AGR2 ameliorates tumor necrosis factor-α-induced epithelial barrier dysfunction via suppression of NF-κB p65-mediatedMLCK/p-MLC pathway activation

International Journal of Molecular Medicine

Volumn 39, Issue 5, 2017, Pages 1206-1214

  Ye, Xiaolin ^a   Sun, Mei ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Anterior gradient protein 2 homologue; Inflammatory bowel disease; Intestinal epithelial barrier; Myosin light chain kinase; Tight junction; Tumor necrosis factor

Indexed keywords

ANTERIOR GRADIENT PROTEIN 2 HOMOLOG; CLAUDIN 1; F ACTIN; MESSENGER RNA; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; OCCLUDIN; PROTEIN DISULFIDE ISOMERASE; PROTEIN ZO1; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ACTIN; AGR2 PROTEIN, HUMAN; PROTEIN; TIGHT JUNCTION PROTEIN; TJP1 PROTEIN, HUMAN;

ARTICLE; CACO-2 CELL LINE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; INTESTINE EPITHELIUM; PROTEIN EXPRESSION; TIGHT JUNCTION; CELL MEMBRANE PERMEABILITY; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; SIGNAL TRANSDUCTION;

ACTINS; CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; CLAUDIN-1; EPITHELIAL CELLS; GENE EXPRESSION; HUMANS; INTESTINAL MUCOSA; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; PROTEINS; SIGNAL TRANSDUCTION; TIGHT JUNCTION PROTEINS; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA; ZONULA OCCLUDENS-1 PROTEIN;

EID: 85018783756     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2017.2928     Document Type: Article

References (43)

