Heterologous prime/boost immunization with p53-based vaccines combined with Toll-like receptor stimulation enhances tumor regression

Journal of Immunotherapy

Volumn 33, Issue 6, 2010, Pages 609-617

  Ishizaki, Hidenobu ^a   Song, Guang Yun ^a   Srivastava, Tumul ^a   Carroll, Kyla Driscoll ^b   Shahabi, Vafa ^b   Manuel, Edwin R ^a   Diamond, Don J ^a   Ellenhorn, Joshua D I ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b ADVAXIS INC   (United States)

Author keywords

Cancer vaccine; Heterologous prime boost immunization; Listeria; Modified vaccinia Ankara; P53; Toll like receptor agonist

Indexed keywords

CANCER VACCINE; CPG OLIGODEOXYNUCLEOTIDE; DOUBLE STRANDED RNA; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN P53; TOLL LIKE RECEPTOR; VACCINIA VACCINE; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; IMMUNIZATION; IMMUNOGENICITY; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR REGRESSION;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CANCER VACCINES; CELL LINE, TUMOR; CELL PROLIFERATION; GENETIC VECTORS; GRAFT REJECTION; HUMANS; IMMUNIZATION, SECONDARY; MICE; MICE, INBRED BALB C; NEOPLASM TRANSPLANTATION; OLIGODEOXYRIBONUCLEOTIDES; RNA, DOUBLE-STRANDED; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77954959459     PISSN: 15249557     EISSN: None     Source Type: Journal    
DOI: 10.1097/CJI.0b013e3181e032c6     Document Type: Article

References (52)

