Inhibitors of B7-CD28 costimulation in urologic malignancies

Immunotherapy

Volumn 1, Issue 1, 2009, Pages 129-139

  Thompson, R Houston ^b   Kwon, Eugene D ^c   Allison, James P ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c MAYO CLINIC COLLEGE OF MEDICINE   (United States)

Author keywords

Lymphocyte activation; Prostatic neoplasm; Regulatory T lymphocyte; Renal cell carcinoma; Urinary bladder neoplasm

Indexed keywords

B7 ANTIGEN; B7 H3 ANTIGEN; B7X ANTIGEN; CD28 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; HUMAN MONOCLONAL ANTIBODY; IPILIMUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN; TICILIMUMAB; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; AUTOIMMUNE DISEASE; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER MORTALITY; CANCER RECURRENCE; CELLULAR IMMUNITY; CLINICAL TRIAL; CYTOTOXIC T LYMPHOCYTE; HUMAN; KIDNEY CANCER; KIDNEY CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; TUMOR IMMUNITY; URINARY TRACT CANCER;

ANTIBODIES, BLOCKING; ANTIGENS, CD; ANTIGENS, CD28; ANTIGENS, CD80; APOPTOSIS REGULATORY PROTEINS; CARCINOMA; CLINICAL TRIALS AS TOPIC; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; IMMUNITY, CELLULAR; IMMUNOTHERAPY; KIDNEY NEOPLASMS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MARKERS, BIOLOGICAL;

EID: 77953411724     PISSN: 1750743X     EISSN: None     Source Type: Journal    
DOI: 10.2217/1750743X.1.1.129     Document Type: Review

References (80)

