Polyfunctional Melan-A-specific tumor-reactive CD8⁺ T cells elicited by dacarbazine treatment before peptide-vaccination depends on AKT activation sustained by ICOS

References

• Nisticò P, Capone I, Palermo B, Del Bello D, Ferraresi V, Moschella F, Aricò E, Valentini M, Bracci L, Cognetti F et al. Chemotherapy enhances vaccine-induced antitumor immunity in melanoma patients. Int J Cancer 2009; 124:130-9; PMID:18839429; http://dx.doi.org/10.1002/ijc.23886
   PubMed Web of Science ®Google Scholar
• Palermo B, Del Bello D, Sottini A, Serana F, Ghidini C, Gualtieri N, Ferraresi V, Catricalà C, Belardelli F, Proietti E et al. Dacarbazine treatment before peptide vaccination enlarges T-cell repertoire diversity of melan-a-specific, tumor-reactive CTL in melanoma patients. Cancer Res 2010; 70:7084-92; PMID:20823160; http://dx.doi.org/10.1158/0008-5472.CAN-10-1326
   PubMed Web of Science ®Google Scholar
• Frauwirth KA, Thompson CB. Activation and inhibition of lymphocytes by costimulation. J Clin Invest 2002; 109:295-299; PMID:11827987; http://dx.doi.org/10.1172/JCI0214941
   PubMed Web of Science ®Google Scholar
• Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-64; PMID:22437870; http://dx.doi.org/10.1038/nrc3239
   PubMed Web of Science ®Google Scholar
• Lenschow DJ, Walunas TL, Bluestone JA. CD28/B7 system of T cell costimulation. Annu Rev Immunol 1996; 14:233-58; PMID:8717514; http://dx.doi.org/10.1146/annurev.immunol.14.1.233
   PubMed Web of Science ®Google Scholar
• Acuto O, Michel F. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 2003; 3:939-51; PMID:14647476; http://dx.doi.org/10.1038/nri1248
   PubMed Web of Science ®Google Scholar
• Agematsu K, Kobata T, Sugita K, Freeman GJ, Beckmann MP, Schlossman SF, Morimoto C. Role of CD27 in T cell immune response. Analysis by recombinant soluble CD27. J Immunol 1994; 153:1421-9; PMID:8046222
   PubMed Web of Science ®Google Scholar
• Denoeud J1, Moser M. Role of CD27/CD70 pathway of activation in immunity and tolerance. J Leukoc Biol 2011; 89:195-203; PMID:20699361; http://dx.doi.org/10.1189/jlb.0610351
   PubMed Web of Science ®Google Scholar
• Appay V, Dunbar PR, Callan M, Klenerman P, Gillespie GM, Papagno L, Ogg GS, King A, Lechner F, Spina CA et al. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat Med 2002; 8:379-85; PMID:11927944; http://dx.doi.org/10.1038/nm0402-379
   PubMed Web of Science ®Google Scholar
• Plunkett FJ, Franzese O, Belaramani LL, Fletcher JM, Gilmour KC, Sharifi R, Khan N, Hislop AD, Cara A, Salmon M et al. The impact of telomere erosion on memory CD8+ T cells in patients with X-linked lymphoproliferative syndrome. Mech Ageing Dev 2005; 126:855-65; PMID:15992610; http://dx.doi.org/10.1016/j.mad.2005.03.006
   PubMed Web of Science ®Google Scholar
• Kopf M, Coyle AJ, Schmitz N, Barner M, Oxenius A, Gallimore A, Gutierrez-Ramos JC, Bachmann MF. Inducible costimulator protein (ICOS) controls T helper cell subset polarization after virus and parasite infection. J Exp Med 2000; 192:53-61; PMID:10880526
   Google Scholar
• Plunkett FJ, Franzese O, Finney HM, Fletcher JM, Belaramani LL, Salmon M, Dokal I, Webster D, Lawson AD, Akbar AN. The loss of telomerase activity in highly differentiated CD8+CD28-CD27- T cells is associated with decreased Akt (Ser473) phosphorylation. J Immunol 2007; 178:7710-9; PMID:17548608; http://dx.doi.org/10.4049/jimmunol.178.12.7710
   PubMed Web of Science ®Google Scholar
• Dong C, Juedes AE, Temann UA, Shresta S, Allison JP, Ruddle NH, Flavell RA. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 2001; 409:97-101; PMID:11343121; http://dx.doi.org/10.1038/35051100
   PubMed Web of Science ®Google Scholar
• Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, Kroczek RA. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999; 397:263-6; PMID:9930702; http://dx.doi.org/10.1038/16717
   PubMed Web of Science ®Google Scholar
• Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol 2002; 2:116-26; PMID:11910893; http://dx.doi.org/10.1038/nri727
   PubMed Web of Science ®Google Scholar
• Takahashi N, Matsumoto K, Saito H, Nanki T, Miyasaka N, Kobata T, Azuma M, Lee SK, Mizutani S, Morio T. Impaired CD4 and CD8 effector function and decreased memory T cell populations in ICOS-deficient patients. J Immunol 2009; 182:5515-27; PMID:19380800; http://dx.doi.org/10.4049/jimmunol.0803256
   PubMed Web of Science ®Google Scholar
• Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, Kalia V, Subramaniam S, Blattman JN, Barber DL, Ahmed R. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007; 27:670-84; PMID:17950003; http://dx.doi.org/10.1016/j.immuni.2007.09.006
   PubMed Web of Science ®Google Scholar
• Shin H, Wherry EJ. CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol 2007; 19:408-15; PMID:17656078; http://dx.doi.org/10.1016/j.coi.2007.06.004
   PubMed Web of Science ®Google Scholar
• McMahan RH, Golden-Mason L, Nishimura MI, McMahon BJ, Kemper M, Allen TM, Gretch DR, Rosen HR. Tim-3 expression on PD-1+ HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J Clin Invest 2010; 120:4546-57; PMID:21084749; http://dx.doi.org/10.1172/JCI43127
   PubMed Web of Science ®Google Scholar
• Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, Wunderlich JR, Mixon A, Farid S, Dudley ME et al. PD-1 identifies the patient-specific CD8 tumor-reactive repertoire infiltrating human tumors. J Clin Invest 2014; 124:2246-59; PMID:24667641; http://dx.doi.org/10.1172/JCI73639
   PubMed Web of Science ®Google Scholar
• Duraiswamy J, Ibegbu CC, Masopust D, Miller JD, Araki K, Doho GH, Tata P, Gupta S, Zilliox MJ, Nakaya HI et al. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J Immunol 2011; 186:4200-12; PMID:21383243; http://dx.doi.org/10.4049/jimmunol.1001783
   PubMed Web of Science ®Google Scholar
• Baitsch L, Legat A, Barba L, Fuertes Marraco SA, Rivals JP, Baumgaertner P, Christiansen-Jucht C, Bouzourene H, Rimoldi D, Pircher H et al. Extended co-expression of inhibitory receptors by human CD8 T-cells depending on differentiation, antigen-specificity and anatomical localization. PLoS One 2012; 7:30852; PMID:22347406; http://dx.doi.org/10.1371/journal.pone.0030852
   PubMed Web of Science ®Google Scholar
• Legat A, Speiser DE, Pircher H, Zehn D, Fuertes Marraco SA. Inhibitory Receptor Expression Depends More Dominantly on Differentiation and Activation than “Exhaustion” of Human CD8 T Cells. Front Immunol 2013; 4:455; PMID:24391639; http://dx.doi.org/10.3389/fimmu.2013.00455
   PubMed Web of Science ®Google Scholar
• Parry RV, Chemnitz JM, Frauwirth KA, Lanfranco AR, Braunstein I, Kobayashi SV, Linsley PS, Thompson CB, Riley JL. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol 2005; 25:9543-53; PMID:16227604; http://dx.doi.org/10.1128/MCB.25.21.9543-9553.2005
   PubMed Web of Science ®Google Scholar
• Kane LP, Weiss A. The PI-3 kinase/Akt pathway and T cell activation: pleiotropic pathways downstream of PIP3. Immunol Rev 2003; 192:7-20; PMID:12670391; http://dx.doi.org/10.1034/j.1600-065X.2003.00008.x
   PubMed Web of Science ®Google Scholar
• Finlay D, Cantrell DA. Metabolism, migration and memory in cytotoxic T cells. Nat Rev Immunol 2011; 11:109-17; PMID:21233853; http://dx.doi.org/10.1038/nri2888
   PubMed Web of Science ®Google Scholar
• Kim EH, Suresh M. Role of PI3K/Akt signaling in memory CD8 T cell differentiation. Front Immunol 2013; 4:20; PMID:23378844; http://dx.doi.org/10.3389/fimmu.2013.00020
   PubMed Web of Science ®Google Scholar
