Immunotherapy for prostate cancer: Biology and therapeutic approaches

Journal of Clinical Oncology

Volumn 29, Issue 27, 2011, Pages 3677-3685

  Cha, Edward ^a   Fong, Lawrence ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; ANTINEOPLASTIC AGENT; APC 8015 F; BCG VACCINE; BISPHOSPHONIC ACID DERIVATIVE; BUDESONIDE; CANCER VACCINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DNA VACCINE; DOCETAXEL; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; INTERLEUKIN 2; IPILIMUMAB; MDX 1106; NILUTAMIDE; PROGRAMMED DEATH 1 RECEPTOR; PROSTATE SPECIFIC ANTIGEN; PROSTATE SPECIFIC ANTIGEN POXVIRUS VACCINE; PROSTVAC VF; PROVENGE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ADRENAL INSUFFICIENCY; ANTIGEN PRESENTING CELL; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER SURGERY; CANCER SURVIVAL; CASTRATION RESISTANT PROSTATE CANCER; CEREBROVASCULAR ACCIDENT; CHILL; COLITIS; DENDRITIC CELL; DIARRHEA; DRUG EFFICACY; DRUG ERUPTION; DRUG FEVER; DRUG INDUCED HEADACHE; ENDOCRINE DISEASE; FATIGUE; HUMAN; HYPERTRANSAMINASEMIA; HYPOTHYROIDISM; MELANOMA; NAUSEA; NONHUMAN; OVERALL SURVIVAL; PAN HYPOPITUITARISM; PATIENT IDENTIFICATION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; PRURITUS; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

BIOLOGICAL MARKERS; HUMANS; IMMUNOTHERAPY; MALE; PROSTATIC NEOPLASMS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; VACCINES;

EID: 80053064081     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2010.34.5025     Document Type: Review

References (78)

