Authors:
S. Bereswill Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Berlin, Germany

Search for other papers by S. Bereswill in
Current site
Google Scholar
PubMed
Close
,
A. Fischer Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Berlin, Germany

Search for other papers by A. Fischer in
Current site
Google Scholar
PubMed
Close
,
I. R. Dunay Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Berlin, Germany
Department of Microbiology and Hygiene, University of Magdeburg, Magdeburg, Germany

Search for other papers by I. R. Dunay in
Current site
Google Scholar
PubMed
Close
,
A. A. Kühl Department of Internal Medicine, Rheumatology and Clinical Immunology/Research Center Immunosciences (RCIS), Charité, University Medicine Berlin, Berlin, Germany

Search for other papers by A. A. Kühl in
Current site
Google Scholar
PubMed
Close
,
U. B. Göbel Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Berlin, Germany

Search for other papers by U. B. Göbel in
Current site
Google Scholar
PubMed
Close
,
O. Liesenfeld Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Berlin, Germany

Search for other papers by O. Liesenfeld in
Current site
Google Scholar
PubMed
Close
, and
M. M. Heimesaat Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Berlin, Germany
Department of Microbiology and Hygiene, Charité, University Medicine Berlin, Centrum 5, Campus Benjamin Franklin, Hindenburgdamm 27, D-12203, Berlin, Germany

Search for other papers by M. M. Heimesaat in
Current site
Google Scholar
PubMed
Close
Restricted access

Abstract

Non-pathogenic Escherichia coli (Ec) strains K12 (EcK12) and Nissle 1917 (EcN) are used for gene technology and probiotic treatment of intestinal inflammation, respectively. We investigated intestinal colonization and potential pro-inflammatory properties of EcK12, EcN, and commensal E. coli (EcCo) strains in Toxoplasma (T.) gondii-induced acute ileitis. Whereas gnotobiotic animals generated by quintuple antibiotic treatment were protected from ileitis, mice replenished with conventional microbiota suffered from small intestinal necrosis 7 days post-T. gondii infection (p.i.). Irrespective of the Ec strain, recolonized mice revealed mild to moderate histopathological changes in their ileal mucosa. Upon stable recolonization with EcK12, EcN, or EcCo, development of inflammation was accompanied by pro-inflammatory responses at day 7 p.i., including increased ileal T lymphocyte and apoptotic cell numbers compared to T. gondii-infected gnotobiotic controls. Strikingly, either Ec strain was capable to translocate to extraintestinal locations, such as MLN, spleen, and liver. Taken together, Ec strains used in gene technology and probiotic treatment are able to exert inflammatory responses in a murine model of small intestinal inflammation. In conclusion, the therapeutic use of Ec strains in patients with broad-spectrum antibiotic treatment and/or intestinal inflammation should be considered with caution.

  • 1. H.W. Smith 1978 Is it safe to use Escherichia coli K 12 in recombinant DNA experiments? J Infect Dis 137 655 660.

  • 2. R. Curtiss 3rd 1978 Biological containment and cloning vector transmissibility J Infect Dis 137 668 675.

  • 3. J. Lederberg E.L. Tatum 1946 Gene recombination in Escherichia coli Nature 158 558.

  • 4. H.W. Smith 1975 Survival of orally administered E. coli K 12 in alimentary tract of man Nature 255 500 502.

  • 5. A.K. Moller M.P. Leatham T. Conway P.J. Nuijten L.A. de Haan et al.2003 An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine Infect Immun 71 2142 2152.

    • Search Google Scholar
    • Export Citation
  • 6. Hayashi K , Morooka N, Yamamoto Y, Fujita K, Isono K et al.: Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2006. 0007 (2006).

    • Search Google Scholar
    • Export Citation
  • 7. R. Lodinova-Zadnikova U. Sonnenborn 1997 Effect of preventive administration of a nonpathogenic Escherichia coli strain on the colonization of the intestine with microbial pathogens in newborn infants Biol Neonate 71 224 232.

    • Search Google Scholar
    • Export Citation
  • 8. F. Shanahan 2000 Probiotics and inflammatory bowel disease: is there a scientific rationale? Inflamm Bowel Dis 6 107 115.

  • 9. F. Shanahan 2001 Probiotics in inflammatory bowel disease Gut 48 609.

