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PMID: 15574492 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Structure of the streptococcal endopeptidase IdeS, a cysteine proteinase with strict specificity for IgG.

Wenig K, Chatwell L, von Pawel-Rammingen U, Björck L, Huber R, Sondermann P

Abstract

Pathogenic bacteria have developed complex and diverse virulence mechanisms that weaken or disable the host immune defense system. IdeS (IgG-degrading enzyme of Streptococcus pyogenes) is a secreted cysteine endopeptidase from the human pathogen S. pyogenes with an extraordinarily high degree of substrate specificity, catalyzing a single proteolytic cleavage at the lower hinge of human IgG. This proteolytic degradation promotes inhibition of opsonophagocytosis and interferes with the killing of group A Streptococcus. We have determined the crystal structure of the catalytically inactive mutant IdeS-C94S by x-ray crystallography at 1.9-A resolution. Despite negligible sequence homology to known proteinases, the core of the structure resembles the canonical papain fold although with major insertions and a distinct substrate-binding site. Therefore IdeS belongs to a unique family within the CA clan of cysteine proteinases. Based on analogy with inhibitor complexes of papain-like proteinases, we propose a model for substrate binding by IdeS.

MeSH Terms
Amino Acid Sequence Binding Sites Catalysis Crystallography, X-Ray Cysteine/genetics,metabolism Cysteine Endopeptidases/chemistry,genetics,metabolism Immunoglobulin Fc Fragments/chemistry,metabolism Immunoglobulin G/chemistry,metabolism Models, Molecular Molecular Sequence Data Papain/chemistry,metabolism Protein Structure, Tertiary Sequence Alignment Streptococcus pyogenes/enzymology,genetics Substrate Specificity
Chemicals
Immunoglobulin Fc Fragments Immunoglobulin G Cysteine Endopeptidases Papain Cysteine
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wenig Katja
Department of Structural Research, Max Planck Institute for Biochemistry, D-82152 Martinsried, Germany. [email protected]
Chatwell Lorenz
von Pawel-Rammingen Ulrich
Björck Lars
Huber Robert
Sondermann Peter
References (41)
41 references, click to expand
  1. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps.
    Acta Crystallogr D Biol Crystallogr. 1999 Apr;55(Pt 4):938-40 PMID: 10089341
  2. Inhibition of mammalian legumain by some cystatins is due to a novel second reactive site.
    J Biol Chem. 1999 Jul 2;274(27):19195-203 PMID: 10383426
  3. Crystal structure of the zymogen form of the group A Streptococcus virulence factor SpeB: an integrin-binding cysteine protease.
    Proc Natl Acad Sci U S A. 2000 Feb 29;97(5):2235-40 PMID: 10681429
  4. Bacterial proteinases as targets for the development of second-generation antibiotics.
    Biochim Biophys Acta. 2000 Mar 7;1477(1-2):35-50 PMID: 10708847
  5. Pathogenesis of group A streptococcal infections.
    Clin Microbiol Rev. 2000 Jul;13(3):470-511 PMID: 10885988
  6. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex.
    Nature. 2000 Jul 20;406(6793):267-73 PMID: 10917521
  7. Description of staphylococcus serine protease (ssp) operon in Staphylococcus aureus and nonpolar inactivation of sspA-encoded serine protease.
    Infect Immun. 2001 Jan;69(1):159-69 PMID: 11119502
  8. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG.
    EMBO J. 2001 Jun 15;20(12):3046-55 PMID: 11406581
  9. Evasion of human innate and acquired immunity by a bacterial homolog of CD11b that inhibits opsonophagocytosis.
    Nat Med. 2001 Dec;7(12):1298-305 PMID: 11726969
  10. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G.
    EMBO J. 2002 Apr 2;21(7):1607-15 PMID: 11927545
  11. ARP/wARP's model-building algorithms. I. The main chain.
    Acta Crystallogr D Biol Crystallogr. 2002 Jun;58(Pt 6 Pt 2):968-75 PMID: 12037299
  12. Substructure solution with SHELXD.
    Acta Crystallogr D Biol Crystallogr. 2002 Oct;58(Pt 10 Pt 2):1772-9 PMID: 12351820
  13. Streptococcus pyogenes and phagocytic killing.
    Nat Med. 2002 Oct;8(10):1044-5; author reply 1045-6 PMID: 12357219
  14. Opsonophagocytosis-inhibiting mac protein of group a streptococcus: identification and characteristics of two genetic complexes.
    Infect Immun. 2002 Dec;70(12):6880-90 PMID: 12438365
