1,25-Dihydroxyvitamin D protects intestinal epithelial barrier by regulating the myosin light chain kinase signaling pathway

Inflammatory Bowel Diseases

Volumn 21, Issue 11, 2015, Pages 2495-2506

  Du, Jie ^a   Chen, Yunzi ^a   Shi, Yongyan ^a,b   Liu, Tianjing ^a,b   Cao, Yong ^a   Tang, Yue ^a   Ge, Xin ^a   Nie, Hongguang ^a   Zheng, Changqing ^a   Li, Yan Chun ^a,b  

^a CHINA MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

colitis; inflammatory bowel diseases; intestinal epithelial barrier; myosin light chain kinase; tight junction; Vitamin D

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYOSIN II; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; PARICALCITOL; PEROXIDASE; SYNAPTOTAGMIN I; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA; 1,25-DIHYDROXYVITAMIN D; CALCITRIOL RECEPTOR; TUMOR NECROSIS FACTOR; VITAMIN D;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CACO 2 CELL LINE; CHROMATIN IMMUNOPRECIPITATION; COLON BIOPSY; COLON MUCOSA; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; EPITHELIUM CELL; GENE; HCT116 CELL LINE; HUMAN; HUMAN TISSUE; INTESTINE MUCOSA PERMEABILITY; MLCK GENE; MOLECULAR MECHANICS; MONOLAYER CULTURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ULCERATIVE COLITIS; UPREGULATION; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CACO-2 CELL LINE; CHEMICALLY INDUCED; COLITIS; COLON; DRUG EFFECTS; HCT 116 CELL LINE; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; PERMEABILITY; PHOSPHORYLATION; TUMOR CELL CULTURE;

ANIMALS; CACO-2 CELLS; COLITIS; COLON; EPITHELIAL CELLS; HCT116 CELLS; HUMANS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MYOSIN-LIGHT-CHAIN KINASE; NF-KAPPA B; PERMEABILITY; PHOSPHORYLATION; RECEPTORS, CALCITRIOL; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA; VITAMIN D;

EID: 84945280216     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000526     Document Type: Article

References (57)

