Bacteriocin-producing strains of inhibit adhesion of to extracellular matrix: quantitative insight and implications in antibacterial therapy Free

Abstract

In the present study, the adhesion of bacteriocin-producing probiotic strains of onto extracellular matrix (ECM) proteins such as collagen and mucin and their potential to prevent pathogen invasion onto the ECM was ascertained. Fluorescence-based assays indicated that strains CRA21, CRA38 and CRA52 displayed considerable adhesion to ECM molecules, which was comparable to the probiotic GG. Flow cytometry-based quantitative assessment of the adhesion potential suggested that CRA21 exhibited superior adhesion onto the ECM as compared with other lactic acid bacteria strains. Furthermore, fluorescence-based assays suggested that the highest inhibition of adhesion onto collagen and mucin by bacteriocin-producing strains was observed in the exclusion mode as compared with the competition and displacement modes. This observation was supported by the higher binding affinity ( ) for the ECM exhibited by the strains as compared with . Interestingly, a crude plantaricin A extract from food isolates of displayed potent antibacterial activity on ECM-adhered cells. It is envisaged that the isolates displaying bacteriocinogenic and ECM-adhering traits can perhaps be explored to develop safe antibacterial therapeutic agents.

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2015-12-01
2024-03-28
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References

  1. Acton D. S., Tempelmans Plat-Sinnige M. J., van Wamel W., de Groot N., van Belkum A. 2009; Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact?. Eur J Clin Microbiol Infect Dis 28:115–127 [View Article][PubMed]
    [Google Scholar]
  2. Alander M., Satokari R., Korpela R., Saxelin M., Vilpponen-Salmela T., Mattila-Sandholm T., von Wright A. 1999; Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol 65:351–354[PubMed]
    [Google Scholar]
  3. Begley M., Hill C., Gahan C. G. M. 2006; Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72:1729–1738 [View Article][PubMed]
    [Google Scholar]
  4. Bernbom N., Jelle B., Brogren C. H., Vogensen F. K., Nørrung B., Licht T. R. 2009; Pediocin PA-1 and a pediocin producing Lactobacillus plantarum strain do not change the HMA rat microbiota. Int J Food Microbiol 130:251–257 [View Article][PubMed]
    [Google Scholar]
  5. Bhalla A., Aron D. C., Donskey C. J. 2007; Staphylococcus aureus intestinal colonization is associated with increased frequency of S. aureus on skin of hospitalized patients. BMC Infect Dis 7:105–112 [View Article][PubMed]
    [Google Scholar]
  6. Calasso M., Di Cagno R., De Angelis M., Campanella D., Minervini F., Gobbetti M. 2013; Effects of the peptide pheromone plantaricin A and cocultivation with Lactobacillus sanfranciscensis DPPMA174 on the exoproteome and the adhesion capacity of Lactobacillus plantarum DC400. Appl Environ Microbiol 79:2657–2669 [View Article][PubMed]
    [Google Scholar]
  7. Collado M. C., Meriluoto J., Salminen S. 2007; Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett Appl Microbiol 45:454–460 [View Article][PubMed]
    [Google Scholar]
  8. Coolbear T., Crow V., Harnett J., Harvey S., Holland R., Martley F. 2008; Developments in cheese microbiology in New Zealand - use of starter and non-starter lactic acid bacteria and their enzymes in determining flavour. Int Dairy J 18:705–713 [View Article]
    [Google Scholar]
  9. Cotter P. D., Hill C., Ross R. P. 2005; Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788 [View Article][PubMed]
    [Google Scholar]
