Rebeccamycin attenuates TNF-α-induced intestinal epithelial barrier dysfunction by inhibiting myosin light chain kinase production

Cellular Physiology and Biochemistry

Volumn 41, Issue 5, 2017, Pages 1924-1934

  Watari, Akihiro ^a   Sakamoto, Yuta ^a   Hisaie, Kota ^a   Iwamoto, Kazuki ^a   Fueta, Miho ^a   Yagi, Kiyohito ^a   Kondoh, Masuo ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Checkpoint kinase 1; Epithelial barrier; Intestinal cells; Myosin light chain kinase; Tight junction; TNF

Indexed keywords

9,12 EPOXY 9,10,11,12 TETRAHYDRO 1H DIINDOLO[1,2,3 FG:3',2',1' KL]PYRROLO[3,4 I][1,6]BENZODIAZOCINE 1,3(2H) DIONE; CHECKPOINT KINASE 1; CLAUDIN 5; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; OCCLUDIN; PROTEIN ZO1; REBECCAMYCIN; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR; CARBAZOLE DERIVATIVE; CHEK1 PROTEIN, HUMAN; CLDN5 PROTEIN, HUMAN;

ARTICLE; CACO-2 CELL LINE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TIGHT JUNCTION; TRANSEPITHELIAL RESISTANCE; UPREGULATION; BIOSYNTHESIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; INTESTINE MUCOSA; METABOLISM; PHOSPHORYLATION;

CACO-2 CELLS; CARBAZOLES; CHECKPOINT KINASE 1; CLAUDIN-5; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTESTINAL MUCOSA; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; PHOSPHORYLATION; TIGHT JUNCTIONS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85018486755     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000472367     Document Type: Article

References (48)

