bayer W, Wildner O. In situ tumor vaccination with adenovirus vectors encoding measles virus fusogenic membrane proteins and cytokines. World J Gastroenterol 2007;13:3063-70.
31. Hoffmann D, Wildner O. Enhanced killing of pancreatic cancer cells by expression of fusogenic membrane glycoproteins in combination with chemotherapy. Mol Cancer Ther 2006;5:2013-22.
32. Hoffmann D, Bayer W, Grunwald T, Wildner O. Intratumoral expression of respiratory syncytial virus fusion protein in combination with cytokines encoded by adenoviral vectors as in silu tumor vaccine for colorectal cancer. Mol Cancer Ther 2007;6:1942-50.
33. Hoffmann D, Bayer W, Wildner O. Therapeutic immune response induced by intratumoral expression of the fusogenic membrane protein of vesicular stomatitis virus and cytokines encoded by adenoviral vectors. Int J Mol Med 2007;20:673-81.
34. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, Zheng Z, Nahvi A, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science (New York, NY) 2006; 314:126-9.
35. Engleman EG. Dendritic cell-based cancer immunotherapy. Semin Oncol 2003;30:23-9.
36. Morisaki T, Matsumoto K, Onishi H, Kuroki H, Baba E, Tasaki A, Kubo M, Nakamura M, Inaba S, Yamaguchi K, Tanaka M, Katano M. Dendritic cell-based combined immunotherapy with autologous tumor-pulsed dendritic cell vaccine and activated T cells for cancer patients: rationale, current progress, and perspectives. Hum Cell 2003;16:175-82.
37. Gilboa E. DC-based cancer vaccines. J Clin Invest 2007;117:1195-203.
38. Rosenberg SA, Dudley ME. Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes. Proc Natl Acad Sci USA 2004;101(Suppl 2):14639-45.
39. Thorne SH, Contag CH. Combining immune cell and viral therapy for the treatment of cancer. Cell Mol Life Sci 2007;64:1449-51.
40. Raykov Z, Grekova S, Galabov AS, Balboni G, Koch U, Aprahamian M, Rommelaere J. Combined oncolytic and vaccination activities of parvovirus H-1 in a metastatic tumor model. Oncol Rep 2007;17: 1493-9.
41. Schirrmacher V, Haas C, Bonifer R, Ahlert T, Gerhards R, Ertel C. Human tumor cell modification by virus infection: an efficient and safe way to produce cancer vaccine with pleiotropic immune stimulatory properties when using Newcastle disease virus. Gene Ther 1999; 6:63-73.
42. Schirrmacher V. Clinical trials of antitumor vaccination with an autologous tumor cell vaccine modified by virus infection: improvement of patient survival based on improved antitumor immune memory. Cancer Immunol Immunother 2005;54:587-98.
43. Bai L, Koopmann J, Fiola C, Fournier P, Schirrmacher V. Dendritic cells pulsed with viral oncolysates potently stimulate autologous T cells from cancer patients. Int J Oncol 2002;21:685-94.
44. Qiao J, Kottke T, Willmon C, Galivo F, Wongthida P, Diaz RM, Thompson J, Ryno P, Barber GN, Chester J, Selby P, Harrington K, et al. Purging metastases in lymphoid organs using a combination of antigen-nonspecific adoptive T cell therapy, oncolytic virotherapy and immunotherapy. Nat Med 2008;14:37-44.
45. Hoffmann D, Bayer W, Wildner O. Local and distant immune-mediated control of colon cancer growth with fusogenic membrane glycoproteins in combination with viral oncolysis. Hum Gene Ther 2007;18:435-50.
46. Yotnda P, Savoldo B, Charlet-Berguerand N, Rooney C, Brenner M. Targeted delivery of adenoviral vectors by cytotoxic T cells. Blood 2004;104:2272-80.
47. Kurozumi K, Hardcastle J, Thakur R, Yang M, Christoforidis G, Fulci G, Hochberg FH, Weissleder R, Carson W, Chiocca EA, Kaur B. Effect of tumor microenvironment modulation on the efficacy of oncolytic virus therapy. J Natl Cancer Inst 2007;99:1768-81.
48. Binotto G, Trentin L, Semenzato G. Ifosfamide and cyclophosphamide: effects on immunosurveillance. Oncology 2003;65(Suppl 2): 17-20.
49. Fulci G, Breymann L, Gianni D, Kurozomi K, Rhee SS, Yu J, Kaur B, Louis DN, Weissleder R, Caligiuri MA, Chiocca EA. Cyclophosphamide enhances glioma virotherapy by inhibiting innate immune responses. Proc Natl Acad Sci USA 2006;103:12873-8.
50. Kambara H, Saeki Y, Chiocca EA. Cyclophosphamide allows for in vivo dose reduction of a potent oncolytic virus. Cancer Res 2005;65:11255-8.
51. Ikeda K, Ichikawa T, Wakimoto H, Silver JS, Deisboeck TS, Finkelstein D, Harsh GRT, Louis DN, Bartus RT, Hochberg FH, Chiocca EA. Oncolytic virus therapy of multiple tumors in the brain requires suppression of innate and elicited antiviral responses. Nat Med 1999;5:881-7.
