Lactobacillus reuteri inhibition of enteropathogenic Escherichia coli adherence to human intestinal epithelium

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Walsham, Alistair D S ^a,b   MacKenzie, Donald A ^b   Cook, Vivienne ^c   Wemyss Holden, Simon ^c   Hews, Claire L ^b,d   Juge, Nathalie ^b   Schüller, Stephanie ^a,b  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^c NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Adherence; Diarrhea; EPEC; Human intestinal epithelium; L. reuteri; Mucus; Probiotic

Indexed keywords

ARTICLE; BACTERIUM ADHERENCE; CANCER CELL LINE; COLON CARCINOMA; COLONY FORMING UNIT; CONTROLLED STUDY; DUODENUM BIOPSY; ENTEROPATHOGENIC ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; INTESTINE EPITHELIUM; LACTOBACILLUS REUTERI; NONHUMAN; SCANNING ELECTRON MICROSCOPY;

EID: 84964324855     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00244     Document Type: Article

References (43)

1. Bartman, A. E., Sanderson, S. J., Ewing, S. L., Niehans, G. A., Wiehr, C. L., Evans, M. K., et al. (1999). Aberrant expression of MUC5AC and MUC6 gastric mucin genes in colorectal polyps. Int. J. Cancer 80, 210-218. doi: 10.1002/(SICI)1097-0215(19990118)80:2<210::AID-IJC9>3.3.CO;2-L
2. Bernet, M. F., Brassart, D., Neeser, J. R., and Servin, A. L. (1994). Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35, 483-489. doi: 10.1136/gut.35.4.483
3. Bray, J. (1945). Isolation of antigenically homogenous strains of Bact. coli neapolitanum from summer diarrhoea of infants. J. Pathol. Bacteriol. 57, 239-247. doi: 10.1002/path.1700570210
4. Casas, I. A., and Dobrogosz, J. (2000). Validation of the probiotic concept: Lactobacillus reuteri confers broad-spectrum protection against disease in humans and animals. Microb. Ecol. Health Dis. 12, 247-285. doi: 10.1080/08910600050216246-1
5. De Keersmaecker, S. C., Verhoeven, T. L., Desair, J., Marchal, K., Vanderleyden, J., and Nagy, I. (2006). Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiol. Lett. 259, 89-96. doi: 10.1111/j.1574-6968.2006.00250.x
6. Etzold, S., and Juge, N. (2014). Structural insights into bacterial recognition of intestinal mucins. Curr. Opin. Struct. Biol. 28, 23-31. doi: 10.1016/j.sbi.2014.07.002
7. Etzold, S., Kober, O. I., MacKenzie, D. A., Tailford, L. E., Gunning, A. P., Walshaw, J., et al. (2014a). Structural basis for adaptation of lactobacilli to gastrointestinal mucus. Environ. Microbiol. 16, 888-903. doi: 10.1111/1462-2920.12377
8. Etzold, S., MacKenzie, D. A., Jeffers, F., Walshaw, J., Roos, S., Hemmings, A. M., et al. (2014b). Structural and molecular insights into novel surface-exposed mucus adhesins from Lactobacillus reuteri human strains. Mol. Microbiol. 92, 543-556. doi: 10.1111/mmi.12574
9. Forestier, C., De Champs, C., Vatoux, C., and Joly, B. (2001). Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Res. Microbiol. 152, 167-173. doi: 10.1016/S0923-2508(01)01188-3
10. Frese, S. A., Benson, A. K., Tannock, G. W., Loach, D. M., Kim, J., Zhang, M., et al. (2011). The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet. 7:e1001314. doi: 10.1371/journal.pgen.1001314
11. Havenaar, R., Ten Brink, B., and Huis In't Veld, J. H. J. (1992). "Selection of strains for probiotic use, "in Probiotics: The Scientific Basis, ed. R. Fuller (London: Chapman & Hall), 209-224
