S-adenosylmethionine prevents chronic alcohol-induced mitochondrial dysfunction in the rat liver

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 291, Issue 5, 2006, Pages

  Bailey, Shannon M ^a   Robinson, Gloria ^a   Pinner, Anita ^a   Chamlee, Laura ^a   Ulasova, Elena ^b   Pompilius, Melissa ^b   Page, Grier P ^a   Chhieng, David ^b   Jhala, Nirag ^b   Landar, Aimee ^b   Kharbanda, Kusum K ^c   Ballinger, Scott ^b   Darley Usmar, Victor ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c VA Alcohol Research Center   (United States)

Author keywords

Blue native gel electrophoresis; Cytochrome c oxidase; Mitochondrial DNA; Oxidative stress; Prohibitin; Proteome

Indexed keywords

ALCOHOL; CHAPERONE; CYTOCHROME C OXIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; S ADENOSYLMETHIONINE; SUPEROXIDE;

ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; ENZYME INDUCTION; FATTY LIVER; GENOME; IMMUNOBLOTTING; LIVER MITOCHONDRION; MALE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; RAT; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CYTOCHROME P-450 CYP2E1; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LIVER; LIVER DISEASES, ALCOHOLIC; LIVER FUNCTION TESTS; MALE; MITOCHONDRIA, LIVER; MOLECULAR CHAPERONES; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S-ADENOSYLMETHIONINE;

EID: 33751082953     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00044.2006     Document Type: Article

References (80)

