Interleukin 10-deficient mice exhibit defective colonic Muc2 synthesis before and after induction of colitis by commensal bacteria

Inflammatory Bowel Diseases

Volumn 10, Issue 6, 2004, Pages 811-823

  Schwerbrock, Nicole M J ^a,b   Makkink, Mireille K ^a   van der Sluis, Maria ^a   Büller, Hans A ^a   Einerhand, Alexandra W C ^a   Sartor, R Balfour ^b   Dekker, Jan ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Colitis; Enteric bacteria; Germ free animals; Goblet cells; Interleukin 10; Muc2; Sulfation

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 12; MESSENGER RNA; MUCIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; CHRONIC DISEASE; COLITIS; COLON MUCOSA; COMMENSALISM; CONTROLLED STUDY; CYTOKINE RELEASE; HISTOPATHOLOGY; INFECTION SENSITIVITY; INTESTINE FLORA; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SCORING SYSTEM; SULFATION; WILD TYPE;

ANIMALS; BACTERIA; BLOTTING, NORTHERN; COLITIS, ULCERATIVE; INTERLEUKIN-10; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MUCINS; RNA, MESSENGER; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 9144231385     PISSN: 10780998     EISSN: None     Source Type: Journal    
DOI: 10.1097/00054725-200411000-00016     Document Type: Article

References (59)

