1887

Abstract

The interaction with the host plasminogen/plasmin system represents a novel component in the molecular cross-talk between bifidobacteria and human host. Here, we demonstrated that the plasminogen-binding bifidobacterial species , , and share the key glycolytic enzyme enolase as a surface receptor for human plasminogen. Enolase was visualized on the cell surface of the model strain BI07. The His-tagged recombinant protein showed a high affinity for human plasminogen, with an equilibrium dissociation constant in the nanomolar range. By site-directed mutagenesis we demonstrated that the interaction between the BI07 enolase and human plasminogen involves an internal plasminogen-binding site homologous to that of pneumococcal enolase. According to our data, the positively charged residues Lys-251 and Lys-255, as well as the negatively charged Glu-252, of the BI07 enolase are crucial for plasminogen binding. Acting as a human plasminogen receptor, the bifidobacterial surface enolase is suggested to play an important role in the interaction process with the host.

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2009-10-01
2020-10-24
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. 1990; Basic local alignment search tool. J Mol Biol215:403–410
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402
    [Google Scholar]
  3. Antikainen J., Kuparinen V., Lähteenmäki K., Korhonen T. K.. 2007a; Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol Med Microbiol51:526–534
    [Google Scholar]
  4. Antikainen J., Hurmalainen V., Lähteenmäki K., Korhonen T. K.. 2007b; pH-dependent association of enolase and GAPDH of Lactobacillus crispatus with the cell wall and lipoteichoic acid. J Bacteriol189:4539–4543
    [Google Scholar]
  5. Bergmann S., Hammerschmidt S.. 2007; Fibrinolysis and host response in bacterial infections. Thromb Haemost98:512–520
    [Google Scholar]
  6. Bergmann S., Rohde M., Chhatwal G. S., Hammerschmidt S.. 2001; α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol40:1273–1287
    [Google Scholar]
  7. 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 Microbiol49:411–423
    [Google Scholar]
  8. 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 Haemost94:304–311
    [Google Scholar]
  9. Boël G., Pichereau V., Mijakovic I., Mazé A., Poncet S., Gilet S., Giard J. C., Hartke A., Auffray Y., Deutscher J.. 2004; Is 2-phosphoglycerate-dependent automodification of bacterial enolases implicated in their export?. J Mol Biol337:485–496
    [Google Scholar]
  10. 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 Bacteriol189:5929–5936
    [Google Scholar]
  11. Candela M., Miccoli G., Bergmann S., Turroni S., Vitali B., Hammerschmidt S., Brigidi P.. 2008; Plasminogen-dependent proteolytic activity in Bifidobacterium lactis. Microbiology154:2457–2462
    [Google Scholar]
  12. Castaldo C., Vastano V., Siciliano R. A., Candela M., Vici M., Muscariello L., Marasco R., Sacco M.. 2009; Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb Cell Fact8:14
    [Google Scholar]
  13. Claverys J. P., Havarstein L. S.. 2007; Cannibalism and fratricide: mechanisms and raisons d'être. Nat Rev Microbiol5:219–229
    [Google Scholar]
  14. Collen D., Verstraete M.. 1975; Molecular biology of human plasminogen. II. Metabolism in physiological and some pathological conditions in man. Thromb Diath Haemorrh34:403–408
    [Google Scholar]
  15. Crowe J. D., Sievwright I. K., Auld G. C., Moore N. R., Gow N. A., Booth N. A.. 2003; Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol Microbiol47:1637–1651
    [Google Scholar]
  16. Cuff J. A., Clamp M. E., Siddiqui A. S., Finlay M., Barton G. J.. 1998; JPRED: a consensus secondary structure prediction server. Bioinformatics14:892–893
    [Google Scholar]
  17. Derbise A., Song Y. P., Parikh S., Fischetti V. A., Pancholi V.. 2004; Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect Immun72:94–105
    [Google Scholar]
  18. Ehinger S., Schubert W. D., Bergmann S., Hammerschmidt S., Heinz D. W.. 2004; Plasmin(ogen)-binding alpha-enolase from Streptococcus pneumoniae: crystal structure and evaluation of plasmin(ogen)-binding sites. J Mol Biol343:997–1005
    [Google Scholar]
  19. Esgleas M., Li Y., Hancock M. A., Harel J., Dubreuil J. D., Gottschalk M.. 2008; Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology154:2668–2679
    [Google Scholar]
  20. Guarner F., Malagelada J. R.. 2003; Gut flora in health and disease. Lancet361:512–519
    [Google Scholar]
