The co-receptor BTLA negatively regulates human Vg9Vd2 T-cell proliferation: A potential way of immune escape for lymphoma cells

Blood

Volumn 122, Issue 6, 2013, Pages 922-931

  Gertner Dardenne, Julie ^a   Fauriat, Cyril ^a   Orlanducci, Florence ^b   Thibult, Marie Laure ^a   Pastor, Sonia ^a   Fitzgibbon, Jude ^c   Bouabdallah, Reda ^d   Xerri, Luc ^a,b,d   Olive, Daniel ^a,b,d  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT PAOLI CALMETTES   (France)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

B AND T LYMPHOCYTE ATTENUATOR; CD27 ANTIGEN; HERPESVIRUS ENTRY MEDIATOR; MONOCLONAL ANTIBODY; RECEPTOR; UNCLASSIFIED DRUG; BTLA PROTEIN, HUMAN; IMMUNOGLOBULIN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ATTENUATION; CELL POPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; LYMPH NODE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; SURFACE PROPERTY; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; CELL CYCLE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GENETICS; HODGKIN DISEASE; IMMUNOLOGY; METABOLISM; NONHODGKIN LYMPHOMA; PHYSIOLOGY; TUMOR ESCAPE;

ANTIBODIES, MONOCLONAL; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HODGKIN DISEASE; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOMA, NON-HODGKIN; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, IMMUNOLOGIC; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; S PHASE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TUMOR ESCAPE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84886895500     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-11-464685     Document Type: Article

References (51)

