Home LiteratureArticle Details
PMID: 22219336 Published · ppublish English Journal Article Review

Determinants of colonic barrier function in inflammatory bowel disease and potential therapeutics.

The Journal of physiology ·Vol. 590 ·No. 5 ·2012-03-01 ·Pages 1035-44

Hering NA, Fromm M, Schulzke JD

Abstract

Intestinal barrier dysfunction is a main feature of the inflammatory bowel diseases (IBD), Crohn's disease and ulcerative colitis. Leak flux diarrhoea and a facilitated uptake of noxious antigens are the two consequences resulting from an impaired epithelial barrier. Barrier perturbations in IBD comprise alterations in epithelial tight junctions (TJ), i.e. a reduced number of horizontal TJ strands and an altered TJ protein expression and subcellular distribution. Moreover, increased incidence of apoptotic events as well as erosions and ulcerations can add to that leakiness. These barrier defects are attributed to enhanced activity of pro-inflammatory cytokines like TNFα, INFγ, IL-1β and IL-13, which are highly expressed in the chronically inflamed intestine. Although the aetiology of IBD is far from being clear, chronic inflammation is believed to result from an inadequate immune response as a consequence of genetic predisposition as well as changes in, and altered responses to, the intestinal microbiota. On the other hand, an insufficient mucosal response to bacterial stimuli results in an insufficient immune response towards intestinal pathogens. However, detailed characterization of barrier defects offers the opportunity to consider and test therapeutic interventions. Beside cytokine antagonists, different plant compounds and probiotics have been shown to stabilize the barrier function by affecting TJ protein expression and distribution.

MeSH Terms
Animals Colon/physiopathology Cytokines/immunology Humans Inflammatory Bowel Diseases/drug therapy,immunology,physiopathology Tight Junctions/physiology
Chemicals
Cytokines
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Hering Nina A
Department of Gastroenterology, Division of Nutritional Medicine, Charité, Campus Benjamin Franklin, Berlin, Germany.
Fromm Michael
Schulzke Jörg-Dieter
References (81)
81 references, click to expand
  1. NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression.
    Gut. 2004 Nov;53(11):1658-64 PMID: 15479689
  2. Zinc supplementation tightens "leaky gut" in Crohn's disease.
    Inflamm Bowel Dis. 2001 May;7(2):94-8 PMID: 11383597
  3. Mechanisms of diarrhea in collagenous colitis.
    Gastroenterology. 2002 Aug;123(2):433-43 PMID: 12145796
  4. Crohn's disease and the NOD2 gene: a role for paneth cells.
    Gastroenterology. 2003 Jul;125(1):47-57 PMID: 12851870
  5. Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease.
    Lab Invest. 2006 Feb;86(2):191-201 PMID: 16402035
  6. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis.
    Am J Physiol Gastrointest Liver Physiol. 2009 May;296(5):G1140-9 PMID: 19221015
  7. Stimulation of sodium chloride absorption from secreting rat colon by short-chain fatty acids.
    Dig Dis Sci. 1999 Sep;44(9):1924-30 PMID: 10505736
  8. Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity.
    PLoS One. 2007 Dec 12;2(12):e1308 PMID: 18074031
  9. TNF-alpha and IFN-gamma regulate the expression of the NOD2 (CARD15) gene in human intestinal epithelial cells.
    Gastroenterology. 2003 Apr;124(4):1001-9 PMID: 12671897
  10. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice.
    Infect Immun. 1998 Nov;66(11):5224-31 PMID: 9784526
  11. Claudin-2, a component of the tight junction, forms a paracellular water channel.
    J Cell Sci. 2010 Jun 1;123(Pt 11):1913-21 PMID: 20460438
  12. Differential expression of claudin-2 along the human intestine: Implication of GATA-4 in the maintenance of claudin-2 in differentiating cells.
