Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse

Gut

Volumn 58, Issue 7, 2009, Pages 910-919

  Dawson, P A ^a   Huxley, S ^a   Gardiner, B ^a   Tran, T ^b   McAuley, J L ^b   Grimmond, S ^a   McGuckin, M A ^b   Markovich, D ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MATER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CARBONATE DEHYDRATASE I; DEXTRAN SULFATE; DRINKING WATER; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; MESSENGER RNA; MUCIN; PHTHALYLSULFATHIAZOLE; SIALOMUCIN; SULFOMUCIN; TRIACYLGLYCEROL LIPASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD EXAMINATION; CAMPYLOBACTER JEJUNI; COLITIS; COMPARATIVE STUDY; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; GASTROINTESTINAL TRACT FUNCTION; GENETIC TRANSCRIPTION; HISTOLOGY; HOMEOSTASIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STAINING; SULFONATION; UPREGULATION; WILD TYPE;

EID: 67649654276     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gut.2007.147595     Document Type: Article

References (68)

1. Markovich D. Physiological roles and regulation of mammalian sulfate transporters. Physiol Rev 2001;81:1499-1534 (Pubitemid 32947778)
2. Mulder GJ, Jakoby WB. Sulfation. In: Mulder GJ, ed. Conjugation reactions in drug metabolism: an integrated approach: substrates, co-substrates, enzymes and their interactions in vivo and in vitro. London: Taylor and Francis, 1990:107-161
3. Gendler SJ, Spicer AP. Epithelial mucin genes [review]. Annu Rev Physiol 1995;57:607-634
4. Brockhausen I. Sulphotransferases acting on mucin-type oligosaccharides. Biochem Soc Trans 2003;31:318-325 (Pubitemid 36520666)
5. Hanisch FG. O-Glycosylation of the mucin type. Biol Chem 2001;382:143-149 (Pubitemid 32243924)
6. Dekker J, Rossen JW, Buller HA, et al. The MUC family: an obituary. Trends Biochem Sci 2002;27:126-131 (Pubitemid 34219322)
7. Gum JR Jr, Crawley SC, Hicks JW, et al. MUC17, a novel membrane-tethered mucin. Biochem Biophys Res Commun 2002;291:466-475 (Pubitemid 34687369)
8. Chen Y, Zhao YH, Kalaslavadi TB, et al. Genome-wide search and identification of a novel gel-forming mucin MUC19/Muc19 in glandular tissues. Am J Respir Cell Mol Biol 2003;30:155-165
9. Pallesen LT, Berglund L, Rasmussen LK, et al. Isolation and characterization of MUC15, a novel cell membrane-associated mucin. Eur J Biochem 2002;269:2755-2763 (Pubitemid 34595643)
10. Shirazi T, Longman RJ, Corfield AP, et al. Mucins and inflammatory bowel disease. 2000;76:473-478
11. Buisine MP, Desreumaux P, Leteurtre E, et al. Mucin gene expression in intestinal epithelial cells in Crohn's disease. Gut 2001;49:544-551 (Pubitemid 32896986)
12. Silva F, Carvalho F, Peixoto A, et al. MUC1 polymorphism confers increased risk for intestinal metaplasia in a Colombian population with chronic gastritis. Eur J Hum Genet 2003;11:380-384 (Pubitemid 36656686)
13. Kardon R, Price RE, Julian J, et al. Bacterial conjunctivitis in Muc1 null mice. Invest Ophthalmol Vis Sci 1999;40:1328-1335 (Pubitemid 29252322)
14. McAuley JL, Linden SK, Png CW, et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007;117:2313-2324 (Pubitemid 47219576)
15. McGuckin MA, Every A, Skene CD, et al. Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis. Gastroenterology 2007;133:1210-1218 (Pubitemid 47494449)
16. Van der Sluis M, De Koning BA, De Bruijn AC, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 2006;131:117-129 (Pubitemid 44015753)
17. Velcich A, Yang W, Heyer J, et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 2002;295:1726-1729 (Pubitemid 34202910)
18. 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.
19. An G, Wei B, Xia B, et al. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med 2007;204:1417-1429 (Pubitemid 46919879)
20. Nieuw Amerongen AV, Bolscher JG, Bloemena E, et al. Sulfomucins in the human body. Biol Chem 1998;379:1-18. (Pubitemid 28052389)
21. Einerhand AW, Renes IB, Makkink MK, et al. Role of mucins in inflammatory bowel disease: important lessons from experimental models. Eur J Gastroenterol Hepatol 2002;14:757-765 (Pubitemid 34753960)
