Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T14:40:39.825Z Has data issue: false hasContentIssue false
  • English
  • Français

Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88

Published online by Cambridge University Press:  08 March 2007

Marianna Roselli ,
Alberto Finamore ,
Maria Serena Britti  and
Elena Mengheri
Marianna Roselli
Affiliation:
Istituto Nazionale di Ricerca per gli Alimenti e la Nutrizione (INRAN)Via Ardeatina 54600178 RomeItaly
Alberto Finamore
Affiliation:
Istituto Nazionale di Ricerca per gli Alimenti e la Nutrizione (INRAN)Via Ardeatina 54600178 RomeItaly
Maria Serena Britti
Affiliation:
Istituto Nazionale di Ricerca per gli Alimenti e la Nutrizione (INRAN)Via Ardeatina 54600178 RomeItaly
Elena Mengheri*
Affiliation:
Istituto Nazionale di Ricerca per gli Alimenti e la Nutrizione (INRAN)Via Ardeatina 54600178 RomeItaly
*
*Corresponding author: Dr E. Mengheri, fax +39 06 51494550, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Probiotic bacteria may provide protection against intestinal damage induced by pathogens, but the underlying mechanisms are still largely unknown. We investigated whether Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG (LGG) protected intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli (ETEC) K88, by inhibiting pathogen attachment to the cells, which is the first step of ETEC pathogenicity, and regulating neutrophil recruitment, a crucial component of inflammation. A partial reduction of ETEC adhesion was exerted by probiotics and their culture supernatant fractions either undigested or digested with proteases. ETEC viability was unaffected by the presence of B. animalis, LGG or their supernatant fractions in the culture medium, indicating an absence of probiotic bactericidal activity. Probiotics and their supernatant fractions, either undigested or digested with proteases, strongly inhibited the neutrophil transmigration caused by ETEC. Both B. animalis and LGG counteracted the pathogen-induced up regulation of IL-8, growth-related oncogene-α and epithelial neutrophil-activating peptide-78 gene expression, which are chemokines essential for neutrophil migration. Moreover, the probiotics prevented the ETEC-induced increased expression of IL-1β and TNF-α and decrease of transforming growth factor-α, which are regulators ofchemokine expression. These results indicate that B. animalisMB5 and LGG protect intestinal cells from the inflammation-associated response caused by ETEC K88 by partly reducing pathogen adhesion and by counteracting neutrophil migration, probably through the regulation of chemokine and cytokine expression.

Keywords

ProbioticsIntestinal cellsInflammation-associated responseNeutrophil migrationAdhesion
Type
Research Article
Information
British Journal of Nutrition , Volume 95 , Issue 6 , June 2006 , pp. 1177 - 1184
Copyright
Copyright © The Nutrition Society 2006

