Immunotherapy and therapeutic vaccines in prostate cancer: An update on current strategies and clinical implications

Asian Journal of Andrology

Volumn 16, Issue 3, 2014, Pages 364-371

  Singh, B Harpreet ^a   Gulley, James L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Androgen deprivation; Immunotherapy; Prostate cancer; Therapeutic cancer vaccines

Indexed keywords

ABIRATERONE; BIOLOGICAL MARKER; CANCER VACCINE; DOCETAXEL; ENZALUTAMIDE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; IPILIMUMAB; PREDNISONE; RILIMOGENE GALVACIREPVEC; SIPULEUCEL T; MONOCLONAL ANTIBODY; TISSUE EXTRACT; TUMOR MARKER;

CANCER IMMUNOTHERAPY; CANCER PATIENT; CASTRATION RESISTANT PROSTATE CANCER; DERMATITIS; DRUG TOLERABILITY; ENDOCRINE DISEASE; ENTEROCOLITIS; FEVER; FLU LIKE SYNDROME; HEPATITIS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSTIMULATION; INJECTION SITE REACTION; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TUMOR GROWTH; TUMOR VOLUME; UNSPECIFIED SIDE EFFECT; IMMUNOLOGY; IMMUNOTHERAPY; MALE; PROCEDURES; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; SECONDARY; T LYMPHOCYTE;

ANTIBODIES, MONOCLONAL; CANCER VACCINES; CLINICAL TRIALS, PHASE III AS TOPIC; HUMANS; IMMUNOTHERAPY; MALE; PROSTATIC NEOPLASMS; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; T-LYMPHOCYTES; TISSUE EXTRACTS; TUMOR MARKERS, BIOLOGICAL;

EID: 84894786991     PISSN: 1008682X     EISSN: 17457262     Source Type: Journal    
DOI: 10.4103/1008-682X.122585     Document Type: Review

References (88)

