Identification of binding sites of Lactobacillus plantarum enolase involved in the interaction with human plasminogen

Microbiological Research

Volumn 168, Issue 2, 2013, Pages 65-72

  Vastano, Valeria ^a   Capri, Ugo ^a   Candela, Marco ^b   Siciliano, Rosa Anna ^c   Russo, Luigi ^d   Renda, Mario ^a   Sacco, Margherita ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c CNR   (Italy)

^d MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Adhesins; Enolase; Lactobacillus plantarum; Plasminogen; Probiotics

Indexed keywords

ADHESINS; ENOLASE; LACTOBACILLUS PLANTARUM; PLASMINOGEN; PROBIOTICS;

BACILLI; CELL MEMBRANES; ENZYME ACTIVITY; PROTEINS;

AMINO ACIDS;

ENOLASE; PLASMIN; PLASMINOGEN; PROBIOTIC AGENT;

AMINO ACID; BACTERIUM; CELL ORGANELLE; ENZYME ACTIVITY; PATHOGEN; PROBIOTICS; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LACTOBACILLUS PLANTARUM; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; BINDING SITES; FIBRINOLYSIN; HUMANS; LACTOBACILLUS PLANTARUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPYRUVATE HYDRATASE; PLASMINOGEN; PROBIOTICS; PROTEIN BINDING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS; LACTOBACILLUS PLANTARUM; STREPTOCOCCUS PNEUMONIAE;

EID: 84872613642     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2012.10.001     Document Type: Article

References (48)

