BTLA marks a less-differentiated tumor-infiltrating lymphocyte subset in melanoma with enhanced survival properties

OncoImmunology

Volumn 4, Issue 8, 2015, Pages

  Haymaker, Cara L ^a   Wu, Richard C ^a,b,c,d   Ritthipichai, Krit ^a,c   Bernatchez, Chantale ^a,d   Forget, Marie Andrée ^a   Chen, Jie Qing ^a,e   Liu, Hui ^f   Wang, Ena ^f,g   Marincola, Francesco ^h,i   Hwu, Patrick ^a,e   Radvanyi, Laszlo G ^a,e,i  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e Lion Biotechnologies   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

^g SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

^h NATIONAL CANCER INSTITUTE   (United States)

ⁱ H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

B and T lymphocyte attenuator; CD8+ effector memory; melanoma; T cell survival persistence; tumor infiltrating lymphocytes

Indexed keywords

CD27 ANTIGEN; CD28 ANTIGEN; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; HERPESVIRUS ENTRY MEDIATOR LIGAND; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; OMIPALISIB; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN BCL XL; PROTEIN KINASE B; STAT5 PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE T LYMPHOCYTE THERAPY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SELECTION; CELL THERAPY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; CYTOLYSIS; FLOW CYTOMETRY; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; METASTATIC MELANOMA; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; RNA EXTRACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE;

EID: 84940492696     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1014246     Document Type: Article

References (47)

