Androgen ablation augments prostate cancer vaccine immunogenicity only when applied after immunization

Prostate

Volumn 69, Issue 6, 2009, Pages 571-584

  Koh, Yi T ^a,b   Gray, Andrew ^a   Higgins, Sean A ^a   Hubby, Bolyn ^c,d   Kast, W Martin ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c AlphaVax Inc   (United States)

^d Liquidia Technologies   (United States)

Author keywords

Hormonal therapy; Immunotherapy; Prostate cancer

Indexed keywords

CYTOKINE; ANDROGEN; CANCER VACCINE; L SELECTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CASTRATION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IMMUNOTHERAPY; LEUKOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; T LYMPHOCYTE; ANIMAL; APOPTOSIS; B LYMPHOCYTE; C57BL MOUSE; CD4+ T LYMPHOCYTE; DBA MOUSE; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; MALE; METHODOLOGY; MIXED LYMPHOCYTE CULTURE; ORCHIECTOMY; PATHOLOGY; PROSTATE TUMOR;

ANDROGENS; ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; IMMUNIZATION; L-SELECTIN; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; ORCHIECTOMY; PROSTATIC NEOPLASMS; T-LYMPHOCYTES;

EID: 65549114089     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.20906     Document Type: Article

References (61)

1. Huggins C, Stevens RE Jr, Hodges CV. Studies of prostate cancer and the effects of castration on advanced cancer of the prostate. Arch Surg 1941;43:209.
2. Huggins C, Hodges CV. Studies on prostatic cancer. I. The effect of castration, of estrogen and androgen injection on serum phosphatases in metastatic carcinoma of the prostate. CA Cancer J Clin 1972;22(4):232-240.
3. Bolla M, Gonzalez D, Warde P, Dubois JB, Mirimanoff R-O, Storme G, Bernier J, Kuten A, Sternberg C, Gil T, Collette L, Pierart M. Improved survival in patients with locally advanced prostate cancer treated with radiotherapy and goserelin. N Engl J Med 1997;337(5):295-300. (Pubitemid 27318990)
4. Messing EM, Manola J, Sarosdy M, Wilding G, Crawford ED, Trump D. Immediate hormonal therapy compared with observation after radical prostatectomy and pelvic lymphadenectomy in men with node-positive prostate cancer. N Engl J Med 1999;341(24):1781-1788.
5. Berthold DR, Sternberg CN, Tannock IF. Management of advanced prostate cancer after first-line chemotherapy. J Clin Oncol 2005;23(32):8247-8252. (Pubitemid 46211562)
6. Petrylak DP. Docetaxel-based chemotherapy trials in androgen-independent prostate cancer: First demonstration of a survival benefit. Curr Oncol Rep 2005;7(3):205-206.
7. Mu LJ, Kyte JA, Kvalheim G, Aamdal S, Dueland S, Hauser M, Hammerstad H, Waehre H, Raabe N, Gaudernack G. Immunotherapy with allotumour mRNA-transfected dendritic cells in androgen-resistant prostate cancer patients. Br J Cancer 2005;93(7):749-756. (Pubitemid 41486433)
8. Schellhammer PF, Hershberg RM. Immunotherapy with autologous antigen presenting cells for the treatment of androgen independent prostate cancer. World J Urol 2005;23(1):47-49. (Pubitemid 40425170)
9. Ragde H, Cavanagh WA, Tjoa BA. Dendritic cell based vaccines: Progress in immunotherapy studies for prostate cancer. J Urol 2004;172(6 Pt 2):2532-2538.
10. Scholz M. Newly diagnosed prostate cancer: Evaluating the options Part 2 of 3. PCRInsights 2003;6:1-11.
11. Posma E, Moes H, Heineman MJ, Faas MM. The effect of testosterone on cytokine production in the specific and nonspecific immune response. Am J Reprod Immunol 2004;52(4):237-243. (Pubitemid 39462193)
12. Cutolo M, Seriolo B, Villaggio B, Pizzorni C, Craviotto C, Sulli A. Androgens and estrogens modulate the immune and inflammatory responses in rheumatoid arthritis. Ann NY Acad Sci 2002;966:131-142. (Pubitemid 34729169)
