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PMID: 19088856 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Mucin dynamics in intestinal bacterial infection.

PloS one ·Vol. 3 ·No. 12 ·2008-00-00 ·Pages e3952

Lindén SK, Florin TH, McGuckin MA

Abstract

Bacterial gastroenteritis causes morbidity and mortality in humans worldwide. Murine Citrobacter rodentium infection is a model for gastroenteritis caused by the human pathogens enteropathogenic Escherichia coli and enterohaemorrhagic E. coli. Mucin glycoproteins are the main component of the first barrier that bacteria encounter in the intestinal tract. Using Immunohistochemistry, we investigated intestinal expression of mucins (Alcian blue/PAS, Muc1, Muc2, Muc4, Muc5AC, Muc13 and Muc3/17) in healthy and C. rodentium infected mice. The majority of the C. rodentium infected mice developed systemic infection and colitis in the mid and distal colon by day 12. C. rodentium bound to the major secreted mucin, Muc2, in vitro, and high numbers of bacteria were found in secreted MUC2 in infected animals in vivo, indicating that mucins may limit bacterial access to the epithelial surface. In the small intestine, caecum and proximal colon, the mucin expression was similar in infected and non-infected animals. In the distal colonic epithelium, all secreted and cell surface mucins decreased with the exception of the Muc1 cell surface mucin which increased after infection (p<0.05). Similarly, during human infection Salmonella St Paul, Campylobacter jejuni and Clostridium difficile induced MUC1 in the colon. Major changes in both the cell-surface and secreted mucins occur in response to intestinal infection.

