Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset

Blood

Volumn 120, Issue 11, 2012, Pages 2269-2279

  Harly, Christelle ^a,b,c   Guillaume, Yves ^d   Nedellec, Steven ^a,b,c   Peigné, Cassie Marie ^a,b,c   Mönkkönen, Hannu ^e   Mönkkönen, Jukka ^e   Li, Jianqiang ^f   Kuball, Jürgen ^g   Adams, Erin J ^h   Netzer, Sonia ⁱ   Déchanet Merville, Julie ⁱ   Léger, Alexandra ^a,b,c   Herrmann, Thomas ^f   Breathnach, Richard ^a,b,c   Olive, Daniel ^d   Bonneville, Marc ^a,b,c   Scotet, Emmanuel ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c CNRS   (France)

^d INSTITUT PAOLI CALMETTES   (France)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

^f UNIVERSITY OF WÜRZBURG   (Germany)

^g UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^h UNIVERSITY OF CHICAGO   (United States)

ⁱ CNRS Bordeaux Segalen University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BUTYROPHILIN 3; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; PAMIDRONIC ACID; T LYMPHOCYTE ANTIGEN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL STRESS; CELLULAR STRESS SIGNAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; T LYMPHOCYTE ACTIVATION; TARGET CELL; UPREGULATION;

EID: 84866308872     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-05-430470     Document Type: Article

References (48)