  15. IdeS and SpeB: immunoglobulin-degrading cysteine proteinases of Streptococcus pyogenes.
    Curr Opin Microbiol. 2003 Feb;6(1):50-5 PMID: 12615219
  16. Histidine and aspartic acid residues important for immunoglobulin G endopeptidase activity of the group A Streptococcus opsonophagocytosis-inhibiting Mac protein.
    Infect Immun. 2003 May;71(5):2881-4 PMID: 12704162
  17. Defense against own arms: staphylococcal cysteine proteases and their inhibitors.
    Acta Biochim Pol. 2003;50(3):715-24 PMID: 14515151
  18. Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes.
    Curr Protein Pept Sci. 2003 Dec;4(6):397-407 PMID: 14683426
  19. The crystal structure of Pseudomonas avirulence protein AvrPphB: a papain-like fold with a distinct substrate-binding site.
    Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):302-7 PMID: 14694194
  20. Raster3D Version 2.0. A program for photorealistic molecular graphics.
    Acta Crystallogr D Biol Crystallogr. 1994 Nov 1;50(Pt 6):869-73 PMID: 15299354
  21. Crystal structure of aspartic proteinase from Irpex lacteus in complex with inhibitor pepstatin.
    J Mol Biol. 2004 Aug 27;341(5):1227-35 PMID: 15321718
  22. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons.
    Proteins. 1991;11(4):281-96 PMID: 1758883
  23. The refined 2.15 A X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity.
    EMBO J. 1991 Sep;10(9):2321-30 PMID: 1868826
  24. Contribution of the glutamine 19 side chain to transition-state stabilization in the oxyanion hole of papain.
    Biochemistry. 1991 Sep 17;30(37):8924-8 PMID: 1892809
  25. A PROTEOLYTIC ENZYME PRODUCED BY GROUP A STREPTOCOCCI WITH SPECIAL REFERENCE TO ITS EFFECT ON THE TYPE-SPECIFIC M ANTIGEN.
    J Exp Med. 1945 Jun 1;81(6):573-92 PMID: 19871477
  26. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  27. Bacterial growth blocked by a synthetic peptide based on the structure of a human proteinase inhibitor.
    Nature. 1989 Jan 26;337(6205):385-6 PMID: 2643059
  28. Processing of X-ray diffraction data collected in oscillation mode.
    Methods Enzymol. 1997;276:307-26 PMID: 27754618
  29. [27] Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods.
    Methods Enzymol. 1997;276:472-494 PMID: 27799110
  30. Degradation of elastin by a cysteine proteinase from Staphylococcus aureus.
    J Biol Chem. 1988 Feb 25;263(6):2664-7 PMID: 3422637
  31. Human low-Mr kininogen contains three copies of a cystatin sequence that are divergent in structure and in inhibitory activity for cysteine proteinases.
    Biochem J. 1986 Mar 1;234(2):429-34 PMID: 3521586
  32. On the size of the active site in proteases. I. Papain.
    Biochem Biophys Res Commun. 1967 Apr 20;27(2):157-62 PMID: 6035483
  33. L-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L.
    Biochem J. 1982 Jan 1;201(1):189-98 PMID: 7044372
  34. Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins.
    J Biol Chem. 1995 Apr 28;270(17):9862-7 PMID: 7730368
  35. Searching protein structure databases has come of age.
    Proteins. 1994 Jul;19(3):165-73 PMID: 7937731
  36. X-ray crystallographic structure of a papain-leupeptin complex.
    FEBS Lett. 1993 Jan 2;315(1):38-42 PMID: 8416808
  37. Are bacterial proteinases pathogenic factors?
    Trends Microbiol. 1995 Oct;3(10):405-7 PMID: 8564361
  38. Clostripain linker deletion variants yield active enzyme in Escherichia coli: a possible function of the linker peptide as intramolecular inhibitor of clostripain automaturation.
    Curr Microbiol. 1996 Nov;33(5):281-6 PMID: 8875906
  39. Binding of chloromethyl ketone substrate analogues to crystalline papain.
    Biochemistry. 1976 Aug 24;15(17):3731-8 PMID: 952885
  40. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  41. A natural variant of the cysteine protease virulence factor of group A Streptococcus with an arginine-glycine-aspartic acid (RGD) motif preferentially binds human integrins alphavbeta3 and alphaIIbbeta3.
    Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):242-7 PMID: 9874803
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2004-12-14
Epub
2004-00-01
Pages
17371-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC536041
Subset
IM
Databases
PDB
Analysis Services
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