Loss of intestinal core 1-derived O-glycans causes spontaneous colitis in mice

Journal of Clinical Investigation

Volumn 121, Issue 4, 2011, Pages 1657-1666

  Fu, Jianxin ^a,b   Wei, Bo ^c   Wen, Tao ^a   Johansson, Malin E V ^d   Liu, Xiaowei ^a,g   Bradford, Emily ^e   Thomsson, Kristina A ^d   McGee, Samuel ^a   Mansour, Lilah ^f   Tong, Maomeng ^c   McDaniel, J Michael ^a   Sferra, Thomas J ^f   Turner, Jerrold R ^e   Chen, Hong ^a,f   Hansson, Gunnar C ^d   Braun, Jonathan ^c   Xia, Lijun ^a,b,f  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b SOOCHOW UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^g CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CORE 1BETA1,3 GALACTOSYLTRANSFERASE SPECIFIC CHAPERONE 1; OLIGOSACCHARIDE; TN ANTIGEN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL SPECIFICITY; COLITIS; COLON MUCOSA; GLYCOSYLATION; INTESTINE EPITHELIUM; LYMPHOCYTE; MISSENSE MUTATION; MOUSE; MUTATIONAL ANALYSIS; MYELOID DENDRITIC CELL; NONHUMAN; PRIORITY JOURNAL; ULCERATIVE COLITIS;

ANIMALS; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; BASE SEQUENCE; COLITIS; COLON; DISEASE MODELS, ANIMAL; DNA PRIMERS; GALACTOSYLTRANSFERASES; HUMANS; INTESTINAL MUCOSA; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR CHAPERONES; MUTATION; POLYSACCHARIDES;

EID: 79953307656     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45538     Document Type: Article

References (49)

1. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448(7152):427-434. (Pubitemid 47123518)
2. Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med. 2009;361(21):2066-2078.
3. Garrett WS, Gordon JI, Glimcher LH. Homeostasis and inflammation in the intestine. Cell. 2010;140(6):859-870.
4. Johansson ME, Holmén Larsson JM, Hansson GC. Microbes and Health Sackler Colloquium: The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. [published online ahead of print June 25, 2010]. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1006451107.
5. Ponda PP, Mayer L. Mucosal epithelium in health and disease. Curr Mol Med. 2005;5(6):549-556. (Pubitemid 41236555)
6. Zaph C, et al. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature. 2007;446(7135):552-556. (Pubitemid 46514719)
7. Olson TS, et al. The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med. 2006;203(3):541-552.
8. 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 U S A. 2008;105(39):15064-15069.
9. Gum JR Jr, Hicks JW, Toribara NW, Siddiki B, Kim YS. Molecular cloning of human intestinal mucin (MUC2) cDNA. Identification of the amino terminus and overall sequence similarity to prepro-von Willebrand factor. J Biol Chem. 1994;269(4):2440-2446.
10. Ju T, Brewer K, D'Souza A, Cummings RD, Canfield WM. Cloning and expression of human core 1 beta1,3-galactosyltransferase. J Biol Chem. 2002;277(1):178-186. (Pubitemid 34952043)
11. Fu J, et al. Endothelial cell O-glycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J Clin Invest. 2008;118(11):3725-3737.
12. Xia L, et al. Defective angiogenesis and fatal embryonic hemorrhage in mice lacking core 1-derived O-glycans. J Cell Biol. 2004;164(3):451-459. (Pubitemid 38174772)
13. Ju T, Aryal RP, Stowell CJ, Cummings RD. Regulation of protein O-glycosylation by the endoplasmic reticulum-localized molecular chaperone Cosmc. J Cell Biol. 2008;182(3):531-542.
14. Smithson JE, Campbell A, Andrews JM, Milton JD, Pigott R, Jewell DP. Altered expression of mucins throughout the colon in ulcerative colitis. Gut. 1997;40(2):234-240. (Pubitemid 27093100)
15. Podolsky DK, Isselbacher KJ. Composition of human colonic mucin. Selective alteration in inflammatory bowel disease. J Clin Invest. 1983;72(1):142-153. (Pubitemid 13026637)
16. Rhodes JM. Colonic mucus and ulcerative colitis. Gut. 1997;40(6):807-808. (Pubitemid 27305480)
17. Corfield AP, et al. Colonic mucins in ulcerative colitis: evidence for loss of sulfation. Glycoconj J. 1996;13(5):809-822. (Pubitemid 26354274)
18. Podolsky DK, Fournier DA. Alterations in mucosal content of colonic glycoconjugates in inflammatory bowel disease defined by monoclonal antibodies. Gastroenterology. 1988;95(2):379-387.
19. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem. 2002;277(36):33275-33283. (Pubitemid 34984848)
20. Elson CO, Cong Y, McCracken VJ, Dimmitt RA, Lorenz RG, Weaver CT. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev. 2005;206:260-276. (Pubitemid 41105175)
21. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992;68(5):869-877.
22. McEver RP. Adhesive interactions of leukocytes, platelets, and the vessel wall during hemostasis and inflammation. Thromb Haemost. 2001;86(3):746-756. (Pubitemid 32834182)
23. An G, et al. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med. 2007;204(6):1417-1429.
24. el Marjou F, et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis. 2004;39(3):186-193.
25. Marchiando AM, et al. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol. 2010;189(1):111-126.
26. Kaser A, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. 2008;134(5):743-756.
27. Kornfeld R, Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631-664. (Pubitemid 15073660)
28. Tarp MA, Clausen H. Mucin-type O-glycosylation and its potential use in drug and vaccine development. Biochim Biophys Acta. 2008;1780(3):546-563.
29. Samali A, Fitzgerald U, Deegan S, Gupta S. Methods for monitoring endoplasmic reticulum stress and the unfolded protein response. [published online ahead of print October 12, 2009]. Int J Cell Biol. doi:10.1155/2010/ 83037.
30. Ju T, Cummings RD. Protein glycosylation: chaperone mutation in Tn syndrome. Nature. 2005;437(7063):1252. (Pubitemid 41568663)
31. Ju T, et al. Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res. 2008;68(6):1636-1646. (Pubitemid 351416547)
32. Corfield AP, Carroll D, Myerscough N, Probert CS. Mucins in the gastrointestinal tract in health and disease. Front Biosci. 2001;6:D1321-D1357.
33. Van Klinken BJ, Van der Wal JW, Einerhand AW, Buller HA, Dekker J. Sulphation and secretion of the predominant secretory human colonic mucin MUC2 in ulcerative colitis. Gut. 1999;44(3):387-393. (Pubitemid 29119336)
34. Van der Sluis M, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131(1):117-129. (Pubitemid 44015753)
35. Heazlewood CK, et al. Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med. 2008;5(3):e54.
36. Johansson ME, et al. Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS One. 2010;5(8):e12238.
37. Bergstrom KS, et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 2010;6(5):e1000902.
38. Hasnain SZ, et al. Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection. Gastroenterology. 2010;138(5):1763-1771.
39. Shirazi T, Longman RJ, Corfield AP, Probert CS. Mucins and inflammatory bowel disease. Postgrad Med J. 2000;76(898):473-478. (Pubitemid 30639056)
40. Prescott NJ, et al. A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn's disease and is independent of CARD15 and IBD5. Gastroenterology. 2007;132(5):1665-1671. (Pubitemid 46677945)
41. McGovern DP, et al. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet. 2010;19(17):3468-3476.
42. Varki A, et al. Essentials of Glycobiology. Cold Spring Harbor, New York, USA: Cold Spring Harbor Press; 2009.
43. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007;117(3):514-521. (Pubitemid 46348505)
44. Garrett WS, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007;131(1):33-45. (Pubitemid 47505255)
45. Martens EC, Chiang HC, Gordon JI. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe. 2008;4(5):447-457.
46. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol. 2002;20:495-549. (Pubitemid 34293433)
47. Williams SA, Xia L, Cummings RD, McEver RP, Stanley P. Fertilization in mouse does not require terminal galactose or N-acetylglucosamine on the zona pellucida glycans. J Cell Sci. 2007;120(pt 8):1341-1349. (Pubitemid 46780027)
48. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124(4):783-801. (Pubitemid 43261452)
49. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229-241. (Pubitemid 38962578)