Defect of mitochondrial respiratory chain is a mechanism of ROS overproduction in a rat model of alcoholic liver disease: Role of zinc deficiency

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 310, Issue 3, 2016, Pages G205-G214

  Sun, Qian ^a   Zhong, Wei ^a   Zhang, Wenliang ^a   Zhou, Zhanxiang ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Alcoholic liver disease; Mitochondrial complex; Ros; Zinc

Indexed keywords

4 HYDROXYNONENAL; ADENOSINE TRIPHOSPHATE; ALCOHOL; FATTY ACID; MITOCHONDRIAL DNA; MITOCHONDRIAL RESPIRATORY COMPLEX I; MITOCHONDRIAL RESPIRATORY COMPLEX III; MITOCHONDRIAL RESPIRATORY COMPLEX IV; MITOCHONDRIAL RESPIRATORY COMPLEX V; MITOCHONDRIAL TRANSCRIPTION FACTOR A; NUCLEAR RESPIRATORY FACTOR 1; OXIDOREDUCTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ZINC;

ALCOHOL LIVER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL RESPIRATION; CONTROLLED STUDY; HEPG2 CELL LINE; LIPID LIVER LEVEL; LIPID STORAGE; LIVER; LIVER MITOCHONDRION; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY CHAIN; ZINC DEFICIENCY; ANIMAL; BIOSYNTHESIS; DEFICIENCY; DRUG EFFECTS; ELECTRON TRANSPORT; HUMAN; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; METABOLISM; TUMOR CELL LINE; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE, TUMOR; ELECTRON TRANSPORT; HUMANS; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; LIVER; LIVER DISEASES, ALCOHOLIC; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, LIVER; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; ZINC;

EID: 84956946670     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00270.2015     Document Type: Article

References (60)

