Home LiteratureArticle Details
PMID: 21407243 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Mucin dynamics and enteric pathogens.

Nature reviews. Microbiology ·Vol. 9 ·No. 4 ·2011-04-00 ·Pages 265-78

McGuckin MA, Lindén SK, Sutton P, Florin TH

Abstract

The extracellular secreted mucus and the cell surface glycocalyx prevent infection by the vast numbers of microorganisms that live in the healthy gut. Mucin glycoproteins are the major component of these barriers. In this Review, we describe the components of the secreted and cell surface mucosal barriers and the evidence that they form an effective barricade against potential pathogens. However, successful enteric pathogens have evolved strategies to circumvent these barriers. We discuss the interactions between enteric pathogens and mucins, and the mechanisms that these pathogens use to disrupt and avoid mucosal barriers. In addition, we describe dynamic alterations in the mucin barrier that are driven by host innate and adaptive immune responses to infection.

MeSH Terms
Adaptive Immunity Animals Bacterial Infections/immunology,microbiology Gastric Mucosa/immunology,microbiology Gastrointestinal Diseases/immunology,microbiology Gastrointestinal Tract/immunology,metabolism,microbiology Glycocalyx/chemistry Goblet Cells/metabolism Humans Immunity, Innate Intestinal Mucosa/immunology,microbiology Mucins/chemistry,genetics,immunology,metabolism Mucus/chemistry Paneth Cells/metabolism
Chemicals
Mucins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
McGuckin Michael A
Immunity, Infection and Inflammation Program, Mater Medical Research Institute and The University of Queensland School of Medicine, South Brisbane, Queensland 4101, Australia. mmcguckin@mmri.mater.org.au
Lindén Sara K
Sutton Philip
Florin Timothy H
References (182)
182 references, click to expand
  1. Muc1 cell surface mucin attenuates epithelial inflammation in response to a common mucosal pathogen.
    J Biol Chem. 2010 Jul 2;285(27):20547-57 PMID: 20430889
  2. Effect of trefoil factors on the viscoelastic properties of mucus gels.
    Eur J Clin Invest. 2002 Jul;32(7):519-27 PMID: 12153553
  3. Paneth cell development, differentiation, and function: new molecular cues.
    Gastroenterology. 2009 Jul;137(1):30-3 PMID: 19497398
  4. Structure and function of the polymeric mucins in airways mucus.
    Annu Rev Physiol. 2008;70:459-86 PMID: 17850213
  5. Mucin secretion by the human colon cell line LS174T is regulated by bile salts.
    Glycobiology. 1999 Jan;9(1):13-9 PMID: 9884402
  6. Altered expression and allelic association of the hypervariable membrane mucin MUC1 in Helicobacter pylori gastritis.
    Gastroenterology. 2002 Jul;123(1):41-9 PMID: 12105832
  7. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa.
    PLoS Pathog. 2010 May 13;6(5):e1000902 PMID: 20485566
  8. MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy.
    PLoS Pathog. 2009 Oct;5(10):e1000617 PMID: 19816567
  9. Homeostasis and function of goblet cells during rotavirus infection in mice.
    Virology. 2005 Jul 5;337(2):210-21 PMID: 15882887
  10. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells.
    Nature. 2008 Nov 13;456(7219):259-63 PMID: 18849966
  11. Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli.
    Infect Immun. 1999 Nov;67(11):5587-96 PMID: 10531204
  12. Gut feelings: enteropathogenic E. coli (EPEC) interactions with the host.
    Annu Rev Cell Dev Biol. 2000;16:173-89 PMID: 11031234
  13. A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn.
    Glycobiology. 2009 Jul;19(7):756-66 PMID: 19321523
  14. IFN-gamma-induced expression of MUC4 in pancreatic cancer cells is mediated by STAT-1 upregulation: a novel mechanism for IFN-gamma response.
    Oncogene. 2007 Nov 8;26(51):7251-61 PMID: 17525742
  15. Control of mucus hydration as a Donnan equilibrium process.
    Nature. 1981 Jul 23;292(5821):340-2 PMID: 7195985
  16. Increased faecal mucin sulphatase activity in ulcerative colitis: a potential target for treatment.
    Gut. 1995 Apr;36(4):570-6 PMID: 7737566
  17. Modification of gastric mucin oligosaccharide expression in rhesus macaques after infection with Helicobacter pylori.
