Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells

Cellular Microbiology

Volumn 9, Issue 2, 2007, Pages 356-367

  Johnson henry, Kathene C ^a   Hagen, Karen E ^b   Gordonpour, Mahsa ^a   Tompkins, Thomas A ^b   Sherman, Philip M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b LALLEMAND SAS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL MEMBRANE PROTEIN; SURFACE LAYER PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; CELL FUNCTION; CELL POLARITY; CELL VIABILITY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EPITHELIUM CELL; ESCHERICHIA COLI O157; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; LACTOBACILLUS HELVETICUS; MONOLAYER CULTURE; NONHUMAN; PATHOGENESIS; PHASE CONTRAST MICROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL LINE; EPITHELIAL CELLS; ESCHERICHIA COLI O157; LACTOBACILLUS HELVETICUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LACTOBACILLUS HELVETICUS;

EID: 33846253580     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00791.x     Document Type: Article

References (55)

1. Amieva, M., and Vogelmann, R. (2004) Epithelial cells and pathogens -the Odyssey® System brings light into the darkness. Tight junction barrier function in epithelial cells. [WWW document]. URL http://www.licor.com/bio/PDF/EpithelialCells.pdf.
2. Åvall-Jääskelainen, S., and Palva, A. (2005) Lactobacillus surface layers and their applications. FEMS Microbiol Rev 29: 511-529.
3. Berkes, J., Viswanathan, V.K., Savkovic, S.D., and Hecht, G. (2003) Intestinal epithelial responses to enteric pathogens: Effects on tight junction barrier, ion transport, and inflammation. Gut 52: 439-451.
4. Blaser, M.J. (2004) Bacteria and diseases of unknown cause: hemolytic-uremic syndrome. J Infect Dis 189: 552-555.
5. Boonaert, C.J.P., and Rouxhet, P.G. (2000) Surface of lactic acid bacteria: Relationships between chemical composition and physicochemical properties. Appl Environ Microbiol 66: 2548-2554.
6. Buck, B.L., Altermann, E., Svingerud, T., and Klaenhammer, T.R. (2005) Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71: 8344-8351.
7. Ceponis, P.J., Riff, J.D., and Sherman, P.M. (2005) Epithelial cell signaling responses to enterohemorrhagic Escherichia coli infection. Mem Inst Oswaldo Cruz 100: 199-203.
8. Cesena, C., Morelli, L., Alander, M., Siljander, T., Tuomola, E., Salminen, S., et.al. (2001) Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J Dairy Sci 84: 1001-1010.
9. Drumm, B., Neumann, A.W., Policova, Z., and Sherman, P. (1989) Bacterial cell surface hydrophobicity properties in the mediation of in vitro adhesion by the rabbit enteric pathogen Escherichia coli strain RDEC-1. J Clin Invest 84: 1588-1594.
10. Ehrmann, M.A., Kurzak, P., Bauer, J., and Vogel, R.F. (2002) Characterization of lactobacilli towards their use as probiotic adjuncts in poultry. J Appl Microbiol 92: 966-975.
11. Finlay, B.B., and Caparon, M. (2005) Bacterial adherence to cell surfaces and extracellular matrix. In Cellular Microbiology. Cossart, P., Boquet, P., Normark, S., and Rappuoli, R. (eds). Washington, DC: American Society for Microbiology Press, pp. 105-120
12. Frece, J., Kos, B., Svetec, I.K., Zgaga, Z., Mrša, V., and Šušković, J. (2005) Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J Appl Microbiol 98: 285-292.
13. Gopal, P.K., Prasad, J., Smart, J., and 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.
14. Granato, D., Perotti, F., Masserey, I., Rouvet, M., Golliard, M., Servin, A., and Brassart, D. (1999) Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl Environ Microbiol 65: 1071-1077.
15. Hagen, K.E., Guan Hunter, L., Tannock, G.W., Korver, D.R., and Allison, G.E. (2005) Detection, characterization, and in vitro and in vivo expression of genes encoding S-proteins in Lactobacillus gallinarum strains isolated from chicken crops. Appl Environ Microbiol 71: 6633-6643.
