2g9h Citations

Crystal structure of staphylococcal enterotoxin I (SEI) in complex with a human major histocompatibility complex class II molecule.

J. Biol. Chem. 281 25356-64 (2006)
Cited: 34 times
EuropePMC logo PMID: 16829512

Abstract

Superantigens are bacterial or viral proteins that elicit massive T cell activation through simultaneous binding to major histocompatibility complex (MHC) class II and T cell receptors. This activation results in uncontrolled release of inflammatory cytokines, causing toxic shock. A remarkable property of superantigens, which distinguishes them from T cell receptors, is their ability to interact with multiple MHC class II alleles independently of MHC-bound peptide. Previous crystallographic studies have shown that staphylococcal and streptococcal superantigens belonging to the zinc family bind to a high affinity site on the class II beta-chain. However, the basis for promiscuous MHC recognition by zinc-dependent superantigens is not obvious, because the beta-chain is polymorphic and the MHC-bound peptide forms part of the binding interface. To understand how zinc-dependent superantigens recognize MHC, we determined the crystal structure, at 2.0 A resolution, of staphylococcal enterotoxin I bound to the human class II molecule HLA-DR1 bearing a peptide from influenza hemagglutinin. Interactions between the superantigen and DR1 beta-chain are mediated by a zinc ion, and 22% of the buried surface of peptide.MHC is contributed by the peptide. Comparison of the staphylococcal enterotoxin I.peptide.DR1 structure with ones determined previously revealed that zinc-dependent superantigens achieve promiscuous binding to MHC by targeting conservatively substituted residues of the polymorphic beta-chain. Additionally, these superantigens circumvent peptide specificity by engaging MHC-bound peptides at their conformationally conserved N-terminal regions while minimizing sequence-specific interactions with peptide residues to enhance cross-reactivity.

Articles - 2g9h mentioned but not cited (6)

  1. Electrostatic modifications of the human leukocyte antigen-DR P9 peptide-binding pocket and susceptibility to primary sclerosing cholangitis. Hov JR, Kosmoliaptsis V, Traherne JA, Olsson M, Boberg KM, Bergquist A, Schrumpf E, Bradley JA, Taylor CJ, Lie BA, Trowsdale J, Karlsen TH. Hepatology 53 1967-1976 (2011)
  2. Limitations of Ab initio predictions of peptide binding to MHC class II molecules. Zhang H, Wang P, Papangelopoulos N, Xu Y, Sette A, Bourne PE, Lund O, Ponomarenko J, Nielsen M, Peters B. PLoS ONE 5 e9272 (2010)
  3. Prediction of the binding affinities of peptides to class II MHC using a regularized thermodynamic model. Bordner AJ, Mittelmann HD. BMC Bioinformatics 11 41 (2010)
  4. MHC class II complexes sample intermediate states along the peptide exchange pathway. Wieczorek M, Sticht J, Stolzenberg S, Günther S, Wehmeyer C, El Habre Z, Álvaro-Benito M, Noé F, Freund C. Nat Commun 7 13224 (2016)
  5. An effective and effecient peptide binding prediction approach for a broad set of HLA-DR molecules based on ordered weighted averaging of binding pocket profiles. Shen WJ, Zhang S, Wong HS. Proteome Sci 11 S15 (2013)
  6. An automated framework for understanding structural variations in the binding grooves of MHC class II molecules. Yeturu K, Utriainen T, Kemp GJ, Chandra N. BMC Bioinformatics 11 Suppl 1 S55 (2010)


Reviews citing this publication (16)

