Emerging immunotherapies for bladder cancer

Current Opinion in Oncology

Volumn 27, Issue 3, 2015, Pages 191-200

  Kim, Joseph W ^a   Tomita, Yusuke ^b   Trepel, Jane ^b   Apolo, Andrea B ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

adoptive T cell therapy; B7 H3; bladder cancer; immune escape; immunotherapy; NY ESO 1; OX40; programmed death ligand 1; urothelial carcinoma

Indexed keywords

B7 H3 ANTIGEN; CANCER VACCINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FALIMAREV; IMMUNE CHECKPOINT INHIBITOR; IMMUNOMODULATING AGENT; MELANOMA ANTIGEN 3; NY ESO 1 ANTIGEN; PROGRAMMED DEATH 1 LIGAND 1; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VESIGENURTUCEL L; ANTINEOPLASTIC AGENT;

ADOPTIVE TRANSFER; ANTIGEN PRESENTATION; BLADDER CARCINOMA; CANCER IMMUNOTHERAPY; CANCER PATIENT; CLINICAL TRIAL (TOPIC); CONTROLLED CLINICAL TRIAL (TOPIC); CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; HUMAN; IMMUNE EVASION; IMMUNOREGULATION; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; TUMOR CELL; UPREGULATION; CARCINOMA, TRANSITIONAL CELL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; PATHOLOGY; URINARY BLADDER NEOPLASMS; UROTHELIUM;

ANTINEOPLASTIC AGENTS; CANCER VACCINES; CARCINOMA, TRANSITIONAL CELL; HUMANS; IMMUNOTHERAPY; RANDOMIZED CONTROLLED TRIALS AS TOPIC; T-LYMPHOCYTES, CYTOTOXIC; URINARY BLADDER NEOPLASMS; UROTHELIUM;

EID: 84928468444     PISSN: 10408746     EISSN: 1531703X     Source Type: Journal    
DOI: 10.1097/CCO.0000000000000177     Document Type: Review

References (89)

