Insulin resistance, ceramide accumulation and endoplasmic reticulum stress in experimental chronic alcohol-induced steatohepatitis

Alcohol and Alcoholism

Volumn 48, Issue 1, 2013, Pages 39-52

  Ramirez, Teresa ^a   Longato, Lisa ^a   Tong, Ming ^a   Wands, Jack R ^a   de la Monte, Suzanne M ^a   Dostalek, Miroslav ^b  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CERAMIDE; COLONY STIMULATING FACTOR 1; CXCL1 CHEMOKINE; CYTOKINE; EOTAXIN; ERYTHROPOIETIN; GAMMA INTERFERON; GLYCOGEN SYNTHASE KINASE 3BETA; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; PROLINE; PROTEIN KINASE B; S6 KINASE;

ALCOHOLIC FATTY LIVER; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CHRONICITY; CONTROLLED STUDY; DISEASE COURSE; DISORDERS OF LIPID METABOLISM; DNA DAMAGE; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME SUBSTRATE; HISTOPATHOLOGY; INFLAMMATION; INSULIN RESISTANCE; LIPID PEROXIDATION; LIPID STORAGE; LIQUID CHROMATOGRAPHY; LIVER FIBROSIS; LIVER INJURY; LIVER STRUCTURE; LONG EVANS RAT; MALE; MITOCHONDRIAL VOLUME; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UPREGULATION;

ANIMALS; CERAMIDES; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; ETHANOL; FATTY LIVER, ALCOHOLIC; INSULIN RESISTANCE; MALE; RATS; RATS, LONG-EVANS;

RATTUS;

EID: 84871565729     PISSN: 07350414     EISSN: 14643502     Source Type: Journal    
DOI: 10.1093/alcalc/ags106     Document Type: Article

References (103)

