Ethanol causes endoplasmic reticulum stress and impairment of insulin secretion in pancreatic β-cells

Alcohol

Volumn 46, Issue 1, 2012, Pages 89-99

  Nguyen, Khanh Hoa ^a   Lee, Jong Han ^a   Nyomba, B L Grégoire ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Beta cell death; Endoplasmic reticulum stress; Inositol trisphosphate receptor; Insulin genes; Insulin secretion; Islets

Indexed keywords

ADENINE; ADENOSINE TRIPHOSPHATE; ALCOHOL; ALCOHOL DEHYDROGENASE; CYCLIC AMP; CYTOSINE; DIAZOXIDE; GLUCOSE; GUANOSINE; INSULIN; POTASSIUM CHLORIDE; PROTEIN KINASE C; PYRAZOLE DERIVATIVE; THYMINE; TOLBUTAMIDE; URACIL;

ALCOHOL CONSUMPTION; ALCOHOL METABOLISM; ARTICLE; B LYMPHOCYTE; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; HOMEOBOX; HUMAN; HUMAN CELL; INSULIN RELEASE; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; CELL LINE; CENTRAL NERVOUS SYSTEM DEPRESSANTS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ETHANOL; GENE EXPRESSION; GLUCOSE; HEAT-SHOCK PROTEINS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; PROTEIN DISULFIDE-ISOMERASES; PROTEIN KINASE C; TRANSCRIPTION FACTOR CHOP;

MURINAE;

EID: 84855546796     PISSN: 07418329     EISSN: 18736823     Source Type: Journal    
DOI: 10.1016/j.alcohol.2011.04.001     Document Type: Article

References (53)

