Skip to main content Accessibility help
×
Home

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

  • Marianna Roselli (a1), Alberto Finamore (a1), Maria Serena Britti (a1) and Elena Mengheri (a1)

Abstract

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.

    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      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
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      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
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      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
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Dr E. Mengheri, fax +39 06 51494550, email mengheri@inran.it

References

Hide All
Abbott, A, Gut reaction. Nature 2004 427 284286.
Baggiolini, M, Loetscher, P, Moser, B, Interleukin-8 and the chemokine family. Int J Immunopharmacol 1995 17 103108.
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 635648.
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 439451.
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 483489.
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 370376.
Dotan, I, Rachmilewitz, D, Probiotics in inflammatory bowel disease: possible mechanisms of action. Curr Opin Gastroenterol 2005 21 426–376.
Elliott, SN, Wallace, JL, Neutrophil-mediated gastrointestinal injury. Can J Gastroenterol 1998 12 559568.
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 191198.
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 167173.
Gewirtz, AT, Liu, Y, Sitaraman, SV, Madara, JL, Intestinal epithelial pathobiology: past, present and future. Best Pract Res Clin Gastroenterol 2002 16 851867.
Gorbach, SL, Probiotics and gastrointestinal health. Am J Gastroenterol 2000 95 S2S4.
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 10711077.
Guarner, F, Malagelada, JR, Gut flora in health and disease. Lancet 2003 8 512519.
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 7987.
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 195205.
Hampson, DJPostweaning Escherichia coli diarrhoea in pigs. In Escherichia coli in Domestic Animals and Humans, (Gyles, CL) Wallingford, UK: CAB International. 1994 171191.
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 270274.
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 428436.
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 255265.
Jaye, DL, Parkos, CA, Neutrophil migration across intestinal epithelium. Ann N Y Acad Sci 2000 915 151161.
Jenkins, B, Holsten, S, Bengmark, S, Martindale, R, Probiotics: a practical review of their role in specific clinical scenarios. Nutr Clin Pract 2000 20 262270.
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 13581373.
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 42004204.
Jin, LZ, Zhao, X, Intestinal receptors for adhesive fimbriae of enterotoxigenic Escherichia coli (ETEC) K88 in swine – a review. Appl Microbiol Biotechnol 2000 54 311318.
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 G75G82.
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 4147.
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 125132.
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 803811.
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 377384.
Majamaa, H, Isolauri, E, Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol 1997 99 179185.
Majamaa, H, Isolauri, E, Saxelin, M, Vesikari, T, Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr 1995 203 333338.
Marteau, PR, de Vrese, M, Cellier, CJ, Schrezenmeir, J, Protection from gastrointestinal disease with use of probiotics. Am J Clin Nutr 2001 73 430S436S.
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 22512257.
Mercenier, A, Pavan, S, Pot, B, Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr Pharm Des 2003 9 175191.
Michail, S, Abernathy, F, Lactobacillus plantarum inhibits the intestinal epithelial migration of neutrophils induced by enteropathogenic Escherichia coli. J Pediatr Gastroenterol Nutr 2003 36 385391.
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 372378.
Neish, AS, The gut microflora and intestinal epithelial cells: a continuing dialogue. Microbes Infect 2002 4 309317.
Neutra, M, Louvard, D, Differentiation of intestinal cells in vitro. Mol Cell Biol 1989 8 363398.
O'Sullivan, GC, Kelly, P, O'Halloran, S, Collins, C, Collins, JK, Dunne, C, Shanahan, F, Probiotics: an emerging therapy. Curr Pharm Des 2005 11 310.
Otte, JM, Cario, E, Podolsky, DK, Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. Am J Physiol 2004 286 G613G626.
Ouwehand, AC, Salminen, S, Isolauri, E, Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek 2002 82 279289.
Parkos, CA, Delp, C, Arnaout, MA, Madara, JL, Neutrophil transmigration across a cultured intestinal epithelium. J Clin Invest 1991 88 16051612.
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 51855192.
Resta-Lenert, S, Barrett, KE, Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive. Escherichia coli (EIEC). Gut 2003 52 988997.
Rollins, BJ, Chemokines. Blood 1997 90 909928.
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 40774082.
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 113123.
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 44804487.
Schroder, JM, Chemoattractants as mediators of neutrophilic tissue recruitment. Clin Dermatol 2000 18 245263.
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 399406.
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 64346439.
Szekanecz, Z, Strieter, RM, Kunkel, SL, Koch, AE, Chemokines in rheumatoid arthritis. Springer Semin Immunopathol 1998 20 115132.
Teitelbaum, JE, Walker, WA, Nutritional impact of pre and probiotics as protective gastrointestinal organisms. Annu Rev Nutr 2002 22 107138.
Vaughan, EE, de Vries, MC, Zoetendal, EG, Ben-Amor, K, Akkermans, AD, de Vos, WM, The intestinal LABs. Antonie Van Leeuwenhoek 2002 82 341352.
Walz, A, Strieter, RM, Schnyder, S, Neutrophil-activating peptide ENA-78. Adv Exp Med Biol 1993 351 129137.
Zhou, JS, Pillidge, CJ, Gopal, PK, Gill, HS, Antibiotic susceptibilityprofiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiol 2005 98 211217.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed