Protective effect of Clostridium tyrobutyricum in acute dextran sodium sulphate-induced colitis: differential regulation of tumour necrosis factor-α and interleukin-18 in BALB/c and severe combined immunodeficiency mice
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
22236013
PubMed Central
PMC3278703
DOI
10.1111/j.1365-2249.2011.04498.x
Knihovny.cz E-zdroje
- MeSH
- akutní nemoc MeSH
- antigeny CD11b biosyntéza genetika MeSH
- aplikace rektální MeSH
- bakteriální translokace MeSH
- butyráty metabolismus MeSH
- Clostridium tyrobutyricum fyziologie MeSH
- fosfoproteiny biosyntéza genetika MeSH
- imunokompetence MeSH
- interleukin-18 biosyntéza genetika MeSH
- kolon metabolismus mikrobiologie patologie MeSH
- mastné kyseliny metabolismus MeSH
- membránové proteiny biosyntéza genetika MeSH
- mucin 2 biosyntéza genetika MeSH
- muciny biosyntéza MeSH
- myši inbrední BALB C MeSH
- myši SCID MeSH
- myši MeSH
- organismy bez specifických patogenů MeSH
- probiotika terapeutické užití MeSH
- protein zonula occludens 1 MeSH
- síran dextranu toxicita MeSH
- těžká kombinovaná imunodeficience genetika imunologie MeSH
- TNF-alfa biosyntéza genetika MeSH
- ulcerózní kolitida chemicky indukované genetika imunologie mikrobiologie patologie MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- antigeny CD11b MeSH
- butyráty MeSH
- fosfoproteiny MeSH
- interleukin-18 MeSH
- mastné kyseliny MeSH
- membránové proteiny MeSH
- Muc2 protein, mouse MeSH Prohlížeč
- mucin 2 MeSH
- muciny MeSH
- protein zonula occludens 1 MeSH
- síran dextranu MeSH
- Tjp1 protein, mouse MeSH Prohlížeč
- TNF-alfa MeSH
One of the promising approaches in the therapy of ulcerative colitis is administration of butyrate, an energy source for colonocytes, into the lumen of the colon. This study investigates the effect of butyrate producing bacterium Clostridium tyrobutyricum on dextran sodium sulphate (DSS)-induced colitis in mice. Immunocompetent BALB/c and immunodeficient severe combined immunodeficiency (SCID) mice reared in specific-pathogen-free (SPF) conditions were treated intrarectally with C. tyrobutyricum 1 week prior to the induction of DSS colitis and during oral DSS treatment. Administration of DSS without C. tyrobutyricum treatment led to an appearance of clinical symptoms - bleeding, rectal prolapses and colitis-induced increase in the antigen CD11b, a marker of infiltrating inflammatory cells in the lamina propria. The severity of colitis was similar in BALB/c and SCID mice as judged by the histological damage score and colon shortening after 7 days of DSS treatment. Both strains of mice also showed a similar reduction in tight junction (TJ) protein zonula occludens (ZO)-1 expression and of MUC-2 mucin depression. Highly elevated levels of cytokine tumour necrosis factor (TNF)-α in the colon of SCID mice and of interleukin (IL)-18 in BALB/c mice were observed. Intrarectal administration of C. tyrobutyricum prevented appearance of clinical symptoms of DSS-colitis, restored normal MUC-2 production, unaltered expression of TJ protein ZO-1 and decreased levels of TNF-α and IL-18 in the descending colon of SCID and BALB/c mice, respectively. Some of these features can be ascribed to the increased production of butyrate in the lumen of the colon and its role in protection of barrier functions and regulation of IL-18 expression.