  21. Hurmalainen V., Edelman S., Antikainen J., Baumann M., Lähteenmäki K., Korhonen T. K.. 2007; Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology153:1112–1122
    [Google Scholar]
  22. Jeffery C. J.. 1999; Moonlighting proteins. Trends Biochem Sci24:8–11
    [Google Scholar]
  23. Klijn A., Mercenier A., Arigoni F.. 2005; Lessons from the genomes of bifidobacteria. FEMS Microbiol Rev29:491–509
    [Google Scholar]
  24. 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 Bacteriol189:3246–3255
    [Google Scholar]
  25. Kolberg J., Aase A., Bergmann S., Herstad T. K., Rødal G., Frank R., Rohde M., Hammerschmidt S.. 2006; Streptococcus pneumoniae enolase is important for plasminogen binding despite low abundance of enolase protein on the bacterial cell surface. Microbiology152:1307–1317
    [Google Scholar]
  26. Lähteenmäki K., Edelman S., Korhonen T. K.. 2005; Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol13:79–85
    [Google Scholar]
  27. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M.. 1993; PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallograph26:283–291
    [Google Scholar]
  28. Lee J. H., Kang H. K., Moon Y. H., Cho D. L., Kim D., Choe J. Y., Honzatko R., Robyt J. F.. 2006; Cloning, expression and characterization of an extracellular enolase from Leuconostoc mesenteroides. FEMS Microbiol Lett259:240–248
    [Google Scholar]
  29. Marti-Renom M. A., Stuart A. C., Fiser A., Sanchez R., Melo F., Sali A.. 2000; Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct29:291–325
    [Google Scholar]
  30. Pancholi V.. 2001; Multifunctional α-enolase: its role in diseases. Cell Mol Life Sci58:902–920
    [Google Scholar]
  31. Pancholi V., Chhatwal G. S.. 2003; Housekeeping enzymes as virulence factors for pathogens. Int J Med Microbiol293:391–401
    [Google Scholar]
  32. Pancholi V., Fischetti V. A.. 1998; Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem273:14503–14515
    [Google Scholar]
  33. Parkkinen J., Korhonen T. K.. 1989; Binding of plasminogen to Escherichia coli adhesion proteins. FEBS Lett250:437–440
    [Google Scholar]
  34. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., Meng E. C., Ferrin T. E.. 2004; UCSF chimera – a visualization system for exploratory research and analysis. J Comput Chem25:1605–1612
    [Google Scholar]
  35. Redlitz A., Fowler B. J., Plow E. F., Miles L. A.. 1995; The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem227:407–415
    [Google Scholar]
  36. Saksela O., Rifkin D. B.. 1988; Cell-associated plasminogen activation: regulation and physiological functions. Annu Rev Cell Biol4:93–126
    [Google Scholar]
  37. 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 Chem281:25965–25971
    [Google Scholar]
  38. 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 Bacteriol189:1435–1440
    [Google Scholar]
  39. 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. Proteomics4:2991–3006
    [Google Scholar]
  40. Schell M. A., Karmirantzou M., Snel B., Vilanova D., Berger B., Pessi G., Zwahlen M. C., Desire F., Bork P.. other authors 2002; The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A99:14422–14427
    [Google Scholar]
  41. Shevchenko A., Wilm M., Vorm O., Mann M.. 1996; Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem68:850–858
    [Google Scholar]
  42. 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 Infect7:9–18
    [Google Scholar]
  43. Thompson J. D., Higgins D. G., Gibson T. J.. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res22:4673–4680
    [Google Scholar]
  44. Vassalli J. D., Sappino A. P., Belin D.. 1991; The plasminogen activator/plasmin system. J Clin Invest88:1067–1072
    [Google Scholar]
  45. Ventura M., O'Connell-Motherway M., Leahy S., Moreno-Munoz J. A., Fitzgerald G. F., van Sinderen D.. 2007; From bacterial genome to functionality; case bifidobacteria. Int J Food Microbiol120:2–12
    [Google Scholar]
  46. 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 Microbiol7:61–71
    [Google Scholar]
  47. Willard L., Ranjan A., Zhang H., Monzavi H., Boyko R. F., Sykes B. D., Wishart D. S.. 2003; VADAR: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res31:3316–3319
    [Google Scholar]
  48. Zambelli B., Turano P., Musiani F., Neyroz P., Ciurli S.. 2009; Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation. Proteins74:222–239
    [Google Scholar]
  49. 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 Haemost87:493–501
    [Google Scholar]
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