1. Antikainen J., Kuparinen V., Lähteenmäki K., Korhonen T.K. Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol Med Microbiol 2007, 51:526-534.
2. Amdekar S., Dwivedi D., Roy P., Kushwah S., Singh V. Probiotics: multifarious oral vaccine against infectious traumas. FEMS Immunol Med Microbiol 2010, 58:299-306.
3. Bergman S., Wild D., Diekmann O., Frank R., Bracht D., Chhatwal G.S., et al. Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumonie. Mol Microbiol 2003, 49:411-423.
4. Bergman S., Hammerschmidt S. Fibrinolysis and host response in bacterial infections. Thromb Haemost 2007, 98:512-520.
5. Bokarewa M.I., Jin T., Tarkowski A. Staphylococcus aureus: Staphylokinase. Int J Biochem Cell Biol 2006, 38:504-509.
6. Cacace G., Mazzeo M.F., Sorrentino A., Spada V., Malorni A., Siciliano R.A. Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. J Proteomics 2010, 73:2021-2030.
7. Candela M., Miccoli G., Bergman S., Turroni S., Vitali B., Hammerschmidt S., et al. Plasminogen-dependent proteolytic activity in Bifidobacterium lactis. Microbiology 2008, 154:2457-2462.
8. Candela M., Biagi E., Centanni M., Turroni S., Vici M., Musiani F., et al. Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology 2009, 155:3294-3303.
9. Capello M., Ferri-Borgogno S., Capello P., Novelli F. α-Enolase: a promising therapeutic and diagnostic tumor target. FEBS J 2011, 278:1064-1074.
10. Castaldo C., Vastano V., Siciliano R.A., Candela M., Vici M., Muscariello L., et al. Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb Cell Fact 2009, 8:14.
11. Castellino F.J., Ploplis V.A. Structure and function of the plasminogen/plasmin system. Thromb Haemost 2005, 93(2005):647-654.
12. Centanni M., Bergmann S., Turroni S., Hammerschmidt S., Chhatwal G.S., Brigidi P., et al. Tumor necrosis factor alpha modulates the dynamics of the plasminogen-mediated early interaction between Bifidobacterium animalis subsp. lactis and human enterocytes. Appl Environ Microbiol 2012, 78:2465-2469.
13. Chivian D., Kim D.E., Malmstrom L., Bradley P., Robertson T., Murphy P., et al. Automated prediction of CASP-% structures using the Robetta server. Proteins 2003, 53:524-533.
14. Cork A.J., Jergic S., Hammerschmidt S., Kobe B., Pancholi V., Benesch J.L., et al. Defining the structural basis of human plasminogen binding by streptococcal surface enolase. J Biol Chem 2009, 284:17129-17137.
15. Derbise A., Song Y.P., Parikh S., Fischetti V.A., Pancholi V. Role of C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect Immun 2004, 72:94-105.
16. Dian C., Eshaghi S., Urbig T., McSweeney S., Heijbel A., Salbert G., et al. Strategies for the purification and on-column cleavage of glutathione-S-transferase fusion target proteins. J Chromatogr B Analyt Technol Biomed Life Sci 2002, 769:133-144.
17. Du L., Liu F., Huo G. Adhesion capability of the first two domains at N terminus of NP_785232 protein and their interaction with a UV-absorbing components from human mucus. Lett Appl Microbiol 2010, 51:400-405.
18. Ehinger S., Schubert W., Bergmann S., Hammerschmidt S., Heinz D.W. Plasmin(ogen)-binding a-enolase from Streptococcus pneumonia: crystal structure and evaluation of plasmin(ogen)-binding sites. J Mol Biol 2004, 343:997-1005.
19. Ferland C., Flamand N., Davoine F., Chakir J., Laviotette M. Il-16 activates plasminogen-plasmin system and promotes human eosinophil migration into extracellular matrix via CCR3-chemokine-mediated signalling and by modulating CD4 eosinophil expression. J Immunol 2004, 173:4417-4424.
20. Gareau M.G., Sherman P.M., Walker W.A. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 2010, 7:503-514.
21. Ghosh A.K., Jacobs-Lorena M. Surface-expressed enolases of Plasmodium and other pathogens. Mem Inst Oswaldo Cruz 2011, 106:85-90.
22. Gross G., Snel J., Boekhorst J., Smits M.A., Kleerebezem M. Biodiversity of mannose-specific adhesion in Lactobacillus plantarum revisited: strain-specific domain composition of the mannose-adhesin. Benef Microbes 2010, 1:61-66.
23. Heissig B., Ohki M., Ishihara M., Tashiro Y., Nishida C., Gritli I., et al. Contribution of fibrinolytic pathway to hematopoietic regeneration. J Cell Physiol 2009, 221:521-525.
24. Hooper L.V., Gordon J.I. Commensal host-bacterial relationships in the gut. Science 2002, 292:1115-1118.
25. Hurmalainen V., Edelman S., Antikainen J., Baumann M., Lähteenmäki K., Korhonen T.K. Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 2007, 153:1112-1122.
26. Juge N. Microbial adhesins to gastrointestinal mucus. Trends Microbiol 2012, 20:30-39.
27. Kim D.E., Chivian D., Baker D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 2004, 32:W526-W531.
28. Kim J.W., Dang C.V. Multifaced roles of glycolytic enzymes. Trends Biochem Sci 2005, 30:142-150.
29. Kleerebezem M., Vaughan E.E. Probiotics and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 2009, 63:269-290.
30. Knaust A., Weber M.V., Hammerschmidt S., Bergman S., Frosch M., Kurzai O. Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitis. J Bacteriol 2007, 189:3246-3255.
31. Kühnel K., Luisi B.F. Crystal structure of the Escherichia coli RNA degradosome component enolase. J Mol Biol 2001, 313:583-592.
32. Kwaan H.C., McMahon B. The role of plasminogen-plasmin system in cancer. Cancer Treat Res 2009, 148:43-66.
33. Lähteenmäki K., Kuusela P., Korhonen T.K. Bacterial plasminogen activators and receptors. FEMS Microbiol Rev 2001, 25:531-552.
34. Lähteenmäki K., Edelman S., Korhonen T.K. Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol 2005, 13:79-85.
35. Liu Z., Shen T., Chen H., Zhou Y., Zhang P., Ma Y., et al. Functional characterization of MIMP for its adhesion to the intestinal epithelium. Front Biosci 2011, 17:2106-2127.
36. Mölkänen T., Tyynelä J., Helin J., Kalkkinen N., Kuusela P. Enhanced activation of bound plasminogen on Staphylococcus aureus by staphylokinase. FEBS Lett 2002, 517:72-78.
37. Muñoz-Provencio D., Pérez-Martinez G., Monedero V. Characterization of a fibronectin-binding protein from Lactobacillus casei BL23. J Appl Microbiol 2010, 108:1050-1059.
38. Pancholi V. Multifunctional α-enolase: its role in diseases. Cell Mol Life Sci 2001, 58:902-920.
39. Pancholi V., Fischetti V.A. Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem 1998, 273:14503-14515.
40. Ramiah K., van Reenen C.A., Dicks L.M. Surface-bound proteins of Lactobacillus plantarum 423 that contribute to adhesion of Caco-2 cells and their role in competitive exclusion and displacement of Clostridium sporogenes and Enterococcus faecalis. Res Microbiol 2008, 159:470-475.
41. Reid G., Younes J.A., Van der Mei H.C., Gloor G.B., Knight R., Busscher H.J. Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 2011, 9:27-38.
42. Sanchez B., Urdaci M.C. Extracellular proteins from Lactobacillus plantarum BMCM12 prevent adhesion of enteropathogens to mucin. Curr Microbiol 2012, 64:592-596.
43. Schaller J., Gerber S.S. The plasmin-antiplasmin system: structural and functional aspects. Cell Mol Life Sci 2011, 68:785-801.
44. Sha J., Erova T.E., Alyea R.A., Wang S., Olano J.P., Pancholi V., et al. Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. J Bacteriol 2009, 191:3095-3107.
45. Siezen R.J., van Hylckama Vlieg J.E. Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb Cell Fact 2011, 10:S3.
46. Spurbeck R.R., Arvidson C.G. Lactobacillus jensenii surfaced-associated proteins inhibit Neisseria gonorrhoeae adherence to epithelial cells. Infect Immun 2010, 78:3103-3111.
47. Velez M.P., De Keersmaecker S.C., Vanderleyden J. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol Lett 2007, 276:140-148.
48. Ventura M., O'Flaherty S., Claesson M.J., Turroni F., Klaenhammer T.R., van Sinderen D., et al. Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 2009, 7:61-71.