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Tlaskalova-Hogenova H, Tuckova L, Stepankova R, et al. Involvement of innate immunity in the development of inflammatory and autoimmune diseases. Ann NY Acad Sci. 2005;1051:787–98. PubMed
Frolova L, Drastich P, Rossmann P, Klimesova K, Tlaskalova-Hogenova H. Expression of Toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J Histochem Cytochem. 2008;56:267–74. PubMed PMC
Cooper HS, Murthy SN, Shah RS, Sedergran DJ. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993;69:238–49. PubMed
Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, Elson CO. Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology. 1994;107:1643–52. PubMed
Stepankova R, Powrie F, Kofronova O, et al. Segmented filamentous bacteria in a defined bacterial cocktail induces intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm Bowel Dis. 2007;13:1202–11. PubMed
Hudcovic T, Stepankova R, Cebra J, Tlaskalova-Hogenova 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. 2001;46:565–72. PubMed
Johansson ME, Gustafsson JK, Sjoberg KE, et al. Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS ONE. 2010;5:e12238. PubMed PMC
Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990;98:694–702. PubMed
Tytgat KM, Bovelander FJ, Opdam FJ, Einerhand AW, Buller HA, Dekker J. Biosynthesis of rat MUC2 in colon and its analogy with human MUC2. Biochem J. 1995;309:221–9. PubMed PMC
Renes IB, Boshuizen JA, Van Nispen DJ, et al. Alterations in Muc2 biosynthesis and secretion during dextran sulfate sodium-induced colitis. Am J Physiol. 2002;282:G382–9. PubMed
Araki Y, Fujiyama Y, Andoh A, Koyama S, Kanauchi O, Bamba T. The dietary combination of germinated barley foodstuff plus Clostridium butyricum suppresses the dextran sulfate sodium-induced experimental colitis in rats. Scand J Gastroenterol. 2000;35:1060–7. PubMed
Gaudier E, Rival M, Buisine MP, Robineau I, Hoebler C. Butyrate enemas upregulate Muc genes expression but decrease adherent mucus thickness in mice colon. Physiol Res. 2009;58:111–19. PubMed
Venkatraman A, Ramakrishna BS, Pulimood AB, Patra S, Murthy S. Increased permeability in dextran sulphate colitis in rats: time course of development and effect of butyrate. Scand J Gastroenterol. 2000;35:1053–9. PubMed
Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC. Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr. 2011;141:769–76. PubMed
Karczewski J, Troost FJ, Konings I, et al. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol. 2010;298:G851–9. PubMed
Zyrek AA, Cichon C, Helms S, Enders C, Sonnenborn U, Schmidt MA. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol. 2007;9:804–16. PubMed
Desreumaux P, Colombel JF. Intestinal microflora and chronic inflammatory bowel diseases. Gastroenterol Clin Biol. 2001;25:C89–93. PubMed
Nanda Kumar NS, Balamurugan R, Jayakanthan K, Pulimood A, Pugazhendhi S, Ramakrishna BS. Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J Gastroenterol Hepatol. 2008;23:1834–9. PubMed
Peran L, Camuesco D, Comalada M, et al. A comparative study of the preventative effects exerted by three probiotics, Bifidobacterium lactis, Lactobacillus casei and Lactobacillus acidophilus, in the TNBS model of rat colitis. J Appl Microbiol. 2007;103:836–44. PubMed
Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27:104–19. PubMed
Okamoto T, Sasaki M, Tsujikawa T, Fujiyama Y, Bamba T, Kusunoki M. Preventive efficacy of butyrate enemas and oral administration of Clostridium butyricum M588 in dextran sodium sulfate-induced colitis in rats. J Gastroenterol. 2000;35:341–6. PubMed
Schallehn G, Wolff MH. Morphological changes in human embryonic lung fibroblasts caused by cytotoxins of various Clostridium species. Zentralbl Bakteriol Mikrobiol Hyg. 1988;267:367–78. PubMed
Khoruts A, Sadowsky MJ. Therapeutic transplantation of the distal gut microbiota. Mucosal Immunol. 2011;4:4–7. PubMed
Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001;81:1031–64. PubMed
Melgar S, Karlsson A, Michaelsson E. Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am J Physiol. 2005;288:G1328–38. PubMed
Bauer C, Loher F, Dauer M, et al. The ICE inhibitor pralnacasan prevents DSS-induced colitis in C57BL/6 mice and suppresses IP-10 mRNA but not TNF-alpha mRNA expression. Dig Dis Sci. 2007;52:1642–52. PubMed
Elinav E, Strowig T, Kau AL, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 2011;145:745–57. PubMed PMC