1. Ajmo JM, Liang X, Rogers CQ, Pennock B, You M. Resveratrolalleviates alcoholic fatty liver in mice. Am J Physiol Gastrointest Liver Physiol 295: G833–G842, 2008.
2. Bailey SM, Cunningham CC. Contribution of mitochondria to oxidativestress associated with alcoholic liver disease. Free Radic Biol Med 32:11–16, 2002.
3. Bansal S, Srinivasan S, Anandasadagopan S, Chowdhury AR, Selvaraj V, Kalyanaraman B, Joseph J, Avadhani NG. Additive effects ofmitochondrion-targeted cytochrome CYP2E1 and alcohol toxicity oncytochrome c oxidase function and stability of respirosome complexes. JBiol Chem 287: 15284–15297, 2012.
4. Bayeva M, Gheorghiade M, Ardehali H. Mitochondria as a therapeutictarget in heart failure. J Am Coll Cardiol 61: 599–610, 2013.
5. Bobba A, Amadoro G, Valenti D, Corsetti V, Lassandro R, Atlante A. Mitochondrial respiratory chain Complexes I and IV are impaired bybeta-amyloid via direct interaction and through Complex I-dependent ROSproduction, respectively. Mitochondrion 13: 298–311, 2013.
6. Cahill A, Baio DL, Ivester P, Cunningham CC. Differential effects ofchronic ethanol consumption on hepatic mitochondrial and cytoplasmicribosomes. Alcohol Clin Exp Res 20: 1362–1367, 1996.
7. Cahill A, Wang X, Hoek JB. Increased oxidative damage to mitochondrialDNA following chronic ethanol consumption. Biochem Biophys ResCommun 235: 286–290, 1997.
8. Cai H, Dikalov S, Griendling KK, Harrison DG. Detection of reactiveoxygen species and nitric oxide in vascular cells and tissues: comparisonof sensitivity and specificity. Methods Mol Med 139: 293–311, 2007.
9. Coleman WB, Cunningham CC. Effect of chronic ethanol consumptionon hepatic mitochondrial transcription and translation. Biochim BiophysActa 1058: 178–186, 1991.
10. Coleman WB, Cunningham CC. Effects of chronic ethanol consumptionon the synthesis of polypeptides encoded by the hepatic mitochondrialgenome. Biochim Biophys Acta 1019: 142–150, 1990.
11. De Filippis B, Valenti D, de Bari L, De Rasmo D, Musto M, Fabbri A, Ricceri L, Fiorentini C, Laviola G, Vacca RA. Mitochondrial freeradical overproduction due to respiratory chain impairment in the brain ofa mouse model of Rett syndrome: protective effect of CNF1. Free RadicBiol Med 83: 167–177, 2015.
12. Evans MJ, Scarpulla RC. NRF-1: a trans-activator of nuclear-encodedrespiratory genes in animal cells. Genes Dev 4: 1023–1034, 1990.
13. Feldmann G, Maurice M, Husson JM, Fiessinger JN, Camilleri JP, Benhamou JP, Housset E. Hepatocyte giant mitochondria: an almostconstant lesion in systemic scleroderma. Virchows Arch A Pathol AnatHistol 374: 215–227, 1977.
14. Forman HJ, Kennedy JA. Role of superoxide radical in mitochondrialdehydrogenase reactions. Biochem Biophys Res Commun 60: 1044–1050,1974.
15. Fukada T, Yamasaki S, Nishida K, Murakami M, Hirano T. Zinchomeostasis and signaling in health and diseases: Zinc signaling. J BiolInorg Chem 16: 1123–1134, 2011.
16. Galati D, Srinivasan S, Raza H, Prabu SK, Hardy M, Chandran K, Lopez M, Kalyanaraman B, Avadhani NG. Role of nuclear-encodedsubunit Vb in the assembly and stability of cytochrome c oxidase complex:implications in mitochondrial dysfunction and ROS production. BiochemJ 420: 439–449, 2009.
17. Gao B, Bataller R. Alcoholic liver disease: pathogenesis and new therapeutictargets. Gastroenterology 141: 1572–1585, 2011.
18. Garcia-Villafranca J, Guillen A, Castro J. Ethanol consumption impairsregulation of fatty acid metabolism by decreasing the activity of AMPactivatedprotein kinase in rat liver. Biochimie 90: 460–466, 2008.
19. Han D, Ybanez MD, Johnson HS, McDonald JN, Mesropyan L, Sancheti H, Martin G, Martin A, Lim AM, Dara L, Cadenas E, Tsukamoto H, Kaplowitz N. Dynamic adaptation of liver mitochondriato chronic alcohol feeding in mice: biogenesis, remodeling, and functionalalterations. J Biol Chem 287: 42165–42179, 2012.
20. Hardie DG. AMPK: positive and negative regulation, and its role inwhole-body energy homeostasis. Curr Opin Cell Biol 33: 1–7, 2015.
21. Huo L, Scarpulla RC. Mitochondrial DNA instability and peri-implantationlethality associated with targeted disruption of nuclear respiratoryfactor 1 in mice. Mol Cell Biol 21: 644–654, 2001.
22. Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activatedprotein kinase (AMPK) action in skeletal muscle via direct phosphorylationof PGC-1alpha. Proc Natl Acad Sci USA 104: 12017–12022, 2007.
23. Kang X, Zhong W, Liu J, Song Z, McClain CJ, Kang YJ, Zhou Z. Zinc supplementation reverses alcohol-induced steatosis in mice through reactivating hepatocyte nuclear factor-4alpha and peroxisome proliferatoractivatedreceptor-alpha. Hepatology 50: 1241–1250, 2009.
24. Ki SH, Choi JH, Kim CW, Kim SG. Combined metadoxine and garlicoil treatment efficaciously abrogates alcoholic steatosis and CYP2E1induction in rat liver with restoration of AMPK activity. Chem BiolInteract 169: 80–90, 2007.
