Regulation of mitochondrial function by voltage dependent anion channels in ethanol metabolism and the Warburg effect

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 6, 2012, Pages 1536-1544

  Lemasters, John J ^a,b   Holmuhamedov, Ekhson L ^c,d   Czerny, Christoph ^e   Zhong, Zhi ^a   Maldonado, Eduardo N ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c AURORA HEALTH CARE   (United States)

^d CENTER FOR THEORETICAL PROBLEMS OF PHYSICOCHEMICAL PHARMACOLOGY   (Russian Federation)

^e GOETHE UNIVERSITY   (Germany)

Author keywords

Acetaldehyde; Glycogen synthase kinase 3 ; Hepatoma; Liver mitochondrion; Protein kinase A; Tubulin

Indexed keywords

ACETALDEHYDE; ACYL COENZYME A; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALCOHOL; ALDEHYDE DEHYDROGENASE; COLCHICINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3BETA; HEXOKINASE; NOCODAZOLE; PROTEIN BCL 2; PROTEIN KINASE C EPSILON; PYRUVIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ROTENONE; TUBULIN; VOLTAGE DEPENDENT ANION CHANNEL;

AEROBIC METABOLISM; ALCOHOL LIVER DISEASE; ALCOHOL METABOLISM; APOPTOSIS; CELL MEMBRANE POTENTIAL; CELL STRAIN HEPG2; CHANNEL GATING; DEPOLARIZATION; DEPOLYMERIZATION; FATTY LIVER; GLYCOLYSIS; HUMAN; HYDROLYSIS; LIVER CELL; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL OUTER MEMBRANE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OUTER MEMBRANE; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; UREA CYCLE; WARBURG PHENOMENON;

ANIMALS; ETHANOL; GLYCOLYSIS; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; NEOPLASMS; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84859763834     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.11.034     Document Type: Review

References (94)

