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PMID: 11406581 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG.

The EMBO journal ·Vol. 20 ·No. 12 ·2001-06-15 ·Pages 3046-55

Collin M, Olsén A

Abstract

Streptococcus pyogenes is an important human pathogen that selectively interacts with proteins involved in the humoral defense system, such as immunoglobulins and complement factors. In this report we show that S.pyogenes has the ability to hydrolyze the chitobiose core of the asparagine-linked glycan on immuno globulin G (IgG) when bacteria are grown in the presence of human plasma. This activity is associated with the secretion of a novel 108 kDa protein denoted EndoS. EndoS has endoglycosidase activity on purified soluble IgG as well as IgG bound to the bacterial surface. EndoS is required for the activity on IgG, as an isogenic EndoS mutant could not hydrolyze the glycan on IgG. In addition, we show that the secreted streptococcal cysteine proteinase SpeB cleaves IgG in the hinge region in a papain-like manner. This is the first example of an endoglycosidase produced by a bacterial pathogen that selectively hydrolyzes human IgG, and reveals a novel mechanism which may contribute to S.pyogenes pathogenesis.

MeSH Terms
Amino Acid Sequence Bacterial Proteins Carbohydrate Sequence Disaccharides/metabolism Glycoside Hydrolases/classification,genetics,metabolism Humans Hydrolysis Immunoglobulin G/metabolism Molecular Sequence Data Mutagenesis Polysaccharides/metabolism Sequence Homology, Amino Acid Streptococcus pyogenes/enzymology,genetics
Chemicals
Bacterial Proteins Disaccharides Immunoglobulin G Polysaccharides chitobiose Glycoside Hydrolases NDOS protein, Streptococcus pyogenes
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Collin M
Department of Cell and Molecular Biology, Section for Molecular Pathogenesis, BMC-B14, SE-221 84, Lund, Sweden.
Olsén A
References (68)
68 references, click to expand
  1. Streptococcal protein H forms soluble complement-activating complexes with IgG, but inhibits complement activation by IgG-coated targets.
    J Biol Chem. 1997 Aug 15;272(33):20774-81 PMID: 9252400
  2. A nonradioactive biochemical characterization of membrane proteins using enhanced chemiluminescence.
    Anal Biochem. 1992 Nov 1;206(2):267-72 PMID: 1443597
  3. Complete genome sequence of an M1 strain of Streptococcus pyogenes.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4658-63 PMID: 11296296
  4. A protein sequenator.
    Eur J Biochem. 1967 Mar;1(1):80-91 PMID: 6059350
  5. The conformational effects of N-glycosylation on the tailpiece from serum IgM.
    Eur J Biochem. 1991 May 23;198(1):131-9 PMID: 2040275
  6. Identification of endo-beta-N-acetylglucosaminidase and N-acetylmuramyl-L-alanine amidase as cluster-dispersing enzymes in Staphylococcus aureus.
    J Bacteriol. 1995 Mar;177(6):1491-6 PMID: 7883705
  7. Multiple endoglycosidase F activities expressed by Flavobacterium meningosepticum endoglycosidases F2 and F3. Molecular cloning, primary sequence, and enzyme expression.
    J Biol Chem. 1993 May 5;268(13):9702-8 PMID: 8486657
  8. Amplified expression of streptomyces endo-beta-N-acetylglucosaminidase H in Escherichia coli and characterization of the enzyme product.
    J Biol Chem. 1985 May 10;260(9):5683-90 PMID: 3921547
  9. Cloning and expression of the beta-N-acetylglucosaminidase gene from Streptococcus pneumoniae. Generation of truncated enzymes with modified aglycon specificity.
    J Biol Chem. 1995 Apr 14;270(15):8805-14 PMID: 7721787
  10. Enzymatic deglycosylation of asparagine-linked glycans: purification, properties, and specificity of oligosaccharide-cleaving enzymes from Flavobacterium meningosepticum.
    Methods Enzymol. 1994;230:44-57 PMID: 8139511
  11. Characterization of an erythromycin resistance (erm) plasmid in Streptococcus pyogenes.
    APMIS. 1995 Jan;103(1):59-68 PMID: 7695892
  12. Protein H--a novel IgG binding bacterial protein.
    Mol Immunol. 1990 Jun;27(6):523-31 PMID: 2199820
  13. Isolation and characterization of erythrogenic toxins. V. Communication: identity of erythrogenic toxin type B and streptococcal proteinase precursor.
    Zentralbl Bakteriol Mikrobiol Hyg A. 1983 Sep;255(2-3):221-33 PMID: 6359775
