Poxvirus-based vaccines for cancer immunotherapy: New insights from combined cytokines/co-stimulatory molecules delivery and "uncommon" strains

Anti-Cancer Agents in Medicinal Chemistry

Volumn 14, Issue 2, 2014, Pages 183-189

  Izzi, Valerio ^a   Buler, Marcin ^a   Masuelli, Laura ^b   Giganti, Maria G ^c   Modesti, Andrea ^c   Bei, Roberto ^c  

^a UNIVERSITY OF OULU   (Finland)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Avipoxviruses; Cancer vaccine; Cytokines; Immunostimulation; Poxviruses; Tumour associated antigens

Indexed keywords

ADAPTIVE IMMUNITY; ANTIGENS, NEOPLASM; AVIPOXVIRUS; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; CYTOKINES; GENETIC VECTORS; HUMANS; IMMUNITY, INNATE; IMMUNIZATION; IMMUNOLOGIC FACTORS; IMMUNOTHERAPY; NEOPLASMS; TUMOR MICROENVIRONMENT; VACCINES, ATTENUATED;

EID: 84893513814     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/18715206113136660376     Document Type: Review

References (62)

1. Baltimore, D. Expression of animal virus genomes. Bacteriol. Rev., 1971, 35(3), 235-241.
2. Kaufman, H. L. The role of poxviruses in tumor immunotherapy. Surgery, 2003, 134(5), 731-737.
3. King, A. M. Q.; Lefkowitz, E.; Adams, M. J.; Carstens, E. B. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Academic Press, 2011.
4. Schlom, J. Therapeutic cancer vaccines: current status and moving forward. J. Natl. Cancer Inst., 2012, 104(8), 599-613.
5. Moss, B. Genetically engineered poxviruses for recombinant gene expression, vaccination, and safety. Proc. Natl. Acad. Sci. USA, 1996, 93(21), 11341-11348.
6. Hodge, J. W.; Higgins, J.; Schlom, J. Harnessing the unique local immunostimulatory properties of modified vaccinia Ankara (MVA) virus to generate superior tumor-specific immune responses and antitumor activity in a diversified prime and boost vaccine regimen. Vaccine, 2009, 27(33), 4475-4482.
7. Marshall, J. L.; Hoyer, R. J.; Toomey, M. A.; Faraguna, K.; Chang, P.; Richmond, E.; Pedicano, J. E.; Gehan, E.; Peck, R. A.; Arlen, P.; Tsang, K. Y.; Schlom, J. Phase I study in advanced cancer patients of a diversified prime-and-boost vaccination protocol using recombinant vaccinia virus and recombinant nonreplicatingavipox virus to elicit anti-carcinoembryonic antigen immune responses. J. Clin. Oncol., 2000, 18(23), 3964-3973.
8. Hodge, J. W.; Grosenbach, D. W.; Aarts, W. M.; Poole, D. J.; Schlom, J. Vaccine therapy of established tumors in the absence of autoimmunity. Clin Cancer Res., 2003, 9(5), 1837-1849.
9. Turriziani, M.; Fantini, M.; Benvenuto, M.; Izzi, V.; Masuelli, L.; Sacchetti, P.; Modesti, A.; Bei, R. Carcinoembryonic antigen (CEA)-based cancer vaccines: Recent patents and antitumor effects from experimental models to clinical trials. Rec. Pat. Anticancer Drug. Discov., 2012, 7(3), 265-296.
10. Bei, R.; Kantor, J.; Kashmiri, S. V.; Abrams, S.; Schlom, J. Enhanced immune responses and anti-tumor activity by baculovirus recombinant carcinoembryonic antigen (CEA) in mice primed with the recombinant vaccinia CEA. J. Immunother. Emphasis Tumor Immunol., 1994, 16(4), 275-282.
11. Kantor, J.; Irvine, K.; Abrams, S.; Kaufman, H.; Di Pietro, J.; Schlom, J. Antitumor activity and immune responses induced by a recombinant carcinoembryonic antigen-vaccinia virus vaccine. J. Natl. Cancer Inst., 1992, 84(14), 1084-1091.
