Skip to main content

Advertisement

Log in

The protective potency of probiotic bacteria and their microbial products against enteric infections-review

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

The intestinal environment accommodates a wide range of contents ranging from harmless beneficial dietary and microbial flora to harmful pathogenic bacteria. This has resulted in the development of highly adapted epithelial cells lining the intestine. This adaptation involves the potential of crypt cells to proliferate and to constantly replace villous cells that are lost due to maturity or death. As a result, the normal intestinal epithelial integrity and functions are maintained. This phenomenon is eminent in intestinal defense whereby the intestinal epithelial cells serve as a physical barrier against luminal agents. The protection against agents in the gut lumen can only be effective if the epithelium is intact. Restitution of the damaged epithelium is therefore crucial in this type of defense.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Hsp(s):

heat-shock protein(s)

IL:

interleukin

References

  • Andoh A., Fujiyama Y., Hata K., Araki Y., Takaya H., Shimada M., Bamba T.: Counter-regulatory effect of sodium butyrate on tumuor necrosis factor-α (TNF-α)-induced complement C3 and factor B biosynthesis in human intestinal epithelial cells. Clin.Exp.Immunol.118, 23–29 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Asanuma N., Kawato M., Hino T.: Presence of Butyrivibrio fibrisolvens in the digestive tract of dogs and cats, and its contribution to butyrate production. J.Gen.Appl.Microbiol.47, 313–319 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Awane M., Andres P.G., Li D.J., Reinecker H.C.: NF-κB-inducing kinase is a common mediator of IL-17, TNF-α-, and IL-1β-induced chemokine promoter activation in intestinal epithelial cells. J.Immunol.162, 5337–5344 (1999).

    PubMed  CAS  Google Scholar 

  • Bernard J.A., Warwick G.: Butyrate rapidly induces growth inhibition and differentiation in HT-29 cells. Cell Growth Differ. 4, 495–501 (1993).

    Google Scholar 

  • Cahill C.M., Waterman W.R., Xie Y., Auron P.E., Calderwood S.K.: Transcriptional repression of the proinflammatory 1β gene by heat shock factor 1. J.Biol.Chem.271, 24874–24879 (1996).

    PubMed  CAS  Google Scholar 

  • Castagliuolo I., Riegler M.F., Valenick L., Lamont J.T., Pothoulakis C.: Saccharomyces boulardii protease inhibits the effects of Clostridium difficile toxins A and B in human colonic mucosa. Infect.Immun.67, 302–307 (1999).

    PubMed  CAS  Google Scholar 

  • Chu E.K., Ribeiro S.P., Slutsky A.S.: Heat stress increases survival rates in lipopolysaccharide-stimulated rats. Crit.Care Med.25, 1727–1732 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Coconnier M.-H., Bernet-Camard M.F., Servin A.L.: How intestinal epithelial cell differentiation inhibits the cell-entry of Yersinia pseudotuberculosis in colon carcinoma Caco-2 cell line in culture. Differentiation58, 87–94 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Coconnier M.-H., Lievin V., Lorrot M., Servin A.L.: Antagonistic activity of Lactobacillus acidophilus LB against intracellular Salmonella enterica serovar typhimurium infecting human enterocyte-like Caco-2/TC-7 cells. Appl.Environ.Microbiol.66, 1152–1157 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Cummings J.H., Branch W.J.: Fermentation and production of short chain fatty acids in human large intestine, pp. 131–152 in G.B. Vahouny, D. Kritchevesky (Eds): Dietary Fiber: Basic and Clinical Aspects. Plenum Press, New York 1990.

    Google Scholar 

  • Cummings J.H., Pomare E.W., Branch W.J., Naylor C.P.E., MacFarlane G.T.: Short-chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut28, 1221–1227 (1987).

    Article  PubMed  CAS  Google Scholar 

  • Elewaut D., DiDonato J.A., Kim J.M., Truong F., Eckmann L., Kagnoff M.F.: NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J.Immunol.163, 1457–1466 (1999).

    PubMed  CAS  Google Scholar 

  • Fajdiga S., Koninkx J.F.J.G., Tooten P.C.J., Marinšek-Logar R.: Interference of Salmonella enteritidis and Lactobacillus spp. with IL-8 levels and transepithelial electrical resistance of enterocyte-like Caco-2 cells. Folia Microbiol.51, 286–272 (2006).

    Article  Google Scholar 

  • Frankel W.L., Zhang W., Singh A., Klurfeld D.M., Don S., Sakata T., Modlin I., Rombeau J.L.: Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology106, 375–380 (1994).

    PubMed  CAS  Google Scholar 

  • Fukushima Y., Kawata Y., Hara H., Terada A., Mitsuoka T.: Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. Internat.J.Food Microbiol.42, 39–44 (1998).