1. Chambers CA, Kuhns MS, Egen JG, Allison JP: CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Ann. Rev. Immunol. 19, 565-594 (2001).
2. Schwartz RH: T cell anergy. Ann. Rev. Immunol. 21, 305-334 (2003).
3. Zang X, Allison JP: The B7 family and cancer therapy: costimulation and coinhibition. Clin Cancer Res. 13, 5271-5279 (2007). (Pubitemid 47510350)
4. Frauwirth KA, Thompson CB: Activation and inhibition of lymphocytes by costimulation. J. Clin. Invest. 109, 295-299 (2002).
5. Thompson RH, Allison JP, Kwon ED: Anti-cytotoxic T lymphocyte antigen-4 (CTLA-4) immunotherapy for the treatment of prostate cancer. Urol. Oncol. 24, 442-447 (2006).
6. Strome SE, Chen L: Costimulation-based immunotherapy for head and neck cancer. Curr. Treat. Options Oncol. 5, 27-33 (2004).
7. Weinberg AD, Rivera MM, Prell R et al.: Engagement of the OX-40 receptor in vivo enhances antitumor immunity. J. Immunol. 164, 2160-2169 (2000). (Pubitemid 30108775)
8. Gramaglia I, Weinberg AD, Lemon M, Croft M: OX-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J. Immunol. 161, 6510-6517 (1998). (Pubitemid 28562188)
9. Cheuk AT, Mufti GJ, Guinn BA: Role of 4-1BB:4-1BB ligand in cancer immunotherapy. Cancer Gene Ther. 11, 215-226 (2004).
10. Chen L: Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat. Rev. Immunol. 4, 336-347 (2004). ■ Excellent review of B7-CD28 family function and mechanism.
11. Chambers CA, Cado D, Truong T, Allison JP: Thymocyte development is normal in CTLA-4-deficient mice. Proc. Natl Acad. Sci. USA 94, 9296-9301 (1997).
12. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH: Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3, 541-547 (1995).
13. Waterhouse P, Penninger JM, Timms E et al.: Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 270, 985-988 (1995).
14. Leach DR, Krummel MF, Allison JP: Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734-1736 (1996).
15. Kwon ED, Hurwitz AA, Foster BA et al.: Manipulation of T cell costimulatory and inhibitory signals for immunotherapy of prostate cancer. Proc. Natl Acad. Sci. USA 94, 8099-8103 (1997).
16. Kwon ED, Foster BA, Hurwitz AA et al.: Elimination of residual metastatic prostate cancer after surgery and adjunctive cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) blockade immunotherapy. Proc. Natl Acad. Sci. USA 96, 15074-15079 (1999).
17. Hurwitz AA, Foster BA, Kwon ED et al.: Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cancer Res. 60, 2444-2448 (2000).
18. Hurwitz AA, Yu TF, Leach DR, Allison JP: CTLA-4 blockade synergizes with tumor-derived granulocyte-macrophage colony-stimulating factor for treatment of an experimental mammary carcinoma. Proc. Natl Acad. Sci. USA 95, 10067-10071 (1998).
19. 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. 190, 355-366 (1999).
20. Hanahan D, Lanzavecchia A, Mihich E: Fourteenth Annual Pezcoller Symposium: the novel dichotomy of immune interactions with tumors. Cancer Res. 63, 3005-3008 (2003). (Pubitemid 36667177)
21. Hodi FS, Mihm MC, Soiffer RJ et al.: Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc. Natl Acad. Sci. USA 100, 4712-4717 (2003).
22. Krejci KG, Markiewicz MA, Kwon ED: Immunotherapy for urological malignancies. J. Urol. 171, 870-876 (2004).
23. Beck KE, Blansfield JA, Tran KQ et al.: Enterocolitis in patients with cancer after antibody blockade of cytotoxic T-lymphocyte-associated antigen 4. J. Clin. Oncol. 24, 2283-2289 (2006).
24. Ribas A, Camacho LH, Lopez-Berestein G et al.: Antitumor activity in melanoma and anti-self responses in a Phase 1 trial with the anti-cytotoxic T lymphocyte-associated antigen 4 monoclonal antibody CP-675,206. J. Clin. Oncol. 23, 8968-8977 (2005).
25. Dong H, Zhu G, Tamada K, Chen L: B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat. Med. 5, 1365-1369 (1999).
26. Dong H, Strome SE, Salomao DR et al.: Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8, 793-800 (2002).
27. 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).
28. Konishi J, Yamazaki K, Azuma M, Kinoshita I, Dosaka-Akita H, Nishimura M: B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin. Cancer Res. 10, 5094-5100 (2004).
