Three-dimensional structure of the complex between a T cell receptor β chain and the superantigen staphylococcal enterotoxin B

Immunity

Volumn 9, Issue 6, 1998, Pages 807-816

  Hongmin, Li ^a   Llera, Andrea ^a   Tsuchiya, Daisuke ^a   Leder, Lukas ^a,b   Ysern, Xavier ^c   Schlievert, Patrick M ^d   Karjalainen, Klaus ^e   Mariuzza, Roy A ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e BASEL INSTITUTE FOR IMMUNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

STAPHYLOCOCCUS ENTEROTOXIN B; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ARTICLE; COMPLEX FORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; T LYMPHOCYTE; TOXIN ANALYSIS;

EID: 0032412391     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80646-9     Document Type: Article

References (68)

1. Alam, S.M., Travers, P.J., Wung, J.L., Nasholds, W., Redpath, S., Jameson, S.C., and Gascoigne, N.R.J. (1996). T-cell receptor affinity and thymocyte positive selection. Nature 381, 616-620.
2. Bacon, D.J., and Anderson, W.F. (1988). A fast algorithm for rendering space-filling molecule pictures. J. Mol. Graph. 6, 219-220.
3. Bentley, G.A., Boulot, G., Karjalainen, K., and Mariuzza, R.A. (1995). Crystal structure of the β chain of a T cell antigen receptor. Science 267, 1984-1987.
4. Bhat, T.N., Bentley, G.A., Boulot, G., Greene, M.I., Tello, D., Dall'Acqua, W., Souchon, H., Schwarz, F.P., Mariuzza, R.A., and Poljak, R.J. (1994). Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc. Natl. Acad. Sci. USA 97, 1089-1093.
5. Blackman, M.A., and Woodland, D.L. (1996). Role of the T cell receptor α-chain in superantigen recognition. Immunol. Res. 15, 98-113.
6. Bohach, G.A., Fast, D.J., Nelson, R.D., and Schlievert, P.M. (1990). Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit. Rev. Microbiol. 17, 251-272.
7. Borrero, H., Donson, D., Cervera, C., Rexer, C., and Macphail, S. (1995). T cell receptor Vα4 is expressed by a subpopulation of Vβ6 T cells that respond to the bacterial superantigen staphylococcal enterotoxin B. J. Immunol. 154, 4247-4260.
8. Brocke, S., Gaur, A., Piercy, C., Gautam, A., Gijbels, K., Fathman, C.G., and Steinman, L. (1993). Induction of relapsing paralysis in experimental autoimmune encephalomyelitis by bacterial superantigen. Nature 365, 642-644.
9. Brunger, A.T. (1992). X-PLOR Version 3.1. A System for X-ray Crystallography and NMR. Yale University Press, New Haven.
10. Ciurli, C., Posnett, D.N., Sekaly, R.-P., and Denis, F. (1998). Highly biased CDR3 usage in restricted sets of β chain variable regions during viral superantigen 9 response. J. Exp. Med. 187, 253-258.
11. Cole, B.C., and Griffiths, M.M. (1993). Triggering and exacerbation of autoimmune arthritis by the Mycoplasma arthritidis superantigen MAM. Arthritis Rheum. 36, 994-1002.
12. Collaborative Computational Project No. 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763.
13. Conrad, B., Weidmann, E., Trucco, G., Rudert, W.A., Behboo, R., Ricordi, C., Rodriquez-Rilo, H., Finegold, D., and Trucco, M. (1994). Evidence for superantigen involvement in insulin-dependent diabetes mellitus aetiology. Nature 371, 351-355.
14. Corr, M., Slanetz, A.E., Boyd, L.F., Jelonek, M.T., Khilko, S., Al-Ramadi, B.K., Kim, Y.S., Maher, S.E., Bothwell, A.L., and Margulies, D.H. (1994). T cell receptor-MHC class I peptide interactions: affinity, kinetics, and specificity. Science 265, 946-948.