References

Abbott, A, Gut reaction. Nature 2004 427 284–286.CrossRefGoogle ScholarPubMed
Baggiolini, M, Loetscher, P, Moser, B, Interleukin-8 and the chemokine family. Int J Immunopharmacol 1995 17 103–108.CrossRefGoogle ScholarPubMed
Berin, MC, Darfeuille-Michaud, A, Egan, LJ, Miyamoto, Y, Kagnoff, MF, Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol 2002 4 635–648.CrossRefGoogle ScholarPubMed
Berkes, J, Viswanathan, VK, Savkovic, SD, Hecht, G, ntestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation. Gut 2003 52 439–451.CrossRefGoogle Scholar
Bernet, MF, Brassart, D, Neesr, JR, Servin, AL, Lactobacillus acidophilusLA1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 1994 35 483–489.CrossRefGoogle ScholarPubMed
Dieleman, LA, Goerres, MS, Arends, A, Sprengers, D, Torrice, C, Hoentjen, F, Grenther, WB, Sartor, RB, Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut 2003 52 370–376.CrossRefGoogle ScholarPubMed
Dotan, I, Rachmilewitz, D, Probiotics in inflammatory bowel disease: possible mechanisms of action. Curr Opin Gastroenterol 2005 21 426–376.Google ScholarPubMed
Elliott, SN, Wallace, JL, Neutrophil-mediated gastrointestinal injury. Can J Gastroenterol 1998 12 559–568.Google Scholar
Finamore, A, Roselli, M, Merendino, N, Nobili, F, Vignolini, F, Mengheri, E, Zinc deficiency suppresses the development of oral tolerance in rats. J Nutr 2003 133 191–198.CrossRefGoogle ScholarPubMed
Forestier, C, De Champs, C, Vatoux, C, Joly, B, Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Res Microbiol 2001 152 167–173.Google Scholar
Gewirtz, AT, Liu, Y, Sitaraman, SV, Madara, JL, Intestinal epithelial pathobiology: past, present and future. Best Pract Res Clin Gastroenterol 2002 16 851–867.Google Scholar
Gorbach, SL, Probiotics and gastrointestinal health. Am J Gastroenterol 2000 95 S2–S4.Google Scholar
Granato, D, Perotti, F, Masserey, I, Rouvet, M, Golliard, M, Servin, A, Brassart, D, 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 1999 65 1071–1077.CrossRefGoogle ScholarPubMed
Guarner, F, Malagelada, JR, Gut flora in health and disease. Lancet 2003 8 512–519.CrossRefGoogle Scholar
Haller, D, Bode, C, Hammes, WP, Pfeifer, AMA, Schiffrin, EJ, Blum, S, Non pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leukocyte co-cultures. Gut 2000 47 79–87.CrossRefGoogle ScholarPubMed
Haller, D, Serrant, P, Peruisseau, G, Bode, C, Hammes, WP, Schiffrin, E, Blum, S, IL-10 producing CD14low monocytes inhibit lymphocyte-dependent activation of intestinal epithelial cells by commensal bacteria. Microbiol Immunol 2002 46 195–205.Google Scholar
Hampson, DJPostweaning Escherichia coli diarrhoea in pigs. In Escherichia coli in Domestic Animals and Humans, (Gyles, CL) Wallingford, UK: CAB International. 1994 171–191.Google Scholar
Hidemura, A, Saito, H, Fukatsu, K, Matsuda, T, Kitayama, J, Ikeda, S, Kang, W, Nagawa, H, Oral administration of Bifidobacterium longum culture condensate in a diet-restricted murine peritonitis model enhances polymorphonuclear neutrophil recruitment into the local inflammatory site. Nutrition 2003 19 270–274.Google Scholar
Ibnou-Zekri, N, Blum, S, Schiffrin, EJ, von der Weid, T, Divergent patterns of colonisation and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infect Immun 2003 71 428–436.Google Scholar
Jarai, G, Sukkar, M, Garrett, S, Duroudier, N, Westwick, J, Adcock, I, Chung, KF, Effects of interleukin-1beta, interleukin-13 and transforming growth factor-beta on gene expression in human airway smooth muscle using gene microarrays. Eur J Pharmacol 2004 497 255–265.Google Scholar
Jaye, DL, Parkos, CA, Neutrophil migration across intestinal epithelium. Ann N Y Acad Sci 2000 915 151–161.CrossRefGoogle ScholarPubMed
Jenkins, B, Holsten, S, Bengmark, S, Martindale, R, Probiotics: a practical review of their role in specific clinical scenarios. Nutr Clin Pract 2000 20 262–270.Google Scholar
Jijon, H, Backer, J, Diaz, H, Yeung, H, Thiel, D, McKaigney, C, De Simone, C, Madsen, K, (2004) DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology 2004 126 1358–1373.CrossRefGoogle ScholarPubMed
Jin, LZ, Marquardt, RR, Zhao, X, A strain of Enterococcus faecium (18C23) inhibits adhesion of enterotoxigenic Escherichia coli K88 to porcine small intestine mucus. Appl Environ Microbiol 2000 66 4200–4204.CrossRefGoogle ScholarPubMed
Jin, LZ, Zhao, X, Intestinal receptors for adhesive fimbriae of enterotoxigenic Escherichia coli (ETEC) K88 in swine – a review. Appl Microbiol Biotechnol 2000 54 311–318.Google Scholar
Keates, S, Keates, AC, Mizoguch, E, Bhan, A, Kelly, CP, Enterocytes are the primary source of the chemokine ENA-78 in normal colon and in ulcerative colitis. Am J Physiol 1997 273 G75–G82.Google ScholarPubMed
Kim, HY, Kim, HJ, Min, HS, Kim, S, Park, WS, Park, SH, Chung, DH, NKT cells promote antibody-induced joint inflammation by suppressing transforming growth factor beta1 production. J Exp Med 2005 3 41–47.CrossRefGoogle Scholar
Lehto, EM, Salminen, SJ, Inhibition of Salmonella typhimurium adhesion to Caco-2 cell cultures by Lactobacillus strain GG spent culture supernate: only a pH effect?. FEMS Immunol Med Microbiol 1997 18 125–132.CrossRefGoogle Scholar