29. Ohigashi Y, Sho M, Yamada Y et al.: Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clin. Cancer Res. 11, 2947-2953 (2005).
30. Wintterle S, Schreiner B, Mitsdoerffer M et al.: Expression of the B7-related molecule B7-H1 by glioma cells: a potential mechanism of immune paralysis. Cancer Res. 63, 7462-7467 (2003). (Pubitemid 37413489)
31. Curiel TJ, Wei S, Dong H et al.: Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat. Med. 9, 562-567 (2003).
32. Parsa AT, Waldron JS, Panner A et al.: Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat. Med. 13, 84-88 (2007).
33. Dong H, Chen L: B7-H1 pathway and its role in the evasion of tumor immunity. J. Mol. Med. 81, 281-287 (2003).
34. Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N: Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl Acad. Sci. USA 99, 12293-12297 (2002).
35. + T lymphocytes. Immunity 20, 327-336 (2004).
36. Azuma T, Yao S, Zhu G, Flies AS, Flies SJ, Chen L: B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells. Blood 111, 3635-3643 (2008).
37. 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). ■ Evaluated B7-H1 and programmed death (PD)-1 blockade in multiple murine cancer models. (Pubitemid 40216472)
38. Webster WS, Thompson RH, Harris KJ et al.: Targeting molecular and cellular inhibitory mechanisms for improvement of antitumor memory responses reactivated by tumor cell vaccine. J. Immunol. 179, 2860-2869 (2007).
39. Thompson RH, Gillett MD, Cheville JC et al.: Costimulatory B7-H1 in renal cell Carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc. Natl Acad. Sci. USA 101, 17174-17179 (2004). ■ First to suggest that negative costimulatory molecules diminish survival.
40. Thompson RH, Dong H, Kwon ED: Implications of B7-H1 expression in clear cell carcinoma of the kidney for prognostication and therapy. Clin. Cancer Res. 13, 709S-15S (2007).
41. Thompson RH, Gillett MD, Cheville J et al.: Costimulatory molecule B7-H1 in primary and metastatic clear cell renal cell carcinoma. Cancer 104, 2084-2091 (2005). (Pubitemid 41579953)
42. Thompson RH, Webster WS, Cheville JC et al.: B7-H1 glycoprotein blockade: a novel strategy to enhance immunotherapy in patients with renal cell carcinoma. Urol. 66, 10-14 (2005).
43. Thompson RH, Kuntz SM, Leibovich BC et al.: Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 66, 3381-3385 (2006).
44. Nakanishi J, Wada Y, Matsumoto K, Azuma M, Kikuchi K, Ueda S: Overexpression of B7-H1 (PD-L1) significantly associates with tumor grade and postoperative prognosis in human urothelial cancers. Cancer Immunol. Immunother. 56, 1173-1182 (2007).
45. 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 109, 1499-1505 (2007). (Pubitemid 46595684)
46. Roth TJ, Sheinin Y, Lohse CM et al.: B7-H3 ligand expression by prostate cancer: a novel marker of prognosis and potential target for therapy. Cancer Res. 67, 7893-7900 (2007). (Pubitemid 47281385)
47. Ishida Y, Agata Y, Shibahara K, Honjo T: Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11, 3887-3895 (1992).
48. Zha Y, Blank C, Gajewski TF: Negative regulation of T-cell function by PD-1. Crit. Rev. Immunol. 24, 229-237 (2004).
49. Keir ME, Butte MJ, Freeman GJ, Sharpe AH: PD-1 and its ligands in tolerance and immunity. Ann. Rev. Immunol. 26, 677-704 (2008). ■ Excellent review of programmed death (PD)-1.
50. Lazar-Molnar E, Yan Q, Cao E, Ramagopal U, Nathenson SG, Almo SC: Crystal structure of the complex between programmed death-1 (PD-1) and its ligand PD-L2. Proc. Natl Acad. Sci. USA 105, 10483-10488 (2008).
51. Yamazaki T, Akiba H, Iwai H et al.: Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169, 5538-5545 (2002). (Pubitemid 35291652)
52. + resting regulatory T cells from activated T cells. J. Immunol. 176, 2808-2816 (2006). (Pubitemid 43306940)
53. Dorfman DM, Brown JA, Shahsafaei A, Freeman GJ: Programmed death-1 (PD-1) is a marker of germinal center-associated T cells and angioimmunoblastic T-cell lymphoma. Am. J. Surg. Pathol. 30, 802-810 (2006).