15. Dall'Acqua, W., Goldman, E.R., Lin, W., Teng, C., Tsuchiya, D., Li, H., Ysern, X., Braden, B.C., Li, Y., Smith-Gill, S.J., et al. (1998). A mutational analysis of binding interactions in an antigen-antibody protein-protein complex. Biochemistry 37, 7981-7991.
16. Daly, K., Nguyen, P., Hankley, D., Zhang, W.J., Woodland, D.L., and Blackman, M.A. (1995). Contribution of the TCR α-chain to the differential recognition of bacterial and retroviral superantigens. J. Immunol. 755, 27-34.
17. Davies, D.R., and Padlan, E.E. (1992). Twisting into shape. Curr. Biol. 2, 254-256.
18. Deckhut, A.M., Chien, Y., Blackman, M.A., and Woodland, D.L. (1994). Evidence for a functional interaction between the β chain of major histocompatibility complex class II and the T cell receptor α chain during recognition of a bacterial superantigen. J. Exp. Med. 180, 1931-1935.
19. Ding, Y.-H., Smith, K.J., Garboczi, D.N., Utz, U., Biddison, W.E., and Wiley, D.C. (1998). Two human T cell receptors bind in a similar diagonal mode to the HLA-A2/Tax peptide complex using different TCR amino acids. Immunity 8, 403-411.
20. Donson, D., Borrero, H., Rutman, M., Pergolizzi, R., Malhado, N., and Macphail, S. (1997). Gene transfer directly demonstrates a role for TCR Vα elements in superantigen recognition. J. Immunol. 158, 5229-5236.
21. Fields, B.A., Goldbaum, F.A., Ysern, X., Poljak, R.J., and Mariuzza, R.A. (1995). Molecular basis of antigen mimicry by an anti-idiotope. Nature 374, 739-742.
22. Fields, B.A., Malchiodi, E.L., Li, H.-M., Ysern, X., Stauffacher, C.V., Schlievert, P.M., Karjalainen, K., and Mariuzza, R.A. (1996). Crystal structure of the β chain of a T-cell receptor complexed with a superantigen. Nature 384, 188-192.
23. Garboczi, D.N., Ghosh, P., Utz, U., Fan, Q.R., Biddison, W.E., and Wiley, D.C. (1996). Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141.
24. Garcia, K.C., Degano, M., Stanfield, R.L., Brunmark, A., Jackson, M.R., Peterson, P.A., Teyton, L., and Wilson, I.A. (1996). An αβ T cell receptor structure at 2.5 Å and its orientation in the TCR-MHC complex. Science 274, 209-219.
25. Garcia, K.C., Degano, M., Pease, L.R., Huang, M., Peterson, P.A., Teyton, L., and Wilson, I.A. (1998). Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279, 1166-1172.
26. Hodtsev, A.S., Choi, Y., Spanopoulou, E., and Posnett, D.N. (1998). Mycoplasma superantigen is a CDR3-dependent ligand for the T cell antigen receptor. J. Exp. Med. 187, 319-327.
27. Hoffmann, M.L., Jablonski, L.M., Crum, K.K., Hackett, S.P., Chi, Y.-I., Stauffacher, C.V., Stevens, D.L., and Bohach, G.A. (1994). Predictions of T cell receptor and major histocompatibility complex binding sites on staphylococcal enterotoxin C3. Infect. Immun. 62, 3396-3407.
28. Housset, D., Mazza, G., Gregoire, C., Piras, C., Malissen, B., and Fontecilla-Camps, J.C. (1997). The three-dimensional structure of a T-cell antigen receptor VαVβ heterodimer reveals a novel arrangement of the Vβ domain. EMBO J. 16, 4205-4216.
29. Imanishi, K.H., Igarashi, H., and Uchiyama, T. (1990). Activation of murine T cells by streptococcal pyrogenic exotoxin A. J. Immunol. 145, 3170-3176.
30. Ito, Y., Abe, J., Yoshino, K., Takeda, T., and Koshaka, T. (1995). Sequence analysis of the gene for a novel superantigen produced by Yersinia pseudotuberculosis and expression of the recombinant protein. J. Immunol. 154, 5896-5906.
31. Jancarik, J., and Kim, S.-H. (1991). Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallog. 24, 409-411.