1. Alkhouri N, Dixon LJ, Feldstein AE. (2009) Lipotoxicity in nonalcoholic fatty liver disease: not all lipids are created equal.Expert Rev Gastroenterol Hepatol 3:445-51.
2. Anderson N, Borlak J. (2008) Molecular mechanisms and therapeutic targets in steatosis and steatohepatitis. Pharmacol Rev 60:311-57.
3. Bielawski J, Szulc ZM, Hannun YA et al. (2006) Simultaneous quantitative analysis of bioactive sphingolipids by highperformance liquid chromatography-tandem mass spectrometry.Methods 39:82-91.
4. Bielawski J, Pierce JS, Snider J et al. (2009) Comprehensive quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods Mol Biol 579:443-67.
5. Bielawski J, Pierce JS, Snider J et al. (2010) Sphingolipid analysis by high performance liquid chromatography-tandem mass spectrometry(HPLC-MS/MS). Adv Exp Med Biol 688:46-59.
6. Boslem E, MacIntosh G, Preston AM et al. (2011) A lipidomic screen of palmitate-treated MIN6 beta-cells links sphingolipid metabolites with endoplasmic reticulum (ER) stress and impaired protein trafficking. Biochem J 435:267-76.
7. Bourbon NA, Sandirasegarane L, Kester M. (2002) Ceramideinduced inhibition of Akt is mediated through protein kinase Czeta: implications for growth arrest. J Biol Chem 277:3286-92.
8. Carracedo A, Lorente M, Egia A et al. (2006) The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell 9:301-12.
9. Cohen JI, Nagy LE. (2011) Pathogenesis of alcoholic liver disease:interactions between parenchymal and non-parenchymal cells.J Dig Dis 12:3-9.
10. Cohen AC, Tong M, Wands JR et al. (2007) Insulin and insulin-like growth factor resistance with neurodegeneration in an adult chronic ethanol exposure model. Alcohol Clin Exp Res 31:1558-73.
11. Dara L, Ji C, Kaplowitz N. (2011) The contribution of endoplasmic reticulum stress to liver diseases. Hepatology 53:1752-63.
12. de la Monte SM. (2012) Alcohol-induced liver and brain degeneration:roles of insulin resistance, toxic ceramides, and endoplasmic reticulum stress. In Sova Ms (ed). Alcohol, Nutrition, and Health Consequences. New York: Humana Press.
13. de la Monte SM, Neely TR, Cannon J et al. (2001) Ethanol impairs insulin-stimulated mitochondrial function in cerebellar granule neurons. Cell Mol Life Sci 58:1950-60.
14. de la Monte SM, Yeon JE, Tong M et al. (2008) Insulin resistance in experimental alcohol-induced liver disease. J Gastroenterol Hepatol 23:e477-86.
15. de la Monte SM, Longato L, Tong M et al. (2009a) The liver-brain axis of alcohol-mediated neurodegeneration: role of toxic lipids.Int J Environ Res Public Health 6:2055-75.
16. de la Monte SM, Tong M, Lawton M et al. (2009b) Nitrosamine exposure exacerbates high fat diet-mediated type 2 diabetes mellitus,non-alcoholic steatohepatitis, and neurodegeneration with cognitive impairment. Mol Neurodegener 4:54.
17. de la Monte SM, Pang M, Chaudhry R et al. (2011) Peroxisome proliferator-activated receptor agonist treatment of alcohol-induced hepatic insulin resistance. Hepatol Res 41:386-98.
18. de la Monte SM, Re E, Longato L et al. (2012) Dysfunctional proceramide, ER stress, and insulin/IGF signaling networks with progression of Alzheimer's disease. J Alzheimers Dis 30:S217-29.
19. Denucci SM, Tong M, Longato L et al. (2010) Rat strain differences in susceptibility to alcohol-induced chronic liver injury and hepatic insulin resistance. Gastroenterol Res Pract 2010:16.doi: 10.1155/2010/312790.
20. Derdak Z, Lang CH, Villegas KA et al. (2011) Activation of p53 enhances apoptosis and insulin resistance in a rat model of alcoholic liver disease. J Hepatol 54:164-72.
21. Ding WX, Manley S, Ni HM. (2011) The emerging role of autophagy in alcoholic liver disease. Exp Biol Med (Maywood)236:546-56.
22. Esfandiari F, Villanueva JA, Wong DH et al. (2005) Chronic ethanol feeding and folate deficiency activate hepatic endoplasmic reticulum stress pathway in micropigs. Am J Physiol Gastrointest Liver Physiol 289:G54-63.
23. Feldstein AE, Bailey SM. (2011) Emerging role of redox dysregulation in alcoholic and nonalcoholic fatty liver disease. Antioxid Redox Signal 15:421-4.