12. Hodge, J. W.; Abrams, S.; Schlom, J.; Kantor, J. A. Induction of antitumor immunity by recombinant vaccinia viruses expressing B7-1 or B7-2 costimulatory molecules. Cancer Res., 1994, 54(21), 5552-5555.
13. Kantor, J.; Irvine, K.; Abrams, S.; Snoy, P.; Olsen, R.; Greiner, J.; Kaufman, H.; Eggensperger, D.; Schlom, J. Immunogenicity and safety of a recombinant vaccinia virus vaccine expressing the carcinoembryonic antigen gene in a nonhuman primate. Cancer Res., 1992, 52(24), 6917-6925.
14. Kantor, J.; Abrams, S.; Irvine, K.; Snoy, P.; Kaufman, H.; Schlom, J. Specific immunotherapy using a recombinant vaccinia virus expressing human carcinoembryonic antigen. Ann. N Y Acad. Sci., 1993, 690, 370-373.
15. Horig, H.; Lee, C. S.; Kaufman, H. L. Prostate-specific antigen vaccines for prostate cancer. Exp. Opin. Biol. Ther., 2002, 2(4), 395-408.
16. Bei, R.; Scardino, A. TAA polyepitope DNA-based vaccines: a potential tool for cancer therapy. J. Biomed. Biotechnol., 2010, 2010, 102758.
17. Tarassoff, C. P.; Arlen, P. M.; Gulley, J. L. Therapeutic vaccines for prostate cancer. The Oncologist, 2006, 11(5), 451-462.
18. Van der Burg, S. H.; Menon, A. G.; Redeker, A.; Bonnet, M. C.; Drijfhout, J. W.; Tollenaar, R. A.; Van de Velde, C. J.; Moingeon, P.; Kuppen, P. J.; Offringa, R.; Melief, C. J. Induction of p53-specific immune responses in colorectal cancer patients receiving a recombinant ALVAC-p53 candidate vaccine. Clin. Cancer Res., 2002, 8(5), 1019-1027.
19. Acres, R. B.; Hareuveni, M.; Balloul, J. M.; Kieny, M. P. Vaccinia virus MUC1 immunization of mice: immune response and protection against the growth of murine tumors bearing the MUC1 antigen. J Immunother Emphasis Tumor Immunol., 1993, 14(2), 136-143.
20. Zaloudik, J.; Li, W.; Jacob, L.; Kieny, M. P.; Somasundaram, R.; Acres, B.; Song, H.; Zhang, T.; Li, J.; Herlyn, D. Inhibition of tumor growth by recombinant vaccinia virus expressing GA733/CO17-1A/EpCAM/KSA/KS1-4 antigen in mice. Cancer Gene Ther., 2002, 9(4), 382-389.
21. Masuelli, L.; Marzocchella, L.; Focaccetti, C.; Lista, F.; Nardi, A.; Scardino, A.; Mattei, M.; Turriziani, M.; Modesti, M.; Forni, G.; Schlom, J.; Modesti, A.; Bei, R. Local delivery of recombinant vaccinia virus encoding for neu counteracts growth of mammary tumors more efficiently than systemic delivery in neu transgenic mice. Cancer Immunol. Immunother., 2010, 59(8), 1247-1258.
22. Mulryan, K.; Ryan, M. G.; Myers, K. A.; Shaw, D.; Wang, W.; Kingsman, S. M.; Stern, P. L.; Carroll, M. W. Attenuated recombinant vaccinia virus expressing oncofetal antigen (tumor-associated antigen) 5T4 induces active therapy of established tumors. Mol Cancer Ther., 2002, 1(12), 1129-1137.
23. Zajac, P.; Oertli, D.; Marti, W.; Adamina, M.; Bolli, M.; Guller, U.; Noppen, C.; Padovan, E.; Schultz-Thater, E.; Heberer, M.; Spagnoli, G. Phase I/II clinical trial of a nonreplicative vaccinia virus expressing multiple HLA-A0201-restricted tumor-associated epitopes and costimulatory molecules in metastatic melanoma patients. Hum Gene Ther., 2003, 14(16), 1497-1510.
24. Schütz, A.; Oertli, D.; Marti, W. R.; Noppen, C.; Padovan, E.; Spagnoli, G. C.; Heberer, M.; Zajac, P. Immunogenicity of nonreplicating recombinant vaccinia expressing HLA-A201 targeted or complete MART-1/Melan-A antigen. Cancer Gene Ther., 2001, 8(9), 655-661.
25. Zajac, P.; Oertli, D.; Spagnoli, G. C.; Noppen, C.; Schaefer, C.; Heberer, M.; Marti, W. R. Generation of tumoricidal cytotoxic T lymphocytes from healthy donors after in vitro stimulation with a replication-incompetent vaccinia virus encoding MART-1/Melan-A 27-35 epitope. Int J Cancer., 1997, 71(3), 491-496.