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90.
2. Dudek AM, Grotenhuis AJ, Vermeulen SH, et al. Urinary bladder cancer susceptibility markers. What do we know about functional mechanisms? Int J Mol Sci 2013; 14:12346-12366.
3. Sylvester RJ, van der Meijden AP, Oosterlinck W, et al. Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol 2006; 49:465-466.
4. Milowsky MI, Kim WY. The geriatrics and genetics behind bladder cancer. Am Soc Clin Oncol Educ Book 2014; e192-e195.
5. Raghavan D, Burgess E, Gaston KE, et al. Neoadjuvant and adjuvant chemotherapy approaches for invasive bladder cancer. Semin Oncol 2012; 39:588-597.
6. Grossman HB, Natale RB, Tangen CM, et al. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med 2003; 349:859-866.
7. Griffiths G, Hall R, Sylvester R, et al. International phase III trial assessing neoadjuvant cisplatin, methotrexate, and vinblastine chemotherapy for muscle-invasive bladder cancer: long-term results of the BA06 30894 trial. J Clin Oncol 2011; 29:2171-2177.
8. Advanced Bladder Cancer (ABC) Meta-Analysis Collaboration. Neoadjuvant chemotherapy in invasive bladder cancer: update of a systematic review and meta-analysis of individual patient data advanced bladder cancer (ABC) metaanalysis collaboration. Eur Urol 2005; 48:202-205.
9. Advanced Bladder Cancer (ABC) Meta-Analysis Collaboration. Neoadjuvant chemotherapy in invasive bladder cancer: a systematic review and metaanalysis. Lancet 2003; 361:1927-1934.
10. Arcangeli G, Arcangeli S, Strigari L. A systematic review and meta-analysis of clinical trials of bladder-sparing trimodality treatment for muscle-invasive bladder cancer (MIBC). Crit Rev Oncol Hematol 2014. [Epub ahead of print]
11. Logothetis CJ, Dexeus FH, Finn L, et al. A prospective randomized trial comparing MVAC and CISCA chemotherapy for patients with metastatic urothelial tumors. J Clin Oncol 1990; 8:1050-1055.
12. Loehrer PJ Sr, Einhorn LH, Elson PJ, et al. A randomized comparison of cisplatin alone or in combination with methotrexate, vinblastine, and doxorubicin in patients with metastatic urothelial carcinoma: a cooperative group study. J Clin Oncol 1992; 10:1066-1073.
13. Saxman SB, Propert KJ, Einhorn LH, et al. Long-term follow-up of a phase III intergroup study of cisplatin alone or in combination with methotrexate, vinblastine, and doxorubicin in patients with metastatic urothelial carcinoma: a cooperative group study. J Clin Oncol 1997; 15:2564-2569.
14. von der Maase H, Hansen SW, Roberts JT, et al. Gemcitabine and cisplatin versus methotrexate, vinblastine, doxorubicin, and cisplatin in advanced or metastatic bladder cancer: results of a large, randomized, multinational, multicenter, phase III study. J Clin Oncol 2000; 18:3068-3077.
15. von der Maase H, Sengelov L, Roberts JT, et al. Long-term survival results of a randomized trial comparing gemcitabine plus cisplatin, with methotrexate, vinblastine, doxorubicin, plus cisplatin in patients with bladder cancer. J Clin Oncol 2005; 23:4602-4608.
16. Sternberg CN, de Mulder P, Schornagel JH, et al. Seven year update of an EORTC phase III trial of high-dose intensity M-VAC chemotherapy and G-CSF versus classic M-VAC in advanced urothelial tract tumours. Eur J Cancer 2006; 42:50-54.
17. Galsky MD, Chen GJ, Oh WK, et al. Comparative effectiveness of cisplatinbased and carboplatin-based chemotherapy for treatment of advanced urothelial carcinoma. Ann Oncol 2012; 23:406-410.
18. De Santis M, Bellmunt J, Mead G, et al. Randomized phase II/III trial assessing gemcitabine/carboplatin and methotrexate/carboplatin/vinblastine in patients with advanced urothelial cancer who are unfit for cisplatin-based chemotherapy: EORTC study 30986. J Clin Oncol 2012; 30:191-199.
19. Kantoff PW, Higano CS, Shore ND, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 2010; 363:411-422.
20. Hodi FS, ODay SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-723.
21. Brandau S, Suttmann H. Thirty years of BCG immunotherapy for nonmuscle invasive bladder cancer: a success story with room for improvement. Biomed Pharmacother 2007; 61:299-305.
22. Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013; 39:1-10.
23. Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res 2013; 19:5300-5309.
24. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-264.
25. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-2454.
26. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-2465.
27. Wolchok JD, Kluger H, Callahan MK, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-133.
28. Herbst RS, Soria JC, Kowanetz M, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014; 515:563-567.
29. Powles T, Eder JP, Fine GD, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 2014; 515:558-562.
30. Guo C, Manjili MH, Subjeck JR, et al. Therapeutic cancer vaccines: past, present, and future. Adv Cancer Res 2013; 119:421-475.
31. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008; 26:677-704.
32. Sharpe AH, Wherry EJ, Ahmed R, Freeman GJ. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol 2007; 8:239-245.
33. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 2010; 236:219-242.
34. Nakanishi J, Wada Y, Matsumoto K, et al. Overexpression of B7-H1 (PD-L1) significantly associates with tumor grade and postoperative prognosis in human urothelial cancers. Cancer Immunol Immunother 2007; 56:1173-1182.
35. Inman BA, Sebo TJ, Frigola X, et al. PD-L1 (B7-H1) expression by urothelial carcinoma of the bladder and BCG-induced granulomata: associations with localized stage progression. Cancer 2007; 109:1499-1505.
36. Wang Y, Zhuang Q, Zhou S, et al. Costimulatory molecule B7-H1 on the immune escape of bladder cancer and its clinical significance. J Huazhong Univ Sci Technolog Med Sci 2009; 29:77-79.
37. Xylinas E, Robinson BD, Kluth LA, et al. Association of T-cell co-regulatory protein expression with clinical outcomes following radical cystectomy for urothelial carcinoma of the bladder. Eur J Surg Oncol 2014; 40:121-127.
38. Mullane SA, Werner L, Callahan MK, et al. PD-L1 expression in mononuclear cells and not in tumor cells, correlated with prognosis in metastatic urothelial carcinoma. J Clin Oncol 2014; 32:. 5s (suppl; abstr 4552).
39. Harshman LC, Drake CG, Wargo JA, et al. Cancer immunotherapy highlights from the 2014 ASCO Meeting. Cancer Immunol Res 2014; 2:714-719.
40. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunitys roles in cancer suppression and promotion. Science 2011; 331:1565-1570.
41. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013; 19:1423-1437.
42. Chapoval AI, Ni J, Lau JS, et al. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol 2001; 2:269-274.
43. Hofmeyer KA, Ray A, Zang X. The contrasting role of B7-H3. Proc Natl Acad Sci U S A 2008; 105:10277-10278.
44. Suh WK, Gajewska BU, Okada H, et al. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol 2003; 4:899-906.
45. Boorjian SA, Sheinin Y, Crispen PL, et al. T-cell coregulatory molecule expression in urothelial cell carcinoma: clinicopathologic correlations and association with survival. Clin Cancer Res 2008; 14:4800-4808.
46. Carthon BC, Wolchok JD, Yuan J, et al. Preoperative CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial. Clin Cancer Res 2010; 16:2861-2871.
47. Jensen SM, Maston LD, Gough MJ, et al. Signaling through OX40 enhances antitumor immunity. Semin Oncol 2010; 37:524-532.
48. Aranda F, Vacchelli E, Eggermont A, et al. Trial Watch: immunostimulatory monoclonal antibodies in cancer therapy. Oncoimmunology 2014; 3:e27297.
49. Curti BD, Kovacsovics-Bankowski M, Morris N, et al. OX40 is a potent immune-stimulating target in late-stage cancer patients. Cancer Res 2013; 73:7189-7198.
50. Malmstrom PU, Loskog AS, Lindqvist CA, et al. AdCD40L immunogene therapy for bladder carcinoma: the first phase I/IIa trial. Clin Cancer Res 2010; 16:3279-3287.
51. Vonderheide RH, Glennie MJ. Agonistic CD40 antibodies and cancer therapy. Clin Cancer Res 2013; 19:1035-1043.
52. Vonderheide RH, Flaherty KT, Khalil M, et al. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007; 25:876-883.
53. Fransen MF, Sluijter M, Morreau H, et al. Local activation of CD8 T cells and systemic tumor eradication without toxicity via slow release and local delivery of agonistic CD40 antibody. Clin Cancer Res 2011; 17:2270-2280.
54. Sandin LC, Orlova A, Gustafsson E, et al. Locally delivered CD40 agonist antibody accumulates in secondary lymphoid organs and eradicates experimental disseminated bladder cancer. Cancer Immunol Res 2014; 2:80-90.
55. Kawashima A, Nakayama M, Kakuta Y, et al. Excision repair cross-complementing group 1 may predict the efficacy of chemoradiation therapy for muscle-invasive bladder cancer. Clin Cancer Res 2011; 17:2561-2569.
56. Sandin LC, Totterman TH, Mangsbo SM. Local immunotherapy based on agonistic CD40 antibodies effectively inhibits experimental bladder cancer. Oncoimmunology 2014; 3:e27400.
57. 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 2010; 59:663-674.
58. Sheikh NA, Petrylak D, Kantoff PW, et al. Sipuleucel-T immune parameters correlate with survival: an analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer. Cancer Immunol Immunother 2013; 62:137-147.
59. Kim JW, Gulley JL. Poxviral vectors for cancer immunotherapy. Expert Opin Biol Ther 2012; 12:463-478.
60. Bilusic M, Gulley JL. Endpoints, patient selection, and biomarkers in the design of clinical trials for cancer vaccines. Cancer Immunol Immunother 2012; 61:109-117.
61. Mohebtash M, Tsang KY, Madan RA, et al. A pilot study of MUC-1/CEA/TRICOM poxviral-based vaccine in patients with metastatic breast and ovarian cancer. Clin Cancer Res 2011; 17:7164-7173.