13. Liva SM, Voskuhl RR. Testosterone acts directly on CD4+ T lymphocytes to increase IL-10 production. J Immunol 2001;167(4):2060-2067. (Pubitemid 32747513)
14. Asirvatham AJ, Schmidt M, Gao B, Chaudhary J. Androgens regulate the immune/inflammatory response and cell survival pathways in rat ventral prostate epithelial cells. Endocrinology 2006;147(1):257-271. (Pubitemid 43004280)
15. Desai KV, Michalowska AM, Kondaiah P, Ward JM, Shih JH, Green JE. Gene expression profiling identifies a unique androgen-mediated inflammatory/immune signature and a PTEN (phosphatase and tensin homolog deleted on chromosome 10)-mediated apoptotic response specific to the rat ventral prostate. Mol Endocrinol 2004;18(12):2895-2907. (Pubitemid 39577914)
16. Grossman CJ. Interactions between the gonadal steroids and the immune system. Science 1985;227(4684):257-261. (Pubitemid 15151935)
17. Sutherland JS, Goldberg GL, Hammett MV, Uldrich AP, Berzins SP, Heng TS, Blazar BR, Millar JL, Malin MA, Chidgey AP, Boyd RL. Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol 2005;175(4):2741-2753. (Pubitemid 41113891)
18. Viselli SM, Stanziale S, Shults K, Kovacs WJ, Olsen NJ. Castration alters peripheral immune function in normal male mice. Immunology 1995;84(2):337-342.
19. Roden AC, Moser MT, Tri SD, Mercader M, Kuntz SM, Dong H, Hurwitz AA, McKean DJ, Celis E, Leibovich BC, Allison JP, Kwon ED. Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol 2004;173(10):6098-6108.
20. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991;9:271-296.
21. Guery JC, Adorini L. Dendritic cells are the most efficient in presenting endogenous naturally processed self-epitopes to class II-restricted T cells. J Immunol 1995;154(2):536-544.
22. Rodriguez-Pinto D, Moreno J. B cells can prime naive CD4+ T cells in vivo in the absence of other professional antigen-presenting cells in a CD154-CD40-dependent manner. Eur J Immunol 2005;35(4):1097-1105. (Pubitemid 40542216)
23. Ahmadi T, Flies A, Efebera Y, Sherr DH. CD40 Ligand-activated, antigen-specific B cells are comparable to mature dendritic cells in presenting protein antigens and major histocompatibility complex class I- and class II-binding peptides. Immunology 2008;124(1):129-140.
24. Pozzi LA, Maciaszek JW, Rock KL. Both dendritic cells and macrophages can stimulate naive CD8 T cells in vivo to proliferate, develop effector function, and differentiate into memory cells. J Immunol 2005;175(4):2071-2081. (Pubitemid 41113812)
25. Rini BI, Weinberg V, Fong L, Conry S, Hershberg RM, Small EJ. Combination immunotherapy with prostatic acid phosphatase pulsed antigen-presenting cells (provenge) plus bevacizumab in patients with serologic progression of prostate cancer after definitive local therapy. Cancer 2006;107(1):67-74. (Pubitemid 43939032)
26. Murphy GP, Tjoa BA, Simmons SJ, Ragde H, Rogers M, Elgamal A, Kenny GM, Troychak MJ, Salgaller ML, Boynton AL. Phase II prostate cancer vaccine trial: Report of a study involving 37 patients with disease recurrence following primary treatment. Prostate 1999;39(1):54-59.
27. Murphy GP, Tjoa BA, Simmons SJ, Rogers MK, Kenny GM, Jarisch J. Higher-dose and less frequent dendritic cell infusions with PSMA peptides in hormone-refractory metastatic prostate cancer patients. Prostate 2000;43(1):59-62. (Pubitemid 30164244)
28. Mercader M, Bodner BK, Moser MT,KwonPS, Park ES, Manecke RG, Ellis TM, Wojcik EM, Yang D, Flanigan RC, Waters WB, Kast WM, Kwon ED. T cell infiltration of the prostate induced by androgen withdrawal in patients with prostate cancer. Proc Natl Acad Sci USA 2001;98(25):14565-14570.