• Henson SM, Franzese O, Macaulay R, Libri V, Azevedo RI, Kiani-Alikhan S, Plunkett FJ, Masters JE, Jackson S, Griffiths SJ et al. KLRG1 signaling induces defective Akt (ser473) phosphorylation and proliferative dysfunction of highly differentiated CD8+ T cells. Blood 2009; 113:6619-28; PMID:19406987; http://dx.doi.org/10.1182/blood-2009-01-199588
   PubMed Web of Science ®Google Scholar
• Macintyre AN, Finlay D, Preston G, Sinclair LV, Waugh CM, Tamas P, Feijoo C, Okkenhaug K, Cantrell DA. Protein kinase B controls transcriptional programs that direct cytotoxic T cell fate but is dispensable for T cell metabolism. Immunity 2011; 34:224-36; PMID:21295499; http://dx.doi.org/10.1016/j.immuni.2011.01.012
   PubMed Web of Science ®Google Scholar
• Ding ZC, Huang L, Blazar BR, Yagita H, Mellor AL, Munn DH, Zhou G. Polyfunctional CD4+ T cells are essential for eradicating advanced B-cell lymphoma after chemotherapy. Blood 2012; 120:2229-39; PMID:22859605; http://dx.doi.org/10.1182/blood-2011-12-398321
   PubMed Web of Science ®Google Scholar
• Graw F, Regoes RR. Predicting the impact of CD8+ T cell polyfunctionality on HIV disease progression. J Virol 2014; 88:10134-45; PMID:24965450; http://dx.doi.org/10.1128/JVI.00647-14
   PubMed Web of Science ®Google Scholar
• Chiu YL, Shan L, Huang H, Haupt C, Bessell C, Canaday DH, Zhang H, Ho YC, Powell JD, Oelke M et al. Sprouty-2 regulates HIV-specific T cell polyfunctionality. J Clin Invest 2014; 124:198-208; PMID:24292711; http://dx.doi.org/10.1172/JCI70510
   PubMed Web of Science ®Google Scholar
• Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13:843-50; PMID:17558415; http://dx.doi.org/10.1038/nm1592
   PubMed Web of Science ®Google Scholar
• McKee MD, Roszkowski JJ, Nishimura MI. T cell avidity and tumor recognition: implications and therapeutic strategies. J Transl Med 2005; 3:35; PMID:16174302; http://dx.doi.org/10.1186/1479-5876-3-35
   PubMed Web of Science ®Google Scholar
• Yi JS, Cox MA, Zajac AJ. T-cell exhaustion: characteristics, causes and conversion. Immunology 2010; 129:474-81; PMID:20201977; http://dx.doi.org/10.1111/j.1365-2567.2010.03255.x
   PubMed Web of Science ®Google Scholar
• Henson SM, Macaulay R, Franzese O, Akbar AN. Reversal of functional defects in highly differentiated young and old CD8 T cells by PDL blockade. Immunology 2012; 135:355-63; PMID:22211948; http://dx.doi.org/10.1111/j.1365-2567.2011.03550.x
   PubMed Web of Science ®Google Scholar
• Voehringer D, Koschella M, Pircher H. Lack of proliferative capacity of human effector and memory T cells expressing killer cell lectinlike receptor G1 (KLRG1). Blood 2002; 100:3698-702; PMID:12393723; http://dx.doi.org/10.1182/blood-2002-02-0657
   PubMed Web of Science ®Google Scholar
• Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA, Qin XF, Liu YJ, Gilliet M. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007; 204:105-15; PMID:17200410; http://dx.doi.org/10.1084/jem.20061660
   PubMed Web of Science ®Google Scholar
• Zheng J, Chan PL, Liu Y, Qin G, Xiang Z, Lam KT, Lewis DB, Lau YL, Tu W. ICOS regulates the generation and function of human CD4+ Treg in a CTLA-4 dependent manner. PLoS One 2013; 8:82203; PMID:24312642; http://dx.doi.org/10.1371/journal.pone.0082203
   PubMed Web of Science ®Google Scholar
• Martin-Orozco N, Li Y, Wang Y, Liu S, Hwu P, Liu YJ, Dong C, Radvanyi L. Melanoma cells express ICOS ligand to promote the activation and expansion of T-regulatory cells. Cancer Res 2010; 70:9581-90; PMID:21098714; http://dx.doi.org/10.1158/0008-5472.CAN-10-1379
   PubMed Web of Science ®Google Scholar
