PD-1 expression conditions T cell avidity within an antigen-specific repertoire

OncoImmunology

Volumn 5, Issue 1, 2016, Pages

  Simon, Sylvain ^a,b,c   Vignard, Virginie ^a,b,c   Florenceau, Laetitia ^a,b,c   Dreno, B ^a,b,c   Khammari, A ^a,b,c   Lang, F ^a,b   Labarriere, N ^a,b,c  

^a Team 12   (France)

^b Oncology"   (France)

^c NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Adoptive T cell transfer; immunotherapy; Melan A; melanoma; PD 1; T cell avidity

Indexed keywords

BIOLOGICAL MARKER; GAMMA INTERFERON; PROGRAMMED DEATH 1 RECEPTOR; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR;

ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MELANOMA; METHYLATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; REAL TIME REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE;

EID: 84982752093     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1104448     Document Type: Article

References (33)

1. Kamphorst AO, Ahmed R. Manipulating the PD-1 pathway to improve immunity. Curr Opin Immunol 2013; 25:381-8; PMID:23582509; http://dx.doi.org/10.1016/j.coi.2013.03.003
2. Moll M, Kuylenstierna C, Gonzalez VD, Andersson SK, Bosnjak L, Sonnerborg A, Quigley MF, Sandberg JK. Severe functional impairment and elevated PD-1 expression in CD1d-restricted NKT cells retained during chronic HIV-1 infection. Eur J Immunol 2009; 39:902-11; PMID:19197939; http://dx.doi.org/10.1002/eji.200838780
3. Riley JL. PD-1 signaling in primary T cells. Immunol Rev 2009; 229:114-25; PMID:19426218; http://dx.doi.org/10.1111/j.1600-065X.2009.00767.x
4. Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999; 11:141-51; PMID:10485649; http://dx.doi.org/10.1016/S1074-7613(00)80089-8
5. Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, Sasayama S, Mizoguchi A, Hiai H, Minato N et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001; 291:319-22; PMID:11209085; http://dx.doi.org/10.1126/science.291.5502.319
6. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008; 26:677-704; PMID:18173375; http://dx.doi.org/10.1146/annurev.immunol.26.021607.090331
7. Sheppard KA, Fitz LJ, Lee JM, Benander C, George JA, Wooters J, Qiu Y, Jussif JM, Carter LL, Wood CR et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett 2004; 574:37-41; PMID:15358536; http://dx.doi.org/10.1016/j.febslet.2004.07.083
8. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, Roche PC, Lu J, Zhu G, Tamada K et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002; 8:793-800; PMID:12091876; http://dx.doi.org/10.1038/nm0902-1039c
9. Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-5; PMID:23243584; http://dx.doi.org/10.4161/onci.21335
10. Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE, Rosenberg SA. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 2009; 114:1537-44; PMID:19423728; http://dx.doi.org/10.1182/blood-2008-12-195792
11. 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
12. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, Wolchok JD, Hersey P, Joseph RW, Weber JS et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013; 369:134-44; PMID:23724846; http://dx.doi.org/10.1056/NEJMoa1305133
13. 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
14. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-33; PMID:23724867; http://dx.doi.org/10.1056/NEJMoa1302369
15. Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, Chen L, Pardoll DM, Topalian SL, Anders RA. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014; 20:5064-74; PMID:24714771; http://dx.doi.org/10.1158/1078-0432.CCR-13-3271
16. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515:568-71; PMID:25428505; http://dx.doi.org/10.1038/nature13954
17. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015; 348:124-8; PMID:25765070; http://dx.doi.org/10.1126/science.aaa1348
18. Labarriere N, Fortun A, Bellec A, Khammari A, Dreno B, Saiagh S, Lang F. A full GMP process to select and amplify epitope-specific T lymphocytes for adoptive immunotherapy of metastatic melanoma. Clin Dev Immunol 2013; 2013:932318; PMID:24194775; http://dx.doi.org/10.1155/2013/932318
