Crystal structure of microbial superantigen staphylococcal enterotoxin B at 1.5 Å resolution: Implications for superantigen recognition by MHC class II molecules and T-cell receptors

Journal of Molecular Biology

Volumn 277, Issue 1, 1998, Pages 61-79

  Papageorgiou, Anastassios C ^a   Tranter, Howard S ^b   Acharya, K Ravi ^a  

^a BA2 7AY ^*  (United Kingdom)

^b PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

Major histocompatibility complex; Staphylococcal enterotoxin B; Superantigens; T cell receptor; X ray crystallography

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; STAPHYLOCOCCUS ENTEROTOXIN A; STAPHYLOCOCCUS ENTEROTOXIN B; SUPERANTIGEN; T LYMPHOCYTE RECEPTOR;

ANTIGEN RECOGNITION; ARTICLE; BINDING SITE; CHEMICAL BOND; CRYSTAL STRUCTURE; GEOMETRY; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL;

POSIBACTERIA; STAPHYLOCOCCUS;

EID: 0032549518     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1577     Document Type: Article

References (70)

1. Abrahmsén L., Dohlsten M., Segren S., Bjork P., Jonsson E., Kalland T. Characterization of two distinct sites MHC class II binding sites in the superantigen staphylococcal enterotoxin A. EMBO J. 14:1995;2978-2986
2. Acharya K.R., Passalacqua E.F., Jones E.Y., Harlos K., Stuart D.I., Brehm R.D., Tranter H.S. Structural basis of superantigen action inferred from crystal structure of toxic-shock syndrome toxin-1. Nature. 367:1994;94-97
3. Alouf J.E., Knoll H., Kohler W. The family of mitogenic, shock-inducing and superantigenic toxins from Staphylococci and Streptococci. Alouf J.E., Freer J.H. Sourcebook of Bacterial Protein Toxins. 1991;367 Academic Press Ltd, London
4. Barton G.J. ALSCRIPT a tool to format multiple sequence alignments. Protein Eng. 6:1993;37-40
5. Bergdoll M.S. Enterotoxins. Easmon C.S.F., Adlam C. Staphylococci and Staphylococcal Infections. 1983;559-598 Academic Press Ltd, London
6. Blomster-Hautamaa D.A., Kreiswirth B.N., Kornblum J.S., Norvick R.P., Schlievert P.M. The nucleotide and partial amino acid sequence of toxic shock syndrome toxin-1. J. Biol. Chem. 261:1986;15783-15786
7. Bohach G.A., Fast D.J., Nelson R.D., Schlievert P.M. Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit. Rev. Microbiol. 17:1990;251-272
8. Brehm R.D., Tranter H.S., Hambleton P., Melling J. Large scale purification of staphylococcal enterotoxins A, B and C2 by dye ligand affinity chromatography. Appl. Envirom. Microbiol. 56:1990;1067-1072
9. Brünger A.T. Free R value a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-474
10. Brünger A.T. X-PLOR Version 3. 1. A System for Crystallography and NMR. 1992;Yale University, New Haven, CT
11. Chatterjee S., Khullar M., Shi W.Y. Digalactosylceramide is the receptor for staphylococcal enterotoxin-B in human kidney proximal tubular cells. Glycobiology. 5:1995;327-333
12. The CCP4 suite programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763
13. Engh R.A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400
14. Fields B.A., Malchiodi E.L., Li H., Ysern X., Stauffacher C.V., Schlievert P.M., Karjalainen K., Mariuzza R.A. Crystal structure of a T-cell receptor β-chain complexed with superantigen. Nature. 384:1996;188-192
15. Fraser J.D., Urban R.G., Strominger J.L., Robinson H. Zinc regulates the function of two superantigens. Proc. Natl Acad. Sci. USA. 89:1992;5507-5511
16. Garboczi D.N., Ghosh P., Utz U., Fan Q.R., Biddison W.E., Wiley D.C. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature. 384:1996;134-141
17. Goshorn S.C., Schlievert P.M. Bacteriophage association of streptococcal pyrogenic exotoxin type C. J. Bacteriol. 171:1989;3068-3073
18. Hamad A.R.A., Marrack P., Kappler J.W. Transcytosis of staphylococcal superantigen toxins. J. Expt. Med. 185:1997;1447-1454
19. Hargreaves R.E.G., Brehm R.D., Tranter H., Warrens A.N., Lombardi G., Lechler R. Definition of sites on HLA-DR1 involved in the T cell response to staphylococcal enterotoxins E and C2. Eur. J. Immunol. 25:1995;3437-3444