    J Cell Physiol. 2005 Apr;203(1):15-26 PMID: 15389642
  13. Regulation of mucosal structure and barrier function in rat colon exposed to tumor necrosis factor alpha and interferon gamma in vitro: a novel model for studying the pathomechanisms of inflammatory bowel disease cytokines.
    Scand J Gastroenterol. 2009;44(10):1226-35 PMID: 19658020
  14. Multifunctional strands in tight junctions.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):285-93 PMID: 11283726
  15. Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process.
    FASEB J. 2005 Jun;19(8):923-33 PMID: 15923402
  16. Microscopic colitis demonstrates a T helper cell type 1 mucosal cytokine profile.
    J Clin Pathol. 2007 Apr;60(4):382-7 PMID: 16775121
  17. Microbial diversity of inflamed and noninflamed gut biopsy tissues in inflammatory bowel disease.
    Inflamm Bowel Dis. 2007 Jun;13(6):675-83 PMID: 17262808
  18. Loss of claudin-15, but not claudin-2, causes Na+ deficiency and glucose malabsorption in mouse small intestine.
    Gastroenterology. 2011 Mar;140(3):913-23 PMID: 20727355
  19. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis.
    Gastroenterology. 1999 Feb;116(2):301-9 PMID: 9922310
  20. Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative colitis.
    Gut. 1994 Jan;35(1):73-6 PMID: 8307454
  21. Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88.
    Br J Nutr. 2006 Jun;95(6):1177-84 PMID: 16768842
  22. Further observations on the fine structure of freeze-cleaved tight junctions.
    J Cell Sci. 1973 Nov;13(3):763-86 PMID: 4203962
  23. Claudin-10 exists in six alternatively spliced isoforms that exhibit distinct localization and function.
    J Cell Sci. 2009 May 15;122(Pt 10):1507-17 PMID: 19383724
  24. TNFalpha up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling.
    Cell Tissue Res. 2009 Apr;336(1):67-77 PMID: 19214581
  25. Epithelial barriers in intestinal inflammation.
    Antioxid Redox Signal. 2011 Sep 1;15(5):1255-70 PMID: 21294654
  26. Cloning of the human claudin-2 5'-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1alpha.
    J Biol Chem. 2002 Jun 14;277(24):21361-70 PMID: 11934881
  27. Arcobacter butzleri induces barrier dysfunction in intestinal HT-29/B6 cells.
    J Infect Dis. 2009 Sep 1;200(5):756-64 PMID: 19604116
  28. Hepatocyte nuclear factor 4alpha orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver.
    Proc Natl Acad Sci U S A. 2006 May 30;103(22):8419-24 PMID: 16714383
  29. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial.
    Lancet. 1999 Aug 21;354(9179):635-9 PMID: 10466665
  30. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability.
    J Clin Invest. 2001 May;107(10):1319-27 PMID: 11375422
  31. NOD2/CARD15 mediates induction of the antimicrobial peptide human beta-defensin-2.
    J Biol Chem. 2006 Jan 27;281(4):2005-11 PMID: 16319062
  32. MLCK-dependent exchange and actin binding region-dependent anchoring of ZO-1 regulate tight junction barrier function.
    Proc Natl Acad Sci U S A. 2010 May 4;107(18):8237-41 PMID: 20404178
  33. Reduced ratio of protective versus proinflammatory cytokine responses to commensal bacteria in HLA-B27 transgenic rats.
    Clin Exp Immunol. 2004 Apr;136(1):30-9 PMID: 15030511
  34. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease.
    Gut. 2000 Sep;47(3):397-403 PMID: 10940278
  35. Glutamine deprivation facilitates tumour necrosis factor induced bacterial translocation in Caco-2 cells by depletion of enterocyte fuel substrate.
    Gut. 2003 Feb;52(2):224-30 PMID: 12524404
  36. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease.
