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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 371 210-21 (2007)
Cited: 32 times
EuropePMC logo PMID: 17560605

Abstract

Superantigens (SAGs) interact with host immune receptors to induce a massive release of inflammatory cytokines that can lead to toxic shock syndrome and death. Bacterial SAGs can be classified into five distinct evolutionary groups. Group V SAGs are characterized by the alpha3-beta8 loop, a unique approximately 15 amino acid residue extension that is required for optimal T cell activation. Here, we report the X-ray crystal structures of the group V SAG staphylococcal enterotoxin K (SEK) alone and in complex with the TCR hVbeta5.1 domain. SEK adopts a unique TCR binding orientation relative to other SAG-TCR complexes, which results in the alpha3-beta8 loop contacting the apical loop of framework region 4, thereby extending the known TCR recognition site of SAGs. These interactions are absolutely required for TCR binding and T cell activation by SEK, and dictate the TCR Vbeta domain specificity of SEK and other group V SAGs.

Reviews - 2nts mentioned but not cited (2)

  1. Manipulation of Innate and Adaptive Immunity by Staphylococcal Superantigens. Tuffs SW, Haeryfar SMM, McCormick JK. Pathogens 7 E53 (2018)
  2. Cure lies in nature: medicinal plants and endophytic fungi in curbing cancer. Tyagi G, Kapoor N, Chandra G, Gambhir L. 3 Biotech 11 263 (2021)

Articles - 2nts mentioned but not cited (5)

  1. 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)
  2. Modeling the ternary complex TCR-Vbeta/CollagenII(261-273)/HLA-DR4 associated with rheumatoid arthritis. De Rosa MC, Giardina B, Bianchi C, Carelli Alinovi C, Pirolli D, Ferraccioli G, De Santis M, Di Sante G, Ria F. PLoS One 5 e11550 (2010)
  3. Transcriptome-wide Interrogation of the Functional Intronome by Spliceosome Profiling. Chen W, Moore J, Ozadam H, Shulha HP, Rhind N, Weng Z, Moore MJ. Cell 173 1031-1044.e13 (2018)
  4. Population Analysis of Staphylococcus aureus Reveals a Cryptic, Highly Prevalent Superantigen SElW That Contributes to the Pathogenesis of Bacteremia. Vrieling M, Tuffs SW, Yebra G, van Smoorenburg MY, Alves J, Pickering AC, Park JY, Park N, Heinrichs DE, Benedictus L, Connelley T, Seo KS, McCormick JK, Fitzgerald JR. mBio 11 e02082-20 (2020)
  5. T cell receptor variable β20-1 harbors a nucleotide binding pocket in the CDR2β loop. Watkins S, Pichler WJ. Open J Immunol 3 165-174 (2013)


Reviews citing this publication (13)

  1. Food poisoning and Staphylococcus aureus enterotoxins. Argudín MÁ, Mendoza MC, Rodicio MR. Toxins (Basel) 2 1751-1773 (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. Staphylococcal and streptococcal superantigen exotoxins. Spaulding AR, Salgado-Pabón W, Kohler PL, Horswill AR, Leung DY, Schlievert PM. Clin Microbiol Rev 26 422-447 (2013)
  4. Staphylococcus aureus Secreted Toxins and Extracellular Enzymes. Tam K, Torres VJ. Microbiol Spectr 7 (2019)
  5. Staphylococcal superantigens in colonization and disease. Xu SX, McCormick JK. Front Cell Infect Microbiol 2 52 (2012)
  6. Survey of the year 2007 commercial optical biosensor literature. Rich RL, Myszka DG. J Mol Recognit 21 355-400 (2008)
  7. Gram-positive bacterial superantigen outside-in signaling causes toxic shock syndrome. Brosnahan AJ, Schlievert PM. FEBS J 278 4649-4667 (2011)
  8. Toxins from bacteria. Henkel JS, Baldwin MR, Barbieri JT. EXS 100 1-29 (2010)
  9. Staphylococcal enterotoxins and enterotoxin-like toxins with special reference to dairy products: An overview. Benkerroum N. Crit Rev Food Sci Nutr 58 1943-1970 (2018)
  10. T Cell Immunity to Bacterial Pathogens: Mechanisms of Immune Control and Bacterial Evasion. Shepherd FR, McLaren JE. Int J Mol Sci 21 E6144 (2020)
  11. The systemic and pulmonary immune response to staphylococcal enterotoxins. Kumar S, Ménoret A, Ngoi SM, Vella AT. Toxins (Basel) 2 1898-1912 (2010)
  12. Molecular Characteristics and Pathogenicity of Staphylococcus aureus Exotoxins. Zhu Z, Hu Z, Li S, Fang R, Ono HK, Hu DL. Int J Mol Sci 25 395 (2023)
  13. Novel insights into the immune response to bacterial T cell superantigens. Tuffs SW, Dufresne K, Rishi A, Walton NR, McCormick JK. Nat Rev Immunol (2024)