1. K. Adachi, T. Matsuhashi, Y. Nishizawa, J. Usukura, J. Popinigis, T. Wakabayashi, Studies on urea synthesis in the liver of rats treated chronically with ethanol using perfused livers, isolated hepatocytes, and mitochondria, Biochem. Pharmacol. 50 (1995) 1391-1399.
2. M. Adachi, H. Ishii, Role of mitochondria in alcoholic liver injury, Free Radic. Biol. Med. 32 (2002) 487-491. (Pubitemid 34215033)
3. H. Azoulay-Zohar, A. Israelson, S. Abu-Hamad, V. Shoshan-Barmatz, In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death, Biochem. J. 377 (2004) 347-355. (Pubitemid 38142190)
4. C.P. Baines, C.X. Song, Y.T. Zheng, G.W. Wang, J. Zhang, O.L. Wang, Y. Guo, R. Bolli, E.M. Cardwell, P. Ping, Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria, Circ. Res. 92 (2003) 873-880. (Pubitemid 36542528)
5. J. Banerjee, S. Ghosh, Bax increases the pore size of rat brain mitochondrial voltage-dependent anion channel in the presence of tBid, Biochem. Biophys. Res. Commun. 323 (2004) 310-314. (Pubitemid 39206288)
6. K. Bartlett, S. Eaton, Mitochondrial beta-oxidation, Eur. J. Biochem. 271 (2004) 462-469.
7. M. Bayrhuber, T. Meins, M. Habeck, S. Becker, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, K. Zeth, Structure of the human voltage-dependent anion channel, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 15370-15375.
8. A.D. Beavis, H. vatol-Hag, The mitochondrial inner membrane anion channel is inhibited by DIDS, J. Bioenerg. Biomembr. 28 (1996) 207-214. (Pubitemid 126707067)
9. A.K. Bera, S. Ghosh, Dual mode of gating of voltage-dependent anion channel as revealed by phosphorylation, J. Struct. Biol. 135 (2001) 67-72.
10. A.K. Bera, S. Ghosh, S. Das,Mitochondrial VDAC can be phosphorylated by cyclic AMPdependent protein kinase, Biochem. Biophys. Res. Commun. 209 (1995) 213-217.
11. I. Bergheim, C.J. McClain, G.E. Arteel, Treatment of alcoholic liver disease, Dig. Dis. 23 (2005) 275-284. (Pubitemid 43325927)
12. E. Blachly-Dyson, M. Forte, VDAC channels, IUBMB Life 52 (2001) 113-118. (Pubitemid 33731563)
13. S. Bonnet, S.L. Archer, J. Allalunis-Turner, A. Haromy, C. Beaulieu, R. Thompson, C.T. Lee, G.D. Lopaschuk, L. Puttagunta, S. Bonnet, G. Harry, K. Hashimoto, C.J. Porter, M.A. Andrade, B. Thebaud, E.D. Michelakis, A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth, Cancer Cell 11 (2007) 37-51. (Pubitemid 46054520)
14. B.U. Bradford, N. Enomoto, K. Ikejima, M.L. Rose, H.K. Bojes, D.T. Forman, R.G. Thurman, Peroxisomes are involved in the swift increase in alcohol metabolism, J. Pharmacol. Exp. Ther. 288 (1999) 254-259. (Pubitemid 29113498)
15. B.U. Bradford, I. Rusyn, Swift increase in alcoholmetabolism(SIAM): understanding the phenomenon of hypermetabolism in liver, Alcohol 35 (2005) 13-17. (Pubitemid 40726307)
16. B.U. Bradford, I. Rusyn, Swift increase in alcoholmetabolism(SIAM): understanding the phenomenon of hypermetabolism in liver, Alcohol 35 (2005) 13-17. (Pubitemid 40726307)
17. B.R. Brinkley, S.S. Barham, S.C. Barranco, G.M. Fuller, Rotenone inhibition of spindle microtubule assembly in mammalian cells, Exp. Cell Res. 85 (1974) 41-46.
18. E. Bustamante, H.P. Morris, P.L. Pedersen, Energy metabolism of tumor cells. Requirement for a form of hexokinase with a propensity for mitochondrial binding, J. Biol. Chem. 256 (1981) 8699-8704. (Pubitemid 12254812)
19. S. Caldwell, C. Argo, The natural history of non-alcoholic fatty liver disease, Dig. Dis. 28 (2010) 162-168.
