Persistence of CTL clones targeting melanocyte differentiation antigens was insufficient to mediate significant melanoma regression in humans

Clinical Cancer Research

Volumn 21, Issue 3, 2015, Pages 534-543

  Chandran, Smita S ^a   Paria, Biman C ^a   Srivastava, Abhishek K ^a   Rothermel, Luke D ^a   Stephens, Daniel J ^a   Dudley, Mark E ^a   Somerville, Robert ^a   Wunderlich, John R ^a   Sherry, Richard M ^a   Yang, James C ^a   Rosenberg, Steven A ^a   Kammula, Udai S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ANTIGEN; GLYCOPROTEIN GP 100; HLA A2 ANTIGEN; INTERLEUKIN 2; MELAN A; MELANOCYTE DIFFERENTIATION ANTIGEN; UNCLASSIFIED DRUG; MELANOCYTE PROTEIN PMEL 17; MELANOMA ANTIGEN; T LYMPHOCYTE RECEPTOR;

ADOPTIVE TRANSFER; ADULT; AGED; ARTICLE; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CELL CLONE; CELL THERAPY; CLINICAL ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG MEGADOSE; EVIDENCE BASED MEDICINE; FEMALE; HUMAN; IN VIVO STUDY; LYMPHOCYTE SUBPOPULATION; MALE; MELANOCYTE; METASTATIC MELANOMA; MIDDLE AGED; OUTCOME ASSESSMENT; PHASE 2 CLINICAL TRIAL; TARGET CELL; THERAPY EFFECT; TUMOR VOLUME; ADOPTIVE IMMUNOTHERAPY; ADVERSE EFFECTS; CLINICAL TRIAL; CYTOTOXICITY; DERMATITIS; GENETICS; IMMUNOLOGY; MELANOMA; METABOLISM; PATHOLOGY; TREATMENT OUTCOME; TUMOR ASSOCIATED LEUKOCYTE;

ADULT; AGED; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; DERMATITIS; FEMALE; GP100 MELANOMA ANTIGEN; HLA-A2 ANTIGEN; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MART-1 ANTIGEN; MELANOMA; MELANOMA-SPECIFIC ANTIGENS; MIDDLE AGED; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES, CYTOTOXIC; TREATMENT OUTCOME; TUMOR BURDEN;

EID: 84961291217     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-2208     Document Type: Article

References (42)