1. Agrimi G, Di Noia MA, Marobbio CM, Fiermonte G, Lasorsa FM, and Palmieri F. Identification of the human mitochondrial S-adenosylmethionine transporter: bacterial expression, reconstitution, functional characterization and tissue distribution. Biochem J 379: 183-190, 2004.
2. Arteel GE, Iimuro Y, Yin M, Raleigh JA, and Thurman RG. Chronic enteral ethanol treatment causes hypoxia in rat liver tissue in vivo. Hepatology 25: 920-926, 1997.
3. Arteel GE, Raleigh JA, Bradford BU, and Thurman RG. Acute alcohol produces hypoxia directly in rat liver tissue in vivo: role of Kupffer cells. Am J Physiol Gastrointest Liver Physiol 271: G494-G500, 1996.
4. Bailey SM and Cunningham CC. Acute and chronic ethanol increases reactive oxygen species generation and decreases viability in fresh, isolated rat hepatocytes. Hepatology 28: 1318-1326, 1998.
5. Bailey SM and Cunningham CC. Contribution of mitochondria to oxidative stress associated with alcoholic liver disease. Free Radic Biol Med 32: 11-16, 2002.
6. Bailey SM, Patel VB, Young TA, Asayama K, and Cunningham CC. Chronic ethanol consumption alters the glutathione/glutathione peroxidase-1 system and protein oxidation status in rat liver. Alcohol Clin Exp Res 25: 726-733, 2001.
7. Barak AJ, Beckenhauer HC, Badakhsh S, and Tuma DJ. The effect of betaine in reversing alcoholic steatosis. Alcohol Clin Exp Res 21: 1100-1102, 1997.
8. Barak AJ, Beckenhauer HC, Mailliard ME, Kharbanda KK, and Tuma DJ. Betaine lowers elevated S-adenosylhomocysteine levels in hepatocytes from ethanol-fed rats. J Nutr 133: 2845-2848, 2003.
9. Bedford MT and Richard S. Arginine methylation an emerging regulator of protein function. Mol Cell 18: 263-272, 2005.
10. Brookes PS, Kraus DW, Shiva S, Doeller JE, Barone MC, Patel RP, Lancaster JR Jr, and Darley-Usmar V. Control of mitochondrial respiration by NO*, effects of low oxygen and respiratory state. J Biol Chem 278: 31603-31609, 2003.
11. Brookes PS, Pinner A, Ramachandran A, Coward L, Barnes S, Kim H, and Darley-Usmar VM. High throughput two-dimensional blue-native electrophoresis: a tool for functional proteomics of mitochondria and signaling complexes. Proteomics 2: 969-977, 2002.
12. Cahill A, Baio DL, Ivester PI, and Cunningham CC. Differential effects of chronic ethanol consumption on hepatic mitochondrial and cytoplasmic ribosomes. Alcohol Clin Exp Res 20: 1362-1367, 1996.
13. Cahill A and Cunningham CC. Effects of chronic ethanol feeding on the protein composition of mitochondrial ribosomes. Electrophoresis 21: 3420-3426, 2000.
14. Cahill A, Wang X, and Hoek JB. Increased oxidative damage to mitochondrial DNA following chronic ethanol consumption. Biochem Biophys Res Commun 235: 286-290, 1997.
15. Caro AA and Cederbaum AI. Inhibition of CYP2E1 catalytic activity in vitro by S-adenosyl-L-methionine. Biochem Pharmacol 69: 1081-1093, 2005.
16. Carroll J, Fearnley IM, Skehel JM, Runswick MJ, Shannon RJ, Hirst J, and Walker JE. The post-translational modifications of the nuclear encoded subunits of complex I from bovine heart mitochondria. Mol Cell Proteomics 4: 693-699, 2005.
17. Chandel NS, Budinger GR, Choe SH, and Schumacker PT. Cellular respiration during hypoxia. Role of cytochrome oxidase as the oxygen sensor in hepatocytes. J Biol Chem 272: 18808-18816, 1997.
18. Chen R, Fearnley IM, Palmer DN, and Walker JE. Lysine 43 is trimethylated in subunit C from bovine mitochondrial ATP synthase and in storage bodies associated with batten disease. J Biol Chem 279: 21883-21887, 2004.
19. Coates PJ, Nenutil R, McGregor A, Picksley SM, Crouch DH, Hall PA, and Wright EG. Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp Cell Res 265: 262-273, 2001.
20. Coleman WB and Cunningham CC. Effects of chronic ethanol consumption on the synthesis of polypeptides encoded by the hepatic mitochondrial genome. Biochim Biophys Acta 1019: 142-150, 1990.