    Gastroenterology. 2009 Sep;137(3):1061-71, 1071.e1-8 PMID: 19375420
  18. Mucin exocytosis.
    Am Rev Respir Dis. 1991 Sep;144(3 Pt 2):S33-7 PMID: 1892323
  19. Mucin-related epitopes distinguish M cells and enterocytes in rabbit appendix and Peyer's patches.
    Infect Immun. 1999 Jan;67(1):357-67 PMID: 9864237
  20. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria.
    Science. 2004 Mar 12;303(5664):1662-5 PMID: 15016999
  21. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin.
    Nature. 2003 Apr 3;422(6931):522-6 PMID: 12660734
  22. MUC1 oncoprotein activates the IkappaB kinase beta complex and constitutive NF-kappaB signalling.
    Nat Cell Biol. 2007 Dec;9(12):1419-27 PMID: 18037881
  23. Generation of ligand-receptor alliances by "SEA" module-mediated cleavage of membrane-associated mucin proteins.
    Protein Sci. 2002 Mar;11(3):698-706 PMID: 11847293
  24. Human salivary mucin MG1 selectively forms heterotypic complexes with amylase, proline-rich proteins, statherin, and histatins.
    J Dent Res. 1997 Mar;76(3):734-43 PMID: 9109822
  25. Mucin glycosylation is altered by pro-inflammatory signaling in pancreatic-cancer cells.
    J Proteome Res. 2009 Apr;8(4):1876-86 PMID: 19714813
  26. Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein.
    J Proteome Res. 2009 Jul;8(7):3549-57 PMID: 19432394
  27. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing.
    Infect Immun. 2009 Oct;77(10):4668-78 PMID: 19635824
  28. Haemagglutinin/protease expression and mucin gel penetration in El Tor biotype Vibrio cholerae.
    Microbiology (Reading). 2003 Jul;149(Pt 7):1883-1891 PMID: 12855739
  29. Helicobacter pylori uses motility for initial colonization and to attain robust infection.
    Infect Immun. 2002 Apr;70(4):1984-90 PMID: 11895962
  30. Culture-independent analysis of indomethacin-induced alterations in the rat gastrointestinal microbiota.
    Appl Environ Microbiol. 2006 Oct;72(10):6707-15 PMID: 17021222
  31. Carbohydrate expression in the intestinal mucosa.
    Adv Anat Embryol Cell Biol. 2001;160:III-IX, 1-91 PMID: 11443891
  32. The trefoil protein TFF1 is bound to MUC5AC in human gastric mucosa.
    Cell Mol Life Sci. 2004 Aug;61(15):1946-54 PMID: 15289936
  33. Glycocalyx on rabbit intestinal M cells displays carbohydrate epitopes from Muc2.
    Infect Immun. 2001 Feb;69(2):1061-71 PMID: 11160003
  34. Tumor necrosis factor-alpha converting enzyme/ADAM 17 mediates MUC1 shedding.
    J Biol Chem. 2003 Jan 31;278(5):3386-94 PMID: 12441351
  35. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin.
    Science. 2004 Jul 23;305(5683):519-22 PMID: 15273394
  36. The role of secretory antibodies in infection immunity.
    Nat Rev Microbiol. 2010 Sep;8(9):656-67 PMID: 20694027
  37. Setting research priorities to reduce global mortality from childhood diarrhoea by 2015.
    PLoS Med. 2009 Mar 10;6(3):e41 PMID: 19278292
  38. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis.
    J Clin Invest. 2008 Feb;118(2):534-44 PMID: 18172556
  39. TagA is a secreted protease of Vibrio cholerae that specifically cleaves mucin glycoproteins.
    Microbiology (Reading). 2011 Feb;157(Pt 2):516-525 PMID: 20966091
  40. Mucins in the host defence against Naegleria fowleri and mucinolytic activity as a possible means of evasion.
    Microbiology (Reading). 2008 Dec;154(Pt 12):3895-3904 PMID: 19047756
  41. Human susceptibility and resistance to Norwalk virus infection.
    Nat Med. 2003 May;9(5):548-53 PMID: 12692541
  42. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria.
    Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15064-9 PMID: 18806221
  43. Critical role of lipid composition in membrane permeabilization by rabbit neutrophil defensins.
    J Biol Chem. 1997 Sep 26;272(39):24224-33 PMID: 9305875
  44. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis.
    PLoS Med. 2008 Mar 4;5(3):e54 PMID: 18318598
  45. Characterization of novel beta-galactosidase activity that contributes to glycoprotein degradation and virulence in Streptococcus pneumoniae.
    Infect Immun. 2010 Jan;78(1):348-57 PMID: 19841081
  46. Structure, function, and membrane integration of defensins.
    Curr Opin Struct Biol. 1995 Aug;5(4):521-7 PMID: 8528769
  47. Secretory component: a new role in secretory IgA-mediated immune exclusion in vivo.
    Immunity. 2002 Jul;17(1):107-15 PMID: 12150896
  48. Changes in the mucosal barrier during acute and chronic Trichuris muris infection.
    Parasite Immunol. 2011 Jan;33(1):45-55 PMID: 21155842
  49. Nucleotide-induced mucin release from primary hamster tracheal surface epithelial cells involves the P2u purinoceptor.
    Eur Respir J. 1996 Mar;9(3):542-8 PMID: 8730017
  50. Shigella flexneri regulates tight junction-associated proteins in human intestinal epithelial cells.
    Cell Microbiol. 2002 Jun;4(6):367-81 PMID: 12067320
  51. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents.
    Cancer Cell. 2004 Feb;5(2):163-75 PMID: 14998492
  52. Calcium-dependent protein interactions in MUC5B provide reversible cross-links in salivary mucus.
    J Biol Chem. 2003 Aug 1;278(31):28703-10 PMID: 12756239
  53. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production.
    J Clin Invest. 2009 Oct;119(10):2914-24 PMID: 19759516
  54. Normal mouse intestinal mucus release requires cystic fibrosis transmembrane regulator-dependent bicarbonate secretion.
    J Clin Invest. 2009 Sep;119(9):2613-22 PMID: 19726884
  55. MT1-MMP mediates MUC1 shedding independent of TACE/ADAM17.
    Biochem J. 2004 Aug 15;382(Pt 1):363-73 PMID: 15130087
  56. Structure and function of the cell surface (tethered) mucins.
    Annu Rev Physiol. 2008;70:431-57 PMID: 17850209
  57. Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin.
    Nat Struct Mol Biol. 2006 Jan;13(1):71-6 PMID: 16369486
  58. Bacteria of the human intestinal microbiota produce glycosidases specific for lacto-series glycosphingolipids.
    J Biochem. 1990 Sep;108(3):466-74 PMID: 2277039
  59. TNF-alpha activates MUC2 transcription via NF-kappaB but inhibits via JNK activation.
    Cell Physiol Biochem. 2005;15(1-4):29-40 PMID: 15665513
  60. Proteolytic degradation of human salivary MUC5B by dental biofilms.
    Microbiology (Reading). 2009 Sep;155(Pt 9):2866-2872 PMID: 19556293
  61. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection.
    J Clin Invest. 2007 Aug;117(8):2313-24 PMID: 17641781
  62. Paneth cells and innate mucosal immunity.
    Curr Opin Gastroenterol. 2010 Nov;26(6):547-53 PMID: 20693892
  63. Campylobacter pyloridis degrades mucin and undermines gastric mucosal integrity.
    Biochem Biophys Res Commun. 1987 Apr 14;144(1):307-14 PMID: 3579908
  64. The human trefoil peptide, TFF1, is present in different molecular forms that are intimately associated with mucus in normal stomach.
    Gut. 2000 Mar;46(3):312-20 PMID: 10673290
  65. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine?
    Nat Immunol. 2004 Jun;5(6):569-73 PMID: 15164016
  66. Interleukin-4 induces specific pp-GalNAc-T expression and alterations in mucin O-glycosylation in colonic epithelial cells.
