IL-15, TIM-3 and NK cells subsets predict responsiveness to anti-CTLA-4 treatment in melanoma patients

References

• Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995; 182:459-65; PMID:7543139; http://dx.doi.org/10.1084/jem.182.2.459
   PubMed Web of Science ®Google Scholar
• Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271:1734-36; PMID:8596936; http://dx.doi.org/10.1126/science.271.5256.1734
   PubMed Web of Science ®Google Scholar
• Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000; 192:1027-34; PMID:11015443; http://dx.doi.org/10.1084/jem.192.7.1027
   PubMed Web of Science ®Google Scholar
• Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol 2015; 33:1974-82; PMID:25605845; http://dx.doi.org/10.1200/JCO.2014.59.4358
   PubMed Web of Science ®Google Scholar
• Postow MA, Chesney J, Pavlick AC, Robert C, Grossmann K, McDermott D, Linette GP, Meyer N, Giguere JK, Agarwala SS et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med 2015; 372:2006-17; PMID:25891304; http://dx.doi.org/10.1056/NEJMoa1414428
   PubMed Web of Science ®Google Scholar
• Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
   PubMed Web of Science ®Google Scholar
• Weide B, Di Giacomo AM, Fonsatti E, Zitvogel L. Immunologic correlates in the course of treatment with immunomodulating antibodies. Semin Oncol 2015; 42:448-58; PMID:25965363; http://dx.doi.org/10.1053/j.seminoncol.2015.02.016
   PubMed Web of Science ®Google Scholar
• Ascierto PA, Kalos M, Schaer DA, Callahan MK, Wolchok JD. Biomarkers for immunostimulatory monoclonal antibodies in combination strategies for melanoma and other tumor types. Clin Cancer Res 2013; 19:1009-20; PMID:23460532; http://dx.doi.org/10.1158/1078-0432.CCR-12-2982
   PubMed Web of Science ®Google Scholar
• Kitano S, Tsuji T, Liu C, Hirschhorn-Cymerman D, Kyi C, Mu Z, Allison JP, Gnjatic S, Yuan JD, Wolchok JD. Enhancement of tumor-reactive cytotoxic CD4+ T cell responses after ipilimumab treatment in four advanced melanoma patients. Cancer Immunol Res 2013; 1:235-44; PMID:24396833; http://dx.doi.org/10.1158/2326-6066.CIR-13-0068
   PubMed Web of Science ®Google Scholar
• Wang W, Yu D, Sarnaik AA, Yu B, Hall M, Morelli D, Zhang Y, Zhao X, Weber JS. Biomarkers on melanoma patient T cells associated with ipilimumab treatment. J Transl Med 2012; 10:146; PMID:22788688; http://dx.doi.org/10.1186/1479-5876-10-146
   PubMed Web of Science ®Google Scholar
• Simeone E, Gentilcore G, Giannarelli D, Grimaldi AM, Caracò C, Curvietto M, Esposito A, Paone M, Palla M, Cavalcanti E et al. Immunological and biological changes during ipilimumab treatment and their potential correlation with clinical response and survival in patients with advanced melanoma. Cancer Immunol Immunother 2014; 63:675-83; PMID:24695951; http://dx.doi.org/10.1007/s00262-014-1545-8
   PubMed Web of Science ®Google Scholar
• Weide B, Martens A, Hassel JC, Berking C, Postow MA, Bisschop K Simeone E, Mangana J, Schilling B, Di Giacomo AM et al. Baseline biomarkers for outcome of melanoma patients treated with pembrolizumab. Clin Cancer Res 2016; clincanres. 0127.2016; PMID:27185375; http://dx.doi.org/10.1158/1078-0432.CCR-16-0127
   Web of Science ®Google Scholar
• Martens A, Wistuba-Hamprecht K, Geukes Foppen M, Yuan J, Postow MA, Wong P, Romano E, Khammari A, Dreno B, Capone M et al. Baseline Peripheral Blood Biomarkers Associated with Clinical Outcome of Advanced Melanoma Patients Treated with Ipilimumab. Clin Cancer Res 2016; 22:2908-18; PMID:26787752; http://dx.doi.org/10.1158/1078-0432.CCR-15-2412
   PubMed Web of Science ®Google Scholar
• Martens A, Wistuba-Hamprecht K, Yuan J, Postow MA, Wong P, Capone M, Madonna G, Khammari A, Schilling B, Sucker A et al. Increases in absolute lymphocytes and circulating CD4+ and CD8+ T cells are associated with positive clinical outcome of melanoma patients treated with ipilimumab. Clin Cancer Res 2016; 22(19):4848-4858; pii: clincanres.0249.2016; PMID:27169993; http://dx.doi.org/10.1158/1078-0432.CCR-16-0249
   PubMed Web of Science ®Google Scholar
• Kvistborg P, Philips D, Kelderman S, Hageman L, Ottensmeier C, Joseph-Pietras D, Welters MJ, van der Burg S, Kapiteijn E, Michielin O et al. Anti-CTLA-4 therapy broadens the melanoma-reactive CD8+ T cell response. Sci Transl Med 2014; 6:254ra128; http://dx.doi.org/10.1126/scitranslmed.3008918