21. Cunningham CC, Coleman WB, and Spach PI. The effects of chronic ethanol consumption on hepatic mitochondrial energy metabolism. Alcohol Alcohol 25: 127-136, 1990.
22. Deaciuc IV, Fortunato F, D'Souza NB, Hill DB, Schmidt J, Lee EY, and McClain CJ. Modulation of capase-3 activity and Fas ligand mRNA expression in rat liver cells in vivo by alcohol and lipopolysaccharide. Alcohol Clin Exp Res 23: 349-356, 1999.
23. Dickinson DA, Moellering DR, Iles KE, Patel RP, Levonen AL, Wigley A, Darley-Usmar VM, and Forman HJ. Cytoprotection against oxidative stress and the regulation of glutathione synthesis. Biol Chem 384: 527-537, 2003.
24. Duce AM, Ortiz P, Cabrero C, and Mato JM. S-adenosyl-L-methionine synthetase and phospholipid methyltransferase are inhibited in human cirrhosis. Hepatology 8: 65-68, 1988.
25. Fernandez-Checa JC, Colell A, and Garcia-Ruiz C. S-adenosyl-L-methionine and mitochondrial reduced glutathione depletion in alcoholic liver disease. Alcohol 27: 179-183, 2002.
26. Fu W, Dudman NP, Perry MA, Young K, and Wang XL. Interrelations between plasma homocysteine and intracellular S-adenosylhomocysteine. Biochem Biophys Res Commun 271: 47-53, 2000.
27. Garcia-Ruiz C, Morales A, Colell A, Ballesta A, Rodes J, Kaplowitz N, and Fernandez-Checa JC. Feeding S-adenosyl-L-methionine attenuates both ethanol-induced depletion of mitochondrial glutathione and mitochondrial dysfunction in periportal and perivenous rat hepatocytes. Hepatology 21: 207-214, 1995.
28. Halsted CH, Villanueva JA, Devlin AM, Niemela O, Parkkila S, Garrow TA, Wallock LM, Shigenaga MK, Melnyk S, and James SJ. Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig. Proc Natl Acad Sci USA 99: 10072-10077, 2002.
29. He L and Lemasters JJ. Heat shock suppresses the permeability transition in rat liver mitochondria. J Biol Chem 278: 16755-16760, 2003.
30. Helm M, Brule H, Degoul F, Cepanec C, Leroux JP, Giege R, and Florentz C. The presence of modified nucleotides is required for clover-leaf folding of a human mitochondrial tRNA. Nucleic Acids Res 26: 1636-1643, 1998.
31. Hines IN and Wheeler MD. Recent advances in alcoholic liver disease. III. Role of the innate immune response in alcoholic hepatitis. Am J Physiol Gastrointest Liver Physiol 287: G310-G314, 2004.
32. Ivester P, Lide MJ, and Cunningham CC. Effect of chronic ethanol consumption on the energy state and structural stability of periportal and perivenous hepatocytes. Arch Biochem Biophys 322: 14-21, 1995.
33. Ji C and Kaplowitz N. Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 124: 1488-1499, 2003.
34. Kessova I and Cederbaum AI. CYP2E1: biochemistry, toxicology, regulation and function in ethanol-induced liver injury. Curr Mol Med 3: 509-518, 2003.
35. Kharbanda KK, Rogers DD, 2nd Mailliard ME, Siford GL, Barak AJ, Beckenhauer HC, Sorrell MF, and Tuma DJ. A comparison of the effects of betaine and S-adenosylmethionine on ethanol-induced changes in methionine metabolism and steatosis in rat hepatocytes. J Nutr 135: 519-524, 2005.
36. Kim JS, He L, and Lemasters JJ. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 304: 463-470, 2003.
37. Kleinert H, Pautz A, Linker K, and Schwarz PM. Regulation of the expression of inducible nitric oxide synthase. Eur J Pharmacol 500: 255-266, 2004.
38. Knight-Lozano CA, Young CG, Burow DL, Hu ZY, Uyeminami D, Pinkerton KE, Ischiropoulos H, and Ballinger SW. Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues. Circulation 105: 849-854, 2002.
39. Lieber CS. S-adenosyl-L-methionine and alcoholic liver disease in animal models: implications for early intervention in human beings. Alcohol 27: 173-177, 2002.
40. Lieber CS, Casini A, DeCarli LM, Kim CI, Lowe N, Sasaki R, and Leo MA. S-adenosyl-L-methionine attenuates alcohol-induced liver injury in the baboon. Hepatology 11: 165-172, 1990.