• Badr G, Bédard N, Abdel-Hakeem MS, Trautmann L, Willems B, Villeneuve JP, Haddad EK, Sékaly RP, Bruneau J, Shoukry NH. Early interferon therapy for hepatitis C virus infection rescues polyfunctional, long-lived CD8+ memory T cells. J Virol 2008; 820:10017-31; PMID:18667516; http://dx.doi.org/10.1128/JVI.01083-08
   Web of Science ®Google Scholar
• Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, Bornstein E, Asher TE, Samri A, Schnuriger A, Theodorou I et al. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 2007; 204:2473-85; PMID:17893201; http://dx.doi.org/10.1084/jem.20070784
   PubMed Web of Science ®Google Scholar
• Janbazian L, Price DA, Canderan G, Filali-Mouhim A, Asher TE, Ambrozak DR, Scheinberg P, Boulassel MR, Routy JP, Koup RA et al. Clonotype and repertoire changes drive the functional improvement of HIV-specific CD8 T cell populations under conditions of limited antigenic stimulation. J Immunol 2012; 188:1156-67; PMID:22210916; http://dx.doi.org/10.4049/jimmunol.1102610
   PubMed Web of Science ®Google Scholar
• Darrah PA1, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13:843-50; PMID:17558415; http://dx.doi.org/10.1038/nm1592
   PubMed Web of Science ®Google Scholar
• Yuan J, Gnjatic S, Li H, Powel S, Gallardo HF, Ritter E, Ku GY, Jungbluth AA, Segal NH, Rasalan TS et al. CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit. Proc Natl Acad Sci U S A 2008; 105:20410-20415; PMID:19074257; http://dx.doi.org/10.1073/pnas.0810114105
   PubMed Web of Science ®Google Scholar
• Ayyoub M, Dojcinovic D, Pignon P, Raimbaud I, Schmidt J, Luescher I, Valmori D. Monitoring of NY-ESO-1 specific CD4+ T cells using molecularly defined MHC class II/His-tag-peptide tetramers. Proc Natl Acad Sci U S A 2010; 107:7437-7442; PMID:20368442; http://dx.doi.org/10.1073/pnas.1001322107
   PubMed Web of Science ®Google Scholar
• Kim EH, Sullivan JA, Plisch EH, Tejera MM, Jatzek A, Choi KY, Suresh M. Signal integration by Akt regulates CD8 T cell effector and memory differentiation. J Immunol 2012; 188:4305-14; PMID:22467649; http://dx.doi.org/10.4049/jimmunol.1103568
   PubMed Web of Science ®Google Scholar
• van der Waart AB, van de Weem NM, Maas F, Kramer CS, Kester MG, Falkenburg JH, Schaap N, Jansen JH, van der Voort R, Gattinoni L et al. Inhibition of Akt signaling promotes the generation of superior tumor-reactive T cells for adoptive immunotherapy. Blood 2014; 124:3490-500; PMID:25336630; http://dx.doi.org/10.1182/blood-2014-05-578583
   PubMed Web of Science ®Google Scholar
• Crompton JG, Sukumar M, Roychoudhuri R, Clever D, Gros A, Eil RL, Tran E, Hanada K, Yu Z, Palmer DC, Kerkar SP, Michalek RD et al. Akt inhibition enhances expansion of potent tumor-specific lymphocytes with memory cell characteristics. Cancer Res 2015; 75:296-305; PMID:25432172; http://dx.doi.org/10.1158/0008-5472.CAN-14-2277
   PubMed Web of Science ®Google Scholar
• Abu Eid R, Friedman KM, Mkrtichyan M, Walens A, King W, Janik J, Khleif SN. Akt1 and -2 inhibition diminishes terminal differentiation and enhances central memory CD8+ T-cell proliferation and survival. Oncoimmunology 2015; 4:1005448; PMID:26155399; http://dx.doi.org/10.1080/2162402X.2015.1005448
   PubMed Web of Science ®Google Scholar
• Bukczynski J, Wen T, Watts TH. Costimulation of human CD28- T cells by 4-1BB ligand. Eur J Immunol 2003; 33:446-54; PMID:12645943; http://dx.doi.org/10.1002/immu.200310020
   PubMed Web of Science ®Google Scholar
• Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol 2006; 6:595-601; PMID:16868550; http://dx.doi.org/10.1038/nri1901
   PubMed Web of Science ®Google Scholar
• Arimura Y, Kato H, Dianzani U, Okamoto T, Kamekura S, Buonfiglio D, Miyoshi-Akiyama T, Uchiyama T, Yagi J. A co-stimulatory molecule on activated T cells, H4/ICOS, delivers specific signals in T(h) cells and regulates their responses. Int Immunol 2002; 14:555-66; PMID:12039907; http://dx.doi.org/10.1093/intimm/dxf022