1. Adachi M., Higuchi H., Miura S., Azuma T., Inokuchi S., Saito H., et al. Bax interacts with the voltage-dependent anion channel and mediates ethanol-induced apoptosis in rat hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287:G695-G705.
2. Baliunas D.O., Taylor B.J., Irving H., Roerecke M., Patra J., Mohapatra S., et al. Alcohol as a risk factor for type 2 diabetes: a systematic review and meta-analysis. Diabetes Care 2009, 32:2123-2132.
3. Beulens J.W., Rimm E.B., Hendriks H.F., Hu F.B., Manson J.E., Hunter D.J., et al. Alcohol consumption and type 2 diabetes: influence of genetic variation in alcohol dehydrogenase. Diabetes 2007, 56:2388-2394.
4. Bokkala S., Rubin E., Joseph S.K. Effect of chronic ethanol exposure on inositol trisphosphate receptors in WB rat liver epithelial cells. Alcohol. Clin. Exp. Res. 1999, 23:1875-1883.
5. Bühler R., Pestalozzi D., Hess M., Von Wartburg J.P. Immunohistochemical localization of alcohol dehydrogenase in human kidney, endocrine organs and brain. Pharmacol. Biochem. Behav. 1983, 18:55-59.
6. Carlsson S., Hammar N., Efendic S., Persson P.G., Ostenson C.G., Grill V. Alcohol consumption, Type 2 diabetes mellitus and impaired glucose tolerance in middle-aged Swedish men. Diabet. Med. 2000, 17:776-781.
7. Chu J., Tong M., de la Monte S.M. Chronic ethanol exposure causes mitochondrial dysfunction and oxidative stress in immature central nervous system neurons. Acta Neuropathol. 2007, 113:659-673.
8. Dembele K., Nguyen K.H., Hernandez T.A., Nyomba B.L. Effects of ethanol on pancreatic beta-cell death: interaction with glucose and fatty acids. Cell Biol. Toxicol. 2009, 25:141-152.
9. Dey A., Cederbaum A.I. Alcohol and oxidative liver injury. Hepatology 2006, 43:S63-S74.
10. Eysseric H., Gonthier B., Soubeyran A., Bessard G., Saxod R., Barret L. Characterization of the production of acetaldehyde by astrocytes in culture after ethanol exposure. Alcohol Clin. Exp. Res. 1997, 21:1018-1023.
11. Flanagan D.E., Pratt E., Murphy J., Vaile J.C., Petley G.W., Godsland I.F., et al. Alcohol consumption alters insulin secretion and cardiac autonomic activity. Eur. J. Clin. Invest. 2002, 32:187-192.
12. Garcia-Ocana A., Takane K.K., Syed M.A., Philbrick W.M., Vasavada R.C., Stewart A.F. Hepatocyte growth factor overexpression in the islet of transgenic mice increases beta cell proliferation, enhances islet mass, and induces mild hypoglycemia. J. Biol. Chem. 2000, 275:1226-1232.
13. Gilon P., Henquin J.C. Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Endocr. Rev. 2001, 22:565-604.
14. Gonzalez A., Pariente J.A., Salido G.M. Ethanol impairs calcium homeostasis following CCK-8 stimulation in mouse pancreatic acinar cells. Alcohol 2008, 42:565-573.
15. Hafko R., Orecná M., Bacová Z., Kolláriková G., Lacík I., Strbák V. Mechanism of ethanol-induced insulin secretion from INS-1 and INS-1E tumor cell lines. Cell Physiol. Biochem. 2009, 24:441-450.
16. He L., Marecki J.C., Serrero G., Simmen F.A., Ronis M.J., Badger T.M. Dose-dependent effects of alcohol on insulin signaling: partial explanation for biphasic alcohol impact on human health. Mol. Endocrinol. 2007, 21:2541-2550.
17. Henquin J.C. Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 2009, 52:739-751.
18. Higa M., Zhou Y., Ravazzola M., Baetens D., Orci L., Unger R.H. Troglitazone prevents mitochondrial alterations, beta cell destruction, and diabetes in obese prediabetic rats. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11513-11518.
19. Hoa N.K., Norberg A., Sillard R., Van Phan D., Thuan N.D., Dzung D.T., et al. The possible mechanisms by which phanoside stimulates insulin secretion from rat islets. J. Endocrinol. 2007, 192:389-394.
20. Hoa N.K., Phan D.V., Thuan N.D., Ostenson C.G. Insulin secretion is stimulated by ethanol extract of Anemarrhena asphodeloides in isolated islet of healthy Wistar and diabetic Goto-Kakizaki rats. Exp. Clin. Endocrinol. Diabetes 2004, 112:520-525.
21. Holbrook T.L., Barrett-Connor E., Wingard D.L. Aprospective population-based study of alcohol use and non-insulin-dependent diabetes mellitus. Am. J. Epidemiol. 1990, 132:902-909.
22. Hong-Brown L.Q., Frost R.A., Lang C.H. Alcohol impairs protein synthesis and degradation in cultured skeletal muscle cells. Alcohol Clin. Exp. Res. 2001, 25:1373-1382.
23. Huang Z., Sjoholm A. Ethanol acutely stimulates islet blood flow, amplifies insulin secretion, and induces hypoglycemia via nitric oxide and vagally mediated mechanisms. Endocrinology 2008, 149:232-236.
24. Joseph S.K. The inositol triphosphate receptor family. Cell Signal 1996, 8:1-7.
25. Koko V., Todorovic V., Nikolic J.A., Glisic R., Cakic M., Lackovic V., et al. Rat pancreatic B-cells after chronic alcohol feeding. A morphometric and fine structural study. Histol. Histopathol. 1995, 10:325-337.