41. Lieber CS, Robins SJ, and Leo MA. Hepatic phosphatidylethanolamine methyltransferase activity is decreased by ethanol and increased by phosphatidylcholine. Alcohol Clin Exp Res 18: 592-595, 1994.
42. Lu SC, Huang ZZ, Yang H, Mato JM, Avila MA, and Tsukamoto H. Changes in methionine adenosyltransferase and S-adenosylmethionine homeostasis in alcoholic rat liver. Am J Physiol Gastrointest Liver Physiol 279: G178-G185, 2000.
43. Lu SC, Huang ZZ, Yang JM, and Tsukamoto H. Effect of ethanol and high-fat feeding on hepatic gamma-glutamylcysteine synthetase subunit expression in the rat. Hepatology 30: 209-214, 1999.
44. Majano PL, Garcia-Monzon C, Garcia-Trevijano ER, Corrales FJ, Camara J, Ortiz P, Mato JM, Avila MA, and Moreno-Otero R. S-adenosylmethionine modulates inducible nitric oxide synthase gene expression in rat liver and isolated hepatocytes. J Hepatol 35: 692-699, 2001.
45. Mari M and Cederbaum AI. CYP2E1 overexpression in HepG2 cells induces glutathione synthesis by transcriptional activation of gamma-glutamylcysteine synthetase. J Biol Chem 275: 15563-15571, 2000.
46. Martinez-Chantar ML, Corrales FJ, Martinez-Cruz LA, Garcia-Trevijano ER, Huang ZZ, Chen L, Kanel G, Avila MA, Mato JM, and Lu SC. Spontaneous oxidative stress and liver tumors in mice lacking methionine adenosyltransferase 1A. FASEB J 16: 1292-1294, 2002.
47. Mato JM, Alvarez L, Ortiz P, and Pajares MA. S-adenosylmethionine synthesis: molecular mechanisms and clinical implications. Pharmacol Ther 73: 265-280, 1997.
48. Mato JM, Camara J, Fernandez de Paz J, Caballeria L, Coll S, Caballero A, Garcia-Buey L, Beltran J, Benita V, Caballeria J, Sola R, Moreno-Otero R, Barrao F, Martin-Duce A, Correa JA, Pares A, Barrao E, Garcia-Magaz I, Puerta JL, Moreno J, Boissard G, Ortiz P, and Rodes J. S-adenosylmethionine in alcoholic liver cirrhosis: a randomized, placebo-controlled, double-blind, multicenter clinical trial. J Hepatol 30: 1081-1089, 1999.
49. McKim SE, Gabele E, Isayama F, Lambert JC, Tucker LM, Wheeler MD, Connor HD, Mason RP, Doll MA, Hein DW, and Arteel GE. Inducible nitric oxide synthase is required in alcohol-induced liver injury: studies with knockout mice. Gastroenterology 125: 1834-1844, 2003.
50. Mishra S, Murphy LC, Nyomba BL, and Murphy LJ. Prohibitin: a potential target for new therapeutics. Trends Mol Med 11: 192-197, 2005.
51. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, and Grivell LA. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19: 2444-2451, 2000.
52. Noga AA, Zhao Y, and Vance DE. An unexpected requirement for phosphatidylethanolamine N-methyltransferase in the secretion of very low density lipoproteins. J Biol Chem 277: 42358-42365, 2002.
53. Oh SI, Kim CI, Chun HJ, and Park SC. Chronic ethanol consumption affects glutathione status in rat liver. J Nutr 128: 758-763, 1998.
54. Patel VB and Cunningham CC. Altered hepatic mitochondrial ribosome structure following chronic ethanol consumption. Arch Biochem Biophys 398: 41-50, 2002.
55. Prudova A, Bauman Z, Braun A, Vitvitsky V, Lu SC, and Banerjee R. S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity. Proc Natl Acad Sci USA 103: 6489-6494, 2006.
56. Pryor WA, Houk KN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, and Davies KJ. Free radical biology and medicine: it's a gas, man! Am J Physiol Regul Integr Comp Physiol 291: R491-R511, 2006.
57. Puzziferri I, Signorile A, Guerrieri F, Papa S, Cuomo V, and Steardo L. Chronic low dose ethanol intake: biochemical characterization of liver mitochondria in rats. Life Sci 66: 477-484, 2000.
58. Radi R, Cassina A, Hodara R, Quijano C, and Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33: 1451-1464, 2002.
59. Santamaria E, Avila MA, Latasa MU, Rubio A, Martin-Duce A, Lu SC, Mato JM, and Corrales FJ. Functional proteomics of nonalcoholic steatohepatitis: mitochondrial proteins as targets of S-adenosylmethionine. Proc Natl Acad Sci USA 100: 3065-3070, 2003.