12. Jensen, H., Roos, S., Jonsson, H., Rud, I., Grimmer, S., Van Pijkeren, J. P., et al. (2014). Role of Lactobacillus reuteri cell and mucus-binding protein A (CmbA) in adhesion to intestinal epithelial cells and mucus in vitro. Microbiology 160, 671-681. doi: 10.1099/mic.0.073551-0
13. Johansson, M. E., Larsson, J. M., and Hansson, G. C. (2011). The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. U.S.A. 108(Suppl. 1), 4659-4665. doi: 10.1073/pnas.1006451107
14. Juge, N. (2012). Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 20, 30-39. doi: 10.1016/j.tim.2011.10.001
15. Kim, Y., Kim, S. H., Whang, K. Y., Kim, Y. J., and Oh, S. (2008). Inhibition of Escherichia coli O157:H7 attachment by interactions between lactic acid bacteria and intestinal epithelial cells. J. Microbiol. Biotechnol. 18, 1278-1285
16. Knutton, S., Baldwin, T., Williams, P. H., and McNeish, A. S. (1989). Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 57, 1290-1298
17. Lanata, C. F., Fischer-Walker, C. L., Olascoaga, A. C., Torres, C. X., Aryee, M. J., and Black, R. E. (2013). Global causes of diarrheal disease mortality in children < 5 years of age: a systematic review. PLoS ONE 8:e72788. doi: 10.1371/journal.pone.0072788
18. Lebeer, S., Vanderleyden, J., and De Keersmaecker, S. C. (2008). Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 72, 728-764. doi: 10.1128/MMBR.00017-08
19. Levine, M. M., Berquist, E. J., Nalin, D. R., Waterman, D. H., Hornick, R. B., Young, C. R., et al. (1978). Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1, 1119-1122. doi: 10.1016/S0140-6736(78)90299-4
20. MacKenzie, D. A., Jeffers, F., Parker, M. L., Vibert-Vallet, A., Bongaerts, R. J., Roos, S., et al. (2010). Strain-specific diversity of mucus-binding proteins in the adhesion and aggregation properties of Lactobacillus reuteri. Microbiology 156, 3368-3378. doi: 10.1099/mic.0.043265-0
21. Miyoshi, Y., Okada, S., Uchimura, T., and 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. doi: 10.1271/bbb.50688
22. Moon, H. W., Whipp, S. C., Argenzio, R. A., Levine, M. M., and Giannella, R. A. (1983). Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41, 1340-1351
23. Nataro, J. P., and Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11, 142-201
24. Navabi, N., McGuckin, M. A., and Lindén, S. K. (2013). Gastrointestinal cell lines form polarized epithelia with an adherent mucus layer when cultured in semi-wet interfaces with mechanical stimulation. PLoS ONE 8:e68761. doi: 10.1371/journal.pone.0068761
25. Ogawa, M., Shimizu, K., Nomoto, K., Tanaka, R., Hamabata, T., Yamasaki, S., et al. (2001). Inhibition of in vitro growth of Shiga toxin-producing Escherichia coli O157:H7 by probiotic Lactobacillus strains due to production of lactic acid. Int. J. Food Microbiol. 68, 135-140. doi: 10.1016/S0168-1605(01)00465-2
26. Oh, P. L., Benson, A. K., Peterson, D. A., Patil, P. B., Moriyama, E. N., Roos, S., et al. (2010). Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J. 4, 377-387. doi: 10.1038/ismej.2009.123
27. Ouwehand, A. C., Salminen, S., Tolkko, S., Roberts, P., Ovaska, J., and Salminen, E. (2002). Resected human colonic tissue: new model for characterizing adhesion of lactic acid bacteria. Clin. Diagn. Lab. Immunol. 9, 184-186
28. Roos, S., and Jonsson, H. (2002). A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148, 433-442. doi: 10.1099/00221287-148-2-433
