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Structural, energetic, and functional analysis of a protein-protein interface at distinct stages of affinity maturation.

Sundberg EJ, Andersen PS, Schlievert PM, Karjalainen K, Mariuzza RA
Structure 11 1151-61 (2003)
Related entries: 1jws, 1jwu

Cited: 26 times
EuropePMC logo PMID: 12962633

Abstract

Due to a paucity of studies that synthesize structural, energetic, and functional analyses of a series of protein complexes representing distinct stages in an affinity maturation pathway, the biophysical basis for the molecular evolution of protein-protein interactions is poorly understood. Here, we combine crystal structures and binding-free energies of a series of variant superantigen (SAG)-major histocompatibility complex (MHC) class II complexes exhibiting increasingly higher affinity to reveal that this affinity maturation pathway is controlled largely by two biophysical factors: shape complementarity and buried hydrophobic surface. These factors, however, do not contribute equivalently to the affinity maturation of the interface, as the former dominates the early steps of the maturation process while the latter is responsible for improved binding in later steps. Functional assays reveal how affinity maturation of the SAG-MHC interface corresponds to T cell activation by SAGs.

Reviews - 1jwm mentioned but not cited (2)

  1. Conformational variation in structures of classical and non-classical MHCII proteins and functional implications. Painter CA, Stern LJ. Immunol Rev 250 144-157 (2012)
  2. Streptococcal superantigens and the return of scarlet fever. Hurst JR, Brouwer S, Walker MJ, McCormick JK. PLoS Pathog 17 e1010097 (2021)

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Reviews citing this publication (1)

  1. Soluble T cell receptor Vβ domains engineered for high-affinity binding to staphylococcal or streptococcal superantigens. Sharma P, Wang N, Kranz DM. Toxins (Basel) 6 556-574 (2014)

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  1. Structural analysis of B-cell epitopes in antibody:protein complexes. Kringelum JV, Nielsen M, Padkjær SB, Lund O. Mol. Immunol. 53 24-34 (2013)
  2. Model for the peptide-free conformation of class II MHC proteins. Painter CA, Cruz A, López GE, Stern LJ, Zavala-Ruiz Z. PLoS ONE 3 e2403 (2008)
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  4. A major histocompatibility complex-peptide-restricted antibody and t cell receptor molecules recognize their target by distinct binding modes: crystal structure of human leukocyte antigen (HLA)-A1-MAGE-A1 in complex with FAB-HYB3. Hülsmeyer M, Chames P, Hillig RC, Stanfield RL, Held G, Coulie PG, Alings C, Wille G, Saenger W, Uchanska-Ziegler B, Hoogenboom HR, Ziegler A. J. Biol. Chem. 280 2972-2980 (2005)
  5. Crystal structure of staphylococcal enterotoxin I (SEI) in complex with a human major histocompatibility complex class II molecule. Fernández MM, Guan R, Swaminathan CP, Malchiodi EL, Mariuzza RA. J. Biol. Chem. 281 25356-25364 (2006)
  6. Magnitude of the hydrophobic effect at central versus peripheral sites in protein-protein interfaces. Li Y, Huang Y, Swaminathan CP, Smith-Gill SJ, Mariuzza RA. Structure 13 297-307 (2005)
  7. Structural basis of affinity maturation and intramolecular cooperativity in a protein-protein interaction. Cho S, Swaminathan CP, Yang J, Kerzic MC, Guan R, Kieke MC, Kranz DM, Mariuzza RA, Sundberg EJ. Structure 13 1775-1787 (2005)
  8. Assessing energetic contributions to binding from a disordered region in a protein-protein interaction . Cho S, Swaminathan CP, Bonsor DA, Kerzic MC, Guan R, Yang J, Kieke MC, Andersen PS, Kranz DM, Mariuzza RA, Sundberg EJ. Biochemistry 49 9256-9268 (2010)
  9. Crystal structures of T cell receptor (beta) chains related to rheumatoid arthritis. Li H, Van Vranken S, Zhao Y, Li Z, Guo Y, Eisele L, Li Y. Protein Sci. 14 3025-3038 (2005)
  10. Flanking residues are central to DO11.10 T cell hybridoma stimulation by ovalbumin 323-339. Roy BM, Zhukov DV, Maynard JA. PLoS ONE 7 e47585 (2012)
  11. Molecular basis of in vitro affinity maturation and functional evolution of a neutralizing anti-human GM-CSF antibody. Eylenstein R, Weinfurtner D, Härtle S, Strohner R, Böttcher J, Augustin M, Ostendorp R, Steidl S. MAbs 8 176-186 (2016)
  12. Deciphering evolution of immune recognition in antibodies. Kaur H, Sain N, Mohanty D, Salunke DM. BMC Struct. Biol. 18 19 (2018)
  13. Molecular Basis of Broad Spectrum N-Glycan Specificity and Processing of Therapeutic IgG Monoclonal Antibodies by Endoglycosidase S2. Klontz EH, Trastoy B, Deredge D, Fields JK, Li C, Orwenyo J, Marina A, Beadenkopf R, Günther S, Flores J, Wintrode PL, Wang LX, Guerin ME, Sundberg EJ. ACS Cent Sci 5 524-538 (2019)
  14. Staphylococcal Enterotoxin B and C Mutants and Vaccine Toxoids. Schlievert PM. Microbiol Spectr e0444622 (2023)


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