VRP immunotherapy targeting neu: Treatment efficacy and evidence for immunoediting in a stringent rat mammary tumor model

Breast Cancer Research and Treatment

Volumn 106, Issue 3, 2007, Pages 371-382

  Laust, Amanda K ^b   Sur, Brandon W ^a   Wang, Kehui ^a   Hubby, Bolyn ^c   Smith, Jonathan F ^c   Nelson, Edward L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c AlphaVax Inc   (United States)

Author keywords

Breast cancer; Immunoediting; Immunoselection; Immunotherapy; Neu; Venezuelan Equine Encephalitis replicon; VRP

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST TUMOR; CANCER IMMUNOTHERAPY; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; FEMALE; IMMUNE RESPONSE; IMMUNOTHERAPY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; RAT; REPLICON; STATISTICAL ANALYSIS; TREATMENT PLANNING; TUMOR GROWTH; TUMOR IMMUNITY; VIRUS LIKE AGENT;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NEOPLASM; DENDRITIC CELLS; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; FEMALE; GENETIC VECTORS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; MAMMARY NEOPLASMS, EXPERIMENTAL; MOLECULAR SEQUENCE DATA; RATS; RATS, INBRED F344; REPLICON;

EID: 35648935417     PISSN: 01676806     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10549-007-9517-8     Document Type: Article

References (81)