1. Turner JR: Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009;9:799-809.
2. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J: Restoration of barrier function in injured intestinal mucosa. Physiol Rev 2007;87:545-564.
3. Groschwitz KR, Hogan SP: Intestinal barrier function: Molecular regulation and disease pathogenesis. J Allergy Clin Immunol 2009;124:3-20; quiz 21-22.
4. Ferraris RP, Diamond J: Regulation of intestinal sugar transport. Physiol Rev 1997;77:257-302.
5. Kunzelmann K, Mall M: Electrolyte transport in the mammalian colon: Mechanisms and implications for disease. Physiol Rev 2002;82:245-289.
6. Broer S: Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 2008;88:249-286.
7. Odenwald MA, Turner JR: Intestinal permeability defects: Is it time to treat?. Clin Gastroenterol Hepatol 2013;11:1075-1083.
8. Farquhar MG, Palade GE: Junctional complexes in various epithelia. J Cell Biol 1963;17:375-412.
9. Tsukita S, Furuse M, Itoh M: Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001;2:285-293.
10. Van Itallie CM, Anderson JM: Claudins and epithelial paracellular transport. Annu Rev Physiol 2006;68:403-429.
11. Hering NA, Fromm M, Schulzke JD: Determinants of colonic barrier function in inflammatory bowel disease and potential therapeutics. J Physiol 2012;590:1035-1044.
12. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, Turner JR: 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. Al-Sadi R, Ye D, Dokladny K, Ma TY: Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 2008;180:5653-5661.
14. Suzuki T, Yoshinaga N, Tanabe S: Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 2011;286:31263-31271.
15. Weber CR, Raleigh DR, Su L, Shen L, Sullivan EA, Wang Y, Turner JR: Epithelial myosin light chain kinase activation induces mucosal interleukin-13 expression to alter tight junction ion selectivity. J Biol Chem 2010;285:12037-12046.
16. Sandborn WJ, Targan SR: Biologic therapy of inflammatory bowel disease. Gastroenterology 2002;122:1592-1608.
17. Braegger CP, Nicholls S, Murch SH, Stephens S, MacDonald TT: Tumour necrosis factor alpha in stool as a marker of intestinal inflammation. Lancet 1992;339:89-91.
18. Murch SH, Braegger CP, Walker-Smith JA, MacDonald TT: Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease. Gut 1993;34:1705-1709.
19. van Deventer SJ: Anti-TNF antibody treatment of Crohn's disease. Ann Rheum Dis 1999;58:I114-120.
20. Ricart E, Panaccione R, Loftus EV, Tremaine WJ, Sandborn WJ: Infliximab for Crohn's disease in clinical practice at the Mayo Clinic: The first 100 patients. Am J Gastroenterol 2001;96:722-729.
21. Neurath MF, Fuss I, Pasparakis M, Alexopoulou L, Haralambous S, Meyer zum Buschenfelde KH, Strober W, Kollias G: Predominant pathogenic role of tumor necrosis factor in experimental colitis in mice. Eur J Immunol 1997;27:1743-1750.
22. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM: TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 2004;286:G367-376.
23. Rodriguez P, Heyman M, Candalh C, Blaton MA, Bouchaud C: Tumour necrosis factor-alpha induces morphological and functional alterations of intestinal HT29 cl.19A cell monolayers. Cytokine 1995;7:441-448.
24. 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.
25. Ma TY, Boivin MA, Ye D, Pedram A, Said HM: 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 2005;288:G422-430.
26. Zolotarevsky Y, Hecht G, Koutsouris A, Gonzalez DE, Quan C, Tom J, Mrsny RJ, Turner JR: A membrane-permeant peptide that inhibits MLC kinase restores barrier function in in vitro models of intestinal disease. Gastroenterology 2002;123:163-172.
27. Amasheh M, Fromm A, Krug SM, Amasheh S, Andres S, Zeitz M, Fromm M, Schulzke JD: TNFalpha-induced and berberine-antagonized tight junction barrier impairment via tyrosine kinase, Akt and NFkappaB signaling. J Cell Sci 2010;123:4145-4155.
28. Facompre M, Baldeyrou B, Bailly C, Anizon F, Marminon C, Prudhomme M, Colson P, Houssier C: DNA targeting of two new antitumour rebeccamycin derivatives. Eur J Med Chem 2002;37:925-932.
29. Watari A, Hasegawa M, Yagi K, Kondoh M: Checkpoint Kinase 1 Activation Enhances Intestinal Epithelial Barrier Function via Regulation of Claudin-5 Expression. PLoS One 2016;11:e0145631.
30. Cao M, Wang P, Sun C, He W, Wang F: Amelioration of IFN-gamma and TNF-alpha-induced intestinal epithelial barrier dysfunction by berberine via suppression of MLCK-MLC phosphorylation signaling pathway. PLoS One 2013;8:e61944.
31. Chen SW, Zhu J, Zuo S, Zhang JL, Chen ZY, Chen GW, Wang X, Pan YS, Liu YC, Wang PY: Protective effect of hydrogen sulfide on TNF-alpha and IFN-gamma-induced injury of intestinal epithelial barrier function in Caco-2 monolayers. Inflamm Res 2015;64:789-797.
32. He F, Peng J, Deng XL, Yang LF, Camara AD, Omran A, Wang GL, Wu LW, Zhang CL, Yin F: Mechanisms of tumor necrosis factor-alpha-induced leaks in intestine epithelial barrier. Cytokine 2012;59:264-272.
33. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM: Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 1996;274:787-789.
34. Mankertz J, Amasheh M, Krug SM, Fromm A, Amasheh S, Hillenbrand B, Tavalali S, Fromm M, Schulzke JD: TNFalpha up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res 2009;336:67-77.
35. Luettig J, Rosenthal R, Lee IM, Krug SM, Schulzke JD: The ginger component 6-shogaol prevents TNF-alpha-induced barrier loss via inhibition of PI3K/Akt and NF-kappaB signaling. Mol Nutr Food Res 2016;60:2576-2586.
36. Petrache I, Verin AD, Crow MT, Birukova A, Liu F, Garcia JG: Differential effect of MLC kinase in TNF-alpha-induced endothelial cell apoptosis and barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 2001;280:L1168-1178.
37. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL: Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol 1997;273:C1378-1385.
38. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, Watterson DM, Clarke LL, Mrsny RJ, Turner JR: Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J Clin Invest 2005;115:2702-2715.
39. Tsukamoto O, Kitakaze M: Biochemical and physiological regulation of cardiac myocyte contraction by cardiac-specific myosin light chain kinase. Circ J 2013;77:2218-2225.
40. Roos WP, Kaina B: DNA damage-induced cell death by apoptosis. Trends Mol Med 2006;12:440-450.
41. Zhang Y, Hunter T: Roles of Chk1 in cell biology and cancer therapy. Int J Cancer 2014;134:1013-1023.
42. Campbell KJ, Witty JM, Rocha S, Perkins ND: Cisplatin mimics ARF tumor suppressor regulation of RelA (p65) nuclear factor-kappaB transactivation. Cancer Res 2006;66:929-935.
43. Graham WV, Wang F, Clayburgh DR, Cheng JX, Yoon B, Wang Y, Lin A, Turner JR: Tumor necrosis factor-induced 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.
44. Ye D, Ma TY: Cellular and molecular mechanisms that mediate basal and tumour necrosis factor-alpha-induced regulation of myosin light chain kinase gene activity. J Cell Mol Med 2008;12:1331-1346.
45. Hering NA, Schulzke JD: Therapeutic options to modulate barrier defects in inflammatory bowel disease. Dig Dis 2009;27:450-454.
46. Watari A, Yagi K, Kondoh M: A simple reporter assay for screening claudin-4 modulators. Biochem Biophys Res Commun 2012;426:454-460.
47. Watari A, Hashegawa M, Muangman T, Yagi K, Kondoh M: Use of cell-based screening to identify small-molecule compounds that modulate claudin-4 expression. Biotechnol Lett 2015;37:1177-1185.
48. Han C, Ding Z, Shi H, Qian W, Hou X, Lin R: The Role of Probiotics in Lipopolysaccharide-Induced Autophagy in Intestinal Epithelial Cells. Cell Physiol Biochem 2016;38:2464-2478.