1. Markowicz S, Engleman EG: Granulocyte-macrophage colony-stimulating factor promotes differentiation and survival of human peripheral blood dendritic cells in vitro. J Clin Invest 85:955-961, 1990 (Pubitemid 20087502)
2. Iwasaki A, Medzhitov R: Regulation of adaptive immunity by the innate immune system. Science 327:291-295, 2010
3. Fong L, Small EJ: Anti-cytotoxic T-lymphocyte antigen-4 antibody: The first in an emerging class of immunomodulatory antibodies for cancer treatment. J Clin Oncol 26:5275-5283, 2008
4. Brown JA, Dorfman DM, Ma FR, et al: Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production. J Immunol 170:1257-1266, 2003 (Pubitemid 36139491)
5. Fong L, Small EJ: Immunotherapy for prostate cancer. Curr Urol Rep 7:239-246, 2006 (Pubitemid 44624010)
6. Shariat SF, Shalev M, Menesses-Diaz A, et al: Preoperative plasma levels of transforming growth factor beta(1) (TGF-beta(1)) strongly predict progression in patients undergoing radical prostatectomy. J Clin Oncol 19:2856-2864, 2001 (Pubitemid 32538195)
7. Miller AM, Lundberg K, Ozenci V, et al: CD4+CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients. J Immunol 177:7398-7405, 2006 (Pubitemid 44715110)
8. Chang CC, Ogino T, Mullins DW, et al: Defective human leukocyte antigen class I-associated antigen presentation caused by a novel beta2- microglobulin loss-of-function in melanoma cells. J Biol Chem 281:18763-18773, 2006 (Pubitemid 44035537)
9. Chang CC, Campoli M, Restifo NP, et al: Immune selection of hot-spot beta 2-microglobulin gene mutations, HLA-A2 allospecificity loss, and antigen-processing machinery component downregulation in melanoma cells derived from recurrent metastases following immunotherapy. J Immunol 174:1462-1471, 2005
10. Getnet D, Maris CH, Hipkiss EL, et al: Tumor recognition and self-recognition induce distinct transcriptional profiles in antigen-specific CD4 T cells. J Immunol 182:4675-4685, 2009
11. Shafer-Weaver KA, Anderson MJ, Stagliano K, et al: Cutting edge: Tumor-specific CD8+ T cells infiltrating prostatic tumors are induced to become suppressor cells. J Immunol 183:4848-4852, 2009
12. Small EJ, Reese DM, Um B, et al: Therapy of advanced prostate cancer with granulocyte macrophage colony-stimulating factor. Clin Cancer Res 5:1738-1744, 1999 (Pubitemid 29334454)
13. Rini BI, Weinberg V, Bok R, et al: Prostate-specific antigen kinetics as a measure of the biologic effect of granulocyte-macrophage colony-stimulating factor in patients with serologic progression of prostate cancer. J Clin Oncol 21:99-105, 2003
14. Rini BI, Stadler WM, Spielberger RT, et al: Granulocyte-macrophage-colony stimulating factor in metastatic renal cell carcinoma: A phase II trial. Cancer 82:1352-1358, 1998 (Pubitemid 28155398)
15. Spitler LE, Grossbard ML, Ernstoff MS, et al: Adjuvant therapy of stage III and IV malignant melanoma using granulocyte-macrophage colony-stimulating factor. J Clin Oncol 18:1614-1621, 2000 (Pubitemid 30220539)
16. Fong L, Dao V, O'Brien S, et al: Neoadjuvant immunotherapy for prostate cancer with GM-CSF and tumor infiltration by antigen presenting cells. J Clin Oncol 26:147s, 2008 (suppl; abstr 3063)
17. Heiser A, Coleman D, Dannull J, et al: Autologous dendritic cells transfected with prostatespecific antigen RNA stimulate CTL responses against metastatic prostate tumors. J Clin Invest 109:409-417, 2002 (Pubitemid 34141815)
18. Fong L, Brockstedt D, Benike C, et al: Dendritic cell-based xenoantigen vaccination for prostate cancer immunotherapy. J Immunol 167:7150-7156, 2001 (Pubitemid 33144213)
19. Fong L, Brockstedt D, Benike C, et al: Dendritic cells injected via different routes induce immunity in cancer patients. J Immunol 166:4254-4259, 2001 (Pubitemid 32224961)
20. Pandha HS, John RJ, Hutchinson J, et al: Dendritic cell immunotherapy for urological cancers using cryopreserved allogeneic tumour lysatepulsed cells: A phase I/II study. BJU Int 94:412-418, 2004 (Pubitemid 39120190)
21. Kantoff PW, Higano CS, Shore ND, et al: Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363:411-422, 2010
22. Higano CS, Schellhammer PF, Small EJ, 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 115:3670-3679, 2009
23. Small EJ, Schellhammer PF, Higano CS, 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 24:3089-3094, 2006 (Pubitemid 46638945)
24. Kantoff PW, Schuetz TJ, Blumenstein BA, 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 28:1099-1105, 2010
25. Gulley JL, Arlen PM, Madan RA, 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 59:663-674, 2010
26. 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 14:4526-4531, 2008
27. Higano C, Saad F, Somer B, et al: A phase III trial of GVAX immunotherapy for prostate cancer versus docetaxel plus prednisone in asymptomatic, castration-resistant prostate cancer (CRPC). Presented at the Genitourinary Cancers Symposium, Orlando, FL, February 26-28, 2009 (abstr LBA150)
