Chlorogenic acid enhances intestinal barrier by decreasing MLCK expression and promoting dynamic distribution of tight junction proteins in colitic rats

Journal of Functional Foods

Volumn 26, Issue , 2016, Pages 698-708

  Ruan, Zheng ^a   Mi, Shumei ^a   Zhou, Lili ^a   Zhou, Yan ^a   Li, Jing ^a   Liu, Wenhui ^a   Deng, Zeyuan ^a   Yin, Yulong ^a,b  

^a NANCHANG UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Chlorogenic acid; Colitis; Dynamic distribution; Intestinal barrier; Myosin light chain kinase; Tight junction

Indexed keywords

EID: 84985916742     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2016.08.038     Document Type: Article

References (39)

1. Antoni, L., Nuding, S., Wehkamp, J., Stange, E.F., Intestinal barrier in inflammatory bowel disease. World Journal of Gastroenterology 20:5 (2014), 1165–1179.
2. Bergmann, H., Rogoll, D., Scheppach, W., Melcher, R., Richling, E., The Ussing type chamber model to study the intestinal transport and modulation of specific tight-junction genes using a colonic cell line. Molecular Nutrition & Food Research 53:10 (2009), 1211–1225.
3. Bressebot, A., Pooya, S., Bossenmeyer-Pourie, C., Gauchotte, G., Germain, A., Chevaux, J.B., Coste, F., Vignaud, J.M., Guéant, J.L., Peyrin-Biroulet, L., Methyl donor deficiency affects small-intestinal differentiation and barrier function in rats. The British Journal of Nutrition 109:4 (2013), 1–11.
4. Cao, M., Wang, P., Sun, C., He, W., 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(6), 2013, e61944.
5. Chen, Y., Lu, Q., Goodenough, D.A., Jeansonne, B., Nonreceptor tyrosine kinase c-yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Molecular Biology of the Cell 13:4 (2002), 1227–1237.
6. Clayburgh, D.R., Barrett, T.Y., Meddings, J.B., Van Eldik, L.J., Watterson, D.M., Clarke, L.L., Mrsny, R.J., Turner, J.R., Epithelial myosin light chain kinase-dependent barrier dysfunction mediates t cell activation-induced diarrhea in vivo. The Journal of Clinical Investigation 115:10 (2005), 2702–2715.
7. Clifford, M.N., Chlorogenic acids and other cinnamates – Nature, occurrence and dietary burden. Journal of the Science of Food and Agriculture 79:3 (1999), 362–372.
8. Cunningham, K.E., Turner, J.R., Myosin light chain kinase: Pulling the strings of epithelial tight junction function. Annals of the New York Academy of Sciences 1258:12 (2012), 34–42.
9. Du, J., Chen, Y., Shi, Y., Liu, T., Cao, Y., Tang, Y., Ge, X., Nie, H., Zheng, C., Chun, Y., 1,25-dihydroxyvitamin d protects intestinal epithelial barrier by regulating the myosin light chain kinase signaling pathway. Inflammatory Bowel Diseases 21:11 (2015), 2495–2506.
10. 203 of claudin-1, a putative phosphorylation site for MAP kinase, is required to promote the barrier function of tight junctions. Experimental Cell Research 295:1 (2004), 36–47.
11. Gagat, M., Grzanka, D., Izdebska, M., Sroka, W.D., Hałas-Wiśniewska, M., Grzanka, A., Tropomyosin-1 protects transformed alveolar epithelial cells against cigarette smoke extract through the stabilization of F-actin-dependent cell-cell junctions. Acta Histochemica 118:3 (2016), 225–235.
12. Grilli, E., Tugnoli, B., Passey, J.L., Stahl, C.H., Piva, A., Moeser, A.J., Impact of dietary organic acids and botanicals on intestinal integrity and inflammation in weaned pigs. BMC Veterinary Research, 11, 2015, 96, 10.1186/s12917-015-0410-0.
13. Guttman, J.A., Li, Y., Wickham, M.E., Deng, W., Vogl, A.W., Finlay, B.B., Attaching and effacing pathogen-induced tight junction disruption in vivo. Cellular Microbiology 8:4 (2006), 634–645.
14. He, S., Liu, F., Xu, L., Yin, P., Li, D., Mei, C., Jiang, L., Ma, Y., Xu, J., Protective effects of ferulic acid against heat stress-induced intestinal epithelial barrier dysfunction in vitro and in vivo. PLoS ONE, 11(2), 2016, e0145236.
15. Ivanov, A.I., Actin motors that drive formation and disassembly of epithelial apical junctions. Frontiers in Bioscience 13:17 (2008), 6662–6681.
16. Keshavarzian, A., Farhadi, A., Forsyth, C.B., Rangan, J., Jakate, S., Shaikh, M., Banan, A., Fields, J.Z., Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. Journal of Hepatology 50:3 (2009), 538–547.
17. Li, X., Akhtar, S., Choudhry, M.A., Alteration in intestine tight junction protein phosphorylation and apoptosis is associated with increase in IL-18 levels following alcohol intoxication and burn injury. Biochimica et Biophysica Acta 1822:2 (2012), 196–203.
18. Li, Y., Shen, D., Tang, X., Li, X., Da, W., Yan, H., Song, R., Feng, J., Li, P., Zhang, J., Li, J., Chlorogenic acid prevents isoproterenol-induced hypertrophy in neonatal rat myocytes. Toxicology Letters 226:3 (2014), 257–263.