20. A.A. Caro, A.I. Cederbaum, Oxidative stress, toxicology, and pharmacology of CYP2E1, Annu. Rev. Pharmacol. Toxicol. 44 (2004) 27-42. (Pubitemid 38263832)
21. M. Cave, K.C. Falkner, M. Ray, S. Joshi-Barve, G. Brock, R. Khan, H.M. Bon, C.J. McClain, Toxicant-associated steatohepatitis in vinyl chloride workers, Hepatology 51 (2010) 474-481.
22. D.J. Chiang, M.T. Pritchard, L.E. Nagy, Obesity, diabetes mellitus, and liver fibrosis, Am. J. Physiol. Gastrointest. Liver Physiol. 300 (2011) G697-G702.
23. M. Colombini, VDAC: the channel at the interface between mitochondria and the cytosol, Mol. Cell. Biochem. 256-257 (2004) 107-115. (Pubitemid 38181239)
24. M. Colombini, VDAC: the channel at the interface between mitochondria and the cytosol, Mol. Cell. Biochem. 256-257 (2004) 107-115. (Pubitemid 38181239)
25. M. Colombini, The published 3D structure of the VDAC channel: native or not? Trends Biochem. Sci. 34 (2009) 382-389.
26. M. Colombini, C.L. Yeung, J. Tung, T. Konig, The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion, Biochim. Biophys. Acta 905 (1987) 279-286. (Pubitemid 18004526)
27. W.J. Craigen, B.H. Graham, Genetic strategies for dissecting mammalian and Drosophila voltage-dependent anion channel functions, J. Bioenerg. Biomembr. 40 (2008) 207-212.
28. S. Das, R.Wong,N. Rajapakse, E.Murphy, C. Steenbergen, Glycogen synthase kinase 3 inhibition slows mitochondrial adenine nucleotide transport and regulates voltagedependent anion channel phosphorylation, Circ. Res. 103 (2008) 983-991.
29. P. De, V.G. Prezioso, F. Thinnes, T.A. Link, F. Palmieri, Peptide-specific antibodies and proteases as probes of the transmembrane topology of the bovine heart mitochondrial porin, Biochemistry 30 (1991) 10191-10200.
30. J.C. Fernandez-Checa, N. Kaplowitz, Hepatic mitochondrial glutathione: transport and role in disease and toxicity, Toxicol. Appl. Pharmacol. 204 (2005) 263-273. (Pubitemid 40545231)
31. S.W. French, N.C. Benson, P.S. Sun, Centrilobular liver necrosis induced by hypoxia in chronic ethanol-fed rats, Hepatology 4 (1984) 912-917. (Pubitemid 14007665)
32. B. Fromenty, S. Grimbert, A. Mansouri, M. Beaugrand, S. Erlinger, A. Rotig, D. Pessayre, Hepatic mitochondrial DNA deletion in alcoholics: association with microvesicular steatosis, Gastroenterology 108 (1995) 193-200.
33. B. Fromenty, D. Pessayre, Inhibition of mitochondrial beta-oxidation as a mechanism of hepatotoxicity, Pharmacol. Ther. 67 (1995) 101-154.
34. L. Galdieri, S.Mehrotra, S. Yu, A. Vancura, Transcriptional regulation in yeast during diauxic shift and stationary phase, OMICS 14 (2010) 629-638.
35. S.S. Gambhir, Molecular imaging of cancer with positron emission tomography, Nat. Rev. Cancer 2 (2002) 683-693. (Pubitemid 37328919)
36. R.A. Gatenby, R.J. Gillies, Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 4 (2004) 891-899. (Pubitemid 39472955)
37. J.F. Geschwind, C.S. Georgiades, Y.H. Ko, P.L. Pedersen, Recently elucidated energy catabolism pathways provide opportunities for novel treatments in hepatocellular carcinoma, Expert Rev. Anticancer Ther. 4 (2004) 449-457. (Pubitemid 38745116)
38. A.J. Harvey, K.L. Kind, J.G. Thompson, REDOX regulation of early embryo development, Reproduction 123 (2002) 479-486. (Pubitemid 34303149)
39. S. Hiller, R.G. Garces, T.J. Malia, V.Y. Orekhov, M. Colombini, G. Wagner, Solution structure of the integral human membrane protein VDAC-1 in detergent micelles, Science 321 (2008) 1206-1210.