1. Rosenberg SA, Yang JC, Restifo NP (2004) Cancer immunotherapy: moving beyond current vaccines. Nat Med 10(9):909-915
2. Bishop MR, Fowler DH, Marchigiani D, Castro K, Kasten-Sportes C, Steinberg SM, Gea-Banacloche JC, Dean R, Chow CK, Carter C et al. (2004) Allogeneic lymphocytes induce tumor regression of advanced metastatic breast cancer. J Clin Oncol 22(19):3886-3892
3. Dean RM, Bishop MR (2004) Allogeneic hematopoietic stem cell transplantation for lymphoma. Clin Lymphoma 4(4):238-249
4. Levy R (2004) Vaccines in lymphoma. Clin Adv Hematol Oncol 2(7):426-427
5. Schattenberg AV, Dolstra H (2005) Cellular adoptive immunotherapy after allogeneic stem cell transplantation. Curr Opin Oncol 17(6):617-621
6. Igney FH, Krammer PH (2002) Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol 71(6):907-920
7. Khong HT, Restifo NP (2002) Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat Immunol 3(11):999-1005
8. Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S (2000) Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 74:181-273
9. Riker A, Cormier J, Panelli M, Kammula U, Wang E, Abati A, Fetsch P, Lee KH, Steinberg S, Rosenberg S et al. (1999) Immune selection after antigen-specific immunotherapy of melanoma. Surgery 126(2):112-120
10. Slingluff CL Jr, Colella TA, Thompson L, Graham DD, Skipper JC, Caldwell J, Brinckerhoff L, Kittlesen DJ, Deacon DH, Oei C et al. (2000) Melanomas with concordant loss of multiple melanocytic differentiation proteins: immune escape that may be overcome by targeting unique or undefined antigens. Cancer Immunol Immunother 48(12):661-672
11. Powell DJ Jr, Dudley ME, Robbins PF, Rosenberg SA (2005) Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105(1):241-250
12. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, Finkelstein SE, Theoret MR, Rosenberg SA, Restifo NP (2005) Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8(+) T cells. J Clin Invest 115(6):1616-1626
13. Huang J, Khong HT, Dudley ME, El-Gamil M, Li YF, Rosenberg SA, Robbins PF (2005) Survival, persistence, and progressive differentiation of adoptively transferred tumor-reactive T cells associated with tumor regression. J Immunother 28(3):258-267
14. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA et al. (2005) Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23(10):2346-2357
15. Zhou J, Dudley ME, Rosenberg SA, Robbins PF (2005) Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J Immunother 28(1):53-62
16. Timmerman JM, Levy R (2004) Cancer vaccines: pessimism in check. Nat Med 10(12):1279; author reply 1279-1280
17. Rosenberg SA, Yang JC, Restifo NP (2004) Reply-cancer vaccines: pessimism in check. Nat Med 10(12):1279-1280
18. Amici A, Smorlesi A, Noce G, Santoni G, Cappelletti P, Capparuccia L, Coppari R, Lucciarini R, Petrelli C, Provinciali M (2000) DNA vaccination with full-length or truncated neu induces protective immunity against the development of spontaneous mammary tumors in HER-2/neu transgenic mice. Gene Ther 7(8):703-706
19. Amici A, Venanzi FM, Concetti A (1998) Genetic immunization against neu/erbB2 transgenic breast cancer. Cancer Immunol Immunother 47(4):183-190
20. Cefai D, Morrison BW, Sckell A, Favre L, Balli M, Leunig M, Gimmi CD (1999) Targeting HER-2/neu for active-specific immunotherapy in a mouse model of spontaneous breast cancer. Int J Cancer 83(3):393-400
21. Chen SA, Tsai MH, Wu FT, Hsiang A, Chen YL, Lei HY, Tzai TS, Leung HW, Jin YT, Hsieh CL et al. (2000) Induction of antitumor immunity with combination of HER2/neu DNA vaccine and interleukin 2 gene-modified tumor vaccine. Clin Cancer Res 6(11):4381-4388
22. Chen Y, Emtage P, Zhu Q, Foley R, Muller W, Hitt M, Gauldie J, Wan Y (2001) Induction of ErbB-2/neu-specific protective and therapeutic antitumor immunity using genetically modified dendritic cells: enhanced efficacy by cotransduction of gene encoding IL-12. Gene Ther 8(4):316-323
23. Clinchy B, Gazdar A, Rabinovsky R, Yefenof E, Gordon B, Vitetta ES (2000) The growth and metastasis of human, HER-2/neu-overexpressing tumor cell lines in male SCID mice. Breast Cancer Res Treat 61(3):217-228
