Activation of muscarinic cholinoceptor ameliorates tumor necrosis factor-α-induced barrier dysfunction in intestinal epithelial cells

FEBS Letters

Volumn 589, Issue 23, 2015, Pages 3640-3647

  Khan, Md Rafiqul Islam ^a,g   Uwada, Junsuke ^a   Yazawa, Takashi ^a   Islam, Md Tariqul ^a   Krug, Susanne M ^b   Fromm, Michael ^b   Karaki, Shin Ichiro ^c   Suzuki, Yuichi ^c,d   Kuwahara, Atsukazu ^c   Yoshiki, Hatsumi ^e   Sada, Kiyonao ^e   Muramatsu, Ikunobu ^f   Anisuzzaman, Abu Syed Md ^g   Taniguchi, Takanobu ^a  

^a ASAHIKAWA MEDICAL COLLEGE   (Japan)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c UNIVERSITY OF SHIZUOKA   (Japan)

^d Sendai Shirayuri Women's College   (Japan)

^e UNIVERSITY OF FUKUI   (Japan)

^f KANAZAWA MEDICAL UNIVERSITY   (Japan)

^g UNIVERSITY OF RAJSHAHI   (Bangladesh)

Author keywords

Inflammatory bowel disease (IBD); Intestinal barrier; Intestinal epithelium; Muscarinic acetylcholine receptor; Tumor necrosis factor (TNF)

Indexed keywords

CYCLOOXYGENASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MUSCARINIC RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ADULT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ELECTRIC RESISTANCE; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; TRANSEPITHELIAL ELECTRICAL RESISTANCE; UPREGULATION; ANIMAL; COLON; CYTOLOGY; DRUG EFFECTS; HT 29 CELL LINE; INTESTINE MUCOSA; METABOLISM; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

ANIMALS; COLON; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; NF-KAPPA B; RATS; RECEPTORS, MUSCARINIC; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947050944     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.10.029     Document Type: Article

References (45)