1. M.E.Dudley, J.R.Wunderlich, J.C.Yang, R.M.Sherry, S.L.Topalian, N.P.Restifo, R.E.Royal, U.Kammula, D.E.White, S.A.Mavroukakis, 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; PMID:15800326; http://dx.doi.org/10.1200/JCO.2005.00.240
2. L.G.Radvanyi, C.Bernatchez, M.Zhang, P.S.Fox, P.Miller, J.Chacon, R.Wu, G.Lizee, S.Mahoney, G.Alvarado, et al. Specific lymphocyte subsets predict response to adoptive cell therapy using expanded autologous tumor-infiltrating lymphocytes in metastatic melanoma patients. Clin Cancer Res 2012; 18:6758-70; PMID:23032743; http://dx.doi.org/10.1158/1078-0432.CCR-12-1177
3. M.J.Besser, R.Shapira-Frommer, A.J.Treves, D.Zippel, O.Itzhaki, L.Hershkovitz, D.Levy, A.Kubi, E.Hovav, N.Chermoshniuk, et al. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res 2010; 16:2646-55; PMID:20406835; http://dx.doi.org/10.1158/1078-0432.CCR-10-0041
4. C.A.Klebanoff, L.Gattinoni, N.P.Restifo. Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? J Immunother 2012; 35:651-60; PMID:23090074; http://dx.doi.org/10.1097/CJI.0b013e31827806e6
5. N.Watanabe, M.Gavrieli, J.R.Sedy, J.Yang, F.Fallarino, S.K.Loftin, M.A.Hurchla, N.Zimmerman, J.Sim, X.Zang, et al. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol 2003; 4:670-9; PMID:12796776; http://dx.doi.org/10.1038/ni944
6. L.Derre, J.P.Rivals, C.Jandus, S.Pastor, D.Rimoldi, P.Romero, O.Michielin, D.Olive, D.E.Speiser. BTLA mediates inhibition of human tumor-specific CD8+ T cells that can be partially reversed by vaccination. J Clin Invest 2010; 120:157-67; PMID:20038811; http://dx.doi.org/10.1172/JCI40070
7. J.Fourcade, Z.Sun, O.Pagliano, P.Guillaume, I.F.Luescher, C.Sander, J.M.Kirkwood, D.Olive, V.Kuchroo, H.M.Zarour. CD8(+) T cells specific for tumor antigens can be rendered dysfunctional by the tumor microenvironment through upregulation of the inhibitory receptors BTLA and PD-1. Cancer Res 2012; 72:887-96; PMID:22205715; http://dx.doi.org/10.1158/0008-5472.CAN-11-2637
8. M.Gavrieli, K.M.Murphy. Association of Grb-2 and PI3K p85 with phosphotyrosile peptides derived from BTLA. Biochem Biophys Res Commun 2006; 345:1440-5; PMID:16725108; http://dx.doi.org/10.1016/j.bbrc.2006.05.036
9. E.Wakamatsu, D.Mathis, C.Benoist. Convergent and divergent effects of costimulatory molecules in conventional and regulatory CD4+ T cells. Proc Natl Acad Sci 2013; 110:1023-8; PMID:23277554; http://dx.doi.org/10.1073/pnas.1220688110
10. N.E.Serriari, F.Gondois-Rey, Y.Guillaume, E.B.Remmerswaal, S.Pastor, N.Messal, A.Truneh, I.Hirsch, R.A.van Lier, D.Olive. B- and T- lymphocyte attenuator is highly expressed on CMV-specific T cells during infection and regulates their function. J Immunol 2010; 185:3140-8; PMID:20693422
11. A.Legat, D.E.Speiser, H.Pircher, D.Zehn, S.A.Fuertes Marraco. 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
12. L.Baitsch, A.Legat, L.Barba, S.A.Fuertes Marraco, J.P.Rivals, P.Baumgaertner, C.Christiansen-Jucht, H.Bouzourene, D.Rimoldi, H.Pircher, 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:e30852; PMID:22347406; http://dx.doi.org/10.1371/journal.pone.0030852
13. I.A.Parish, S.Rao, G.K.Smyth, T.Juelich, G.S.Denyer, G.M.Davey, A.Strasser, W.R.Heath. The molecular signature of CD8+ T cells undergoing deletional tolerance. Blood 2009; 113:4575-85; PMID:19204323; http://dx.doi.org/10.1182/blood-2008-10-185223
14. I.A.Parish, S.M.Kaech. Diversity in CD8(+) T cell differentiation. Curr Opin Immunol 2009; 21:291-7; PMID:19497720; http://dx.doi.org/10.1016/j.coi.2009.05.008
15. I.R.Turnbull, M.Colonna. Activating and inhibitory functions of DAP12. Nat Rev Immunol 2007; 7:155-61; PMID:17220916; http://dx.doi.org/10.1038/nri2014