22. Yamori T, Kimura H, Stewart K, et al. Differential production of high molecular weight sulfated glycoproteins in normal colonic mucosa, primary colon carcinoma, and metastases. Cancer Res 1987;47:2741-2747 (Pubitemid 17083169)
23. Raouf AH, Tsai HH, Parker N, et al. Sulphation of colonic and rectal mucin in inflammatory bowel disease: reduced sulphation of rectal mucus in ulcerative colitis. Clin Sci 1992;83:623-626
24. Irimura T, Wynn DM, Hager LG, et al. Human colonic sulfomucin identified by a specific monoclonal antibody. Cancer Res 1991;51:5728-5735
25. Klassen CD, Boles J. The importance of 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J 1997;11:404-418 (Pubitemid 27259982)
26. +-sulfate cotransporter gene Nas1: cloning, tissue distribution, gene structure, chromosomal assignment, and transcriptional regulation by vitamin D. J Biol Chem 2000;275:11880-11890
27. Lee A, Beck L, Markovich D. The human renal sodium sulfate cotransporter (SLC13A1; hNaSi-1) cDNA and gene: organisation, chromosomal localization, and functional characterization. Genomics 2000;70:354-363 (Pubitemid 32095434)
28. Dawson PA, Beck L, Markovich D. Hyposulfatemia, growth retardation, reduced fertility, and seizures in mice lacking a functional NaSi-1 gene. Proc Natl Acad Sci USA 2003;100:13704-13709 (Pubitemid 37444803)
29. Colliver DW, Crawford NP, Eichenberger MR, et al. Molecular profiling of ulcerative colitis-associated neoplastic progression. Exp Mol Pathol 2006;80:1-10. (Pubitemid 41828222)
30. Dieckgraefe BK, Crimmins DL, Landt V, et al. Expression of the regenerating gene family in inflammatory bowel disease mucosa: Reg Ialpha upregulation, processing, and antiapoptotic activity. J Investig Med 2002;50:421-434 (Pubitemid 35278683)
31. Rinella ES, Eversley CD, Carroll IM, et al. Human epithelial-specific response to pathogenic Campylobacter jejuni. FEMS Microbiol Lett 2006;262:236-243 (Pubitemid 44272801)
32. Lee S, Dawson PA, Hewavitharana AK, et al. Disruption of NaS1 sulfate transport function in mice leads to enhanced acetaminophen-induced hepatotoxicity. Hepatology 2006;43:1241-1247 (Pubitemid 43980102)
33. Dawson PA, Gardiner B, Grimmond S, et al. Transcriptional profile reveals altered hepatic lipid and cholesterol metabolism in hyposulfatemic NaS1 null mice. Physiol Genomics 2006;26:116-124 (Pubitemid 44061320)
34. Matsuo K, Ota H, Akamatsu T, et al. Histochemistry of the surface mucous gel layer of the human colon. Gut 1997;40:782-789 (Pubitemid 27305472)
35. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990;98:694-702. (Pubitemid 20069706)
36. Cooper HS, Murthy SN, Shah RS, et al. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 1993;69:238-249 (Pubitemid 23262505)
37. Kennedy RJ, Hoper M, Deodhar K, et al. Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease. 2000;87:1346-1351
38. Bartosch S, Fite A, Macfarlane GT, et al. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using realtime PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 2004;70:3575-3581 (Pubitemid 38745906)
39. Nadkarni MA, Martin FE, Jacques NA, et al. Determination of bacterial load by realtime PCR using a broad-range (universal) probe and primers set. Microbiology 2002;148:257-266 (Pubitemid 34083204)
40. Challen GA, Martinez G, Davis MJ, et al. Identifying the molecular phenotype of renal progenitor cells. J Am Soc Nephrol 2004;15:2344-2357 (Pubitemid 39159334)
41. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003;31:265-273 (Pubitemid 37338763)
42. Corfield AP, Myerscough N, Bradfield N, et al. Colonic mucins in ulcerative colitis: evidence for loss of sulfation. Glycoconj J 1996;13:809-822 (Pubitemid 26354274)
43. Smithson JE, Campbell A, Andrews JM, et al. Altered expression of mucins throughout the colon in ulcerative colitis. Gut 1997;40:234-240 (Pubitemid 27093100)
44. Van Klinken BJ, Van Der Wal JW, Einerhand AW, et al. Sulphation and secretion of the predominant secretory human colonic mucin MUC2 in ulcerative colitis. Gut 1999;44:387-393 (Pubitemid 29119336)