24. Gao L, Zhang X, Wang FR et al. (2010) Chronic ethanol consumption up-regulates protein-tyrosine phosphatase-1B (PTP1B) expression in rat skeletal muscle. Acta pharmacologica Sinica 31:1576-82.
25. Garcia-Ruiz C, Colell A, Mari M et al. (2003) Defective TNF-alpha-mediated hepatocellular apoptosis and liver damage in acidic sphingomyelinase knockout mice. J Clin Invest 111:197-208.
26. Hajduch E, Balendran A, Batty IH et al.(2001) Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells. Diabetologia 44:173-83.
27. Hannun YA, Obeid LM. (2008) Principles of bioactive lipid signalling:lessons from sphingolipids. Nat Rev Mol Cell Biol 9:139-50.
28. Hannun YA, Obeid LM. (2011) Many ceramides. J Biol Chem 286:27855-62.
29. He J, de la Monte S, Wands JR. (2007) Acute ethanol exposure inhibits insulin signaling in the liver. Hepatology 46:1791-800.
30. He J, de la Monte SM, Wands JR. (2010) The p85-beta regulatory subunit of PI3K serves as a substrate for PTEN protein phosphatase activity during insulin mediated signaling. Biochem Biophys Res Commun 397:513-9.
31. Holland WL, Summers SA. (2008) Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr Rev 29:381-402.
32. Holland WL, Knotts TA, Chavez JA et al. (2007) Lipid mediators of insulin resistance. Nutr Rev 65:S39-46.
33. Hotamisligil GS. (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140:900-17.
34. Ikonen E, Vainio S. (2005) Lipid microdomains and insulin resistance:Is there a connection? Sci STKE 2005:pe3.
35. Inokuchi J. (2011) Inhibition of ganglioside biosynthesis as a novel therapeutic approach in insulin resistance. Handbook Exp Pharmacol 203:165-78
36. Jager R, Bertrand MJ, Gorman AM et al. (2012) The unfolded protein response at the crossroads of cellular life and death during endoplasmic reticulum stress. Biol Cell 104:259-70.
37. Jelkmann W. (2011) Regulation of erythropoietin production.J Physiol 589:1251-8.
38. Ji C, Kaplowitz N. (2003) Betaine decreases hyperhomocysteinemia,endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 124:1488-99.
39. Kabayama K, Sato T, Kitamura F et al. (2005) TNFalpha-induced insulin resistance in adipocytes as a membrane microdomain disorder: involvement of ganglioside GM3. Glycobiology 15:21-9.
40. Kabayama K, Sato T, Saito K et al. (2007) Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc Natl Acad Sci USA 104:13678-83.
41. Kao Y, Youson JH, Holmes JA et al. (1999) Effects of insulin on lipid metabolism of larvae and metamorphosing landlocked sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 114:405-14.
42. Kaplowitz N, Ji C. (2006) Unfolding new mechanisms of alcoholic liver disease in the endoplasmic reticulum. J Gastroenterol Hepatol 21(Suppl 3):S7-9.
43. Kaplowitz N, Than TA, Shinohara M et al. (2007) Endoplasmic reticulum stress and liver injury. Semin Liver Dis 27:367-77.
44. Koybasi S, Senkal CE, Sundararaj K et al. (2004) Defects in cell growth regulation by C18:0-ceramide and longevity assurance gene 1 in human head and neck squamous cell carcinomas.J Biol Chem 279:44311-19.
45. Kraegen EW, Cooney GJ. (2008) Free fatty acids and skeletal muscle insulin resistance. Curr Opin Lipidol 19:235-41.
46. Kuznetsov JN, Leclerc GJ, Leclerc GM et al. (2011) AMPK and Akt determine apoptotic cell death following perturbations of
47. Langeveld M, Aerts JM. (2009) Glycosphingolipids and insulin resistance.Prog Lipid Res 48:196-205.
48. Levy M, Futerman AH. (2010) Mammalian ceramide synthases.IUBMB Life 62:347-56.
49. Li LO, Klett EL, Coleman RA. (2010)Acyl-CoA synthesis,lipid metabolism and lipotoxicity. Biochim Biophys Acta 1801:246-51.
50. Liangpunsakul S, Sozio MS, Shin E et al. (2010) Inhibitory effect of ethanol on AMPK phosphorylation is mediated in part through elevated ceramide levels. Am J Physiol Gastrointest Liver Physiol 298:G1004-12.
51. Lonardo A, Lombardini S, Ricchi M et al. (2005) Review article:hepatic steatosis and insulin resistance. Aliment Pharmacol Ther 22(Suppl 2):64-70.
52. Longato L, Ripp K, Setshedi M et al. (2012a) Insulin resistance,ceramide accumulation, and endoplasmic reticulum stress in human chronic alcohol-related liver disease. Oxid Med Cell Longev 2012:479348. [doi 10.1155/2012/479348].