  10. Cotter P. D., Ross R. P., Hill C. 2013; Bacteriocins - a viable alternative to antibiotics?. Nat Rev Microbiol 11:95–105 [View Article][PubMed]
    [Google Scholar]
  11. De Vries M. C., Vaughan E. E., Kleerebezem M., De Vos W. M. 2006; Lactobacillus plantarum - survival, functional and potential probiotic properties in the human intestinal tract. Int Dairy J 16:1018–1028 [View Article]
    [Google Scholar]
  12. Doron S., Snydman D. R., Gorbach S. L. 2005; Lactobacillus GG: bacteriology and clinical applications. Gastroenterol Clin North Am 34:483–498 [View Article][PubMed]
    [Google Scholar]
  13. Drider D., Fimland G., Héchard Y., McMullen L. M., Prévost H. 2006; The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564–582 [View Article][PubMed]
    [Google Scholar]
  14. Elliott S. N., Buret A., McKnight W., Miller M. J. S., Wallace J. L. 1998; Bacteria rapidly colonize and modulate healing of gastric ulcers in rats. Am J Physiol 275:G425–G432[PubMed]
    [Google Scholar]
  15. Flemming K., Ackermann G. 2007; Prevalence of enterotoxin producing Staphylococcus aureus in stools of patients with nosocomial diarrhea. Infection 35:356–358 [View Article][PubMed]
    [Google Scholar]
  16. Foster T. J., Geoghegan J. A., Ganesh V. K., Höök M. 2014; Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus . Nat Rev Microbiol 12:49–62 [View Article][PubMed]
    [Google Scholar]
  17. Fuller M. E., Streger S. H., Rothmel R. K., Mailloux B. J., Hall J. A., Onstott T. C., Fredrickson J. K., Balkwill D. L., DeFlaun M. F. 2000; Development of a vital fluorescent staining method for monitoring bacterial transport in subsurface environments. Appl Environ Microbiol 66:4486–4496 [View Article][PubMed]
    [Google Scholar]
  18. Gopal P. K., Prasad J., Smart J., Gill H. S. 2001; In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli . Int J Food Microbiol 67:207–216 [View Article][PubMed]
    [Google Scholar]
  19. Gries D. M., Pultz N. J., Donskey C. J. 2005; Growth in cecal mucus facilitates colonization of the mouse intestinal tract by methicillin-resistant Staphylococcus aureus . J Infect Dis 192:1621–1627 [View Article][PubMed]
    [Google Scholar]
  20. Guarner F., Malagelada J. R. 2003; Gut flora in health and disease. Lancet 361:512–519 [View Article][PubMed]
    [Google Scholar]
  21. Hansen U., Hussain M., Villone D., Herrmann M., Robenek H., Peters G., Sinha B., Bruckner P. 2006; The anchorless adhesin Eap (extracellular adherence protein) from Staphylococcus aureus selectively recognizes extracellular matrix aggregates but binds promiscuously to monomeric matrix macromolecules. Matrix Biol 25:252–260 [View Article][PubMed]
    [Google Scholar]
  22. Jagannath A., Ramesh A., Ramesh M. N., Chandrashekar A., Varadaraj M. C. 2001; Predictive model for the behaviour of Listeria monocytogenes Scott A in Shrikhand, prepared with a biopreservative pediocin K7. Food Microbiol 18:335–343 [View Article]
    [Google Scholar]
  23. Jones R. J., Hussein H. M., Zagorec M., Brightwell G., Tagg J. R. 2008; Isolation of lactic acid bacteria with inhibitory activity against pathogens and spoilage organisms associated with fresh meat. Food Microbiol 25:228–234 [View Article][PubMed]
    [Google Scholar]
  24. Lebeer S., Vanderleyden J., De Keersmaecker S. C. 2008; Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764 [View Article][PubMed]
    [Google Scholar]
  25. Lebeer S., Vanderleyden J., De Keersmaecker S. C. J. 2010; Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 8:171–184 [View Article][PubMed]
    [Google Scholar]
  26. Lee Y. K., Lim C. Y., Teng W. L., Ouwehand A. C., Tuomola E. M., Salminen S. 2000; Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells and their competition with enterobacteria. Appl Environ Microbiol 66:3692–3697 [View Article][PubMed]