45. Chou DK, Schachner M, Jungalwala FB. HNK-1 sulfotransferase null mice express glucuronyl glycoconjugates and show normal cerebellar granule neuron migration in vivo and in vitro. J Neurochem 2002;82:1239-1251 (Pubitemid 34966636)
46. Honke K, Taniguchi N. Sulfotransferases and sulfated oligosaccharides. Med Res Rev 2002;22:637-654 (Pubitemid 35299536)
47. Senn C, Kutsche M, Saghatelyan A, et al. Mice deficient for the HNK-1 sulfotransferase show alterations in synaptic efficacy and spatial learning and memory. Mol Cell Neurosci 2002;20:712-729
48. Shworak NW, HajMohammadi S, de Agostini AI, et al. Mice deficient in heparan sulfate 3-O-sulfotransferase-1: normal hemostasis with unexpected perinatal phenotypes. Glycoconj J 2002;19:355-361 (Pubitemid 37174566)
49. Uchimura K, Kadomatsu K, Nishimura H, et al. Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development, and oversulfated chondroitin sulfates. J Biol Chem 2002;277:1443-1450 (Pubitemid 34968899)
50. Linden SK, Sutton P, Karlsson NG, et al. Mucins in the mucosal barrier to infection. Mucosal Immunol 2008;1:183-197 (Pubitemid 351541304)
51. McGuckin MA, Eri R, Simms LA, et al. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 2008.
52. Mahler M, Bristol IJ, Leiter EH, et al. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. 1998;274:G544-51.
53. Linden SK, Wickstrom C, Lindell G, et al. Four modes of adhesion are used during Helicobacter pylori binding to human mucins in the oral and gastric niches. Helicobacter 2008;13:81-93. (Pubitemid 351347660)
54. Corfield AP, Wagner SA, Clamp JR, et al. Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria. Infect Immun 1992;60:3971-3978
55. Roberton AM, Wright DP. Bacterial glycosulphatases and sulphomucin degradation. Can J Gastroenterol 1997;11:361-366 (Pubitemid 27263197)
56. Homer KA, Whiley RA, Beighton D. Production of specific glycosidase activities by Streptococcus intermedius strain UNS35 grown in the presence of mucin. J Med Microbiol 1994;41:184-190 (Pubitemid 24274270)
57. Corfield AP, Wagner SA, O'Donnell LJ, et al. The roles of enteric bacterial sialidase, sialate O-acetyl esterase and glycosulfatase in the degradation of human colonic mucin. Glycoconj J 1993;10:72-81. (Pubitemid 23168574)
58. Haider K, Hossain A, Wanke C, et al. Production of mucinase and neuraminidase and binding of Shigella to intestinal mucin. J Diarrhoeal Dis Res 1993;11:88-92.
59. Slomiany BL, Murty VL, Piotrowski J, et al. Glycosulfatase activity of Helicobacter pylori toward gastric mucin. Biochem Biophys Res Commun 1992;183:506-513
60. Slomiany BL, Murty VL, Piotrowski J, et al. Glycosulfatase activity of Helicobacter pylori towards gastric sulfomucin: effect of nitecapone. J Physiol Pharmacol 1993;44:7-16. (Pubitemid 23132654)
61. Lee JK, Bhakta S, Rosen SD, et al. Cloning and characterization of a mammalian N-acetylglucosamine-6-sulfotransferase that is highly restricted to intestinal tissue. Biochem Biophys Res Commun 1999;263:543-549 (Pubitemid 29467231)
62. Pastorekova S, Parkkila S, Pastorek J, et al. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J Enzyme Inhib Med Chem 2004;19:199-229. (Pubitemid 39004275)
63. Endeward V, Kleinke T, Gros G. Carbonic anhydrase in the gastrointestinal mucus of mammals - possible protective role against carbon dioxide. Comp Biochem Physiol A Mol Integr Physiol 2003;136:281-287 (Pubitemid 37153368)
64. Simonsson I, Lindskog S. The interaction of sulfate with carbonic anhydrase. Eur J Biochem 1982;123:29-36.
65. Caprilli R, Frieri G, Latella G, et al. Faecal excretion of bicarbonate in ulcerative colitis. Digestion 1986;35:136-142 (Pubitemid 16001673)
66. Pan PW, Rodriguez A, Parkkila S. A systematic quantification of carbonic anhydrase transcripts in the mouse digestive system. BMC Mol Biol 2007;8:22. (Pubitemid 46511049)
67. D'Agostino D, Lowe ME. Pancreatic lipase-related protein 2 is the major colipase-dependent pancreatic lipase in suckling mice. J Nutr 2004;134:132-134 (Pubitemid 38057435)
68. Heimerl S, Moehle C, Zahn A, et al. Alterations in intestinal fatty acid metabolism in inflammatory bowel disease. Biochim Biophys Acta 2006;1762:341-350 (Pubitemid 43172850)