    Article  CAS  Google Scholar 

  • Gionchetti P., Rizello F., Venturi A., Brigidi P., Matteuzzi D., Bazzocchi G., Poggiolo G., Miglioli M., Campieri M.: Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind placebo-controlled trial. Gastroenterology119, 305–309 (2000a).

    Article  PubMed  CAS  Google Scholar 

  • Gionchetti P., Rizzello F., Venturi A., Campieri M.: Probiotics in infective diarrhea and inflammatory bowel diseases. J.Gastroenterol.Hepatol.15, 489–493 (2000b).

    Article  PubMed  CAS  Google Scholar 

  • Goldin B.R., Gorbach S.L., Saxelin M., Barakat S., Gualtieri L., Salminen S.: Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig.Dis.Sci.37, 121–128 (1992).

    Article  PubMed  CAS  Google Scholar 

  • Hobbie S., Chen L.M., Davis R.J., Galan J.E.: Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J.Immunol.159, 5550–5559 (1997).

    PubMed  CAS  Google Scholar 

  • Horosová K., Bujňáková D., Kmeť V.: Effect of lactobacilli on E. coli adhesion to Caco-2 cells in vitro. Folia Microbiol.51, 281–282 (2006).

    Article  Google Scholar 

  • Huang N., Katz J.P., Martin D.R., Wu G.D.: Inhibition of IL-8 gene expression in Caco-2 cells by compounds which induce histone hyperacetylation. Cytokine9, 27–36 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Hudcovic T., Štěpánková R., Kozáková H., Hrnčíř T., Tlaskalová-Hogenová H.: Effects of monoclonization with Escherichia coli strains O6K13 and Nissle 1917 on the development of experimentally induced acute and chronic intestinal inflammation in germ-free immunocompetent and immunodeficient mice. Folia Microbiol.52, 618–626 (2007).

    Article  CAS  Google Scholar 

  • Kokešová A., Frolová L., Kverka M., Sokol D., Rossmann P., Bártová J., Tlaskalová-Hogenová H.: Oral administration of probiotic bacteria (E. coli Nissle, E. coli O83, Lactobacillus casei) influences the severity of dextran-sodium-sulfate-induced colitis in BALB/c mice. Folia Microbiol.51, 478–484 (2006).

    Article  Google Scholar 

  • Kopečný J., Zorec M., Mrázek J., Kobayashi Y., Marinšek-Logar R.: Butyrivibrio hungatei sp.nov. and Pseudobutyrivibrio xylanivorans sp.nov., butyrate-producing bacteria from the rumen. Internat.J.Syst.Evol.Microbiol.53, 201–209 (2003).

    Article  CAS  Google Scholar 

  • Koninkx J.F.J.G.: Enterocyte-like Caco-2 cells as a tool to study lectin interaction, pp. 81–101 in A. Pusztai, S. Bardocz (Eds): Lectins: Biomedical Perpectives. Taylor and Francis, London 1995.

    Google Scholar 

  • Koninkx J.F.J.G., Hendriks H.G.C.J.M., van Rossum J.M.A., van den Ingh T.S.G.A.M., Mouwen J.M.V.M.: Interaction of legume lectins with the cellular metabolism of differentiated Caco-2 cells. Gastroenterology102, 1516–1523 (1992).

    PubMed  CAS  Google Scholar 

  • Koyasu S., Nishida E., Kadowaki T., Matsuzaki F., Iida K., Harada F., Kasuga M., Sakai H., Yahara I.: Two mammalian heat shock proteins, Hsp90 and Hsp100, are actin binding proteins. Proc.Nat.Acad.Sci.USA83, 8054–8058 (1986).

    Article  PubMed  CAS  Google Scholar 

  • Liang P., MacRae T.H.: Molecular chaperones and the cytoskeleton. J.Cell Sci.110, 1431–1440 (1997).

    PubMed  CAS  Google Scholar 

  • Mackie R.I., Sghir A., Gaskins H.R.: Developmental microbial ecology of the neonatal gastrointestinal tract. Am.J.Clin.Nutr.69, 1035S–1045S (1999).

    PubMed  CAS  Google Scholar 

  • Malago J.J., Koninkx J.F.J.G., van Dijk J.E.: The heat shock response and cytoprotection of the intestinal epithelium. Cell. Stress & Chaperones7, 191–199 (2002).

    Article  CAS  Google Scholar 

  • Malago J.J., Koninkx J.F.J.G., Ovelgönne H.H., van Asten F.J.A.M., Swennenhuis J.F., van Dijk J.E.: Expression levels of heat shock proteins in enterocyte-like Caco-2 cells after exposure to Salmonella enteritidis. Cell Stress & Chaperones8, 194–203 (2003).