1. Constant P, Davodeau F, Peyrat MA, et al. Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science. 1994; 264(5156):267-270.
2. Bukowski JF, Morita CT, Tanaka Y, Bloom BR, Brenner MB, Band H. V gamma 2V delta 2 TCRdependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J Immunol. 1995;154(3):998-1006.
3. Halary F, Peyrat MA, Champagne E, et al. Control of self-reactive cytotoxic T lymphocytes expressing gamma delta T cell receptors by natural killer inhibitory receptors. Eur J Immunol. 1997;27(11):2812-2821.
4. Sireci G, Espinosa E, Di Sano C, Dieli F, Fourni é JJ, Salerno A. Differential activation of human gammadelta cells by nonpeptide phosphoantigens. Eur J Immunol. 2001;31(5):1628-1635.
5. Gober HJ, Kistowska M, Angman L, Jenö P, Mori L, De Libero G. Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med. 2003;197(2):163-168.
6. Morita CT, Beckman EM, Bukowski JF, et al. Direct presentation of nonpeptide prenyl pyrophosphate antigens to human gamma delta T cells. Immunity. 1995;3(4):495-507.
7. Bank I, Book M, Huszar M, Baram Y, Schnirer I, Brenner H. V delta 21 gamma delta T lymphocytes are cytotoxic to the MCF 7 breast carcinoma cell line and can be detected among the T cells that infiltrate breast tumors. Clin Immunol Immunopathol. 1993;67(1):17-24.
8. Schilbach KE, Geiselhart A, Wessels JT, Niethammer D, Handgretinger R. Human gammadelta T lymphocytes exert natural and IL-2-induced cytotoxicity to neuroblastoma cells. J Immunother. 2000;23(5):536-548.
9. Viey E, Fromont G, Escudier B, et al. Phosphostim-activated gamma delta T cells kill autologous metastatic renal cell carcinoma. J Immunol. 2005;174(3):1338-1347.
10. Corvaisier M, Moreau-Aubry A, Diez E, et al. V gamma 9V delta 2 T cell response to colon carcinoma cells. J Immunol. 2005;175(8):5481-5488.
11. Liu Z, Guo BL, Gehrs BC, Nan L, Lopez RD. Ex vivo expanded human Vgamma9Vdelta21 gammadelta-T cells mediate innate antitumor activity against human prostate cancer cells in vitro. J Urol. 2005;173(5):1552-1556.
12. Wilhelm M, Kunzmann V, Eckstein S, et al. Gammadelta T cells for immune therapy of patients with lymphoid malignancies. Blood. 2003; 102(1):200-206.
13. Gertner-Dardenne J, Bonnafous C, Bezombes C, et al. Bromohydrin pyrophosphate enhances antibody-dependent cell-mediated cytotoxicity induced by therapeutic antibodies. Blood. 2009; 113(20):4875-4884.
14. D'Asaro M, La Mendola C, Di Liberto D, et al. V gamma 9V delta 2 T lymphocytes efficiently recognize and kill zoledronate-sensitized, imatinib-sensitive, and imatinib-resistant chronic myelogenous leukemia cells. J Immunol. 2010; 184(6):3260-3268.
15. Gertner J, Wiedemann A, Poupot M, Fournié JJ. Human gammadelta T lymphocytes strip and kill tumor cells simultaneously. Immunol Lett. 2007; 110(1):42-53.
16. French JD, Roark CL, Born WK, O'brien RL. gammadelta T cell homeostasis is established in competition with alphabeta T cells and NK cells. Proc Natl Acad Sci USA. 2005;102(41): 14741-14746.
17. Iwasaki M, Tanaka Y, Kobayashi H, et al. Expression and function of PD-1 in human gd T cells that recognize phosphoantigens. Eur J Immunol. 2010.
18. Watanabe N, Gavrieli M, Sedy JR, et al. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol. 2003;4(7): 670-679.
19. Sedy JR, Gavrieli M, Potter KG, et al. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol. 2005;6(1):90-98.
20. Oya Y, Watanabe N, Owada T, et al. Development of autoimmune hepatitis-like disease and production of autoantibodies to nuclear antigens in mice lacking B and T lymphocyte attenuator. Arthritis Rheum. 2008; 58(8):2498-2510.
21. Han P, Goularte OD, Rufner K,Wilkinson B, Kaye J. An inhibitory Ig superfamily protein expressed by lymphocytes and APCs is also an early marker of thymocyte positive selection. J Immunol. 2004; 172(10):5931-5939.
22. Krieg C, Boyman O, Fu YX, Kaye JB. B and T lymphocyte attenuator regulates CD81 T cellintrinsic homeostasis and memory cell generation. Nat Immunol. 2007;8(2):162-171.
23. Harrop JA, McDonnell PC, Brigham-Burke M, et al. Herpesvirus entry mediator ligand (HVEML), a novel ligand for HVEM/TR2, stimulates proliferation of T cells and inhibits HT29 cell growth. J Biol Chem. 1998;273(42):27548-27556.
24. Krieg C, Han P, Stone R, Goularte OD, Kaye J. Functional analysis of B and T lymphocyte attenuator engagement on CD41 and CD81 T cells. J Immunol. 2005;175(10):6420-6427.
25. Gavrieli M, Sedy J, Nelson CA, Murphy KM. BTLA and HVEM cross talk regulates inhibition and costimulation. Adv Immunol. 2006;92:157-185.
26. Derré L, Rivals JP, Jandus C, et al. BTLA mediates inhibition of human tumor-specific CD81 T cells that can be partially reversed by vaccination. J Clin Invest. 2010;120(1):157-167.
