1887

Microbiology Society logo

Volume 156, Issue 6

DnaK from subsp. is a surface-exposed human plasminogen receptor upregulated in response to bile salts Free

Abstract

subsp. lives in the gastrointestinal tract of most mammals, including humans. Recently, for the probiotic strain subsp. BI07, a dose-dependent plasminogen-binding activity was demonstrated and five putative plasminogen-binding proteins were identified. Here we investigated the role of surface DnaK as a subsp. BI07 plasminogen receptor. DnaK was visualized on the bacterial cell surface by transmission electron microscopy. The His-tagged recombinant DnaK protein showed a high affinity for human plasminogen, with an equilibrium dissociation constant in the nanomolar range. The capability to tolerate physiological concentrations of bile salts is a crucial feature for an intestinal symbiont micro-organism. By proteome analysis we demonstrated that the long-term exposure of subsp. BI07 to bile salts results in the upregulation of important surface plasminogen receptors such as DnaK and enolase. Moreover, adaptation of subsp. BI07 to physiological concentrations of bile salts significantly increased its capacity to interact with the host plasminogen system. By enhancing the bacterial capacity to interact with the host plasminogen, the gut bile environment may facilitate the colonization of the human host by subsp. BI07.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): Anti-Eno, anti-pneumococcal enolase antiserum , BSH, bile salt hydrolase , EACA, ϵ-aminocaproic acid , GIT, gastrointestinal tract , PA, plasminogen activator(s) , Plg, plasminogen and uPA, urokinase plasminogen activator
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.038307-0
2010-06-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/6/1609.html?itemId=/content/journal/micro/10.1099/mic.0.038307-0&mimeType=html&fmt=ahah