    World J Gastroenterol. 2007 May 28;13(20):2826-32 PMID: 17569118
  37. Permeability of human HT-29/B6 colonic epithelium as a function of apoptosis.
    J Physiol. 2001 Sep 1;535(Pt 2):541-52 PMID: 11533143
  38. Yersinia enterocolitica induces epithelial barrier dysfunction through regional tight junction changes in colonic HT-29/B6 cell monolayers.
    Lab Invest. 2011 Feb;91(2):310-24 PMID: 20956974
  39. Antioxidant effect of zinc in humans.
    Free Radic Biol Med. 2004 Oct 15;37(8):1182-90 PMID: 15451058
  40. TGF-beta1 and Smad7 in the regulation of IBD.
    Mucosal Immunol. 2008 Nov;1 Suppl 1:S50-3 PMID: 19079231
  41. Leaks in the epithelial barrier caused by spontaneous and TNF-alpha-induced single-cell apoptosis.
    FASEB J. 2000 Sep;14(12):1749-53 PMID: 10973924
  42. The effect of berberine chloride on experimental colitis in rats in vivo and in vitro.
    J Pharmacol Exp Ther. 2000 Sep;294(3):822-9 PMID: 10945829
  43. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice.
    J Cell Biol. 2002 Mar 18;156(6):1099-111 PMID: 11889141
  44. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo.
    J Cell Biol. 2010 Apr 5;189(1):111-26 PMID: 20351069
  45. Oral and fecal Campylobacter concisus strains perturb barrier function by apoptosis induction in HT-29/B6 intestinal epithelial cells.
    PLoS One. 2011;6(8):e23858 PMID: 21887334
  46. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution.
    Gastroenterology. 2005 Aug;129(2):550-64 PMID: 16083712
  47. Claudin-3 acts as a sealing component of the tight junction for ions of either charge and uncharged solutes.
    Biochim Biophys Acta. 2010 Nov;1798(11):2048-57 PMID: 20655293
  48. Claudins and epithelial paracellular transport.
    Annu Rev Physiol. 2006;68:403-29 PMID: 16460278
  49. Contribution of claudin-5 to barrier properties in tight junctions of epithelial cells.
    Cell Tissue Res. 2005 Jul;321(1):89-96 PMID: 16158492
  50. Loss of hepatocyte-nuclear-factor-4alpha affects colonic ion transport and causes chronic inflammation resembling inflammatory bowel disease in mice.
    PLoS One. 2009 Oct 29;4(10):e7609 PMID: 19898610
  51. Escherichia coli alpha-haemolysin induces focal leaks in colonic epithelium: a novel mechanism of bacterial translocation.
    Cell Microbiol. 2007 Oct;9(10):2530-40 PMID: 17587334
  52. Increased intestinal permeability and NOD2 variants in familial and sporadic Crohn's disease.
    Aliment Pharmacol Ther. 2006 May 15;23(10):1455-61 PMID: 16669960
  53. Genetic basis for increased intestinal permeability in families with Crohn's disease: role of CARD15 3020insC mutation?
    Gut. 2006 Mar;55(3):342-7 PMID: 16000642
  54. Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6.
    J Cell Sci. 1999 Jan;112 ( Pt 1):137-46 PMID: 9841910
  55. Downregulation of epithelial apoptosis and barrier repair in active Crohn's disease by tumour necrosis factor alpha antibody treatment.
    Gut. 2004 Sep;53(9):1295-302 PMID: 15306588
  56. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration.
    J Cell Biol. 1998 Jul 13;142(1):117-27 PMID: 9660867
  57. Hepatocyte nuclear factor 4alpha enhances the hepatocyte nuclear factor 1alpha-mediated activation of transcription.
    Nucleic Acids Res. 2004 May 11;32(8):2586-93 PMID: 15141028
  58. 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 (Praha). 2001;46(6):565-72 PMID: 11898350
  59. Open-label study of adalimumab in patients with ulcerative colitis including those with prior loss of response or intolerance to infliximab.
