1887

Abstract

Since the late 1980s, a worldwide increase of severe infections has been associated with strains of the M1 serotype, strains which all secrete the streptococcal inhibitor of complement-mediated lysis (SIC). Previous work has shown that SIC blocks complement-mediated haemolysis, inhibits the activity of antibacterial peptides and has affinity for the human plasma proteins clusterin and histidine-rich glycoprotein; the latter is a member of the cystatin protein family. The present work demonstrates that SIC binds to cystatin C, high-molecular-mass kininogen (HK) and low-molecular-mass kininogen, which are additional members of this protein family. The binding sites in HK are located in the cystatin-like domain D3 and the endothelial cell-binding domain D5. Immobilization of HK to cellular structures plays a central role in activation of the human contact system. SIC was found to inhibit the binding of HK to endothelial cells, and to reduce contact activation as measured by prolonged blood clotting time and impaired release of bradykinin. These results suggest that SIC modifies host defence systems, which may contribute to the virulence of strains of the M1 serotype.

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2010-12-01
2019-12-13
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References

  1. Abrahamson, M. ( 1994; ). Cystatins. Methods Enzymol 244, 685–700.
    [Google Scholar]
  2. Abrahamson, M., Barrett, A. J., Salvesen, G. & Grubb, A. ( 1986; ). Isolation of six cysteine proteinase inhibitors from human urine. Their physicochemical and enzyme kinetic properties and concentrations in biological fluids. J Biol Chem 261, 11282–11289.
    [Google Scholar]
  3. Abrahamson, M., Dalboge, H., Olafsson, I., Carlsen, S. & Grubb, A. ( 1988; ). Efficient production of native, biologically active human cystatin C by Escherichia coli. FEBS Lett 236, 14–18.[CrossRef]
    [Google Scholar]
  4. Åkesson, P., Cooney, J., Kishimoto, F. & Björck, L. ( 1990; ). Protein H – a novel IgG binding bacterial protein. Mol Immunol 27, 523–531.[CrossRef]
    [Google Scholar]
  5. Åkesson, P., Schmidt, K. H., Cooney, J. & Björck, L. ( 1994; ). M1 protein and protein H: IgGFc- and albumin-binding streptococcal surface proteins encoded by adjacent genes. Biochem J 300, 877–886.
    [Google Scholar]
  6. Åkesson, P., Sjöholm, A. G. & Björck, L. ( 1996; ). Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J Biol Chem 271, 1081–1088.[CrossRef]
    [Google Scholar]
  7. Auerswald, E. A., Rossler, D., Mentele, R. & Assfalg-Machleidt, I. ( 1993; ). Cloning, expression and characterization of human kininogen domain 3. FEBS Lett 321, 93–97.[CrossRef]
    [Google Scholar]
  8. Ben Nasr, A., Olsén, A., Sjöbring, U., Müller-Esterl, W. & Björck, L. ( 1996; ). Assembly of human contact phase proteins and release of bradykinin at the surface of curli-expressing Escherichia coli. Mol Microbiol 20, 927–935.[CrossRef]
    [Google Scholar]
  9. Ben Nasr, A., Herwald, H., Sjöbring, U., Renne, T., Müller-Esterl, W. & Björck, L. ( 1997; ). Absorption of kininogen from human plasma by Streptococcus pyogenes is followed by the release of bradykinin. Biochem J 326, 657–660.
    [Google Scholar]
  10. Berge, A. & Björck, L. ( 1995; ). Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J Biol Chem 270, 9862–9867.[CrossRef]
    [Google Scholar]
  11. Bhoola, K. D., Figueroa, C. D. & Worthy, K. ( 1992; ). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol Rev 44, 1–80.