24. Esserman LJ, Lopez T, Montes R, Bald LN, Fendly BM, Campbell MJ (1999) Vaccination with the extracellular domain of p185neu prevents mammary tumor development in neu transgenic mice. Cancer Immunol Immunother 47(6):337-342
25. Disis ML, Bernhard H, Shiota FM, Hand SL, Gralow JR, Huseby ES, Gillis S, Cheever MA (1996) Granulocyte-macrophage colony-stimulating factor: an effective adjuvant for protein and peptide-based vaccines. Blood 88(1):202-210
26. Disis ML, Gralow JR, Bernhard H, Hand SL, Rubin WD, Cheever MA (1996) Peptide-based, but not whole protein, vaccines elicit immunity to HER-2/neu, oncogenic self-protein. J Immunol 156(9):3151-3158
27. Disis ML, Shiota FM, Cheever MA (1998) Human HER-2/neu protein immunization circumvents tolerance to rat neu: a vaccine strategy for 'self' tumour antigens. Immunology 93(2):192-199
28. Hess AD, Thoburn C, Chen W, Miura Y, Van der Wall E (2001) The N-terminal flanking region of the invariant chain peptide augments the immunogenicity of a cryptic "self" epitope from a tumor-associated antigen. Clin Immunol 101(1):67-76
29. Bhattachary R, Bukkapatnam R, Prawoko I, Soto J, Morgan M, Salup RR (2002) Efficacy of vaccination with plasmid DNA encoding for HER2/neu or HER2/neu-eGFP fusion protein against prostate cancer in rats. Int Immunopharmacol 2(6):783-796
30. Nelson EL, Smith J (2004) Alphaviral-based strategies for the immunotherapy of cancer. In: Morse M, Lyerly HK, Clay T (eds) Handbook of cancer vaccines. Humana Press, Totowa, NJ, pp 203-224
31. Pushko P, Parker M, Ludwig GV, Davis NL, Johnston RE, Smith JF (1997) Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology 239(2):389-401
32. MacDonald GH, Johnston RE (2000) Role of dendritic cell targeting in Venezuelan equine encephalitis virus pathogenesis. J Virol 74(2):914-922
33. Moran TP, Collier M, McKinnon KP, Davis NL, Johnston RE, Serody JS (2005) A novel viral system for generating antigen-specific T cells. J Immunol 175(5):3431-3438
34. Nishimoto KP, Laust AK, Wang K, Kamrud KI, Hubby B, Smith JF, Nelson EL (2006) Restricted and selective tropism of a Venezuelan equine encephalitis virus-derived replicon vector for human dendritic cells. Viral Immunol (in press)
35. Liljestrom P, Garoff H (1991) A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (NY) 9(12):1356-1361
36. Nelson EL, Prieto D, Alexander TG, Pushko P, Lofts LA, Rayner JO, Kamrud KI, Fralish B, Smith JF (2003) Venezuelan equine encephalitis replicon immunization overcomes intrinsic tolerance and elicits effective anti-tumor immunity to the 'self' tumor-associated antigen, neu in a rat mammary tumor model. Breast Cancer Res Treat 82(3):169-183
37. Wang X, Wang JP, Maughan MF, Lachman LB (2005) Alphavirus replicon particles containing the gene for HER2/neu inhibit breast cancer growth and tumorigenesis. Breast Cancer Res 7(1):R145-155
38. Velders MP, McElhiney S, Cassetti MC, Eiben GL, Higgins T, Kovacs GR, Elmishad AG, Kast WM, Smith LR (2001) Eradication of established tumors by vaccination with Venezuelan equine encephalitis virus replicon particles delivering human papillomavirus 16 E7 RNA. Cancer Res 61(21):7861-7867
39. Cassetti MC, McElhiney SP, Shahabi V, Pullen JK, Le Poole IC, Eiben GL, Smith LR, Kast WM (2004) Antitumor efficacy of Venezuelan equine encephalitis virus replicon particles encoding mutated HPV16 E6 and E7 genes. Vaccine 22(3-4):520-527
40. Goldberg SM, Bartido SM, Gardner JP, Guevara-Patino JA, Montgomery SC, Perales MA, Maughan MF, Dempsey J, Donovan GP, Olson WC et al. (2005) Comparison of two cancer vaccines targeting tyrosinase: plasmid DNA and recombinant alphavirus replicon particles. Clin Cancer Res 11(22):8114-8121
41. Mendiratta SK, Thai G, Eslahi NK, Thull NM, Matar M, Bronte V, Pericle F (2001) Therapeutic tumor immunity induced by polyimmunization with melanoma antigens gp100 and TRP-2. Cancer Res 61(3):859-863
