Anti-CTLA-4 therapy in melanoma: Role of ipilimumab (MDX-010)

Expert Review of Dermatology

Volumn 4, Issue 3, 2009, Pages 199-210

  Ridolfi, Laura ^a   Ridolfi, Ruggero ^a  

^a DEPARTMENT OF MEDICAL ONCOLOGY   (Italy)

Author keywords

Advanced melanoma; Anti CTLA 4 monoclonal antibody; Immunotherapy; Ipilimumab; Melanoma treatment; New evaluation criteria

Indexed keywords

ALPHA INTERFERON; ANTINEOPLASTIC AGENT; B7 ANTIGEN; BUDESONIDE; CD28 ANTIGEN; CD86 ANTIGEN; CORTICOSTEROID; CPG OLIGODEOXYNUCLEOTIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DACARBAZINE; INFLIXIMAB; INTERLEUKIN 2; IPILIMUMAB; MDX 1379; MELANOMA VACCINE; PEPTIDE VACCINE; STEROID; UNCLASSIFIED DRUG;

ABDOMINAL PAIN; ANTIGEN RECOGNITION; ARTHRALGIA; ARTICLE; CANCER STAGING; CELL THERAPY; CLINICAL TRIAL; COLITIS; DERMATITIS; DIARRHEA; DISEASE COURSE; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; ENDOCRINE DISEASE; ENTEROCOLITIS; ERYTHEMA; FATIGUE; FEVER; GASTROINTESTINAL SYMPTOM; HEPATITIS; HEPATOBILIARY DISEASE; HUMAN; HYPOPHYSITIS; IMMUNE RESPONSE; IMMUNOPATHOLOGY; LYMPHOCYTE TRANSFER; MELANOMA; NAUSEA; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PRURITUS; RASH; SIDE EFFECT; SINGLE DRUG DOSE; SKIN DISEASE; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE; TUMOR GROWTH; UVEITIS;

EID: 69949151357     PISSN: 17469872     EISSN: None     Source Type: Journal    
DOI: 10.1586/edm.09.11     Document Type: Article

References (103)