    Biochim Biophys Acta. 2008 Mar;1780(3):577-84 PMID: 17916404
  67. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus.
    Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1482-7 PMID: 17244708
  68. Altering mucus rheology to "solidify" human mucus at the nanoscale.
    PLoS One. 2009;4(1):e4294 PMID: 19173002
  69. A novel bacterial mucinase, glycosulfatase, is associated with bacterial vaginosis.
    J Clin Microbiol. 2005 Nov;43(11):5504-8 PMID: 16272477
  70. Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis.
    Gastroenterology. 2007 Oct;133(4):1210-8 PMID: 17919495
  71. Characterization of two different endo-alpha-N-acetylgalactosaminidases from probiotic and pathogenic enterobacteria, Bifidobacterium longum and Clostridium perfringens.
    Glycobiology. 2008 Sep;18(9):727-34 PMID: 18559962
  72. IL-6 and IL-8 increase the expression of glycosyltransferases and sulfotransferases involved in the biosynthesis of sialylated and/or sulfated Lewisx epitopes in the human bronchial mucosa.
    Biochem J. 2008 Feb 15;410(1):213-23 PMID: 17944600
  73. The increase in mucin exocytosis and the upregulation of MUC genes encoding for membrane-bound mucins induced by the thiol-activated exotoxin listeriolysin O is a host cell defence response that inhibits the cell-entry of Listeria monocytogenes.
    Cell Microbiol. 2005 Jul;7(7):1035-48 PMID: 15953034
  74. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA.
    Science. 2003 May 30;300(5624):1430-4 PMID: 12775840
  75. Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense.
    Science. 1999 Oct 1;286(5437):113-7 PMID: 10506557
  76. SAM pointed domain ETS factor (SPDEF) regulates terminal differentiation and maturation of intestinal goblet cells.
    Exp Cell Res. 2010 Feb 1;316(3):452-65 PMID: 19786015
  77. Allergen-induced IL-9 directly stimulates mucin transcription in respiratory epithelial cells.
    J Clin Invest. 1999 Nov;104(10):1375-82 PMID: 10562299
  78. The protein disulfide isomerase AGR2 is essential for production of intestinal mucus.
    Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):6950-5 PMID: 19359471
  79. CD4+ T-cell-dependent goblet cell proliferation and expulsion of Gymnophalloides seoi from the intestine of C57BL/6 mice.
    J Parasitol. 2009 Jun;95(3):581-90 PMID: 19061302
  80. Campylobacter jejuni response to human mucin MUC2: modulation of colonization and pathogenicity determinants.
    J Med Microbiol. 2008 Jul;57(Pt 7):795-802 PMID: 18566135
  81. Tumor necrosis factor-alpha (TNF-alpha) stimulates mucin secretion and gene expression in airway epithelium in vitro.
    Chest. 1995 Mar;107(3 Suppl):133S-135S PMID: 7533072
  82. Mucin biosynthesis in the bovine goblet cell induced by Cooperia oncophora infection.
    Vet Parasitol. 2009 Nov 12;165(3-4):281-9 PMID: 19647371
  83. Effects of VIP on the regulation of mucin secretion in cultured human pancreatic cancer cells (Capan-1).
    In Vitro Cell Dev Biol Anim. 1995 Mar;31(3):227-33 PMID: 7757305
  84. Glycan foraging in vivo by an intestine-adapted bacterial symbiont.
    Science. 2005 Mar 25;307(5717):1955-9 PMID: 15790854
  85. The immune geography of IgA induction and function.
    Mucosal Immunol. 2008 Jan;1(1):11-22 PMID: 19079156
  86. ER stress and the unfolded protein response in intestinal inflammation.
    Am J Physiol Gastrointest Liver Physiol. 2010 Jun;298(6):G820-32 PMID: 20338921
  87. The rotavirus surface protein VP8 modulates the gate and fence function of tight junctions in epithelial cells.
    J Cell Sci. 2004 Nov 1;117(Pt 23):5509-19 PMID: 15494377
  88. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions.
    Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4659-65 PMID: 20615996
  89. IL-13 induces mucin production by stimulating epidermal growth factor receptors and by activating neutrophils.
    Am J Physiol Lung Cell Mol Physiol. 2001 Jan;280(1):L134-40 PMID: 11133503
  90. Mucin biosynthesis: upregulation of core 2 beta 1,6 N-acetylglucosaminyltransferase by retinoic acid and Th2 cytokines in a human airway epithelial cell line.
    Am J Physiol Lung Cell Mol Physiol. 2005 Jan;288(1):L116-24 PMID: 15591039
  91. Entry of microbes into the host: using M cells to break the mucosal barrier.
    Curr Opin Immunol. 1995 Aug;7(4):474-8 PMID: 7495510
  92. Tight junctions as targets of infectious agents.
    Biochim Biophys Acta. 2009 Apr;1788(4):832-41 PMID: 19059200
  93. Improved in vitro model systems for gastrointestinal infection by choice of cell line, pH, microaerobic conditions, and optimization of culture conditions.
    Helicobacter. 2007 Aug;12(4):341-53 PMID: 17669108
  94. Effects of weaning and infection with Teladorsagia circumcincta on mucin carbohydrate profiles of early weaned lambs.
    Vet Parasitol. 2010 Aug 4;171(3-4):354-60 PMID: 20434846
  95. Microbial-host interactions specifically control the glycosylation pattern in intestinal mouse mucosa.
    Histochem Cell Biol. 2002 Aug;118(2):149-61 PMID: 12189518
  96. Mucin gene (MUC 2 and MUC 5AC) upregulation by Gram-positive and Gram-negative bacteria.
    Biochim Biophys Acta. 1998 Apr 28;1406(3):251-9 PMID: 9630659
  97. The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells.
    Am J Physiol Gastrointest Liver Physiol. 2007 Jan;292(1):G315-22 PMID: 16973917
  98. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases.
    Inflamm Bowel Dis. 2011 Jan;17(1):179-84 PMID: 20839241
  99. The ability to utilize mucin affects the regulation of virulence gene expression in Streptococcus pneumoniae.
    FEMS Microbiol Lett. 2008 Jan;278(2):231-5 PMID: 18053067
  100. LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells.
    Cell Immunol. 2003 Jan;221(1):42-9 PMID: 12742381
  101. Regulated airway goblet cell mucin secretion.
    Annu Rev Physiol. 2008;70:487-512 PMID: 17988208
  102. Mucin dynamics in intestinal bacterial infection.
    PLoS One. 2008;3(12):e3952 PMID: 19088856
  103. M cells and the pathogenesis of mucosal and systemic infections.
    Trends Microbiol. 1996 Jan;4(1):22-9 PMID: 8824791
  104. Cellular routes of invasion by enteropathogens.
    Curr Opin Microbiol. 2000 Feb;3(1):54-9 PMID: 10679413
  105. Alteration of the murine gut microbiota during infection with the parasitic helminth Heligmosomoides polygyrus.
    Inflamm Bowel Dis. 2010 Nov;16(11):1841-9 PMID: 20848461
  106. Early epithelial invasion by Salmonella enterica serovar Typhimurium DT104 in the swine ileum.
    Vet Pathol. 2002 Nov;39(6):712-20 PMID: 12450202
  107. Interleukin-13 mediates a fundamental pathway for airway epithelial mucus induced by CD4 T cells and interleukin-9.
    Am J Respir Cell Mol Biol. 2002 Nov;27(5):593-602 PMID: 12397019
  108. Characterization of the StcE protease activity of Escherichia coli O157:H7.
    J Bacteriol. 2006 Jul;188(13):4646-53 PMID: 16788173
  109. Stimulation of airway mucin gene expression by interleukin (IL)-17 through IL-6 paracrine/autocrine loop.
    J Biol Chem. 2003 May 9;278(19):17036-43 PMID: 12624114
  110. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo.
    Am J Physiol Gastrointest Liver Physiol. 2001 May;280(5):G922-9 PMID: 11292601
  111. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine.
    Cell. 2010 Jun 25;141(7):1135-45 PMID: 20602997
  112. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa.