1. Gulley JL, Drake CG. Immunotherapy for prostate cancer: Recent advances, lessons learned, and areas for further research. Clin Cancer Res 2011; 17: 3884-91
2. Bostwick DG, Pacelli A, Blute M, Roche P, Murphy GP. Prostate specific membrane antigen expression in prostatic intraepithelial neoplasia and adenocarcinoma: Study of 184 cases. Cancer 1998; 82: 2256-61
3. Goldfarb DA, Stein BS, Shamszadeh M, Petersen RO. Age-related changes in tissue levels of prostatic acid phosphatase and prostate specific antigen. J Urol 1986; 136: 1266-9
4. Wang MC, Valenzuela LA, Murphy GP, Chu TM. Purification of a human prostate specific antigen. Invest Urol 1979; 17: 159-63
5. Gulley JL. Therapeutic vaccines: The ultimate personalized therapy?. Hum Vaccin Immunother 2013; 9: 219-21
6. Disis ML, Wallace DR, Gooley TA, Dang Y, Slota M, et al. Concurrent trastuzumab and HER2/neu-specific vaccination in patients with metastatic breast cancer. J Clin Oncol 2009; 27: 4685-92
7. Hardwick N, Chain B. Epitope spreading contributes to effective immunotherapy in metastatic melanoma patients Immunotherapy 2011; 3: 731-3
8. Walter S, Weinschenk T, Stenzl A, Zdrojowy R, Pluzanska A, et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 2012; 18: 1254-61
9. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995; 182: 459-65
10. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711-23
11. Patel PH, Kockler DR. Sipuleucel-T: Vaccine for metastatic, asymptomatic, androgen-independent prostate cancer. Ann Pharmacother 2008; 42: 91-8
12. Rini BI. Technology evaluation: PC-8015, Dendreon. Curr Opin Mol Ther 2002; 4: 76-9
13. Small EJ, Schellhammer PF, Higano CS, Redfern CH, Nemunaitis JJ, et al. Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015 in patients with metastatic, asymptomatic hormone refractory prostate cancer. J Clin Oncol 2006; 24: 3089-94
14. Higano CS, Schellhammer PF, Small EJ, Burch PA, Nemunaitis J, et al. Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer. Cancer 2009; 115: 3670-9
15. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Eng J Med 2010; 363: 411-22
16. Small EJ, Higano C, Kantoff P, Whitmore JB, Frohlich MW, et al. Relationship of sipuleucel-T with time to first use of opioid analgesics (TFOA) in patients (pts) with asymptomatic or minimally symptomatic metastatic castration-resistant prostate cancer (mCRPC) on the IMPACT trial [poster]. J Clin Oncol 2013; 31 (suppl 6):Bstr 74
17. Sheikh NA, Petrylak D, Kantoff PW, Dela Rosa C, Stewart FP, et al. Sipuleucel-T immune parameters correlate with survival: N analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer. Cancer Immunol Immunother 2013; 62: 137-47
18. Fong L, Weinberg VK, Corman JM, Amling CL, Stephenson RA, et al. Immune responses in prostate tumor tissue following neoadjuvant sipuleucel-T in patients with localized prostate cancer. J Clin Oncol 2012; 30 (Supp 5):Bstr 181
19. Schellhammer PF, Chodak G, Whitmore JB, Sims R, Frohlich MW, et al. Lower baseline prostate-specific antigen is associated with a greater overall survival benefit from sipuleucel-T in the Immunotherapy for Prostate Adenocarcinoma Treatment (IMPACT) trial. Urology 2013; 81: 1297-302
20. Beer TM, Bernstein GT, Corman JM, Glode LM, Hall SJ, et al. Randomized trial of autologous cellular immunotherapy with sipuleucel-T in androgen-dependent prostate cancer. Clin Cancer Res 2011; 17: 4558-67
21. Madan RA, Arlen PM, Mohebtash M, Hodge JW, Gulley JL. Prostvac-VF: Vector-based vaccine targeting PSA in prostate cancer. Expert Opin Investig Drugs 2009; 18: 1001-11
22. Longo DL. New therapies for castration-resistant prostate cancer. N Engl J Med 2010; 363: 479-81
23. Arlen PM, Skarupa L, Pazdur M, Seetharam M, Tsang KY, et al. Clinical safety of a viral vector based prostate cancer vaccine strategy. J Urol 2007; 178: 1515-20
24. Eder JP, Kantoff PW, Roper K, Xu GX, Bubley GJ, et al. A phase I trial of a recombinant vaccinia virus expressing prostate-specific antigen in advanced prostate cancer. Clin Cancer Res 2000; 6: 1632-8
25. Marshall JL, Hoyer RJ, Toomey MA, Faraguna K, Chang P, et al. Phase I study in advanced cancer patients of a diversified prime-And-boost vaccination protocol using recombinant vaccinia virus and recombinant nonreplicating avipox virus to elicit anti-carcinoembryonic antigen immune responses. J Clin Oncol 2000; 18: 3964-73