60. Sastre J, Minana JB, Alguacil P, Malet G, Gomez-Cambronero L, Marin JA, Vina JR, and Vina J. Chronic ethanol feeding causes oxidative stress in rat liver mitochondria. Prevention by S-adenosyl methionine. Free Radic Res 30: 325-327, 1999.
61. Seidel-Rogol BL, McCulloch V, and Shadel GS. Human mitochondrial transcription factor B1 methylates ribosomal RNA at a conserved stem-loop. Nat Genet 33: 23-24, 2003.
62. Shadel GS. Coupling the mitochondrial transcription machinery to human disease. Trends Genet 20: 513-519, 2004.
63. Shepherd JA and Garland GP. Citrate synthase from rat liver. Methods Enzymol 13: 11-19, 1969.
64. Shiva S, Oh JY, Landar AL, Ulasova E, Venkatraman A, Bailey SM, and Darley-Usmar VM. Nitroxia: the pathological consequence of dysfunction in the nitric oxide-cytochrome c oxidase signaling pathway. Free Radic Biol Med 38: 297-306, 2005.
65. 2) receptor. Biochim Biophys Acta 1743: 205-213, 2005.
66. Song Z, Zhou Z, Chen T, Hill D, Kang J, Barve S, and McClain C. S-adenosylmethionine (SAMe) protects against acute alcohol induced hepatotoxicity in mice. J Nutr Biochem 14: 591-597, 2003.
67. Spach PI, Bottenus RE, and Cunningham CC. Control of adenine nucleotide metabolism in hepatic mitochondria from rats with ethanol-induced fatty liver. Biochem J 202: 445-452, 1982.
68. Stipanuk MH, Dominy JE Jr, Lee JI, and Coloso RM. Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J Nutr 136: 1652S-1659S, 2006.
69. Sykora P and Cahill A. Effects of AdoMet upon ethanol-elicited lesions of the 55S mitochondrial ribosome and the electron transport chain (Abstract). Alcohol Clin Exp Res 29: 123A, 2005.
70. Tarpey MM and Fridovich I. Methods of detection of vascular reactive species: nitric oxide, superoxide, hydrogen peroxide, and peroxynitrite. Circ Res 89: 224-236, 2001.
71. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE, and Thomas K. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 142: 4076-4085, 2001.
72. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27: 502-522, 1969.
73. Vargiu C, Belliardo S, Cravanzola C, Grillo MA, and Colombatto S. Oxygen regulation of rat hepatocyte iNOS gene expression. J Hepatol 32: 567-573, 2000.
74. Veal N, Hsieh CL, Xiong S, Mato JM, Lu S, and Tsukamoto H. Inhibition of lipopolysaccharide-stimulated TNF-alpha promoter activity by S-adenosylmethionine and 5′-methylthioadenosine. Am J Physiol Gastrointest Liver Physiol 287: G352-G362, 2004.
75. Venkatraman A, Landar A, Davis AJ, Chamlee L, Sanderson T, Kim H, Page G, Pompilius M, Ballinger S, Darley-Usmar V, and Bailey SM. Modification of the mitochondrial proteome in response to the stress of ethanol-dependent hepatotoxicity. J Biol Chem 279: 22092-22101, 2004.
76. Venkatraman A, Landar A, Davis AJ, Ulasova E, Page G, Murphy MP, Darley-Usmar V, and Bailey SM. Oxidative modification of hepatic mitochondria protein thiols: effect of chronic alcohol consumption. Am J Physiol Gastrointest Liver Physiol 286: G521-G527, 2004.
77. Venkatraman A, Shiva S, Davis AJ, Bailey SM, Brookes PS, and Darley-Usmar V. Chronic alcohol consumption increases the senstivity of rat liver mitochondrial respiration to inhibition by nitric oxide. Hepatology 38: 141-147, 2003.
78. Venkatraman A, Shiva S, Wigley A, Ulasova E, Chhieng D, Bailey SM, and Darley-Usmar V. The role of iNOS in alcohol-dependent hepatoxicity and mitochondrial dysfunction. Hepatology 40: 565-573, 2004.
79. Vijayasarathy C, Damle S, Prabu SK, Otto CM, and Avadhani NG. Adaptive changes in the expression of nuclear and mitochondrial encoded subunits of cytochrome c oxidase and the catalytic activity during hypoxia. Eur J Biochem 270: 871-879, 2003.
80. Wharton DC and Tzagoloff A. Cytochrome oxidase from beef heart mitochondria. Methods Enzymol 10: 245-250, 1967.