1. Hayday AC. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity. 2009;31(2):184-196.
2. Bonneville M, O'Brien RL, Born WK. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat Rev Immunol. 2010;10(7):467-478.
3. Chien YH, Konigshofer Y. Antigen recognition by gammadelta T cells. Immunol Rev. 2007;215:46-58.
4. Fournie JJ, Bonneville M. Stimulation of gamma delta T cells by phosphoantigens. Res Immunol. 1996;147(5):338-347. (Pubitemid 26258847)
5. Bonneville M, Scotet E. Human Vgamma9Vdelta2 T cells: promising new leads for immunotherapy of infections and tumors. Curr Opin Immunol. 2006; 18(5):539-546. (Pubitemid 44311448)
6. Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vgamma2Vdelta2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev. 2007;215:59-76. (Pubitemid 46212230)
7. Tanaka Y, Morita CT, Nieves E, Brenner MB, Bloom BR. Natural and synthetic non-peptide antigens recognized by human gamma delta T cells. Nature. 1995;375(6527):155-158.
8. Hintz M, Reichenberg A, Altincicek B, et al. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human gammadelta T cells in Escherichia coli. FEBS Lett. 2001;509(2):317-322. (Pubitemid 34015963)
9. Kunzmann V, Bauer E, Wilhelm M. Gamma/delta T-cell stimulation by pamidronate. N Engl J Med. 1999;340(9):737-738.
10. Gober HJ, Kistowska M, Angman L, Jeno 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. (Pubitemid 36152311)
11. Lang F, Peyrat MA, Constant P, et al. Early activation of human V gamma 9V delta 2 T cell broad cytotoxicity and TNF production by nonpeptidic mycobacterial ligands. J Immunol. 1995;154(11): 5986-5994.
12. Bukowski JF, Morita CT, Band H, Brenner MB. Crucial role of TCR gamma chain junctional region in prenyl pyrophosphate antigen recognition by gamma delta T cells. J Immunol. 1998;161(1): 286-293. (Pubitemid 28285534)
13. Allison TJ, Winter CC, Fournie JJ, Bonneville M, Garboczi DN. Structure of a human gammadelta T-cell antigen receptor. Nature. 2001;411(6839): 820-824. (Pubitemid 32588108)
14. 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.
15. Lenschow DJ, Walunas TL, Bluestone JA. CD28/B7 system of T cell costimulation. Annu Rev Immunol. 1996;14233-258.
16. Lewis JM, Girardi M, Roberts SJ, Barbee SD, Hayday AC, Tigelaar RE. Selection of the cutaneous intraepithelial gammadelta+ T cell repertoire by a thymic stromal determinant. Nat Immunol. 2006;7(8):843-850. (Pubitemid 44084091)
17. Boyden LM, Lewis JM, Barbee SD, et al. Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal gammadelta T cells. Nat Genet. 2008; 40(5):656-662. (Pubitemid 351601202)
18. Barbee SD, Woodward MJ, Turchinovich G, et al. Skint-1 is a highly specific, unique selecting component for epidermal T cells. Proc Natl Acad Sci U S A. 2011;108(8):3330-3335.
19. Turchinovich G, Hayday AC. Skint-1 identifies a common molecular mechanism for the development of interferon-gamma-secreting versus interleukin-17-secreting gammadelta T cells. Immunity. 2011;35(1):59-68.
20. Henry J, Miller MM, Pontarotti P. Structure and evolution of the extended B7 family. Immunol Today. 1999;20(6):285-288. (Pubitemid 29258166)
21. Rhodes DA, Stammers M, Malcherek G, Beck S, Trowsdale J. The cluster of BTN genes in the extended major histocompatibility complex. Genomics. 2001;71(3):351-362. (Pubitemid 32174830)
22. Smith IA, Knezevic BR, Ammann JU, et al. BTN1A1, the mammary gland butyrophilin, and BTN2A2 are both inhibitors of T-cell activation. J Immunol. 2010;184(7):3514-3525.
23. Yamashiro H, Yoshizaki S, Tadaki T, Egawa K, Seo N. Stimulation of human butyrophilin 3 molecules results in negative regulation of cellular immunity. J Leukoc Biol. 2010;88(4):757-767.
24. Cubillos-Ruiz JR, Martinez D, Scarlett UK, et al. CD277 is a negative co-stimulatory molecule universally expressed by ovarian cancer microenvironmental cells. Oncotarget. 2010;1(5):329-338.
25. Messal N, Mamessier E, Sylvain A, et al. Differential role for CD277 as a co-regulator of the immune signal in T and NK cells. Eur J Immunol. 2011;41(12):3443-3454.
26. Compte E, Pontarotti P, Collette Y, Lopez M, Olive D. Frontline: Characterization of BT3 molecules belonging to the B7 family expressed on immune cells. Eur J Immunol. 2004;34(8):2089-2099. (Pubitemid 39256090)
27. Marcu-Malina V, Heijhuurs S, van Buuren M, et al. Redirecting alphabeta T cells against cancer cells by transfer of a broadly tumor-reactive gammadelta T-cell receptor. Blood. 2011;118(1): 50-59.