16. Hansen, K.K., Sherman, P.M., Cellars, L., Andrade-Gordon, P., Pan, Z., Baruch, A., et.al. (2005) A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci USA 102: 8363-8368.
17. Henriksson, A., Szewzyk, R., and Conway, P.L. (1991) Characteristics of the adhesive determinants of Lactobacillus fermentum 104. Appl Environ Microbiol 57: 499-502.
18. Hewick, R.M., Hunkapiller, M.W., Hood, L.E., and Dreyer, W.S. (1981) A gas liquid solid phase peptide and protein sequencer. J Biol Chem 256: 7990-7997.
19. Horie, M., Ishiyama, A., Fujihira-Ueki, Y., Sillanpää, J., Korhonen, T.K., and Toba, T.A. (2002) Inhibition of the adherence of Escherichia coli strains to basement membrane by Lactobacillus crispatus expressing S-layer. J Appl Microbiol 92: 396-403.
20. Johnson-Henry, K., Wallace, J.L., Basappa, N.S., Soni, R., Wu, G.K.P., and Sherman, P.M. (2001) Inhibition of attaching and effacing lesion formation following enteropathogenic Escherichia coli and Shiga toxin-producing E.coli infection. Infect Immun 69: 7152-7158.
21. Johnson-Henry, K.C., Nadjafi, M., Mitchell, D., Avitzur, Y., Ngan, B.-Y., Galindo-Mata, E., et.al. (2005a) Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J Infect Dis 191: 2106-2117.
22. Johnson-Henry, K.C., Riff, J.D., Gordanpour, M., and Sherman, P.M. (2005b) Benefits of probiotics in models of gastrointestinal bacterial infections. Nutrafoods 23: 29-36.
23. Kaper, J.B., Nataro, J.P., and Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
24. Kos, B., Šušković, J., Vuković, S., Šimpraga, M., Frece, J., and Matošić, S. (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94: 981-987.
25. Li, Z., Elliot, E., Payne, J., Isaacs, J., Gunning, P., and O'Loughlin, E.V. (1999) Shiga toxin-producing Escherichia coli can impair T84 cell structure and function without inducing attaching/effacing lesions. Infect Immun 67: 5938-5945.
26. Lortal, S., van Heijenoort, J., Gruber, K., and Sleytr, U.B. (1992) S-layer of L.helveticus ATCC 12046: Isolation, chemical characterization and re-formation after extraction with LiCl. J Gen Microbiol 138: 611-618.
27. Mack, D.R., and Sherman, P.M. (1999) Hydrophobicity and the gastrointestinal tract: Methods of determination, its source and implications for bacterial adherence. Colloids Surfaces B Biointerfaces 15: 355-363.
28. Mack, D.R., Ahrne, S., Hyde, L., Wei, S., and Hollingsworth, M.A. (2003) Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52: 827-833.
29. Madsen, K.L., Doyle, J.S., Jewell, L.D., Tavernini, M.M., and Fedorak, R.N. (1999) Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 1107-1114.
30. Mercenier, A., Pavan, S., and Pot, B. (2003) Probiotics as biotherapeutic agents: Present knowledge and future prospects. Curr Pharm Des 9: 175-191.
31. Morita, H., He, F., Fuse, T., Ouwehand, A.C., Hashimoto, H., Hosoda, M., et.al. (2002) Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol Immunol 46: 293-297.
32. Naser, S.M., Hagen, K.E., Vancanneyt, M., Cleenwerck, I., Swings, J., Tompkins, T.A. (2006) Reclassification of Lactobacillus suntoryeus Cachat and Priest 2005 as a later synonym of Lactobacillus helveticus (Orla-Jensen 1919) Bergey et.al. 1925 (Approved Lists 1980). Int J Syst Evol Microbiol 56: 355-360.
33. Ohkubo, R., Tomita, M., Holta, Y., Nagira, M., and Hayashi, M. (2003) Comparative study of flux of FITC-labeled dextran 4000 on normal (iso) and hyper-osmolarity in basal side in Caco-2 cell monolayers. Drug Metab Pharmacokinet 18: 404-408.
34. Pretzer, G., Snel, J., Molenaar, D., Wiersma, A., Bron, P.A., Lambert, J., et.al. (2005) Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J Bacteriol 187: 6128-6136.
35. Reid, G., Jass, J., Sebulsky, M.T., and McCormick, J.K. (2003) Potential uses of probiotics in clinical practice. Clin Microbiol Rev 16: 658-672.