Articles citing this publication (12)

  1. Bacterial superantigens promote acute nasopharyngeal infection by Streptococcus pyogenes in a human MHC Class II-dependent manner. Kasper KJ, Zeppa JJ, Wakabayashi AT, Xu SX, Mazzuca DM, Welch I, Baroja ML, Kotb M, Cairns E, Cleary PP, Haeryfar SM, McCormick JK. PLoS Pathog 10 e1004155 (2014)
  2. 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)
  3. The T cell receptor beta-chain second complementarity determining region loop (CDR2beta governs T cell activation and Vbeta specificity by bacterial superantigens. Nur-ur Rahman AK, Bonsor DA, Herfst CA, Pollard F, Peirce M, Wyatt AW, Kasper KJ, Madrenas J, Sundberg EJ, McCormick JK. J Biol Chem 286 4871-4881 (2011)
  4. Detection and measurement of staphylococcal enterotoxin-like K (SEl-K) secretion by Staphylococcus aureus clinical isolates. Aguilar JL, Varshney AK, Wang X, Stanford L, Scharff M, Fries BC. J Clin Microbiol 52 2536-2543 (2014)
  5. 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)
  6. Human scFvs That Counteract Bioactivities of Staphylococcus aureus TSST-1. Rukkawattanakul T, Sookrung N, Seesuay W, Onlamoon N, Diraphat P, Chaicumpa W, Indrawattana N. Toxins (Basel) 9 E50 (2017)
  7. A restricted clonal T-cell receptor αβ repertoire in Sézary syndrome is indicative of superantigenic stimulation. van der Fits L, Sandberg Y, Darzentas N, Zoutman WH, Tielemans D, Wolvers-Tettero IL, Vermeer MH, Langerak AW. Br J Dermatol 165 78-84 (2011)
  8. Immunochemical assay with monoclonal antibodies for detection of staphylococcal enterotoxin H. Rudenko NV, Karatovskaya AP, Noskov AN, Shepelyakovskaya AO, Shchannikova MP, Loskutova IV, Artyemieva OA, Nikanova DA, Gladyr EA, Brovko FA. J Food Drug Anal 26 741-750 (2018)
  9. Inhibition of emetic and superantigenic activities of staphylococcal enterotoxin A by synthetic peptides. Maina EK, Hu DL, Asano K, Nakane A. Peptides 38 1-7 (2012)
  10. Staphylococcus enterotoxin profile of China isolates and the superantigenicity of some novel enterotoxins. Shen M, Li Y, Zhang L, Dai S, Wang J, Li Y, Zhang L, Huang J. Arch Microbiol 199 723-736 (2017)
  11. Herpes B virus gD interaction with its human receptor--an in silico analysis approach. Li L, Qiu Z, Li Y, Liang F, Ye H, Cai Y, Guo W, Li Y, Yue J. Theor Biol Med Model 11 27 (2014)
  12. Evaluation of a recombinant double mutant of staphylococcal enterotoxin B (SEB-H32Q/K173E) with enhanced antitumor activity effects and decreased pyrexia. Gu L, Yue J, Zheng Y, Zheng X, Wang J, Wang Y, Li J, Jiang Y, Jiang H. PLoS One 8 e55892 (2013)


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