16. M.J.Smyth, Y.Hayakawa, K.Takeda, H.Yagita. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2002; 2:850-61; PMID:12415255; http://dx.doi.org/10.1038/nrc928
17. J.Duraiswamy, C.C.Ibegbu, D.Masopust, J.D.Miller, K.Araki, G.H.Doho, P.Tata, S.Gupta, M.J.Zilliox, H.I.Nakaya, 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
18. T.Willinger, T.Freeman, H.Hasegawa, A.J.McMichael, M.F.Callan. Molecular signatures distinguish human central memory from effector memory CD8 T cell subsets. J Immunol 2005; 175:5895-903; PMID: 16237082; http://dx.doi.org/10.4049/jimmunol.175.9.5895
19. Y.Li, S.Liu, J.Hernandez, L.Vence, P.Hwu, L.Radvanyi. MART-1-specific melanoma tumor-infiltrating lymphocytes maintaining CD28 expression have improved survival and expansion capability following antigenic restimulation in vitro. J Immunol 2010; 184:452-65; PMID:19949105; http://dx.doi.org/10.4049/jimmunol.0901101
20. N.P.Weng, A.N.Akbar, J.Goronzy. CD28(-) T cells: their role in the age-associated decline of 676 immune function. Trends Immunol 2009; 30:306-12; PMID:19540809; http://dx.doi.org/10.1016/j.it.2009.03.013
21. K.M.Brumbaugh, B.A.Binstadt, D.D.Billadeau, R.A.Schoon, C.J.Dick, R.M.Ten, P.J.Leibson. Functional role for Syk tyrosine kinase in natural killer cell-mediated natural cytotoxicity. J Exp Med 1997; 186:1965-74; PMID:9396765; http://dx.doi.org/10.1084/jem.186.12.1965
22. A.Poli, T.Michel, M.Theresine, E.Andres, F.Hentges, J.Zimmer. CD56bright natural killer (NK) cells: an important NK cell subset. Immunology 2009; 126:458-65; PMID:19278419; http://dx.doi.org/10.1111/j.1365-2567.2008.03027.x
23. N.Sugimoto, T.Oida, K.Hirota, K.Nakamura, T.Nomura, T.Uchiyama, S.Sakaguchi. Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis. Int Immunol 2006; 18:1197-209; PMID:16772372; http://dx.doi.org/10.1093/intimm/dxl060
24. M.Safford, S.Collins, M.A.Lutz, A.Allen, C.T.Huang, J.Kowalski, A.Blackford, M.R.Horton, C.Drake, R.H.Schwartz, et al. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat Immunol 2005; 6:472-80; PMID:15834410; http://dx.doi.org/10.1038/ni1193
25. B.J.Calnan, S.Szychowski, F.K.Chan, D.Cado, A.Winoto. A role for the orphan steroid receptor Nur77 in apoptosis accompanying antigen-induced negative selection. Immunity 1995; 3:273-82; PMID:7552993; http://dx.doi.org/10.1016/1074-7613(95)90113-2
26. L.Baitsch, P.Baumgaertner, E.Devevre, S.K.Raghav, A.Legat, L.Barba, S.Wieckowski, H.Bouzourene, B.Deplancke, P.Romero, et al. Exhaustion of tumor-specific CD8(+) T cells in metastases from melanoma patients. J Clin Invest 2011; 121:2350-60; PMID:21555851; http://dx.doi.org/10.1172/JCI46102
27. E.J.Wherry, S.J.Ha, S.M.Kaech, W.N.Haining, S.Sarkar, V.Kalia, S.Subramaniam, J.N.Blattman, D.L.Barber, R.Ahmed. 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
28. F.Sallusto, J.Geginat, A.Lanzavecchia. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004; 22:745-63; PMID:15032595; http://dx.doi.org/10.1146/annurev.immunol.22.012703.104702
29. M.Strioga, V.Pasukoniene, D.Characiejus. CD8+ CD28- and CD8+ CD57+ T cells and their role in 695 health and disease. Immunology 2011; 134:17-32; PMID:21711350; http://dx.doi.org/10.1111/j.1365-2567.2011.03470.x
30. S.A.Rosenberg, J.C.Yang, R.M.Sherry, U.S.Kammula, M.S.Hughes, G.Q.Phan, D.E.Citrin, N.P.Restifo, P.F.Robbins, J.R.Wunderlich, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011; 17:4550-7; PMID:21498393; http://dx.doi.org/10.1158/1078-0432.CCR-11-0116
31. N.D.Collins, C.D'Souza, B.Albrecht, M.D.Robek, L.Ratner, W.Ding, P.L.Green, M.D.Lairmore. Proliferation response to interleukin-2 and Jak/Stat activation of T cells immortalized by human T-cell lymphotropic virus type 1 is independent of open reading frame I expression. J Virol 1999; 73:9642-9; PMID:10516077