1. Marincola FM, Jaffee EM, Hicklin JD, Ferrone S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv. Immunol. 174, 181-273 (2000).
2. Shiozaki A, Kataoka K, Fujimura M, Yuki H, Sakai M, Saito S. Survivin inhibits apoptosis in cytotrophoblasts. Placenta 24(1), 65-76 (2003).
3. Ridolfi L, Petrini M, Fiammenghi L, Riccobon A, Ridolfi R. Human embryo immune escape mechanisms rediscovered by the tumor. Immunobiology 214(1), 61-76 (2009).
4. Smyth MJ, Dunn GP, Schreiber RD. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv. Immunol. 90, 1-50 (2006).
5. Takeda K, Hayakawa Y, Smyth MJ et al. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat. Med. 7(1), 94-100 (2001).
6. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4(1), 71-78 (2004).
7. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 6(11), 836-848 (2006).
8. Bui JD, Schreiber RD. Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes? Curr. Opin. Immunol. 19(2), 203-208 (2007).
9. Lin EY, Pollard JW. Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res. 67(11), 5064-5066 (2007).
10. Street SE, Zerafa N, Iezzi M et al. Host perforin reduces tumor number but does not increase survival in oncogene-driven mammary adenocarcinoma. Cancer Res. 67(11), 5454-5460 (2007).
11. Stewart TJ, Greeneltch KM, Lutsiak ME, Abrams SI. Immunological responses can have both pro- and antitumour effects: implications for immunotherapy. Expert Rev. Mol. Med. 9(4), 1-20 (2007).
12. Moschos S, Varanasi S, Kirkwood JM. Interferons in the treatment of solid tumors. Cancer Treat. Res. 126, 207-241 (2005).
13. Kirkwood JM, Strawderman MH, Ernstoff MS, Smith TJ, Borden EC, Blum RH. Interferon α-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J. Clin. Oncol. 14(1), 7-17 (1996).
14. Kirkwood JM, Ibrahim JG, Sondak VK et al. High- and low-dose interferon α-2b in high-risk melanoma: first analysis of intergroup trial E1690/S9111/C9190. J. Clin. Oncol. 18(12), 2444-2458 (2000).
15. Moschos SJ, Edington HD, Land SR et al. Neoadjuvant treatment of regional stage IIIB melanoma with high-dose interferon α-2b induces objective tumor regression in association with modulation of tumor infiltrating host cellular immune responses. J. Clin. Oncol. 24(19), 3164-3171 (2006).
16. Lui P, Cashin R, Machado M, Hemels M, Corey-Lisle PK, Einarson TR. Treatments for metastatic melanoma: synthesis of evidence from randomized trials. Cancer Treat. Rev. 33(8), 665-680 (2007).
17. Kirkwood JM, Tawbi HA, Tarhini AA, Moschos SJ. Does pegylated interferon α-2b confer additional benefit in the adjuvant treatment of high-risk melanoma? Nat. Clin. Pract. Oncol. 6(2), 70-71 (2009).
18. Moschos SJ, Mandic M, Kirkwood JM, Storkus WJ, Lotze MT. Focus on FOCIS: interleukin 2 treatment associated autoimmunity. Clin. Immunol. 127(2), 123-129 (2008).
19. Atkins MB, Lotze MT, Dutcher JP et al. High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J. Clin. Oncol. 17(7), 2105-2116 (1999).
20. Sasse AD, Sasse EC, Clark LG, Ulloa L, Clark OA. Chemoimmunotherapy versus chemotherapy for metastatic malignant melanoma. Cochrane Database Syst. Rev. 1, CD005413 (2007).
21. Ives NJ, Stowe RL, Lorigan P, Wheatley K. Chemotherapy compared with biochemotherapy for the treatment of metastatic melanoma: a meta-analysis of 18 trials involving 2,621 patients. J. Clin. Oncol. 25(34), 5426-5434 (2007).
22. Dudley ME, Wunderlich JR, Yang JC et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J. Clin. Oncol. 23(10), 2346-2357 (2005).
23. Fang L, Lonsdorf AS, Hwang ST. Immunotherapy for advanced melanoma. J. Invest. Dermatol. 128(11), 2596-2605 (2008).
24. Dudley ME, Yang JC, Sherry R et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 26(32), 5233-5239. (2008).
25. Sanderson K, Scotland R, Lee P et al. Autoimmunity in a phase I trial of a fully human anti-cytotoxic T-lymphocyte antigen-4 monoclonal antibody with multiple melanoma peptides and Montanide ISA 51 for patients with resected stages III and IV melanoma. J. Clin. Oncol. 23(4), 741-750 (2005).