References

  1. Barrangou R., Briczinski E. P., Traeger L. L., Loquasto J. R., Richards M., Horvath P., Coute-Monvoisin A. C., Leyer G., Rendulic S. other authors 2009; Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J Bacteriol 191:4144–4151
     [Google Scholar]
  2. Bergmann S., Hammerschmidt S. 2007; Fibrinolysis and host response in bacterial infections. Thromb Haemost 98:512–520
     [Google Scholar]
  3. Bergmann S., Wild D., Diekmann O., Frank R., Bracht D., Chhatwal G. S., Hammerschmidt S. 2003; Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumoniae. Mol Microbiol 49:411–423
     [Google Scholar]
  4. Bergmann S., Rohde M., Preissner K. T., Hammerschmidt S. 2005; The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration. Thromb Haemost 94:304–311
     [Google Scholar]
  5. Bernstein H., Payne C. M., Bernstein C., Schneider J., Beard S. E., Crowley C. L. 1999; Activation of the promoters of genes associated with DNA damage, oxidative stress, ER stress, and protein malfolding by the bile salt, deoxycholate. Toxicol Lett 108:37–46
     [Google Scholar]
  6. Bukau B., Horwich A. L. 1998; The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366
     [Google Scholar]
  7. Candela M., Bergmann S., Vici M., Vitali B., Turroni S., Eikmanns B. J., Hammerschmidt S., Brigidi P. 2007; Binding of human plasminogen to Bifidobacterium. J Bacteriol 189:5929–5936
     [Google Scholar]
  8. Candela M., Fiori J., Dipalo S., Naldi M., Gotti R., Brigidi P. 2008a; Rapid MALDI-TOF-MS analysis in the study of interaction between whole bacterial cells and human target molecules: binding of Bifidobacterium to human plasminogen. J Microbiol Methods 73:276–278
     [Google Scholar]
  9. Candela M., Miccoli G., Bergmann S., Turroni S., Vitali B., Hammerschmidt S., Brigidi P. 2008b; Plasminogen-dependent proteolytic activity in Bifidobacterium lactis. Microbiology 154:2457–2462
     [Google Scholar]
  10. Candela M., Biagi E., Centanni M., Turroni S., Vici M., Musini F., Vitali B., Bergmann S., Hammerschmidt S., Brigidi P. 2009; Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology 155:3294–3303
     [Google Scholar]
  11. Claverys J. P., Havarstein L. S. 2007; Cannibalism and fratricide: mechanisms and raisons d'etre. Nat Rev Microbiol 5:219–229
     [Google Scholar]
  12. Coleman R., Iqbal S., Godfrey P. P., Billington D. 1979; Membranes and bile formation. Composition of several mammalian biles and their membrane-damaging properties. Biochem J 178:201–208
     [Google Scholar]
  13. Collen D., Verstraete M. 1975; Molecular biology of human plasminogen. II. Metabolism in physiological and some pathological conditions in man. Thromb Diath Haemorrh 34:403–408
     [Google Scholar]
  14. Gill S. R., Pop M., Deboy R. T., Eckburg P. B., Turnbaugh P. J., Samuel B. S., Gordon J. I., Relman D. A., Fraser-Liggett C. M., Nelson K. E. 2006; Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359
     [Google Scholar]
  15. Guarner F., Malagelada J. R. 2003; Gut flora in health and disease. Lancet 361:512–519
     [Google Scholar]
  16. Hafkenscheid J. C., Hectors M. P. 1975; An enzymatic method for the determination of the glycine/taurine ratio of conjugated bile acids in bile. Clin Chim Acta 65:67–74
     [Google Scholar]
  17. Hardie K., Williams P. 1998; Introduction: fractionation of bacterial cell envelopes. Methods Microbiol 27:185–190
     [Google Scholar]
  18. Hurmalainen V., Edelman S., Antikainen J., Baumann M., Lähteenmäki K., Korhonen T. K. 2007; Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 153:1112–1122
     [Google Scholar]
  19. Kelly P., Maguire P. B., Bennett M., Fitzgerald D. J., Edwards R. J., Thiede B., Treumann A., Collins J. K., O'Sullivan J. C. other authors 2005; Correlation of probiotic Lactobacillus salivarius growth phase with its cell-wall associated proteome. FEMS Microbiol Lett 252:153–159
     [Google Scholar]
  20. Klijn A., Mercenier A., Arigoni F. 2005; Lessons from the genomes of bifidobacteria. FEMS Microbiol Rev 29:491–509
     [Google Scholar]
  21. Knaust A., Weber M. V., Hammerschmidt S., Bergmann S., Frosch M., Kurzai O. 2007; Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J Bacteriol 189:3246–3255
     [Google Scholar]
  22. Lähteenmäki K., Kuusela P., Korhonen T. K. 2001; Bacterial plasminogen activators and receptors. FEMS Microbiol Rev 25:531–552
     [Google Scholar]
  23. Lähteenmäki K., Edelman S., Korhonen T. K. 2005; Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol 13:79–85
     [Google Scholar]
  24. Ley R. E., Hamady M., Lozupone C., Turnbaugh P. J., Ramey R. R., Bircher J. S., Schlegel M. L., Tucker T. A., Schrenzel M. D. other authors 2008; Evolution of mammals and their gut microbes. Science 320:1647–1651
