The molecular basis for modulation of human Vγ9Vδ2 T cell responses by CD277/butyrophilin-3 (BTN3A)-specific antibodies

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 32780-32790

  Palakodeti, Aparna ^a   Sandstrom, Andrew ^a   Sundaresan, Lakshmi ^a   Harly, Christelle ^b   Nedellec, Steven ^b   Olive, Daniel ^c   Scotet, Emmanuel ^b   Bonneville, Marc ^b   Adams, Erin J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITÉ DE NANTES   (France)

^c INSTITUT PAOLI CALMETTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ORIENTATION; EXTRACELLULAR; HIGH AFFINITY; HOMODIMERS; ISOFORMS; MOLECULAR BASIS; MOLECULAR MECHANISM; STRUCTURAL HOMOLOGY; T CELL RECEPTOR; T CELLS; T-CELL RESPONSE; TUMORIGENESIS; VALENCIES;

CELL CULTURE; CELL MEMBRANES; CELL PROLIFERATION; MOLECULES;

ANTIBODIES;

B7 ANTIGEN; BUTYROPHILIN 3A ANTIBODY; BUTYROPHILIN 3A1; BUTYROPHILIN 3A2; BUTYROPHILIN 3A3; EPITOPE; IMMUNOGLOBULIN; PROTEIN ANTIBODY; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; LIGHT SCATTERING; LYMPHOCYTE ACTIVATION; MOLECULAR CLONING; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MODIFICATION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE; T LYMPHOCYTE;

ANTIBODIES; ANTIGENS, CD; HUMANS; LYMPHOCYTE ACTIVATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; T-LYMPHOCYTES;

EID: 84866525950     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384354     Document Type: Article

References (39)

