Oncolytic vaccinia virus: From bedside to benchtop and back

Current Opinion in Molecular Therapeutics

Volumn 10, Issue 4, 2008, Pages 387-392

  Thorne, S H ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Cancer therapy; Cell carrier; Clinical trial; Immunotherapy; Oncolytic virus; Vaccinia virus

Indexed keywords

ONCOLYTIC VIRUS;

ANTINEOPLASTIC ACTIVITY; CELL BASED GENE THERAPY; CELL TYPE; CLINICAL STUDY; CLINICAL TRIAL; EXPERIMENTAL MODEL; GENE DELETION; GENE REPLICATION; HUMAN; LIFE CYCLE; LYSIS; MOLECULAR THERAPY; NEOPLASM; NONHUMAN; ONCOLYTIC VIROTHERAPY; PATHOGENESIS; REVIEW; VACCINIA; VACCINIA VIRUS; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS STRAIN;

ANIMALS; CLINICAL TRIALS AS TOPIC; GENE DELETION; HUMANS; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; VACCINIA VIRUS;

ADENOVIRIDAE; MEASLES VIRUS; NEWCASTLE DISEASE VIRUS; ORTHOREOVIRUS; PICORNAVIRIDAE; POLIOVIRUS; SIMPLEXVIRUS; SINDBIS VIRUS; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 49249083599     PISSN: 14648431     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (50)