42. Bellone M, Cantarella D, Castiglioni P, Crosti MC, Ronchetti A, Moro M, Garancini MP, Casorati G, Dellabona P (2000) Relevance of the tumor antigen in the validation of three vaccination strategies for melanoma. J Immunol 165(5):2651-2656
43. Bronte V, Apolloni E, Ronca R, Zamboni P, Overwijk WW, Surman DR, Restifo NP, Zanovello P (2000) Genetic vaccination with "self" tyrosinase-related protein 2 causes melanoma eradication but not vitiligo. Cancer Res 60(2):253-258
44. Attia MA, DeOme KB, Weiss DW (1965) Immunology of spontaneous mammary carcinomas in mice II. Resistance to a rapidly and a slowly developing tumor. Cancer Res 25:451-457
45. Houghton AN (1994) Cancer antigens: immune recognition of self and altered self. J Exp Med 180(1):1-4
46. Tuttle TM, Anderson BW, Thompson WE, Lee JE, Sahin A, Smith TL, Grabstein KH, Wharton JT, Ioannides CG, Murray JL (1998) Proliferative and cytokine responses to class II HER-2/neu-associated peptides in breast cancer patients. Clin Cancer Res 4(8):2015-2024
47. Disis ML, Grabstein KH, Sleath PR, Cheever MA (1999) Generation of immunity to the HER-2/neu oncogenic protein in patients with breast and ovarian cancer using a peptide-based vaccine. Clin Cancer Res 5(6):1289-1297
48. Knutson KL, Disis ML (2002) Clonal diversity of the T-cell population responding to a dominant HLA-A2 epitope of HER-2/neu after active immunization in an ovarian cancer patient. Hum Immunol 63(7):547-557
49. Brossart P, Stuhler G, Flad T, Stevanovic S, Rammensee HG, Kanz L, Brugger W (1998) Her-2/neu-derived peptides are tumor-associated antigens expressed by human renal cell and colon carcinoma lines and are recognized by in vitro induced specific cytotoxic T lymphocytes. Cancer Res 58(4):732-736
50. Kono K, Takahashi A, Amemiya H, Ichihara F, Sugai H, Iizuka H, Fujii H, Matsumoto Y (2002) Frequencies of HER-2/neu overexpression relating to HLA haplotype in patients with gastric cancer. Int J Cancer 98(2):216-220
51. Perez SA, Sotiropoulou PA, Sotiriadou NN, Mamalaki A, Gritzapis AD, Echner H, Voelter W, Pawelec G, Papamichail M, Baxevanis CN (2002) HER-2/neu-derived peptide 884-899 is expressed by human breast, colorectal and pancreatic adenocarcinomas and is recognized by in-vitro-induced specific CD4(+) T cell clones. Cancer Immunol Immunother 50(11):615-624
52. Scardino A, Alves P, Gross DA, Tourdot S, Graff-Dubois S, Angevin E, Firat H, Chouaib S, Lemonnier F, Nadler LM et al. (2001) Identification of HER-2/neu immunogenic epitopes presented by renal cell carcinoma and other human epithelial tumors. Eur J Immunol 31(11):3261-3270
53. Schwaab T, Lewis LD, Cole BF, Deo Y, Fanger MW, Wallace P, Guyre PM, Kaufman PA, Heaney JA, Schned AR et al. (2001) Phase I pilot trial of the bispecific antibody MDXH210 (anti-Fc gamma RI X anti-HER-2/neu) in patients whose prostate cancer overexpresses HER-2/neu. J Immunother 24(1):79-87
54. Pegram M, Slamon D (2000) Biological rationale for HER2/neu (c-erbB2) as a target for monoclonal antibody therapy. Semin Oncol 27(5 Suppl 9):13-19
55. Ricci C, Polito L, Nanni P, Landuzzi L, Astolfi A, Nicoletti G, Rossi I, De Giovanni C, Bolognesi A, Lollini PL (2002) HER/erbB receptors as therapeutic targets of immunotoxins in human rhabdomyosarcoma cells. J Immunother 25(4):314-323
56. Yamamoto T, Ikawa S, Akiyama T, Semba K, Nomura N, Miyajima N, Saito T, Toyoshima K (1986) Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor. Nature 319(6050):230-234
57. Baxevanis CN, Sotiriadou NN, Gritzapis AD, Sotiropoulou PA, Perez SA, Cacoullos NT, Papamichail M (2006) Immunogenic HER-2/neu peptides as tumor vaccines. Cancer Immunol Immunother 55(1):85-95
58. Choudhury A, Kiessling R (2004) Her-2/neu as a paradigm of a tumor-specific target for therapy. Breast Dis 20:25-31
59. Curigliano G, Spitaleri G, Pietri E, Rescigno M, de Braud F, Cardillo A, Munzone E, Rocca A, Bonizzi G, Brichard V et al. (2006) Breast cancer vaccines: a clinical reality or fairy tale? Ann Oncol 17(5):750-762
60. Disis ML, Schiffman K, Salazar LG, Almand B, Knutson KL (2003) HER-2/neu vaccines. Cancer Chemother Biol Response Modif 21:275-285