Lievin-Le, Moal V, Amsellem, R, Servin, AL, Coconnier, MH, Lactobacillus acidophilus (strain LB) from the resident adult human gastrointestinal microflora exerts activity against brush border damage promoted by a diarrhoeagenic Escherichia coli in human enterocyte-like cells. Gut 2002 50 803–811.Google Scholar
Lugering, N, Kucharzik, T, Gockel, H, Sorg, C, Stoll, R, Domschke, W, Human intestinal epithelial cells down-regulate IL-8 expression in human intestinal microvascular endothelial cells; role of transforming growth factor-beta 1 (TGF-beta1). Clin Exp Immunol 1998 114 377–384.CrossRefGoogle Scholar
Majamaa, H, Isolauri, E, Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol 1997 99 179–185.CrossRefGoogle ScholarPubMed
Majamaa, H, Isolauri, E, Saxelin, M, Vesikari, T, Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr 1995 203 333–338.Google Scholar
Marteau, PR, de Vrese, M, Cellier, CJ, Schrezenmeir, J, Protection from gastrointestinal disease with use of probiotics. Am J Clin Nutr 2001 73 430S–436S.CrossRefGoogle ScholarPubMed
Mengheri, E, Nobili, F, Vignolini, F, Pesenti, M, Brandi, G, Biavati, B, Bifidobacterium animalis protects intestine from damage induced by zinc deficiency in rats. J Nutr 1999 129 2251–2257.CrossRefGoogle ScholarPubMed
Mercenier, A, Pavan, S, Pot, B, Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr Pharm Des 2003 9 175–191.CrossRefGoogle ScholarPubMed
Michail, S, Abernathy, F, Lactobacillus plantarum inhibits the intestinal epithelial migration of neutrophils induced by enteropathogenic Escherichia coli. J Pediatr Gastroenterol Nutr 2003 36 385–391.Google Scholar
Nagineni, CN, Detrick, B, Hooks, JJ, Transforming growth factor-beta expression in human retinal pigment epithelial cells is enhanced by Toxoplasma gondii: a possible role in the immunopathogenesis of retinochoroiditis. Clin Exp Immunol 2002 128 372–378.Google Scholar
Neish, AS, The gut microflora and intestinal epithelial cells: a continuing dialogue. Microbes Infect 2002 4 309–317.CrossRefGoogle ScholarPubMed
Neutra, M, Louvard, D, Differentiation of intestinal cells in vitro. Mol Cell Biol 1989 8 363–398.Google Scholar
O'Sullivan, GC, Kelly, P, O'Halloran, S, Collins, C, Collins, JK, Dunne, C, Shanahan, F, Probiotics: an emerging therapy. Curr Pharm Des 2005 11 3–10.Google Scholar
Otte, JM, Cario, E, Podolsky, DK, Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. Am J Physiol 2004 286 G613–G626.Google Scholar
Ouwehand, AC, Salminen, S, Isolauri, E, Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 2002 82 279–289.CrossRefGoogle ScholarPubMed
Parkos, CA, Delp, C, Arnaout, MA, Madara, JL, Neutrophil transmigration across a cultured intestinal epithelium. J Clin Invest 1991 88 1605–1612.Google Scholar
Peran, L, Camuesco, D, Comalada, M, Nieto, A, Concha, A, Diaz-Ropero, MP, Olivares, M, Xaus, J, Zarzuelo, A, Galvez, J, Preventative effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis. World J Gastroenterol 2005 11 5185–5192.Google ScholarPubMed
Resta-Lenert, S, Barrett, KE, Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive. Escherichia coli (EIEC). Gut 2003 52 988–997.Google Scholar
Rollins, BJ, Chemokines. Blood 1997 90 909–928.CrossRefGoogle ScholarPubMed
Roselli, M, Finamore, A, Garaguso, I, Britti, MS, Mengheri, E, Zinc oxide protects cultured enterocytes from the damage induced by Escherichia coli.. J Nutr 2003 133 4077–4082.CrossRefGoogle ScholarPubMed
Rudack, C, Maune, S, Eble, J, Schroeder, JM, The primary role in biologic activity of the neutrophil chemokines IL-8 and GROalpha in cultured nasal epithelial cells. J Interferon Cytokine Res 2003 23 113–123.Google Scholar
Savkovic, SD, Koutsouris, A, Hecht, G, Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli to cultured human intestinal epithelial monolayers induces transmigration of neutrophils. Infect Immun 1996 64 4480–4487.Google Scholar
Schroder, JM, Chemoattractants as mediators of neutrophilic tissue recruitment. Clin Dermatol 2000 18 245–263.Google Scholar
Shibolet, O, Karmeli, F, Eliakim, R, Swennen, E, Brigidi, P, Gionchetti, P, Campieri, M, Morgenstern, S, Rachmilewitz, D, Variable response to probiotics in two models of experimental colitis in rats. Inflamm Bowel Dis 2002 8 399–406.Google Scholar
Smith, DL, Harris, AD, Johnson, JA, Silbergeld, EK, Morris, GM, Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. PNAS 2002 99 6434–6439.Google Scholar
Szekanecz, Z, Strieter, RM, Kunkel, SL, Koch, AE, Chemokines in rheumatoid arthritis. Springer Semin Immunopathol 1998 20 115–132.CrossRefGoogle ScholarPubMed
Teitelbaum, JE, Walker, WA, Nutritional impact of pre and probiotics as protective gastrointestinal organisms. Annu Rev Nutr 2002 22 107–138.Google Scholar
Vaughan, EE, de Vries, MC, Zoetendal, EG, Ben-Amor, K, Akkermans, AD, de Vos, WM, The intestinal LABs. Antonie Van Leeuwenhoek 2002 82 341–352.Google Scholar
Walz, A, Strieter, RM, Schnyder, S, Neutrophil-activating peptide ENA-78. Adv Exp Med Biol 1993 351 129–137.CrossRefGoogle ScholarPubMed
Zhou, JS, Pillidge, CJ, Gopal, PK, Gill, HS, Antibiotic susceptibilityprofiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiol 2005 98 211–217.Google Scholar