Jacobs LR, Huber PW. Regional distribution and alterations of lectin binding to colorectal mucin in mucosal biopsies from controls and subjects with inflammatory bowel diseases. J Clin Invest. 1985;75:112–18. PubMed PMC
Van der Sluis M, De Koning BA, De Bruijn AC, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131:117–29. PubMed
Amit-Romach E, Reifen R, Uni Z. Mucosal function in rat jejunum and ileum is altered by induction of colitis. Int J Molecular Med. 2006;18:721–7. PubMed
Einerhand AW, Renes IB, Makkink MK, van der Sluis M, Buller HA, Dekker J. Role of mucins in inflammatory bowel disease: important lessons from experimental models. Eur J Gastroenterol Hepatol. 2002;14:757–65. PubMed
Poritz LS, Garver KI, Green C, Fitzpatrick L, Ruggiero F, Koltun WA. Loss of the tight junction protein ZO-1 in dextran sulfate sodium induced colitis. J Surg Res. 2007;140:12–19. PubMed
Shintani N, Nakajima T, Okamoto T, Kondo T, Nakamura N, Mayumi T. Involvement of CD4+ T cells in the development of dextran sulfate sodium-induced experimental colitis and suppressive effect of IgG on their action. Gen Pharmacol. 1998;31:477–81. PubMed
Friswell M, Campbell B, Rhodes J. The role of bacteria in the pathogenesis of inflammatory bowel disease. Gut Liver. 2010;4:295–306. PubMed PMC
Siegmund B, Fantuzzi G, Rieder F, et al. Neutralization of interleukin-18 reduces severity in murine colitis and intestinal IFN-gamma and TNF-alpha production. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1264–73. PubMed
Kolinska J, Lisa V, Clark JA, et al. Constitutive expression of IL-18 and IL-18R in differentiated IEC-6 cells: effect of TNF-alpha and IFN-gamma treatment. J Interferon Cytokine Res. 2008;28:287–96. PubMed
Bauer C, Duewell P, Mayer C, et al. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 2010;59:1192–9. PubMed
Siegmund B. Interleukin-18 in intestinal inflammation: friend and foe? Immunity. 2010;32:300–2. PubMed
Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, Kanneganti TD. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity. 2010;32:379–91. PubMed PMC
Dupaul-Chicoine J, Yeretssian G, Doiron K, et al. Control of intestinal homeostasis, colitis, and colitis-associated colorectal cancer by the inflammatory caspases. Immunity. 2010;32:367–78. PubMed
Mahida YR. The key role of macrophages in the immunopathogenesis of inflammatory bowel disease. Inflamm Bowel Dis. 2000;6:21–33. PubMed
Reinecker HC, Steffen M, Witthoeft T, et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol. 1993;94:174–81. PubMed PMC
Thibault R, Blachier F, Darcy-Vrillon B, de Coppet P, Bourreille A, Segain JP. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflam Bowel Dis. 2010;16:684–95. PubMed
Noor SO, Ridgway K, Scovell L, et al. Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota. BMC Gastroenterol. 2010;10:134. PubMed PMC
Willing BP, Finlay BB. Gut microbiology: fitting into the intestinal neighbourhood. Curr Biol. 2009;19:R457–9. PubMed
Wachtershauser A, Stein J. Rationale for the luminal provision of butyrate in intestinal diseases. Eur J Nutr. 2000;39:164–71. PubMed
Hamer HM, Jonkers DM, Vanhoutvin SA, et al. Effect of butyrate enemas on inflammation and antioxidant status in the colonic mucosa of patients with ulcerative colitis in remission. Clin Nutr. 2010;29:738–44. PubMed
Cario E, Gerken G, Podolsky DK. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology. 2004;127:224–38. PubMed
Nafday SM, Chen W, Peng L, Babyatsky MW, Holzman IR, Lin J. Short-chain fatty acids induce colonic mucosal injury in rats with various postnatal ages. Pediatr Res. 2005;57:201–4. PubMed
Nancey S, Moussata D, Graber I, Claudel S, Saurin JC, Flourie B. Tumor necrosis factor alpha reduces butyrate oxidation in vitro in human colonic mucosa: a link from inflammatory process to mucosal damage? Inflam Bowel Dis. 2005;11:559–66. PubMed
Kalina U, Koyama N, Hosoda T, et al. Enhanced production of IL-18 in butyrate-treated intestinal epithelium by stimulation of the proximal promoter region. Eur J Immunol. 2002;32:2635–43. PubMed
Kolinska J, Zakostelecka M, Schwarzer M, Stepankova R, Hudcovic T, Kozakova H. Effect of nonpathogenic Escherichia coli monoassociation on small intestinal brush-border glycoconjugate moieties and cytokine production after colonization in ex-germ-free rats and piglets. Int J Interferon Cytokine Mediat Res. 2010;2:73–84.
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