61. Emens LA, Reilly RT, Jaffee EM (2005) Breast cancer vaccines: maximizing cancer treatment by tapping into host immunity. Endocr Relat Cancer 12(1):1-17
62. Sauer G, Kurzeder C, Heilmann V, Kreienberg R, Deissler H (2005) Immunotherapy and cancer vaccines in the management of breast cancer. Curr Pharm Des 11(27):3475-3483
63. Machiels JP, Reilly RT, Emens LA, Ercolini AM, Lei RY, Weintraub D, Okoye FI, Jaffee EM (2001) 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 61(9):3689-3697
64. Wolpoe ME, Lutz ER, Ercolini AM, Murata S, Ivie SE, Garrett ES, Emens LA, Jaffee EM, Reilly RT (2003) HER-2/neu-specific monoclonal antibodies collaborate with HER-2/neu-targeted granulocyte macrophage colony-stimulating factor secreting whole cell vaccination to augment CD8+ T cell effector function and tumor-free survival in Her-2/neu-transgenic mice. J Immunol 171(4):2161-2169
65. Zitvogel L, Tesniere A, Kroemer G (2006) Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat Rev Immunol 6(10):715-727
66. Seliger B (2005) Strategies of tumor immune evasion. BioDrugs 19(6):347-354
67. Strater J, Hinz U, Hasel C, Bhanot U, Mechtersheimer G, Lehnert T, Moller P (2005) Impaired CD95 expression predisposes for recurrence in curatively resected colon carcinoma: clinical evidence for immunoselection and CD95L mediated control of minimal residual disease. Gut 54(5):661-665
68. Pawelec G (2004) Immunotherapy and immunoselection-tumour escape as the final hurdle. FEBS Lett 567(1):63-66
69. Garcia-Lora A, Algarra I, Garrido F (2003) MHC class I antigens, immune surveillance, and tumor immune escape. J Cell Physiol 195(3):346-355
70. Garcia-Lora A, Algarra I, Gaforio JJ, Ruiz-Cabello F, Garrido F (2001) Immunoselection by T lymphocytes generates repeated MHC class I-deficient metastatic tumor variants. Int J Cancer 91(1):109-119
71. Dunn GP, Koebel CM, Schreiber RD (2006) Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6(11):836-848
72. Knutson KL, Lu H, Stone B, Reiman JM, Behrens MD, Prosperi CM, Gad EA, Smorlesi A, Disis ML (2006) Immunoediting of cancers may lead to epithelial to mesenchymal transition. J Immunol 177(3):1526-1533
73. Smyth MJ, Dunn GP, Schreiber RD (2006) Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 90:1-50
74. Manjili MH, Arnouk H, Knutson KL, Kmieciak M, Disis ML, Subjeck JR, Kazim AL (2006) Emergence of immune escape variant of mammary tumors that has distinct proteomic profile and a reduced ability to induce "danger signals". Breast Cancer Res Treat 96(3):233-241
75. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 3(11):991-998
76. Gardner JP, Durso RJ, Jacques S, Arrigale RR, Maughan M, Donovan GP, Schulke N, Israel RJ, Olson WC (2005) Novel prime-boost combinations of PSMA-based vaccines for prostate cancer. In: 41st Annual Meeting ASCO: May 13-17, 2005; Orlando, FL; Abstract 2572
77. Caley IJ, Betts MR, Davis NL, Swanstrom R, Frelinger JA, Johnston RE (1999) Venezuelan equine encephalitis virus vectors expressing HIV-1 proteins: vector design strategies for improved vaccine efficacy. Vaccine 17(23-24):3124-3135
78. Caley IJ, Betts MR, Irlbeck DM, Davis NL, Swanstrom R, Frelinger JA, Johnston RE (1997) Humoral, mucosal, and cellular immunity in response to a human immunodeficiency virus type 1 immunogen expressed by a Venezuelan equine encephalitis virus vaccine vector. J Virol 71(4):3031-3038
79. Davis NL, Caley IJ, Brown KW, Betts MR, Irlbeck DM, McGrath KM, Connell MJ, Montefiori DC, Frelinger JA, Swanstrom R et al. (2000) Vaccination of macaques against pathogenic simian immunodeficiency virus with Venezuelan equine encephalitis virus replicon particles [published erratum appears in J Virol 2000 Apr; 74(7):3430]. J Virol 74(1):371-378
80. Davis NL, West A, Reap E, MacDonald G, Collier M, Dryga S, Maughan M, Connell M, Walker C, McGrath K et al. (2002) Alphavirus replicon particles as candidate HIV vaccines. IUBMB Life 53(4-5):209-211
81. Wilson JA, Hart MK (2001) Protection from Ebola virus mediated by cytotoxic T lymphocytes specific for the viral nucleoprotein. J Virol 75(6):2660-2664