     [Google Scholar]
  25. Meile L., Ludwig W., Rueger U., Gut C., Kaufmann P., Dasen G., Wenger S., Teuber M. 1997; Bifidobacterium lactis sp. nov., a moderately oxygen tolerant species isolated from fermented milk. Syst Appl Microbiol 20:57–64
     [Google Scholar]
  26. Neish A. S. 2009; Microbes in gastrointestinal health and disease. Gastroenterology 136:65–80
     [Google Scholar]
  27. Parkkinen J., Korhonen T. K. 1989; Binding of plasminogen to Escherichia coli adhesion proteins. FEBS Lett 250:437–440
     [Google Scholar]
  28. Ridlon J. M., Kang D., Hylemon P. B. 2006; Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241–259
     [Google Scholar]
  29. Round J. L., Mazmanian S. K. 2009; The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323
     [Google Scholar]
  30. Ruiz L., Sanchez B., Ruas-Madiedo P., de los Reyes-Gavilan C. G., Margolles A. 2007; Cell-envelope changes in Bifidobacterium animalis ssp. lactis as a response to bile. FEMS Microbiol Lett 274:316–322
     [Google Scholar]
  31. Ruiz L., Coutè Y., Sanchez B., de los Reyes-Gavilan C. G., Sanchez J. C., Margolles A. 2009; The cell-envelop proteome of Bifidobacterium longum in an in vitro bile environment. Microbiology 155:957–967
     [Google Scholar]
  32. Saksela O., Rifkin D. B. 1988; Cell-associated plasminogen activation: regulation and physiological functions. Annu Rev Cell Biol 4:93–126
     [Google Scholar]
  33. Sanchez B., Champomier-Verges M. C., Anglade P., Baraige F., de los Reyes-Gavilan C. G., Margolles A., Zagorec M. 2005; Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J Bacteriol 187:5799–5808
     [Google Scholar]
  34. Sanchez B., Champomier-Verges M. C., Stuer-Lauridsen B., Ruas-Madiedo P., Anglade P., Baraige F., de los Reyes-Gavilan C. G., Johansen E., Zagorec M., Margolles A. 2007; Adaptation and response of Bifidobacterium animalis subsp. lactis to bile: a proteomic and physiological approach. Appl Environ Microbiol 73:6757–6767
     [Google Scholar]
  35. Sanderson-Smith M. L., Walker M. J., Ranson M. 2006; The maintenance of high affinity plasminogen binding by group A streptococcal plasminogen-binding M-like protein is mediated by arginine and histidine residues within the a1 and a2 repeat domains. J Biol Chem 281:25965–25971
     [Google Scholar]
  36. Sanderson-Smith M. L., Dowton M., Ranson M., Walker M. J. 2007; The plasminogen binding group A streptococcal M protein-related protein Prp binds plasminogen via arginine and histidine residues. J Bacteriol 189:1435–1440
     [Google Scholar]
  37. Schaumburg J., Diekmann O., Hagendorff P., Bergmann S., Rohde M., Hammerschmidt S., Jansch L., Wehland J., Karst U. 2004; The cell wall subproteome of Listeria monocytogenes. Proteomics 4:2991–3006
     [Google Scholar]
  38. Sha J., Erova T. E., Alyea R. A., Wang S., Olano J. P., Pancholi V., Chopra A. K. 2009; Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. J Bacteriol 191:3095–3107
     [Google Scholar]
  39. Sijbrandi R., Den Blaauwen T., Tame J. R. H., Oudega B., Luirink J., Otto B. R. 2005; Characterization of an iron-regulated alpha-enolase of Bacteroides fragilis. Microbes Infect 7:9–18
     [Google Scholar]
  40. Stie J., Bruni G., Fox D. 2009; Surface-associated plasminogen binding of Cryptococcus neoformans promotes extracellular matrix invasion. PLoS One 4:e5780
     [Google Scholar]
  41. Turroni F., van Sinderen D., Ventura M. 2009; Bifidobacteria: from ecology to genomics. Front Biosci 14:4673–4684
     [Google Scholar]
  42. Vassalli J. D., Sappino A. P., Belin D. 1991; The plasminogen activator/plasmin system. J Clin Invest 88:1067–1072
     [Google Scholar]
  43. Ventura M., O'Flaherty S., Claesson M. J., Turroni F., Klaenhammer T. R., van Sinderen D., O'Toole P. W. 2009; Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7:61–71
     [Google Scholar]
  44. Xolalpa W., Vallecillo A. J., Lara M., Mendoza-Hernadez G., Comini M., Spallek R., Singh M., Espitia C. 2007; Identification of novel bacterial plasminogen-binding proteins in the human pathogen Mycobacterium tuberculosis. Proteomics 7:3332–3341
     [Google Scholar]
  45. Zhang L., Seiffert D., Fowler B. J., Jenkins G. R., Thinnes T. C., Loskutoff D. J., Parmer R. J., Miles L. A. 2002; Plasminogen has a broad extrahepatic distribution. Thromb Haemost 87:493–501
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.038307-0
Loading
DnaK from Bifidobacterium animalis subsp. lactis is a surface-exposed human plasminogen receptor upregulated in response to bile salts
Microbiology 156, 1609 (2010); https://doi.org/10.1099/mic.0.038307-0
/content/journal/micro/10.1099/mic.0.038307-0
/content/journal/micro/10.1099/mic.0.038307-0
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