1. Salim SY and Söderholm JD: Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm Bowel Dis 17: 362-381, 2011.
2. Petersson J, Schreiber O, Hansson GC, Gendler SJ, Velcich A, Lundberg JO, Roos S, Holm L and Phillipson M: Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastrointest Liver Physiol 300: G327-G333, 2011.
3. Fernández-Blanco JA, Estévez J, Shea-Donohue T, Martínez V, and Vergara P: Changes in epithelial barrier function in response to parasitic infection: implications for IBD pathogenesis. J Crohns Colitis 9: 463-476, 2015.
4. Edelblum KL and Turner JR: The tight junction in inflammatory disease: communication breakdown. Curr Opin Pharmacol 9: 715-720, 2009.
5. Alipour M, Zaidi D, Valcheva R, Jovel J, Martínez I, Sergi C, Walter J, Mason AL, Wong GK, Dieleman LA, et al: Mucosal barrier depletion and loss of bacterial diversity are primary abnormalities in paediatric ulcerative colitis. J Crohns Colitis 10: 462-471, 2016.
6. Vetrano S, Rescigno M, Cera MR, Correale C, Rumio C, Doni A, Fantini M, Sturm A, Borroni E, Repici A, et al: Unique role of junctional adhesion molecule-A in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 135: 173-184, 2008.
7. Neurath MF and Travis SP: Mucosal healing in inflammatory bowel diseases: a systematic review. Gut 61: 1619-1635, 2012.
8. Suzuki T, Yoshinaga N and Tanabe S: Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 286: 31263-31271, 2011.
9. Amasheh M, Grotjohann I, Amasheh S, Fromm A, Söderholm JD, Zeitz M, Fromm M and Schulzke JD: Regulation of mucosal structure and barrier function in rat colon exposed to tumor necrosis factor alpha and interferon gamma in vitro: a novel model for studying the pathomechanisms of inflammatory bowel disease cytokines. Scand J Gastroenterol 44: 1226-1235, 2009.
10. Liu H, Wang P, Cao M, Li M and Wang F: Protective role of oligomycin against intestinal epithelial barrier dysfunction caused by IFN-γ and TNF-α. Cell Physiol Biochem 29: 799-808, 2012.
11. Michielan A and D'Incà R: Intestinal permeability in inflammatory bowel disease: pathogenesis, clinical evaluation, and therapy of leaky gut. Mediators Inflamm 2015: 628157, 2015.
12. Suzuki T: Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70: 631-659, 2013.
13. Shen L, Weber CR, Raleigh DR, Yu D and Turner JR: Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73: 283-309, 2011.
14. Chen Y, Li D, Dai Z, Piao X, Wu Z, Wang B, Zhu Y and Zeng Z: L-methionine supplementation maintains the integrity and barrier function of the small-intestinal mucosa in post-weaning piglets. Amino Acids 46: 1131-1142, 2014.
15. Turner JR: Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809, 2009.
16. Marchiando AM, Shen L, Graham WV, Edelblum KL, Duckworth CA, Guan Y, Montrose MH, Turner JR and Watson AJ: The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology 140: 1208-1218, 2011.
17. Assasi N, Blackhouse G, Xie F, Marshall JK, Irvine EJ, Gaebel K, Robertson D, Campbell K, Hopkins R and Goeree R: Patient outcomes after anti TNF-alpha drugs for Crohn's disease. Expert Rev Pharmacoecon Outcomes Res 10: 163-175, 2010.
18. Wang QY, Sun AM, Song J, Chen Y, Wang JD and Li CG: Cytokine tumor necrosis factor alpha induces intestinal epithelial barrier dysfunction. Cytokine 58: 226-230, 2012.
19. Huys L, Van Hauwermeiren F, Dejager L, Dejonckheere E, Lienenklaus S, Weiss S, Leclercq G and Libert C: Type I interferon drives tumor necrosis factor-induced lethal shock. J Exp Med 206: 1873-1882, 2009.
20. Takahashi N, Vanlaere I, de Rycke R, Cauwels A, Joosten LA, Lubberts E, van den Berg WB and Libert C: IL-17 produced by Paneth cells drives TNF-induced shock. J Exp Med 205: 1755-1761, 2008.
21. Suzuki M, Nagaishi T, Yamazaki M, Onizawa M, Watabe T, Sakamaki Y, Ichinose S, Totsuka M, Oshima S, Okamoto R, et al: Myosin light chain kinase expression induced via tumor necrosis factor receptor 2 signaling in the epithelial cells regulates the development of colitis-associated carcinogenesis. PLoS One 9: e88369, 2014.
22. Feng Y and Teitelbaum DH: Tumour necrosis factor-induced loss of intestinal barrier function requires TNFR1 and TNFR2 signalling in a mouse model of total parenteral nutrition. J Physiol 591: 3709-3723, 2013.
23. Du J, Chen Y, Shi Y, Liu T, Cao Y, Tang Y, Ge X, Nie H, Zheng C and Li YC: 1, 25-Dihydroxyvitamin D protects intestinal epithelial barrier by regulating the myosin light chain kinase signaling pathway. Inflamm Bowel Dis 21: 2495-2506, 2015.
24. Liu X, Xu J, Mei Q, Han L and Huang J: Myosin light chain kinase inhibitor inhibits dextran sulfate sodium-induced colitis in mice. Dig Dis Sci 58: 107-114, 2013.
25. Park SW, Zhen G, Verhaeghe C, Nakagami Y, Nguyenvu LT, Barczak AJ, Killeen N and Erle DJ: The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proc Natl Acad Sci USA 106: 6950-6955, 2009.
26. Zheng W, Rosenstiel P, Huse K, Sina C, Valentonyte R, Mah N, Zeitlmann L, Grosse J, Ruf N, Nürnberg P, et al: Evaluation of AGR2 and AGR3 as candidate genes for inflammatory bowel disease. Genes Immun 7: 11-18, 2006.
27. Lai YR, Lu YF, Lien HW, Huang CJ and Hwang SP: Foxa2 and Hif1ab regulate maturation of intestinal goblet cells by modulating agr2 expression in zebrafish embryos. Biochem J 473: 2205-2218, 2016.
28. Zhao F, Edwards R, Dizon D, Afrasiabi K, Mastroianni JR, Geyfman M, Ouellette AJ, Andersen B and Lipkin SM: Disruption of Paneth and goblet cell homeostasis and increased endoplasmic reticulum stress in Agr2-/-mice. Dev Biol 338: 270-279, 2010.
29. Su L, Shen L, Clayburgh DR, Nalle SC, Sullivan EA, Meddings JB, Abraham C and Turner JR: Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis. Gastroenterology 136: 551-563, 2009.
30. Liu Z, Li N and Neu J: Tight junctions, leaky intestines, and pediatric diseases. Acta Paediatr 94: 386-393, 2005.
31. Lin N, Xu LF and Sun M: The protective effect of trefoil factor 3 on the intestinal tight junction barrier is mediated by toll-like receptor 2 via a PI3K/Akt dependent mechanism. Biochem Biophys Res Commun 440: 143-149, 2013.
32. Xu LF, Teng X, Guo J and Sun M: Protective effect of intestinal trefoil factor on injury of intestinal epithelial tight junction induced by platelet activating factor. Inflammation 35: 308-315, 2012.
33. Blander JM: Death in the intestinal epithelium-basic biology and implications for inflammatory bowel disease. FEBS J 283: 2720-2730, 2016.
34. Xiao YT, Yan WH, Cao Y, Yan JK and Cai W: Neutralization of IL-6 and TNF-α ameliorates intestinal permeability in DSS-induced colitis. Cytokine 83: 189-192, 2016.
35. Chen S, Zhu J, Chen G, Zuo S, Zhang J, Chen Z, Wang X, Li J, Liu Y and Wang P: 1,25-Dihydroxyvitamin D3 preserves intestinal epithelial barrier function from TNF-alpha induced injury via suppression of NF-kB p65 mediated MLCK-P-MLC signaling pathway. Biochem Biophys Res Commun 460: 873-878, 2015.
36. He F, Peng J, Deng XL, Yang LF, Camara AD, Omran A, Wang GL, Wu LW, Zhang CL and Yin F: Mechanisms of tumor necrosis factor-alpha-induced leaks in intestine epithelial barrier. Cytokine 59: 264-272, 2012.
37. Cao M, Wang P, Sun C, He W and Wang F: Amelioration of IFN-γ and TNF-α-induced intestinal epithelial barrier dysfunction by berberine via suppression of MLCK-MLC phosphorylation signaling pathway. PLoS One 8: e61944, 2013.
38. Zhang J, Lu Y, Wei J, Li L and Han L: Protective effect of carboxytmethylpachymaran on TNF-alpha-induced damage in Caco-2 cell monolayers. Int J Biol Macromol 93 (Pt A): 506-511, 2016.
39. Kuhlmann CR, Tamaki R, Gamerdinger M, Lessmann V, Behl C, Kempski OS and Luhmann HJ: Inhibition of the myosin light chain kinase prevents hypoxia-induced blood-brain barrier disruption. J Neurochem 102: 501-507, 2007.
40. Boivin MA, Ye D, Kennedy JC, Al-Sadi R, Shepela C and Ma TY: Mechanism of glucocorticoid regulation of the intestinal tight junction barrier. Am J Physiol Gastrointest Liver Physiol 292: G590-G598, 2007.
41. Cunningham KE and Turner JR: Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann NY Acad Sci 1258: 34-42, 2012.
42. Ye D and 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 12: 1331-1346, 2008.
43. Al-Sadi R, Guo S, Ye D, Rawat M and Ma TY: TNF-alpha modulation of intestinal tight junction permeability is mediated by NIK/IKK-alpha axis activation of the canonical NF-κB pathway. Am J Pathol 186: 1151-1165, 2016.