1887

Abstract

Interleukin-10 gene-deficient ( ) mice show a hyper-reaction to normal intestinal bacteria and develop spontaneous colitis similar to that of human Crohn's disease when raised under conventional (but not germ-free) conditions. The lack of IL10 protein in these mice leads to changes in intestinal metabolic and signalling processes. The first aim of this study was to identify changes in the bacterial community of the caeca at 7 weeks of age (preclinical colitis) and at 12 weeks of age (when clinical signs of colitis are present), and establish if there were any changes that could be associated with the mouse genotype. We have previously shown that dietary n-3 and n-6 polyunsaturated fatty acids (PUFA) have anti-inflammatory effects and affect colonic gene expression profiles in mice; therefore, we also aimed to test the effect of the n-3 PUFA eicosapentaenoic acid (EPA) and the n-6 PUFA arachidonic acid (AA) on the bacterial community of caeca in both and C57 mice fed these diets. The lower number of caecal bacteria observed before colitis (7 weeks of age) in compared to C57 mice suggests differences in the intestinal bacteria that might be associated with the genotype, and this could contribute to the development of colitis in this mouse model. The number and diversity of caecal bacteria increased after the onset of colitis (12 weeks of age). The increase in caecal numbers in both inflamed and healthy C57 mice might be attributed to the dietary PUFA (especially dietary AA), and thus not be a cause of colitis development. A possible protective effect of mediated by PUFA supplementation and associated changes in the bacterial environment could be a subject for further investigation to define the mode of action of PUFA in colitis.

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2010-11-01
2024-03-29
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References

  1. Balish E., Warner T. 2002; Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol 160:2253–2257
    [Google Scholar]
  2. Barnett M. P., McNabb W. C., Cookson A. L., Zhu S., Davy M., Knoch B., Nones K., Hodgkinson A. J., Roy N. C. 2010; Changes in colon gene expression associated with increased colon inflammation in interleukin-10 gene-deficient mice inoculated with Enterococcus species. BMC Immunol 11:39
    [Google Scholar]
  3. Bibiloni R., Simon M. A., Albright C., Sartor B., Tannock G. W. 2005; Analysis of the large bowel microbiota of colitic mice using PCR/DGGE. Lett Appl Microbiol 41:45–51
    [Google Scholar]
  4. Burnens A. P., Stanley J., Morgenstern R., Nicolet J. 1994; Gastroenteritis associated with Helicobacter pullorum. Lancet 344:1569–1570
    [Google Scholar]
  5. Calder P. C. 2006; n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 83:6 Suppl1505S–1519S
    [Google Scholar]
  6. Carey M. C., Small D. M., Bliss C. M. 1983; Lipid digestion and absorption. Annu Rev Physiol 45:651–677
    [Google Scholar]
  7. Ceelen L. M., Decostere A., Van den Buick K., On S. L. W., Baele M., Ducatelle R., Haesebrouck F. 2006; Helicobacter pullorum in chickens. Belgium. Emerg Infect Dis 12:263–267
    [Google Scholar]
  8. Claesson M. J., O'Sullivan O., Wang Q., Nikkilä J., Marchesi J. R., Smidt H., de Vos W. M., Ross R. P., O'Toole P. 2009; Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE 4:e6669
    [Google Scholar]
  9. Colombel J. F., Lemann M., Cassagnou M., Bouhnik Y., Duclos B., Dupas J. L., Notteghem B., Mary J. Y. 1997; A controlled trial comparing ciprofloxacin with trial mesalazine for the treatment of active Crohn's disease. Gastroenterology 112:A951–A951
    [Google Scholar]
  10. Cummings J. H., Wiggins H. S., Jenkins D. J. A., Houston H., Jivraj T., Drasar B. S., Hill M. J. 1978; Influence of diets high and low in animal fat on bowel habit, gastrointestinal transit-time, fecal microflora, bile-acid, and fat excretion. J Clin Invest 61:953–963
    [Google Scholar]
  11. Das U. N. 2002; Essential fatty acids as possible enhancers of the beneficial actions of probiotics. Nutrition 18:786–789
    [Google Scholar]
  12. Eastwood M. A., Allgood G. S. 1995; The effect of olestra on breath gas production and faecal microbial counts. Eur J Clin Nutr 49:627–639
    [Google Scholar]