   PubMed Web of Science ®Google Scholar
• Weber JS, Hamid O, Chasalow SD, Wu DY, Parker SM, Galbraith S, Gnjatic S, Berman D. Ipilimumab increases activated T cells and enhances humoral immunity in patients with advanced melanoma. J Immunother 2012; 35:89-97; PMID:22130166; http://dx.doi.org/10.1097/CJI.0b013e31823aa41c
   PubMed Web of Science ®Google Scholar
• Romano E, Kusio-Kobialka M, Foukas PG, Baumgaertner P, Meyer C, Ballabeni P, Michielin O, Weide B, Romero P, Speiser DE. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc Natl Acad Sci U S A 2015; 112:6140-45; PMID:25918390; http://dx.doi.org/10.1073/pnas.1417320112
   PubMed Web of Science ®Google Scholar
• Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, Nomura T, Sakaguchi S. CTLA-4 control over Foxp3+ regulatory T cell function. Science 2008; 322:271-5; PMID:18845758; http://dx.doi.org/10.1126/science.1160062
   PubMed Web of Science ®Google Scholar
• Suarez N, Alfaro C, Dubrot J, Palazon A, Bolaños E, Erro L, Hervas-Stubbs S, Martinez-Forero I, Morales-Kastresana A, Martin-Algarra S et al. Synergistic effects of CTLA-4 blockade with tremelimumab and elimination of regulatory T lymphocytes in vitro and in vivo. Int J Cancer 2011; 129:374-86; PMID:20853321; http://dx.doi.org/10.1002/ijc.25681
   PubMed Web of Science ®Google Scholar
• Simpson TR, Li F, Montalvo-Ortiz W, Sepulveda MA, Bergerhoff K, Arce F, Roddie C, Henry JY, Yagita H, Wolchok JD et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J Exp Med 2013; 210:1695-710; PMID:23897981; http://dx.doi.org/10.1084/jem.20130579
   PubMed Web of Science ®Google Scholar
• Kiessling R, Klein E, Wigzell H. “Natural” killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol 1975; 5:112-7; PMID:1234049; http://dx.doi.org/10.1002/eji.1830050208
   PubMed Web of Science ®Google Scholar
• Kiessling R, Klein E, Pross H, Wigzell H. “Natural” killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 1975; 5:117-21; PMID:1086218; http://dx.doi.org/10.1002/eji.1830050209
   PubMed Web of Science ®Google Scholar
• Kärre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986; 319:675-8; PMID:3951539; http://dx.doi.org/10.1038/319675a0
   PubMed Web of Science ®Google Scholar
• Lakshmikanth T, Burke S, Ali TH, Kimpfler S, Ursini F, Ruggeri L, Capanni M, Umansky V, Paschen A, Sucker A et al. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J Clin Invest 2009; 119:1251-63; PMID:19349689; http://dx.doi.org/10.1172/JCI36022
   PubMed Web of Science ®Google Scholar
• Ferrari de Andrade L, Ngiow SF, Stannard K, Rusakiewicz S, Kalimutho M, Khanna KK, Tey SK, Takeda K, Zitvogel L, Martinet L et al. Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma. Cancer Res 2014; 74:7298-308; PMID:25351955; http://dx.doi.org/10.1158/0008-5472.CAN-14-1339
   PubMed Web of Science ®Google Scholar
• Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, Gonçalves A, André P, Romagné F, Thibault G et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest 2011; 121:3609-22; PMID:21841316; http://dx.doi.org/10.1172/JCI45816
   PubMed Web of Science ®Google Scholar
• Delahaye NF, Rusakiewicz S, Martins I, Ménard C, Roux S, Lyonnet L, Paul P, Sarabi M, Chaput N, Semeraro M et al. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med 2011; 17:700-7; PMID:21552268; http://dx.doi.org/10.1038/nm.2366
   PubMed Web of Science ®Google Scholar
• Takeuchi H, Maehara Y, Tokunaga E, Koga T, Kakeji Y, Sugimachi K. Prognostic significance of natural killer cell activity in patients with gastric carcinoma: a multivariate analysis. Am J Gastroenterol 2001; 96:574-8; PMID:11232710; http://dx.doi.org/10.1111/j.1572-0241.2001.03535.x
   PubMed Web of Science ®Google Scholar
• Ali TH, Pisanti S, Ciaglia E, Mortarini R, Anichini A, Garofalo C, Tallerico R, Santinami M, Gulletta E, Ietto C et al. Enrichment of CD56(dim)KIR + CD57 + highly cytotoxic NK cells in tumour-infiltrated lymph nodes of melanoma patients. Nat Commun 2014; 5:5639; PMID:25472612; http://dx.doi.org/10.1038/ncomms6639
   PubMed Web of Science ®Google Scholar