54. Barber DL, Wherry EJ, Masopust D et al.: Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687 (2006). ■ Suggests that PD-1 may play a role in tolerance of chronic virus infections. (Pubitemid 43237609)
55. + T cells leads to reversible immune dysfunction. Nat. Med. (2006).
56. Day CL, Kaufmann DE, Kiepiela P et al.: PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 433, 350-354 (2006). (Pubitemid 44435155)
57. + T cell survival in HIV infection. J. Exp. Med. 203, 2281-2292 (2006).
58. Thompson RH, Dong H, Lohse CM et al.: PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clin. Cancer Res. 13, 1757-1761 (2007).
59. Chapoval AI, Ni J, Lau JS et al.: B7-H3: a costimulatory molecule for T cell activation and IFN-γ production. Nat. Immunol. 2, 269-274 (2001).
60. 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. 4, 899-906 (2003).
61. Castriconi R, Dondero A, Augugliaro R et al.: Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc. Natl Acad. Sci. USA 101, 12640-12645 (2004).
62. Prasad DV, Nguyen T, Li Z et al.: Murine B7-H3 is a negative regulator of T cells. J. Immunol. 173, 2500-2506 (2004). (Pubitemid 39063108)
63. Sun Y, Wang Y, Zhao J et al.: B7-H3 and B7-H4 expression in non-small-cell lung cancer. Lung Cancer 53, 143-151 (2006). (Pubitemid 43994236)
64. Wu CP, Jiang JT, Tan M et al.: Relationship between co-stimulatory molecule B7-H3 expression and gastric carcinoma histology and prognosis. World J. Gastroenterol. 12, 457-459 (2006).
65. + cytolytic T cells. J. Immunol. 173, 5445-5450 (2004). (Pubitemid 39392128)
66. Lupu CM, Eisenbach C, Kuefner MA et al.: An orthotopic colon cancer model for studying the B7-H3 antitumor effect in vivo. J. Gastrointest. Surg. 10, 635-645 (2006).
67. Sun X, Vale M, Leung E, Kanwar JR, Gupta R, Krissansen GW: Mouse B7-H3 induces antitumor immunity. Gene Ther. 10, 1728-1734 (2003). (Pubitemid 37121044)
68. Zang X, Thompson RH, Al-Ahmadie HA et al.: B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome. Proc. Natl Acad. Sci. USA 104, 19458-19463 (2007).
69. Zang X, Loke P, Kim J, Murphy K, Waitz R, Allison JP: B7x: a widely expressed B7 family member that inhibits T cell activation. Proc. Natl Acad. Sci. USA 100, 10388-10392 (2003).
70. Sica GL, Choi IH, Zhu G et al.: B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 18, 849-861 (2003). (Pubitemid 36776432)
71. Prasad DV, Richards S, Mai XM, Dong C: B7S1, a novel B7 family member that negatively regulates T cell activation. Immunity 18, 863-873 (2003). (Pubitemid 36776433)
72. Salceda S, Tang T, Kmet M et al.: The immunomodulatory protein B7-H4 is overexpressed in breast and ovarian cancers and promotes epithelial cell transformation. Exp. Cell. Res. 306, 128-141 (2005).
73. Choi IH, Zhu G, Sica GL et al.: Genomic organization and expression analysis of B7-H4, an immune inhibitory molecule of the B7 family. J. Immunol. 171, 4650-4654 (2003). (Pubitemid 37310581)
74. Tringler B, Zhuo S, Pilkington G et al.: B7-H4 is highly expressed in ductal and lobular breast cancer. Clin. Cancer Res. 11, 1842-1848 (2005).
75. Tringler B, Liu W, Corral L et al.: B7-H4 overexpression in ovarian tumors. Gynecol. Oncol. 100, 44-52 (2006).
76. Miyatake T, Tringler B, Liu W et al.: B7-H4 (DD-O110) is overexpressed in high risk uterine endometrioid adenocarcinomas and inversely correlated with tumor T-cell infiltration. Gynecol. Oncol. 106, 119-127 (2007).
77. Krambeck AE, Thompson RH, Dong H et al.: B7-H4 expression in renal cell carcinoma and tumor vasculature: associations with cancer progression and survival. Proc. Natl Acad. Sci. USA 103, 10391-10396 (2006).
78. Simon I, Zhuo S, Corral L et al.: B7-H4 is a novel membrane-bound protein and a candidate serum and tissue biomarker for ovarian cancer. Cancer Res. 66, 1570-1575 (2006). (Pubitemid 43259939)
79. O'Mahony D, Morris JC, Quinn C et al.: A pilot study of CTLA-4 blockade after cancer vaccine failure in patients with advanced malignancy. Clin. Cancer Res. 13, 958-964 (2007).
80. Small EJ, Tchekmedyian NS, Rini BI, Fong L, Lowy I, Allison JP: 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).