Skip to main content

Advertisement

Springer Nature Link
Log in

Effects of monocolonization withEscherichia coli strains O6K13 and nissle 1917 on the development of experimentally induced acute and chronic intestinal inflammation in germ-free immunocompetent and immunodeficient mice

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Germ-free immunocompetent (BALB/c) and immunodeficient (SCID) mice were colonized either byE. coli O6K 13 or byE. coli strain Nissle 1917 and intestinal inflammation was induced by administering 2.5 % dextran sulfate sodium (DSS) in drinking water. Controls were germ-free mice which demonstrated only mild inflammatory changes after induction of an acute intestinal inflammation with DSS as compared with conventional mice in which acute colitis of the colon mucosa similar to human ulcerative colitis is elicited. In mice monocolonized with the nonpathogenicE. coli Nissle 1917 the inflammatory disease did not develop (damage grade 0) while animals monocolonized with uropathogenicE. coli O6K 13 exhibited inflammatory changes similar to those elicited in conventionally reared mice (damage grade 3). In the chronic inflammation model, immunocompetent BALB/c mice monocolonized withE. coli Nissle 1917 showed no conspicuous inflammatory changes of the colon mucosa whereas those monocolonized withE. coli O6K 13 developed colon inflammation associated with marked infiltration of inflammatory cells. In contrast to germ-free immunodeficient SCID mice that died after application of DSS, the colon mucosa of SCID mice monoassociated withE. coli Nissle 1917 exhibited only moderate inflammatory changes which were less pronounced than changes of colon mucosa of SCID mice monoassociated withE. coli O6K 13.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CFU:

colony forming units

CV:

conventional(ly)

DSS:

dextran sulfate sodium

GF:

germ-free

IBD:

inflammatory bowel disease

IL-2:

interleukin-2

INF-γ:

interferon γ

SCID:

severe combined immunodeficiency

UC:

ulcerative colitis

References

  • Altenhoefer A., Oswald S., Sonnenborn U., Enders C., Schulze J., Hacker J., Oelschlaeger T.A.: The probioticEscherichia coli strain Nissle 1917 interferes with invasion of human intestinal epithelial cells by different enteroinvasive bacterial pathogens.Immunol.Med.Microbiol.9, 223–229 (2004).

    Article  CAS  Google Scholar 

  • Blum G., Marre R., Hacker J.: Properties ofEscherichia coli strains of serotype O6.Infection23, 234–236 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Bylund-Fellenius A.C., Lanström E., Axelsson L.G., Midtvedt T.: Experimental colitis induced by dextran sulfate in normal and germfree mice.Microb.Ecol.Health Dis.7, 207–215 (1994).

    Article  Google Scholar 

  • Cebra J.J.: Influences of microbiota on intestinal immune system development.Am.J.Clin.Nutr.69, 1046–1051 (1999).

    Google Scholar 

  • Cooper H.S., Murthy S.N.S., Snak R.S., Sedergran D.S.: Clinicopathologic study of dextran sulfate sodium experimental murine colitis.U.S. & Canad.Acad.Pathol.69, 238 (1993).

    CAS  Google Scholar 

  • Dahlgren U.I.H., Wold A.E., Hanson L.A., Mercereau-Puijalon O., Midtvedt T.: Expression of a dietary protein inEscherichia coli renders it strongly antigenic to gut lymphoid tissue.Immunology73, 394–397 (1991).

    PubMed  CAS  Google Scholar 

  • Darfeuille-Michaud A., Boudeau J., Bulois P., Neut C., Glasser A.L., Barnich N., Bringer M.A., Swidsinski A., Beaugerie L., Colombel J.F.: High prevalence of adherent-invasiveEscherichia coli associated with ileal mucosa in Crohn’s disease.Gastroenterology127, 412–421 (2004).

    Article  PubMed  Google Scholar 

  • Dianda L., Hanby A.M., Wright N.A., Sebesteny A., Hayday A.C., Owen M.J.: T-Cell receptor-αβ-deficient mice fail to develop colitis in the absence of a microbial environment.Am.J.Pathol.150, 91–97 (1997).