    Trends Microbiol. 2004 Nov;12(11):509-17 PMID: 15488392
  113. Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells.
    Am J Physiol. 1999 May;276(5):L835-43 PMID: 10330040
  114. Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response.
    Cancer Cell. 2005 Feb;7(2):167-78 PMID: 15710329
  115. Fut2-null mice display an altered glycosylation profile and impaired BabA-mediated Helicobacter pylori adhesion to gastric mucosa.
    Glycobiology. 2009 Dec;19(12):1525-36 PMID: 19706747
  116. Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein.
    Gastroenterology. 1995 Aug;109(2):516-23 PMID: 7615201
  117. Commensal ocular bacteria degrade mucins.
    Br J Ophthalmol. 2002 Dec;86(12):1412-6 PMID: 12446377
  118. Direct secretory effect of interleukin-1 via type I receptors in human colonic mucous epithelial cells (HT29-C1.16E).
    Gut. 1996 Feb;38(2):240-2 PMID: 8801204
  119. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease.
    Cell. 2008 Sep 5;134(5):743-56 PMID: 18775308
  120. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection.
    Gastroenterology. 2006 Jul;131(1):117-29 PMID: 16831596
  121. Effects of activation of polymorphonuclear leukocytes on airway goblet cell mucin release in a co-culture system.
    Inflamm Res. 2003 Jun;52(6):258-62 PMID: 12835897
  122. Two-hybrid analysis of human salivary mucin MUC7 interactions.
    Biochim Biophys Acta. 2005 Oct 30;1746(1):65-72 PMID: 16203048
  123. Direct effects of IL-4/IL-13 and the nematode Nippostrongylus brasiliensis on intestinal epithelial cells in vitro.
    Parasite Immunol. 2010 Jun;32(6):420-9 PMID: 20500673
  124. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes.
    Gastroenterology. 2010 Dec;139(6):1844-1854.e1 PMID: 20816835
  125. Regulation of secretion from mucous and serous cells in the excised ferret trachea.
    Respir Physiol. 2001 Jun;126(2):163-71 PMID: 11348643
  126. pS2/TFF1 interacts directly with the VWFC cysteine-rich domains of mucins.
    Gastroenterology. 2000 Jan;118(1):70-80 PMID: 10611155
  127. Candidacidal activity prompted by N-terminus histatin-like domain of human salivary mucin (MUC7)1.
    Biochim Biophys Acta. 1999 Apr 12;1431(1):107-19 PMID: 10209284
  128. TNF-alpha in the regulation of MUC5AC secretion: some aspects of cytokine-induced mucin hypersecretion on the in vitro model.
    Cytokine. 2000 Nov;12(11):1732-6 PMID: 11052828
  129. Tumor necrosis factor alpha is a critical component of interleukin 13-mediated protective T helper cell type 2 responses during helminth infection.
    J Exp Med. 1999 Oct 4;190(7):953-62 PMID: 10510085
  130. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression.
    J Immunol. 2001 Aug 15;167(4):1882-5 PMID: 11489966
  131. MUC1 gene polymorphism and gastric cancer--an epidemiological study.
    Glycoconj J. 1997 Jan;14(1):107-11 PMID: 9076520
  132. The use of lectins in monitoring degradation of oligosaccharide chains in mucin by oral streptococci.
    Caries Res. 1994;28(4):257-61 PMID: 7520835
  133. Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection.
    Gastroenterology. 2010 May;138(5):1763-71 PMID: 20138044
  134. Response of germfree rat colonic mucous cells to peroral endotoxin application.
    Eur J Cell Biol. 1996 Sep;71(1):99-104 PMID: 8884183
  135. Adequate oral threonine is critical for mucin production and gut function in neonatal piglets.
    Am J Physiol Gastrointest Liver Physiol. 2007 May;292(5):G1293-301 PMID: 17234895
  136. The ets-domain transcription factor Spdef promotes maturation of goblet and paneth cells in the intestinal epithelium.