1. Bonneville, M., O'Brien, R. L., and Born, W. K. (2010) γδ T cell effector functions. A blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10, 467-478
2. Hayday, A. C. (2009) γδ T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196
3. Bonneville, M., and Scotet, E. (2006) Human Vγ9Vδ2 T cells. Promising new leads for immunotherapy of infections and tumors. Curr. Opin. Immunol 18, 539-546 (Pubitemid 44311448)
4. Morita, C. T., Jin, C., Sarikonda, G., and Wang, H. (2007) Nonpeptide antigens, presentation mechanisms, and immunological memory of human Vγ2Vδ2 T cells. Discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol. Rev. 215, 59-76 (Pubitemid 46212230)
5. Kabelitz, D. (2010) Human γδ T lymphocytes for immunotherapeutic strategies against cancer. F1000 Med. Rep. 2, 45
6. Bukowski, J. F., Morita, C. T., Tanaka, Y., Bloom, B. R., Brenner, M. B., and Band, H. (1995) Vγ2Vδ2 TCR-dependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J. Immunol. 154, 998-1006
7. Wang, H., Fang, Z., and Morita, C. T. (2010) Vγ2Vδ2 T cell receptor recognition of prenyl pyrophosphates is dependent on all CDRs. J. Immunol. 184, 6209-6222
8. Allison, T. J., Winter, C. C., Fournié, J. J., Bonneville, M., and Garboczi, D. N. (2001) Structure of a human γδ T-cell antigen receptor. Nature 411, 820-824 (Pubitemid 32588108)
9. Morita, C. T., Beckman, E. M., Bukowski, J. F., Tanaka, Y., Band, H., Bloom, B. R., Golan, D. E., and Brenner, M. B. (1995) Direct presentation of nonpeptide prenyl pyrophosphate antigens to human γδ T cells. Immunity 3, 495-507
10. Wei, H., Huang, D., Lai, X., Chen, M., Zhong, W., Wang, R., and Chen, Z. W. (2008) Definition of APC presentation of phosphoantigen (E)-4-hydroxy-3- methyl-but-2-enyl pyrophosphate to Vγ2Vδ2 TCR. J. Immunol. 181, 4798-4806
11. Lang, F., Peyrat, M. A., Constant, P., Davodeau, F., David-Ameline, J., Poquet, Y., Vié, H., Fournié, J. J., and Bonneville, M. (1995) Early activation of human Vγ9Vδ2 T cell broad cytotoxicity and TNF production by non-peptidic mycobacterial ligands. J. Immunol. 154, 5986-5994
12. Wang, H., Lee, H. K., Bukowski, J. F., Li, H., Mariuzza, R. A., Chen, Z. W., Nam, K. H., and Morita, C. T. (2003) Conservation of nonpeptide antigen recognition by rhesus monkey Vγ2Vδ2 T cells. J. Immunol. 170, 3696-3706 (Pubitemid 36359240)
13. Harly, C., Guillaume, Y., Nedellec, S., Mönkkönen, H., Mönkkönen, J., Kuball, J., Adams, E. J., Netzer, S., Déchanet-Merville, J., Léger, A., Breathnach, R., Olive, D., Bonneville, M., and Scotet, E. (2012) Key implication of CD277/Butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T cell subset. Blood, in press
14. Greenwald, R. J., Freeman, G. J., and Sharpe, A. H. (2005) The B7 family revisited. Annu. Rev. Immunol. 23, 515-548 (Pubitemid 40563179)
15. Compte, E., Pontarotti, P., Collette, Y., Lopez, M., and Olive, D. (2004) Frontline. Characterization of BT3 molecules belonging to the B7 family expressed on immune cells. Eur. J. Immunol. 34, 2089-2099 (Pubitemid 39256090)
16. Arnett, H. A., Escobar, S. S., and Viney, J. L. (2009) Regulation of costimulation in the era of butyrophilins. Cytokine 46, 370-375
17. Yamashiro, H., Yoshizaki, S., Tadaki, T., Egawa, K., and Seo, N. (2010) Stimulation of human butyrophilin 3 molecules results in negative regulation of cellular immunity. J. Leukocyte Biol. 88, 757-767
18. Yamazaki, T., Goya, I., Graf, D., Craig, S., Martin-Orozco, N., and Dong, C. (2010) A butyrophilin family member critically inhibits T cell activation. J. Immunol. 185, 5907-5914
19. Smith, I. A., Knezevic, B. R., Ammann, J. U., Rhodes, D. A., Aw, D., Palmer, D. B., Mather, I. H., and Trowsdale, J. (2010) BTN1A1, the mammary gland butyrophilin, and BTN2A2 are both inhibitors of T cell activation. J. Immunol. 184, 3514-3525
20. Ruddy, D. A., Kronmal, G. S., Lee, V. K., Mintier, G. A., Quintana, L., Domingo, R., Jr., Meyer, N. C., Irrinki, A., McClelland, E. E., Fullan, A., Mapa, F. A., Moore, T., Thomas, W., Loeb, D. B., Harmon, C., Tsuchihashi, Z., Wolff, R. K., Schatzman, R. C., and Feder, J. N. (1997) A 1.1-Mb transcript map of the hereditary hemochromatosis locus. Genome Res. 7, 441-456 (Pubitemid 27232008)
21. Tazi-Ahnini, R., Henry, J., Offer, C., Bouissou-Bouchouata, C., Mather, I. H., and Pontarotti, P. (1997) Cloning, localization, and structure of new members of the butyrophilin gene family in the juxta-telomeric region of the major histocompatibility complex. Immunogenetics 47, 55-63 (Pubitemid 28062034)
22. Rhodes, D. A., Stammers, M., Malcherek, G., Beck, S., and Trowsdale, J. (2001) The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71, 351-362 (Pubitemid 32174830)
23. Ikemizu, S., Gilbert, R. J., Fennelly, J. A., Collins, A. V., Harlos, K., Jones, E. Y., Stuart, D. I., and Davis, S. J. (2000) Structure and dimerization of a soluble form of B7-1. Immunity 12, 51-60 (Pubitemid 30069214)
24. Zhang, X., Schwartz, J. C., Almo, S. C., and Nathenson, S. G. (2003) Crystal structure of the receptor-binding domain of human B7-2. Insights into organization and signaling. Proc. Natl. Acad. Sci. U.S.A. 100, 2586-2591 (Pubitemid 36297542)
25. Chen, Y., Liu, P., Gao, F., Cheng, H., Qi, J., and Gao, G. F. (2010) A dimeric structure of PD-L1. Functional units or evolutionary relics? Protein Cell 1, 153-160
26. Lin, D. Y., Tanaka, Y., Iwasaki, M., Gittis, A. G., Su, H. P., Mikami, B., Okazaki, T., Honjo, T., Minato, N., and Garboczi, D. N. (2008) The PD-1/PD-L1 complex resembles the antigen-binding Fv domains of antibodies and T cell receptors. Proc. Natl. Acad. Sci. U.S.A. 105, 3011-3016 (Pubitemid 351723659)
27. Clements, C. S., Reid, H. H., Beddoe, T., Tynan, F. E., Perugini, M. A., Johns, T. G., Bernard, C. C., and Rossjohn, J. (2003) The crystal structure of myelin oligodendrocyte glycoprotein, a key autoantigen in multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 100, 11059-11064 (Pubitemid 37140152)
28. Clegg, R. M. (1992) Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211, 353-388
29. Luo, B. H., Carman, C. V., and Springer, T. A. (2007) Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647 (Pubitemid 46697919)
30. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
31. Holden, H. M., Ito, M., Hartshorne, D. J., and Rayment, I. (1992) X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase, at 2.8 A resolution. J. Mol. Biol. 227, 840-851
32. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
33. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
34. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
35. DeBartolo, J., Colubri, A., Jha, A. K., Fitzgerald, J. E., Freed, K. F., and Sosnick, T. R. (2009) Mimicking the folding pathway to improve homology-free protein structure prediction. Proc. Natl. Acad. Sci. U.S.A. 106, 3734-3739
36. Haddadian, E. J., Gong, H., Jha, A. K., Yang, X., Debartolo, J., Hinshaw, J. R., Rice, P. A., Sosnick, T. R., and Freed, K. F. (2011) Automated real-space refinement of protein structures using a realistic backbone move set. Biophys. J. 101, 899-909
37. Sugita, M., Moody, D. B., Jackman, R. M., Grant, E. P., Rosat, J. P., Behar, S. M., Peters, P. J., Porcelli, S. A., and Brenner, M. B. (1998) CD1. A new paradigm for antigen presentation and T cell activation. Clin. Immunol. Immunopathol. 87, 8-14 (Pubitemid 28194157)
38. Wang, Z., Raifu, M., Howard, M., Smith, L., Hansen, D., Goldsby, R., and Ratner, D. (2000) Universal PCR amplification of mouse immunoglobulin gene variable regions. The design of degenerate primers and an assessment of the effect of DNA polymerase 3′ to 5′ exonuclease activity. J. Immunol. Methods 233, 167-177 (Pubitemid 30058245)
39. Maynard, J., Adams, E. J., Krogsgaard, M., Petersson, K., Liu, C. W., and Garcia, K. C. (2005) High level bacterial secretion of single-chain αβ T-cell receptors. J. Immunol. Methods 306, 51-67 (Pubitemid 41739840)