  • 10. A. Nissle 1918 Die antagonistische Behandlung chronischer Darmstörungen mit Colibekaterien Med Klin 2 29 30.

  • 11. G. Blum R. Marre J. Hacker 1995 Properties of Escherichia coli strains of serotype O6 Infection 23 234 236.

  • 12. J. Henker M. Laass B.M. Blokhin Y.K. Bolbot V.G. Maydannik et al.2007 The probiotic Escherichia coli strain Nissle 1917 (EcN) stops acute diarrhoea in infants and toddlers Eur J Pediatr 166 311 318.

    • Search Google Scholar
    • Export Citation
  • 13. W. Kruis P. Fric J. Pokrotnieks M. Lukas B. Fixa et al.2004 Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine Gut 53 1617 1623.

    • Search Google Scholar
    • Export Citation
  • 14. S. Fujimori A. Tatsuguchi K. Gudis T. Kishida K. Mitsui et al.2007 High dose probiotic and prebiotic cotherapy for remission induction of active Crohn's disease J Gastroenterol Hepatol 22 1199 1204.

    • Search Google Scholar
    • Export Citation
  • 15. O. Liesenfeld J. Kosek J.S. Remington Y. Suzuki 1996 Association of CD4+ T cell-dependent, interferon-gamma-mediated necrosis of the small intestine with genetic susceptibility of mice to peroral infection with Toxoplasma gondii J Exp Med 184 597 607.

    • Search Google Scholar
    • Export Citation
  • 16. O. Liesenfeld 2002 Oral infection of C 57BL/6 mice with Toxoplasma gondii: a new model of inflammatory bowel disease? J Infect Dis 185Suppl1 S96 S101.

    • Search Google Scholar
    • Export Citation
  • 17. M.M. Heimesaat S. Bereswill A. Fischer D. Fuchs D. Struck et al.2006 Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii J Immunol 177 8785 8795.

    • Search Google Scholar
    • Export Citation
  • 18. I.A. Khan J.D. Schwartzman T. Matsuura L.H. Kasper 1997 A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice Proc Natl Acad Sci U S A 94 13955 13960.

    • Search Google Scholar
    • Export Citation
  • 19. F.J. Mennechet L.H. Kasper N. Rachinel W. Li A. Vandewalle et al.2002 Lamina propria CD4+ T lymphocytes synergize with murine intestinal epithelial cells to enhance proinflammatory response against an intracellular pathogen J Immunol 168 2988 2996.

    • Search Google Scholar
    • Export Citation
  • 20. O. Liesenfeld H. Kang D. Park T.A. Nguyen C.V. Parkhe et al.1999 TNF-alpha, nitric oxide and IFN-gamma are all critical for development of necrosis in the small intestine and early mortality in genetically susceptible mice infected perorally with Toxoplasma gondii Parasite Immunol 21 365 376.

    • Search Google Scholar
    • Export Citation
  • 21. A. Vossenkamper D. Struck C. Alvarado-Esquivel T. Went K. Takeda et al.2004 Both IL-12 and IL-18 contribute to small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii, but IL-12 is dominant over IL-18 in parasite control Eur J Immunol 34 3197 3207.

    • Search Google Scholar
    • Export Citation
  • 22. M. Munoz M.M. Heimesaat K. Danker D. Struck U. Lohmann et al.2009 Interleukin (IL)-23 mediates Toxoplasma gondiiinduced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. 2 and IL-22 but independent of IL-17 J Exp Med 206 3047 3059.

    • Search Google Scholar
    • Export Citation
  • 23. D. Struck I. Frank S. Enders U. Steinhoff C. Schmidt A. Stallmach O. Liesenfeld M.M. Heimesaat 2012 Treatment with Interleukin-18 binding protein ameliorates Toxoplasma gondii-induced small intestinal pathology that is induced by bone marrow cell-derived Interleukin-18 Eur J Microbiol Immunol 2 249 257.

    • Search Google Scholar
    • Export Citation
  • 24. M.M. Heimesaat A. Fischer H.K. Jahn J. Niebergall M. Freudenberg et al.2007 Exacerbation of murine ileitis by Toll-like receptor 4 mediated sensing of lipopolysaccharide from commensal Escherichia coli Gut 56 941 948.