26. Reading, P. C.; Smith, G. L. A kinetic analysis of immune mediators in the lungs of mice infected with vaccinia virus and comparison with intradermal infection. J. Gen. Virol., 2003, 84(8), 1973-1983.
27. Odunsi, K.; Matsuzaki, J.; Karbach, J.; Neumann, A.; Mhawech-Fauceglia, P.; Miller, A.; Beck, A.; Morrison, C. D.; Ritter, G.; Godoy, H.; Lele, S.; DuPont, N.; Edwards, R.; Shrikant, P.; Old, L. J.; Gnjatic, S.; Jäger, E. Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc. Natl. Acad. Sci. USA., 2012, 109(15), 5797-5802.
28. Jacobs, N.; Chen, R. A.; Gubser, C.; Najarro, P.; Smith, G. L. Intradermal immune response after infection with vaccinia virus. J. Gen. Virol., 2006, 87(5), 1157-1161.
29. Worschech, A.; Haddad, D.; Stroncek, D. F.; Wang, E.; Marincola, F. M.; Szalay, A. A. The immunologic aspects of poxvirus oncolytic therapy. Cancer Immunol. Immunother., 2009, 58(9), 1355-1362.
30. Beukema, E. L.; Brown, M. P.; Hayball, J. D. The potential role of fowlpox virus in rational vaccine design. Exp. Rev. Vaccines, 2006, 5(4), 565-577.
31. Tran, L.; Judor, J. P.; Gauttier, V.; Geist, M.; Hoffman, C.; Rooke, R.; Vassaux, G.; Conchon, S. The immunogenicity of the tumorassociated antigen γ-fetoprotein is enhanced by a fusion with a transmembrane domain. J. Biomed. Biotechnol., 2012, 2012, 878657.
32. Bei, R.; Mizejewski, G. J. Alpha fetoprotein is more than a hepatocellular cancer biomarker: from spontaneous immune response in cancer patients to the development of an AFP-based cancer vaccine. Curr. Mol. Med., 2011, 11(7), 564-581.
33. Krupa, M.; Canamero, M.; Gomez, C. E.; Najera, J. L.; Gil, J.; Esteban, M. Immunization with recombinant DNA and modified vaccinia virus Ankara (MVA) vectors delivering PSCA and STEAP1 antigens inhibits prostate cancer progression. Vaccine., 2011, 29(7), 1504-1513.
34. Ishizaki, H.; Manuel, E. R.; Song, G. Y.; Srivastava, T.; Sun, S.; Diamond, D. J.; Ellenhorn, J. D. Modified vaccinia Ankara expressing survivin combined with gemcitabine generates specific antitumor effects in a murine pancreatic carcinoma model. Cancer Immunol. Immunother., 2011, 60(1), 99-109.
35. Harrop, R.; Ryan, M. G.; Myers, K. A.; Redchenko, I.; Kingsman, S. M.; Carroll, M. W. Active treatment of murine tumors with a highly attenuated vaccinia virus expressing the tumor associated antigen 5T4 (TroVax) is CD4+ T cell dependent and antibody mediated. Cancer Immunol. Immunother., 2006, 55(9), 1081-1090.
36. Kaufman, H. L.; Wang, W.; Manola, J.; DiPaola, R. S.; Ko, Y. J.; Sweeney, C.; Whiteside, T. L.; Schlom, J.; Wilding, G.; Weiner, L. M. Phase II randomized study of vaccine treatment of advanced prostate cancer (E7897): a trial of the eastern cooperative oncology group. J. Clin. Oncol., 2004, 22(11), 2122-2132.
37. Radaelli, A.; Pozzi, E.; Pacchioni, S.; Zanotto, C.; MorghenCde, G. Fowlpox virus recombinants expressing HPV-16 E6 and E7 oncogenes for the therapy of cervical carcinoma elicit humoral and cell-mediated responses in rabbits. J. Transl. Med., 2010, 21(8), 40-52.
38. Izzi, V.; Masuelli, L.; Tresoldi, I.; Foti, C.; Modesti, A.; Bei, R. Immunity and malignant mesothelioma: from mesothelial cell damage to tumor development and immune response-based therapies. Cancer Lett., 2012, 322(1), 18-34.
