1887

Microbiology Society logo

Volume 157, Issue 7

Interaction of and with the kallikrein–kinin system Open Access

Abstract

Many bacterial pathogens interfere with the contact system (kallikrein–kinin system) in human plasma. Activation of this system has two consequences: cleavage of high-molecular-mass kininogen (HK) resulting in release of the potent proinflammatory peptide bradykinin, and initiation of the intrinsic pathway of coagulation. In this study, two species of the Gram-negative anaerobic commensal organism , namely and , were found to bind HK and fibrinogen, the major clotting protein, from human plasma as shown by immunoelectron microscopy and Western blot analysis. In addition, these species were capable of activating the contact system at its surface leading to a significant prolongation of the intrinsic coagulation time and also to the release of bradykinin. Members of the genus have been known to act as opportunistic pathogens outside the gut, with being the most common isolate from clinical infections, such as intra-abdominal abscesses and bacteraemia. The present results thus provide more insight into how species cause infection.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Funding
This study was supported by the:
  • Swedish Research Council (Award 7480)
  • Foundations of Crafoord, Bergvall and Österlund
  • Royal Physiographic Society
  • Hansa Medical AB
  • Science Foundation Ireland (Award 08/RFP/BMT1596)
  • National Development Plan of Ireland
  • FAS Science Challenge
© 2011 SGM
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.046862-0
2011-07-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/7/2094.html?itemId=/content/journal/micro/10.1099/mic.0.046862-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. ( 1990). Basic local alignment search tool. J Mol Biol 215:403–410[PubMed] [CrossRef]
     [Google Scholar]
  2. Barbasz A., Guevara-Lora I., Rapala-Kozik M., Kozik A. ( 2008). Kininogen binding to the surfaces of macrophages. Int Immunopharmacol 8:211–216 [View Article][PubMed]
     [Google Scholar]
  3. Ben Nasr A. B., Herwald H., Müller-Esterl W., Björck L. ( 1995). Human kininogens interact with M protein, a bacterial surface protein and virulence determinant. Biochem J 305:173–180[PubMed]
     [Google Scholar]
  4. 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 [View Article][PubMed]
     [Google Scholar]
  5. Bhoola K. D., Figueroa C. D., Worthy K. ( 1992). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol Rev 44:1–80[PubMed]
     [Google Scholar]
  6. Björck L. ( 1988). Protein L. A novel bacterial cell wall protein with affinity for IgL chains. J Immunol 140:1194–1197[PubMed]
     [Google Scholar]
  7. Cardoso L. S., Araujo M. I., Góes A. M., Pacífico L. G., Oliveira R. R., Oliveira S. C. ( 2007). Polymyxin B as inhibitor of LPS contamination of Schistosoma mansoni recombinant proteins in human cytokine analysis. Microb Cell Fact 6:1 [View Article][PubMed]
     [Google Scholar]
  8. Dahlbäck B. ( 2000). Blood coagulation. Lancet 355:1627–1632 [View Article][PubMed]
     [Google Scholar]
  9. Emsley J., McEwan P. A., Gailani D. ( 2010). Structure and function of factor XI. Blood 115:2569–2577 [View Article][PubMed]
     [Google Scholar]
  10. Ferreira E. O., de Carvalho J. B., Peixoto R. J., Lobo L. A., Zingalli R. B., Smith C. J., Rocha E. R., Domingues R. M. ( 2009). The interaction of Bacteroides fragilis with components of the human fibrinolytic system. FEMS Immunol Med Microbiol 56:48–55 [View Article][PubMed]
     [Google Scholar]
  11. 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 [View Article][PubMed]
     [Google Scholar]
  12. Frick I. M., Björck L., Herwald H. ( 2007). The dual role of the contact system in bacterial infectious disease. Thromb Haemost 98:497–502[PubMed]