40. J.B. Hoek, A. Cahill, J.G. Pastorino, Alcohol and mitochondria: a dysfunctional relationship, Gastroenterology 122 (2002) 2049-2063. (Pubitemid 34651446)
41. E. Holmuhamedov, J.J. Lemasters, Ethanol exposure decreases mitochondrial outer membrane permeability in cultured rat hepatocytes, Arch. Biochem. Biophys. 481 (2009) 226-233.
42. E.L. Holmuhamedov, C. Czerny, C.C. Beeson, J.J. Lemasters, Ethanol Suppresses Ureagenesis in Rat Hepatocytes: Role of Acetaldehyde,, 2011.
43. S.B. Horwitz,Mechanismof action of taxol, Trends Pharmacol. Sci. 13 (1992) 134-136.
44. S.B. Horwitz, L. Lothstein, J.J. Manfredi, W. Mellado, J. Parness, S.N. Roy, P.B. Schiff, L. Sorbara, R. Zeheb, Taxol: mechanisms of action and resistance, Ann. N. Y. Acad. Sci. 466 (1986) 733-744. (Pubitemid 16012884)
45. A.C. Lee, M. Zizi, M. Colombini, Beta-NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6, J. Biol. Chem. 269 (1994) 30974-30980. (Pubitemid 24377586)
46. J.H. Lefkowitch, Morphology of alcoholic liver disease, Clin. Liver Dis. 9 (2005) 37-53. (Pubitemid 40341945)
47. J.J. Lemasters, Modulation of mitochondrial membrane permeability in pathogenesis, autophagy and control of metabolism, J. Gastroenterol. Hepatol. 22 (Suppl 1) (2007) S31-S37. (Pubitemid 46848987)
48. J.J. Lemasters, E. Holmuhamedov, Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box, Biochim. Biophys. Acta 1762 (2006) 181-190. (Pubitemid 43006024)
49. C.S. Lieber, Alcoholic fatty liver: its pathogenesis and mechanism of progression to inflammation and fibrosis, Alcohol 34 (2004) 9-19. (Pubitemid 40163989)
50. Y. Lu, A.I. Cederbaum, CYP2E1 and oxidative liver injury by alcohol, Free Radic. Biol. Med. 44 (2008) 723-738.
51. M.R. Lucey, P. Mathurin, T.R. Morgan, Alcoholic hepatitis, N. Engl. J. Med. 360 (2009) 2758-2769.
52. E.N. Maldonado, J. Patnaik, M.R. Mullins, J.J. Lemasters, Free tubulin modulates mitochondrial membrane potential in cancer cells, Cancer Res. 70 (2010) 10192-10201.
53. S.A. Marchitti, C. Brocker, D. Stagos, V. Vasiliou, Non-P450 aldehyde oxidizing enzymes: the aldehyde dehydrogenase superfamily, Expert Opin. DrugMetab. Toxicol. 4 (2008) 697-720. (Pubitemid 352003194)
54. L.E. Marshall, R.H. Himes, Rotenone inhibition of tubulin self-assembly, Biochim. Biophys. Acta 543 (1978) 590-594. (Pubitemid 9043433)
55. S.P.Mathupala, Y.H. Ko, P.L. Pedersen, Hexokinase-2 bound tomitochondria: cancer's stygian link to the "Warburg effect" and a pivotal target for effective therapy, Semin. Cancer Biol. 19 (2009) 17-24.
56. T. Matsuhashi, M. Karbowski, X. Liu, J. Usukura, M. Wozniak, T. Wakabayashi, Complete suppresion of ethanol-induced formation of megamitochondria by 4-hydroxy-2,2,6,6-tetramethyl-piperidine-1-oxyl (4-OH-TEMPO), Free Radic. Biol. Med. 24 (1998) 139-147. (Pubitemid 28006445)
57. J.H. Mendelson, N.K. Mello, Experimental analysis of drinking behavior of chronic alcoholics, Ann. N. Y. Acad. Sci. 133 (1966) 828-845.
58. E.D. Michelakis, G. Sutendra, P. Dromparis, L. Webster, A. Haromy, E. Niven, C. Maguire, T.L. Gammer, J.R. Mackey, D. Fulton, B. Abdulkarim, M.S. McMurtry, K.C. Petruk, Metabolic modulation of glioblastoma with dichloroacetate, Sci. Transl. Med. 2 (2010) 31ra34.
59. R.A. Nakashima, M.G. Paggi, P.L. Pedersen, Contributions of glycolysis and oxidative phosphorylation to adenosine 5′-triphosphate production in AS-30D hepatoma cells, Cancer Res. 44 (1984) 5702-5706. (Pubitemid 15183582)