    Inflamm Bowel Dis. 2009 Sep;15(9):1302-7 PMID: 19408340
  60. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure.
    J Cell Sci. 2006 May 15;119(Pt 10):2095-106 PMID: 16638813
  61. Epithelial myosin light chain kinase activation induces mucosal interleukin-13 expression to alter tight junction ion selectivity.
    J Biol Chem. 2010 Apr 16;285(16):12037-46 PMID: 20177070
  62. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells.
    J Cell Biol. 2005 Dec 19;171(6):939-45 PMID: 16365161
  63. Na+ absorption defends from paracellular back-leakage by claudin-8 upregulation.
    Biochem Biophys Res Commun. 2009 Jan 2;378(1):45-50 PMID: 19000657
  64. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells.
    J Nutr. 2008 Jun;138(6):1067-73 PMID: 18492835
  65. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota.
    Immunol Rev. 2005 Aug;206:260-76 PMID: 16048554
  66. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease.
    Gut. 2007 Jan;56(1):61-72 PMID: 16822808
  67. Hepatocyte nuclear factor 4alpha in the intestinal epithelial cells protects against inflammatory bowel disease.
    Inflamm Bowel Dis. 2008 Jul;14(7):908-20 PMID: 18338782
  68. Genome-wide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region.
    Nat Genet. 2009 Dec;41(12):1330-4 PMID: 19915572
  69. Interferon gamma induces translocation of commensal Escherichia coli across gut epithelial cells via a lipid raft-mediated process.
    Gastroenterology. 2005 May;128(5):1258-67 PMID: 15887109
  70. Cell polarity-determining proteins Par-3 and PP-1 are involved in epithelial tight junction defects in coeliac disease.
    Gut. 2012 Feb;61(2):220-8 PMID: 21865402
  71. Cellular and molecular mechanism of interleukin-1β modulation of Caco-2 intestinal epithelial tight junction barrier.
    J Cell Mol Med. 2011 Apr;15(4):970-82 PMID: 20406328
  72. The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding.
    Gastroenterology. 2011 Apr;140(4):1208-1218.e1-2 PMID: 21237166
  73. Associations with tight junction genes PARD3 and MAGI2 in Dutch patients point to a common barrier defect for coeliac disease and ulcerative colitis.
    Gut. 2008 Apr;57(4):463-7 PMID: 17989107
  74. Occludin: a novel integral membrane protein localizing at tight junctions.
    J Cell Biol. 1993 Dec;123(6 Pt 2):1777-88 PMID: 8276896
  75. Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells.
    J Cell Sci. 2002 Dec 15;115(Pt 24):4969-76 PMID: 12432083
  76. Enhanced translocation of bacteria across metabolically stressed epithelia is reduced by butyrate.
    Inflamm Bowel Dis. 2010 Jul;16(7):1138-48 PMID: 20024905
  77. Transforming growth factor-β, a whey protein component, strengthens the intestinal barrier by upregulating claudin-4 in HT-29/B6 cells.
    J Nutr. 2011 May;141(5):783-9 PMID: 21430244
  78. Cellular and molecular mechanisms that mediate basal and tumour necrosis factor-alpha-induced regulation of myosin light chain kinase gene activity.
    J Cell Mol Med. 2008 Aug;12(4):1331-46 PMID: 18363837
  79. Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets.
    Br J Nutr. 2009 Sep;102(5):687-93 PMID: 19267955
  80. Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability.
    Mol Biol Cell. 2009 Aug;20(16):3713-24 PMID: 19535456
  81. TNFalpha-induced and berberine-antagonized tight junction barrier impairment via tyrosine kinase, Akt and NFkappaB signaling.
    J Cell Sci. 2010 Dec 1;123(Pt 23):4145-55 PMID: 21062898
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
1469-7793
Published
2012-03-01
Epub
2012-00-04
Pages
1035-44
Language
English
Region
England
NLM ID
0266262
PMCID
PMC3381811
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com