28. Small E, Demkow T, Gerritsen W, et al: A phase III trial of GVAX immunotherapy for prostate cancer in combination with docetaxel versus docetaxel plus prednisone in symptomatic, castration-resistant prostate cancer (CRPC). Presented at the 2009 Genitourinary Cancers Symposium, Orlando, FL, February 26-28, 2009 (abstr 7)
29. Small EJ, Fratesi P, Reese DM, et al: Immunotherapy of hormone-refractory prostate cancer with antigen-loaded dendritic cells. J Clin Oncol 18:3894-3903, 2000
30. Fong L, Ruegg CL, Brockstedt D, et al: Induction of tissue-specific autoimmune prostatitis with prostatic acid phosphatase immunization: Implications for immunotherapy of prostate cancer. J Immunol 159:3113-3117, 1997 (Pubitemid 127482067)
31. McNeel DG, Nguyen LD, Disis ML: Identification of T helper epitopes from prostatic acid phosphatase. Cancer Res 61:5161-5167, 2001 (Pubitemid 32681549)
32. Sheikh NA, Wesley JD, Chadwick E, et al: Characterization of antigen-specific T-cell activation and cytokine expression induced by sipuleucel-T. Presented at the 2011 Genitourinary Cancers Symposium, Orlando, FL, February 17-19, 2011 (abstr 155)
33. George DJ, Nabhan C, Gomella LG, et al: Subsequent treatment with APC8015F and its effect on survival in the control arm of phase III sipuleucel-t studies. Presented at the 2011 Genitourinary Cancers Symposium, Orlando, FL, February 17-19, 2011 (abstr 139)
34. Madan RA, Arlen PM, Mohebtash M, et al: Prostvac-VF: A vector-based vaccine targeting PSA in prostate cancer. Expert Opin Investig Drugs 18:1001-1011, 2009
35. Kaufman HL, Wang W, Manola J, et al: Phase II randomized study of vaccine treatment of advanced prostate cancer (E7897): A trial of the eastern cooperative oncology group. J Clin Oncol 22:2122-2132, 2004 (Pubitemid 41095145)
36. DiPaola RS, Plante M, Kaufman H, et al: A phase I trial of pox PSA vaccines (PROSTVAC-VF) with B7-1, ICAM-1, and LFA-3 co-stimulatory molecules (TRICOM) in patients with prostate cancer J Transl Med 4:1, 2006
37. Arlen PM, Skarupa L, Pazdur M, et al: Clinical safety of a viral vector based prostate cancer vaccine strategy. J Urol 178:1515-1520, 2007 (Pubitemid 47368382)
38. Vergati M, Cereda V, Madan RA, et al: Analysis of circulating regulatory T cells in patients with metastatic prostate cancer pre- versus postvaccination. Cancer Immunol Immunother 60:197-206, 2011
39. Gabrilovich DI, Nagaraj S: Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9:162-174, 2009
40. McNeel DG, Dunphy EJ, Davies JG, et al: Safety and immunological efficacy of a DNA vaccine encoding prostatic acid phosphatase in patients with stage D0 prostate cancer. J Clin Oncol 27:4047-4054, 2009
41. Becker JT, Olson BM, Johnson LE, et al: DNA vaccine encoding prostatic acid phosphatase (PAP) elicits long-term T-cell responses in patients with recurrent prostate cancer. J Immunother 33:639-647, 2010
42. Ward JE, McNeel DG: GVAX: An allogeneic, whole-cell, GM-CSF-secreting cellular immunotherapy for the treatment of prostate cancer Expert Opin Biol Ther 7:1893-1902, 2007 (Pubitemid 350247490)
43. Wada S, Yoshimura K, Hipkiss EL, et al: Cyclophosphamide augments antitumor immunity: Studies in an autochthonous prostate cancer model. Cancer Res 69:4309-4318, 2009
44. Hodi FS, O'Day SJ, McDermott DF, et al: Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363:711-723, 2010
45. Small EJ, Tchekmedyian NS, Rini BI, et al: A pilot trial of CTLA-4 blockade with human anti-CTLA-4 in patients with hormone-refractory prostate cancer. Clin Cancer Res 13:1810-1815, 2007 (Pubitemid 46952950)
46. Fong L, Kwek SS, O'Brien S, et al: Potentiating endogenous antitumor immunity to prostate cancer through combination immunotherapy with CTLA4 blockade and GM-CSF. Cancer Res 69:609-615, 2009
47. Small E, Higano C, Tchekmedyian N, et al: Randomized phase II study comparing 4 monthly doses of ipilimumab (MDX-010) as a single agent or in combination with a single dose of docetaxel in patients with hormone-refractory prostate cancer. J Clin Oncol 24:243s, 2006 (suppl; abstr 4609)
48. Madan RA, Mohebtash M, Arlen PM, et al: Overall survival (OS) analysis of a phase l trial of a vector-based vaccine (PSA-TRICOM) and ipilimumab (ipi) in the treatment of metastatic castration-resistant prostate cancer (mCRPC). J Clin Oncol 28:216s, 2010 (suppl; abstr 2550)
49. Gerritsen W, Van den Eertwegh AJ, De Gruijl T, et al: Expanded phase I combination trial of GVAX immunotherapy for prostate cancer and ipilimumab in patients with metastatic hormone-refractory prostate cancer (mHPRC). J Clin Oncol 26:285s, 2008 (suppl; abstr 5146)
50. Hodi FS: Overcoming immunological tolerance to melanoma: Targeting CTLA-4. Asia Pac J Clin Oncol 6:S16-S23, 2010 (suppl 1)