32. D.Herndler-Brandstetter, S.Schwaiger, E.Veel, C.Fehrer, D.P.Cioca, G.Almanzar, M.Keller, G.Pfister, W.Parson, R.Würzner, et al. CD25-expressing CD8+ T cells are potent memory cells in old age. J Immunol 2005; 175:1566-74; PMID:16034095; http://dx.doi.org/10.4049/jimmunol.175.3.1566
33. E.A.Eisenhauer, P.Therasse, J.Bogaerts, L.H.Schwartz, D.Sargent, R.Ford, J.Dancey, S.Arbuck, S.Gwyther, M.Mooney, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009; 45:228-47; PMID:19097774; http://dx.doi.org/10.1016/j.ejca.2008.10.026
34. J.D.Wolchok, A.Hoos, S.O'Day, J.S.Weber, O.Hamid, C.Lebbe, M.Maio, M.Binder, O.Bohnsack, G.Nichol, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009; 15:7412-20; PMID:19934295; http://dx.doi.org/10.1158/1078-0432.CCR-09-1624
35. L.G.Radvanyi, Y.Shi, H.Vaziri, A.Sharma, R.Dhala, G.B.Mills, R.G.Miller. CD28 costimulation inhibits TCR-induced apoptosis during a primary T cell response. J Immunol 1996; 156:1788-98; PMID:8596028
36. M.A.Hurchla, J.R.Sedy, K.M.Murphy. Unexpected role of B and T lymphocyte attenuator in sustaining cell survival during chronic allostimulation. J Immunol 2007; 178:6073-82; PMID:17475832; http://dx.doi.org/10.4049/jimmunol.178.10.6073
37. A.Bergmann. Survival signaling goes BAD. Dev Cell 2002; 3:607-8; PMID:12431365; http://dx.doi.org/10.1016/S1534-5807(02)00328-3
38. K.M.Murphy, C.A.Nelson, J.R.Sedy. Balancing co-stimulation and inhibition with BTLA and HVEM. Nat Rev Immunol 2006; 6:671-81; PMID:16932752; http://dx.doi.org/10.1038/nri1917
39. G.Henel, K.Singh, D.Cui, S.Pryshchep, W.W.Lee, C.M.Weyand, J.J.Goronzy. Uncoupling of T-cell effector functions by inhibitory killer immunoglobulin-like receptors. Blood 2006; 107:4449-57; PMID:16469873; http://dx.doi.org/10.1182/blood-2005-06-2519
40. N.K.Bjorkstrom, V.Beziat, F.Cichocki, L.L.Liu, J.Levine, S.Larsson, R.A.Koup, S.K.Anderson, H.G.Ljunggren, K.J.Malmberg, et al. CD8 T cells express randomly selected KIRs with distinct specificities compared with NK cells. Blood 2012; 120:3455-65; PMID:22968455; http://dx.doi.org/10.1182/blood-2012-03-416867
41. + T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009; 10:29-37; PMID:19043418; http://dx.doi.org/10.1038/ni.1679
42. H.S.Robins, P.V.Campregher, S.K.Srivastava, A.Wacher, C.J.Turtle, O.Kahsai, S.R.Riddell, E.H.Warren, C.S.Carlson. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 2009; 114:4099-107; PMID:19706884; http://dx.doi.org/10.1182/blood-2009-04-217604
43. R.Flynn, T.Hutchinson, K.M.Murphy, C.F.Ware, M.Croft, S.Salek-Ardakani. CD8 T cell memory to a viral pathogen requires trans cosignaling between HVEM and BTLA. PLoS One 2013; 8:e77991; PMID:24205056; http://dx.doi.org/10.1371/journal.pone.0077991
44. A.C.Vendel, J.Calemine-Fenaux, A.Izrael-Tomasevic, V.Chauhan, D.Arnott, D.L.Eaton. B and T lymphocyte attenuator regulates B cell receptor signaling by targeting Syk and BLNK. J Immunol 2009; 182:1509-17; PMID:19155498; http://dx.doi.org/10.4049/jimmunol.182.3.1509
45. P.Soroosh, T.A.Doherty, T.So, A.K.Mehta, N.Khorram, P.S.Norris, S.Scheu, K.Pfeffer, C.Ware, M.Croft. Herpesvirus entry mediator 731 (TNFRSF14) regulates the persistence of T helper memory cell populations. J Exp Med 2011; 208:797-809; PMID:21402741; http://dx.doi.org/10.1084/jem.20101562
46. T.C.Cheung, M.W.Steinberg, L.M.Oborne, M.G.Macauley, S.Fukuyama, H.Sanjo, C.D'Souza, P.S.Norris, K.Pfeffer, K.M.Murphy, et al. Unconventional ligand activation of herpesvirus entry mediator signals cell survival. Proc Natl Acad Sci 2009; 106:6244-9; PMID:19332782; http://dx.doi.org/10.1073/pnas.0902115106
47. H.Meisner, B.R.Conway, D.Hartley, M.P.Czech. Interactions of Cbl with Grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol Cell Biol 1995; 15:3571-8; PMID:7791764