Mice overexpressing β-1,4-galactosyltransferase i are resistant to TNF-induced inflammation and DSS-induced colitis

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Vanhooren, Valerie ^a,b   Vandenbroucke, Roosmarijn E ^a,b   Dewaele, Sylviane ^a,b   Van Hamme, Evelien ^a,b   Haigh, Jody J ^a,b   Hochepied, Tino ^a,b   Libert, Claude ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,4 GALACTOSYLTRANSFERASE I; GALACTOSYLTRANSFERASE; UNCLASSIFIED DRUG; BETA-1,4-GALACTOSYLTRANSFERASE I; DEXTRAN SULFATE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; COLITIS; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMBRYO; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME ISOLATION; ENZYME LOCALIZATION; FEMALE; FIRMICUTES; IN VIVO STUDY; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; LETHALITY; MALE; MOUSE; NONHUMAN; ORGAN SIZE; PHENOTYPE; PROTEIN EXPRESSION; TRANSGENIC MOUSE; WEIGHT REDUCTION; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; INFLAMMATION; INTESTINE MUCOSA; MICROBIOLOGY; MICROFLORA;

ANIMALS; COLITIS; DEXTRAN SULFATE; DISEASE SUSCEPTIBILITY; FEMALE; GALACTOSYLTRANSFERASES; GENE EXPRESSION; HUMANS; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICE, TRANSGENIC; MICROBIOTA; PHENOTYPE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84891944540     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079883     Document Type: Article

References (71)

1. Fu J, Wei B, Wen T, Johansson ME, Liu X, et al. (2011) Loss of intestinal core 1- derived O-glycans causes spontaneous colitis in mice. The Journal of clinical investigation 121: 1657-1666.
2. McGuckin MA, Linden SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265-278.
3. Thornton DJ, Rousseau K, McGuckin MA (2008) Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol 70: 459-486. (Pubitemid 351738188)
4. Macao B, Johansson DG, Hansson GC, Hard T (2006) Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 13: 71-76. (Pubitemid 43049405)
5. Kotani N, Asano M, Iwakura Y, Takasaki S (2001) Knockout of mouse beta 1,4- galactosyltransferase-1 gene results in a dramatic shift of outer chain moieties of N-glycans from type 2 to type 1 chains in hepatic membrane and plasma glycoproteins. The Biochemical journal 357: 827-834. (Pubitemid 32735163)
6. Hennet T (2002) The galactosyltransferase family. Cell Mol Life Sci 59: 1081-1095.
7. Asano M, Furukawa K, Kido M, Matsumoto S, Umesaki Y, et al. (1997) Growth retardation and early death of beta-1,4-galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells. EMBO J 16: 1850-1857. (Pubitemid 27170946)
8. Asano M, Nakae S, Kotani N, Shirafuji N, Nambu A, et al. (2003) Impaired selectin-ligand biosynthesis and reduced inflammatory responses in beta-1,4- galactosyltransferase-I-deficient mice. Blood 102: 1678-1685. (Pubitemid 37022560)
9. Van Hauwermeiren F, Vandenbroucke RE, Libert C (2011) Treatment of TNF mediated diseases by selective inhibition of soluble TNF or TNFR1. Cytokine Growth Factor Rev 22: 311-319.
10. Xu D, Cui Z, Liu W, Tao R, Tao T, et al. (2011) Tumor necrosis factor-alpha up-regulates the expression of beta1,4-galactosyltransferase-I in human fibroblast- like synoviocytes. Inflammation 34: 531-538.
11. Yan M, Xia C, Niu S, Shao X, Cheng C, et al. (2007) The role of TNF-alpha and its receptors in the production of beta-1,4 galactosyltransferase I and V mRNAs by rat primary astrocytes. J Mol Neurosci 33: 155-162. (Pubitemid 47574938)
12. Yuan Q, Yang H, Cheng C, Li C, Wu X, et al. (2012) beta-1,4- Galactosyltransferase I involved in Schwann cells proliferation and apoptosis induced by tumor necrosis factor-alpha via the activation of MAP kinases signal pathways. Mol Cell Biochem 365: 149-158.