1. D.R. Clayburgh, L. Shen, and J.R. Turner A porous defense: the leaky epithelial barrier in intestinal disease Lab. Invest. 84 2004 282 291
2. S.K. Yang, L. Eckmann, A. Panja, and M.F. Kagnoff Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells Gastroenterology 113 1997 1214 1223
3. + exchanger blockade inhibits enterocyte inflammatory response and protects against colitis Am. J. Physiol. Gasterointest. Liver Physiol. 283 2002 122 132
4. A.T. Gewirtz, P.O.J. Simon, C.K. Schmitt, L.J. Taylor, C.H. Hagedorn, A.D. O'Brien, A.S. Neish, and J.L. Madara Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response J. Clin. Invest. 107 2001 99 109
5. L. Mazzucchelli, C. Hauser, K. Zgraggen, H. Wagner, M. Hess, J.A. Laissue, and C. Mueller Expression of interleukin-8 gene in inflammatory bowel disease is related to the histologocal grade of active inflammation Am. J. Pathol. 144 1994 997 1007
6. Y.R. Mahida, M. Ceska, F. Effenberger, L. Kurlak, I. Lindley, and C.J. Hawkey Enhanced synthesis of neutrophil-activating peptide-1/interleukin-8 in active ulcerative colitis Clin. Sci. 82 1992 273 275
7. R.S. Izzo, K. Witkon, A.I. Chen, C. Hadjiyane, M.I. Weinstein, and C. Pellecchia Neutrophil activating peptide (interleukin-8) in colonic mucosa from patients with Crohn's disease Scand. J. Gastroenterol. 28 1993 296 300
8. K. Mitsuyama, A. Toyonaga, E. Sasaki, K. Watanabe, H. Tateishi, T. Nishiyama, T. Saiki, H. Ikeda, O. Tsuruta, and K. Tanikawa IL-8 as an important chemoattractant for neutrophils in ulcerative colitis and Crohn's disease Clin. Exp. Immunol. 96 1994 432 436
9. P. Gibon, and O. Rosella Interleukin-8 secretion by colonic crypt cells in vitro: response to injury suppressed by butyrate and enhanced in inflammatory bowel disease Gut 37 1995 536 543
10. H.B. Jijon, W.J. Panenka, K.L. Madsen, and H.G. Parsons MAP kinases contribute to IL-8 secretion by intestinal epithelial cells via a posttranscriptional mechanism Am. J. Physiol. Cell Physiol. 283 2002 C31 C41
11. M.J. May, and S. Ghosh Signal transduction through NF-kB Immunology 19 1998 80 88
12. A.S. Baldwin The NF-kB and IkB proteins: new discoveries and insights Annu. Rev. Immunol. 14 1996 649 683
13. C.L. Hirota, and D.M. MacKay Cholinergic regulation of epithelial ion transport in the mammalian intestine Br. J. Pharm. 149 2006 463 479
14. Z. Peng, J. Heath, C. Drachenberg, J.P. Raufman, and G. Xie Cholinergic muscarinic receptor activation augments murine intestinal epithelial cell proliferation and tumorigenesis BMC Cancer 13 2013 204
15. M.R.I. Khan, A.S.M. Anisuzzaman, S. Semba, Y. Ma, J. Uwada, H. Hayashi, Y. Suzuki, T. Takano, H. Ikeuchi, M. Uchino, A. Maemoto, F. Ushikubi, I. Muramatsu, and T. Taniguchi M1 is a major subtype of muscarinic acetylcholine receptors on mouse colonic epithelial cells J. Gastroenterol. 48 2013 885 896
16. M.R.I. Khan, T. Yazawa, A.S.M. Anisuzzaman, S. Semba, Y. Ma, J. Uwada, H. Hayashi, Y. Suzuki, H. Ikeuchi, M. Uchino, A. Maemoto, I. Muramatsu, and T. Taniguchi Activation of focal adhesion kinase via M1 muscarinic acetylcholine receptor is required in restitution of intestinal barrier function after epithelial injury Biochim. Biophys. Acta 1842 2014 635 645
17. R. Kopp, G. Lambrecht, E. Mutschier, U. Moser, R. Tacke, and A. Pfeiffer Human HT-29 colon carcinoma cells contain muscarinic M3 receptors coupled to phosphoinositide metabolism Eur. J. Pharmacol. 172 1989 397 405
18. A. Belo, K. Cheng, A. Chahdi, J. Shant, G. Xie, S. Khurana, and J.P. Raufman Muscarinic receptor agonists stimulate human colon cancer cell migration and invasion Am. J. Physiol. Gastrointest. Liver Physiol. 300 2011 G749 G760
19. M.P. Caulfield, and N.J. Birdsall International union of pharmacology. XVII. Classification of muscarinic acetylcholine receptors Pharmacol. Rev. 50 1998 279 290
20. M. Ishii, and Y. Kurachi Muscarinic acetylcholine receptors Curr. Pharm. Des. 12 2006 3573 3581
21. S. Lesko, I. Wessler, G. Gabel, C. Petto, and H. Pfannkuche Cholinergic modulation of epithelial integrity in the proximal colon of pigs Cells Tissues Organs 197 2013 411 420
22. Y. Zhang, and J. Li Carbachol ameliorates lipopolysaccharide-induced intestinal epithelial tight junction damage by down-regulating NF-kappabeta and myosin light-chain kinase pathways Biochem. Biophys. Res. Commun. 428 2012 321 326
23. I. Kaji, S. Karaki, and A. Kuwahara Effects of luminal thymol on epithelial transport in human and rat colon Am. J. Physiol. Gastrointest. Liver Physiol. 300 2011 G1132 G1143
24. - secretion in epithelial monolayers of mucus-forming human colon cells Am. J. Physiol. Cell Physiol. 261 1991 574 582
25. T. Yazawa, S. Kawabe, M. Kanno, T. Mizutani, Y. Imamichi, Y. Ju, T. Matsumura, Y. Yamazaki, Y. Usami, M. Kuribayashi, M. Shimada, T. Kitano, A. Umezawa, and K. Miyamoto Androgen/androgen receptor pathway regulates expression of the genes for cyclooxygenase-2 and amphiregulin in periovulatory granulosa cells Mol. Cell. Endocrinol. 369 2013 42 51