    • Search Google Scholar
    • Export Citation
  • 25. C. Erridge S.H. Duncan S. Bereswill M.M. Heimesaat 2010 The induction of colitis and ileitis in mice is associated with marked increases in intestinal concentrations of stimulants of TLRs 2, 4, and 5 PLoS One 5 e9125.

    • Search Google Scholar
    • Export Citation
  • 26. Haag LM , Fischer A, Otto B, Plickert R, Kühl AA et al.: Intestinal microbiota shifts towards elevated commensal Escherichia coli loads abrogate colonization resistance against Campylobacter jejuni in mice. PLoS One 7, e35988 (2012).

    • Search Google Scholar
    • Export Citation
  • 27. M.M. Heimesaat A. Fischer B. Siegmund A. Kupz J. Niebergall et al.2007 Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4 PLoS One 2 e662.

    • Search Google Scholar
    • Export Citation
  • 28. M.M. Heimesaat A. Nogai S. Bereswill R. Plickert A. Fischer et al.2010 MyD88/TLR9 mediated immunopathology and gut microbiota dynamics in a novel murine model of intestinal graft-versus-host disease Gut 59 1079 1087.

    • Search Google Scholar
    • Export Citation
  • 29. S. Bereswill M. Munoz A. Fischer R. Plickert L.M. Haag et al.2010 Anti-inflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation PLoS One 5 e15099.

    • Search Google Scholar
    • Export Citation
  • 30. L.M. Haag A. Fischer B. Otto U. Grundmann A.A. Kühl et al.2012 Campylobacter jejuni infection of infant mice: acute enterocolitis is followed by asymptomatic intestinal and extra-intestinal immune response Eur J Microbiol Immunol 2 2 11.

    • Search Google Scholar
    • Export Citation
  • 31. Bereswill S , Fischer A, Plickert R, Haag LM, Otto B et al.: Novel murine infection models provide deep insights into the “menage a trois” of Campylobacter jejuni, microbiota and host innate immunity. PLoS One 6, e20953 (2011).

    • Search Google Scholar
    • Export Citation
  • 32. P.I. Zigra V.E. Maipa Y.P. Alamanos 2007 Probiotics and remission of ulcerative colitis: a systematic review Neth J Med 65 411 418.

    • Search Google Scholar
    • Export Citation
  • 33. A.C. Senok A.Y. Ismaeel G.A. Botta 2005 Probiotics: facts and myths Clin Microbiol Infect 11 958 966.

  • 34. S. Lebeer J. Vanderleyden S.C. De Keersmaecker 2010 Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens Nat Rev Microbiol 8 171 184.

    • Search Google Scholar
    • Export Citation
  • 35. I. Trebichavsky I. Splichal V. Rada A. Splichalova 2010 Modulation of natural immunity in the gut by Escherichia coli strain Nissle 1917 Nutr Rev 68 459 464.

    • Search Google Scholar
    • Export Citation
  • 36. A. Bleich J.P. Sundberg A. Smoczek R. von Wasielewski M.F. de Buhr et al.2008 Sensitivity to Escherichia coli Nissle 1917 in mice is dependent on environment and genetic background Int J Exp Pathol 89 45 54.

    • Search Google Scholar
    • Export Citation
  • 37. S.N. Ukena A.M. Westendorf W. Hansen M. Rohde R. Geffers et al.2005 The host response to the probiotic Escherichia coli strain Nissle 1917: specific up-regulation of the proinflammatory chemokine MCP-1 BMC Med Genet 6 43.

    • Search Google Scholar
    • Export Citation
  • 38. R.A. Welch V. Burland G. Plunkett 3rd P. Redford P. Roesch et al.2002 Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli Proc Natl Acad Sci U S A 99 17020 17024.

    • Search Google Scholar
    • Export Citation
  • 39. L. Grozdanov C. Raasch J. Schulze U. Sonnenborn G. Gottschalk et al.2004 Analysis of the genome structure of the non-pathogenic probiotic Escherichia coli strain Nissle 1917 J Bacteriol 186 5432 5441.