26. Gulley J, Chen AP, Dahut W, Arlen PM, Bastian A, et al. Phase I study of a vaccine using recombinant vaccinia virus expressing PSA (rV-PSA) in patients with metastatic androgen-independent prostate cancer. Prostate 2002; 53: 109-17
27. Kaufman HL, Wang W, Manola J, DiPaola RS, Ko YJ, et al. Phase II randomized study of vaccine treatment of advanced prostate cancer (E7897): Trial of the Eastern Cooperative Oncology Group. J Clin Oncol 2004; 22: 2122-32
28. Gulley JL, Arlen PM, Madan RA, Tsang KY, Pazdur MP, et al. Immunologic and prognostic factors associated with overall survival employing a poxviral-based PSA vaccine in metastatic castrate-resistant prostate cancer. Cancer Immunol Immunother 2010; 59: 663-74
29. Kantoff PW, Schuetz TJ, Blumenstein BA, Glode LM, Bilhartz DL, et al. Overall survival analysis of a phase II randomized controlled trial of a Poxviral-based PSA-Targeted immunotherapy in metastatic castration-resistant prostate cancer. J Clin Oncol 2010; 28: 1099-105
30. Campbell CT, Gulley JL, Oyelaran O, Hodge JW, Schlom J, et al. Serum antibodies to blood group A predict survival on PROSTVAC-VF. Clin Cancer Res 2013; 19: 1290-9
31. A Randomized, Double-blind, Phase 3 Efficacy Trial of PROSTVAC-V/F +/- GM-CSF in Men With Asymptomatic or Minimally Symptomatic Metastatic Castrate-Resistant Prostate Cancer (Prospect). Available from: Http: //clinicaltrials.gov/ct2/show/ NCT01322490. [Last accessed on 2013 Aug 29
32. Cell Genesys Halts VITAL-2 GVAX Trial in Advanced Prostate Cancer. 2008. Available from: Http: //phx.corporate-ir.net/phoenix.zhtml̈c=98399 and P=irol-newsArticle and ID=1191052 [Last accessed on 2013 Aug 29
33. Cell Genesys Announces Termination of VITAL-1 Phase 3 Trial of GVAX Immunotherapy for Prostate Cancer. 2008. Available from: Http: //www.drugs.com/ news/cell-genesys-Announces-Termination-vital-1-phase-3-Trial-gvax- immunotherapyprostate-cancer-14159. html [Last accessed on 2013 Aug 29
34. van Elsas A, Hurwitz AA, Allison JP. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-Associated antigen 4 (CTLA-4) and granulocyte/ macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J Exp Med 1999; 190: 355-66
35. van Den Eertwegh AJ, Versluis J, van Den Berg HP, Santegoets SJ, van Moorselaar RJ, et al. Combined immunotherapy with granulocyte-macrophage colony-stimulating factor-Transduced allogeneic prostate cancer cells and ipilimumab in patients with metastatic castration-resistant prostate cancer: Phase 1 dose-escalation trial. Lancet Oncol 2012; 13: 509-17
36. Santegoets SJ, Stam AG, Lougheed SM, Gall H, Scholten PE, et al. T cell profiling reveals high CD4+CTLA-4+T cell frequency as dominant predictor for survival after prostate GVAX/ipilimumab treatment. Cancer Immunol Immunother 2013; 62: 245-56
37. Phan GQ, Yang JC, Sherry RM, Hwu P, Topalian SL, et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-Associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci U S A 2003; 100: 8372-7
38. Weber JS, O'Day S, Urba W, Powderly J, Nichol G, et al. Phase I/II study of ipilimumab for patients with metastatic melanoma. J Clin Oncol 2008; 26: 5950-6
39. Slovin SF, Higano CS, Hamid O, Tejwani S, Harzstark A, et al. Ipilimumab alone or in combination with radiotherapy in metastatic castration-resistant prostate cancer: Results from an open-label, multicenter phase I/II study. Ann Oncol 2013; 24: 1813-21
40. Phase 3 Study of Immunotherapy to Treat Advanced Prostate Cancer. Available from: Http: //www.clinicaltrials.gov/ct2/show/NCT01057810 [Last accessed on 2013 August 29
41. Study of Immunotherapy to Treat Advanced Prostate Cancer. Available from: Http: //www.clinicaltrials.gov/ct2/show/NCT00861614 [Last accessed on 2013 August 29
42. Gerritsen WR, Fizazi A, Drake CG. A randomized, multicenter, double-blind phase 3 trial comparing overall survival (OS) in patients (pts) with post-docetaxel castration resistant prostate cancer (CRPC) and bone metastases treated with ipilimumab (ipi vs placebo (pbo), each following single-dose radiotherapy (RT). European Cancer Congress 2013, Amsterdam, The Netherlands; Abst 2850
43. Harty JT, Badovinac VP. Shaping and reshaping CD8+T-cell memory. Nat Rev Immunol 2008; 8: 107-19
44. Schlom J, Arlen PM, Gulley JL. Cancer vaccines: Moving beyond current paradigms. Clin Cancer Res 2007; 13: 3776-82
45. Madan RA, Gulley JL, Fojo T, Dahut WL. Therapeutic cancer vaccines in prostate cancer: The paradox of improved survival without changes in time to progression. Oncologist 2010; 15: 969-75