60. A.A. Nanji, E.K. Yang, F. Fogt, S.M. Sadrzadeh, A.J. Dannenberg, Medium chain triglycerides and vitamin E reduce the severity of established experimental alcoholic liver disease, J. Pharmacol. Exp. Ther. 277 (1996) 1694-1700. (Pubitemid 27167189)
61. D. Neumann, J. Buckers, L. Kastrup, S.W. Hell, S. Jakobs, Two-color STED microscopy reveals different degrees of colocalization between hexokinase-I and the three human VDAC isoforms, PMC Biophys. 3 (2010) 4.
62. A.L. Nieminen, A.M. Byrne, B. Herman, J.J. Lemasters, Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species, Am. J. Physiol. 272 (1997) C1286-C1294.
63. R.S. O'Shea, S. Dasarathy, A.J. McCullough, Alcoholic liver disease, Hepatology 51 (2010) 307-328.
64. P. Pediaditakis, J.S. Kim, L. He, X. Zhang, L.M. Graves, J.J. Lemasters, Inhibition of the mitochondrial permeability transition by protein kinase A in rat liver mitochondria and hepatocytes, Biochem. J. 431 (2010) 411-421.
65. A.M. Porcelli, A. Ghelli, C. Zanna, P. Pinton, R. Rizzuto, M. Rugolo, pH difference across the outer mitochondrial membrane measured with a green fluorescent protein mutant, Biochem. Biophys. Res. Commun. 326 (2005) 799-804. (Pubitemid 39655990)
66. T.K. Rostovtseva, B. Antonsson, M. Suzuki, R.J. Youle, M. Colombini, S.M. Bezrukov, Bid, but not Bax, regulates VDAC channels, J. Biol. Chem. 279 (2004) 13575-13583. (Pubitemid 38468883)
67. T.K. Rostovtseva, A. Komarov, S.M. Bezrukov, M. Colombini, VDAC channels differentiate between natural metabolites and synthetic molecules, J. Membr. Biol. 187 (2002) 147-156. (Pubitemid 34526479)
68. T.K. Rostovtseva, K.L. Sheldon, E. Hassanzadeh, C. Monge, V. Saks, S.M. Bezrukov, D.L. Sackett, Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 18746-18751.
69. O. Schmidt, N. Pfanner, C. Meisinger, Mitochondrial protein import: from proteomics to functional mechanisms, Nat. Rev. Mol. Cell Biol. 11 (2010) 655-667.
70. G.L. Semenza, HIF-1 mediates the Warburg effect in clear cell renal carcinoma, J. Bioenerg. Biomembr. 39 (2007) 231-234. (Pubitemid 47619375)
71. G. Serviddio, F. Bellanti, G. Vendemiale, E. Altomare, Mitochondrial dysfunction in nonalcoholic steatohepatitis, Expert Rev. Gastroenterol. Hepatol. 5 (2011) 233-244.
72. K.L. Sheldon, E.N. Maldonado, J.J. Lemasters, T. Rostovtseva, S.M. Bezrukov, Phosphorylation of Voltage-Dependent Anion Channel by Serine/Threonine Kinases Governs Its Interaction with Tubulin,, 2011.
73. J.J. Shelmet, G.A. Reichard, C.L. Skutches, R.D. Hoeldtke, O.E. Owen, G. Boden, Ethanol causes acute inhibition of carbohydrate, fat, and protein oxidation and insulin resistance, J. Clin. Invest. 81 (1988) 1137-1145.
74. V. Shoshan-Barmatz, D. Gincel, The voltage-dependent anion channel: characterization, modulation, and role in mitochondrial function in cell life and death, Cell Biochem. Biophys. 39 (2003) 279-292. (Pubitemid 41270796)
75. V. Shoshan-Barmatz, D. Gincel, The voltage-dependent anion channel: characterization, modulation, and role in mitochondrial function in cell life and death, Cell Biochem. Biophys. 39 (2003) 279-292. (Pubitemid 41270796)
76. S.W. Tait, D.R. Green, Mitochondria and cell death: outer membrane permeabilization and beyond, Nat. Rev. Mol. Cell Biol. 11 (2010) 621-632.