51. Hersh EM, O'Day SJ, Powderly J, et al: A phase II multicenter study of ipilimumab with or without dacarbazine in chemotherapy-naive patients with advanced melanoma. Invest New Drugs 29:489-498, 2010
52. O'Day SJ, Maio M, Chiarion-Sileni V, et al: Efficacy and safety of ipilimumab monotherapy in patients with pretreated advanced melanoma: A multicenter single-arm phase II study. Ann Oncol 21:1712-1717, 2010
53. Weber J, Thompson JA, Hamid O, et al: A randomized, double-blind, placebo-controlled, phase II study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma. Clin Cancer Res 15:5591-5598, 2009
54. Hirano F, Kaneko K, Tamura H, et al: Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res 65:1089-1096, 2005 (Pubitemid 40216472)
55. Iwai Y, Terawaki S, Honjo T: PD-1 blockade inhibits hematogenous spread of poorly immunogenic tumor cells by enhanced recruitment of effector T cells. Int Immunol 17:133-144, 2005 (Pubitemid 40246578)
56. Sfanos KS, Bruno TC, Meeker AK, et al: Human prostate-infiltrating CD8+ T lymphocytes are oligoclonal and PD-1+. Prostate 69:1694-1703, 2009
57. Ahmadzadeh M, Johnson LA, Heemskerk B, et al: Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 114:1537-1544, 2009
58. Brahmer JR, Drake CG, Wollner I, 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 28:3167-3175, 2010
59. McDermott DF, Drake CG, Sznol M, et al: A phase I study to evaluate safety and antitumor activity of biweekly BMS-936558 (anti-PD-1, MDX-1106/ONO-4538) in patients with RCC and other advanced refractory malignancies. Presented at the 2011 Genitourinary Cancers Symposium, Orlando, FL, February 17-19, 2011 (abstr 331)
60. Ghiringhelli F, Apetoh L, Tesniere A, et al: Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med 15:1170-1178, 2009
61. Green DR, Ferguson T, Zitvogel L, et al: Immunogenic and tolerogenic cell death. Nat Rev Immunol 9:353-363, 2009
62. Apetoh L, Ghiringhelli F, Tesniere A, et al: Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13:1050-1059, 2007 (Pubitemid 47517504)
63. Apetoh L, Ghiringhelli F, Tesniere A, et al: The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol Rev 220:47-59, 2007 (Pubitemid 350045573)
64. Vicari AP, Luu R, Zhang N, et al: Paclitaxel reduces regulatory T cell numbers and inhibitory function and enhances the anti-tumor effects of the TLR9 agonist PF-3512676 in the mouse. Cancer Immunol Immunother 58:615-628, 2009
65. Slovin SF, Beer TM, Higano CS, et al: Initial phase II experience of ipilimumab (IPI) alone and in combination with radiotherapy (XRT) in patients with metastatic castration-resistant prostate cancer (mCRPC). J Clin Oncol 27:268s, 2009 (suppl; abstr 5138)
66. Gulley JL, Arlen PM, Bastian A, et al: Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res 11:3353-3362, 2005 (Pubitemid 40627887)
67. Sutherland JS, Goldberg GL, Hammett MV, et al: Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol 175:2741-2753, 2005 (Pubitemid 41113891)
68. Roden AC, Moser MT, Tri SD, et al: Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol 173:6098-6108, 2004 (Pubitemid 39487766)
69. Mercader M, Bodner BK, Moser MT, et al: T cell infiltration of the prostate induced by androgen withdrawal in patients with prostate cancer. Proc Natl Acad Sci U S A 98:14565-14570, 2001 (Pubitemid 33121432)
70. Ku GY, Yuan J, Page DB, et al: Singleinstitution experience with ipilimumab in advanced melanoma patients in the compassionate use setting: Lymphocyte count after 2 doses correlates with survival. Cancer 116:1767-1775, 2010
71. Bogunovic D, O'Neill DW, Belitskaya-Levy I, et al: Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci U S A 106:20429-20434, 2009
72. Fong L, Small EJ: Immunotherapy for prostate cancer. Curr Oncol Rep 9:226-233, 2007 (Pubitemid 46736354)
73. Hoos A, Eggermont AM, Janetzki S, et al: Improved endpoints for cancer immunotherapy trials. J Natl Cancer Inst 102:1388-1397, 2010
74. Collette L, Burzykowski T, Schröder FH: Prostate-specific antigen (PSA) alone is not an appropriate surrogate marker of long-term therapeutic benefit in prostate cancer trials. Eur J Cancer 42:1344-1350, 2006 (Pubitemid 43922404)
75. Scher HI, Jia X, De Bono JS, et al: Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: A reanalysis of IMMC38 trial data. Lancet Oncol 10:233-239, 2009
76. Wolchok JD, Hoos A, O'Day S, et al: Guidelines for the evaluation of immune therapy activity in solid tumors: Immune-related response criteria. Clin Cancer Res 15:7412-7420, 2009
77. Shimatani K, Nakashima Y, Hattori M, et al: PD-1+ memory phenotype CD4+ T cells expressing C/EBPalpha underlie T cell immunodepression in senescence and leukemia. Proc Natl Acad Sci U S A 106:15807-15812, 2009
78. Willimsky G, Blankenstein T: Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 437:141-146, 2005 (Pubitemid 41613441)