    Gastroenterology. 2009 Oct;137(4):1333-45.e1-3 PMID: 19549527
  137. Histochemistry of the surface mucous gel layer of the human colon.
    Gut. 1997 Jun;40(6):782-9 PMID: 9245933
  138. Up-regulation of mucin secretion in HT29-MTX cells by the pro-inflammatory cytokines tumor necrosis factor-alpha and interleukin-6.
    Eur Cytokine Netw. 2001 Mar;12(1):119-25 PMID: 11282555
  139. Disruption of Paneth and goblet cell homeostasis and increased endoplasmic reticulum stress in Agr2-/- mice.
    Dev Biol. 2010 Feb 15;338(2):270-9 PMID: 20025862
  140. MUC1 mucin is a negative regulator of toll-like receptor signaling.
    Am J Respir Cell Mol Biol. 2008 Mar;38(3):263-8 PMID: 18079492
  141. Interleukin-1beta induces MUC2 gene expression and mucin secretion via activation of PKC-MEK/ERK, and PI3K in human airway epithelial cells.
    J Korean Med Sci. 2002 Dec;17(6):765-71 PMID: 12482999
  142. Altered expression of goblet cell- and mucin glycosylation-related genes in the intestinal epithelium during infection with the nematode Nippostrongylus brasiliensis in rat.
    APMIS. 2006 Apr;114(4):270-8 PMID: 16689826
  143. Selective growth of mucolytic bacteria including Clostridium perfringens in a neonatal piglet model of total parenteral nutrition.
    Am J Clin Nutr. 2002 Nov;76(5):1117-25 PMID: 12399288
  144. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria.
    Am J Gastroenterol. 2010 Nov;105(11):2420-8 PMID: 20648002
  145. Regulation of IL-1beta-mediated MUC2 gene in NCI-H292 human airway epithelial cells.
    Biochem Biophys Res Commun. 2000 Jul 21;274(1):112-6 PMID: 10903904
  146. Characterization of Porphyromonas gingivalis-induced degradation of epithelial cell junctional complexes.
    Infect Immun. 2000 Mar;68(3):1441-9 PMID: 10678958
  147. Nitric oxide induces MUC5AC mucin in respiratory epithelial cells through PKC and ERK dependent pathways.
    Respir Res. 2007 Mar 29;8:28 PMID: 17391532
  148. IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo.
    J Immunol. 1999 May 15;162(10):6233-7 PMID: 10229869
  149. Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response.
    Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3300-5 PMID: 19202076
  150. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci.
    Nat Genet. 2010 Dec;42(12):1118-25 PMID: 21102463
  151. Lipopolysaccharide Induces Mucus Cell Metaplasia in Mouse Lung.
    Am J Respir Cell Mol Biol. 2001 Jan;24(1):66-73 PMID: 11152652
  152. Growth in and breakdown of purified rabbit small intestinal mucin by Yersinia enterocolitica.
    Infect Immun. 1993 Oct;61(10):4131-8 PMID: 8406802
  153. Structural and immunochemical identification of Le(a), Le(b), H type 1, and related glycolipids in small intestinal mucosa of a group O Le(a-b-) nonsecretor.
    Glycoconj J. 1997 Feb;14(2):209-23 PMID: 9111138
  154. The spatial orientation of Helicobacter pylori in the gastric mucus.
    Proc Natl Acad Sci U S A. 2004 Apr 6;101(14):5024-9 PMID: 15044704
  155. Chemotactic behavior of Campylobacter jejuni.
    Infect Immun. 1988 Jun;56(6):1560-6 PMID: 3372020
  156. Proinflammatory cytokines trigger MUC gene expression and mucin release in the intestinal cancer cell line LS180.
    Inflamm Res. 2000 Apr;49(4):162-9 PMID: 10858016
  157. Cytosolic phospholipase A2 activation in Helicobacter pylori lipopolysaccharide-induced interference with gastric mucin synthesis.
    IUBMB Life. 2006 Apr;58(4):217-23 PMID: 16754300
  158. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea.
    PLoS Pathog. 2010 Sep 09;6(9):e1001097 PMID: 20844578
  159. A novel mucin-sulphatase activity found in Burkholderia cepacia and Pseudomonas aeruginosa.
    J Med Microbiol. 1999 Jun;48(6):551-557 PMID: 10359304
  160. SPDEF regulates goblet cell hyperplasia in the airway epithelium.
    J Clin Invest. 2007 Apr;117(4):978-88 PMID: 17347682
  161. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells.