32. Jardetzky, T.S., Brown, J.H., Gorga, J.C., Stern, L.J., Urban, R.G., Chi, Y., Stauffacher, C., Strominger, J.L., and Wiley, D.C. (1994). Three-dimensional structure of a human class II histocompatibility molecule complexed with superantigen. Nature 368, 711-718.
33. Khandekar, S.S., Brauer, P.P., Naylor, J.W., Chang, H.-C., Kern, P., Newcomb, J.R., LeClair, K.P., Stump, H.S., Bettencourt, B.M., Kawasaki, E., et al. (1997). Affinity and kinetics of the interactions between an αβ T-cell receptor and its superantigen and class II-MHC/peptide ligands. Mol. Immunol. 34, 493-503.
34. Kotzin, B.L., Leung, D.Y.M., Kappler, J., and Marrack, P. (1993). Superantigens and their potential role in human disease. Adv. Immunol. 54, 99-166.
35. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
36. Labrecque, N., Thibodeau, J., Mourad, W., and Sekaly, R.-P. (1994). T cell receptor-major histocombatibility complex class II interaction is required for the T cell response to bacterial superantigens. J. Exp. Med. 180, 1921-1929.
37. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26, 283-291.
38. Lawrence, M.C., and Colman, P.M. (1993). Shape complementarity at protein-protein interfaces. J. Mol. Biol. 234, 946-950.
39. Leder, L., Llera, A., Lavoie, P.M., Lebedeva, M.I., Li, H., Sekaly, R.-P., Bohach, G.A., Gahr, P.J., Schlievert, P.M., Karjalainen, K., et al. (1998). A mutational analysis of the binding of staphylococcal enterotoxins B and C3 to the T cell receptor β chain and major histocompatibility complex class II. J. Exp. Med. 187, 823-833.
40. Li, P.-L., Teidemann, R.E., Moffat, S.L., and Fraser, J.D. (1997). The superantigen streptococcal pyrogenic exotoxin C (SPE-C) exhibits a novel mode of action. J. Exp. Med. 186, 375-383.
41. Li, H., Lebedeva, M.I., Llera, A.S., Fields, B.A., Brenner, M.A., and Mariuzza, R.A. (1998). Structure of the Vδ domain of a human γδ T-cell antigen receptor. Nature 391, 502-506.
42. Malchiodi, E.L., Eisenstein, E., Fields, B.A., Ohlendorf, D.H., Schlievert, P.M., Karjalainen, K., and Mariuzza, R.A. (1995). Superantigen binding to a T cell receptor β chain of known three-dimensional structure. J. Exp. Med. 182, 1833-1845.
43. k complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 91, 12862-12866.
44. Merritt, E.A., and Bacon, D.J. (1997). Raster3D: photorealistic molecular graphics. Methods Enzymol. 277, 505-524.
45. Miyoshi-Akiyama, T., Abe, A., Kato, H., Kawahara, K., Narimatsu, H., and Uchiyama, T. (1995). DNA sequencing of the gene encoding a bacterial superantigen, Yersinia pseudotuberculosis-derived mitogen (YPM), and characterization of the gene product, cloned YPM. J. Immunol. 154, 5228-5234.
46. Navaza, J. (1994). AM oRe: an automated package for molecular replacement. Acta Crystallogr. A50, 157-163.
47. Otwinowski, Z., and Minor, W. (1997). Processing X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
48. Padlan, E.A. (1994). Anatomy of the antibody molecule. Mol. Immunol. 31, 169-217.
49. Paliard, X., West, S.G., Lafferty, J.A., Clements, J.R., Kappler, J.W., Marrack, P., and Kotzin, B.L. (1992). Evidence for the effects of a superantigen in rheumatoid arthritis. Science 253, 325-329.
50. Papageorgiou, A., Acharya, K.R., Shapiro, R., Passalacqua, E.F., Brehm, R.D., and Tranter, H.S. (1995). Crystal structure of the superantigen enterotoxin C2 from Stapylococcus aureus reveals a zinc-binding site. Structure 3, 769-779.