62. Ahmad S, Lam TB, NDow J. Significance of MUC1 in bladder cancer. BJU Int 2015; 115:161-162.
63. Lae M, Couturier J, Oudard S, et al. Assessing HER2 gene amplification as a potential target for therapy in invasive urothelial bladder cancer with a standardized methodology: results in 1005 patients. Ann Oncol 2010; 21:815-819.
64. Simonetti S, Russo R, Ciancia G, et al. Role of polysomy 17 in transitional cell carcinoma of the bladder: immunohistochemical study of HER2/neu expression and fish analysis of c-erbB-2 gene and chromosome 17. Int J Surg Pathol 2009; 17:198-205.
65. Zhao J, Xu W, Zhang Z, et al. Prognostic role of HER2 expression in bladder cancer: a systematic review and meta-analysis. Int Urol Nephrol 2015; 47:87-94.
66. Press M, ODonnell PH, Plimack E, et al. HER2 expression in patients (pts) with surgically resected urothelial cancer at high risk of recurrence screened for the phase II randomized, open-label trial of DN24-02, an autologous cellular immunotherapy targeting HER2. J Clin Oncol 2013; 31 (Suppl 6); abstr 292.
67. Yin B, Zeng Y, Liu G, et al. MAGE-A3 is highly expressed in a cancer stem celllike side population of bladder cancer cells. Int J Clin Exp Pathol 2014; 7:2934-2941.
68. Dyrskjot L, Zieger K, Kissow Lildal T, et al. Expression of MAGE-A3, NY-ESO-1, LAGE-1 and PRAME in urothelial carcinoma. Br J Cancer 2012; 107:116-122.
69. Fradet Y, Picard V, Bergeron A, LaRue H. Cancer-testis antigen expression in bladder cancer. Prog Urol 2006; 16:421-428.
70. Sharma P, Gnjatic S, Jungbluth AA, et al. Frequency of NY-ESO-1 and LAGE-1 expression in bladder cancer and evidence of a new NY-ESO-1 T-cell epitope in a patient with bladder cancer. Cancer Immun 2003; 3:19.
71. Sharma P, Bajorin DF, Jungbluth AA, et al. Immune responses detected in urothelial carcinoma patients after vaccination with NY-ESO-1 protein plus BCG and GM-CSF. J Immunother 2008; 31:849-857.
72. Tsuji T, Matsuzaki J, Kelly MP, et al. Antibody-targeted NY-ESO-1 to mannose receptor or DEC-205 in vitro elicits dual human CD8+ and CD4+ T cell responses with broad antigen specificity. J Immunol 2011; 186:1218-1227.
73. Morgan RA, Chinnasamy N, Abate-Daga D, et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 2013; 36:133-151.
74. Rosenberg SA, Yang JC, Sherry RM, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011; 17:4550-4557.
75. Hinrichs CS, Rosenberg SA. Exploiting the curative potential of adoptive T-cell therapy for cancer. Immunol Rev 2014; 257:56-71.
76. Robbins PF, Morgan RA, Feldman SA, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 2011; 29:917-924.
77. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 2010; 107:4275-4280.
78. Sznol M, Kluger H, Callahan MK, et al. Survival, response duration, and activity by BRAF mutation (MT) status of nivolumab (NIVO, anti-PD-1, BMS-936558, ONO-4538) and ipilimumab (IPI) concurrent therapy in advanced melanoma (MEL). J Clin Oncol 2014; 32:. (5s):abstr LBA9003.
79. Hammers H, Plimack E, Infante J, et al. Phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma (mRCC). J Clin Oncol 2014; 32:. (5s):abstr 4504.
80. Apolo AB, Parnes H, Madan RA, et al. A phase II study of cabozantinib in patients (pts) with relapsed or refractory metastatic urothelial carcinoma (mUC). J Clin Oncol 2014; 32 (Suppl 4); abstr 307.
81. Apolo AB, Tomita Y, Lee M, et al. Effect of cabozantinib on immunosuppressive subsets in metastatic urothelial carcinoma. J Clin Oncol 2014; 32:. (5s):abstr 4501.
82. Kwilas AR, Ardiani A, Donahue RN, et al. Dual effects of a targeted smallmolecule inhibitor (cabozantinib) on immune-mediated killing of tumor cells and immune tumor microenvironment permissiveness when combined with a cancer vaccine. J Transl Med 2014; 12:294.
83. Voron T, Colussi O, Marcheteau E, et al. VEGF-A modulates expression of inhibitory checkpoints on CD8+ T cells in tumors. J Exp Med 2015; 212:139-148.
84. Amin A, Plimack E, Infante J, et al. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) in combination with sunitinib or pazopanib in patients (pts) with metastatic renal cell carcinoma (mRCC). J Clin Oncol 2014; 32:. (5s):abstr 5010.
85. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012; 11:215-233.
86. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013; 31:51-72.
87. Lesterhuis WJ, Punt CJ, Hato SV, et al. Platinum-based drugs disrupt STAT6-mediated suppression of immune responses against cancer in humans and mice. J Clin Invest 2011; 121:3100-3108.
88. Ramakrishnan R, Assudani D, Nagaraj S, et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest 2010; 120:1111-1124.
89. Karzai FH, Apolo AB, Cao L, et al. A phase I study of TRC105 anti-CD105 (endoglin) antibody in metastatic castration-resistant prostate cancer. BJU Int 2014. [Epub ahead of print]