52. Wakimoto H, Ikeda K, Abe T, Ichikawa T, Hochberg FH, Ezekowitz RA, Pasternack MS, Chiocca EA. The complement response against an oncolytic virus is species-specific in its activation pathways. Mol Ther 2002;5:275-82.
53. Lamfers ML, Fulci G, Gianni D, Tang Y, Kurozumi K, Kaur B, Moeniralm S, Saeki Y, Carette JE, Weissleder R, Vandertop WP, van Beusechem VW, et al. Cyclophosphamide increases transgene expression mediated by an oncolytic adenovirus in glioma-bearing mice monitored by bioluminescence imaging. Mol Ther 2006;14:779-88.
54. Wakimoto H, Fulci G, Tyminski E, Chiocca EA. Altered expression of antiviral cytokine mRNAs associated with cyclophosphamide's enhancement of viral oncolysis. Gene Ther 2004;11:214-23.
55. Hermans IF, Chong TW, Palmowski MJ, Harris AL, Cerundolo V. Synergistic effect of metronomic dosing of cyclophosphamide combined with specific antitumor immunotherapy in a murine melanoma model. Cancer Res 2003;63:8408-13.
56. Machiels JP, Reilly RT, Emens LA, Ercolini AM, Lei RY, Weintraub D, Okoye FI, Jaffee EM. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res 2001;61:3689-97.
57. Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C, Chauffert B, Solary E, Bonnotte B, Martin F. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004;34:336-44.
58. Bracci L, Moschella F, Sestili P, La Sorsa V, Valentini M, Canini I, Baccarini S, Maccari S, Ramoni C, Belardelli F, Proietti E. Cyclophosphamide enhances the antitumor efficacy of adoptively transferred immune cells through the induction of cytokine expression. B-cell and. T-cell homeostatic proliferation, and specific tumor infiltration. Clin Cancer Res 2007;13:644-53.
59. Song CK, Han HD, Noh KH, Kang TH, Park YS, Kim JH, Park ES, Shin BC, Kim TW. Chemotherapy enhances CD8(+) T cell-mediated antitumor immunity induced by vaccination with vaccinia virus. Mol Ther 2007;15:1558-63.
60. Tong Y, Song W, Crystal RG. Combined intratumoral injection of bone marrow-derived dendritic cells and systemic chemotherapy to treat pre-existing murine tumors. Cancer Res 2001;61:7530-5.
61. Emens LA, Jaffee EM. Leveraging the activity of tumor vaccines with cytotoxic chemotherapy. Cancer Res 2005;65:8059-64.
62. Matar P, Rozados VR, Gervasoni SI, Scharovsky GO. Th2/Th1 switch induced by a single low dose of cyclophosphamide in a rat metastatic lymphoma model. Cancer Immunol Immunother 2002;50:588-96.
63. Jameson SC. Maintaining the norm: T-cell homeostasis. Nat Rev Immunol 2002;2:547-56.
64. Salem ML, Kadima AN, El-Naggar SA, Rubinstein MP, Chen Y, Gillanders WE, Cole DJ. Defining the ability of cyclophosphamide pre-conditioning to enhance the antigen-specific CD8+ T-cell response to peptide vaccination: creation of a beneficial host microenvironment involving type I IFNs and myeloid cells. J Immunother 2007;30:40-53.
65. Blattman JN, Cheng LE, Greenberg PD. CD8(+) T cell responses: it's all downhill after their prime. Nat Immunol 2002;3:601-2.
66. Askenase PW, Hayden BJ, Gershon RK. Augmentation of delayed-type hypersensitivity by doses of cyclophosphamide which do not affect antibody responses. J Exp Med 1975;141:697-702.
67. Berd D, Maguire HC, Jr., Mastrangelo MJ. Potentiation of human cell-mediated and humoral immunity by low-dose cyclophosphamide. Cancer Res 1984;44:5439-43.
68. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA, Rogers LJ, Gracia GJ, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005; 23:2346-57.
69. Mastrangelo MJ, Maguire HC, Jr, Sato T, Nathan FE, Berd D. Active specific immunization in the treatment of patients with melanoma. Semin Oncol 1996;23:773-81.
70. Mitchell MS, Kan-Mitchell J, Kempf RA, Harel W, Shau HY, Lind S. Active specific immunotherapy for melanoma: phase I trial of allogeneic lysates and a novel adjuvant. Cancer Res 1988;48:5883-93.
71. Galanis E. 4th International Conference on Oncolytic Virus as Cancer Therapeutics. Scottsdale, AZ, 2007.
72. Janke M, Peeters B, de Leeuw O, Moorman R, Arnold A, Fournier P, Schirrmacher V. Recombinant Newcastle disease virus (NDV) with inserted gene coding for GM-CSF as a new vector for cancer immunogene therapy. Gene Ther 2007;14:1639-49.
73. Varghese S, Rabkin SD, Liu R, Nielsen PG, Ipe T, Martuza RL. Enhanced therapeutic efficacy of IL-12, but not GM-CSF, expressing oncolytic herpes simplex virus for transgenic mouse derived prostate cancers. Cancer Gene Ther 2006;13:253-65.
74. Lee YS, Kim JH, Choi KJ, Choi IK, Kim H, Cho S, Cho BC, Yun CO. Enhanced antitumor effect of oncolytic adenovirus expressing interleukin-12 and B7-1 in an immunocompetent murine model. Clin Cancer Res 2006;12:5859-68.