    [Google Scholar]
  27. Lee Y. K., Puong K. Y., Ouwehand A. C., Salminen S. 2003; Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J Med Microbiol 52:925–930 [View Article][PubMed]
    [Google Scholar]
  28. Lee Y. K., Ho P. S., Low C. S., Arvilommi H., Salminen S. 2004; Permanent colonization by Lactobacillus casei is hindered by the low rate of cell division in mouse gut. Appl Environ Microbiol 70:670–674 [View Article][PubMed]
    [Google Scholar]
  29. Leroy F., De Vuyst L. 2004; Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67–78 [View Article]
    [Google Scholar]
  30. Lorca G., Torino M. I., Font de Valdez G., Ljungh A,A. 2002; Lactobacilli express cell surface proteins which mediate binding of immobilized collagen and fibronectin. FEMS Microbiol Lett 206:31–37 [View Article][PubMed]
    [Google Scholar]
  31. McGuckin M. A., Lindén S. K., Sutton P., Florin T. H. 2011; Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265–278 [View Article][PubMed]
    [Google Scholar]
  32. Millette M., Cornut G., Dupont C., Shareck F., Archambault D., Lacroix M. 2008; Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl Environ Microbiol 74:1997–2003 [View Article][PubMed]
    [Google Scholar]
  33. Miyoshi Y., Okada S., Uchimura T., Satoh E. 2006; A mucus adhesion promoting protein, MapA, mediates the adhesion of Lactobacillus reuteri to Caco-2 human intestinal epithelial cells. Biosci Biotechnol Biochem 70:1622–1628 [View Article][PubMed]
    [Google Scholar]
  34. Mukherjee S., Singh A. K., Adhikari M. D., Ramesh A. 2013; Quantitative appraisal of the probiotic attributes and in vitro adhesion potential of anti-listerial bacteriocin-producing lactic acid bacteria. Probiotics Antimicrob Proteins 5:99–109 [View Article]
    [Google Scholar]
  35. Muñoz-Provencio D., Llopis M., Antolín M., de Torres I., Guarner F., Pérez-Martínez G., Monedero V. 2009; Adhesion properties of Lactobacillus casei strains to resected intestinal fragments and components of the extracellular matrix. Arch Microbiol 191:153–161 [View Article][PubMed]
    [Google Scholar]
  36. O'Callaghan J., Buttó L. F., MacSharry J., Nally K., O'Toole P. W. 2012; Influence of adhesion and bacteriocin production by Lactobacillus salivarius on the intestinal epithelial cell transcriptional response. Appl Environ Microbiol 78:5196–5203 [View Article][PubMed]
    [Google Scholar]
  37. O'Connor P. M., Ross R. P., Hill C., Cotter P. D. 2015; Antimicrobial antagonists against food pathogens: a bacteriocin perspective. Curr Opin Food Sci 2:51–57 [View Article]
    [Google Scholar]
  38. O'Shea E. F., Cotter P. D., Stanton C., Ross R. P., Hill C. 2012; Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol 152:189–205 [View Article][PubMed]
    [Google Scholar]
  39. Ouwehand A. C., Salminen S. 2003; In vitro adhesion assays for probiotics and their in vivo relevance: a review. Microb Ecol Health Dis 15:175–184 [View Article]
    [Google Scholar]
  40. Ouwehand A. C., Tuomola E. M., Tölkkö S., Salminen S. 2001; Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. Int J Food Microbiol 64:119–126 [View Article][PubMed]
    [Google Scholar]
  41. Ouwehand A. C., Salminen S., Isolauri E. 2002; Probiotics: an overview of beneficial effects. Antonie van Leeuwenhoek 82:279–289 [View Article][PubMed]
    [Google Scholar]
  42. Pagnini C., Saeed R., Bamias G., Arseneau K. O., Pizarro T. T., Cominelli F. 2010; Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci U S A 107:454–459 [View Article][PubMed]
    [Google Scholar]