• Conlon KC, Lugli E, Welles HC, Rosenberg SA, Fojo AT, Morris JC, Fleisher TA, Dubois SP, Perera LP, Stewart DM et al. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J Clin Oncol 2015; 33:74-82; PMID:25403209; http://dx.doi.org/10.1200/JCO.2014.57.3329
   PubMed Web of Science ®Google Scholar
• Wang H, Zhu JY, Liu CC, Zhu MY, Wang JH, Geng QR, Lu Y. Increased serum levels of interleukin 15 correlate with negative prognostic factors in extra nodal NK / T cell lymphoma. Med Oncol 2015; 32:370; PMID:25428383; http://dx.doi.org/10.1007/s12032-014-0370-4
   PubMed Web of Science ®Google Scholar
• Waldmann TA. Interleukin-15 in the treatment of cancer. Expert Rev Clin Immunol 2014; 10:1689-701; PMID:25359408; http://dx.doi.org/10.1586/1744666X.2014.973856
   PubMed Web of Science ®Google Scholar
• Ndhlovu LC, Lopez-Vergès S, Barbour JD, Jones RB, Jha AR, Long BR, Schoeffler EC, Fujita T, Nixon DF, Lanier LL. Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity. Blood 2012; 119:3734-43; PMID:22383801; http://dx.doi.org/10.1182/blood-2011-11-392951
   PubMed Web of Science ®Google Scholar
• da Silva IP, Gallois A, Jimenez-Baranda S, Khan S, Anderson AC, Kuchroo VK, Osman I, Bhardwaj N. Reversal of NK-cell exhaustion in advanced melanoma by Tim-3 blockade. Cancer Immunol Res 2014; 2:410-22; PMID:24795354; http://dx.doi.org/10.1158/2326-6066.CIR-13-0171
   PubMed Web of Science ®Google Scholar
• Gallois A, Silva I, Osman I, Bhardwaj N. Reversal of natural killer cell exhaustion by TIM-3 blockade. Oncoimmunology 2015; 3:e946365; PMID:25964857; http://dx.doi.org/10.4161/21624011.2014.946365
   PubMed Web of Science ®Google Scholar
• Elpek KG, Rubinstein MP, Bellemare-Pelletier A, Goldrath AW, Turley SJ. Mature natural killer cells with phenotypic and functional alterations accumulate upon sustained stimulation with IL-15/IL-15Ralpha complexes. Proc Natl Acad Sci U S A 2010; 107:21647-52; PMID:21098276; http://dx.doi.org/10.1073/pnas.1012128107
   PubMed Web of Science ®Google Scholar
• Gleason MK, Lenvik TR, McCullar V, Felices M, O'Brien MS, Cooley SA, Verneris MR, Cichocki F, Holman CJ, Panoskaltsis-Mortari A et al. Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood 2012; 119:3064-72; PMID:22323453; http://dx.doi.org/10.1182/blood-2011-06-360321
   PubMed Web of Science ®Google Scholar
• Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 2015; 350:1079-84; PMID:2654161; http://dx.doi.org/10.1126/science.aad1329
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Ménard C, Martin F, Zitvogel L. The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression. Immunol Rev 2006; 214:229-38; PMID:17100888; http://dx.doi.org/10.1111/j.1600-065X.2006.00445.x
   PubMed Web of Science ®Google Scholar
• Laurent S, Queirolo P, Boero S, Salvi S, Piccioli P, Boccardo S, Minghelli S, Morabito A, Fontana V, Pietra G et al. The engagement of CTLA-4 on primary melanoma cell lines induces antibody-dependent cellular cytotoxicity and TNF-α production. J Transl Med 2013; 11:108; PMID:23634660; http://dx.doi.org/10.1186/1479-5876-11-108
   PubMed Web of Science ®Google Scholar
• Uen WC, Hsieh CH, Tseng TT, Jiang SS, Tseng JC, Lee SC. Anchorage independency promoted tumor malignancy of melanoma cells under reattachment through elevated interleukin-8 and CXC chemokine receptor 1 expression. Melanoma Res 2015; 25:35-46; PMID:25426644; http://dx.doi.org/10.1097/CMR.0000000000000134
   PubMed Web of Science ®Google Scholar
• Miller JS. Therapeutic applications: natural killer cells in clinic. Hematology Am Soc Hematol Educ Program 2013; 2013:247-53; PMID:24319187; http://dx.doi.org/10.1182/asheducation-2013.1.247
   PubMed Web of Science ®Google Scholar
• Eriksson L, Johansson E. Multi- and Megavariate Data Analysis: Principles and application. Umetrics A B 2001; Umetrics Academics Publishing 533 pp. 2001. ISBN 919737301X, 9789197373012.
   Google Scholar
• Trygg J, Wold S. Orthogonal Projections to Latent Structures (O-PLS). Chemometrics 2002; 16:119-28; http://dx.doi.org/10.1002/cem.695
   Web of Science ®Google Scholar
• Dutta M, Subramani E, Taunk K, Gajbhiye A, Seal S, Pendharkar N, Dhali S, Ray CD, Lodh I, Chakravarty B et al. Investigation of serum proteome alterations in human endometriosis. J Proteomics 2015; 114:182-96; PMID:25449831; http://dx.doi.org/10.1016/j.jprot.2014.10.021
   PubMed Web of Science ®Google Scholar