39. Ingrosso, G.; Fantini, M.; Nardi, A.; Benvenuto, M.; Sacchetti, P.; Masuelli, L.; Ponti, E.; Frajese, G. V.; Lista, F.; Schillaci, O.; Santoni, R.; Modesti, A.; Bei, R. Local radiotherapy increases the level of autoantibodies to ribosomal P0 protein but not to heat shock proteins, extracellular matrix molecules and EGFR/ErbB2 receptors in prostate cancer patients. Oncol. Rep., 2013, 29(3), 1167-1174.
40. Palumbo, C.; Bei, R.; Procopio, A.; Modesti, A. Molecular targets and targeted therapies for malignant mesothelioma. Curr. Med. Chem., 2008, 15(9), 855-867.
41. Bei, R.; Masuelli, L.; Moriconi, E.; Visco, V.; Moretti, A.; Kraus, M. H.; Muraro, R. Immune responses to all ErbB family receptors detectable in serum of cancer patients. Oncogene, 1999, 18(6), 1267-1275.
42. Dasgupta, S.; Bhattacharya-Chatterjee, M.; O'Malley, B. W., Jr; Chatterjee, S. K. Recombinant vaccinia virus expressing interleukin-2 invokes anti-tumor cellular immunity in an orthotopic murine model of head and neck squamous cell carcinoma. Mol. Ther., 2006, 13(1), 183-193.
43. Jourdier, T. M.; Moste, C.; Bonnet, M. C.; Delisle, F.; Tafani, J. P.; Devauchelle, P.; Tartaglia, J.; Moingeon, P. Local immunotherapy of spontaneous feline fibrosarcomas using recombinant poxviruses expressing interleukin 2 (IL2). Gene Ther., 2003, 10(26), 2126-2132.
44. Kaufman, H. L.; Flanagan, K.; Lee, C. S.; Perretta, D. J.; Horig, H. Insertion of interleukin-2 (IL-2) and interleukin-12 (IL-12) genes into vaccinia virus results in effective anti-tumor responses without toxicity. Vaccine, 2002, 20(13-14), 1862-1869.
45. Aarts, W. M.; Schlom, J.; Hodge, J. W. Vector-based vaccine/cytokine combination therapy to enhance induction of immune responses to a self-antigen and antitumor activity. Cancer Res., 2002, 62(20), 5770-5777.
46. Nemeckova, S.; Smahel, M.; Hainz, P.; Mackova, J.; Zurkova, K.; Gabriel, P.; Indrova, M.; Kutinova, L. Combination of intratumoral injections of vaccinia virus MVA expressing GM-CSF and immunization with DNA vaccine prolongs the survival of mice bearing HPV16 induced tumors with downregulated expression of MHC class I molecules. Neoplasma, 2007, 54(4), 326-333.
47. Kass, E.; Panicali, D. L.; Mazzara, G.; Schlom, J.; Greiner, J. W. Granulocyte/macrophage-colony stimulating factor produced by recombinant avian poxviruses enriches the regional lymph nodes with antigen-presenting cells and acts as an immunoadjuvant. Cancer Res., 2001, 61(1), 206-214.
48. Chatterjee, S. K.; Qin, H.; Manna, S.; Tripathi, P. K. Recombinant vaccinia virus expressing cytokine GM-CSF as tumor vaccine. Anticancer Res., 1999, 19(4B), 2869-2873.
49. McLaughlin, J. P.; Abrams, S.; Kantor, J.; Dobrzanski, M. J.; Greenbaum, J.; Schlom, J.; Greiner, J. W. Immunization with a syngeneic tumor infected with recombinant vaccinia virus expressing granulocyte-macrophage colony-stimulating factor (GM-CSF) induces tumor regression and long-lasting systemic immunity. J Immunother., 1997, 20(6), 449-459.
50. Qin, H.; Chatterjee, S. K. Cancer gene therapy using tumor cells infected with recombinant vaccinia virus expressing GM-CSF. Hum Gene Ther., 1996, 7(15), 1853-1860.
51. Sathaiah, M.; Thirunavukkarasu, P.; O'Malley, M. E.; Kavanagh, M. A.; Ravindranathan, R.; Austin, F.; Guo, Z. S.; Bartlett, D. L. Oncolytic poxvirus armed with Fas ligand leads to induction of cellular Fas receptor and selective viral replication in FasRnegative cancer. Cancer Gene Ther., 2012, 19(3), 192-201.