19. Kawakami Y, Eliyahu S, Delgado CH, Robbins PF, Rivoltini L, Topalian SL, Miki T, Rosenberg SA. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc Natl Acad Sci U S A 1994; 91:3515-9; PMID:8170938; http://dx.doi.org/10.1073/pnas.91.9.3515
20. Godet Y, Moreau-Aubry A, Guilloux Y, Vignard V, Khammari A, Dreno B, Jotereau F, Labarriere N. MELOE-1 is a new antigen overexpressed in melanomas and involved in adoptive T cell transfer efficiency. J Exp Med 2008; 205:2673-82; PMID:18936238; http://dx.doi.org/10.1084/jem.20081356
21. Youngblood B, Noto A, Porichis F, Akondy RS, Ndhlovu ZM, Austin JW, Bordi R, Procopio FA, Miura T, Allen TM et al. Cutting edge: Prolonged exposure to HIV reinforces a poised epigenetic program for PD-1 expression in virus-specific CD8 T cells. J Immunol 2013; 191:540-4; PMID:23772031; http://dx.doi.org/10.4049/jimmunol.1203161
22. Youngblood B, Oestreich KJ, Ha SJ, Duraiswamy J, Akondy RS, West EE, Wei Z, Lu P, Austin JW, Riley JL et al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 2011; 35:400-12; PMID:21943489; http://dx.doi.org/10.1016/j.immuni.2011.06.015
23. Bouquie R, Bonnin A, Bernardeau K, Khammari A, Dreno B, Jotereau F, Labarrière N, Lang F. A fast and efficient HLA multimer-based sorting procedure that induces little apoptosis to isolate clinical grade human tumor specific T lymphocytes. Cancer Immunol Immunother 2009; 58:553-66; PMID:18751701; http://dx.doi.org/10.1007/s00262-008-0578-2
24. Trautmann L, Labarriere N, Jotereau F, Karanikas V, Gervois N, Connerotte T, Coulie P, Bonneville M. Dominant TCR V alpha usage by virus and tumor-reactive T cells with wide affinity ranges for their specific antigens. Eur J Immunol 2002; 32:3181-90; PMID:12555663; http://dx.doi.org/10.1002/1521-4141(200211)32:11%3c3181::AID-IMMU3181%3e3.0.CO;2-2
25. Orskov AD, Treppendahl MB, Skovbo A, Holm MS, Friis LS, Hokland M, Grønbæk K. Hypomethylation and up-regulation of PD-1 in T cells by azacytidine in MDS/AML patients: A rationale for combined targeting of PD-1 and DNA methylation. Oncotarget 2015; 6:9612-26; PMID:25823822; http://dx.doi.org/10.18632/oncotarget.3324
26. Martinez GJ, Pereira RM, Aijo T, Kim EY, Marangoni F, Pipkin ME, Togher S, Heissmeyer V, Zhang YC, Crotty S et al. The Transcription Factor NFAT Promotes Exhaustion of Activated CD8 T Cells. Immunity 2015; 42:265-78; PMID:25680272; http://dx.doi.org/10.1016/j.immuni.2015.01.006
27. Oestreich KJ, Yoon H, Ahmed R, Boss JM. NFATc1 regulates PD-1 expression upon T cell activation. J Immunol 2008; 181:4832-9; PMID:18802087; http://dx.doi.org/10.4049/jimmunol.181.7.4832
28. Odorizzi PM, Pauken KE, Paley MA, Sharpe A, Wherry EJ. Genetic absence of PD-1 promotes accumulation of terminally differentiated exhausted CD8+ T cells. J Exp Med 2015; 212:1125-37; PMID:26034050; http://dx.doi.org/10.1084/jem.20142237
29. Blank C, Brown I, Marks R, Nishimura H, Honjo T, Gajewski TF. Absence of programmed death receptor 1 alters thymic development and enhances generation of CD4/CD8 double-negative TCR-transgenic T cells. J Immunol 2003; 171:4574-81; PMID:14568931; http://dx.doi.org/10.4049/jimmunol.171.9.4574
30. Nishimura H, Honjo T, Minato N. Facilitation of beta selection and modification of positive selection in the thymus of PD-1-deficient mice. J Exp Med 2000; 191:891-8; PMID:10704469; http://dx.doi.org/10.1084/jem.191.5.891
31. Wong RM, Scotland RR, Lau RL, Wang C, Korman AJ, Kast WM, Weber JS. Programmed death-1 blockade enhances expansion and functional capacity of human melanoma antigen-specific CTLs. Int Immunol 2007; 19:1223-34; PMID:17898045; http://dx.doi.org/10.1093/intimm/dxm091
32. Inozume T, Hanada K, Wang QJ, Ahmadzadeh M, Wunderlich JR, Rosenberg SA, Yang JC. Selection of CD8+PD-1+ lymphocytes in fresh human melanomas enriches for tumor-reactive T cells. J Immunother 2010; 33:956-64; PMID:20948441; http://dx.doi.org/10.1097/CJI.0b013e3181fad2b0
33. Gervois N, Labarriere N, Le Guiner S, Pandolfino MC, Fonteneau JF, Guilloux Y, Diez E, Dreno B, Jotereau F. High avidity melanoma-reactive cytotoxic T lymphocytes are efficiently induced from peripheral blood lymphocytes on stimulation by peptide-pulsed melanoma cells. Clin Cancer Res 2000; 6:1459-67; PMID:10778978