27. Paulos CM, June CH. Putting the brakes on BTLA in T cell-mediated cancer immunotherapy. J Clin Invest. 2010;120(1):76-80.
28. Murphy KM, Nelson CA, Sedý JR. Balancing costimulation and inhibition with BTLA and HVEM. Nat Rev Immunol. 2006;6(9):671-681.
29. Deppong C, Juehne TI, Hurchla M, et al. Cutting edge: B and T lymphocyte attenuator and programmed death receptor-1 inhibitory receptors are required for termination of acute allergic airway inflammation. J Immunol. 2006;176(7): 3909-3913.
30. Steinberg MW, Turovskaya O, Shaikh RB, et al. A crucial role for HVEM and BTLA in preventing intestinal inflammation. J Exp Med. 2008;205(6): 1463-1476.
31. Otsuki N, Kamimura Y, Hashiguchi M, Azuma M. Expression and function of the B and T lymphocyte attenuator (BTLA/CD272) on human T cells. Biochem Biophys Res Commun. 2006;344(4):1121-1127.
32. Serriari NE, Gondois-Rey F, Guillaume Y, et al. B and T lymphocyte attenuator is highly expressed on CMV-specific T cells during infection and regulates their function. J Immunol. 2010;185(6): 3140-3148.
33. M'Hidi H, Thibult ML, Chetaille B, et al. High expression of the inhibitory receptor BTLA in T-follicular helper cells and in B-cell small lymphocytic lymphoma/chronic lymphocytic leukemia. Am J Clin Pathol. 2009;132(4):589-596.
34. Pasero C, Barbarat B, Just-Landi S, et al. A role for HVEM, but not lymphotoxin-beta receptor, in LIGHT-induced tumor cell death and chemokine production. Eur J Immunol. 2009;39(9): 2502-2514.
35. Cheung KJ, Johnson NA, Affleck JG, et al. Acquired TNFRSF14 mutations in follicular lymphoma are associated with worse prognosis. Cancer Res. 2010;70(22):9166-9174.
36. Launay E, Pangault C, Bertrand P, et al. High rate of TNFRSF14 gene alterations related to 1p36 region in de novo follicular lymphoma and impact on prognosis. Leukemia. 2012;26(3):559-562.
37. Xerri L, Chetaille B, Serriari N, et al. Programmed death 1 is a marker of angioimmunoblastic T-cell lymphoma and B-cell small lymphocytic lymphoma/chronic lymphocytic leukemia. Hum Pathol. 2008;39(7):1050-1058.
38. Dieli F, Poccia F, Lipp M, et al. Differentiation of effector/memory Vdelta2 T cells and migratory routes in lymph nodes or inflammatory sites. J Exp Med. 2003;198(3):391-397.
39. Agata Y, Kawasaki A, Nishimura H, et al. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol. 1996;8(5):765-772.
40. Bennett F, Luxenberg D, Ling V, et al. Program death-1 engagement upon TCR activation has distinct effects on costimulation and cytokinedriven proliferation: attenuation of ICOS, IL-4, and IL-21, but not CD28, IL-7, and IL-15 responses. J Immunol. 2003;170(2): 711-718.
41. Carter L, Fouser LA, Jussif J, et al. PD-1:PD-L inhibitory pathway affects both CD4(1) and CD8 (1) T cells and is overcome by IL-2. Eur J Immunol. 2002;32(3):634-643.
42. Compaan DM, Gonzalez LC, Tom I, Loyet KM, Eaton D, Hymowitz SG. Attenuating lymphocyte activity: the crystal structure of the BTLA-HVEM complex. J Biol Chem. 2005;280(47): 39553-39561.
43. Brunner MC, Chambers CA, Chan FK, Hanke J, Winoto A, Allison JP. CTLA-4-Mediated inhibition of early events of T cell proliferation. J Immunol. 1999;162(10):5813-5820.
44. Greenwald RJ, Oosterwegel MA, van der Woude D, et al. CTLA-4 regulates cell cycle progression during a primary immune response. Eur J Immunol. 2002;32(2):366-373.
45. Ying H, Yang L, Qiao G, et al. Cutting edge: CTLA-4 - B7 interaction suppresses Th17 cell differentiation. J Immunol. 2010;185(3): 1375-1378.
46. Cheung TC, Steinberg MW, Oborne LM, et al. Unconventional ligand activation of herpesvirus entry mediator signals cell survival. Proc Natl Acad Sci USA. 2009;106(15):6244-6249.
47. Cheung TC, Oborne LM, Steinberg MW, et al. T cell intrinsic heterodimeric complexes between HVEM and BTLA determine receptivity to the surrounding microenvironment. J Immunol. 2009; 183(11):7286-7296.
48. Walunas TL, Sperling AI, Khattri R, Thompson CB, Bluestone JA. CD28 expression is not essential for positive and negative selection of thymocytes or peripheral T cell tolerance. J Immunol. 1996;156(3):1006-1013.
49. Krummel MF, Allison JP. CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J Exp Med. 1996;183(6):2533-2540.
50. Hurchla MA, Sedy JR, Murphy KM. Unexpected role of B and T lymphocyte attenuator in sustaining cell survival during chronic allostimulation. J Immunol. 2007;178(10): 6073-6082.
51. Deppong C, Degnan JM, Murphy TL, Murphy KM, Green JM. B and T lymphocyte attenuator regulates T cell survival in the lung. J Immunol. 2008;181(5):2973-2979.