  13. Endo K., Kumemura M., Nakamura K., Fujisawa T., Suzuki K., Benno Y., Mitsuoka T. 1991; Effect of high cholesterol diet and polydextrose supplementation on the microflora, bacteria enzyme activity, putrefactive products, volatile fatty acid (VFA) profile, weight, and pH of the feces in healthy volunteers. Bifidobact Microflora 10:53–64
    [Google Scholar]
  14. Farnworth E. R., Chouinard Y. P., Jacques H., Venkatramanan S., Maf A. A., Defnoun S., Jones P. J. H. 2007; The effect of drinking milk containing conjugated linoleic acid on fecal microbiological profile, enzymatic activity, and fecal characteristics in humans. Nutr J 6:15
    [Google Scholar]
  15. Fox J. G., Gorelick P. L., Kullberg M. C., Ge Z. M., Dewhirst F. E., Ward J. M. 1999; Novel urease-negative Helicobacter species associated with colitis and typhlitis in IL-10-deficient mice. Infect Immun 67:1757–1762
    [Google Scholar]
  16. Frank D. N., Amand A. L. S., Feldmann R. A., Boedeker E. C., Harpaz N., Pace N. R. 2007; Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104:13780–13785
    [Google Scholar]
  17. Gui G. P. H., Thomas P. R. S., Tizard M. L. V., Lake J., Sanderson J. D., Hermon Taylor J. 1997; Two-year-outcomes analysis of Crohn's disease treated with rifabutin and macrolide antibiotics. J Antimicrob Chemother 39:393–400
    [Google Scholar]
  18. Heimesaat M. M., Bereswill S., Fischer A., Fuchs D., Struck D., Niebergall J., Jahn H.-K., Dunay I. R., Moter A. other authors 2006; Gram-negative bacteria aggravate murine small intestinal Th1-Type immunopathology following oral infection with Toxoplasma gondii. J Immunol 177:8785–8795
    [Google Scholar]
  19. Hudault S., Guignot J., Servin A. L. 2001; Escherichia coli strains colonising the gastrointestinal tract protect germfree mice against Salmonella typhimurium infection. Gut 49:47–55
    [Google Scholar]
  20. Huijsdens X. W., Linskens R. K., Mak M. T., Meuwissen S. G. M., Vandenbroucke-Grauls C., Savelkoul P. H. M. 2002; Quantification of bacteria adherent to gastrointestinal mucosa by real-time PCR. J Clin Microbiol 40:4423–4427
    [Google Scholar]
  21. Izcue A., Coombes J. L., Powrie F. 2006; Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol Rev 212:256–271
    [Google Scholar]
  22. Jett B. D., Huycke M. M., Gilmore M. S. 1994; Virulence of Enterococci. Clin Microbiol Rev 7:462
    [Google Scholar]
  23. Kankaanpää P. E., Salminen S. J., Isolauri E., Lee Y. K. 2001; The influence of polyunsaturated fatty acids on probiotic growth and adhesion. FEMS Microbiol Lett 194:149–153
    [Google Scholar]
  24. Kim S. C., Tonkonogy S. L., Albright C. A., Tsang J., Balish E. J., Braun J., Huycke M. M., Sartor R. B. 2005; Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128:891–906
    [Google Scholar]
  25. Kim S. C., Tonkonogy S. L., Karrasch T., Jobin C., Sartor R. B. 2007; Dual-association of gnotobiotic IL-10−/− mice with 2 nonpathogenic commensal bacteria induces aggressive pancolitis. Inflamm Bowel Dis 13:1457–1466
    [Google Scholar]
  26. Kishi D., Takahashi I., Kai Y., Tamagawa H., Iijima H., Obunai S., Nezu R., Ito T., Matsuda H., Kiyono H. 2000; Alteration of V β usage and cytokine production of CD4+ TCR ββ homodimer T cells by elimination of Bacteroides vulgatus prevents colitis in TCR α-chain-deficient mice. J Immunol 165:5891–5899
    [Google Scholar]
  27. Knoch B., Barnett M. P. G., Zhu S., Park Z. A., Nones K., Dommels Y. E. M., Knowles S. O., McNabb W. C., Roy N. C. 2009; Genome-wide analysis of dietary eicosapentaenoic acid- and oleic acid-induced modulation in colon inflammation of interleukin-10 gene-deficient mice. J Nutrigenet Nutrigenomics 2:9–28
    [Google Scholar]
  28. Knoch B., Barnett M. P. G., Cooney J., Barraclough D., Laing W., McNabb W. C., Zhu S., Park Z. A., MacLean P. & other authors (2010a). Molecular characterization of the onset and progression of colitis in interleukin-10 gene-deficient mice: a role for PPAR α. PPAR Res 2010621069
    [Google Scholar]
  29. Knoch B., Barnett M. P. G., McNabb W. C., Zhu S., Park Z. A., Khan A., Roy N. C. 2010b; Dietary arachidonic acid-mediated effects on colon inflammation using transcriptome analysis. Mol Nutr Food Res 54:S62–S74
    [Google Scholar]
  30. Madsen K. L., Doyle J. S., Tavernini M. M., Jewell L. D., Rennie R. P., Fedorak R. N. 2000; Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology 118:1094–1105
    [Google Scholar]