1. Moss B: Vaccinia virus: A tool for research and vaccine development. Science (1991) 252(5013):1662-1667.
2. Moss B: Poxviridae: The viruses and their replication. In: Field's Virology. 4th edition. Knipe DM, Fields BN, Howley PM (Eds), Lippincott-Raven, Philadelphia, PA, USA (2001):2849-2883.
3. Zeh HJ, Bartlett DL: Development of a replication-selective, oncolytic poxvirus for the treatment of human cancers. Cancer Gene Ther (2002) 9(12):1001-1012.
4. Graham BS, Gorse GJ, Schwartz DH, Keefer MC, McElrath MJ, Matthews TJ, Wright PF, Belshe RB, Clements ML, Dolin R, Corey L et al: Determinants of antibody response after recombinant gp160 boosting in vaccinia-naive volunteers primed with gp160-recombinant vaccinia virus. The National Institute of Allergy and Infectious Diseases AIDS Vaccine Clinical Trials Network. J Infect Dis (1994) 170(4):782-786.
5. Picard O, Achour A, Bernard J, Halbreich A, Bizzini B, Boyer V, Desgranges C, Bertho JM, Lachgar A, Polliotti B, Defer MC et al: A 2-year follow-up of an anti-HIV immune reaction in HIV-1 gp160-immunized healthy seronegative humans: Evidence for persistent cell-mediated immunity. J Acquir Immune Defic Syndr (1992) 5(6):539-546.
6. Kanesa-Thasan N, Smucny JJ, Hoke CH, Marks DH, Konishi E, Kurane I, Tang DB, Vaughn DW, Mason PW, Shope RE: Safety and immunogenicity of NYVAC-JEV and ALVAC-JEV attenuated recombinant Japanese encephalitis virus - poxvirus vaccines in vaccinia-nonimmune and vaccinia-immune humans. Vaccine (2000) 19(4-5):483-491.
7. McClain DJ, Summers PL, Harrison SA, Schmaljohn AL, Schmaljohn CS: Clinical evaluation of a vaccinia-vectored Hantaan virus vaccine. J Med Virol (2000) 60(1):77-85.
8. Cadoz M, Strady A, Meignier B, Taylor J, Tartaglia J, Paoletti E, Plotkin S: Immunisation with canarypox virus expressing rabies glycoprotein. Lancet (1992) 339(8807):1429-1432.
9. Ockenhouse CF, Sun PF, Lanar DE, Wellde BT, Hall BT, Kester K, Stoute JA, Magill A, Krzych U, Farley L, Wirtz RA et al: Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J Infect Dis (1998) 177(6):1664-1673.
10. Doehn C, Kausch I, Böhmer T, Sommerauer M, Jocham D: Drug evaluation: Therion's rV-PSA-TRICOM + rF-PSA-TRICOM prime-boost prostate cancer vaccine. Curr Opin Mol Ther (2007) 9(2):183-189.
11. Harrop R, Drury N, Shingler W, Chikoti P, Redchenko I, Carroll MW, Kingsman SM, Naylor S, Griffiths R, Steven N, Hawkins RE: Vaccination of colorectal cancer patients with TroVax given alongside chemotherapy (5-fluorouracil, leukovorin and irinotecan) is safe and induces potent immune responses. Cancer Immunol Immunother (2008) 57(7):977-986.
12. Rochlitz C, Figlin R, Squiban P, Salzberg M, Pless M, Herrmann R, Tartour E, Zhao Y, Bizouarne N, Baudin M, Acres B: Phase I immunotherapy with a modified vaccinia virus (MVA) expressing human MUC1 as antigen-specific immunotherapy in patients with MUC1-positive advanced cancer. J Gene Med (2003) 5(8):690-699.
13. Jager E, Karbach J, Gnjatic S, Neumann A, Bender A, Valmori D, Ayyoub M, Ritter E, Ritter G, Jager D, Panicali D et al: Recombinant vaccinia/fowlpox NY-ESO-1 vaccines induce both humoral and cellular NY-ESO-1-specific immune responses in cancer patients. Proc Natl Acad Sci USA (2006) 103(39):14453-14458.
14. Hunter-Craig I, Newton KA, Westbury G, Lacey BW: Use of vaccinia virus in the treatment of metastatic malignant melanoma. Br Med J (1970) 2(5708):512-515. • First clinical use of the vaccinia vaccine strain following intralesional injection for the treatment of metastatic malignant melanoma.
15. Roenigk HH Jr, Deodhar S, St Jacques R, Burdick K: Immunotherapy of malignant melanoma with vaccinia virus. Arch Dermatol (1974) 109(5):668-673.
16. Milton GW, Brown MM: The limited role of attenuated smallpox virus in the management of advanced malignant melanoma. Aust N Z J Surg (1966) 35(4):286-290.
17. Mastrangelo MJ, Lattime EC: Virotherapy clinical trials for regional disease: In situ immune modulation using recombinant poxvirus vectors. Cancer Gene Ther (2002) 9(12):1013-1021.
18. Mastrangelo MJ, Maguire HC Jr, Eisenlohr LC, Laughlin CE, Monken CE, McCue PA, Kovatich AJ, Lattime EC: Intratumoral recombinant GM-CSF-encoding virus as gene therapy in patients with cutaneous melanoma. Cancer Gene Ther (1999) 6(5):409-422. •• A trial in which vaccination and immunotherapy strategies and, in hindsight, oncolytic activity were combined by treating patients with a vaccinia strain expressing GM-CSF.
19. Puhlmann M, Brown CK, Gnant M, Huang J, Libutti SK, Alexander HR, Bartlett DL: Vaccinia as a vector for tumor-directed gene therapy: Biodistribution of a thymidine kinase-deleted mutant. Cancer Gene Ther (2000) 7(1):66-73.
20. McCart JA, Ward JM, Lee J, Hu Y, Alexander HR, Libutti SK, Moss B, Bartlett DL: Systemic cancer therapy with a tumor-selective vaccinia virus mutant lacking thymidine kinase and vaccinia growth factor genes. Cancer Res (2001) 61(24):8751-8757. •• The first logically designed oncolytic vaccinia strain, which is often referred to as vvDD.
21. Smith GL, Symons JA, Khanna A, Vanderplasschen A, Alcami A: Vaccinia virus immune evasion. Immunol Rev (1997) 159:137-154.
22. Buller RM, Palumbo GJ: Poxvirus pathogenesis. Microbiol Rev (1991) 55(1):80-122.
23. Thorne SH, Negrin RS, Contag CH: Synergistic antitumor effects of immune cell-viral biotherapy. Science (2006) 311(5768):1780- 1784. •• An immune-cell carrier was used to systemically deliver oncolytic vaccinia virus to tumors.
24. Kirn DH, Wang Y, Liang W, Contag CH, Thorne SH: Enhancing poxvirus oncolytic effects through increased spread and immune evasion. Cancer Res (2008) 68(7):2071-2075.
