Role of snail activation in alcohol-induced iNOS-mediated disruption of intestinal epithelial cell permeability

Alcoholism: Clinical and Experimental Research

Volumn 35, Issue 9, 2011, Pages 1635-1643

  Forsyth, Christopher B ^a   Tang, Yueming ^a   Shaikh, Maliha ^a   Zhang, Lijuan ^a   Keshavarzian, Ali ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alcohol; Epithelial mesenchymal transition; INOS; Intestinal permeability; Snail

Indexed keywords

ALCOHOL; INDUCIBLE NITRIC OXIDE SYNTHASE; P21 ACTIVATED KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNAIL;

ANIMAL EXPERIMENT; ARTICLE; CELL DISRUPTION; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; ENZYME ACTIVATION; INTESTINE EPITHELIUM CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CACO-2 CELLS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; ETHANOL; HUMANS; INTESTINAL MUCOSA; LIVER DISEASES, ALCOHOLIC; LYSINE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR TARGETED THERAPY; NITRIC OXIDE SYNTHASE TYPE II; P21-ACTIVATED KINASES; PERMEABILITY; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

GASTROPODA; MUS; RODENTIA;

EID: 80052024454     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2011.01510.x     Document Type: Article

References (49)

1. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA (2009) Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119:1438-1449.
2. Banan A, Choudhary S, Zhang Y, Fields JZ, Keshavarzian A (1999) Ethanol-induced barrier dysfunction and its prevention by growth factors in human intestinal monolayers: evidence for oxidative and cytoskeletal mechanisms. J Pharmacol Exp Ther 291:1075-1085.
3. Banan A, Fields JZ, Decker H, Zhang Y, Keshavarzian A (2000) Nitric oxide and its metabolites mediate ethanol-induced microtubule disruption and intestinal barrier dysfunction. J Pharmacol Exp Ther 294:997-1008.
4. Banan A, Keshavarzian A, Zhang L, Shaikh M, Forsyth CB, Tang Y, Fields JZ (2007) NF-kappaB activation as a key mechanism in ethanol-induced disruption of the F-actin cytoskeleton and monolayer barrier integrity in intestinal epithelium. Alcohol 41:447-460.
5. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2:84-89.
6. Bjarnason I, Peters TJ, Wise RJ (1984) The leaky gut of alcoholism: possible route of entry for toxic compounds. Lancet 1:179-182.
7. Blanco AM, Pascual M, Valles SL, Guerri C (2004) Ethanol-induced iNOS and COX-2 expression in cultured astrocytes via NF-kappa B. Neuroreport 15:681-685.
8. Bode C, Bode JC (2005) Activation of the innate immune system and alcoholic liver disease: effects of ethanol per se or enhanced intestinal translocation of bacterial toxins induced by ethanol? Alcohol Clin Exp Res 29:166S-171S.
9. Bode C, Kugler V, Bode JC (1987) Endotoxemia in patients with alcoholic and non-alcoholic cirrhosis and in subjects with no evidence of chronic liver disease following acute alcohol excess. J Hepatol 4:8-14.
10. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83.
11. Carrozzino F, Soulie P, Huber D, Mensi N, Orci L, Cano A, Feraille E, Montesano R (2005) Inducible expression of Snail selectively increases paracellular ion permeability and differentially modulates tight junction proteins. Am J Physiol Cell Physiol 289:C1002-C1014.
12. Clayburgh DR, Shen L, Turner JR (2004) A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 84:282-291.
13. Djamali A, Reese S, Yracheta J, Oberley T, Hullett D, Becker B (2005) Epithelial-to-mesenchymal transition and oxidative stress in chronic allograft nephropathy. Am J Transplant 5:500-509.
14. Farhadi A, Keshavarzian A, Fields JZ, Sheikh M, Banan A (2006) Resolution of common dietary sugars from probe sugars for test of intestinal permeability using capillary column gas chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 836:63-68.
15. Forsyth CB, Banan A, Farhadi A, Fields JZ, Tang Y, Shaikh M, Zhang LJ, Engen PA, Keshavarzian A (2007) Regulation of oxidant-induced intestinal permeability by metalloprotease-dependent epidermal growth factor receptor signaling. J Pharmacol Exp Ther 321:84-97.
16. Forsyth CB, Pulai J, Loeser RF (2002) Fibronectin fragments and blocking antibodies to alpha2beta1 and alpha5beta1 integrins stimulate mitogen-activated protein kinase signaling and increase collagenase 3 (matrix metalloproteinase 13) production by human articular chondrocytes. Arthritis Rheum 46:2368-2376.
17. Forsyth CB, Tang Y, Shaikh M, Zhang L, Keshavarzian A (2010) Alcohol stimulates activation of snail, epidermal growth factor receptor signaling, and biomarkers of epithelial-mesenchymal transition in colon and breast cancer cells. Alcohol Clin Exp Res 34:19-31.
18. Grant BF, Dufour MC, Harford TC (1988) Epidemiology of alcoholic liver disease. Semin Liver Dis 8:12-25.