29. Savino, F., Fornasero, S., Ceratto, S., De Marco, A., Mandras, N., Roana, J., et al. (2015). Probiotics and gut health in infants: a preliminary case-control observational study about early treatment with Lactobacillus reuteri DSM 17938. Clin. Chim. Acta 451, 82-87. doi: 10.1016/j.cca.2015.02.027
30. Sazawal, S., Hiremath, G., Dhingra, U., Malik, P., Deb, S., and Black, R. E. (2006). Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infect. Dis. 6, 374-382. doi: 10.1016/S1473-3099(06)70495-9
31. Schüller, S., Lucas, M., Kaper, J. B., Girón, J. A., and Phillips, A. D. (2009). The ex vivo response of human intestinal mucosa to enteropathogenic Escherichia coli infection. Cell. Microbiol. 11, 521-530. doi: 10.1111/j.1462-5822.2008.01275.x
32. Servin, A. L. (2004). Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev. 28, 405-440. doi: 10.1016/j.femsre.2004.01.003
33. Sheng, Y. H., Hasnain, S. Z., Florin, T. H., and McGuckin, M. A. (2012). Mucins in inflammatory bowel diseases and colorectal cancer. J. Gastroenterol. Hepatol. 27, 28-38. doi: 10.1111/j.1440-1746.2011.06909.x
34. Sherman, P. M., Johnson-Henry, K. C., Yeung, H. P., Ngo, P. S., Goulet, J., and Tompkins, T. A. (2005). Probiotics reduce enterohemorrhagic Escherichia coli O157:H7-and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect. Immun. 73, 5183-5188. doi: 10.1128/IAI.73.8.5183-5188.2005
35. Shornikova, A. V., Casas, I. A., Isolauri, E., Mykkanen, H., and Vesikari, T. (1997a). Lactobacillus reuteri as a therapeutic agent in acute diarrhea in young children. J. Pediatr. Gastroenterol. Nutr. 24, 399-404. doi: 10.1097/00005176-199704000-00008
36. Shornikova, A. V., Casas, I. A., Mykkanen, H., Salo, E., and Vesikari, T. (1997b). Bacteriotherapy with Lactobacillus reuteri in rotavirus gastroenteritis. Pediatr. Infect. Dis. J. 16, 1103-1107. doi: 10.1097/00006454-199712000-00002
37. Szajewska, H., Urbanska, M., Chmielewska, A., Weizman, Z., and Shamir, R. (2014). Meta-analysis: Lactobacillus reuteri strain DSM 17938 (and the original strain ATCC 55730) for treating acute gastroenteritis in children. Benef. Microbes 5, 285-293. doi: 10.3920/BM2013.0056
38. Talarico, T. L., Casas, I. A., Chung, T. C., and Dobrogosz, W. J. (1988). Production and isolation of reuterin, a growth inhibitor produced by Lactobacillus reuteri. Antimicrob. Agents Chemother. 32, 1854-1858. doi: 10.1128/AAC.32.12.1854
39. Tuomola, E., Crittenden, R., Playne, M., Isolauri, E., and Salminen, S. (2001). Quality assurance criteria for probiotic bacteria. Am. J. Clin. Nutr. 73, 393S-398S
40. Valeur, N., Engel, P., Carbajal, N., Connolly, E., and Ladefoged, K. (2004). Colonization and immunomodulation by Lactobacillus reuteri ATCC 55730 in the human gastrointestinal tract. Appl. Environ. Microbiol. 70, 1176-1181. doi: 10.1128/AEM.70.2.1176-1181.2004
41. van Klinken, B. J., Oussoren, E., Weenink, J. J., Strous, G. J., Buller, H. A., Dekker, J., et al. (1996). The human intestinal cell lines Caco-2 and LS174T as models to study cell-type specific mucin expression. Glycoconj. J. 13, 757-768. doi: 10.1007/BF00702340
42. Viswanathan, V. K., Hodges, K., and Hecht, G. (2009). Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nat. Rev. Microbiol. 7, 110-119. doi: 10.1038/nrmicro2053
43. Wong, A. R., Pearson, J. S., Bright, M. D., Munera, D., Robinson, K. S., Lee, S. F., et al. (2011). Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol. Microbiol. 80, 1420-1438. doi: 10.1111/j.1365-2958.2011.07661.x