53. Longato L, Tong M, Wands JR et al. (2012b) High fat diet induced hepatic steatosis and insulin resistance: role of dysregulated ceramide metabolism. Hepatol Res 42:412-27.
54. Lyn-Cook LE, Jr, Lawton M, Tong M et al. (2009) Hepatic ceramide may mediate brain insulin resistance and neurodegeneration in type 2 diabetes and non-alcoholic steatohepatitis.J Alzheimers Dis 16:715-29.
55. Mackall CL, Fry TJ, Gress RE. (2011)Harnessing the biology of IL-7 for therapeutic application. Nat Rev Immunol 11:330-42.
56. Malhi H, Gores GJ. (2008) Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin Liver Dis 28:360-9.
57. Malhi H, Kaufman RJ. (2011) Endoplasmic reticulum stress in liver disease. J Hepatol 54:795-809.
58. McCullough KD, Martindale JL, Klotz LO et al. (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by downregulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249-59.
59. McCullough AJ, O'Shea RS, Dasarathy S. (2011) Diagnosis and management of alcoholic liver disease. J Dig Dis 12:257-62.
60. McMillian MK, Grant ER, Zhong Z et al. (2001) Nile Red binding to HepG2 cells: an improved assay for in vitro studies of hepatosteatosis.In vitro Mol Toxicol 14:177-90.
61. McVicker BL, Tuma DJ, Kubik JL et al. (2006) Ethanol-induced apoptosis in polarized hepatic cells possibly through regulation of the Fas pathway. Alcohol Clin Exp Res 30:1906-15.
62. Miller AM, Horiguchi N, Jeong WI et al. (2011a) Molecular mechanisms of alcoholic liver disease: innate immunity and cytokines. Alcohol Clin Exp Res 35:787-93.
63. Miller AM, Wang H, Bertola A et al. (2011b) Inflammation-associated interleukin-6/signal transducer and activator of transcription 3 activation ameliorates alcoholic and nonalcoholic fatty liver diseases in interleukin-10-deficient mice.Hepatology 54:846-56.
64. Mohr L, Tanaka S, Wands JR. (1998) Ethanol inhibits hepatocyte proliferation in insulin receptor substrate 1 transgenic mice.Gastroenterology 115:1558-65.
65. Nogueira TC, Anhe GF, Carvalho CR et al. (2008) Involvement of phosphatidylinositol-3 kinase/AKT/PKCzeta/lambda pathway in
66. Onishi Y, Honda M, Ogihara T et al. (2003) Ethanol feeding induces insulin resistance with enhanced PI 3-kinase activation.Biochem Biophys Res Commun 303:788-94.
67. Osawa Y, Uchinami H, Bielawski J et al. (2005) Roles for C16-ceramide and sphingosine 1-phosphate in regulating hepatocyte apoptosis in response to tumor necrosis factor-alpha. J Biol Chem 280:27879-87.
68. O'Shea RS, Dasarathy S, McCullough AJ. (2010) Alcoholic liver disease. Hepatology 51:307-28.Oyadomari S, Mori M. (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381-9.
69. Oyadomari S, Mori M. (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381-9.
70. Ozcan U, Cao Q, Yilmaz E et al. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-61.
71. Pandol SJ, Gorelick FS, Gerloff A et al. (2010) Alcohol abuse,endoplasmic reticulum stress and pancreatitis. Dig Dis 28:776-82.
72. Pang M, de la Monte SM, Longato L et al. (2009) PPARdelta agonist attenuates alcohol-induced hepatic insulin resistance and improves liver injury and repair. J Hepatol 50:1192-201.
73. Patel BC, D'Arville C, Iwahashi M et al. (1991) Impairment of hepatic insulin receptors during chronic ethanol administration.Am J Physiol 261:G199-205.
74. Paula H, Asrani SK, Boetticher NC et al. (2010) Alcoholic liver disease-related mortality in the United States: 1980-2003. Am J Gastroenterol 105:1782-87.
75. Powell DJ, Hajduch E, Kular G et al. (2003) Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCzeta-dependent mechanism.Mol Cell Biol 23:7794-808.
76. Purohit V, Gao B, Song BJ. (2009) Molecular mechanisms of alcoholic fatty liver. Alcohol Clin Exp Res 33:191-205.
77. Ronis MJ, Wands JR, Badger TM et al. (2007) Alcohol-induced disruption of endocrine signaling. Alcohol Clin Exp Res 31:1269-85.
78. Ronis MJ, Butura A, Korourian S et al. (2008) Cytokine and chemokine expression associated with steatohepatitis and hepatocyte proliferation in rats fed ethanol via total enteral nutrition. Exp Biol Med (Maywood) 233:344-55.