13. Niu S, Fei M, Cheng C, Yan M, Gao S, et al. (2008) Altered beta-1,4- galactosyltransferase I expression during early inflammation after spinal cord contusion injury. J Chem Neuroanat 35: 245-256.
14. Shen A, Chen J, Qian J, Zhu J, Hu L, et al. (2009) Elevated beta1,4- galactosyltransferase-I induced by the intraspinal injection of lipopolysaccharide. Glycoconj J 26: 19-31.
15. Dharmani P, Leung P, Chadee K (2011) Tumor necrosis factor-alpha and Muc2 mucin play major roles in disease onset and progression in dextran sodium sulphate-induced colitis. PLoS One 6: e25058.
16. Elson CO, Cong Y, McCracken VJ, Dimmitt RA, Lorenz RG, et al. (2005) Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev 206: 260-276. (Pubitemid 41105175)
17. Van Hauwermeiren FAM, Karagianni N, Kranidioti K, Vandenbroucke RE, Loges S, et al. (2013) Safe TNF-based antitumor therapy following p55TNFR reduction in intestinal epithelium. J Clin Invest May 15. pii: 65624. doi: 10.1172/JCI65624. [Epub ahead of print]
18. Podolsky DK, Isselbacher KJ (1984) Glycoprotein composition of colonic mucosa. Specific alterations in ulcerative colitis. Gastroenterology 87: 991-998. (Pubitemid 14017063)
19. Rhodes JM (1997) Colonic mucus and ulcerative colitis. Gut 40: 807-808. (Pubitemid 27305480)
20. Heazlewood CK, Cook MC, Eri R, Price GR, Tauro SB, et al. (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med 5: e54.
21. Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, et al. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131: 117-129. (Pubitemid 44015753)
22. An G, Wei B, Xia B, McDaniel JM, Ju T, et al. (2007) Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. The Journal of experimental medicine 204: 1417-1429. (Pubitemid 46919879)
23. Stone EL, Ismail MN, Lee SH, Luu Y, Ramirez K, et al. (2009) Glycosyltransferase function in core 2-type protein O glycosylation. Mol Cell Biol 29: 3770-3782.
24. Shinzaki S, Iijima H, Fujii H, Kuroki E, Tatsunaka N, et al. (2012) Altered Oligosaccharide Structures Reduce Colitis Induction in Mice Defective in beta- 1,4-Galactosyltransferase. Gastroenterology.
25. Nyabi O, Naessens M, Haigh K, Gembarska A, Goossens S, et al. (2009) Efficient mouse transgenesis using Gateway-compatible ROSA26 locus targeting vectors and F1 hybrid ES cells. Nucleic Acids Res 37: e55.
26. Betz UA, Vosshenrich CA, Rajewsky K, Muller W (1996) Bypass of lethality with mosaic mice generated by Cre-loxP-mediated recombination. Curr Biol 6: 1307-1316. (Pubitemid 27004916)
27. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol 1: 183-197. (Pubitemid 351541304)
28. Callewaert N, Geysens S, Molemans F, Contreras R (2001) Ultrasensitive profiling and sequencing of N-linked oligosaccharides using standard DNAsequencing equipment. Glycobiology 11: 275-281. (Pubitemid 32600397)
29. Laroy W, Contreras R, Callewaert N (2006) Glycome mapping on DNA sequencing equipment. Nat Protoc 1: 397-405.
30. Vanhooren V, Dewaele S, Kuro OM, Taniguchi N, Dolle L, et al. (2011) Alteration in N-glycomics during mouse aging: a role for FUT8. Aging Cell 10: 1056-1066.