1. Laukoetter MG, Bruewer M, Nusrat A. Regulation of the intestinal epithelial barrier by the apical junctional complex. Curr Opin Gastroenterol. 2006;22:85-89.
2. Gibson PR. Increased gut permeability in Crohn's disease: is TNF the link? Gut. 2004;53:1724-1725.
3. Fasano A, Shea-Donohue T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol. 2005;2:416-422.
4. Su L, Nalle SC, Shen L, et al. TNFR2 activates MLCK-dependent tight junction dysregulation to cause apoptosis-mediated barrier loss and experimental colitis. Gastroenterology. 2013;145:407-415.
5. Cunningham KE, Turner JR. Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann N Y Acad Sci. 2012; 1258:34-42.
6. Kamm KE, Stull JT. Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem. 2001;276:4527-4530.
7. Clayburgh DR, Rosen S, Witkowski ED, et al. A differentiationdependent splice variant of myosin light chain kinase, MLCK1, regulates epithelial tight junction permeability. J Biol Chem. 2004;279: 55506-55513.
8. Shen L, Black ED, Witkowski ED, et al. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci. 2006;119:2095-2106.
9. Rutgeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353: 2462-2476.
10. Colombel JF, Sandborn WJ, Rutgeerts P, et al. Adalimumab for maintenance of clinical response and remission in patients with Crohn's disease: the CHARM trial. Gastroenterology. 2007;132:52-65.
11. Taylor CT, Dzus AL, Colgan SP. Autocrine regulation of epithelial permeability by hypoxia: role for polarized release of tumor necrosis factor alpha. Gastroenterology. 1998;114:657-668.
12. Wang F, Graham WV, Wang Y, et al. Interferon-gamma and tumor necrosis factor-Alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol. 2005;166:409-419.
13. Ma TY, Iwamoto GK, Hoa NT, et al. TNF-Alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol. 2004;286:G367-G376.
14. He F, Peng J, Deng XL, et al. Mechanisms of tumor necrosis factor-Alphainduced leaks in intestine epithelial barrier. Cytokine. 2012;59:264-272.
15. Graham WV, Wang F, Clayburgh DR, et al. Tumor necrosis factorinduced long myosin light chain kinase transcription is regulated by differentiation-dependent signaling events. Characterization of the human long myosin light chain kinase promoter. J Biol Chem. 2006;281: 26205-26215.
16. Ye D, Ma I, Ma TY. Molecular mechanism of tumor necrosis factor-Alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol. 2006;290:G496-G504.
17. Bouillon R, Carmeliet G, Verlinden L, et al. Vitamin D and human health: lessons from vitamin D receptor null mice. Endocr Rev. 2008;29: 726-776.
18. Haussler MR, Whitfield GK, Haussler CA, et al. The nuclear vitamin D receptor: biological and molecular regulatory properties revealed. J Bone Miner Res. 1998;13:325-349.
19. Lim WC, Hanauer SB, Li YC. Mechanisms of disease: vitamin D and inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol. 2005; 2:308-315.
20. Driscoll RH Jr, Meredith SC, Sitrin M, et al. Vitamin D deficiency and bone disease in patients with Crohn's disease. Gastroenterology. 1982;83: 1252-1258.
21. Harries AD, Brown R, Heatley RV, et al. Vitamin D status in Crohn's disease: association with nutrition and disease activity. Gut. 1985;26: 1197-1203.
22. Vogelsang H, Ferenci P, Woloszczuk W, et al. Bone disease in vitamin Ddeficient patients with Crohn's disease. Dig Dis Sci. 1989;34:1094-1099.
23. Pappa HM, Gordon CM, Saslowsky TM, et al. Vitamin D status in children and young adults with inflammatory bowel disease. Pediatrics. 2006; 118:1950-1961.
24. Ananthakrishnan AN, Khalili H, Higuchi LM, et al. Higher predicted vitamin D status is associated with reduced risk of Crohn's disease. Gastroenterology. 2012;142:482-489.
25. Liu W, Chen Y, Golan MA, et al. Intestinal epithelial vitamin D receptor signaling inhibits experimental colitis. J Clin Invest. 2013;123: 3983-3996.
26. Chen Y, Du J, Zhang Z, et al. MicroRNA-346 mediates tumor necrosis factor alpha-induced downregulation of gut epithelial vitamin D receptor in inflammatory bowel diseases. Inflamm Bowel Dis. 2014;20:1910-1918.
27. Kong J, Zhang Z, Musch MW, et al. Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier. Am J Physiol Gastrointest Liver Physiol. 2008;294:G208-G216.
28. Assa A, Vong L, Pinnell LJ, et al. Vitamin D deficiency promotes epithelial barrier dysfunction and intestinal inflammation. J Infect Dis. 2014; 210:1296-1305.
29. Chen SW, Wang PY, Zhu J, et al. Protective effect of 1,25-dihydroxyvitamin d3 on lipopolysaccharide-induced intestinal epithelial tight junction injury in caco-2 cell monolayers. Inflammation. 2015;38:375-383.
30. Wirtz S, Neufert C, Weigmann B, et al. Chemically induced mouse models of intestinal inflammation. Nat Protoc. 2007;2:541-546.