    PubMed  CAS  Google Scholar 

  • Dieleman Levinus A., Ridwan Ben U., Tennyson Gary S., Beagley Kenneth W., Bucy R.P., Elson C.O.: Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice.Gastroenterology107, 1643–1652 (1994).

    PubMed  CAS  Google Scholar 

  • Elson C.O., Cong Y., Kabal N.: Immuno-bacterial homeostasis in the gut: new insight into old enigma.Sem.Immunol.13, 187–194 (2001).

    Article  CAS  Google Scholar 

  • Farkas S., Herfarth H., Rössle M., Schroeder J., Steinbauer M., Guba A.M., Beham A., Schölmerich J., Jauch K.-W., Anthuber M.: Quantification of mucosal leukocyte endothelial cell interaction byin vivo fluorescence microscopy in experimental colitis in mice.Clin.Exp.Immunol.126, 250–258 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Faubion W.A., Sandborn W.J.: Probiotic therapy withE. coli for ulcerative colitis: the good with bad.Gastroenterology118, 630–631 (2001).

    Article  Google Scholar 

  • Fazzi P., Ciancaglini E., Soforza G.: Differential fluorescent staining method for detection of bacteria in blood cultures, cerebrospinal fluid and other clinical specimens.Eur.J.Clin.Microbiol.Infect.Dis.21, 373–378 (2002).

    Article  Google Scholar 

  • Folwaczny C.: Probiotics for prevention of ulcerative colitis recurrence: alternative medicine added to standard treatment?Gastroenterology38, 547–550 (2000).

    CAS  Google Scholar 

  • García-Lafuente A., Antonin M., Guarner F., Crespo E., Salas A., Forcada P., Laguarda M., Cavaldá J., Baena J.A., Vilaseca J., Malagelada J.R.: Incrimination of anaerobic bacteria in the induction of experimental colitis.Am.J.Physiol.272, G10-G15 (1997).

    PubMed  Google Scholar 

  • Grozdanov L., Rasech C., Schulze J., Sonnenborn U., Gottschalk G., Hacker J., Dobrindt U.: Analysis of the genome structure of the nonpathogenic probioticEscherichia coli Nissle 1917.J.Bacteriol.186, 5432–5441 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Hart A.L., Stagg A.J., Kamm A.J.: Related articles, links use of probiotics in the treatment of inflammatory bowel disease.J.Clin.Gastroenterol.36, 111–119 (2003).

    Article  PubMed  Google Scholar 

  • Hudcovic T., Štěpánková R., Cebra J., Tlaskalová-Hogenová H.: The role of microflora in the development of intestinal inflammation: acute and chronic colitis induced by dextran sulfate in germ-free and conventionally reared immunocompetent and immunodeficient mice.Folia Microbiol.46, 565–572 (2001).

    Article  CAS  Google Scholar 

  • Hulten K., Almashhrawi A., El Zastari F.A.: Antibacterial therapy for Crohn’s disease: a review emphasizing therapy directed against mycobacteria.Dig.Dis.Sci.45, 445–456 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Kitajima S., Morimoto M., Sagara E., Shimizu C., Ikeda Z.: Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice.Exp.Anim.50, 387–395 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Kocourková I., Žádníková R., Žižka J., Rosová V.: Effect of oral application of a probioticE. coli strain on the intestinal microflora of children of allergic mothers during the first year of life.Folia Microbiol.52, 189–193 (2007).

    Article  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 

  • Kruis W., Frič P., Pokrotnieks J., Lukáš M., Fixa B., Kaščák M., Kamm M.A., Weismueller J., Beglinger C., Stolte M., Wolff C., Schulze J.: Maintaining remission of ulcerative colitis with the probioticEscherichia coli Nissle 1917 is as effective as with standard mesalazine.Gut53, 1617–1623 (2004).

    Article  PubMed  CAS  Google Scholar 

  • La Ferla K., Seegert D., Schreiber S.: Activation of NF-κB in intestinal byE. coli strain isolate from the colonic mucosa of IBD patients.Internat.J.Colorect.Dis.19, 334–342 (2004).

    Article  Google Scholar 

  • Mercereau-Puijalon O., Royal A., Cami B., Garapin A., Krust A., Gannon F., Kourilsky P.: Synthesis of an ovalbumin-like protein byEscherichia coli K-12 harboring a recombinant plasmid.Nature275, 505–510 (1978).