  14. Inactivation of Streptococcus pyogenes extracellular cysteine protease significantly decreases mouse lethality of serotype M3 and M49 strains.
    J Clin Invest. 1997 Jun 1;99(11):2574-80 PMID: 9169486
  15. Group A streptococcal immunoglobulin-binding proteins: adhesins, molecular mimicry or sensory proteins?
    Trends Microbiol. 1994 Apr;2(4):131-6 PMID: 8012756
  16. A conserved Streptococcus pyogenes extracellular cysteine protease cleaves human fibronectin and degrades vitronectin.
    Microb Pathog. 1993 Nov;15(5):327-46 PMID: 7516997
  17. Endoglycosidases from Flavobacterium meningosepticum application to biological problems.
    Methods Enzymol. 1989;179:505-18 PMID: 2516226
  18. Characterization of immunoglobulin G-degrading proteases of Prevotella intermedia and Prevotella nigrescens.
    Oral Microbiol Immunol. 1995 Jun;10(3):138-45 PMID: 7567062
  19. Agalactosyl glycoforms of IgG autoantibodies are pathogenic.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6123-7 PMID: 8016124
  20. Role for a secreted cysteine proteinase in the establishment of host tissue tropism by group A streptococci.
    Mol Microbiol. 2000 Oct;38(2):242-53 PMID: 11069651
  21. Effect of group A streptococcal cysteine protease on invasion of epithelial cells.
    Infect Immun. 1998 Apr;66(4):1460-6 PMID: 9529068
  22. Purification of the oligosaccharide-cleaving enzymes of Flavobacterium meningosepticum.
    Glycobiology. 1991 Jun;1(3):257-63 PMID: 1794038
  23. An M protein with a single C repeat prevents phagocytosis of Streptococcus pyogenes: use of a temperature-sensitive shuttle vector to deliver homologous sequences to the chromosome of S. pyogenes.
    Mol Microbiol. 1993 May;8(5):809-19 PMID: 8355608
  24. Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity.
    J Biol Chem. 1993 Sep 5;268(25):18567-72 PMID: 8103047
  25. Generation of a mature streptococcal cysteine proteinase is dependent on cell wall-anchored M1 protein.
    Mol Microbiol. 2000 Jun;36(6):1306-18 PMID: 10931281
  26. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  27. Immunoglobulin G: functional sites.
    Mol Immunol. 1985 Mar;22(3):161-206 PMID: 3889592
  28. A comparative analysis of disease-associated changes in the galactosylation of serum IgG.
    J Autoimmun. 1989 Apr;2(2):101-14 PMID: 2504180
  29. Streptococcal sialidase. I. Isolation and properties of sialidase produced by group K Streptococcus.
    J Bacteriol. 1967 Jun;93(6):1753-7 PMID: 4960891
  30. 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
  31. 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
  32. Experimental studies of the pathogenesis of infections owing to Pseudomonas aeruginosa: elastase, an IgG protease.
    Can J Microbiol. 1984 Sep;30(9):1118-24 PMID: 6439405
  33. Sequential deglycosylation and utilization of the N-linked, complex-type glycans of human alpha1-acid glycoprotein mediates growth of Streptococcus oralis.
    Glycobiology. 1999 May;9(5):469-79 PMID: 10207179
  34. Reduced B-cell galactosyltransferase activity in rheumatoid arthritis.
    Lancet. 1987 Dec 26;2(8574):1486-8 PMID: 2892049
  35. Protein H, an antiphagocytic surface protein in Streptococcus pyogenes.
    Infect Immun. 1999 Apr;67(4):1708-14 PMID: 10085008
  36. Ecology and nature of immunoglobulin A1 protease-producing streptococci in the human oral cavity and pharynx.
    Infect Immun. 1981 Mar;31(3):868-73 PMID: 7014463
  37. Fibrinogen cleavage by the Streptococcus pyogenes extracellular cysteine protease and generation of antibodies that inhibit enzyme proteolytic activity.
    Infect Immun. 1999 Sep;67(9):4326-33 PMID: 10456870
  38. Neuraminidase production by streptococci from patients with glomerulonephritis.
    J Infect Dis. 1985 Feb;151(2):259-63 PMID: 2578533
  39. Molecular analysis of Streptococcus pyogenes adhesion.
    Methods Enzymol. 1995;253:269-305 PMID: 7476392
  40. Group A streptococcal infections and acute rheumatic fever.
    N Engl J Med. 1991 Sep 12;325(11):783-93 PMID: 1870652
  41. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  42. The gene sequence and some properties of protein H. A novel IgG-binding protein.
    J Immunol. 1990 May 15;144(10):4046-52 PMID: 2332638