31. Chen S, Law CS, Grigsby CL, et al. Cardiomyocyte-specific deletion of the vitamin D receptor gene results in cardiac hypertrophy. Circulation. 2011;124:1838-1847.
32. Hinoi T, Akyol A, Theisen BK, et al. Mouse model of colonic adenomacarcinoma progression based on somatic Apc inactivation. Cancer Res. 2007;67:9721-9730.
33. Cheadle GA, Costantini TW, Lopez N, et al. Enteric glia cells attenuate cytomix-induced intestinal epithelial barrier breakdown. PLoS One. 2013; 8:e69042.
34. Cani PD, Possemiers S, Van de Wiele T, et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009;58:1091-1103.
35. Yan F, Cao H, Cover TL, et al. Colon-specific delivery of a probioticderived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J Clin Invest. 2011;121:2242-2253.
36. Park CM, Reid PE, Walker DC, et al. A simple, practical 'Swiss roll'method of preparing tissues for paraffin or methacrylate embedding. J Microsc. 1987;145(Pt 1):115-120.
37. Appleyard CB, Wallace JL. Reactivation of hapten-induced colitis and its prevention by anti-inflammatory drugs. Am J Physiol. 1995;269: G119-G125.
38. Hyland NP, Chambers AP, Keenan CM, et al. Differential adipokine response in genetically predisposed lean and obese rats during inflammation: a role in modulating experimental colitis? Am J Physiol Gastrointest Liver Physiol. 2009;297:G869-G877.
39. Li YC, Bolt MJG, Cao L-P, et al. Effects of vitamin D receptor inactivation on the expression of calbindins and calcium metabolism. Am J Physiol Endocrinol Metab. 2001;281:E558-E564.
40. Yuan W, Pan W, Kong J, et al. 1,25-dihydroxyvitamin d3 suppresses renin gene transcription by blocking the activity of the cyclic AMP response element in the renin gene promoter. J Biol Chem. 2007;282: 29821-29830.
41. Prasad S, Mingrino R, Kaukinen K, et al. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Invest. 2005;85:1139-1162.
42. Weber CR, Nalle SC, Tretiakova M, et al. Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest. 2008;88:1110-1120.
43. Weber CR, Raleigh DR, Su L, et al. Epithelial myosin light chain kinase activation induces mucosal interleukin-13 expression to alter tight junction ion selectivity. J Biol Chem. 2010;285:12037-12046.
44. Neurath MF, Fuss I, Kelsall BL, et al. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J Exp Med. 1995;182:1281-1290.
45. te Velde AA, Verstege MI, Hommes DW. Critical appraisal of the current practice in murine TNBS-induced colitis. Inflamm Bowel Dis. 2006;12: 995-999.
46. Al-Sadi R, Guo S, Ye D, et al. TNF-Alpha modulation of intestinal epithelial tight junction barrier is regulated by ERK1/2 activation of Elk-1. Am J Pathol. 2013;183:1871-1884.
47. Assa A, Vong L, Pinnell LJ, et al. Vitamin D deficiency predisposes to adherent-invasive Escherichia coli-induced barrier dysfunction and experimental colonic injury. Inflamm Bowel Dis. 2015;21:297-306.
48. Zhang Z, Yuan W, Sun L, et al. 1,25-Dihydroxyvitamin D(3) targeting of NF-kappaB suppresses high glucose-induced MCP-1 expression in mesangial cells. Kidney Int. 2007;72:193-201.
49. Chen Y, Kong J, Sun T, et al. 1,25-Dihydroxyvitamin D(3) suppresses inflammation-induced expression of plasminogen activator inhibitor-1 by blocking nuclear factor-kappaB activation. Arch Biochem Biophys. 2011; 507:241-247.
50. Chen Y, Liu W, Sun T, et al. 1,25-Dihydroxyvitamin D promotes negative feedback regulation of TLR signaling via targeting microRNA-155-SOCS1 in macrophages. J Immunol. 2013;190:3687-3695.
51. Chen Y, Zhang J, Ge X, et al. Vitamin D receptor inhibits nuclear factor kappaB activation by interacting with IkappaB kinase beta protein. J Biol Chem. 2013;288:19450-19458.
52. Qiu W, Wu B, Wang X, et al. PUMA-mediated intestinal epithelial apoptosis contributes to ulcerative colitis in humans and mice. J Clin Invest. 2011;121:1722-1732.
53. Wang P, Qiu W, Dudgeon C, et al. PUMA is directly activated by NFkappaB and contributes to TNF-Alpha-induced apoptosis. Cell Death Differ. 2009;16:1192-1202.
54. Yamamoto-Furusho JK, Mendivil-Rangel EJ, Fonseca-Camarillo G. Differential expression of occludin in patients with ulcerative colitis and healthy controls. Inflamm Bowel Dis. 2012;18:E1999.
55. Benchimol EI, Ward LM, Gallagher JC, et al. Effect of calcium and vitamin D supplementation on bone mineral density in children with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2007;45: 538-545.
56. Miheller P, Muzes G, Hritz I, et al. Comparison of the effects of 1,25 dihydroxyvitamin D and 25 hydroxyvitamin D on bone pathology and disease activity in Crohn's disease patients. Inflamm Bowel Dis. 2009;15: 1656-1662.
57. Jorgensen SP, Agnholt J, Glerup H, et al. Clinical trial: vitamin D3 treatment in Crohn's disease-A randomized double-blind placebo-controlled study. Aliment Pharmacol Ther. 2010;32:377-383.