26. Cutler CW, Jotwani R, Pulendran B. Dendritic cells: immune saviors or Achilles' heel? Infect. Immun. 69(8), 4703-4708 (2001).
27. Peggs KS, Quezada SA, Allison JP. Cell intrinsic mechanisms of T-cell inhibition and application to cancer therapy. Immunol. Rev. 224, 141-165 (2008).
28. Korman AJ, Peggs KS, Allison JP. Checkpoint blockade in cancer immunotherapy. Adv. Immunol. 90, 297-339 (2006).
29. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat. Rev. Immunol. 2(2), 116-126 (2002).
30. Chen J, He Q, Zhang R et al. Allogenic donor splenocytes pretreated with antisense peptide against B7 prolong cardiac allograft survival. Clin. Exp. Immunol. 138(2), 245-250 (2004).
31. 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(12), 1365-1369 (1999).
32. Tseng SY, Otsuji M, Gorski K et al. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J. Exp. Med. 193(7), 839-846 (2001).
33. Seliger B, Marincola FM, Ferrone S, Abken H. The complex role of B7 molecules in tumor immunology. Trends Mol. Med. 14(12), 550-559 (2008).
34. Brunet JF, Denizot F, Luciani MF et al. A new member of the immunoglobulin superfamily - CTLA-4. Nature 328(6127), 267-270 (1987).
35. Dariavach P, Mattéi MG, Golstein P, Lefranc MP. Human Ig superfamily CTLA-4 gene: chromosomal localization and identity of protein sequence between murine and human CTLA-4 cytoplasmic domains. Eur. J. Immunol. 18(12), 1901-1905 (1988).
36. Thompson CB, Allison JP. The emerging role of CTLA-4 as an immune attenuator. Immunity 7(4), 445-450 (1997).
37. Walunas TL, Lenschow DJ, Bakker CY et al. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1(5), 405-413 (1994).
38. + T cells in vivo is dependent on CD28 costimulation and inhibited by CTLA-4. J. Immunol. 155(3), 1032-1036 (1995).
39. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 182(2), 459-465 (1995).
40. Krummel MF, Sullivan TJ, Allison JP. Superantigen responses and co-stimulation: CD28 and CTLA-4 have opposing effects on T cell expansion in vitro and in vivo. Int. Immunol. 8(4), 519-523 (1996).
41. 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(5), 541-547 (1995).
42. Waterhouse P, Penninger JM, Timms E et al. Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 270(5238), 985-988 (1995).
43. + T cells. Immunity 7(6), 885-895 (1997).
44. Schneider H, Downey J, Smith A et al. Reversal of the TCR stop signal by CTLA-4. Science 313(5795), 1972-1975 (2006).
45. Downey J, Smith A, Schneider H, Hogg N, Rudd CE. TCR/CD3 mediated stop-signal is decoupled in T-cells from Ctla4 deficient mice. Immunol. Lett. 115(1), 70-72 (2008).
46. 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(6), 1810-1815 (2007).
47. Korman A, Yellin M, Keler T. Tumor immunotherapy: preclinical and clinical activity of anti-CTLA4 antibodies. Curr. Opin. Investig. Drugs 6(6), 582-591 (2005).
48. Melero I, Shuford WW, Newby SA et al. Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat. Med. 3(6), 682-685 (1997).
49. 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(3), 355-366 (1999).
50. Keler T, Halk E, Vitale L et al. Activity and safety of CTLA-4 blockade combined with vaccines in cynomolgus macaques. J. Immunol. 171(11), 6251-6259 (2003).
51. Maker AV, Phan GQ, Attia P et al. Tumor regression and autoimmunity in patients treated with cytotoxic T lymphocyte-associated antigen 4 blockade and interleukin 2: a Phase I/II study. Ann. Surg. Oncol. 12(12), 1005-1016 (2005).
52. + T cells in a dose-dependent fashion. Blood 112(4), 1175-1183 (2008).
53. Maker AV, Yang JC, Sherry RM et al. Intrapatient dose escalation of anti-CTLA-4 antibody in patients with metastatic melanoma. J. Immunother. 29(4), 455-463 (2006).
54. + T cells. Eur. J. Immunol. 28(10), 3137-3143 (1998).
55. Jinushi M, Hodi FS, Dranoff G. Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc. Natl Acad. Sci. USA 103(24), 9190-9195 (2006).
56. Contardi E, Palmisano GL, Tazzari PL et al. CTLA-4 is constitutively expressed on tumor cells and can trigger apoptosis upon ligand interaction. Int. J. Cancer 117(4), 538-550 (2005).
