Nitric oxide and hypoxia exacerbate alcohol-induced mitochondrial dysfunction in hepatocytes

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 12, 2011, Pages 1573-1582

  Zelickson, Blake R ^a,b   Benavides, Gloria A ^a,b   Johnson, Michelle S ^a,b   Chacko, Balu K ^a,b   Venkatraman, Aparna ^a,b,c   Landar, Aimee ^a,b   Betancourt, Angela M ^a   Bailey, Shannon M ^a   Darley Usmar, Victor M ^a,b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Bioenergetic; Ethanol; Inducible nitric oxide synthase; Reserve capacity

Indexed keywords

ALCOHOL; CYTOCHROME C OXIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ALCOHOL CONSUMPTION; ALCOHOL LIVER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HYPOXIA; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LIVER CELL; LIVER MITOCHONDRION; LIVER TOXICITY; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT;

ANIMALS; ANOXIA; CELL RESPIRATION; DIET; ENERGY METABOLISM; ETHANOL; HEPATOCYTES; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY;

MUS; RATTUS;

EID: 81155148125     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.09.011     Document Type: Article

References (60)

1. B.G. Hill, B.P. Dranka, S. Bailey, J. Lancaster, V. Darley-Usmar, What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology, J Biol Chem.
2. J.D. Erusalimsky, and S. Moncada Nitric oxide and mitochondrial signaling: from physiology to pathophysiology Arterioscler. Thromb. Vasc. Biol. 27 2007 2524 2531 (Pubitemid 350158901)
3. J. Mateo, M. Garcia-Lecea, S. Cadenas, C. Hernandez, and S. Moncada Regulation of hypoxia-inducible factor-1alpha by nitric oxide through mitochondria-dependent and -independent pathways Biochem. J. 376 2003 537 544 (Pubitemid 38010539)
4. S. Moncada, and E.A. Higgs The discovery of nitric oxide and its role in vascular biology Br. J. Pharmacol. 147 Suppl 1 2006 S193 S201
5. W. Xu, I.G. Charles, and S. Moncada Nitric oxide: orchestrating hypoxia regulation through mitochondrial respiration and the endoplasmic reticulum stress response Cell Res 15 2005 63 65 (Pubitemid 41653968)
6. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87 2007 315 424 (Pubitemid 46217686)
7. S. Shiva, J.Y. Oh, A.L. Landar, E. Ulasova, A. Venkatraman, S.M. Bailey, and V.M. Darley-Usmar Nitroxia: the pathological consequence of dysfunction in the nitric oxide-cytochrome c oxidase signaling pathway Free Radic. Biol. Med. 38 2005 297 306 (Pubitemid 40075573)
8. R. Radi, A. Cassina, R. Hodara, C. Quijano, and L. Castro Peroxynitrite reactions and formation in mitochondria Free Radic. Biol. Med. 33 2002 1451 1464 (Pubitemid 35351588)
9. G.E. Arteel, M.B. Kadiiska, I. Rusyn, B.U. Bradford, R.P. Mason, J.A. Raleigh, and R.G. Thurman Oxidative stress occurs in perfused rat liver at low oxygen tension by mechanisms involving peroxynitrite Mol. Pharmacol. 55 1999 708 715 (Pubitemid 29165436)
10. S.E. McKim, E. Gabele, F. Isayama, J.C. Lambert, L.M. Tucker, M.D. Wheeler, H.D. Connor, R.P. Mason, M.A. Doll, D.W. Hein, and G.E. Arteel Inducible nitric oxide synthase is required in alcohol-induced liver injury: studies with knockout mice Gastroenterology 125 2003 1834 1844 (Pubitemid 37500447)
11. E. Baraona, G.A. Zeballos, L. Shoichet, K.M. Mak, and C.S. Lieber Ethanol consumption increases nitric oxide production in rats, and its peroxynitrite-mediated toxicity is attenuated by polyenylphosphatidylcholine Alcohol. Clin. Exp. Res. 26 2002 883 889 (Pubitemid 34666149)