20. Harris T.O., Grossman D., Kappler J.W., Marrack P., Rich R.R., Betley M.J. Lack of complete correlation between emetic and T-cell stimulatory activities of staphylococcal enterotoxins. Infect. Immun. 61:1993;3175-3183
21. Herman A., Kappler J.W., Marrack P., Pullen A.M. Superantigens-mechanism of T-cell stimulation and role in immune responses. Annu. Rev. Immunol. 9:1991;745-772
22. Hoffmann M.L., Jablonski L.M., Crum K.K., Hackett S.P., Chi Y.-I., Stauffacher C.V., Stevens D.L., Bohach G.A. Predictions of T-cell receptor- and major histocompatibility complex-binding sites on staphylococcal enterotoxin C1. Infect. Immun. 62:1994;3396-3407
23. Hovde C.J., Marr J.C., Hoffmann M.L., Hackett S.P., Chi Y.-I., Crum K.K., Stevens D.L., Stauffacher C.V., Bohach G.A. Investigation of the role of the disulphide bond in the activity and structure of staphylococcal enterotoxin C1. Mol. Microbiol. 13:1994;897-909
24. Hudson K.R., Robinson H., Fraser J.D. Two adjacent residues in staphylococcal enterotoxins A and E determine T-cell receptor Vβ specificity. J. Expt. Med. 177:1993;175-184
25. Hudson K.R., Tiedemann R.E., Urban R.G., Lowe S.C., Strominger J.L., Fraser J.D. Staphylococcal enterotoxin A has two cooperative binding sites on major histocompatibility complex class-II. J. Expt. Med. 189:1995;711-720
26. Jardetzky T.S., Brown J.H., Gorga J.C., Urban R.G., Chi Y.I., Stauffacher C., Strominger J.L., Wiley D.C. Three-dimensional structure of a human class II histocompatibility molecule complexed with superantigen. Nature. 368:1994;711-718
27. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119
28. Kabsch W. Evaluation of single crystal X-ray diffraction from a position-sensitive detector. J. Appl. Crystallog. 21:1988;916-924
29. Kabsch W., Sander C. Dictionary of protein secondary structure pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637
30. Kappler J.W., Herman A., Clements J., Marrack P. Mutations defining functional regions of the superantigen staphylococcal enterotoxin B. J. Expt. Med. 175:1992;387-396
31. Kim J., Urban R.G., Strominger J.L., Wiley D.C. Toxic shock syndrome toxin-1 complexed with a class II major histocompatibility molecule HLA-DR1. Science. 266:1994;1870-1874
32. Kotzin B.L., Leung D.Y.M., Kappler J., Marrack P. Superantigens and their potential role in human disease. Advan. Immunol. 54:1993;99-166
33. Kozono H., Parker D., White J., Marrack P., Kappler J. Multiple binding sites for bacterial superantigens on soluble class II MHC molecules. Immunity. 3:1995;187-196
34. Kraulis P.J. MOLSCRIPT a program to produce both detailed and schematic plots of proteins. J. Appl. Crystallog. 24:1991;946-950
35. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291
36. Marrack P., Kappler J. The staphylococcal enterotoxins and their relatives. Science. 248:1990;705-711
37. 5toxins. Curr. Opin. Struct. Biol. 5:1995;165-171
38. Merritt E.A., Murphy M.E.P. Raster3D version 2.0 a program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873
39. M1pentasaccharide. Protein Sci. 3:1994;166-175
40. Mollick J.A., McMasters R.L., Grossman D., Rich R.R. Localization of a site on bacterial superantigens that determines T cell receptor β chain specificity. J. Expt. Med. 177:1993;283-293
41. Murzin A.G. OB (oligonucleotide/oligosaccharide binding)-fold common structural and functional solution for non-homologous sequences. EMBO J. 12:1993;861-867
42. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP a structural classification of protein database for the investigation of sequences and structure. J. Mol. Biol. 247:1995;536-540
43. Navaza J. AMoRe an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;157-163
44. Nicholls A., Honig B. A rapid finite difference algorithm, utilising successive over relaxation to solve the Poisson-Boltzmann equation. J. Comput. Chem. 12:1991;435-445
45. Otwinowski Z. Sawyer L., Isaacs N., Bailey S. Proceedings of the CCP4 study weekend Data collection and Processing. 1993;56-62 Science and Engineering Research Council, Daresbury Laboratory, Daresbury, England
46. Papageorgiou A.C., Acharya K.R. Superantigens as immunomodulators recent structural insights. Structure. 5:1997;991-996