1. Strous GJ, Dekker J. Mucin-type glycoproteins. Crit Rev Biochem Mol Biol. 1992;27:57-92.
2. Van Klinken BJW, Dekker J, Büller HA, et al. Mucin gene structure and expression: protection versus adhesion [review]. Am J Physiol. 1995;269: G613-G627.
3. Sartor RB. Microbial influences in inflammatory bowel disease. In: Sartor RB, Sandborn WJ, eds. Kirsner's Inflammatory Bowel Diseases. 6th ed. Amsterdam: Elsevier Publishers; 2004:138-162.
4. Berg DJ, Zhang J, Weinstock JV, et al. Rapid development of colitis in NSAID-treated IL-10-deficient mice. Gastroenterology. 2002;123:1527-1542.
5. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003;3:521-533.
6. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347: 417-429.
7. Campieri M, Gionchetti P. Bacteria as the cause of ulcerative colitis. Gut. 2001;48:132-135.
8. Sartor RB. Postoperative recurrence of Crohn's disease: the enemy is within the fecal stream. Gastroenterology. 1998;114:398-400.
9. Sartor RB. Animal models of intestinal inflammation. In: Sartor RB, Sandborn WJ, eds. Kirsner's Inflammatory Bowel Diseases. 6th ed. Amsterdam: Elsevier Publishers; 2004:120-137.
10. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol. 2002;20:495-549.
11. Tytgat KMAJ, Opdam FJM, Einerhand AWC, et al. MUC2 is the prominent colonic mucin expressed in ulcerative colitis. Gut. 1996;38:554-563.
12. Tytgat KMAJ, Van der Wal JWG, Büller HA, et al. Quantitative analysis of MUC2 synthesis in ulcerative colitis. Biochem Biophys Res Commun. 1996;224:397-405.
13. Van Klinken BJW, Van der Wal JWG, Einerhand AWC, et al. Sulfation and secretion of the predominant secretory human colonic mucin MUC2 in ulcerative colitis. Gut. 1999;44:387-393.
14. Buisine MP, Desreumaux P, Leteurtre E, et al. Mucin gene expression in intestinal epithelial cells in Crohn's disease. Gut. 2001;49:544-551.
15. Pullan RD, Thomas GAO, Rhodes M, et al. Thickness of adherent mucus gel on colonic mucosa in humans and its relevance to colitis. Gut. 1994; 35:353-359.
16. Schultz C, Van den Berg FM, Ten Kate FW, et al. The intestinal mucus layer from patients with inflammatory bowel disease harbours high numbers of bacteria compared with controls. Gastroenterology. 1999;117: 1089-1097.
17. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology. 2002;122:44-54.
18. Mähler M, Rozell B, Mahler JF, et al. Pathology of the gastrointestinal tract of genetically engineered and spontaneous mutant mice. In: Ward JM, Mahler JF, Maronpot RR, Sundberg JP, eds. Pathology of Genetically Engineered Mice. Ames, IA:, Iowa State University Press; 2000:267-295.
19. Berg DJ, Davidson N, Kühn R, et al. Enterocolitis and colon cancer in Interleukin-10-deficient mice are associated with aberrant cytokine production and CD4-TH1-like responses. J Clin Invest. 1996;98:1010-1020.
20. Kühn R, Löhler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263-274.
21. Sellon RK, Tonkonogy SL, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66:5224-5231.
22. Dianda L, Hanby AM, Wright NA, et al. T cell receptor-alpha beta-deficient mice fail to develop colitis in the absence of a microbial environment. Am J Pathol. 1997;150:91-97.
23. Schultz M, Tonkonogy SL, Sellon RK, et al. IL-2-deficient mice raised under germ free conditions develop delayed mild focal intestinal inflammation. Am J Physiol. 1999;276:G1461-G1472.
24. Taurog JD, Richardson JA, Croft JT, et al. The germ free state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med. 1994;180:2359-2364.
25. Veltkamp C, Tonkonogy SL, De Jong YP, et al. Continuous stimulation by normal luminal bacteria is essential for the development and perpetuation of colitis in Tg(epsilon26) mice. Gastroenterology 2001;120:900-913.
26. Makkink MK, Schwerbrock NMJ, Mahler M, et al. Fate of goblet cells in experimental colitis. Dig Dis Sci. 2002;47:2286-2297.
27. Van Klinken BJW, Einerhand AWC, Duits LA, et al. Gastrointestinal expression and partial cDNA cloning of murine Muc2. Am J Physiol. 1999; 276:G115-G124.
28. Tytgat KMAJ, Bovelander FJ, Opdam FJM, et al. Biosynthesis of rat Muc2 in colon and its analogy with human MUC2. Biochem J. 1995;309: 221-229.
29. Tytgat KMAJ, Büller HA, Opdam FJM, et al. Biosynthesis of human colonic mucin: MUC2 is the most prominent secretory mucin. Gastroenterology. 1994;107:1352-1363.
30. Dekker J, Van Klinken BJW, Büller HA, et al. Quantitation of biosynthesis and of mucin secretion using metabolic labeling. Methods Mol Biol. 2000;125:65-73.
31. Herrmann A, Davies JR, Lindell G, et al. Studies on the "insoluble" glycoprotein complex from human colon. Identification of reduction-insensitive MUC2 oligomers and C-terminal cleavage. J Biol Chem. 1999;274:15828-15836.