36. Riff, J.D., Callahan, J.W., and Sherman, P.M. (2005) Cholesterol-enriched membrane microdomains are required for inducing host cell cytoskeleton rearrangements in response to attaching-effacing Escherichia coli. Infect Immun 73: 7113-7125.
37. Rojas, M., Ascencio, F., and Conway, P.L. (2002) Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small Intestinal mucus and gastric mucin. Appl Environ Microbiol 68: 2330-2336.
38. Sára, M., and Sleytr, U.B. (2000) S-layer proteins. J Bacteriol 182: 859-868.
39. Schär-Zammaretti, P., and Ubbink, J. (2003) The cell wall of lactic acid bacteria: Surface constituents and macromolecular conformations. Biophys J 85: 4076-4092.
40. Şengül, N., Aslím, B., Uçar, G., Yücel, N., Işik, S., Bozkurt, H., et.al. (2006) Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats. Dis Colon Rectum 49: 250-258.
41. Servin, A.L. (2004) Antogonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28: 405-440.
42. Sherman, L.A., and Savage, D.C. (1986) Lipoteichoic acids in Lactobacillus strains that colonize the mouse gastric epithelium. Appl Environ Microbiol 52: 302-304.
43. Sherman, P.M., Johnson-Henry, K.C., Yeung, H.P., Ngo, P.S.C., Goulet, J., and Tompkins, T.A. (2005) Probiotics reduce enterohemorrhagic Escherichia coli O157H7: H7-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect Immun 73: 5183-5188.
44. Sillanpää, J., Martinez, B., Antikainen, J., Toba, T., Kalkkinen, N., Tankka, S., et.al. (2000) Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol 182: 6440-6450.
45. Sleytr, U.B., and Sára, M. (1997) Bacterial and archaeal S-layer proteins: Structure-function relationships and their biotechnological applications. Trends Biotechnol 15: 20-26.
46. Smit, E., Oling, F., Demel, R., Martinez, B., and Pouwels, P.H. (2001) The S-layer protein of Lactobacillus acidophilus ATCC 4356: identification and characterisation of domains responsible for S-protein assembly and cell wall binding. J Mol Biol 305: 245-257.
47. Szajewska, H., Setty, M., Mrukowicz, J., and Guandalin, S. (2006) Probiotics in gastrointestinal diseases in children: Hard and not-so-hard evidence of efficacy. J Pediatr Gastroenterol Nutr 42: 454-475.
48. Toba, T., Virkola, R., Westerlund, B., Björkman, Y., Sillanpää, J., Vartio, T., et.al. (1995) A collagen-binding S-layer protein in Lactobacillus crispatus. Appl Environ Microbiol 61: 2467-2471.
49. Vadillo-Rodriguez, V., Busscher, H.J., van der Mei, H.C., de Vries, J., and Norde, W. (2005) Role of lactobacillus cell surface hydrophobicity as probed by AFM in adhesion to surfaces at low and high ionic strength. Colloids Surf B Biointerfaces 41: 33-41.
50. Van Calsteren, M.R., Pau-Roblot, C., Begin, A., and Roy, D. (2002) Structure determination of the exopolysaccharides produced by Lactobacillus rhamnosus strains RW-9595M and R. Biochem J 363: 7-17.
51. Ventura, M., Jankovic, I., Walker, C., Pridmore, R.D., and Zink, R. (2002) Identification and characteriaztion of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl Environ Microbiol 68: 6172-6181.
52. Walter, J., Chagnaud, P., Tannock, G.W., Loach, D.M., Dal Bello, F., Jenkinson, H.F., et.al. (2005) A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol 71: 979-986.
53. Wong, C., Lelacic, S., Habeeb, R.L., Watkins, S.L., and Tarr, P.I. (2000) The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157: H7 infection. N Engl J Med 342: 1930-1936.
54. Zhang, R., Barker, L., Pinchev, D., Marshall, J., Rasamoelisolo, M., Smith, C., et.al. (2004) Mining biomarkers in human sera using proteomic tools. Proteomics 4: 244-256.
55. Zhou, X., Giron, J.A., Torres, A.G., Crawford, J.A., Negrete, E., Vogel, S.N., and Kaper, J.B. (2003) Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 71: 2120-2129.