    Article  CAS  Google Scholar 

  • Malago J.J., Koninkx J.F.J.G., Tooten P.C.J., van Liere E.A., van Dijk J.E.: Anti-inflammatory properties of heat shock protein 70 and butyrate on Salmonella-induced interleukin-8 secretion in enterocyte-like Caco-2 cells. Clin.Exp.Immunol.141, 62–71 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Malin M., Suomalainen H., Saxelin M., Isolauri E.: Promotion of IgA immune response in patients with Crohn’s disease by oral bacteriotherapy with Lactobacillus GG. Ann.Nutr.Metab.40, 137–145 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Musch M.W., Sugi K., Straus D., Chang E.B.: Heat shock protein 72 protects against oxidant-induced injury of barrier function of human colonic epithelial Caco-2/bbe cells. Gastroenterology117, 115–122 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Nemeth E., Fajdiga S., Malago J., Koninkx J., Tooten P, van Dijk J.: Inhibition of Salmonella-induced IL-8 synthesis and expression of Hsp70 in enterocyte-like Caco-2 cells after exposure to non-starter lactobacilli. Internat.J.Food Microbiol.112, 266–274 (2006).

    Article  CAS  Google Scholar 

  • Nurmi E., Rantale M.: New aspects of Salmonella infection in broiler production. Nature241, 210–211 (1973).

    Article  PubMed  CAS  Google Scholar 

  • Ovelgönne J.H., Koninkx J.F.J.G., Pusztai A., Bardocz S., Kok W., Ewen S.W.B., Hendriks H.G.C.J.M., van Dijk J.E.: Decreased level of heat shock proteins in gut epithelial cells after exposure to plant lectins. Gut46, 679–687 (2000).

    Article  PubMed  Google Scholar 

  • Paton A.W., Morona R., Paton J.C.: Designer probiotics for prevention of enteric infections. Nature Rev.Microbiol.4, 193–200 (2006).

    Article  CAS  Google Scholar 

  • Perdigon G., de Macias M.E., Alvarez S., Oliver G., de Ruiz Halgado A.A.: Effect of perorally administered lactobacilli on macrophage activation in mice. Infect.Immun.53, 404–410 (1986).

    PubMed  CAS  Google Scholar 

  • Pinto M., Robine-Leon S., Appay M.D., Kedinger M., Triadou N., Dussaulx E., Lacroix B., Simon-Assmann P., Haffen K., Fogh J., Zweibaum A.: Enterocyte-like differentiation and polarization of the human colon carcinoma cell line Caco-2 in culture. Biol.Cell47, 323–330 (1883).

    Google Scholar 

  • Pusztai A., Grant G., Spencer R.J., Duguid T.J., Brown D.S., Ewen S.W.B., Peumans W.J., van Damme E.J.M., Bardocz S.: Kidney bean lectin induced Escherichia coli overgrowth in the small intestine is blocked by GNA, a mannose-specific lectin. J.Appl.Bacteriol.75, 360–368 (1993).

    PubMed  CAS  Google Scholar 

  • Pusztai A., Ewen S.W.B., Grant G., Peumans W.J., van Damme E.J.M., Coates M.E., Bardocz S.: Lectins and also bacteria modify the glycosylation of gut surface receptors in the rat. Glycoconjugate J.12, 22–35 (1995).

    Article  CAS  Google Scholar 

  • Ren H., Musch M.W., Kojima K., Boone D., Ma A.: Short-chain fatty acids induce intestinal epithelial heat shock protein 25 expression in rats and IEC 18 cells. Gastroenterology121, 631–639 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Rousseaux C., Thuru X., Gelot A., Barnich N., Neut C., Dubuqouy L., Dubuquoy C., Merour E., Geboes K., Chamaillard M., Ouwehand A., Leyer G., Carcano D., Colombel J.F., Ardid D., Desreumaux P.: Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nature Med.13, 35–37 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Sugita T., Togawa M.: Efficacy of lactobacillus preparation biolactis powder in children with rotavirus enteritis. Jap.J.Ped.47, 2755–2762 (1994).

    Google Scholar 

  • Trebichavský I., Šplíchal I.: Probiotics manipulate host cytokine response and induce antimicrobial peptides. Folia Microbiol.51, 507–510 (2006).

    Article  Google Scholar 

  • Treem W.R., Ahsan N., Shoup M., Hyams J.: Fecal short-chain fatty acids in children with inflammatory bowel disease. J.Pediatr.Gastroenterol.Nutr.18, 159–164 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Yoo C., Lee S., Lee C., Kim Y.W., Han S.K., Shim Y.: Anti-inflammatory effect of heat shock protein induction is related to stabilization of IκBα through preventing IκB kinase activation in respiratory epithelial cells. J.Immunol.164, 5416–5423 (2000).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. F. J. G. Koninkx.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koninkx, J.F.J.G., Malago, J.J. The protective potency of probiotic bacteria and their microbial products against enteric infections-review. Folia Microbiol 53, 189–194 (2008). https://doi.org/10.1007/s12223-008-0023-0

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-008-0023-0

Keywords

Navigation