26. M. Amasheh, I. Grotjohann, S. Amasheh, A. Fromm, J.D. Soderholm, M. Zeitz, M. Fromm, and J.D. Schulzke 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 2009 1226 1235
27. T. Yamamoto, Y. Maruyama, S. Umegae, K. Matsumoto, and A.R. Saniabadi Mucosal inflammation in the terminal ileum of ulcerative colitis patients: endoscopic findings and cytokine profiles Dig. Liver Dis. 40 2008 253 259
28. P.P. Tak, and G.S. Firestein NF-kappaB: a key role in inflammatory diseases J. Clin. Invest. 107 2001 7 11
29. J. Wang, R.S. Al-Lamki, H. Zhang, N. Kirkiles-Smith, M.L. Gaeta, S. Thiru, J.S. Pober, and J.R. Bradley Histamine antagonizes tumor necrosis factor (TNF) signaling by stimulating TNF receptor shedding from the cell surface and Golgi storage pool J. Biol. Chem. 278 2003 21751 21760
30. K.J. Van Zee, T. Kohno, E. Fischer, C.S. Rock, L.L. Moldawer, and S.F. Lowry Tumor necrosis factor soluble receptors circulate during experimental and clinical inflammation and can protect against excessive tumor necrosis factor alpha in vitro and in vivo Proc. Natl. Acad. Sci. U.S.A. 89 1992 4845 4849
31. J.J. Peschon, J.L. Slack, P. Reddy, K.L. Stocking, S.W. Sunnarborg, D.C. Lee, W.E. Russell, B.J. Castner, R.S. Johnson, J.N. Fitzner, R.W. Boyce, N. Nelson, C.J. Kozlosky, M.F. Wolfson, C.T. Rauch, D.P. Cerretti, R.J. Paxton, C.J. March, and R.A. Black An essential role for ectodomain shedding in mammalian development Science 282 1998 1281 1284
32. C. Gerard, and B.J. Rollins Chemokines and disease Nat. Immunol. 2 2001 108 115
33. K. Gijsbers, G.V. Assche, S. Joossens, S. Struyf, P. Proost, P. Rutgeerts, K. Geboes, and J.V. Damme CXCR1-binding chemokines in inflammatory bowel diseases: down-regulated IL-8/CXCL8 production by leukocytes in Crohn's disease and selective GCP-2/CXCL6 expression in inflamed intestinal tissue Eur. J. Immunol. 34 2004 1992 2000
34. M. Bruewer, A. Luegering, T. Kucharzik, C.A. Parkos, J.L. Madara, A.M. Hopkins, and A. Nusrat Proinflammatory cytokines disrupts epithelial barrier function by apoptosis-independent mechanisms J. Immunol. 171 2003 6164 6172
35. F. Wang, B.T. Schwarz, W.V. Graham, Y. Wang, L. Su, D.R. Clayburgh, C. Abraham, and J.R. Turner IFN-γ-induced TNFR2 expression is required for TNF-dependent intestinal epithelial barrier dysfunction Gastroenterology 131 2006 1153 1163
36. H. Schmitz, M. Fromm, C.J. Bentzel, P. Scholz, K. Detjen, J. Mankertz, H. Bode, H.J. Epple, E.O. Riecken, and J.D. Schulzke Tumor necrosis factor-alpha (TNFa) regulates the epithelial barrier in the human intestinal cell line HT-29/B6 J. Cell Sci. 112 1999 137 146
37. M. Amasheh, A. Fromm, S.M. Krug, S. Amasheh, S. Andres, M. Zeitz, M. Fromm, and J.D. Schulzke TNFa-induced and berberine-antagonized tight junction barrier impairment via tyrosine kinase, Akt and NFkB signaling J. Cell Sci. 123 2010 4145 4155
38. H. Frucht, R.T. Jensen, D. Dexter, W.L. Yang, and Y. Xiao Human colon cancer cell proliferation mediated by the M3 muscarinic cholinergic receptor Clin. Cancer Res. 5 1999 2532 2539
39. S. Lindqvist, J. Hernon, P. Sharp, N. Johns, S. Addison, M. Watson, R. Tighe, S. Greer, J. Mackay, M. Rhodes, M. Lewis, W. Stebbings, C. Speakman, S. Evangelista, I. Johnson, and M. Williams The colon-selective spasmolytic otilonium bromide inhibits muscarinic M(3) receptor-coupled calcium signals in isolated human colonic crypts Br. J. Pharmacol. 137 2002 1134 1142
40. A. Lang, M. Lahav, E. Sakhnini, I. Barshack, H.H. Fidder, B. Avidan, E. Bardan, R. Hershkoviz, S. Bar-Meir, and Y. Chowers Allicin inhibits spontaneous and TNF-alpha induced secretion of proinflammatory cytokines and chemokines from intestinal epithelial cells Clin. Nutr. 23 2004 1199 1208
41. Y. Chowers, L. Cahalon, M. Lahav, H. Schor, R. Tal, S. Bar-Meir, and M. Levite Somatostatin through its specific receptor inhibits spontaneous and TNF-alpha- and bacteria-induced IL-8 and IL-1 beta secretion from intestinal epithelial cells J. Immunol. 165 2000 2955 2961
42. E. Hoffmann, O. Dittrich-Breiholz, H. Holtmann, and M. Kracßht Multiple control of interleukin-8 gene expression J. Leukocyte Biol. 72 2002 847 855
43. R.E. Simone, M. Russo, A. Catalano, G. Monego, K. Froehlich, V. Boehm, and P.P. Mail Lycopene inhibits NF-kB-Mediated IL-8 expression and changes redox and PPARγ signalling in cigarette smoke-stimulated macrophages PLoS ONE 6 2011 e19652
44. S. Dhawan, I.H. Hiemstra, C. Verseijden, F.W. Hilbers, A.A. Te Velde, L.E. Willemsen, J. Stap, J.M. den Haan, and W.J. de Jonge Cholinergic receptor activation on epithelia protects against cytokine-induced barrier dysfunction Acta Physiol. (Oxf.) 213 2015 846 859
45. T.Y. Ma, M.A. Boivin, D. Ye, A. Pedram, and H.M. Said 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 2005 G422 G430