    • Search Google Scholar
    • Export Citation
  • 40. J. Sun F. Gunzer A.M. Westendorf J. Buer M. Scharfe et al.2005 Genomic peculiarity of coding sequences and metabolic potential of probiotic Escherichia coli strain Nissle 1917 inferred from raw genome data J Biotechnol 117 147 161.

    • Search Google Scholar
    • Export Citation
  • 41. E. Adam L. Delbrassine C. Bouillot V. Reynders A.C. Mailleux et al.2010 Probiotic Escherichia coli Nissle 1917 activates DC and prevents house dust mite allergy through a TLR4-dependent pathway Eur J Immunol 40 1995 2005.

    • Search Google Scholar
    • Export Citation
  • 42. H.S. Warren C. Fitting E. Hoff M. Adib-Conquy L. Beasley-Topliffe et al.2010 Resilience to bacterial infection: difference between species could be due to proteins in serum J Infect Dis 201 223 232.

    • Search Google Scholar
    • Export Citation
  • 43. K. Guenther E. Straube W. Pfister A. Guenther A. Huebler 2010 Severe sepsis after probiotic treatment with Escherichia coli NISSLE 1917 Pediatr Infect Dis J 29 188 189.

    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita, Prof. Dr. Pharm, Dr. rer. nat., University of Magdeburg, Germany

Editor(s)-in-Chief: Heimesaat, Markus M., Prof. Dr. med., Charité - University Medicine Berlin, Germany

Editorial Board

  • Berit Bangoura, Dr. DVM. PhD,  University of Wyoming, USA
  • Stefan Bereswill, Prof. Dr. rer. nat., Charité - University Medicine Berlin, Germany
  • Dunja Bruder, Prof. Dr. rer. nat., University of Magdeburg, Germany
  • Jan Buer, Prof. Dr. med., University of Duisburg, Germany
  • Edit Buzas, Prof. Dr. med., Semmelweis University, Hungary
  • Renato Damatta, Prof. PhD, UENF, Brazil
  • Maria Deli, MD, PhD, DSc, Biological Research Center, HAS, Hungary
  • Olgica Djurković-Djaković, Prof. Phd, University of Belgrade, Serbia
  • Jean-Dennis Docquier, Prof. Dr. med., University of Siena, Italy
  • Zsuzsanna Fabry, Prof. Phd, University of Washington, USA
  • Ralf Ignatius, Prof. Dr. med., Charité - University Medicine Berlin, Germany
  • Achim Kaasch, Prof. Dr. med., Otto von Guericke University Magdeburg, Germany
  • Oliver Liesenfeld, Prof. Dr. med., Inflammatix, USA
  • Matyas Sandor, Prof. PhD, University of Wisconsin, USA
  • Ulrich Steinhoff, Prof. PhD, University of Marburg, Germany
  • Michal Toborek, Prof. PhD, University of Miami, USA
  • Susanne A. Wolf, PhD, MDC-Berlin, Germany

 

Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildiko.dunay@med.ovgu.de

Indexing and Abstracting Services:

  • PubMed Central
  • Scopus
  • ESCI
  • CABI
  • CABELLS Journalytics

 

2023  
Web of Science  
Total Cites
WoS
674
Journal Impact Factor 3.3
Rank by Impact Factor

Q2

Impact Factor
without
Journal Self Cites
3.1
5 Year
Impact Factor
3.2
Scimago  
Scimago
H-index
15
Scimago
Journal Rank
0.601
Scimago Quartile Score Microbiology (medical) (Q2)
Microbiology (Q3)
Immunology and Allergy (Q3)
Immunology (Q3)
Scopus  
Scopus
Cite Score
5.0
Scopus
CIte Score Rank
Microbiology (medical) Q2
Scopus
SNIP
0.832

 

European Journal of Microbiology and Immunology
Publication Model Gold Open Access
Online only
Submission Fee none
Article Processing Charge 600 EUR/article
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription Information Gold Open Access
Purchase per Title  

European Journal of Microbiology and Immunology
Language English
Size A4
Year of
Foundation
2011
Volumes
per Year
1
Issues
per Year
4
Founder Akadémiai Kiadó
Founder's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Apr 2024 32 0 0
May 2024 23 0 0
Jun 2024 36 0 0
Jul 2024 92 0 0
Aug 2024 63 0 0
Sep 2024 39 0 0
Oct 2024 27 0 0