25. Thorne SH, Hwang T-H, O'Gorman BE, Bartlett DL, Sei S, Kanji F, Brown C, Werier J, Cho JH, Lee DE, Wang Y et al: Rational strain selection and engineering creates a broad spectrum systemically effective oncolytic poxvirus JX-963. J Clin Invest (2007) 117(11):3350-3358. • A study in which the preclinical development of the vvDD GM-CSF-expressing strain was described.
26. Yu YA, Shabahang S, Timiryasova TM, Zhang Q, Beltz R, Gentschev I, Goebel W, Szalay AA: Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol (2004) 22(3):313-320.
27. 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(3):361-370. • Systemic efficacy was demonstrated following iv delivery of an oncolytic vaccinia strain in mouse, rat and rabbit models.
28. Hengstschläger M, Knöfler M, Müllner EW, Ogris E, Wintersberger E, Wawra E: Different regulation of thymidine kinase during the cell cycle of normal versus DNA tumor virus-transformed cells. J Biol Chem (1994) 269(19):13836-13842.
29. Tzahar E, Moyer JD, Waterman H, Barbacci EG, Bao J, Levkowitz G, Shelly M, Strano S, Pinkas-Kramarski R, Pierce JH, Andrews GC, Yarden Y: Pathogenic poxviruses reveal viral strategies to exploit the ErbB signaling network. EMBO J (1998) 17(20):5948-5963.
30. Zhang Q, Yu YA, Wang E, Chen N, Danner RL, Munson PJ, Marincola FM, Szalay AA: Eradication of solid human breast tumors in nude mice with an intravenously injected light-emitting oncolytic vaccinia virus. Cancer Res (2007) 67(20):10038-10046.
31. Kirn DH, Wang Y, Le Boeuf F, Bell J, Thorne SH: Targeting of interferon-β to produce a multi-mechanistic oncolytic vaccinia virus. PLOS Med (2007) 4(12):e353. • Immune dysfunction in cancer was targeted by the development of an oncolytic vaccinia virus expressing type I IFN that was unable to respond to this cytokine.
32. Guo ZS, Naik A, O'Malley ME, Popovic P, Demarco R, Hu Y, Yin X, Yang S, Zeh HJ, Moss B, Lotze MT, Bartlett DL: The enhanced tumor selectivity of an oncolytic vaccinia lacking the host range and antiapoptosis genes SPI-1 and SPI-2. Cancer Res (2005) 65(21):9991-9998.
33. Thorne SH: Strategies to achieve systemic delivery of therapeutic cells and microbes to tumors. Expert Opin Biol Ther (2007) 7(1):41-51.
34. Law M, Smith GL: Studying the binding and entry of the intracellular and extracellular enveloped forms of vaccinia virus. Methods Mol Biol (2004) 269:187-204.
35. Smith GL, Law M: The exit of vaccinia virus from infected cells. Virus Res (2004) 106(2):189-197.
36. Naito T, Kaneko Y, Kozbor D: Oral vaccination with modified vaccinia virus Ankara attached covalently to TMPEG-modified cationic liposomes overcomes pre-existing poxvirus immunity from recombinant vaccinia immunization. J Gen Virol (2007) 88(1):61-70.
37. Galmiche MC, Rindisbacher L, Wels W, Wittek R, Buchegger F: Expression of a functional single chain antibody on the surface of extracellular enveloped vaccinia virus as a step towards selective tumour cell targeting. J Gen Virol (1997) 78(11):3019-3027.
38. Purow B, Staveley-O'Carroll K: Targeting of vaccinia virus using biotin-avidin viral coating and biotinylated antibodies. J Surg Res (2005) 123(1):49-54.
39. Thorne SH, Contag CH: Combining immune cell and viral therapy for the treatment of cancer. Cell Mol Life Sci (2007) 64(12):1449- 1451.
40. Breitbach CJ, Paterson JM, Lemay CG, Falls TJ, McGuire A, Parato KA, Stojdl DF, Daneshmand M, Speth K, Kirn D, McCart JA et al: Targeted inflammation during oncolytic virus therapy severely compromises tumor blood flow. Mol Ther (2007) 15(9):1686-1693. •• A demonstration of the antivascular effects of systemic oncolytic virus therapy.
41. Halsell JS, Riddle JR, Atwood JE, Gardner P, Shope R, Poland GA, Gray GC, Ostroff S, Eckart RE, Hospenthal DR, Gibson RL et al: Myopericarditis following smallpox vaccination among vaccinia-naive US military personnel. J Am Med Assoc (2003) 289(24):3283-3289.
42. Cono J, Casey CG, Bell DM: Smallpox vaccination and adverse reactions. Guidance for clinicians. MMWR Recomm Rep (2003) 52(RR-4):1- 28.
43. De Clercq E: Cidofovir in the treatment of poxvirus infections. Antiviral Res (2002) 55(1):1-13.
44. Yang G, Pevear DC, Davies MH, Collett MS, Bailey T, Rippen S, Barone L, Burns C, Rhodes G, Tohan S, Huggins JW et al: An orally bioavailable antipoxvirus compound (ST-246) inhibits extracellular virus formation and protects mice from lethal orthopoxvirus challenge. J Virol (2005) 79(20):13139-13149.
45. Reeves PM, Bommarius B, Lebeis S, McNulty S, Christensen J, Swimm A, Chahroudi A, Chavan R, Feinberg MB, Veach D, Bornmann W et al: Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. Nat Med (2005) 11(7):731-739.
46. Deng L, Dai P, Ciro A, Smee DF, Djaballah H, Shuman S: Identification of novel antipoxviral agents: Mitoxantrone inhibits vaccinia virus replication by blocking virion assembly. J Virol (2007) 81(24):13392- 13402.
47. Park BH, Hwang T, Liu TC, Sze DY, Kim JS, Kwon HC, Oh SY, Han SY, Yoon JH, Hong SH, Moon A, et al: Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: A phase I trial. Lancet Oncol (2008) 9(6):533-42. • First data from a clinical trial on next-generation oncolytic vaccinia strategies to treat liver cancer were reported.
48. Mastrangelo MJ, Maguire HC Jr, McCue PA, Lee SS, Alexander HR, Nazarian LN, Eisenlohr LC, Nathan F, Berd D, Lattime EC: A pilot study demonstrating the feasability of using intratumoral vaccinia injections as a vector for gene transfer. Vaccine Res (1995) 4:55-69.
49. Arakawa S Jr, Hamami G, Umezu K, Kamidono S, Ishigami J, Arakawa S: Clinical trial of attenuated vaccinia virus AS strain in the treatment of advanced adenocarcinoma. Report on two cases. J Cancer Res Clin Oncol (1987) 113(1):95-98.
50. Kawa A, Arakawa S: The effect of attenuated vaccinia virus AS strain on multiple myeloma; a case report. Jpn J Exp Med (1987) 57(1):79-81.