12. A. Venkatraman, S. Shiva, A. Wigley, E. Ulasova, D. Chhieng, S.M. Bailey, and V.M. Darley-Usmar The role of iNOS in alcohol-dependent hepatotoxicity and mitochondrial dysfunction in mice Hepatology 40 2004 565 573 (Pubitemid 39265577)
13. A. Venkatraman, A. Landar, A.J. Davis, E. Ulasova, G. Page, M.P. Murphy, V. Darley-Usmar, and S.M. Bailey Oxidative modification of hepatic mitochondria protein thiols: effect of chronic alcohol consumption Am. J. Physiol. Gastrointest. Liver Physiol. 286 2004 G521 G527
14. C.S. Lieber Alcoholic fatty liver: its pathogenesis and mechanism of progression to inflammation and fibrosis Alcohol 34 2004 9 19 (Pubitemid 40163989)
15. A. Venkatraman, S. Shiva, A.J. Davis, S.M. Bailey, P.S. Brookes, and V.M. Darley-Usmar Chronic alcohol consumption increases the sensitivity of rat liver mitochondrial respiration to inhibition by nitric oxide Hepatology 38 2003 141 147 (Pubitemid 36775805)
16. P.S. Brookes, D.W. Kraus, S. Shiva, J.E. Doeller, M.C. Barone, R.P. Patel, J.R. Lancaster Jr., and V. Darley-Usmar Control of mitochondrial respiration by NO*, effects of low oxygen and respiratory state J. Biol. Chem. 278 2003 31603 31609 (Pubitemid 37048338)
17. D.D. Thomas, X. Liu, S.P. Kantrow, and J.R. Lancaster Jr. The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2 Proc. Natl. Acad. Sci. U. S. A. 98 2001 355 360
18. J.H. Lee, E.S. Yang, and J.W. Park Inactivation of NADP+-dependent isocitrate dehydrogenase by peroxynitrite. Implications for cytotoxicity and alcohol-induced liver injury J. Biol. Chem. 278 2003 51360 51371 (Pubitemid 38020375)
19. B.K. Chacko, A. Srivastava, M.S. Johnson, G.A. Benavides, M.J. Chang, Y. Ye, N. Jhala, M.P. Murphy, B. Kalyanaraman, and V.M. Darley-Usmar Mitochondria-targeted ubiquinone (MitoQ) decreases ethanol-dependent micro and macro hepatosteatosis Hepatology 54 2011 153 163
20. E. Cadenas Mitochondrial free radical production and cell signaling Mol. Aspects Med. 25 2004 17 26 (Pubitemid 38401928)
21. N.S. Chandel Mitochondrial regulation of oxygen sensing Adv. Exp. Med. Biol. 661 2010 339 354
22. A. Venkatraman, A. Landar, A.J. Davis, L. Chamlee, T. Sanderson, H. Kim, G. Page, M. Pompilius, S. Ballinger, V. Darley-Usmar, and S.M. Bailey Modification of the mitochondrial proteome in response to the stress of ethanol-dependent hepatotoxicity J. Biol. Chem. 279 2004 22092 22101 (Pubitemid 38679401)
23. P. Ivester, M.J. Lide, and C.C. Cunningham Effect of chronic ethanol consumption on the energy state and structural stability of periportal and perivenous hepatocytes Arch. Biochem. Biophys. 322 1995 14 21
24. D.L. Baio, C.N. Czyz, C.G. Van Horn, P. Ivester, and C.C. Cunningham Effect of chronic ethanol consumption on respiratory and glycolytic activities of rat periportal and perivenous hepatocytes Arch. Biochem. Biophys. 350 1998 193 200 (Pubitemid 28368644)
25. T.A. Young, S.M. Bailey, C.G. Van Horn, and C.C. Cunningham Chronic ethanol consumption decreases mitochondrial and glycolytic production of ATP in liver Alcohol Alcohol 41 2006 254 260
26. S.M. Bailey, and C.C. Cunningham Effect of dietary fat on chronic ethanol-induced oxidative stress in hepatocytes Alcohol. Clin. Exp. Res. 23 1999 1210 1218 (Pubitemid 29352809)