    [Google Scholar]
  12. Binks, M. J., Fernie-King, B. A., Seilly, D. J., Lachmann, P. J. & Sriprakash, K. S. ( 2005; ). Attribution of the various inhibitory actions of the streptococcal inhibitor of complement (SIC) to regions within the molecule. J Biol Chem 280, 20120–20125.[CrossRef]
    [Google Scholar]
  13. Colman, R. W. & Schmaier, A. H. ( 1997; ). Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 90, 3819–3843.
    [Google Scholar]
  14. Colman, R. W., Pixley, R. A., Najamunnisa, S., Yan, W., Wang, J., Mazar, A. & McCrae, K. R. ( 1997; ). Binding of high molecular weight kininogen to human endothelial cells is mediated via a site within domains 2 and 3 of the urokinase receptor. J Clin Invest 100, 1481–1487.[CrossRef]
    [Google Scholar]
  15. Curtis, N. ( 1996; ). Invasive group A streptococcal infection. Curr Opin Infect Dis 9, 191–202.[CrossRef]
    [Google Scholar]
  16. de Château, M. & Björck, L. ( 1994; ). Protein PAB, a mosaic albumin-binding bacterial protein representing the first contemporary example of module shuffling. J Biol Chem 269, 12147–12151.
    [Google Scholar]
  17. DeLa Cadena, R. A. & Colman, R. W. ( 1992; ). The sequence HGLGHGHEQQHGLGHGH in the light chain of high molecular weight kininogen serves as a primary structural feature for zinc-dependent binding to an anionic surface. Protein Sci 1, 151–160.
    [Google Scholar]
  18. Egesten, A., Eliasson, M., Johansson, H. M., Olin, A. I., Mörgelin, M., Mueller, A., Pease, J. E., Frick, I. M. & Björck, L. ( 2007; ). The CXC chemokine MIG/CXCL9 is important in innate immunity against Streptococcus pyogenes. J Infect Dis 195, 684–693.[CrossRef]
    [Google Scholar]
  19. Facklam, R. F., Martin, D. R., Lovgren, M., Johnson, D. R., Efstratiou, A., Thompson, T. A., Gowan, S., Kriz, P., Tyrrell, G. J. & other authors ( 2002; ). Extension of the Lancefield classification for group A streptococci by addition of 22 new M protein gene sequence types from clinical isolates: emm103 to emm124. Clin Infect Dis 34, 28–38.[CrossRef]
    [Google Scholar]
  20. Fernie-King, B. A., Seilly, D. J., Davies, A. & Lachmann, P. J. ( 2002; ). Streptococcal inhibitor of complement inhibits two additional components of the mucosal innate immune system: secretory leukocyte proteinase inhibitor and lysozyme. Infect Immun 70, 4908–4916.[CrossRef]
    [Google Scholar]
  21. Fischetti, V. A. ( 1989; ). Streptococcal M protein: molecular design and biological behavior. Clin Microbiol Rev 2, 285–314.
    [Google Scholar]
  22. Frick, I. M., Åkesson, P., Rasmussen, M., Schmidtchen, A. & Björck, L. ( 2003; ). SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J Biol Chem 278, 16561–16566.[CrossRef]
    [Google Scholar]
  23. Frick, I. M., Åkesson, P., Herwald, H., Mörgelin, M., Malmsten, M., Nägler, D. K. & Björck, L. ( 2006; ). The contact system – a novel branch of innate immunity generating antibacterial peptides. EMBO J 25, 5569–5578.[CrossRef]
    [Google Scholar]
  24. Grubb, A. ( 1992; ). Diagnostic value of analysis of cystatin C and protein HC in biological fluids. Clin Nephrol 38 (Suppl. 1), S20–S27.
    [Google Scholar]
  25. Hartas, J. & Sriprakash, K. S. ( 1999; ). Streptococcus pyogenes strains containing emm12 and emm55 possess a novel gene coding for distantly related SIC protein. Microb Pathog 26, 25–33.[CrossRef]
    [Google Scholar]
  26. Hasan, A. A., Cines, D. B., Herwald, H., Schmaier, A. H. & Müller-Esterl, W. ( 1995; ). Mapping the cell binding site on high molecular weight kininogen domain 5. J Biol Chem 270, 19256–19261.[CrossRef]
    [Google Scholar]
  27. Hasan, A. A., Zisman, T. & Schmaier, A. H. ( 1998; ). Identification of cytokeratin 1 as a binding protein and presentation receptor for kininogens on endothelial cells. Proc Natl Acad Sci U S A 95, 3615–3620.[CrossRef]
    [Google Scholar]
  28. Herwald, H., Hasan, A. A., Godovac-Zimmermann, J., Schmaier, A. H. & Müller-Esterl, W. ( 1995; ). Identification of an endothelial cell binding site on kininogen domain D3. J Biol Chem 270, 14634–14642.
    [Google Scholar]
  29. Herwald, H., Collin, M., Müller-Esterl, W. & Björck, L. ( 1996a; ). Streptococcal cysteine proteinase releases kinins: a virulence mechanism. J Exp Med 184, 665–673.[CrossRef]
    [Google Scholar]
  30. Herwald, H., Dedio, J., Kellner, R., Loos, M. & Müller-Esterl, W. ( 1996b; ). Isolation and characterization of the kininogen-binding protein p33 from endothelial cells. Identity with the gC1q receptor. J Biol Chem 271, 13040–13047.[CrossRef]
    [Google Scholar]
  31. Herwald, H., Mörgelin, M., Olsén, A., Rhen, M., Dahlbäck, B., Müller-Esterl, W. & Björck, L. ( 1998; ). Activation of the contact-phase system on bacterial surfaces – a clue to serious complications in infectious diseases. Nat Med 4, 298–302.[CrossRef]
    [Google Scholar]
  32. Herwald, H., Mörgelin, M., Svensson, H. G. & Sjöbring, U. ( 2001; ). Zinc-dependent conformational changes in domain D5 of high molecular mass kininogen modulate contact activation. Eur J Biochem 268, 396–404.[CrossRef]
    [Google Scholar]
  33. Hoe, N. P., Nakashima, K., Lukomski, S., Grigsby, D., Liu, M., Kordari, P., Dou, S. J., Pan, X., Vuopio-Varkila, J. & other authors ( 1999; ). Rapid selection of complement-inhibiting protein variants in group A Streptococcus epidemic waves. Nat Med 5, 924–929.[CrossRef]
    [Google Scholar]
  34. Kapur, V., Majesky, M. W., Li, L. L., Black, R. A. & Musser, J. M. ( 1993a; ). Cleavage of interleukin 1 beta (IL-1 beta) precursor to produce active IL-1 beta by a conserved extracellular cysteine protease from Streptococcus pyogenes. Proc Natl Acad Sci U S A 90, 7676–7680.[CrossRef]
    [Google Scholar]
  35. Kapur, V., Topouzis, S., Majesky, M. W., Li, L. L., Hamrick, M. R., Hamill, R. J., Patti, J. M. & Musser, J. M. ( 1993b; ). A conserved Streptococcus pyogenes extracellular cysteine protease cleaves human fibronectin and degrades vitronectin. Microb Pathog 15, 327–346.[CrossRef]
    [Google Scholar]
  36. Koide, T. & Odani, S. ( 1987; ). Histidine-rich glycoprotein is evolutionarily related to the cystatin superfamily. Presence of two cystatin domains in the N-terminal region. FEBS Lett 216, 17–21.[CrossRef]
    [Google Scholar]
  37. Lukomski, S., Hoe, N. P., Abdi, I., Rurangirwa, J., Kordari, P., Liu, M., Dou, S. J., Adams, G. G. & Musser, J. M. ( 2000; ). Nonpolar inactivation of the hypervariable streptococcal inhibitor of complement gene (sic) in serotype M1 Streptococcus pyogenes significantly decreases mouse mucosal colonization. Infect Immun 68, 535–542.[CrossRef]
    [Google Scholar]
  38. Mangold, M., Siller, M., Roppenser, B., Vlaminckx, B. J., Penfound, T. A., Klein, R., Novak, R., Novick, R. P. & Charpentier, E. ( 2004; ). Synthesis of group A streptococcal virulence factors is controlled by a regulatory RNA molecule. Mol Microbiol 53, 1515–1527.[CrossRef]
    [Google Scholar]
  39. Martin, D. R. & Single, L. A. ( 1993; ). Molecular epidemiology of group A streptococcus M type 1 infections. J Infect Dis 167, 1112–1117.[CrossRef]
    [Google Scholar]
  40. Mason, J. W., Kleeberg, U., Dolan, P. & Colman, R. W. ( 1970; ). Plasma kallikrein and Hageman factor in Gram-negative bacteremia. Ann Intern Med 73, 545–551.[CrossRef]
    [Google Scholar]
  41. Mattsson, E., Herwald, H., Cramer, H., Persson, K., Sjöbring, U. & Björck, L. ( 2001; ). Staphylococcus aureus induces release of bradykinin in human plasma. Infect Immun 69, 3877–3882.[CrossRef]
    [Google Scholar]
  42. Müller-Esterl, W., Johnson, D. A., Salvesen, G. & Barrett, A. J. ( 1988; ). Human kininogens. Methods Enzymol 163, 240–256.