57. Hoos A, Chasalow SD, Parker SM et al. Ipilimumab 10mg/kg induction dosing promotes T-cell activation in patients with advanced melanoma. Ann. Oncol. 19(8 Suppl.), (2008).
58. Davis TA, Tchekmedyian S, Korman A, Keler T, Deo Y, Small EJ. MDX-010 (human anti-CTLA4): a Phase 1 trial in hormone refractory prostate carcinoma (HRPC). Proc. Am. Soc. Clin. Oncol. 21(Suppl.), (2002).
59. Tchekmedyian S, Glasby J, Korman A, Keler T, Deo Y, Davis TA. MDX-010 (human anti-CTLA4): a Phase I trial in malignant melanoma. Proc. Am. Soc. Clin. Oncol. 21(Suppl.), (2002).
60. 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(8), 4712-4717 (2003).
61. Weber JS, O'Day S, Urba W et al. Phase I/II Study of ipilimumab for patients with metastatic melanoma. J. Clin. Oncol. 26(36), 5950-5956 (2008).
62. Weber JS, Hersh EM, Yellin M et al. The efficacy and safety of ipilimumab (MDX-010) in patients with unresectable stage III or stage IV malignant melanoma. J. Clin. Oncol. 25(18 Suppl.), (2007).
63. Lebbe C, Hoos A, Chin K et al. Effect of dose on efficacy and safety in ipilimumab-treated patients with advanced melanoma-results from a Phase II, randomized, dose-ranging study. Ann. Oncol. 19(8 Suppl.), (2008).
64. Hamid O, Chin K, Li J et al. Dose effect of ipilimumab in patients with advanced melanoma: results from a Phase II, randomized, dose-ranging study. J. Clin. Oncol. 26(20 Suppl.), (2008).
65. O'Day SJ, Ibrahim R, DePril V et al. Efficacy and safety of ipilimumab induction and maintenance dosing in patients with advanced melanoma who progressed on one or more prior therapies. J. Clin. Oncol. 26(20 Suppl.), (2008).
66. Weber JS, Berman D, Siegel J et al. Safety and efficacy of ipilimumab with or without prophylactic budesonide in treatment-naive and previously treated patients with advanced melanoma. J. Clin. Oncol. 26(20 Suppl.), (2008).
67. Ron I, Berman D, Siegel J et al. Efficacy and safety of patients with advanced melanoma treated with ipilimumab with or without the addition of prophylactic budesonide. Ann. Oncol. 19(8 Suppl.), (2008).
68. Ridolfi R, Berman D, Siegel J et al. Efficacy and safety of treatment-naïve and previously treated patients with advanced melanoma receiving ipilimumab. Ann. Oncol. 19(8 Suppl.), (2008).
69. Maio M, Hoos A, Ibrahim R et al. Efficacy and safety of ipilimumab in patients with advanced melanoma who had progressed on one or more prior therapies: results from a single-arm, multicenter study. Ann. Oncol. 19(8 Suppl.), (2008).
70. Hersh E M, Weber JS, Powderly JD et al. Disease control and long-term survival in chemotherapy-naive patients with advanced melanoma treated with ipilimumab (MDX- 010) with or without dacarbazine. J. Clin. Oncol. 26(20 Suppl.), (2008).
71. Maker AV, Attia P, Rosenberg SA. Analysis of the cellular mechanism of antitumor responses and autoimmunity in patients treated with CTLA-4 blockade. J. Immunol. 175(11), 7746-7754 (2005).
72. Attia P, Phan GQ, Maker AV et al. Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4. J. Clin. Oncol. 23(25), 6043-6053 (2005).
73. Korman A, Yellin M, Keler T. Tumor immunotherapy: preclinical and clinical activity of anti-CTLA4 antibodies. Curr. Opin. Investig. Drugs. 6(6), 582-591 (2005).
74. Peggs KS, Quezada SA, Korman AJ, Allison JP. Principles and use of anti-CTLA4 antibody in human cancer immunotherapy. Curr. Opin. Immunol. 18(2), 206-213 (2006).
75. Leach DR, Krummel MF, Allison J. Enhancement of antitumor immunity by CTLA-4 blockade. Science 271(5256), 1734-1736 (1996).
76. Sotomayor EM, Borrello I, Tubb E, Allison JP, Levitsky HI. In vivo blockade of CTLA-4 enhances the priming of responsive T cells but fails to prevent the induction of tumor antigen-specific tolerance. Proc. Natl Acad. Sci. USA 96(20), 11476-11481 (1999).
77. + T cell- and IL-2-dependent mechanism. Immunity 11(4), 483-493 (1999).
78. +) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J. Exp. Med. 194(6), 823-832 (2001).
79. Davila E, Kennedy R, Celis E. Generation of antitumor immunity by cytotoxic T lymphocyte epitope peptide vaccination, CpG-oligodeoxynucleotide adjuvant, and CTLA-4 blockade. Cancer Res. 63(12), 3281-3288 (2003).