    Article  PubMed  CAS  Google Scholar 

  • Okayasu I., Hatakeyama S., Yamada M., Ohkusa T., Inagi Y., Nakya R.: A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice.Gastroenterology98, 694–702 (1990).

    PubMed  CAS  Google Scholar 

  • Powrie F., Leach M.W.: Genetic and spontaneous models of inflammatory bowel disease in rodents: evidence for abnormalities in mucosal immune regulation.Ther.Immunol.2, 115–123 (1995).

    PubMed  CAS  Google Scholar 

  • Schuppler M., Lötzsch K., Waidmann M., Autenrieth I.B.: An abundance ofEscherichia coli is harbored by the mucosa associated bacterial flora of interleukin-2 deficient mice.Infect.Immun.72, 1983–1990 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Sellon R.K., Tonkonogy S., Schultz M., Dieleman L.A., Grenther W., Balish E., Rennick D.M., Sartor R.B.: Resident enteric bacteria are necessary in interleukin-10-deficient mice.Infect.Immun.66, 5224–5231 (1998).

    PubMed  CAS  Google Scholar 

  • Shanahan F.: Probiotics and inflammatory bowel disease: is there a scientific rationale?Inflamm.Bowel Dis.6, 107–115 (2000).

    PubMed  CAS  Google Scholar 

  • Štěpánková R.: Rearing of germ-free rats, mice, and rabbits, pp. 1537–1542 inImmunology Methods Manual (I. Lefkovits, Ed.),Gnotobiological Models (H. Tlaskalová, J. Šterzl, sect. Eds).Academic Press, New York 1997.

    Google Scholar 

  • Swidsinski A., Landhoff A., Pernthaller A., Swidsinski S., Loening-Baucke V., Ordner M., Weber J., Hoffmann U., Schreiber S., Dietel M., Lochs H.: Mucosal flora in inflammatory bowel disease.Gastroenterology122, 44–54 (2002).

    Article  PubMed  Google Scholar 

  • Tlaskalová-Hogenová H., Štěpánková R., Hudcovic T., Tučková L., Cukrowska B., Lodinová-Žádníková R., Kozáková H., Rossmann P., Bártová J., Sokol D., Funda D.P., Borovská D., Řeháková Z., Šinkora J., Hofman J., Drastich P., Kokešová A.: Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases.Immunol.Lett.93, 97–108 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Tlaskalová-Hogenová H., Tučková L., Štěpánková R., Hudcovic T., Palová-Jelínková L., Kozáková H., Rossmann P., Sanchez D., Cinová J., Hrnčíř T., Kverka M., Frolová L., Uhlig H., Powrie F., Bland P.: Involvement of innate immunity in the development of inflammatory and autoimmune diseases.Ann.N.Y.Acad.Sci.1051, 787–98 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Waidmann M., Bechtold O., Frick J., Lehr H., Schubert S., Dobrindt U., Loeffler J., Bohn E., Autenrieth I.B.:Bacteroides vulgatus protects againstEscherichia coli-induced colitis in gnotobiotic interleukin-2-deficient mice.Gastroenterology125, 162–178 (2003).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Immunology and Gnotobiology, Institute of Microbiology, Academy of Sciences of the Czech Republic, 549 22, Nový Hrádek, Czechia

    T. Hudcovic, R. Štěpánková, H. Kozáková, T. Hrnčíř & H. Tlaskalová-Hogenová

Authors
  1. T. Hudcovic
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. R. Štěpánková
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. H. Kozáková
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. T. Hrnčíř
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. H. Tlaskalová-Hogenová
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to T. Hudcovic.

Additional information

This study was supported by grants 303/04/0849 and 303/06/0974 ofCzech Science Foundation, by grant S500 200 572 of theAcademy of Sciences of the Czech Republic, byInstitutional Research Concept no. AV 0Z 5020 0510, and by grants 2B06 155 and 2B06 053 of theMinistry of Education, Youth and Sports of the Czech Republic.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hudcovic, T., Štěpánková, R., Kozáková, H. et al. Effects of monocolonization withEscherichia 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). https://doi.org/10.1007/BF02932191

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02932191

Keywords