     [Google Scholar]
  13. Goldstein E. J. ( 1996). Anaerobic bacteremia. Clin Infect Dis 23:Suppl. 1S97–S101 [View Article][PubMed]
     [Google Scholar]
  14. Hall J. M. ( 1992). Bradykinin receptors: pharmacological properties and biological roles. Pharmacol Ther 56:131–190 [View Article][PubMed]
     [Google Scholar]
  15. Harris S. L., Jones D. W., Gallimore M. J., Nicholls P. J., Winter M. ( 2005). The antigenic binding site(s) of antibodies to factor XII associated with the antiphospholipid syndrome. J Thromb Haemost 3:969–975 [View Article][PubMed]
     [Google Scholar]
  16. 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 [View Article][PubMed]
     [Google Scholar]
  17. Herwald H., Mörgelin M., Dahlbäck B., Björck L. ( 2003). Interactions between surface proteins of Streptococcus pyogenes and coagulation factors modulate clotting of human plasma. J Thromb Haemost 1:284–291 [View Article][PubMed]
     [Google Scholar]
  18. Houston S., Blakely G. W., McDowell A., Martin L., Patrick S. ( 2010). Binding and degradation of fibrinogen by Bacteroides fragilis and characterization of a 54 kDa fibrinogen-binding protein. Microbiology 156:2516–2526 [View Article][PubMed]
     [Google Scholar]
  19. Imamura T., Potempa J., Travis J. ( 2004). Activation of the kallikrein–kinin system and release of new kinins through alternative cleavage of kininogens by microbial and human cell proteinases. Biol Chem 385:989–996 [View Article][PubMed]
     [Google Scholar]
  20. Imamura T., Tanase S., Szmyd G., Kozik A., Travis J., Potempa J. ( 2005). Induction of vascular leakage through release of bradykinin and a novel kinin by cysteine proteinases from Staphylococcus aureus . J Exp Med 201:1669–1676 [View Article][PubMed]
     [Google Scholar]
  21. Joseph K., Kaplan A. P. ( 2005). Formation of bradykinin: a major contributor to the innate inflammatory response. Adv Immunol 86:159–208 [View Article][PubMed]
     [Google Scholar]
  22. Kalter E. S., van Dijk W. C., Timmerman A., Verhoef J., Bouma B. N. ( 1983). Activation of purified human plasma prekallikrein triggered by cell wall fractions of Escherichia coli and Staphylococcus aureus . J Infect Dis 148:682–691 [View Article][PubMed]
     [Google Scholar]
  23. Kaplan A. P., Silverberg M. ( 1987). The coagulation-kinin pathway of human plasma. Blood 70:1–15[PubMed]
     [Google Scholar]
  24. Karkowska-Kuleta J., Rapala-Kozik M., Kozik A. ( 2009). Fungi pathogenic to humans: molecular bases of virulence of Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus . Acta Biochim Pol 56:211–224[PubMed]
     [Google Scholar]
  25. Kellenberger E., Johansen R., Maeder M., Bohrmann B., Stauffer E., Villiger W. ( 1992). Artefacts and morphological changes during chemical fixation. J Microsc 168:181–201[PubMed] [CrossRef]
     [Google Scholar]
  26. Kislak J. W. ( 1972). The susceptibility of Bacteroides fragilis to 24 antibiotics. J Infect Dis 125:295–299 [View Article][PubMed]
     [Google Scholar]
  27. Krinos C. M., Coyne M. J., Weinacht K. G., Tzianabos A. O., Kasper D. L., Comstock L. E. ( 2001). Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414:555–558 [View Article][PubMed]
     [Google Scholar]
  28. 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 [View Article][PubMed]
     [Google Scholar]
  29. Müller-Esterl W. ( 1989). Kininogens, kinins and kinships. Thromb Haemost 61:2–6[PubMed]
     [Google Scholar]
  30. Nesbitt S. A., Horton M. A. ( 1992). A nonradioactive biochemical characterization of membrane proteins using enhanced chemiluminescence. Anal Biochem 206:267–272 [View Article][PubMed]
     [Google Scholar]
  31. Neville D. M. Jr ( 1971). Molecular weight determination of protein-dodecyl sulfate complexes by gel electrophoresis in a discontinuous buffer system. J Biol Chem 246:6328–6334[PubMed]