51. Papageorgiou, A.C., Brehm, R.D., Leonidas, D.D., Tranter, H.S., and Acharya, K.R. (1996). The refined crystal structure of toxic shock syndrome toxin-1 at 2.07 Å resolution. J. Mol. Biol. 260, 553-569.
52. Proft, T. and Fraser, J. (1998). Superantigens: just like peptides only different. J. Exp. Med. 187, 819-821.
53. Racke, M.K., Quigley, L., Cannella, B., Raine, C.S., McFarlin, D.E., and Scott, D.E. (1994). Superantigen modulation of experimental allergic encephalomyelitis: activation or anergy determines outcome. J. Immunol. 152, 2051-2059.
54. Renno, T., and Acha-Orbea, H. (1996). Superantigens in autoimmune disease: still more shades of gray. Immunol. Rev. 154, 175-191.
55. Roussel, A., and Cambillau, C. (1989). TURBO-FRODO. In Silicon Graphics Geometry Partners Directory, pp. 77-78, Silicon Graphics. Mountain View, CA.
56. Roussel, A., Anderson, B.F., Baker, H.M., Fraser, J.D., and Baker, E.N. (1997). Crystal structure of the streptococcal superantigen SPE-C: dimerization and zinc binding suggest a novel mode of interaction with MHC class II molecules. Nat. Struct. Biol. 4, 635-643.
57. Schad, E.M., Zaitseva, I., Zaitsev, V.N., Dohlsten, M., Kalland, T., Schlievert, P.M., Ohlendorf, D.H., and Svensson, L.A. (1995). Crystal structure of the superantigen staphylococcal enterotoxin type A. EMBO J. 14, 3292-3301.
58. Scherer, M.T., Ignatowicz, L., Winslow, G.M., Kappler, J.W., and Marrack, P. (1993). Superantigens: bacterial and viral proteins that manipulate the immune system. Annu. Rev. Cell. Biol. 9, 101-128.
59. Seth, A., Stern, L.S., Ottenhoff, T.H.M., Engel, I., Owen, M.J., Lamb, J.R., Klausner, R.D., and Wiley, D.C. (1994). Binary and ternary complexes between T-cell receptor, class II MHC and superantigen in vitro. Nature 369, 324-327.
60. Swaminathan, S., Furey, W., Pletcher, J., and Sax, M. (1992). Crystal structure of staphylococcal enterotoxin B, a superantigen. Nature 359, 801-806.
61. Tulip, W.R., Varghese, J.N., Laver, W.G., Webster, R.G., and Coleman, P.M. (1992). Refined crystal structure of the influenza virus N9 neuraminidase-NC41 Fab complex. J. Mol. Biol. 227, 122-148.
62. Tate, M.W., Eikenberry, E.F., Barna, S.L., Wall, M.E., Lowrance, J.L., and Gruner, S.M. (1995). A large-format high-resolution area X-ray detector based on a fiber-optically bonded charged-coupled device (CCD). J. Appl. Crystallog. 28, 196-205.
63. Vath, G.M., Earhart, C.A., Rago, J.V., Kim, M.H., Bohach, G.A., Schlievert, P.M., and Ohlendorf, D.H. (1997). The structure of the superantigen exfoliative toxin A suggests a novel regulation as a serine protease. Biochemistry 36, 1559-1566.
64. Wang, J., Lim, K., Smolyar, A., Teng, M., Liu, J., Tse, A.G.D., Liu, J., Hussey, R.E., Chishti, Y., Thomson, C.T.T., et al. (1998). Atomic structure of an αβ T cell receptor (TCR) heterodimer in complex with an anti-TCR Fab fragment derived from a mitogenic antibody. EMBO J. 17, 10-26.
65. Webb, S.R., and Gascoigne, N.R.J. (1994). T-cell activation by superantigens. Curr. Opin. Immunol. 6, 467-475.
66. Wilson, I.A., and Stanfield, R.L. (1993). Antigen-antibody interactions. Curr. Opin. Struct. Biol. 3, 113-118.
67. Wilson, I.A., and Garcia, K.C. (1997). T-cell receptor structure and TCR complexes. Curr. Opin. Struct. Biol. 7, 839-848.
68. Woodland, D.L., and Blackman, M.A. (1993). How do T cell receptors, MHC molecules and superantigens get together? Immunol. Today 14, 208-212.