46. Stein WD, Gulley JL, Schlom J, Madan RA, Dahut W, et al. Tumor regression and growth rates determined in five intramural NCI prostate cancer trials: The growth rate constant as an indicator of therapeutic efficacy. Clin Cancer Res 2011; 17: 907-17
47. DiPaola RS, Chen Y, Bubley GJ. A phase II study of PROSTVAC-V (vaccinia)/ TRICOM and PROSTVAC-F (fowlpox)/TRICOM with GM-CSF in patients with PSA progression after local therapy for prostate cancer: Results of ECOG 9802 [poster]. 2009 Genitourinary Cancers Symposium, February 26-28, Orlando, Florida, USA:Bstr 108
48. Antonarakis ES, Zahurak ML, Lin J, Keizman D, Carducci MA, et al. Changes in PSA kinetics predict metastasis- free survival in men with PSA-recurrent prostate cancer treated with nonhormonal agents: Combined analysis of 4 phase II trials. Cancer 2012; 118: 1533-42
49. Scher HI, Halabi S, Tannock I, Morris M, Sternberg CN, et al. Design and end points of clinical trials for patients with progressive prostate cancer and castrate levels of testosterone: Recommendations of the Prostate Cancer Clinical Trials Working Group. J Clin Oncol 2008; 26: 1148-59
50. Open Label Study of Sipuleucel-T. Available from: Http: //clinicaltrials.gov/show/ NCT00901342 [Last accessed on 2013 Aug 29
51. Madan RA, Mohebtash M, Schlom J, Gulley JL. Therapeutic vaccines in metastatic castration-resistant prostate cancer: Principles in clinical trial design. Expert Opin Biol Ther 2010; 10: 19-28
52. Antonarakis ES, Drake CG. Combining immunological and androgen-directed approaches: N emerging concept in prostate cancer immunotherapy. Curr Opin Oncol 2012; 24: 258-65
53. Green DR, Ferguson T, Zitvogel L, Kroemer G. Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009; 9: 353-63
54. Garnett CT, Palena C, Chakraborty M, Tsang KY, Schlom J, et al. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res 2004; 64: 7985-94
55. Hodge JW, Garnett CT, Farsaci B, Palena C, Tsang KY, et al. Chemotherapy-induced immunogenic modulation of tumor cells enhances killing by cytotoxic T lymphocytes and is distinct from immunogenic cell death. Int J Cancer 2013; 133: 624-36
56. Garnett CT, Schlom J, Hodge JW. Combination of docetaxel and recombinant vaccine enhances T-cell responses and antitumor activity: Effects of docetaxel on immune enhancement. Clin Cancer Res 2008; 14: 3536-44
57. A phase 2 randomized trial of docetaxel alone or in combination with therapeutic cancer vaccine, CEA-, MUC-1-TRICOM. 2012. Available from: Http: //abstracts. webges.com/viewing/view.php?.congress=esmo2012 and congress-id=370 and publication-id=3526 [Last accessed on 2013 Aug 29
58. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, et al. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 2004; 64: 4328-37
59. Chakraborty M, Abrams SI, Camphausen K, Liu K, Scott T, et al. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 2003; 170: 6338-47
60. Gulley JL, Arlen PM, Bastian A, Morin S, Marte J, et al. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res 2005; 11: 3353-62
61. Nesslinger NJ, Ng A, Tsang KY, Ferrara T, Schlom J, et al. A viral vaccine encoding prostate-specific antigen induces antigen spreading to a common set of self-proteins in prostate cancer patients. Clin Cancer Res 2010; 16: 4046-56
62. Heery CR, Madan RA, Bilusic M, Kim JW, Singh NK, et al. A phase II randomized clinical trial of samarium-153 EDTMP (Sm-153) with or without PSA-TRICOM vaccine in metastatic castration-resistant prostate cancer (mCRPC) after docetaxel. J Clin Oncol 2013; 31(S6):Bstr 102
63. Aragon-Ching JB, Williams KM, Gulley JL. Impact of androgen-deprivation therapy on the immune system: Implications for combination therapy of prostate cancer. Front Biosci 2007; 12: 4957-71
64. Mercader M, Bodner BK, Moser MT, Kwon PS, Park ES, et al. T cell infiltration of the prostate induced by androgen withdrawal in patients with prostate cancer. Natl Acad Sci USA 2001; 98: 14565-70
65. Heng TS, Goldberg GL, Gray DH, Sutherland JS, Chidgey AP, et al. Effects of castration on thymocyte development in two different models of thymic involution. J Immunol 2005; 175: 2982-93
66. Drake CG, Doody AD, Mihalyo MA, Huang CT, Kelleher E, et al. Androgen ablation mitigates tolerance to a prostate/prostate cancer-restricted antigen. Cancer Cell 2005; 7: 239-49