32. Karlsson NG, Herrmann A, Karlsson H, et al. The glycosylation of rat intestinal Muc2 mucin varies between rat strains and the small and large intestine. A study of O-linked oligosaccharides by a mass spectrometric approach. J Biol Chem. 1997;272:27025-27034.
33. Madsen KL, Doyle JS, Jewell LD, et al. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology. 1999;116: 1107-1114.
34. Madsen KL, Malfair D, Gray D, et al. Interleukin-10 gene-deficient mice develop a primary intestinal permeability defect in response to enteric microflora. Inflamm Bowel Dis. 1999;5:262-270.
35. Dabbagh K, Takeyama K, Lee HM, et al. IL-4 induces mucin gene expression and goblet cell metaplasia in vitro and in vivo. J Immunol. 1999; 162:6233-6237.
36. Enss ML, Cornberg M, Wagner S, et al. Proinflammatory cytokines trigger MUC gene expression and mucin release in the intestinal cancer cell line LS180. Inflamm Res. 2000;49:162-169.
37. Jono H, Shuto T, Xu H, et al. Transforming growth factor-beta-Smad signaling pathway cooperates with NF-kappaB to mediate nontypeable aemophilus influenzae-induced MUC2 mucin transcription. J Biol Chem. 2002;277:45547-45557.
38. Kim YD, Kwon EJ, Park DW, et al. Interleukin-1 beta induces MUC2 and MUC5AC synthesis through cyclooxygenase-2 in NCI-H292 cells. Mol Pharmacol. 2002;62:1112-1118.
39. Koo JS, Kim YD, Jetten AM, et al. Overexpression of mucin genes induced by interleukin-1 beta, tumor necrosis factor-alpha, lipopolysaccharide, and neutrophil elastase is inhibited by a retinoic acid receptor alpha antagonist. Exp Lung Res. 2002;28:315-332.
40. Perrais M, Pigny P, Copin MC, et al. Induction of MUC2 and MUC5AC mucins by factors of the epidermal growth factor (EGF) family is mediated by EGF receptor/Ras/Raf/extracellular signal-regulated kinase cascade and Sp1. J Biol Chem. 2002;277:32258-32267.
41. Lee CG, Homer RJ, Cohn L, et al. Transgenic overexpression of interleukin (IL)-10 in the lung causes mucus metaplasia, tissue inflammation, and airway remodeling via IL-13-dependent and -independent pathways. J Biol Chem. 2002;277:35466-35474.
42. Fuss IJ, Boirivant M, Lacy B, et al. The interrelated roles of TGF-beta and IL-10 in the regulation of experimental colitis. J Immunol. 2002;168:900-908.
43. Mack DR, Ahrne S, Hyde L, et al. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut. 2003;52:827-833.
44. Mattar AF, Teitelbaum DH, Drongowski RA, et al. Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int. 2002;18:586-590.
45. Corfield AP, Myerscough N, Bradfield N, et al. Colonic mucins in ulcerative colitis: evidence for loss of sulfation. Glycoconj J. 1996;13:809-822.
46. Nieuw Amerongen AV, Bolscher JG, Bloemena E, et al. Sulfomucins in the human body. Biol Chem. 1998;379:1-18.
47. Robertson AM, Wright DP. Bacterial glycosulfatases and sulfomucin degradation. Can J Gastroenterol. 1997;11:361-366.
48. Tsai HH, Dwarakanath AD, Hart CA, et al. Increased faccal mucin sulphatase activity in ulcerative colitis: a potential target for treatment. Gut. 1995;36:570-576.
49. Sellers LA, Allen A, Morris ER, et al. Mucus glycoprotein gels. Role of glycoprotein polymeric structure and carbohydrate side-chains in gel-formation. Carbohydr Res. 1988;178:93-110.
50. Mack DR, Michail S, Wei S, et al. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol. 1999;276:G941-G950.
51. Larson MA, Wei SH, Weber A, et al. Human serum amyloid A3 peptide enhances intestinal MUC3 expression and inhibits EPEC adherence. Biochem Biophys Res Commun. 2003;300:531-540.
52. Ruseler-van Embden JG, Van der Helm R, Van Lieshout LM. Degradation of intestinal glycoproteins by Bacteroides vulgatus. FEMS Microbiol Lett. 1989;49:37-41.
53. Gibson GR, Cummings JH, Macfarlane GT. Growth and activities of sulphate-reducing bacteria in gut contents of healthy subjects and patients with ulcerative colitis. FEMS Microbiol Ecol. 1991;86:103-111.
54. Levine J, Ellis CJ, Furne JK, et al. Fecal hydrogen sulfide production in ulcerative colitis. Am J Gastroenterol. 1998;93:83-87.
55. Magee EA, Richardson CJ, Hughes R, et al. Contribution of dietary protein to sulfide production in the large intestine: an in vitro and a controlled feeding study in humans. Am J Clin Nutr. 2000;72:1488-1494.
56. Zinkevich VV, Beech IB. Screening of sulfate-reducing bacteria in colonoscopy samples from healthy and colitic human gut mucosa. FEMS Microbiol Ecol. 2000;34:147-155.
57. Velcich A, Yang W, Heyer J, et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science. 2002;295:1726-1729.
58. Einerhand AWC, Renes IB, Makkink MK, et al. Role of mucins in inflammatory bowel disease: Important lessons from experimental models. Eur J Gastroenterol Hepathol. 2002;14:757-765.
59. Van der Sluis M, Makkink MK, Sutmuller M, et al. MUC2 mucin knockout mice are more susceptible to dextran sodium sulfate-induced colitis [abstract]. Gastroenterology. 2002;122:T946.