77. W. Tan, M. Colombini, VDAC closure increases calcium ion flux, Biochim. Biophys. Acta 1768 (2007) 2510-2515. (Pubitemid 47532032)
78. R.G. Thurman,W.R.McKenna, T.B.McCaffrey, Pathways responsible for the adaptive increase in ethanol utilization following chronic treatment with ethanol: inhibitor studies with the hemoglobin-free perfused rat liver, Mol. Pharmacol. 12 (1976) 156-166.
79. R.G. Thurman, T. Yuki, M.A. Bleyman, G. Wendell, The adaptive increase in ethanol metabolism due to pretreatment with ethanol: a rapid phenomenon, Drug Alcohol Depend. 4 (1979) 119-129. (Pubitemid 9136348)
80. A. Tikunov, C.B. Johnson, P. Pediaditakis, N.Markevich, J.M.Macdonald, J.J. Lemasters, E. Holmuhamedov, Closure of VDAC causes oxidative stress and accelerates the Ca(2+)-induced mitochondrial permeability transition in rat liver mitochondria, Arch. Biochem. Biophys. 495 (2010) 174-181.
81. N. Timohhina, R. Guzun, K. Tepp, C.Monge,M. Varikmaa, H. Vija, P. Sikk, T. Kaambre, D. Sackett, V. Saks, Directmeasurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for mitochondrial interactosome, J. Bioenerg. Biomembr. 41 (2009) 259-275.
82. R. Ujwal, D. Cascio, J.P. Colletier, S. Faham, J. Zhang, L. Toro, P. Ping, J. Abramson, The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 17742-17747.
83. M.G. Vander Heiden, L.C. Cantley, C.B. Thompson, Understanding theWarburg effect: the metabolic requirements of cell proliferation, Science 324 (2009) 1029-1033.
84. M.G. Vander Heiden, N.S. Chandel, X.X. Li, P.T. Schumacker, M. Colombini, C.B. Thompson, Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival, Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4666-4671. (Pubitemid 30238615)
85. M.G. Vander Heiden, N.S. Chandel, X.X. Li, P.T. Schumacker, M. Colombini, C.B. Thompson, Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival, Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4666-4671. (Pubitemid 30238615)
86. M.G. Vander Heiden, X.X. Li, E. Gottleib, R.B. Hill, C.B. Thompson, M. Colombini, Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane, J. Biol. Chem. 276 (2001) 19414-19419.
87. M.G. Vander Heiden, X.X. Li, E. Gottleib, R.B. Hill, C.B. Thompson, M. Colombini, Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane, J. Biol. Chem. 276 (2001) 19414-19419.
88. L. Videla, Y. Israel, Factors thatmodify themetabolismof ethanol in rat liver and adaptive changes produced by its chronic administration, Biochem. J. 118 (1970) 275-281.
89. O. Warburg, Ueber Den Stoffwechsel Der Tumoren, Constable, London, 1930.
90. M. Watford, The urea cycle: a two-compartment system, Essays Biochem. 26 (49-58) (1991) 49-58.
91. C.D. Williams, J. Stengel, M.I. Asike, D.M. Torres, J. Shaw, M. Contreras, C.L. Landt, S.A. Harrison, Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study, Gastroenterology 140 (2011) 124-131.
92. T. Yuki, R.G. Thurman, Swift increase in alcohol metabolism: time course and involvement of glycolysis, Biochem. J. 186 (1980) 119-126.
93. Z. Zhong, V.K. Ramshesh, H. Rehman, J.J. Lemasters, Acute ethanol causes livermitochondrial depolarization in vivo independent of the mitochondrial permeability transition (MPT) and potassium channel opening, Hepatology 46 (Suppl. 1) (2007) 253A-254A.
94. Z. Zhong, V.K. Ramshesh, H. Rehman, J.J. Lemasters, Acute ethanol-induced liver mitochondrial depolarization in vivo is dependent on alcohol dehydrogenase (ADH) and cytochrome-P450 2E1, Toxicol. Sci. 108 (2009) 237.