67. Sequencing of Sipuleucel-T and ADT in Men With Non-metastatic Prostate Cancer. Available from: Http: //clinicaltrials.gov/show/NCT01431391 [Last accessed on 2013 Sep 12
68. Antonarakis E, Kibel A, Adams G, et al. A randomized phase II study evaluating the optimal sequencing of sipuleucel-T and androgen Deprivation therapy (ADT in biochemically recurrent prostate cancer (BRPC): Immune results. J Clin Oncol 2013; 31S: Sabstr 5016
69. Madan RA, Gulley JL, Schlom J, et al. Analysis of overall survival in patients with nonmetastatic castration-resistant prostate cancer treated with vaccine, nilutamide, and combination therapy. Clin Cancer Res 2008; 14: 4526-31
70. Bilusic M, Gulley J, Heery C, et al. A randomized phase II study of flutamide with or without PSA-TRICOM in nonmetastatic castration-resistant prostate cancer (CRPC). J Clin Oncol 2011; 29 Suppl 7:Bstr 163
71. Wada S, Yoshimura K, Hipkiss EL, Harris TJ, Yen HR, et al. Cyclophosphamide augments antitumor immunity: Studies in an autochthonous prostate cancer model. Cancer Res 2009; 69: 4309-18
72. A Neoadjuvant Study of Androgen Ablation Combined With Cyclophosphamide and GVAX Vaccine for Localized Prostate Cancer. Available from: Http: //clinicaltrials. gov/show/NCT01696877 [Last accessed on 2013 Oct 4
73. Concurrent Versus Sequential Treatment With Sipuleucel-T and Abiraterone in Men With Metastatic Castrate Resistant Prostate Cancer (mCRPC). Available from: Http: //clinicaltrials.gov/show/NCT01487863 [Last accessed on 2013 Oct 4
74. Koh YT, Gray A, Higgins SA, Hubby B, Kast WM. Androgen ablation augments prostate cancer vaccine immunogenicity only when applied after immunization. Prostate 2009; 69: 571-84
75. Arlen PM, Gulley JL, Parker C, Skarupa L, Pazdur M, et al. A randomized phase II study of concurrent docetaxel plus vaccine versus vaccine alone in metastatic androgen-independent prostate cancer. Clin Cancer Res 2006; 12: 1260-9
76. Fairchok MP, Trementozzi DP, Carter PS, Regnery HL, Carter ER. Effect of prednisone on response to influenza virus vaccine in asthmatic children. Arch Pediatr Adolesc Med 1998; 152: 1191-5
77. Small EJ, Lance RS, Redfern CH, Millard FE, Gardner TA, et al. A randomized phase II trial of sipuleucel-T with concurrent or sequential abiraterone acetate (AA) plus prednisone (P) in metastatic castrate-resistant prostate cancer (mCRPC). J Clin Oncol 2013; 31S:Bstr 5047
78. Small EJ, Lance R, Gardner TA, Karsh LI, Stubbs A, et al. A Phase 2 trial of sipuleucel-T in combination with concurrent or sequential abiraterone acetate in patients with metastatic castrate-resistant prostate cancer [poster]. European Cancer Congress 2013, Amsterdam, The Netherlands; Abstr 2860
79. USFDA: Enzalutamide (XTANDI Capsules). Available from: Http: //www.fda.gov/drugs/ informationondrugs/approveddrugs/ucm317997.htm [Last accessed on 2013 Sep 12
80. Enzalutamide in Combination With PSA-TRICOM in Patients With Non-Metastatic Castration Sensitive Prostate Cancer. [4 October 2013]; Available from: Http: // www.clinicaltrials.gov/ct2/show/NCT01875250 [Last accessed on
81. Enzalutamide With or Without Vaccine Therapy for Advanced Prostate Cancer. [4 October 2013]; Available from: Http: //www.clinicaltrials.gov/ct2/ show/ NCT01867333 [Last accessed on
82. Boehm AL, Higgins J, Franzusoff A, Schlom J, Hodge JW. Concurrent vaccination with two distinct vaccine platforms targeting the same antigen generates phenotypically and functionally distinct T-cell populations. Cancer Immunol Immunother 2010; 59: 397-408
83. Madan RA, Mohebtash M, Arlen PM, Vergati M, Rauckhorst M, et al. Ipilimumab and a poxviral vaccine targeting prostate-specific antigen in metastatic castration-resistant prostate cancer: Phase 1 dose-escalation trial. Lancet Oncol 2012; 13: 501-8
84. Hurwitz AA, Foster BA, Kwon ED, Powderly JD, Picus J, et al. Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cancer Res 2000; 60: 2444-8
85. Wada S, Jackson CM, Yoshimura K, Powderly JD, Picus J, et al. Sequencing CTLA-4 blockade with cell-based immunotherapy for prostate cancer. J Transl Med 2013; 11: 89
86. Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, et al. Phase I study of single-Agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: Safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol 2010; 28: 3167-75
87. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366: 2443-54
88. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366: 2455-65.