1. Atkins MB, Lotze MT, Dutcher JP, Fisher RI, Weiss G, Margolin K, 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 1999;17:2105-16.
2. Atkins MB, Kunkel L, Sznol M, Rosenberg SA. High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update. Cancer J Sci Am 2000;6:S11-S14.
3. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survivalwith ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
4. Prieto PA, Yang JC, Sherry RM, Hughes MS, Kammula US, White DE, et al. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin Cancer Res 2012;18:2039-47.
5. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
6. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.
7. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002;298:850-4.
8. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346-57.
9. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
10. Kawakami Y, Eliyahu S, Sakaguchi K, Robbins PF, Rivoltini L, Yannelli JR, et al. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J Exp Med 1994;180:347-52.
11. Kawakami Y, Eliyahu S, Jennings C, Sakaguchi K, Kang X, Southwood S, et al. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J Immunol 1995;154:3961-8.
12. Romero P, Valmori D, Pittet MJ, Zippelius A, Rimoldi D, Levy F, et al. Antigenicity and immunogenicity of Melan-A/MART-1 derived peptides as targets for tumor reactive CTL in human melanoma. Immunol Rev 2002;188:81-96.
13. Rosenberg SA, White DE. Vitiligo in patients with melanoma: normal tissue antigens can be targets for cancer immunotherapy. J Immunother Emphasis Tumor Immunol 1996;19:81-4.
14. Yee C, Thompson JA, Roche P, Byrd DR, Lee PP, Piepkorn M, et al. Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of t cell-mediated vitiligo. J Exp Med 2000;192:1637-44.
15. Robinson MR, Chan CC, Yang JC, Rubin BI, Gracia GJ, Sen HN, et al. Cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma: a new cause of uveitis. J Immunother 2004;27:478-9.
16. Jaber SH, Cowen EW, Haworth LR, Booher SL, Berman DM, Rosenberg SA, et al. Skin reactions in a subset of patients with stage IVmelanoma treated with anti-cytotoxic T-lymphocyte antigen 4 monoclonal antibody as a single agent. Arch Dermatol 2006;142:166-72.
17. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009;114:535-46.
18. Kammula US, Serrano OK. Use of high throughput qPCR screening to rapidly clone low frequency tumour specific T-cells from peripheral blood for adoptive immunotherapy. J Transl Med 2008;6:60.
19. Wang A, Chandran S, Shah SA, Chiu Y, Paria BC, Aghamolla T, et al. The stoichiometric production of IL-2 and IFN-gamma mRNA definesmemory T cells that can self-renew after adoptive transfer in humans. Sci Transl Med 2012;4:149ra120.
20. Dudley ME, Wunderlich JR, Shelton TE, Even J, Rosenberg SA. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J Immunother 2003;26:332-42.
21. Robbins PF, Dudley ME, Wunderlich J, El-Gamil M, Li YF, Zhou J, et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 2004;173:7125-30.
22. Zhou J, Dudley ME, Rosenberg SA, Robbins PF. Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in amelanoma patient receiving adoptive cell transfer therapy. J Immunother 2005;28:53-62.
23. Oshita C, Takikawa M, Kume A, Miyata H, Ashizawa T, Iizuka A, et al. Dendritic cell-based vaccination inmetastatic melanoma patients: phase II clinical trial. Oncol Rep 2012;28:1131-8.
24. + memory T cells. Eur J Immunol 2007;37:3078-88.
25. Kageshita T, Kawakami Y, Hirai S, Ono T. Differential expression of MART- 1 in primary and metastatic melanoma lesions. J Immunother 1997;20: 460-5.
26. de Vries TJ, Smeets M, de GR, Hou-Jensen K, Brocker EB, Renard N, et al. Expression of gp100, MART-1, tyrosinase, and S100 in paraffin-embedded primary melanomas and locoregional, lymph node, and visceral metastases: implications for diagnosis and immunotherapy. A study conducted by the EORTC Melanoma Cooperative Group. J Pathol 2001;193:13-20.
27. Benlalam H, Labarriere N, Linard B, Derre L, Diez E, Pandolfino MC, et al. Comprehensive analysis of the frequency of recognition of melanomaassociated antigen (MAA) by CD8 melanoma infiltrating lymphocytes (TIL): implications for immunotherapy. Eur J Immunol 2001;31:2007-15.
28. Dudley ME, Wunderlich J, Nishimura MI, Yu D, Yang JC, Topalian SL, et al. Adoptive transfer of cloned melanoma-reactive T lymphocytes for the treatment of patients with metastatic melanoma. J Immunother 2001; 24:363-73.
29. + T cells. J Clin Invest 2005;115:1616-26.
30. Dudley ME, Wunderlich JR, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, et al. A phase I study of nonmyeloablative chemotherapy and adoptive transfer of autologous tumor antigen-specific T lymphocytes in patients with metastatic melanoma. J Immunother 2002;25:243-51.
31. + T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 2002;99:16168-73.
32. Vignard V, Lemercier B, Lim A, Pandolfino MC, Guilloux Y, Khammari A, et al. Adoptive transfer of tumor-reactive Melan-A-specific CTL clones in melanoma patients is followed by increased frequencies of additional Melan-A-specific T cells. J Immunol 2005;175:4797-805.
33. Wallen H, Thompson JA, Reilly JZ, Rodmyre RM, Cao J, Yee C. Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. PLoS ONE 2009;4:e4749.
34. Khammari A, Labarriere N, Vignard V, Nguyen JM, Pandolfino MC, Knol AC, et al. Treatment of metastatic melanoma with autologous Melan-A/MART-1-specific cytotoxic T lymphocyte clones. J Invest Dermatol 2009;129:2835-42.
35. + T cells persist, mediate tumor regression, and acquire central memory phenotype. Proc Natl Acad Sci U S A 2012;109:4592-7.
36. + T cells for the treatment of patients with metastatic melanoma. J Clin Oncol 2006;24:5060-9.
37. + T cells. Sci Transl Med 2011;3:80ra34.
38. Powell DJ Jr, Dudley ME, Hogan KA, Wunderlich JR, Rosenberg SA. Adoptive transfer of vaccine-induced peripheral blood mononuclear cells to patients with metastatic melanoma following lymphodepletion. J Immunol 2006;177:6527-39.
39. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006;314:126-9.
40. Chodon T, Comin-Anduix B, Chmielowski B, Koya RC, Wu Z, Auerbach M, et al. Adoptive transfer of MART-1 T-cell receptor transgenic lymphocytes and dendritic cell vaccination in patients with metastatic melanoma. Clin Cancer Res 2014;20:2457-65.
41. Bartlett EK, Fetsch PA, Filie AC, Abati A, Steinberg SM, Wunderlich JR, et al. Human melanoma metastases demonstrate nonstochastic site-specific antigen heterogeneity that correlates with T-cell infiltration. Clin Cancer Res 2014;20:2607-16.
42. Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, Gartner J, et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat Med 2013;19:747-52.