     [Google Scholar]
  32. Nord C. E., Olsson-Liljequist B. ( 1981). Resistance to β-lactam antibiotics in Bacteroides species. J Antimicrob Chemother 8:Suppl. D33–42[PubMed] [CrossRef]
     [Google Scholar]
  33. Oehmcke S., Herwald H. ( 2010). Contact system activation in severe infectious diseases. J Mol Med 88:121–126 [View Article][PubMed]
     [Google Scholar]
  34. Patrick S. ( 2002). Bacteroides. Molecular Medical Microbiology1921–1948 Penn C., Hacker J., Pfaller M. A., Sussman M. London: Academic Press; [View Article]
     [Google Scholar]
  35. Patrick S., Blakely G. W., Houston S., Moore J., Abratt V. R., Bertalan M., Cerdeño-Tárraga A. M., Quail M. A., Corton N. et al. ( 2010). Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis . Microbiology 156:3255–3269 [View Article][PubMed]
     [Google Scholar]
  36. 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 [View Article][PubMed]
     [Google Scholar]
  37. Ponjee G. A., Vader H. L., de Wild P. J., Janssen G. W., van der Graaf F. ( 1991). One-step chromogenic equivalent of activated partial thromboplastin time evaluated for clinical application. Clin Chem 37:1235–1244[PubMed]
     [Google Scholar]
  38. Reid J. H., Patrick S. ( 1984). Phagocytic and serum killing of capsulate and non-capsulate Bacteroides fragilis . J Med Microbiol 17:247–257 [View Article][PubMed]
     [Google Scholar]
  39. Risberg B., Andreasson S., Eriksson E. ( 1991). Disseminated intravascular coagulation. Acta Anaesthesiol Scand Suppl 35:Suppl. s9560–71 [View Article][PubMed]
     [Google Scholar]
  40. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M. A., Barrell B. ( 2000). Artemis: sequence visualization and annotation. Bioinformatics 16:944–945 [View Article][PubMed]
     [Google Scholar]
  41. Sóki J., Gal M., Brazier J. S., Rotimi V. O., Urbán E., Nagy E., Duerden B. I. ( 2006). Molecular investigation of genetic elements contributing to metronidazole resistance in Bacteroides strains. J Antimicrob Chemother 57:212–220 [View Article][PubMed]
     [Google Scholar]
  42. Stuardo M., Gonzalez C. B., Nualart F., Boric M., Corthorn J., Bhoola K. D., Figueroa C. D. ( 2004). Stimulated human neutrophils form biologically active kinin peptides from high and low molecular weight kininogens. J Leukoc Biol 75:631–640 [View Article][PubMed]
     [Google Scholar]
  43. Szöke I., Pascu C., Nagy E., Ljung A., Wadström T. ( 1996). Binding of extracellular matrix proteins to the surface of anaerobic bacteria. J Med Microbiol 45:338–343 [View Article][PubMed]
     [Google Scholar]
  44. Thornton R. F., Kagawa T. F., O'Toole P. W., Cooney J. C. ( 2010). The dissemination of C10 cysteine protease genes in Bacteroides fragilis by mobile genetic elements. BMC Microbiol 10:122 [View Article][PubMed]
     [Google Scholar]
  45. Tzianabos A. O., Onderdonk A. B., Rosner B., Cisneros R. L., Kasper D. L. ( 1993). Structural features of polysaccharides that induce intra-abdominal abscesses. Science 262:416–419 [View Article][PubMed]
     [Google Scholar]
  46. Wexler H. M. ( 2007). Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621 [View Article][PubMed]
     [Google Scholar]
  47. Yokogawa K., Kawata S., Nishimura S., Ikeda Y., Yoshimura Y. ( 1974). Mutanolysin, bacteriolytic agent for cariogenic Streptococci: partial purification and properties. Antimicrob Agents Chemother 6:156–165[PubMed] [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.046862-0
Loading
Interaction of Bacteroides fragilis and Bacteroides thetaiotaomicron with the kallikrein–kinin system
Microbiology 157, 2094 (2011); https://doi.org/10.1099/mic.0.046862-0
/content/journal/micro/10.1099/mic.0.046862-0
/content/journal/micro/10.1099/mic.0.046862-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error