1. Hollstein M, Sidransky D, Vogelstein B, et al. p53 mutations in human cancers. Science. 1991;253:49-53.
2. Harris CC, Hollstein M. Clinical implications of the p53 tumor-suppressor gene. N Engl J Med. 1993;329:1318-1327. (Pubitemid 23317333)
3. Bunz F, Hwang PM, Torrance C, et al. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest. 1999;104:263-269.
4. Zambetti GP, Levine AJ. A comparison of the biological activities of wild-type and mutant p53. FASEB J. 1993;7:855-865.
5. *0201 peptide consensus motif. Cancer Res. 1994;54:1175-1177.
6. Reich NC, Levine AJ. Growth regulation of a cellular tumour antigen, p53, in nontransformed cells. Nature. 1984;308:199-201.
7. Offringa R, Vierboom MP, van der Burg SH, et al. p53: a potential target antigen for immunotherapy of cancer. Ann NY Acad Sci. 2000;910:223-233.
8. McCarty TM, Liu X, Sun JY, et al. Targeting p53 for adoptive T-cell immunotherapy. Cancer Res. 1998;58:2601-2605.
9. Espenschied J, Lamont J, Longmate J, et al. CTLA-4 blockade enhances the therapeutic effect of an attenuated poxvirus vaccine targeting p53 in an established murine tumor model. J Immunol. 2003;170:3401-3407.
10. Daftarian P, Song GY, Ali S, et al. Two distinct pathways of immuno-modulation improve potency of p53 immunization in rejecting established tumors. Cancer Res. 2004;64:5407-5414.
11. Song GY, Gibson G, Haq W, et al. An MVA vaccine overcomes tolerance to human p53 in mice and humans. Cancer Immunol Immunother. 2007;56:1193-1205.
12. Nikitina EY, Clark JI, Van Beynen J, et al. Dendritic cells transduced with full-length wild-type p53 generate antitumor cytotoxic T lymphocytes from peripheral blood of cancer patients. Clin Cancer Res. 2001;7:127-135.
13. Harrington LE, Most RR, Whitton JL, et al. Recombinant vaccinia virus-induced T-cell immunity: quantitation of the response to the virus vector and the foreign epitope. J Virol. 2002;76:3329-3337.
14. Irvine KR, Chamberlain RS, Shulman EP, et al. Enhancing efficacy of recombinant anticancer vaccines with prime/boost regimens that use two different vectors. J Natl Cancer Inst. 1997;89:1595-1601.
15. Schneider J, Gilbert SC, Hannan CM, et al. Induction of CD8+ T cells using heterologous prime-boost immunisation strategies. Immunol Rev. 1999;170:29-38.
16. McConkey SJ, Reece WH, Moorthy VS, et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat Med. 2003;9:729-735.
17. Wallecha A, Maciag PC, Rivera S, et al. Construction and characterization of an attenuated Listeria monocytogenes strain for clinical use in cancer immunotherapy. Clin Vaccine Immunol. 2009;16:96-103.
18. Luo JL, Yang Q, Tong WM, et al. Knock-in mice with a chimeric human/murine p53 gene develop normally and show wild-type p53 responses to DNA damaging agents: a new biomedical research tool. Oncogene. 2001;20:320-328.
19. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 1992;52:1399-1405.
20. Macpherson I, Stoker M. Polyoma transformation of hamster cell clones-an investigation of genetic factors affecting cell competence. Virology. 1962;16:147-151.
21. Dialynas DP, Wilde DB, Marrack P, et al. Characterization of the murine antigenic determinant, designated L3T4a, recognized by monoclonal antibody GK1.5: expression of L3T4a by functional T cell clones appears to correlate primarily with class II MHC antigen-reactivity. Immunol Rev. 1983;74:29-56.
22. Miconnet I, Coste I, Beermann F, et al. Cancer vaccine design: a novel bacterial adjuvant for peptide-specific CTL induction. J Immunol. 2001;166:4612-4619.
23. Wang Z, La Rosa C, Mekhoubad S, et al. Attenuated poxviruses generate clinically relevant frequencies of CMV-specific T cells. Blood. 2004;104:847-856.
24. Peters C, Paterson Y. Enhancing the immunogenicity of bioengineered Listeria monocytogenes by passaging through live animal hosts. Vaccine. 2003;21:1187-1194.
25. Shahabi V, Reyes-Reyes M, Wallecha A, et al. Development of a Listeria monocytogenes based vaccine against prostate cancer. Cancer Immunol Immunother. 2008;57:1301-1313.
26. Whitmore MM, deVeer MJ, Edling A, et al. Synergistic activation of innate immunity by double-stranded RNA and CpG DNA promotes enhanced antitumor activity. Cancer Res. 2004;64:5850-5860.
27. Tormo D, Ferrer A, Bosch P, et al. Therapeutic efficacy of antigen-specific vaccination and toll-like receptor stimulation against established transplanted and autochthonous melanoma in mice. Cancer Res. 2006;66:5427-5435.
28. Cosma A, Nagaraj R, Buhler S, et al. Therapeutic vaccination with MVA-HIV-1 nef elicits Nef-specific T-helper cell responses in chronically HIV-1 infected individuals. Vaccine. 2003;22:21-29.
29. Trevor KT, Hersh EM, Brailey J, et al. Transduction of human dendritic cells with a recombinant modified vaccinia Ankara virus encoding MUC1 and IL-2. Cancer Immunol Immunother. 2001;50:397-407.
30. Drexler I, Antunes E, Schmitz M, et al. Modified vaccinia virus Ankara for delivery of human tyrosinase as melanomaassociated antigen: induction of tyrosi. Cancer Res. 1999;59:4955-4963.
31. Harrop R, Connolly N, Redchenko I, et al. Vaccination of colorectal cancer patients with modified vaccinia Ankara delivering the tumor antigen 5T4 (TroVax) induces immune responses which correlate with disease control: a phase I/II trial. Clin Cancer Res. 2006;12:3416-3424.
32. Marshall JL, Gulley JL, Arlen PM, et al. Phase I study of sequential vaccinations with fowlpox-CEA (6D)-TRICOM alone and sequentially with vaccinia-CEA (6D)-TRICOM, with and without granulocyte-macrophage colony-stimulating factor, in patients with carcinoembryonic antigen-expressing carcinomas. J Clin Oncol. 2005;23:720-731.
33. Busch DH, Pilip IM, Vijh S, et al. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity. 1998;8:353-362.
34. Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev Immunol. 2004;4:812-823.
35. Singh R, Dominiecki ME, Jaffee EM, et al. Fusion to Listeriolysin O and delivery by Listeria monocytogenes enhances the immunogenicity of HER-2/neu and reveals subdominant epitopes in the FVB/N mouse. J Immunol. 2005;175:3663-3673.
36. Pamer EG, Harty JT, Bevan MJ. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes. Nature. 1991;353:852-855.
37. Decatur AL, Portnoy DA. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science. 2000;290:992-995.
38. Maciag PC, Radulovic S, Rothman J. The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine. 2009;27:3975-3983.
39. Chu RS, Targoni OS, Krieg AM, et al. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J Exp Med. 1997;186:1623-1631.
40. Alexopoulou L, Holt AC, Medzhitov R, et al. Recognition of double-stranded RNA and activation of NF-kappaB by Tolllike receptor 3. Nature. 2001;413:732-738.
41. Verdijk RM, Mutis T, Esendam B, et al. Polyriboinosinic polyribocytidylic acid poly (I:C) induces stable maturation of functionally active human dendritic cells. J Immunol. 1999;163:57-61.
42. Gelman AE, Zhang J, Choi Y, et al. Toll-like receptor ligands directly promote activated CD4+ T cell survival. J Immunol. 2004;172:6065-6073.
43. Salem ML, Kadima AN, Cole DJ, et al. Defining the antigenspecific T-cell response to vaccination and poly (I:C)/TLR3 signaling: evidence of enhanced primary and memory CD8 T-cell responses and antitumor immunity. J Immunother. 2005;28:220-228.
44. Cui Z, Qiu F. Synthetic double-stranded RNA poly (I:C) as a potent peptide vaccine adjuvant: therapeutic activity against human cervical cancer in a rodent model. Cancer Immunol Immunother. 2006;55:1267-1279.
45. Hokey DA, Larregina AT, Erdos G, et al. Tumor cell loaded type-1 polarized dendritic cells induce Th1-mediated tumor immunity. Cancer Res. 2005;65:10059-10067.
46. Trinchieri G, Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat Rev Immunol. 2007;7:179-190.
47. Zhu Q, Egelston C, Vivekanandhan A, et al. Toll-like receptor ligands synergize through distinct dendritic cell pathways to induce T cell responses: implications for vaccines. Proc Natl Acad Sci U S A. 2008;105:16260-16265.
48. Bagchi A, Herrup EA, Warren HS, et al. MyD88-dependent and MyD88-independent pathways in synergy, priming, and tolerance between TLR agonists. J Immunol. 2007;178:1164-1171.
49. Smyth MJ, Taniguchi M, Street SE. The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J Immunol. 2000;165:2665-2670.
50. Sivori S, Falco M, Della Chiesa M, et al. CpG and doublestranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci U S A. 2004;101:10116-10121.
51. Van der Burg SH, Menon AG, Redeker A, et al. Induction of p53-specific immune responses in colorectal cancer patients receiving a recombinant ALVAC-p53 candidate vaccine. Clin Cancer Res. 2002;8:1019-1027.
52. Metcalfe S, Wheeler TK, Picken S, et al. P53 autoantibodies in 1006 patients followed up for breast cancer. Breast Cancer Res. 2000;2:438-443.