  43. Glomerular lesions produced by autologous serum and autologous IgG modified by treatment with a culture of a -haemolytic streptooccus.
    J Med Microbiol. 1972 Feb;5(1):1-7 PMID: 4553907
  44. A rapid alkaline extraction procedure for screening recombinant plasmid DNA.
    Nucleic Acids Res. 1979 Nov 24;7(6):1513-23 PMID: 388356
  45. Biological significance of carbohydrate chains on monoclonal antibodies.
    Proc Natl Acad Sci U S A. 1983 Nov;80(21):6632-6 PMID: 6579549
  46. Pathogenesis of group A streptococcal infections.
    Clin Microbiol Rev. 2000 Jul;13(3):470-511 PMID: 10885988
  47. The effect of aglycosylation on the binding of mouse IgG to staphylococcal protein A.
    FEBS Lett. 1983 Dec 12;164(2):227-30 PMID: 6653789
  48. Convergent evolution among immunoglobulin G-binding bacterial proteins.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8532-6 PMID: 1528858
  49. Antiopsonic activity of fibrinogen bound to M protein on the surface of group A streptococci.
    J Clin Invest. 1982 Apr;69(4):1042-5 PMID: 7042754
  50. Streptococcal superantigen, mitogenic factor, and pyrogenic exotoxin B expressed by Streptococcus pyogenes. Structure and function.
    Prep Biochem Biotechnol. 1997 May-Aug;27(2-3):143-72 PMID: 9292924
  51. Novel series of plasmid vectors for gene inactivation and expression analysis in group A streptococci (GAS).
    Gene. 1996 Oct 24;177(1-2):137-47 PMID: 8921859
  52. The labelling of proteins to high specific radioactivities by conjugation to a 125I-containing acylating agent.
    Biochem J. 1973 Jul;133(3):529-39 PMID: 4733239
  53. Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F.
    Biochemistry. 1985 Aug 13;24(17):4665-71 PMID: 4063349
  54. Structural studies of immunoglobulins.
    Science. 1973 May 18;180(4087):713-6 PMID: 4122075
  55. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG.
    Nature. 1985 Aug 1-7;316(6027):452-7 PMID: 3927174
  56. A classification of glycosyl hydrolases based on amino acid sequence similarities.
    Biochem J. 1991 Dec 1;280 ( Pt 2):309-16 PMID: 1747104
  57. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes.
    J Biol Chem. 1987 Jul 25;262(21):10035-8 PMID: 3611052
  58. PAM, a novel plasminogen-binding protein from Streptococcus pyogenes.
    J Biol Chem. 1993 Dec 5;268(34):25417-24 PMID: 8244975
  59. Specific proteolysis of human IgA by Streptococcus pneumoniae and Haemophilus influenzae.
    J Infect Dis. 1980 Apr;141(4):450-6 PMID: 6989925
  60. Agalactosyl IgG in inflammatory bowel disease: correlation with C-reactive protein.
    Gut. 1990 Apr;31(4):431-4 PMID: 2338269
  61. Chemical properties of streptococcal proteinase and its zymogen.
    J Biol Chem. 1963 Jan;238:251-6 PMID: 13931033
  62. Type M12 protein from Streptococcus pyogenes is a receptor for IgG3.
    J Immunol. 1993 Mar 15;150(6):2332-40 PMID: 7680689
  63. Structure of the carbohydrate units of IgA1 immunoglobulin. I. Composition, glycopeptide isolation, and structure of the asparagine-linked oligosaccharide units.
    J Biol Chem. 1974 Nov 25;249(22):7260-9 PMID: 4436308
  64. Streptococcal cysteine proteinase releases kinins: a virulence mechanism.
    J Exp Med. 1996 Aug 1;184(2):665-73 PMID: 8760820
  65. Identification of distinct endoglycosidase (endo) activities in Flavobacterium meningosepticum: endo F1, endo F2, and endo F3. Endo F1 and endo H hydrolyze only high mannose and hybrid glycans.
    J Biol Chem. 1991 Jan 25;266(3):1646-51 PMID: 1899092
  66. Streptococcal infections of skin and soft tissues.
    N Engl J Med. 1996 Jan 25;334(4):240-5 PMID: 8532002
  67. Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins.
    J Biol Chem. 1995 Apr 28;270(17):9862-7 PMID: 7730368
  68. Protein H--a bacterial surface protein with affinity for both immunoglobulin and fibronectin type III domains.
    EMBO J. 1995 Apr 18;14(8):1674-9 PMID: 7737120
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/20.12.3046
Published
2001-06-15
Pages
3046-55
Language
English
Region
England
NLM ID
8208664
PMCID
PMC150189
Subset
IM
Grants
NIAID NIH HHS · AI38406 · United States
External Links
PubMed source DOI: 10.1093/emboj/20.12.3046 PMC Full Text View journal details
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