    [Google Scholar]
  43. Musser, J. M. & Krause, R. M. ( 1998; ). The revival of group A streptococcal diseases with a commentary on staphylococcal toxic shock syndrome. In Emerging Infections, pp. 185–218. Edited by Krause, R. M. & Fauci, A.. San Diego. : Academic Press.
    [Google Scholar]
  44. Musser, J. M., Kapur, V., Kanjilal, S., Shah, U., Musher, D. M., Barg, N. L., Johnston, K. H., Schlievert, P. M., Henrichsen, J. & other authors ( 1993; ). Geographic and temporal distribution and molecular characterization of two highly pathogenic clones of Streptococcus pyogenes expressing allelic variants of pyrogenic exotoxin A (Scarlet fever toxin). J Infect Dis 167, 337–346.[CrossRef]
    [Google Scholar]
  45. Oehmcke, S., Shannon, O., von Köckritz-Blickwede, M., Mörgelin, M., Linder, A., Olin, A. I., Björck, L. & Herwald, H. ( 2009; ). Treatment of invasive streptococcal infection with a peptide derived from human high-molecular weight kininogen. Blood 114, 444–451.[CrossRef]
    [Google Scholar]
  46. Persson, K., Mörgelin, M., Lindbom, L., Alm, P., Björck, L. & Herwald, H. ( 2000; ). Severe lung lesions caused by Salmonella are prevented by inhibition of the contact system. J Exp Med 192, 1415–1424.[CrossRef]
    [Google Scholar]
  47. Pixley, R. A., Zellis, S., Bankes, P., DeLa Cadena, R. A., Page, J. D., Scott, C. F., Kappelmayer, J., Wyshock, E. G., Kelly, J. J. & Colman, R. W. ( 1995; ). Prognostic value of assessing contact system activation and factor V in systemic inflammatory response syndrome. Crit Care Med 23, 41–51.[CrossRef]
    [Google Scholar]
  48. Schmaier, A. H. & Colman, R. W. ( 1989; ). Platelet high-molecular-weight kininogen. Methods Enzymol 169, 276–296.
    [Google Scholar]
  49. Stockbauer, K. E., Grigsby, D., Pan, X., Fu, Y. X., Mejia, L. M., Cravioto, A. & Musser, J. M. ( 1998; ). Hypervariability generated by natural selection in an extracellular complement-inhibiting protein of serotype M1 strains of group A Streptococcus. Proc Natl Acad Sci U S A 95, 3128–3133.[CrossRef]
    [Google Scholar]
  50. Tait, J. F. & Fujikawa, K. ( 1987; ). Primary structure requirements for the binding of human high molecular weight kininogen to plasma prekallikrein and factor XI. J Biol Chem 262, 11651–11656.
    [Google Scholar]
  51. van Deuren, M., Brandtzaeg, P. & van der Meer, J. W. ( 2000; ). Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 13, 144–166.[CrossRef]
    [Google Scholar]
  52. Wachtfogel, Y. T., DeLa Cadena, R. A., Kunapuli, S. P., Rick, L., Miller, M., Schultze, R. L., Altieri, D. C., Edgington, T. S. & Colman, R. W. ( 1994; ). High molecular weight kininogen binds to Mac-1 on neutrophils by its heavy chain (domain 3) and its light chain (domain 5). J Biol Chem 269, 19307–19312.
    [Google Scholar]
  53. Wuillemin, W. A., Fijnvandraat, K., Derkx, B. H., Peters, M., Vreede, W., ten Cate, H. & Hack, C. E. ( 1995; ). Activation of the intrinsic pathway of coagulation in children with meningococcal septic shock. Thromb Haemost 74, 1436–1441.
    [Google Scholar]
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