79. Ruvolo PP. (2003) Intracellular signal transduction pathways activated by ceramide and its metabolites. Pharmacol Res 47:383-92.
80. Sasaki Y, Wands JR. (1994) Ethanol impairs insulin receptor substrate-1 mediated signal transduction during rat liver regeneration.Biochem Biophys Res Commun 199:403-9.
81. Sasaki Y, Hayashi N, Ito T et al. (1994) Influence of ethanol on insulin receptor substrate-1-mediated signal transduction during rat liver regeneration. Alcohol Alcohol 1:99-106.
82. Sauane M, Su ZZ, Dash R et al.(2010) Ceramide plays a prominent role in MDA-7/IL-24-induced cancer-specific apoptosis. J Cell Physiol 222:546-55.
83. Schutyser E, Struyf S, Van Damme J. (2003) The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 14:409-26.
84. Senkal CE, Ponnusamy S, Bielawski J et al. (2010) Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways. FASEB J 24:296-308.
85. Setshedi M, Tong M, Feng D et al. (2010) Ceramide inhibitors and PPAR agonists ameliorate alcohol-induced steatohepatitis in an ex-vivo liver slice culture model. Hepatology 52:121A.
86. Setshedi M, Longato L, Petersen DR et al. (2011) Limited therapeutic effect of N-acetylcysteine on hepatic insulin resistance in an experimental model of alcohol-induced steatohepatitis.Alcohol Clin Exp Res 35:2139-51.
87. Seumois G, Fillet M, Gillet L et al. (2007) De novo C16- and C24-ceramide generation contributes to spontaneous neutrophil apoptosis. J Leukoc Biol 81:1477-86.
88. Sharma NK, Das SK, Mondal AK et al. (2008) Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects. J Clin Endocrinol Metab 93:4532-41.
89. Sundar-Rajan S, Srinivasan V, Balasubramanyam M et al. (2007)Endoplasmic reticulum (ER) stress & diabetes. Indian J Med Res 125:411-24.
90. Szabo G, Mandrekar P, Dolganiuc A. (2007) Innate immune response and hepatic inflammation. Semin Liver Dis 27:339-50.
91. Tagami S, Inokuchi Ji J, Kabayama K et al. (2002) Ganglioside GM3 participates in the pathological conditions of insulin resistance.J Biol Chem 277:3085-92.
92. Teruel T, Hernandez R, Lorenzo M. (2001) Ceramide mediates insulin resistance by tumor necrosis factor-alpha in brown adipocytes by maintaining Akt in an inactive dephosphorylated state.Diabetes 50:2563-71.
93. Tong M, Neusner A, Longato L et al. (2009) Nitrosamine exposure causes insulin resistance diseases: relevance to type 2 diabetes mellitus, non-alcoholic steatohepatitis, and Alzheimer's disease.J Alzheimers Dis 17:827-44.
94. Turinsky J, O'Sullivan DM, Bayly BP. (1990) 1,2-Diacylglycerol and ceramide levels in insulin-resistant tissues of the rat in vivo.J Biol Chem 265:16880-5.
95. Urano F, Bertolotti A, Ron D. (2000) IRE1 and efferent signaling from the endoplasmic reticulum. J Cell Sci 113(Pt 21):3697-702.
96. Vidali M, Stewart SF, Albano E. (2008) Interplay between oxidative stress and immunity in the progression of alcohol-mediated liver injury. Trends Mol Med 14:63-71.
97. Werstuck GH, Lentz SR, Dayal S et al. (2001) Homocysteineinduced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Invest 107:1263-73.
98. Xu J, Yeon JE, Chang H et al. (2003) Ethanol impairs insulinstimulated neuronal survival in the developing brain: role of PTEN phosphatase. J Biol Chem 278:26929-37.
99. Yamashita T, Hashiramoto A, Haluzik M et al. (2003) Enhanced insulin sensitivity in mice lacking ganglioside GM3. Proc Natl Acad Sci USA 100:3445-9.
100. Yang G, Badeanlou L, Bielawski J et al. (2009) Central role of ceramide biosynthesis in body weight regulation, energy metabolism,and the metabolic syndrome. Am J Physiol Endocrinol Metab 297:E211-24.
101. Yao XH, Chen L, Nyomba BL. (2006) Adult rats prenatally exposed to ethanol have increased gluconeogenesis and impaired insulin response of hepatic gluconeogenic genes. J Appl Physiol 100:642-48.
102. Yeon JE, Califano S, Xu J et al. (2003) Potential role of PTEN phosphatase in ethanol-impaired survival signaling in the liver.Hepatology 38:703-14.
103. Zeremski M, Petrovic LM, Talal AH. (2007) The role of chemokines as inflammatory mediators in chronic hepatitis C virus infection.J Viral Hepat 14:675-87.