29. Yang D, Holt GE, Velders MP, Kwon ED, Kast WM. Murine six-transmembrane epithelial antigen of the prostate, prostate stem cell antigen, and prostate-specific membrane antigen: Prostate-specific cell-surface antigens highly expressed in prostate cancer of transgenic adenocarcinoma mouse prostate mice. Cancer Res 2001;61(15):5857-5860.
30. Zhigang Z, Wenlv S. Prostate stem cell antigen (PSCA) expression in human prostate cancer tissues: Implications for prostate carcinogenesis and progression of prostate cancer. Jpn J Clin Oncol 2006;36(2):121.
31. Reiter RE, Gu Z, Watabe T, Thomas G, Szigeti K, Davis E, Wahl M, Nisitani S, Yamashiro J, Le Beau MM, Loda M, Witte ON. Prostate stem cell antigen: A cell surface marker overexpressed in prostate cancer. Proc Natl Acad Sci USA 1998;95(4):1735-1740.
32. Gu Z, Thomas G, Yamashiro J, Shintaku IP, Dorey F, Raitano A, Witte ON, Said JW, Loda M, Reiter RE. Prostate stem cell antigen (PSCA) expression increases with high gleason score, advanced stage and bone metastasis in prostate cancer. Oncogene 2000;19(10):1288-1296. (Pubitemid 30160621)
33. Watabe T, Lin M, Ide H, Donjacour AA, Cunha GR, Witte ON, Reiter RE. Growth regeneration, and tumorigenesis of the prostate activates the PSCA promoter. Proc Natl Acad Sci USA 2002;99(1):401-406. (Pubitemid 34060373)
34. Han KR, Seligson DB, Liu X, Horvath S, Shintaku PI, Thomas GV, Said JW, Reiter RE. Prostate stem cell antigen expression is associated with gleason score, seminal vesicle invasion and capsular invasion in prostate cancer. J Urol 2004;171(3):1117-1121. (Pubitemid 38327539)
35. Pushko P, Parker M, Ludwig GV, Davis NL, Johnston RE, Smith JF. Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: Expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology 1997;239(2):389-401.
36. Garcia-Hernandez Mde L, Gray A, Hubby B, Klinger OT, Kast WM. Prostate stem cell antigen vaccination induces a long-term protective immune response against prostate cancer in the absence of autoimmunity. Cancer Res 2008;68(3):861-869.
37. Feltkamp MC, Smits HL, Vierboom MP, Minnaar RP, de Jongh BM, Drijfhout JW, ter Schegget J, Melief CJ, Kast WM. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol 1993;23(9):2242-2249.
38. Melief CJ, Stukart MJ, de Waal LP, Kast WM, Melvold RW. Specificity and regulation of cytotoxic T-lymphocyte responses analyzed with H-2 mutants. Transplant Proc 1983;15(4):2086-2089. (Pubitemid 14197146)
39. Kast WM, Van Twuyver E, Mooijaart RJ, Verveld M, Kamphuis AG, Melief CJ, De Waal LP. Mechanism of skin allograft enhancement across an H-2 class I mutant difference. Evidence for involvement of veto cells. Eur J Immunol 1988;18(12):2105-2108.
40. Arlen PM, Gulley JL, Parker C, Skarupa L, Pazdur M, Panicali D, Beetham P, Tsang KY, Grosenbach DW, Feldman J, Steinberg SM, Jones E, Chen C, Marte J, Schlom J, Dahut W. A randomized phase II study of concurrent docetaxel plus vaccine versus vaccine alone in metastatic androgen-independent prostate cancer. Clin Cancer Res 2006;12(4):1260-1269. (Pubitemid 43342517)
41. Arlen PM, Gulley JL, Todd N, Lieberman R, Steinberg SM, Morin S, Bastian A, Marte J, Tsang KY, Beetham P, Grosenbach DW, Schlom J, Dahut W. Antiandrogen, vaccine and combination therapy in patients with nonmetastatic hormone refractory prostate cancer. J Urol 2005;174(2):539-546. (Pubitemid 40981596)
42. Arlen PM, Madan RA, Hodge JW, Schlom J, Gulley JL. Combining vaccines with conventional therapies for cancer. Update Cancer Ther 2007;2(1):33-39. (Pubitemid 46963735)
43. Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev 2008;223:87-113.
44. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 1993;260(5107):547-549. (Pubitemid 23161621)
45. Presky DH, Minetti LJ, Gillessen S, Wilkinson VL, Wu CY, Gubler U, Chizzonite R, Gately MK. Analysis of the multiple interactions between IL-12 and the high affinity IL-12 receptor complex. J Immunol 1998;160(5):2174-2179. (Pubitemid 28119896)
46. Heinzel FP, Hujer AM, Ahmed FN, Rerko RM. In vivo production and function of IL-12 p40 homodimers. J Immunol 1997;158(9):4381-4388.
47. Gramaglia I, Jember A, Pippig SD, Weinberg AD, Killeen N, Croft M. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J Immunol 2000;165(6):3043-3050.
48. De Smedt T, Smith J, Baum P, Fanslow W, Butz E, Maliszewski C. Ox40 costimulation enhances the development of T cell responses induced by dendritic cells in vivo. J Immunol 2002;168(2):661-670. (Pubitemid 34049566)
49. Kyte JA, Gaudernack G. Immuno-gene therapy of cancer with tumour-mRNA transfected dendritic cells. Cancer Immunol Immunother 2006;55(11):1432-1442. (Pubitemid 44187676)
50. Michiels A, Tuyaerts S, Bonehill A, Corthals J, Breckpot K, Heirman C, Van Meirvenne S, Dullaers M, Allard S, Brasseur F, van der Bruggen P, Thielemans K. Electroporation of immature and mature dendritic cells: Implications for dendritic cell-based vaccines. Gene Ther 2005;12(9):772-782.
51. Drake CG, Doody AD, Mihalyo MA, Huang CT, Kelleher E, Ravi S, Hipkiss EL, Flies DB, Kennedy EP, Long M, McGary PW, Coryell L, Nelson WG, Pardoll DM, Adler AJ. Androgen ablation mitigates tolerance to a prostate/prostate cancer-restricted antigen. Cancer Cell 2005;7(3):239-249. (Pubitemid 40568683)
52. Lees JR, Charbonneau B, Hayball JD, Diener K, Brown M, Matusik R, Cohen MB, Ratliff TL. T-cell recognition of a prostate specific antigen is not sufficient to induce prostate tissue destruction. Prostate 2006;66(6):578-590.
53. Brenner D, Krammer PH, Arnold R. Concepts of activated T cell death. Crit Rev Oncol Hematol 2008;66(1):52-64.
54. Lenardo M, Chan KM, Hornung F, McFarland H, Siegel R, Wang J, Zheng L. Mature T lymphocyte apoptosis - Immune regulation in a dynamic and unpredictable antigenic environment. Annu Rev Immunol 1999;17:221-253. (Pubitemid 29241124)
55. Mittal A, Papa S, Franzoso G, Sen R. NF-kappaB-dependent regulation of the timing of activation-induced cell death of T lymphocytes. J Immunol 2006;176(4):2183-2189. (Pubitemid 43201665)
56. Gray A, Raff AB, Chiriva-Internati M, Chen SY, Kast WM. A paradigm shift in therapeutic vaccination of cancer patients: The need to apply therapeutic vaccination strategies in the preventive setting. Immunol Rev 2008;222:316-327.
57. Sharp HJ, Wansley EK, Garnett CT, Chakraborty M, Camphausen K, Schlom J, Hodge JW. Synergistic antitumor activity of immune strategies combined with radiation. Front Biosci 2007;12:4900-4910.
58. Gulley JL, Arlen PM, Bastian A, Morin S, Marte J, Beetham P, Tsang KY, Yokokawa J, Hodge JW, Menard C, Camphausen K, Coleman CN, Sullivan F, Steinberg SM, Schlom J, Dahut W. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res 2005;11(9):3353-3362. (Pubitemid 40627887)
59. Gelbard A, Garnett CT, Abrams SI, Patel V, Gutkind JS, Palena C, Tsang KY, Schlom J, Hodge JW. Combination chemotherapy and radiation of human squamous cell carcinoma of the head and neck augments CTL-mediated lysis. Clin Cancer Res 2006;12(6):1897-1905.
60. Emens LA, Jaffee EM. Leveraging the activity of tumor vaccines with cytotoxic chemotherapy. Cancer Res 2005;65(18):8059-8064. (Pubitemid 41330564)
61. Nowak AK, Lake RA, Robinson BW. Combined chemoimmunotherapy of solid tumours: Improving vaccines? Adv Drug Deliv Rev 2006;58(8):975-990.