31. Vanhooren V, Dewaele S, Libert C, Engelborghs S, De Deyn PP, et al. (2010) Serum N-glycan profile shift during human ageing. Exp Gerontol 45: 738-743.
32. Vanhooren V, Laroy W, Libert C, Chen C (2008) N-glycan profiling in the study of human aging. Biogerontology 9: 351-356.
33. Vanhooren V, Liu XE, Franceschi C, Gao CF, Libert C, et al. (2009) N-glycan profiles as tools in diagnosis of hepatocellular carcinoma and prediction of healthy human ageing. Mech Ageing Dev 130: 92-97.
34. Moran AP, Gupta A, Joshi L (2011) Sweet-talk: role of host glycosylation in bacterial pathogenesis of the gastrointestinal tract. Gut 60: 1412-1425.
35. Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, et al. (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15: 1183-1189.
36. Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, et al. (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9: 123.
37. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, et al. (2000) Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1: 113-118.
38. Ayabe T, Satchell DP, Pesendorfer P, Tanabe H, Wilson CL, et al. (2002) Activation of Paneth cell alpha-defensins in mouse small intestine. J Biol Chem 277: 5219-5228. (Pubitemid 34968566)
39. Vandenbroucke RE VI, Van Hauwermeiren F, Van Wonterghem E, Wilson C, Libert C (2013) Pro-inflammatory effects of matrix metalloproteinase 7 in acute inflammation. Mucosal Immunology, In press.
40. Tracey KJ, Beutler B, Lowry SF, Merryweather J, Wolpe S, et al. (1986) Shock and tissue injury induced by recombinant human cachectin. Science 234: 470-474. (Pubitemid 17181429)
41. Ma TY, Boivin MA, Ye D, Pedram A, Said HM (2005) Mechanism of TNF- {alpha} modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am J Physiol Gastrointest Liver Physiol 288: G422-430. (Pubitemid 40261739)
42. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, et al. (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126.
43. Vereecke L, Sze M, Mc Guire C, Rogiers B, Chu Y, et al. (2010) Enterocytespecific A20 deficiency sensitizes to tumor necrosis factor-induced toxicity and experimental colitis. The Journal of experimental medicine 207: 1513-1523.
44. Libert C, Brouckaert P, Shaw A, Fiers W (1990) Induction of interleukin 6 by human and murine recombinant interleukin 1 in mice. Eur J Immunol 20: 691-694. (Pubitemid 20101313)
45. Takahashi N, Vanlaere I, de Rycke R, Cauwels A, Joosten LA, et al. (2008) IL- 17 produced by Paneth cells drives TNF-induced shock. The Journal of experimental medicine 205: 1755-1761.
46. Van Molle W, Wielockx B, Mahieu T, Takada M, Taniguchi T, et al. (2002) HSP70 protects against TNF-induced lethal inflammatory shock. Immunity 16: 685-695. (Pubitemid 34626689)
47. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, et al. (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A 105: 16731-16736.
48. Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, et al. (1994) Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 107: 1643-1652. (Pubitemid 24357616)
49. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, et al. (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98: 694-702. (Pubitemid 20069706)
50. Iwaya H, Maeta K, Hara H, Ishizuka S (2012) Mucosal permeability is an intrinsic factor in susceptibility to dextran sulfate sodium-induced colitis in rats. Exp Biol Med (Maywood).
51. Vandenbroucke RE, Dejonckheere E, Lodens S, Van Hauwermeiren F, De Rycke R, et al. (2013) MMP13 modulates intestinal epithelial barrier integrity in inflammatory diseases. EMBO Mol Med, in press.
52. Kukuruzinska MA, Lennon K (1998) Protein N-glycosylation: molecular genetics and functional significance. Crit Rev Oral Biol Med 9: 415-448. (Pubitemid 29402009)
53. Ohtsubo K, Marth JD (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126: 855-867. (Pubitemid 44310784)
54. Raman R, Raguram S, Venkataraman G, Paulson JC, Sasisekharan R (2005) Glycomics: an integrated systems approach to structure-function relationships of glycans. Nat Methods 2: 817-824. (Pubitemid 41741530)
55. Furukawa K, Sato T (1999) Beta-1,4-galactosylation of N-glycans is a complex process. Biochim Biophys Acta 1473: 54-66.