  1. Staphylococcal enterotoxins. Pinchuk IV, Beswick EJ, Reyes VE. Toxins (Basel) 2 2177-2197 (2010)
  2. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. Hennekinne JA, De Buyser ML, Dragacci S. FEMS Microbiol. Rev. 36 815-836 (2012)
  3. TCR recognition of peptide/MHC class II complexes and superantigens. Sundberg EJ, Deng L, Mariuzza RA. Semin. Immunol. 19 262-271 (2007)
  4. Gram-positive bacterial superantigen outside-in signaling causes toxic shock syndrome. Brosnahan AJ, Schlievert PM. FEBS J. 278 4649-4667 (2011)
  5. Staphylococcal superantigens in colonization and disease. Xu SX, McCormick JK. Front Cell Infect Microbiol 2 52 (2012)
  6. Multiple roles of Staphylococcus aureus enterotoxins: pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Ortega E, Abriouel H, Lucas R, Gálvez A. Toxins (Basel) 2 2117-2131 (2010)
  7. The contribution of group A streptococcal virulence determinants to the pathogenesis of sepsis. Reglinski M, Sriskandan S. Virulence 5 127-136 (2014)
  8. The systemic and pulmonary immune response to staphylococcal enterotoxins. Kumar S, Ménoret A, Ngoi SM, Vella AT. Toxins (Basel) 2 1898-1912 (2010)
  9. The contribution of group A streptococcal virulence determinants to the pathogenesis of sepsis. Reglinski M, Sriskandan S. Virulence 5 127-136 (2014)
  10. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. Hennekinne JA, De Buyser ML, Dragacci S. FEMS Microbiol. Rev. 36 815-836 (2012)
  11. Staphylococcal superantigens in colonization and disease. Xu SX, McCormick JK. Front Cell Infect Microbiol 2 52 (2012)
  12. Gram-positive bacterial superantigen outside-in signaling causes toxic shock syndrome. Brosnahan AJ, Schlievert PM. FEBS J. 278 4649-4667 (2011)
  13. The systemic and pulmonary immune response to staphylococcal enterotoxins. Kumar S, Ménoret A, Ngoi SM, Vella AT. Toxins (Basel) 2 1898-1912 (2010)
  14. Staphylococcal enterotoxins. Pinchuk IV, Beswick EJ, Reyes VE. Toxins (Basel) 2 2177-2197 (2010)
  15. Multiple roles of Staphylococcus aureus enterotoxins: pathogenicity, superantigenic activity, and correlation to antibiotic resistance. Ortega E, Abriouel H, Lucas R, Gálvez A. Toxins (Basel) 2 2117-2131 (2010)
  16. TCR recognition of peptide/MHC class II complexes and superantigens. Sundberg EJ, Deng L, Mariuzza RA. Semin. Immunol. 19 262-271 (2007)

Articles citing this publication (12)

  1. "Natural" human leukocyte antigen antibodies found in nonalloimmunized healthy males. Morales-Buenrostro LE, Terasaki PI, Marino-Vázquez LA, Lee JH, El-Awar N, Alberú J. Transplantation 86 1111-1115 (2008)
  2. A novel loop domain in superantigens extends their T cell receptor recognition site. Günther S, Varma AK, Moza B, Kasper KJ, Wyatt AW, Zhu P, Rahman AK, Li Y, Mariuzza RA, McCormick JK, Sundberg EJ. J. Mol. Biol. 371 210-221 (2007)
  3. Crystal structure of the streptococcal superantigen SpeI and functional role of a novel loop domain in T cell activation by group V superantigens. Brouillard JN, Günther S, Varma AK, Gryski I, Herfst CA, Rahman AK, Leung DY, Schlievert PM, Madrenas J, Sundberg EJ, McCormick JK. J. Mol. Biol. 367 925-934 (2007)
  4. The structure of superantigen complexed with TCR and MHC reveals novel insights into superantigenic T cell activation. Saline M, Rödström KE, Fischer G, Orekhov VY, Karlsson BG, Lindkvist-Petersson K. Nat Commun 1 119 (2010)
  5. Crystal structure of staphylococcal enterotoxin G (SEG) in complex with a mouse T-cell receptor {beta} chain. Fernández MM, Cho S, De Marzi MC, Kerzic MC, Robinson H, Mariuzza RA, Malchiodi EL. J. Biol. Chem. 286 1189-1195 (2011)
  6. Structure of Staphylococcal Enterotoxin E in Complex with TCR Defines the Role of TCR Loop Positioning in Superantigen Recognition. Rödström KE, Regenthal P, Lindkvist-Petersson K. PLoS ONE 10 e0131988 (2015)
  7. Uptake and intracellular trafficking of superantigens in dendritic cells. Ganem MB, De Marzi MC, Fernández-Lynch MJ, Jancic C, Vermeulen M, Geffner J, Mariuzza RA, Fernández MM, Malchiodi EL. PLoS ONE 8 e66244 (2013)
  8. Multiplex reverse transcription polymerase chain reaction to study the expression of virulence and stress response genes in Staphylococcus aureus. Shrihari RY, Singh NP. J. Food Sci. 77 M95-101 (2012)
  9. MHC Class II Binding Prediction by Molecular Docking. Atanasova M, Dimitrov I, Flower DR, Doytchinova I. Mol Inform 30 368-375 (2011)
  10. Using common spatial distributions of atoms to relate functionally divergent influenza virus N10 and N11 protein structures to functionally characterized neuraminidase structures, toxin cell entry domains, and non-influenza virus cell entry domains. Weininger A, Weininger S. PLoS ONE 10 e0117499 (2015)
  11. Weak conservation of structural features in the interfaces of homologous transient protein-protein complexes. Sudha G, Singh P, Swapna LS, Srinivasan N. Protein Sci. 24 1856-1873 (2015)
  12. HLA-typing analysis following allogeneic bone grafting for sinus lifting. Piaia M, Bub CB, Succi GM, Torres M, Costa TH, Pinheiro FC, Napimoga MH. Cell Tissue Bank 18 75-81 (2017)