28. Harly C, Peyrat MA, Netzer S, Dechanet-Merville J, Bonneville M, Scotet E. Upregulation of cytolytic functions of human Vdelta2-gamma T lymphocytes through engagement of ILT2 expressed by tumor target cells. Blood. 2011;117(10):2864-2873.
29. Luhder F, Huang Y, Dennehy KM, et al. Topological requirements and signaling properties of T cell-activating, anti-CD28 antibody superagonists. J Exp Med. 2003;197(8):955-966. (Pubitemid 36523193)
30. Kreiss M, Asmuss A, Krejci K, et al. Contrasting contributions of complementarity-determining region 2 and hypervariable region 4 of rat BV8S2+(Vbeta8.2) TCR to the recognition of myelin basic protein and different types of bacterial superantigens. Int Immunol. 2004;16(5):655-663. (Pubitemid 38628413)
31. Pyz E, Naidenko O, Miyake S, et al. The complementarity determining region 2 of BV8S2 (V beta 8.2) contributes to antigen recognition by rat invariant NKT cell TCR. J Immunol. 2006;176(12): 7447-7455. (Pubitemid 43849047)
32. Espevik T, Nissen-Meyer J. A highly sensitive cell line, WEHI 164 clone 13, for measuring cytotoxic factor/tumor necrosis factor from human monocytes. J Immunol Methods. 1986;95(1):99-105. (Pubitemid 17196641)
33. Nedellec S, Sabourin C, Bonneville M, Scotet E. NKG2D costimulates human Vgamma9Vdelta2 T cell antitumor cytotoxicity through protein kinase Ctheta-dependent modulation of early TCR-induced calcium and transduction signals. J Immunol. 2010;185(1):55-63.
34. Simone R, Barbarat B, Rabellino A, et al. Ligation of the BT3 molecules, members of the B7 family, enhance the proinflammatory responses of human monocytes and monocyte-derived dendritic cells. Mol Immunol. 2010;48(1):109-118.
35. Davodeau F, Peyrat MA, Hallet MM, Houde I, Vie H, Bonneville M. Peripheral selection of antigen receptor junctional features in a major human gamma delta subset. Eur J Immunol. 1993;23(4): 804-808. (Pubitemid 23101061)
36. Yamashita S, Tanaka Y, Harazaki M, Mikami B, Minato N. Recognition mechanism of non-peptide antigens by human gammadelta T cells. Int Immunol. 2003;15(11):1301-1307. (Pubitemid 37369323)
37. Monkkonen H, Auriola S, Lehenkari P, et al. A new endogenous ATP analog (ApppI) inhibits the mitochondrial adenine nucleotide translocase (ANT) and is responsible for the apoptosis induced by nitrogen-containing bisphosphonates. Br J Pharmacol. 2006;147(4):437-445. (Pubitemid 43292286)
38. Devilder MC, Maillet S, Bouyge-Moreau I, Donnadieu E, Bonneville M, Scotet E. Potentiation of antigen-stimulated Vgamma9Vdelta2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. J Immunol. 2006;176(3):1386-1393. (Pubitemid 43134280)
39. Wang H, Fang Z, Morita CT. Vgamma2Vdelta2 T cell receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J Immunol. 2010;184(11):6209- 6222.
40. Jeong J, Rao AU, Xu J, et al. The PRY/SPRY/B30.2 domain of butyrophilin 1A1 (BTN1A1) binds to xanthine oxidoreductase: implications for the function of BTN1A1 in the mammary gland and other tissues. J Biol Chem. 2009;284(33): 22444-22456.
41. James LC, Keeble AH, Khan Z, Rhodes DA, Trowsdale J. Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. Proc Natl Acad Sci U S A. 2007;104(15):6200-6205. (Pubitemid 47186072)
42. Wei H, Huang D, Lai X, et al. Definition of APC presentation of phosphoantigen (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate to Vgamma2Vdelta 2 TCR. J Immunol. 2008;181(7):4798-4806.
43. Sarikonda G, Wang H, Puan KJ, et al. Photoaffinity antigens for human gammadelta T cells. J Immunol. 2008;181(11):7738-7750.
44. Scotet E, Martinez LO, Grant E, et al. Tumor recognition following Vgamma9Vdelta2 T cell receptor interactions with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity. 2005; 22(1):71-80. (Pubitemid 40143452)
45. Mookerjee-Basu J, Vantourout P, Martinez LO, et al. F1-adenosine triphosphatase displays properties characteristic of an antigen presentation molecule for Vgamma9Vdelta2 T cells. J Immunol. 2010;184(12):6920-6928.
46. Chiplunkar S, Dhar S, Wesch D, Kabelitz D. Gammadelta T cells in cancer immunotherapy: current status and future prospects. Immunotherapy. 2009;1(4):663-678.
47. Davey MS, Lin CY, Roberts GW, et al. Human neutrophil clearance of bacterial pathogens triggers anti-microbial gammadelta T-cell responses in early infection. PLoS Pathog. 2011;7(5): e1002040.
48. Bourgarit A, Carcelain G, Samri A, et al. Tuberculosis-associated immune restoration syndrome in HIV-1-infected patients involves tuberculin-specific CD4 Th1 cells and KIR-negative gammadelta T cells. J Immunol. 2009; 183(6):3915-3923.