Core 2 Mucin-Type O-Glycan Is Related to EPEC and EHEC O157:H7 Adherence to Human Colon Carcinoma HT-29 Epithelial Cells

Digestive Diseases and Sciences

Volumn 60, Issue 7, 2015, Pages 1977-1990

  Ye, Jun ^a   Song, Lili ^a   Liu, Yun ^a   Pan, Qiong ^a   Zhong, Xiaoli ^a   Li, Shanshan ^a   Shang, Yangyang ^a   Tian, Yin ^a   He, Yonghong ^a   Chen, Lei ^a   Chen, Wensheng ^a   Peng, Zhihong ^a   Wang, Rongquan ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Adherence; Enterohemorrhagic E. coli O157:H7; Enteropathogenic E. coli; Mucin; O Glycan

Indexed keywords

ASPARAGINE LINKED OLIGOSACCHARIDE; GLYCAN; GREEN FLUORESCENT PROTEIN; MUCIN 2; MUCIN TYPE CORE 2 O GLYCAN; OCCLUDIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ANTIBODY; BENZYL DERIVATIVE; BENZYL-ALPHA-N-ACETYLGALACTOSAMINE; BETA-1,3-GALACTOSYL-O-GLYCOSYL-GLYCOPROTEIN BETA-1,6-N-ACETYLGLUCOSAMINYLTRANSFERASE 3; MUC2 PROTEIN, HUMAN; N ACETYLGALACTOSAMINE; N ACETYLGLUCOSAMINYLTRANSFERASE;

APOPTOSIS; ARTICLE; BACTERIUM ADHERENCE; CELL ADHESION; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL SURFACE; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; GLYCOSYLATION; HOST CELL; HT 29 CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; ANALOGS AND DERIVATIVES; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

ACETYLGALACTOSAMINE; ANTIBODIES; BACTERIAL ADHESION; BENZYL COMPOUNDS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; HT29 CELLS; HUMANS; MUCIN-2; N-ACETYLGLUCOSAMINYLTRANSFERASES; RNA INTERFERENCE;

EID: 84930822976     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-015-3548-5     Document Type: Article

References (39)

1. Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep. 2010;12:319–330.
2. Linden SK, Florin TH, McGuckin MA. Mucin dynamics in intestinal bacterial infection. PLoS One. 2008;3:e3952.
3. Lieleg O, Lieleg C, Bloom J, Buck CB, Ribbeck K. Mucin biopolymers as broad-spectrum antiviral agents. Biomacromolecules. 2012;13:1724–1732.
4. Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol. 1999;276:G941–G950.
5. Wang R, Khatri IA, Forstner JF. C-terminal domain of rodent intestinal mucin Muc3 is proteolytically cleaved in the endoplasmic reticulum to generate extracellular and membrane components. Biochem J. 2002;366:623–631.
6. Moran AP, Gupta A, Joshi L. Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut. 2011;60:1412–1425.
7. Radhakrishnan P, Grandgenett PM, Mohr AM, et al. Expression of core 3 synthase in human pancreatic cancer cells suppresses tumor growth and metastasis. Int J Cancer. 2013;133:2824–2833.
8. Hang HC, Bertozzi CR. The chemistry and biology of mucin-type O-linked glycosylation. Bioorg Med Chem. 2005;13:5021–5034.
9. Stone EL, Ismail MN, Lee SH, et al. Glycosyltransferase function in core 2-type protein O glycosylation. Mol Cell Biol. 2009;29:3770–3782.
10. Yeh JC, Ong E, Fukuda M. Molecular cloning and expression of a novel beta-1,6-N-acetylglucosaminyltransferase that forms core 2, core 4, and I branches. J Biol Chem. 1999;274:3215–3221.
11. Ismail MN, Stone EL, Panico M, et al. High-sensitivity O-glycomic analysis of mice deficient in core 2 {beta}1,6-N-acetylglucosaminyltransferases. Glycobiology. 2011;21:82–98.
12. Guerrant RL, Hughes JM, Lima NL, Crane J. Diarrhea in developed and developing countries: magnitude, special settings, and etiologies. Rev Infect Dis. 1990;12:S41–S50.
13. Jarvis KG, Giron JA, Jerse AE, McDaniel TK, Donnenberg MS, Kaper JB. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci USA. 1995;92:7996–8000.
14. Karch H, Tarr PI, Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol. 2005;295:405–418.
15. Yu AC, Worrall LJ, Strynadka NC. Structural insight into the bacterial mucinase StcE essential to adhesion and immune evasion during enterohemorrhagic E. coli infection. Structure. 2012;20:707–717.
16. Hennebicq-Reig S, Tetaert D, Soudan B, et al. O-Glycosylation and cellular differentiation in a subpopulation of mucin-secreting HT-29 cell line. Exp Cell Res. 1997;235:100–107.
17. Pan Q, Tian Y, Li X, et al. Enhanced membrane-tethered mucin 3 (MUC3) expression by a tetrameric branched peptide with a conserved TFLK motif inhibits bacteria adherence. J Biol Chem. 2013;288:5407–5416.
18. Bell SL, Xu G, Khatri IA, Wang R, Rahman S, Forstner JF. N-linked oligosaccharides play a role in disulphide-dependent dimerization of intestinal mucin Muc2. Biochem J. 2003;373:893–900.
19. Xu G, Huan LJ, Khatri IA, et al. cDNA for the carboxyl-terminal region of a rat intestinal mucin-like peptide. J Biol Chem. 1992;267:5401–5407.
20. Gout S, Marie C, Laine M, Tavernier G, Block MR, Jacquier-Sarlin M. Early enterocytic differentiation of HT-29 cells: biochemical changes and strength increases of adherens junctions. Exp Cell Res. 2004;299:498–510.
21. Mack DR, Hollingsworth MA. Alteration in expression of MUC2 and MUC3 mRNA levels in HT29 colonic carcinoma cells. Biochem Biophys Res Commun. 1994;199:1012–1018.
22. Huet G, Hennebicq-Reig S, de Bolos C, et al. GalNAc-alpha-O-benzyl inhibits NeuAcalpha2-3 glycosylation and blocks the intracellular transport of apical glycoproteins and mucus in differentiated HT-29 cells. J Cell Biol. 1998;141:1311–1322.
23. Tian Y, Pan Q, Shang Y, et al. MicroRNA-200 (miR-200) cluster regulation by achaete scute-like 2 (Ascl2): impact on the epithelial-mesenchymal transition in colon cancer cells. J Biol Chem. 2014;289:36101–36115.
24. Yu D, Zhao L, Xue T, Sun B. Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol. 2012;12:288.
25. Yang Y, Chen L, Tian Y, et al. Numb modulates the paracellular permeability of intestinal epithelial cells through regulating apical junctional complex assembly and myosin light chain phosphorylation. Exp Cell Res. 2013;319:3214–3225.
26. Cleary J, Lai LC, Shaw RK, et al. Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology. 2004;150:527–538.
27. Sherman PM, Johnson-Henry KC, Yeung HP, Ngo PS, Goulet J, Tompkins TA. Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O127:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect Immun. 2005;73:5183–5188.
28. Johansson ME, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol. 2013;10:352–361.
29. Heazlewood CK, Cook MC, Eri R, et al. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med. 2008;5:e54.
30. Strugala V, Dettmar PW, Pearson JP. Thickness and continuity of the adherent colonic mucus barrier in active and quiescent ulcerative colitis and Crohn’s disease. Int J Clin Pract. 2008;62:762–769.
31. Yu H, He Y, Zhang X, et al. The rat IgGFcgammaBP and Muc2 C-terminal domains and TFF3 in two intestinal mucus layers bind together by covalent interaction. PLoS One. 2011;6:e20334.
32. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA. 2008;105:15064–15069.
33. Bergstrom KS, Xia L. Mucin-type O-glycans and their roles in intestinal homeostasis. Glycobiology. 2013;23:1026–1037.
34. Gouyer V, Leteurtre E, Delmotte P, et al. Differential effect of GalNAcalpha-O-bn on intracellular trafficking in enterocytic HT-29 and Caco-2 cells: correlation with the glycosyltransferase expression pattern. J Cell Sci. 2001;114:1455–1471.
35. Sajjan SU, Forstner JF. Characteristics of binding of Escherichia coli serotype O157:H7 strain CL-49 to purified intestinal mucin. Infect Immun. 1990;58:860–867.
36. Zarepour M, Bhullar K, Montero M, et al. The mucin Muc2 limits pathogen burdens and epithelial barrier dysfunction during Salmonella enterica serovar Typhimurium colitis. Infect Immun. 2013;81:3672–3683.
37. Mouricout M, Milhavet M, Durie C, Grange P. Characterization of glycoprotein glycan receptors for Escherichia coli F17 fimbrial lectin. Microb Pathog. 1995;18:297–306.
38. Venegas MF, Navas EL, Gaffney RA, Duncan JL, Anderson BE, Schaeffer AJ. Binding of type 1-piliated Escherichia coli to vaginal mucus. Infect Immun. 1995;63:416–422.
39. Bergstrom KS, Guttman JA, Rumi M, et al. Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun. 2008;76:796–811.