  43. Preidis G. A., Hill C., Guerrant R. L., Ramakrishna B. S., Tannock G. W., Versalovic J. 2011 8–14, 14.e9. Probiotics, enteric and diarrheal diseases, and global health. Gastroenterology 140: [CrossRef]
    [Google Scholar]
  44. Rastall R. A., Gibson G. R., Gill H. S., Guarner F., Klaenhammer T. R., Pot B., Reid G., Rowland I. R., Sanders M. E. 2005; Modulation of the microbial ecology of the human colon by probiotics, prebiotics and synbiotics to enhance human health: an overview of enabling science and potential applications. FEMS Microbiol Ecol 52:145–152 [View Article][PubMed]
    [Google Scholar]
  45. Reid G., Burton J. 2002; Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect 4:319–324 [View Article][PubMed]
    [Google Scholar]
  46. Saxelin M., Tynkkynen S., Mattila-Sandholm T., de Vos W. M. 2005; Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 16:204–211 [View Article][PubMed]
    [Google Scholar]
  47. Shanahan F. 2010; Probiotics in perspective. Gastroenterology 139:1808–1812 [View Article][PubMed]
    [Google Scholar]
  48. Singh A. K., Ramesh A. 2008; Succession of dominant and antagonistic lactic acid bacteria in fermented cucumber: insights from a PCR-based approach. Food Microbiol 25:278–287 [View Article][PubMed]
    [Google Scholar]
  49. Singh A. K., Ramesh A. 2009; Evaluation of a facile method of template DNA preparation for PCR-based detection and typing of lactic acid bacteria. Food Microbiol 26:504–513 [View Article][PubMed]
    [Google Scholar]
  50. Singh A. K., Mukherjee S., Adhikari M. D., Ramesh A. 2012a; Fluorescence-based comparative evaluation of bactericidal potency and food application potential of antilisterial bacteriocin produced by lactic acid bacteria isolated from indigenous samples. Probiotics Antimicrob Proteins 4:122–132 [View Article]
    [Google Scholar]
  51. Singh B., Fleury C., Jalalvand F., Riesbeck K. 2012b; Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 36:1122–1180 [View Article][PubMed]
    [Google Scholar]
  52. Vélez M. P., De Keersmaecker S. C., Vanderleyden J. 2007; Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol Lett 276:140–148 [View Article][PubMed]
    [Google Scholar]
  53. Vesterlund S., Paltta J., Karp M., Ouwehand A. C. 2005; Adhesion of bacteria to resected human colonic tissue: quantitative analysis of bacterial adhesion and viability. Res Microbiol 156:238–244 [View Article][PubMed]
    [Google Scholar]
  54. Vesterlund S., Karp M., Salminen S., Ouwehand A. C. 2006; Staphylococcus aureus adheres to human intestinal mucus but can be displaced by certain lactic acid bacteria. Microbiology 152:1819–1826 [View Article][PubMed]
    [Google Scholar]
  55. Walter J. 2008; Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74:4985–4996 [View Article][PubMed]
    [Google Scholar]
  56. Yadav A. K., Tyagi A., Kaushik J. K., Saklani A. C., Grover S., Batish V. K. 2013; Role of surface layer collagen binding protein from indigenous Lactobacillus plantarum 91 in adhesion and its anti-adhesion potential against gut pathogen. Microbiol Res 168:639–645 [View Article][PubMed]
    [Google Scholar]
  57. Yan H., Yi H., Xia L., Zhan Z., He W., Cao J., Yang P.-C., Liu Z. 2014; Staphylococcal enterotoxin B suppresses Alix and compromises intestinal epithelial barrier functions. J Biomed Sci 21:29–35 [View Article][PubMed]
    [Google Scholar]
  58. Zhou J. S., Gill H. S. 2005; Immunostimulatory probiotic Lactobacillus rhamnosus HN001 and Bifidobacterium lactis HN019 do not induce pathological inflammation in mouse model of experimental autoimmune thyroiditis. Int J Food Microbiol 103:97–104 [View Article][PubMed]
    [Google Scholar]
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