MeSH Terms
Adult Aged Animals Cecum/microbiology,pathology Citrobacter rodentium/isolation & purification,physiology Enterobacteriaceae Infections/complications,metabolism,pathology Female Humans Intestinal Diseases/etiology,metabolism,pathology Intestine, Large/microbiology,pathology Male Mice Mice, Inbred C57BL Middle Aged Mucins/metabolism Tissue Distribution Young Adult
Chemicals
Mucins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lindén Sara K
Mucosal Diseases Program, Mater Medical Research Institute, Mater Health Services, South Brisbane, Queensland, Australia.
Florin Timothy H J
McGuckin Michael A
References (63)
63 references, click to expand
  1. Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity.
    Glycobiology. 2001 Feb;11(2):1R-10R PMID: 11287395
  2. Saponification-induced increase in the periodic acid-Schiff reaction in the gastrointestinal tract. Mechanism and distribution of the reactive substance.
    J Histochem Cytochem. 1973 May;21(5):473-82 PMID: 4125552
  3. Campylobacter colitis.
    Br Med J. 1979 Mar 31;1(6167):857-9 PMID: 435842
  4. Comprehensive study of the intestinal stage of listeriosis in a rat ligated ileal loop system.
    Infect Immun. 1998 Feb;66(2):747-55 PMID: 9453636
  5. Effects of pH on Helicobacter pylori binding to human gastric mucins: identification of binding to non-MUC5AC mucins.
    Biochem J. 2004 Dec 1;384(Pt 2):263-70 PMID: 15260802
  6. Abnormal expression of M1/MUC5AC mucin in distal colon of patients with diverticulitis, ulcerative colitis and cancer.
    Int J Cancer. 2007 Oct 1;121(7):1543-9 PMID: 17565737
  7. Host defences to Citrobacter rodentium.
    Int J Med Microbiol. 2003 Apr;293(1):87-93 PMID: 12755369
  8. Muc13, a novel human cell surface mucin expressed by epithelial and hemopoietic cells.
    J Biol Chem. 2001 May 25;276(21):18327-36 PMID: 11278439
  9. Structure and function of the polymeric mucins in airways mucus.
    Annu Rev Physiol. 2008;70:459-86 PMID: 17850213
  10. Mucin secretion by the human colon cell line LS174T is regulated by bile salts.
    Glycobiology. 1999 Jan;9(1):13-9 PMID: 9884402
  11. Binding of rotavirus by a 46 kD milk-glycoprotein may prevent gastroenteritis.
    J Pediatr Gastroenterol Nutr. 1993 Aug;17(2):228-30 PMID: 8229555
  12. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals.
    Gastroenterology. 2002 Jun;122(7):1967-77 PMID: 12055602
  13. Immunohistochemical detection of MUC2 mucin core protein in ulcerative colitis.
    J Clin Lab Anal. 1998;12(3):150-3 PMID: 9591701
  14. Human milk glycans protect infants against enteric pathogens.
    Annu Rev Nutr. 2005;25:37-58 PMID: 16011458
  15. Synthesis and secretion of Muc4/sialomucin complex: implication of intracellular proteolysis.
    Biochem J. 2002 Nov 15;368(Pt 1):41-8 PMID: 12186632
  16. 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
  17. 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
  18. Mucins in the gastrointestinal tract in health and disease.
    Front Biosci. 2001 Oct 01;6:D1321-57 PMID: 11578958
  19. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection.
    J Biol Chem. 2003 Apr 18;278(16):14112-20 PMID: 12562767
  20. 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
  21. MUC17, a novel membrane-tethered mucin.
    Biochem Biophys Res Commun. 2002 Mar 1;291(3):466-75 PMID: 11855812
  22. 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
  23. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression.
    Am J Physiol. 1999 Apr;276(4):G941-50 PMID: 10198338
  24. Morphological observations on mucus-secreting nongoblet cells in the deep crypts of the rat ascending colon.
    Am J Anat. 1983 May;167(1):95-117 PMID: 6869312
  25. Fcgamma receptor regulation of Citrobacter rodentium infection.
    Infect Immun. 2008 Apr;76(4):1728-37 PMID: 18227164
  26. Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis.
    Gastroenterology. 2007 Oct;133(4):1210-8 PMID: 17919495
  27. Studies on the "insoluble" glycoprotein complex from human colon. Identification of reduction-insensitive MUC2 oligomers and C-terminal cleavage.
    J Biol Chem. 1999 May 28;274(22):15828-36 PMID: 10336486
  28. Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms.
    Gastroenterology. 2002 Dec;123(6):1923-30 PMID: 12454849
  29. 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
  30. 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
  31. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro.
    Gut. 2003 Jun;52(6):827-33 PMID: 12740338
  32. Mucins and mucin binding proteins in colorectal cancer.
    Cancer Metastasis Rev. 2004 Jan-Jun;23(1-2):77-99 PMID: 15000151
  33. Citrobacter rodentium of mice and man.
    Cell Microbiol. 2005 Dec;7(12):1697-706 PMID: 16309456
  34. Sialomucin complex, a heterodimeric glycoprotein complex. Expression as a soluble, secretable form in lactating mammary gland and colon.
    J Biol Chem. 1996 Dec 27;271(52):33476-85 PMID: 8969211
  35. 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
  36. Alterations in the composition of the supramucosal defense barrier in relation to disease severity of ulcerative colitis.
    J Histochem Cytochem. 2006 Dec;54(12):1335-48 PMID: 16924127
  37. Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection.
    Infect Immun. 2004 Jul;72(7):4188-99 PMID: 15213163
  38. Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism.
    Microbiology (Reading). 2007 Apr;153(Pt 4):959-967 PMID: 17379706
  39. Host-bacterial mutualism in the human intestine.
    Science. 2005 Mar 25;307(5717):1915-20 PMID: 15790844
  40. 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
  41. Human milk mucin inhibits rotavirus replication and prevents experimental gastroenteritis.
    J Clin Invest. 1992 Nov;90(5):1984-91 PMID: 1331178
  42. Endoplasmic reticulum stress signaling in disease.
    Physiol Rev. 2006 Oct;86(4):1133-49 PMID: 17015486
  43. Characterization of the StcE protease activity of Escherichia coli O157:H7.
    J Bacteriol. 2006 Jul;188(13):4646-53 PMID: 16788173
  44. Glycoproteins of the human milk fat globule in the protection of the breast-fed infant against infections.
    Biol Neonate. 1998;74(2):143-62 PMID: 9691156
  45. Mucins in the mucosal barrier to infection.
    Mucosal Immunol. 2008 May;1(3):183-97 PMID: 19079178
  46. Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells.
    Am J Physiol. 1999 May;276(5):L835-43 PMID: 10330040
  47. Citrobacter rodentium infection causes iNOS-independent intestinal epithelial dysfunction in mice.
    Can J Physiol Pharmacol. 2006 Dec;84(12):1301-12 PMID: 17487239
  48. Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli.
    J Bacteriol. 2007 Oct;189(20):7426-35 PMID: 17693516
  49. 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
  50. 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
  51. Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland.
    J Biol Chem. 2001 Apr 20;276(16):13057-64 PMID: 11278868
  52. 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
  53. Regulation of secretion from mucous and serous cells in the excised ferret trachea.
    Respir Physiol. 2001 Jun;126(2):163-71 PMID: 11348643
  54. 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
  55. Species-specific cell adhesion of enteropathogenic Escherichia coli is mediated by type IV bundle-forming pili.
    Cell Microbiol. 2002 Jan;4(1):29-42 PMID: 11856171
  56. Src kinase-dependent epidermal growth factor receptor transactivation in PPARgamma ligand-induced suppression of Porphyromonas gingivalis interference with salivary mucin synthesis.
    IUBMB Life. 2004 Mar;56(3):153-9 PMID: 15185749
  57. Rhesus monkey gastric mucins: oligomeric structure, glycoforms and Helicobacter pylori binding.
    Biochem J. 2004 May 1;379(Pt 3):765-75 PMID: 14736333
  58. 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
  59. Cytosolic phospholipase A2 activation in Helicobacter pylori lipopolysaccharide-induced interference with gastric mucin synthesis.
    IUBMB Life. 2006 Apr;58(4):217-23 PMID: 16754300
  60. Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen.
    Infect Immun. 2008 Feb;76(2):796-811 PMID: 17984203
  61. Exogenous nitric oxide stimulates mucin secretion from LS174T colonic adenocarcinoma cells.
    Inflamm Res. 1996 Apr;45(4):209-12 PMID: 8741012
  62. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies.
    Infect Immun. 2004 Jun;72(6):3315-24 PMID: 15155635
  63. Increased levels of mucins in the cystic fibrosis mouse small intestine, and modulator effects of the Muc1 mucin expression.
    Am J Physiol Gastrointest Liver Physiol. 2006 Aug;291(2):G203-10 PMID: 16500918
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2008-00-00
Epub
2008-00-17
Pages
e3952
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC2601037
Subset
IM
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