80. Phan GQ, Yang JC, Sherry RM et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc. Natl Acad. Sci. USA 100(14), 8372-8377 (2003).
81. Fischkoff SA, Hersh E, Weber J et al. Durable responses and long-term progression-free survival observed in a Phase II study of MDX-010 alone or in combination with dacarbazine (DTIC) in metastatic melanoma. J. Clin. Oncol. 23(16 Suppl.), (2005).
82. Reuben JM, Lee BN, Li C et al. Biologic and immunomodulatory events after CTLA-4 blockade with ticilimumab in patients with advanced malignant melanoma. Cancer 106(11), 2437-2444 (2006).
83. Weber JS, Targan S, Scotland R et al. Phase II trial of extended dose anti-CTLA-4 antibody ipilimumab (formerly MDX-010) with a multi-peptide vaccine for resected syages IIIc and IV melanoma. J. Clin. Oncol. 24(18 Suppl.), (2006).
84. 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(15), 2283-2289 (2006).
85. Antonia S, Sosman J, Kirkwood JM et al. Natural history of diarrhea associated with the anti-CTLA-4 monoclonal antibody. J. Clin. Oncol. 25(18 Suppl.), (2007).
86. Blansfield JA, Beck KE, Tran K et al. Cytotoxic T-lymphocyte-associated antigen-4 blockage can induce autoimmune hypophysitis in patients with metastatic melanoma and renal cancer. J. Immunother. 28(6), 593-598 (2005).
87. Chin K, Ibrahim R, Berman D et al. Treatment guidelines for the management of immune-related adverse events in patients treated with ipilimumab, an anti-CTLA-4 therapy. Ann. Oncol. 19(8 Suppl.), (2008).
88. Weber J. Anti-CTLA-4 antibody ipilimumab: case studies of clinical response and immune-related adverse events. Oncologist 12(7), 864-872 (2007).
89. O'Day SJ, Hamid O, Urba WJ. Targeting cytotoxic T-lymphocyte antigen-4 (CTLA-4): a novel strategy for the treatment of melanoma and other malignancies. Cancer 110(12), 2614-2627 (2007).
90. Downey SG, Klapper JA, Smith FO et al. Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin. Cancer Res. 13(22), 6681-6688 (2007).
91. Hamid O, Urba WJ, Yellin M et al. Kinetics of response to ipilimumab (MDX-010) in patients with stage III/IV melanoma. J. Clin. Oncol. 25(18 Suppl.), (2007).
92. 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(32), 5275-5283 (2008).
93. Hodi FS, Butler M, Oble DA et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc. Natl Acad. Sci. USA 105(8), 3005-3010 (2008).
94. Saenger YM, Wolchok JD. The heterogeneity of the kinetics of response to ipilimumab in metastatic melanoma: patient cases. Cancer Immun. 17(8), 1 (2008).
95. Harmankaya K, Pehamberger H, Hoos A et al. Ipilimumab-mediated patterns of response in patients with pretreated, advanced melanoma. Ann. Oncol. 19(8 Suppl.), (2008).
96. Tuma RS. New response criteria proposed for immunotherapies. J. Natl Cancer Inst. 100(18), 1280-1281 (2008).
97. Weber J. Overcoming immunologic tolerance to melanoma: targeting CTLA-4 with ipilimumab (MDX-010). Oncologist 13(4 Suppl.), 16-25 (2008).
98. Weber J. Ipilimumab: controversies in its development, utility and autoimmune adverse events. Cancer Immunol. Immunother. 58(5), 823-830 (2009).
99. Keilholz U. CTLA-4: negative regulator of the immune response and a target for cancer therapy. J. Immunother. 31(5), 431-439 (2008).
100. Lens M, Ferrucci PF, Testori A. Anti-CTLA4 monoclonal antibody ipilimumab in the treatment of metastatic melanoma: recent findings. Recent Pat. Anticancer Drug Discov. 3(2), 105-113 (2008).
101. Kirkwood JM, Tarhini AA, Panelli MC et al. Next generation of immunotherapy for melanoma. J. Clin. Oncol. 26(20), 3445-3455 (2008).
102. Melero I, Hervas-Stubbs S, Glennie M, Pardoll DM, Chen L. Immunostimulatory monoclonal antibodies for cancer therapy. Nat. Rev. Cancer 7(2), 95-106 (2007).
103. Breunis WB, Tarazona-Santos E, Chen R, Kiley M, Rosenberg SA, Chanock SJ. Influence of cytotoxic T lymphocyte-associated antigen 4 (CTLA4) common polymorphisms on outcome in treatment of melanoma patients with CTLA-4 blockade. J. Immunother. 31(6), 586-590 (2008).