27. B.G. Hill, A.N. Higdon, B.P. Dranka, and V.M. Darley-Usmar Regulation of vascular smooth muscle cell bioenergetic function by protein glutathiolation Biochim. Biophys. Acta 1797 2 2010 285 295
28. B.G. Hill, B.P. Dranka, L. Zou, J.C. Chatham, and V.M. Darley-Usmar Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal Biochem. J. 424 2009 99 107
29. B.P. Dranka, B.G. Hill, and V.M. Darley-Usmar Mitochondrial reserve capacity in endothelial cells: the impact of nitric oxide and reactive oxygen species Free Radic. Biol. Med. 48 2010 905 914
30. D.G. Nicholls Spare respiratory capacity, oxidative stress and excitotoxicity Biochem. Soc. Trans. 37 2009 1385 1388
31. S.M. Bailey A review of the role of reactive oxygen and nitrogen species in alcohol-induced mitochondrial dysfunction Free. Radic. Res. 37 2003 585 596 (Pubitemid 36603668)
32. S. Shiva, D. Moellering, A. Ramachandran, A.L. Levonen, A. Landar, A. Venkatraman, E. Ceaser, E. Ulasova, J.H. Crawford, P.S. Brookes, R.P. Patel, and V.M. Darley-Usmar Redox signalling: from nitric oxide to oxidized lipids Biochem. Soc. Symp. 2004 107 120 (Pubitemid 41185480)
33. G.L. Wang, B.H. Jiang, E.A. Rue, and G.L. Semenza Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension Proc. Natl. Acad. Sci. U. S. A. 92 1995 5510 5514
34. G.E. Arteel, R.G. Thurman, and J.A. Raleigh Reductive metabolism of the hypoxia marker pimonidazole is regulated by oxygen tension independent of the pyridine nucleotide redox state Eur. J. Biochem. 253 1998 743 750 (Pubitemid 28223543)
35. S. Shiva, P.S. Brookes, and V.M. Darley-Usmar Methods for measuring the regulation of respiration by nitric oxide Methods Cell Biol. 80 2007 395 416
36. V.S. Hollis, M. Palacios-Callender, R.J. Springett, D.T. Delpy, and S. Moncada Monitoring cytochrome redox changes in the mitochondria of intact cells using multi-wavelength visible light spectroscopy Biochim. Biophys. Acta 1607 2003 191 202 (Pubitemid 37500845)
37. G.C. Brown Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase Biochim. Biophys. Acta 1504 2001 46 57 (Pubitemid 32179657)
38. L.K. Keefer, R.W. Nims, K.M. Davies, and D.A. Wink "NONOates" (1-substituted diazen-1-ium-1,2-diolates) as nitric oxide donors: convenient nitric oxide dosage forms Methods Enzymol. 268 1996 281 293 (Pubitemid 26286370)
39. R.D. Curran, T.R. Billiar, D.J. Stuehr, K. Hofmann, and R.L. Simmons Hepatocytes produce nitrogen oxides from L-arginine in response to inflammatory products of Kupffer cells J. Exp. Med. 170 1989 1769 1774 (Pubitemid 19284575)
40. T.R. Billiar, R.D. Curran, M.A. West, K. Hofmann, and R.L. Simmons Kupffer cell cytotoxicity to hepatocytes in coculture requires L-arginine Arch. Surg. 124 1989 1416 1420
41. discussion 1420-1411.
42. B.J. Song, K.H. Moon, N.U. Olsson, and N. Salem Jr. Prevention of alcoholic fatty liver and mitochondrial dysfunction in the rat by long-chain polyunsaturated fatty acids J. Hepatol. 49 2008 262 273
43. T. Hagen, C.T. Taylor, F. Lam, and S. Moncada Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha Science 302 2003 1975 1978 (Pubitemid 37523507)
44. M. Tsutsumi, J.M. Lasker, M. Shimizu, A.S. Rosman, and C.S. Lieber The intralobular distribution of ethanol-inducible P450IIE1 in rat and human liver Hepatology 10 1989 437 446