26. Lacy P.E., Kostianovsky M. Method for the isolation of intact islets of Langerhans from the rat pancreas. Diabetes 1967, 16:35-39.
27. Lee J.H., Nguyen K.H., Nyomba B.L. Prohibitin is expressed in pancreatic β-cells and protects against oxidative and proapoptotic effects of ethanol. FEBS J. 2010, 277:488-500.
28. Lupi R., Del Guerra S., Fierabracci V., Marselli L., Novelli M., Patanè G., et al. Lipotoxicity in human pancreatic islets and the protective effect of metformin. Diabetes 2002, 51(Suppl 1):S134-S137.
29. Metz R., Berger S., Mako M. Potentiation of the plasma insulin response to glucose by prior administration of alcohol. An apparent islet-priming effect. Diabetes 1969, 18:517-522.
30. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
31. Nammi S., Dembele K., Nyomba B.L. Increased 11beta-hydroxysteroid dehydrogenase type-1 and hexose-6-phosphate dehydrogenase in liver and adipose tissue of rat offspring exposed to alcohol in utero. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R1101-R1109.
32. Nealon W.H., Townsend C.M., Thompson J.C. The time course of beta cell dysfunction in chronic ethanol-induced pancreatitis: a prospective analysis. Surgery 1988, 104:1074-1079.
33. Nordback I.H., Olson J.L., Chacko V.P., Cameron J.L. Detailed characterization of experimental acute alcoholic pancreatitis. Surgery 1995, 117:41-49.
34. Onishi Y., Honda M., Ogihara T., Sakoda H., Anai M., Fujishiro M., et al. Ethanol feeding induces insulin resistance with enhanced PI 3-kinase activation. Biochem. Biophys. Res. Commun. 2003, 303:788-794.
35. Oyadomari S., Koizumi A., Takeda K., Gotoh T., Akira S., Araki E., et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 2002, 109:525-532.
36. Patel D.G., Singh S.P. Effect of ethanol and its metabolites on glucose mediated insulin release from isolated islets of rats. Metabolism 1979, 28:85-89.
37. Robertson R.P., Harmon J., Tran P.O., Tanaka Y., Takahashi H. Glucose toxicity in beta-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 2003, 52:581-587.
38. Robertson R.P., Tanaka Y., Sacchi G., Tran P.O.T., Gleason C., Poitout V. Glucose Toxicity of the Beta-Cell: Cellular and Molecular Mechanisms 2000, Lippincott Williams & Wilkins, New York, NY.
39. Robertson R.P., Zhang H.J., Pyzdrowski K.L., Walseth T.F. Preservation of insulin mRNA levels and insulin secretion in HIT cells by avoidance of chronic exposure to high glucose concentrations. J. Clin. Invest. 1992, 90:320-325.
40. Russell J.C., Amy R.M., Manickavel V., Dolphin P.J. Effects of chronic ethanol consumption in atherosclerosis-prone JCR: LA-corpulent rat. Arteriosclerosis 1989, 9:122-128.
41. Sakuta H., Suzuki T., Katayama Y., Yasuda H., Ito T. Heavy alcohol intake, homocysteine and Type 2 diabetes. Diabet. Med. 2005, 22:1359-1363.
42. Sasaki Y., Wands J.R. Ethanol impairs insulin receptor substrate-1 mediated signal transduction during rat liver regeneration. Biochem. Biophys. Res. Commun. 1994, 199:403-409.
43. Shin J.S., Lee J.J., Yang J.W., Kim C.W. Ethanol decreases basal insulin secretion from HIT-T15 cells. Life Sci. 2002, 70:1989-1997.
44. Simonyi A., Zhang J.P., Sun A.Y., Sun G.Y. Chronic ethanol on mRNA levels of IP3R1, IP3 3-kinase and mGluR1 in mouse Purkinje neurons. Neuroreport 1996, 7:2115-2118.
45. Singh S.P., Patel D.G., Snyder A.K. Ethanol inhibition of insulin secretion by perifused rat islets. Acta Endocrinol. (Copenh.) 1980, 93:61-66.
46. Singh S.P., Patel D.G., Snyder A.K., Pullen G.L. Ethanol influence on insulin secretion from isolated rat islets. Experientia 1986, 42:58-60.
47. Tiengo A., Valerio A., Molinari M., Meneghel A., Lapolla A. Effect of ethanol, acetaldehyde, and acetate on insulin and glucagon secretion in the perfused rat pancreas. Diabetes 1981, 30:705-709.
48. Touquet R., Cspike E., Holloway P., Brown A., Patel T., Seddon A.J., et al. Resuscitation room blood alcohol concentrations: one-year cohort study. Emerg. Med. J. 2008, 25:752-756.
49. Urso T., Gavaler J.S., Van Thiel D.H. Blood ethanol levels in sober alcohol users seen in an emergency room. Life Sci. 1981, 28:1053-1056.
50. Wan Q., Liu Y., Guan Q., Gao L., Lee K.O., Zhao J. Ethanol feeding impairs insulin-stimulated glucose uptake in isolated rat skeletal muscle: role of Gs alpha and cAMP. Alcohol Clin. Exp. Res. 2005, 29:1450-1456.
51. Wei M., Gibbons L.W., Mitchell T.L., Kampert J.B., Blair S.N. Alcohol intake and incidence of type 2 diabetes in men. Diabetes Care 2000, 23:18-22.
52. Zhao L.N., Hao L.P., Yang X.F., Ying C.J., Yu D., Sun X.F. The diabetogenic effects of excessive ethanol: reducing beta-cell mass, decreasing phosphatidylinositol 3-kinase activity and GLUT-4 expression in rats. Br. J. Nutr. 2009, 101:1467-1473.
53. Zuba D., Piekoszewski W., Pach J., Winnik L., Parczewski A. Concentration of ethanol and other volatile compounds in the blood of acutely poisoned alcoholics. Alcohol 2002, 26:17-22.