    Cell. 1996 Mar 22;84(6):923-32 PMID: 8601315
  162. Lectin binding profile of the small intestine of five-week-old pigs in response to the use of chlortetracycline as a growth promotant and under gnotobiotic conditions.
    J Anim Sci. 2007 Jul;85(7):1640-50 PMID: 17400973
  163. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity.
    Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14321-6 PMID: 19706518
  164. The multifaceted Paneth cell.
    Cell Mol Life Sci. 2002 Jan;59(1):156-70 PMID: 11846026
  165. Symbiotic bacteria direct expression of an intestinal bactericidal lectin.
    Science. 2006 Aug 25;313(5790):1126-30 PMID: 16931762
  166. Role of ABO secretor status in mucosal innate immunity and H. pylori infection.
    PLoS Pathog. 2008 Jan;4(1):e2 PMID: 18179282
  167. Histochemical, lectin-histochemical and morphometrical characteristics of intestinal goblet cells of germfree and conventional mice.
    Exp Anim. 1996 Apr;45(2):155-60 PMID: 8726140
  168. Natural antibiotic function of a human gastric mucin against Helicobacter pylori infection.
    Science. 2004 Aug 13;305(5686):1003-6 PMID: 15310903
  169. MUC1 polymorphism confers increased risk for intestinal metaplasia in a Colombian population with chronic gastritis.
    Eur J Hum Genet. 2003 May;11(5):380-4 PMID: 12734543
  170. Colonization of microflora in mice: mucosal defense against luminal bacteria.
    J Gastroenterol. 1999 Feb;34(1):54-60 PMID: 10204611
  171. Enteric defensins are essential regulators of intestinal microbial ecology.
    Nat Immunol. 2010 Jan;11(1):76-83 PMID: 19855381
  172. The roles of enteric bacterial sialidase, sialate O-acetyl esterase and glycosulfatase in the degradation of human colonic mucin.
    Glycoconj J. 1993 Feb;10(1):72-81 PMID: 8358229
  173. Entamoeba histolytica cysteine proteases cleave the MUC2 mucin in its C-terminal domain and dissolve the protective colonic mucus gel.
    Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9298-303 PMID: 16754877
  174. The composition and function of M cell apical membranes: implications for microbial pathogenesis.
    Semin Immunol. 1999 Jun;11(3):171-81 PMID: 10381863
  175. Mucoactive agents for airway mucus hypersecretory diseases.
    Respir Care. 2007 Sep;52(9):1176-93; discussion 1193-7 PMID: 17716385
  176. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont.
    J Biol Chem. 2009 Jul 3;284(27):18445-57 PMID: 19403529
  177. Exogenous nitric oxide stimulates mucin secretion from LS174T colonic adenocarcinoma cells.
    Inflamm Res. 1996 Apr;45(4):209-12 PMID: 8741012
  178. Influence of colonizing micro-flora on the mucin histochemistry of the neonatal mouse colon.
    Histochem J. 1990 Feb;22(2):102-5 PMID: 2329051
  179. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation.
    Science. 2002 Jul 26;297(5581):573-8 PMID: 12142529
  180. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells.
    Nat Med. 2002 Jan;8(1):41-6 PMID: 11786905
  181. Angiogenins: a new class of microbicidal proteins involved in innate immunity.
    Nat Immunol. 2003 Mar;4(3):269-73 PMID: 12548285
  182. Microbiota-immune system interaction: an uneasy alliance.
    Curr Opin Microbiol. 2011 Feb;14(1):99-105 PMID: 20971034
Article Info
Journal
Nature reviews. Microbiology
Abbr.
Nat Rev Microbiol
ISSN
1740-1534
DOI
10.1038/nrmicro2538
Email
mmcguckin@mmri.mater.org.au
Published
2011-04-00
Pages
265-78
Language
English
Region
England
NLM ID
101190261
Subset
IM
External Links
PubMed source DOI: 10.1038/nrmicro2538 View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2