19. Hollander D (1999) Intestinal permeability, leaky gut, and intestinal disorders. Curr Gastroenterol Rep 1:410-416.
20. Hou Y, Ye RD, Browning DD (2004) Activation of the small GTPase Rac1 by cGMP-dependent protein kinase. Cell Signal 16:1061-1069.
21. Ikenouchi J, Matsuda M, Furuse M, Tsukita S (2003) Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci 116:1959-1967.
22. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, van Roy F, Dargemont C, de Herreros AG, Bellacosa A, Larue L (2007) Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 26:7445-7456.
23. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119:1420-1428.
24. Keshavarzian A, Farhadi A, Forsyth CB, Rangan J, Jakate S, Shaikh M, Banan A, Fields JZ (2009) Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J Hepatol 50:538-547.
25. Keshavarzian A, Holmes EW, Patel M, Iber F, Fields JZ, Pethkar S (1999) Leaky gut in alcoholic cirrhosis: a possible mechanism for alcohol-induced liver damage. Am J Gastroenterol 94:200-207.
26. Lambert JC, Zhou Z, Wang L, Song Z, McClain CJ, Kang YJ (2003) Prevention of alterations in intestinal permeability is involved in zinc inhibition of acute ethanol-induced liver damage in mice. J Pharmacol Exp Ther 305:880-886.
27. Laukoetter MG, Nava P, Nusrat A (2008) Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol 14:401-407.
28. Lopez-Novoa JM, Nieto MA (2009) Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 1:303-314.
29. Ma TY, Nguyen D, Bui V, Nguyen H, Hoa N (1999) Ethanol modulation of intestinal epithelial tight junction barrier. Am J Physiol 276:G965-G974.
30. Mandayam S, Jamal MM, Morgan TR (2004) Epidemiology of alcoholic liver disease. Semin Liver Dis 24:217-232.
31. Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495-499.
32. Ohkubo T, Ozawa M (2004) The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J Cell Sci 117:1675-1685.
33. Pautz A, Art J, Hahn S, Nowag S, Voss C, Kleinert H (2010) Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide 23:75-93.
34. Purohit V, Bode JC, Bode C, Brenner DA, Choudhry MA, Hamilton F, Kang YJ, Keshavarzian A, Rao R, Sartor RB, Swanson C, Turner JR (2008) Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: summary of a symposium. Alcohol 42:349-361.
35. Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE, Leake D, Godden EL, Albertson DG, Nieto MA, Werb Z, Bissell MJ (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436:123-127.
36. Rao RK, Seth A, Sheth P (2004) Recent advances in alcoholic liver disease I. Role of intestinal permeability and endotoxemia in alcoholic liver disease. Am J Physiol Gastrointest Liver Physiol 286:G881-G884.
37. Rehm J, Room R, Monteiro M, Gmel G, Graham K, Rehn N, Sempos CT, Jernigan D (2003) Alcohol as a risk factor for global burden of disease. Eur Addict Res 9:157-164.
38. Stockton RA, Schaefer E, Schwartz MA (2004) p21-activated kinase regulates endothelial permeability through modulation of contractility. J Biol Chem 279:46621-46630.
39. Tang Y, Forsyth CB, Farhadi A, Rangan J, Jakate S, Shaikh M, Banan A, Fields JZ, Keshavarzian A (2009) Nitric oxide-mediated intestinal injury is required for alcohol-induced gut leakiness and liver damage. Alcohol Clin Exp Res 33:1220-1230.
40. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442-454.
41. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
42. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142.
43. Tipoe GL, Liong EC, Casey CA, Donohue TM Jr, Eagon PK, So H, Leung TM, Fogt F, Nanji AA (2008) A voluntary oral ethanol-feeding rat model associated with necroinflammatory liver injury. Alcohol Clin Exp Res 32:669-682.
44. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J, Pietras K, Virtanen I, Philipson L, Leopold PL, Crystal RG, de Herreros AG, Moustakas A, Pettersson RF, Fuxe J (2009) A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 11:943-950.
45. Wu SY, Ferkowicz M, McClay DR (2007) Ingression of primary mesenchyme cells of the sea urchin embryo: a precisely timed epithelial mesenchymal transition. Birth Defects Res C Embryo Today 81:241-252.
46. Wu SY, McClay DR (2007) The Snail repressor is required for PMC ingression in the sea urchin embryo. Development 134:1061-1070.
47. Yang Z, Rayala S, Nguyen D, Vadlamudi RK, Chen S, Kumar R (2005) Pak1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions. Cancer Res 65:3179-3184.
48. Zhang A, Jia Z, Guo X, Yang T (2007) Aldosterone induces epithelial-mesenchymal transition via ROS of mitochondrial origin. Am J Physiol Renal Physiol 293:F723-F731.
49. Zhong W, McClain CJ, Cave M, Kang YJ, Zhou Z (2010) The role of zinc deficiency in alcohol-induced intestinal barrier dysfunction. Am J Physiol Gastrointest Liver Physiol 298:G625-G633.