47. Papageorgiou A.C., Acharya K.R., Shapiro R., Passalacqua E.F., Brehm R.D., Tranter H.S. Crystal structure of the superantigen enterotoxin C2 from Staphylococcus aureus reveals a zinc-binding site. Structure. 3:1995;769-779
48. Papageorgiou A.C., Brehm R.D., Leonidas D.D., Tranter H.S., Acharya K.R. The refined crystal structure of toxic shock syndrome toxin-1 at 2.07 Å resolution. J. Mol. Biol. 260:1996;553-569
49. Prasad G.S., Earhart C.A., Murray D.L., Novick R.P., Schlievert P.M., Ohlendorf D.H. Structure of toxic shock syndrome toxin-1. Biochemistry. 32:1993;13761-13766
50. Read R.J. Improved coefficients for map calculation using partial structures with errors. Acta Crystallog. sect. A. 42:1986;140-149
51. Ren K., Bannan J.D., Pancholi V., Cheung A.L., Robbins J.C., Fischetti V.A., Zabriskie J.B. Characterization and biological properties of a new staphylococcal exotoxin. J. Expt. Med. 180:1994;1675-1683
52. Rogers T.J., Zhang L. Structural basis for the interaction of superantigen with the alternative superantigen-binding receptor p85. Mol. Immunol. 34:1997;263-272
53. Roussell A., Anderson B.F., Baker H.M., Fraser J.D., Baker E.N. Crystal structure of the streptococcal superantigen SPE-C dimerization and zinc-binding suggest a novel mode of interaction with MHC class II molecules. Nature Struct. Biol. 4:1997;635-643
54. Schad E.M., Zaitseva I., Zaitsev V.N., Dohlsten M., Kalland T., Schlievert P.M., Ohlendorf D.H., Svensson L.A. Crystal structure of the superantigen staphylococcal enterotoxin type A. EMBO J. 14:1995;3292-3301
55. Schad E.M., Papageorgiou A.C., Svensson L.A., Acharya K.R. A structural and functional comparison of staphylococcal enterotoxins A and C2 reveals remarkable similarity and dissimilarity. J. Mol. Biol. 269:1997;270-280
56. Sears C.L., Kaper J.B. Enteric bacterial toxins Mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60:1996;167-215
57. Sixma T.K., Stein P.E., Hol W.G.J., Read R.J. Comparison of the B-pentamers of heat-labile enterotoxin and verotoxin-1 two structures with remarkable similarity and dissimilarity. Biochemistry. 32:1993;191-198
58. Sheldrick G.M., Schneider T.R. SHELXL high resolution refinement. Methods Enzymol. 277. 319:(343):1997
59. Stein P.E., Boodhoo A., Armstrong G.D., Heerze L.D., Cockle S.A., Klein M.H., Read R.J. Structure of a pertussis toxin-sugar complex as a model for receptor binding. Nature Struct. Biol. 1:1994;591-596
60. Stuart D.I., Levine M., Muirhead H., Stammers D.K. The crystal structure of cat pyruvate kinase at a resolution of 2.6 Å J. Mol. Biol. 134:1979;109-142
61. 2+-mediated homodimerization. EMBO J. 15:1996;6832-6840
62. 2+at 2.7 Å resolution. J. Biol. Chem. 271:1996;32212-32216
63. Swaminathan S., Furey W., Pletcher J., Sax M. Crystal structure of staphylococcal enterotoxin B, a superantigen. Nature. 359:1992;801-806
64. Swaminathan S., Furey W., Pletcher J., Sax M. Residues defining Vβ specificity in staphylococcal enterotoxins. Nature Struct. Biol. 2:1995;680-686
65. Thibodeau J., Cloutier I., Lavoie P.M., Labrecque N., Mourad W., Jardetzsky T., Sékaly R.-P. Subsets of HLA-DR1 molecules defined by SEB and TSST-1 binding. Science. 266:1994;1874-1878
66. 2trimers in solution. Proc. Natl Acad. Sci. USA. 92:1995;12156-12159
67. Tranter H.S., Brehm R.D., Acharya K.R. Molecular topology is important for the function of staphylococcal superantigens. Thibodeau J., Sékaly R.-P. Bacterial Superantigens Structure, Function and Therapeutic Potential. 1995;5-23 Springer-Verlag, Heidelberg, Germany
68. Turner T.N., Smith C.L., Bohach G.A. Residues 20, 22, and 26 determine the subtype specificities of staphylococcal enterotoxins C1 and C2. Infect. Immun. 60:1992;694-697
69. Wang J., Whetshell M., Klein J.R. Local hormone networks and intestinal T cell homeostasis. Science. 275:1997;1937-1939
70. Woody M.A., Krakauer T., Stiles B.G. Staphylococcal enterotoxin B mutants (N23 K and F44 S) biological effects and vaccine potential in a mouse model. Vaccine. 15:1997;133-139