   PubMed Web of Science ®Google Scholar
• Takahashi N, Matsumoto K, Saito H, Nanki T, Miyasaka N, Kobata T, Azuma M, Lee SK, Mizutani S, Morio T. Impaired CD4 and CD8 effector function and decreased memory T cell populations in ICOS-deficient patients. J Immunol 2009; 182:5515-27; PMID:19380800; http://dx.doi.org/10.4049/jimmunol.0803256
   PubMed Web of Science ®Google Scholar
• Wang J, He M, Shi W, Sha H, Feng J, Wang S, Wang Y. Inducible costimulator (ICOS) enhances the cytolytic activity of cytokine-induced killer cells against gallbladder cancer in vitro and in vivo. Cancer Invest 2009; 27:244-50; PMID:19194830; http://dx.doi.org/10.1080/07357900802239124
   PubMed Web of Science ®Google Scholar
• Fan X, Quezada SA, Sepulveda MA, Sharma P, Allison JP. Engagement of the ICOS pathway markedly enhances efficacy of CTLA-4 blockade in cancer immunotherapy. J Exp Med 2014; 211:715-25; PMID:24687957; http://dx.doi.org/10.1084/jem.20130590
   PubMed Web of Science ®Google Scholar
• Okazaki T, Chikuma S, Iwai Y, Fagarasan S, Honjo T. A rheostat for immune responses: the unique properties of PD-1 and their advantages for clinical application. Nat Immunol 2013; 14:1212-8; PMID:24240160; http://dx.doi.org/10.1038/ni.2762
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-1225; PMID:23243584; http://dx.doi.org/10.4161/onci.21335
   PubMed Web of Science ®Google Scholar
• Aranda F, Vacchelli E, Eggermont A, Galon J, Fridman WH, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: Immunostimulatory monoclonal antibodies in cancer therapy. Oncoimmunology 2014; 3:27297; http://dx.doi.org/10.4161/onci.27297
   PubMed Web of Science ®Google Scholar
• Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, Brahmer JR, Lawrence DP, Atkins MB, Powderly JD et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014; 32:1020-30; PMID:24590637; http://dx.doi.org/10.1200/JCO.2013.53.0105
   PubMed Web of Science ®Google Scholar
• Caporali S, Levati L, Starace G, Ragone G, Bonmassar E, Alvino E, D'Atri S. AKT is activated in an ataxia-telangiectasia and Rad3-related-dependent manner in response to temozolomide and confers protection against drug-induced cell growth inhibition. Mol Pharmacol 2008; 74:173-83; PMID:18413665; http://dx.doi.org/10.1124/mol.107.044743
   PubMed Web of Science ®Google Scholar
• Aricò E, Belardelli F. Interferon-α as antiviral and antitumor vaccine adjuvants: mechanisms of action and response signature. J Interferon Cytokine Res 2012; 32:235-47; PMID:22490303; http://dx.doi.org/10.1089/jir.2011.0077
   PubMed Web of Science ®Google Scholar
• Daniotti M, Oggionni M, Ranzani T, Vallacchi V, Campi V, Di Stasi D, Torre GD, Perrone F, Luoni C, Suardi S et al. BRAF alterations are associated with complex mutational profiles in malignant melanoma. Oncogene 2004; 23:5968-77; PMID:15195137; http://dx.doi.org/10.1038/sj.onc.1207780
   PubMed Web of Science ®Google Scholar
• Nisticò P1, Mortarini R, De Monte LB, Mazzocchi A, Mariani M, Malavasi F, Parmiani G, Natali PG, Anichini A. Cell retargeting by bispecific monoclonal antibodies. Evidence of bypass of intratumor susceptibility to cell lysis in human melanoma. J Clin Invest 1992; 90:1093-9; PMID:1387883; http://dx.doi.org/10.1172/JCI1-15925
   PubMed Web of Science ®Google Scholar
• Lövgren T, Baumgaertner P, Wieckowski S, Devêvre E, Guillaume P, Luescher I, Rufer N, Speiser DE. Enhanced cytotoxicity and decreased CD8 dependence of human cancer-specific cytotoxic T lymphocytes after vaccination with low peptide dose. Cancer Immunol Immunother 2012; 61:817-26; PMID:22080404; http://dx.doi.org/10.1007/s00262-011-1140-1
   PubMed Web of Science ®Google Scholar