  31. Mangin I., Bonnet R., Seksik P., Rigottier-Gois L., Sutren M., Bouhnik Y., Neut C., Collins M. D., Colombel J. F. other authors 2004; Molecular inventory of faecal microflora in patients with Crohn's disease. FEMS Microbiol Ecol 50:25–36
    [Google Scholar]
  32. McCarthy J., O'Mahony L., O'Callaghan L., Sheil B., Vaughan E. E., Fitzsimons N., Fitzgibbon J., O'Sullivan G. C., Kiely B. other authors 2003; Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 52:975–980
    [Google Scholar]
  33. Nones K., Knoch B., Dommels Y. E. M., Paturi G., Butts C., McNabb W. C., Roy N. C. 2009; Multidrug resistance gene deficient ( mdr1a–/–) mice have an altered caecal microbiota that precedes the onset of intestinal inflammation. J Appl Microbiol 107:557–566
    [Google Scholar]
  34. Park E. I., Paisley E. A., Mangian H. J., Swartz D. A., Wu M., O'Morchoe P. J., Behr S. R., Visek W. J., Kaput J. 1997; Lipid level and type alter stearoyl CoA desaturase mRNA abundance differently in mice with distinct susceptibilities to diet-influenced diseases. J Nutr 127:566–573
    [Google Scholar]
  35. Phan C. T., Tso P. 2001; Intestinal lipid absorption and transport. Front Biosci 6:D299–D319
    [Google Scholar]
  36. Rath H. C., Wilson K. H., Sartor R. B. 1999; Differential induction of colitis and gastritis in HLA-B27 transgenic rats selectively colonized with Bacteroides vulgatus or Escherichia coli. Infect Immun 67:2969–2974
    [Google Scholar]
  37. Riley L. K., Franklin C. L., Hook R. R., Besch Williford C. 1996; Identification of murine Helicobacters by PCR and restriction enzyme analyses. J Clin Microbiol 34:942–946
    [Google Scholar]
  38. Rinttilä T., Kassinen A., Malinen E., Krogius L., Palva A. 2004; Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97:1166–1177
    [Google Scholar]
  39. Roy N., Barnett M., Knoch B., Dommels Y., McNabb W. 2007; Nutrigenomics applied to an animal model of inflammatory bowel diseases: transcriptomic analysis of the effects of eicosapentaenoic acid- and arachidonic acid-enriched diets. Mutat Res 622:103–116
    [Google Scholar]
  40. Sellon R. K., Tonkonogy S., Schultz M., Dieleman L. A., Grenther W., Balish E., Rennick D. M., Sartor R. B. 1998; Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66:5224–5231
    [Google Scholar]
  41. Strober W., Fuss I., Mannon P. 2007; The fundamental basis of inflammatory bowel disease. J Clin Invest 117:514–521
    [Google Scholar]
  42. Swidsinski A., Weber J., Loening-Baucke V., Hale L. P., Lochs H. 2005; Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 43:3380–3389
    [Google Scholar]
  43. Tannock G. W., Munro K., Harmsen H. J. M., Welling G. W., Smart J., Gopal P. K. 2000; Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl Environ Microbiol 66:2578–2588
    [Google Scholar]
  44. Vaahtovuo J., Toivanen P., Eerola E. 2001; Study of murine faecal microflora by cellular fatty acid analysis; effect of age and mouse strain. Antonie Van Leeuwenhoek 80:35–42
    [Google Scholar]
  45. Vaahtovuo J., Toivanen P., Eerola E. 2003; Bacterial composition of murine fecal microflora is indigenous and genetically guided. FEMS Microbiol Ecol 44:131–136
    [Google Scholar]
  46. Varon C., Duriez A., Lehours P., Menard A., Laye S., Zerbib F., Megraud F., Laharie D. 2009; Study of Helicobacter pullorum proinflammatory properties on human epithelial cells in vitro. Gut 58:629–635
    [Google Scholar]
  47. Waidmann M., Bechtold O., Frick J. S., Lehr H. A., Schubert S., Dobrindt U., Loffler J., Bohn E., Autenrieth I. B. 2003; Bacteroides vulgatus protects against Escherichia coli-induced colitis in gnotobiotic interleukin-2-deficient mice. Gastroenterology 125:162–177
    [Google Scholar]
  48. Wang R. F., Cao W. W., Cerniglia C. E. 1996; PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Appl Environ Microbiol 62:1242–1247
    [Google Scholar]
  49. Wohlgemuth S., Haller D., Blaut M., Loh G. 2009; Reduced microbial diversity and high numbers of one single Escherichia coli strain in the intestine of colitic mice. Environ Microbiol 11:1562–1571
    [Google Scholar]
  50. Zoetendal E. G., Akkermans A. D. L., Akkermans-van Vliet W. M., deVisser J. A. G. M., deVos W. M. 2001; The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis 13:129–134
    [Google Scholar]
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