45. H. Yamazaki, K. Nishiguchi, K. Inoue, T. Yasuyama, and S. Nakanishi Intralobular distribution of rat liver aldehyde dehydrogenase and alcohol dehydrogenase Int. J. Biochem. 20 1988 435 437
46. A. Cahill, C.C. Cunningham, M. Adachi, H. Ishii, S.M. Bailey, B. Fromenty, and A. Davies Effects of alcohol and oxidative stress on liver pathology: the role of the mitochondrion Alcohol. Clin. Exp. Res. 26 2002 907 915 (Pubitemid 34666152)
47. A. Cahill, X. Wang, and J.B. Hoek Increased oxidative damage to mitochondrial DNA following chronic ethanol consumption Biochem. Biophys. Res. Commun. 235 1997 286 290 (Pubitemid 27313697)
48. S.M. Bailey, V.B. Patel, T.A. Young, K. Asayama, and C.C. Cunningham Chronic ethanol consumption alters the glutathione/glutathione peroxidase-1 system and protein oxidation status in rat liver Alcohol. Clin. Exp. Res. 25 2001 726 733 (Pubitemid 32448633)
49. M. Palacios-Callender, M. Quintero, V.S. Hollis, R.J. Springett, and S. Moncada Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 101 2004 7630 7635 (Pubitemid 38658080)
50. C.E. Cooper, and C. Giulivi Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology Am. J. Physiol. Cell Physiol. 292 2007 C1993 C2003
51. M. Quintero, S.L. Colombo, A. Godfrey, and S. Moncada Mitochondria as signaling organelles in the vascular endothelium Proc. Natl. Acad. Sci. U. S. A. 103 2006 5379 5384
52. S.M. Bailey, S.K. Mantena, T. Millender-Swain, Y. Cakir, N.C. Jhala, D. Chhieng, K.E. Pinkerton, and S.W. Ballinger Ethanol and tobacco smoke increase hepatic steatosis and hypoxia in the hypercholesterolemic apoE(-/-) mouse: implications for a "multihit" hypothesis of fatty liver disease Free Radic. Biol. Med. 46 2009 928 938
53. G. Semenza Signal transduction to hypoxia-inducible factor 1 Biochem. Pharmacol. 64 2002 993 998 (Pubitemid 35232274)
54. R.R. Martinez, S. Setty, P. Zong, J.D. Tune, and H.F. Downey Nitric oxide contributes to right coronary vasodilation during systemic hypoxia Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1139 H1146
55. H. Sies Oxygen gradients during hypoxic steady states in liver. Urate oxidase and cytochrome oxidase as intracellular O2 indicators. Hoppe Seylers Z Physiol. Chem. 358 1977 1021 1032 (Pubitemid 8271303)
56. G.E. Arteel, Y. Iimuro, M. Yin, J.A. Raleigh, and R.G. Thurman Chronic enteral ethanol treatment causes hypoxia in rat liver tissue in vivo Hepatology 25 1997 920 926 (Pubitemid 27157135)
57. G.E. Arteel, J.A. Raleigh, B.U. Bradford, and R.G. Thurman Acute alcohol produces hypoxia directly in rat liver tissue in vivo: role of Kupffer cells Am. J. Physiol. 271 1996 G494 G500
58. R.G. Thurman, B.U. Bradford, Y. Iimuro, M.V. Frankenberg, K.T. Knecht, H.D. Connor, Y. Adachi, C. Wall, G.E. Arteel, J.A. Raleigh, D.T. Forman, and R.P. Mason Mechanisms of alcohol-induced hepatotoxicity: studies in rats Front. Biosci. 4 1999 e42 e46
59. M.D. Wheeler, H. Kono, M. Yin, M. Nakagami, T. Uesugi, G.E. Arteel, E. Gabele, I. Rusyn, S. Yamashina, M. Froh, Y. Adachi, Y. Iimuro, B.U. Bradford, O.M. Smutney, H.D. Connor, R.P. Mason, S.M. Goyert, J.M. Peters, F.J. Gonzalez, R.J. Samulski, and R.G. Thurman The role of Kupffer cell oxidant production in early ethanol-induced liver disease Free Radic. Biol. Med. 31 2001 1544 1549 (Pubitemid 34026339)
60. D. Wu, and A.I. Cederbaum Oxidative stress and alcoholic liver disease Semin. Liver Dis. 29 2009 141 154