56. Rini J, Esko J, Varki A (2009) Glycosyltransferases and Glycan-processing Enzymes.
57. Varki A, Lowe JB (2009) Biological Roles of Glycans.
58. Mori R, Kondo T, Nishie T, Ohshima T, Asano M (2004) Impairment of skin wound healing in beta-1,4-galactosyltransferase-deficient mice with reduced leukocyte recruitment. Am J Pathol 164: 1303-1314. (Pubitemid 38387796)
59. Strugala V, Allen A, Dettmar PW, Pearson JP (2003) Colonic mucin: methods of measuring mucus thickness. Proc Nutr Soc 62: 237-243. (Pubitemid 36569835)
60. Rozee KR, Cooper D, Lam K, Costerton JW (1982) Microbial flora of the mouse ileum mucous layer and epithelial surface. Appl Environ Microbiol 43: 1451-1463. (Pubitemid 12061323)
61. Littman DR, Pamer EG (2011) Role of the commensal microbiota in normal and pathogenic host immune responses. Cell Host Microbe 10: 311-323.
62. Sando L, Pearson R, Gray C, Parker P, Hawken R, et al. (2009) Bovine Muc1 is a highly polymorphic gene encoding an extensively glycosylated mucin that binds bacteria. J Dairy Sci 92: 5276-5291.
63. Schroers V, Van Der Marel M, Steinhagen D (2008) Influence of carp intestinal mucus molecular size and glycosylation on bacterial adhesion. Dis Aquat Organ 81: 135-142.
64. Magalhaes A, Gomes J, Ismail MN, Haslam SM, Mendes N, et al. (2009) Fut2- null mice display an altered glycosylation profile and impaired BabA-mediated Helicobacter pylori adhesion to gastric mucosa. Glycobiology 19: 1525-1536.
65. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307: 1955-1959. (Pubitemid 40404703)
66. Keshav S (2006) Paneth cells: leukocyte-like mediators of innate immunity in the intestine. J Leukoc Biol 80: 500-508. (Pubitemid 44835783)
67. Groux-Degroote S, Krzewinski-Recchi MA, Cazet A, Vincent A, Lehoux S, et al. (2008) IL-6 and IL-8 increase the expression of glycosyltransferases and sulfotransferases involved in the biosynthesis of sialylated and/or sulfated Lewisx epitopes in the human bronchial mucosa. The Biochemical journal 410: 213-223. (Pubitemid 351300341)
68. Wu YM, Nowack DD, Omenn GS, Haab BB (2009) Mucin glycosylation is altered by pro-inflammatory signaling in pancreatic-cancer cells. J Proteome Res 8: 1876-1886.
69. Shinzaki S, Iijima H, Nakagawa T, Egawa S, Nakajima S, et al. (2008) IgG oligosaccharide alterations are a novel diagnostic marker for disease activity and the clinical course of inflammatory bowel disease. Am J Gastroenterol 103: 1173-1181. (Pubitemid 351677959)
70. George SH, Gertsenstein M, Vintersten K, Korets-Smith E, Murphy J, et al. (2007) Developmental and adult phenotyping directly from mutant embryonic stem cells. Proc Natl Acad Sci U S A 104: 4455-4460. (Pubitemid 47186247)
71. Van Snick J, Cayphas S, Vink A, Uyttenhove C, Coulie PG, et al. (1986) Purification and NH2-terminal amino acid sequence of a T-cell-derived lymphokine with growth factor activity for B-cell hybridomas. Proc Natl Acad Sci U S A 83: 9679-9683. (Pubitemid 17223420)