19. Ma, Y., Semba, S., Khan, M.R.I., Bochimoto, H., Watanabe, T., Fujiya, M., Kohgo, Y., Liu, Y., Taniguchi, T., Focal adhesion kinase regulates intestinal epithelial barrier function via redistribution of tight junction. Biochimica et Biophysica Acta 1832:1 (2013), 151–159.
20. Madara, J.L., Intestinal absorptive cell tight junctions are linked to cytoskeleton. The American Journal of Physiology 253:1 (1987), C171–C175.
21. Olthof, M.R., Hollman, P.C., Katan, M.B., Chlorogenic acid and caffeic acid are absorbed in humans. The Journal of Nutrition 131:1 (2001), 66–71.
22. Oshima, T., Koseki, J., Chen, X., Matsumoto, T., Miwa, H., Acid modulates the squamous epithelial barrier function by modulating the localization of claudins in the superficial layers. Laboratory Investigation; a Journal of Technical Methods and Pathology 92:1 (2011), 22–31.
23. Prigent, S.V., Gruppen, H., Visser, A.J., Van Koningsveld, G.A., De Jong, G.A., Voragen, A.G., Effects of non-covalent interactions with 5-O-caffeoylquinic acid (chlorogenic acid) on the heat denaturation and solubility of globular proteins. Journal of Agricultural and Food Chemistry 51:17 (2003), 5088–5095.
24. Qiu, W., Wu, B., Wang, X., Buchanan, M.E., Regueiro, M.D., Hartman, D.J., Schoen, R.E., Yu, J., Zhang, L., Puma-mediated intestinal epithelial apoptosis contributes to ulcerative colitis in humans and mice. The Journal of Clinical Investigation 121:5 (2011), 1722–1732.
25. Rao, R., Occludin phosphorylation in regulation of epithelial tight junctions. Annals of the New York Academy of Sciences 1165:1 (2009), 62–68.
26. Ruan, Z., Liu, S., Zhou, Y., Mi, S., Liu, G., Wu, X., Yao, K., Assaad, H., Deng, Z., Hou, Y., Wu, G., Yin, Y., Chlorogenic acid decreases intestinal permeability and increases expression of intestinal tight junction proteins in weaned rats challenged with LPS. PLoS ONE, 9(6), 2014, e97815.
27. Sakakibara, A., Furuse, M., Saitou, M., Ando-Akatsuka, Y., Tsukita, S., Possible involvement of phosphorylation of occludin in tight junction formation. The Journal of Cell Biology 137:6 (1997), 1393–1401.
28. Sandbichler, A.M., Egg, M., Schwerte, T., Pelster, B., Claudin 28b and f-actin are involved in rainbow trout gill pavement cell tight junction remodeling under osmotic stress. The Journal of Experimental Biology 214:9 (2011), 1473–1487.
29. Sato, Y., Itagaki, S., Kurokawa, T., Ogura, J., Kobayashi, M., Hirano, T., Sugawara, M., Iseki, K., In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. International Journal of Pharmaceutics 403:1–2 (2011), 136–138.
30. Scott, K.G., Meddings, J.B., Kirk, D.R., Lees-Miller, S.P., Buret, A.G., Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology 123:4 (2002), 1179–1190.
31. Shen, L., Black, E.D., Witkowski, E.D., Lencer, W.I., Guerriero, V., Schneeberger, E.E., Turner, J.R., Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. Journal of Cell Science 119:10 (2006), 2095–2106.
32. Sheth, P., Santos, N.D., Seth, A., Larusso, N.F., Rao, R.K., Lipopolysaccharide disrupts tight junctions in cholangiocyte monolayers by a c-Src-, TLR4-, and LBP-dependent mechanism. American Journal of Physiology. Gastrointestinal and Liver Physiology 293:1 (2007), 308–318.
33. Sileri, P., Morini, S., Sica, G.S., Schena, S., Rastellini, C., Gaspari, A.L., Benedetti, E., Cicalese, L., Bacterial translocation and intestinal morphological findings in jaundiced rats. Digestive Diseases and Sciences 47:4 (2002), 929–934.
34. Turner, J.R., Molecular basis of epithelial barrier regulation: From basic mechanisms to clinical application. American Journal of Pathology 169:6 (2006), 1901–1909.
35. Turner, J.R., Intestinal mucosal barrier function in health and disease. Nature Reviews. Immunology 9:11 (2009), 799–809.
36. Ulluwishewa, D., Anderson, R.C., McNabb, W.C., Moughan, P.J., Wells, J.M., Roy, N.C., Regulation of tight junction permeability by intestinal bacteria and dietary components. The Journal of Nutrition 141:5 (2011), 769–776.
37. Wang, D., Chadha, G.K., Feygin, A., Ivanov, A.I., F-actin binding protein, anillin, regulates integrity of intercellular junctions in human epithelial cells. Cellular and Molecular Life Sciences: CMLS 72:16 (2015), 1–16.
38. Xu, X., Zhang, L., Shao, B., Sun, X., Ho, C.T., Li, S., Safety evaluation of meso -zeaxanthin. Food Control 32:2 (2013), 678–686.
39. Yang, Y., Li, W., Sun, Y., Han, F., Hu, C.A., Wu, Z., Amino acid deprivation disrupts barrier function and induces protective autophagy in intestinal porcine epithelial cells. Amino Acids 47:10 (2015), 2177–2184.