52. Li, J.; O'Malley, M.; Urban, J.; Sampath, P.; Guo, Z. S.; Kalinski, P.; Thorne, S. H.; Bartlett, D. L. Chemokine expression from oncolyticvaccinia virus enhances vaccine therapies of cancer. Mol. Ther., 2011, 19(4), 650-657.
53. Hörig, H.; Lee, D. S.; Conkright, W.; Divito, J.; Hasson, H.; LaMare, M.; Rivera, A.; Park, D.; Tine, J.; Guito, K.; Tsang, K. W.; Schlom, J.; Kaufman, H. L. Phase I clinical trial of a recombinant canarypoxvirus (ALVAC) vaccine expressing human carcinoembryonic antigen and the B7. 1 co-stimulatory molecule. Cancer Immunol. Immunother., 2000, 49 (9), 504-514.
54. Adamina, M.; Rosenthal, R.; Weber, W. P.; Frey, D. M.; Viehl, C. T.; Bolli, M.; Huegli, R. W.; Jacob, A. L.; Heberer, M.; Oertli, D.; Marti, W.; Spagnoli, G. C.; Zajac, P. Intranodal immunization with a vaccinia virus encoding multiple antigenic epitopes and costimulatory molecules in metastatic melanoma. Mol. Ther., 2010, 18(3), 651-659.
55. Vogel, T. U.; Visan, L.; Ljutic, B.; Gajewska, B.; Caterini, J.; Salha, D.; Wen, T.; He, L.; Parrington, M.; Cao, S. X.; McNeil, B.; Sandhu, D.; Scollard, N.; Zhang, L.; Bradley, B.; Tang, M.; Lovitt, C.; Oomen, R.; Dunn, P.; Tartaglia, J.; Berinstein, N. L. Preclinical qualification of a new multi-antigen candidate vaccine for metastatic melanoma. J. Immunother., 2010, 33(8), 743-758.
56. Madan, R. A.; Bilusic, M.; Heery, C.; Schlom, J.; Gulley, J. L. Clinical evaluation of TRICOM vector therapeutic cancer vaccines. Semin. Oncol., 2012, 39(3), 296-304.
57. Mohebtash, M.; Tsang, K. Y.; Madan, R. A.; Huen, N. Y.; Poole, D. J.; Jochems, C.; Jones, J.; Ferrara, T.; Heery, C. R.; Arlen, P. M.; Steinberg, S. M.; Pazdur, M.; Rauckhorst, M.; Jones, E. C.; Dahut, W. L.; Schlom, J.; Gulley J. L. A pilot study of MUC-1/CEA/TRICOM poxviral-based vaccine in patients with metastatic breast and ovarian cancer. Clin. Cancer Res., 2011, 17(22), 7164-7173.
58. Von Mehren, M.; Arlen, P.; Gulley, J.; Rogatko, A.; Cooper, H. S.; Meropol, N. J.; Alpaugh, R. K.; Davey, M.; McLaughlin, S.; Beard, M. T.; Tsang, K. Y.; Schlom, J.; Weiner, L. M. The influence of granulocyte macrophage colony-stimulating factor and prior chemotherapy on the immunological response to a vaccine (ALVAC-CEA B7. 1) in patients with metastatic carcinoma. Clin. Cancer Res., 2001, 7(5), 1181-1191.
59. Sedegah, M.; Brice, G. T.; Rogers, W. O.; Doolan, D. L.; Charoenvit, Y.; Jones, T. R.; Majam, V. F.; Belmonte, A.; Lu, M.; Belmonte, M.; Carucci, D. J.; Hoffman, S. L. Persistence of protective immunity to malaria induced by DNA priming and poxvirus boosting: characterization of effector and memory CD8(+)-T-cell populations. Infect. Immun., 2002, 70(7), 3493-3499.
60. Tsang, K. Y.; Zhu, M.; Even, J.; Gulley, J.; Arlen, P.; Schlom, J. The infection of human dendritic cells with recombinant avipox vectors expressing a costimulatory molecule transgene (CD80) to enhance the activation of antigen-specific cytolytic T cells. Cancer Res., 2001, 61(20), 7568-7576.
61. Hoos, A.; Eggermont, A. M. M.; Janetzki, S.; Hodi, F. S.; Ibrahim, R.; Anderson, A.; Humphrey, R.; Blumenstein, B.; Oldand, L.; Wolchok, J. Improved endpoints for cancer immunotherapy trials. J. Natl. Cancer Inst., 2010, 102(18), 1388-1397.
62. Disis, M. L. Immunologic biomarkers as correlates of clinical response to cancer immunotherapy. Cancer Immunol. Immunother., 2011, 60(3), 433-442.