25. Koch OR, Fusco S, Ranieri SC, Maulucci G, Palozza P, Larocca LM, Cravero AA, Farre SM, De Spirito M, Galeotti T, Pani G. Role of thelife span determinant P66(shcA) in ethanol-induced liver damage. LabInvest 88: 750–760, 2008.
26. Kono H, Rusyn I, Yin M, Gabele E, Yamashina S, Dikalova A, Kadiiska MB, Connor HD, Mason RP, Segal BH, Bradford BU,Holland SM, Thurman RG. NADPH oxidase-derived free radicals arekey oxidants in alcohol-induced liver disease. J Clin Invest 106: 867–872,2000.
27. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, Kunz WS. Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 279: 4127–4135, 2004.
28. Levene AP, Goldin RD. The epidemiology, pathogenesis and histopathologyof fatty liver disease. Histopathology 61: 141–152, 2012.
29. Liangpunsakul S, Rahmini Y, Ross RA, Zhao Z, Xu Y, Crabb DW. Imipramine blocks ethanol-induced ASMase activation, ceramide generation,and PP2A activation, and ameliorates hepatic steatosis in ethanolfedmice. Am J Physiol Gastrointest Liver Physiol 302: G515–G523, 2012.
30. Liangpunsakul S, Sozio MS, Shin E, Zhao Z, Xu Y, Ross RA, Zeng Y, Crabb DW. Inhibitory effect of ethanol on AMPK phosphorylation ismediated in part through elevated ceramide levels. Am J Physiol GastrointestLiver Physiol 298: G1004–G1012, 2010.
31. Lu Y, Cederbaum AI. CYP2E1 and oxidative liver injury by alcohol. Free Radic Biol Med 44: 723–738, 2008.
32. Mann RE, Smart RG, Govoni R. The epidemiology of alcoholic liverdisease. Alcohol Res Health 27: 209–219, 2003.
33. McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M. AMP-activated protein kinase regulatesGLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 57: 860–867, 2008.
34. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT. Understanding mitochondrial complex I assembly in health and disease. Biochim Biophys Acta 1817: 851–862, 2012.
35. Mohammad MK, Zhou Z, Cave M, Barve A, McClain CJ. Zinc andliver disease. Nutr Clin Pract 27: 8–20, 2012.
36. Patel VB, Cunningham CC. Altered hepatic mitochondrial ribosomestructure following chronic ethanol consumption. Arch Biochem Biophys 398: 41–50, 2002.
37. Prabu SK, Anandatheerthavarada HK, Raza H, Srinivasan S, Spear JF, Avadhani NG. Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardialischemia-related injury. J Biol Chem 281: 2061–2070, 2006.
38. Raimundo N. Mitochondrial pathology: stress signals from the energyfactory. Trends Mol Med 20: 282–292, 2014.
39. Sandstead HH, Lanier VC Jr, Shephard GH, Gillespie DD. Zinc andwound healing. Effects of zinc deficiency and zinc supplementation. Am JClin Nutr 23: 514–519, 1970.
40. Schiavi A, Ventura N. The interplay between mitochondria and autophagyand its role in the aging process. Exp Gerontol 56: 147–153, 2014.
41. Seo YA, Lopez V, Kelleher SL. A histidine-rich motif mediates mitochondriallocalization of ZnT2 to modulate mitochondrial function. Am JPhysiol Cell Physiol 300: C1479–C1489, 2011.
42. Sun Q, Li Q, Zhong W, Zhang J, Sun X, Tan X, Yin X, Sun X, Zhang X, Zhou Z. Dysregulation of hepatic zinc transporters in a mouse modelof alcoholic liver disease. Am J Physiol Gastrointest Liver Physiol 307:G313–G322, 2014.
43. Sun Q, Zhong W, Zhang W, Li Q, Sun X, Tan X, Sun X, Dong D, Zhou Z. Zinc deficiency mediates alcohol-induced apoptotic cell death in theliver of rats through activating ER and mitochondrial cell death pathways. Am J Physiol Gastrointest Liver Physiol 308: G757–G766, 2015.
44. Tan X, Sun X, Li Q, Zhao Y, Zhong W, Sun X, Jia W, McClain CJ, Zhou Z. Leptin deficiency contributes to the pathogenesis of alcoholicfatty liver disease in mice. Am J Pathol 181: 1279–1286, 2012.
45. Thayer WS, Rubin E. Molecular alterations in the respiratory chain of ratliver after chronic ethanol consumption. J Biol Chem 256: 6090–6097,1981.
46. Venkatraman A, Landar A, Davis AJ, Chamlee L, Sanderson T, Kim H, Page G, Pompilius M, Ballinger S, Darley-Usmar V, Bailey SM.Modification of the mitochondrial proteome in response to the stress ofethanol-dependent hepatotoxicity. J Biol Chem 279: 22092–22101, 2004.
47. Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control ofmitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res 79: 208–217, 2008.
48. Voos W. Chaperone-protease networks in mitochondrial protein homeostasis. Biochim Biophys Acta 1833: 388–399, 2013.
49. Watanabe T, Arakawa T, Fukuda T, Higuchi K, Kobayashi K. Zincdeficiency delays gastric ulcer healing in rats. Dig Dis Sci 40: 1340–1344,1995.
50. Wu Y, Song P, Xu J, Zhang M, Zou MH. Activation of proteinphosphatase 2A by palmitate inhibits AMP-activated protein kinase. J BiolChem 282: 9777–9788, 2007.
51. Yoneda T, Benedetti C, Urano F, Clark SG, Harding HP, Ron D.Compartment-specific perturbation of protein handling activates genesencoding mitochondrial chaperones. J Cell Sci 117: 4055–4066, 2004.
52. Young TA, Bailey SM, Van Horn CG, Cunningham CC. Chronicethanol consumption decreases mitochondrial and glycolytic production of ATP in liver. Alcohol Alcohol 41: 254–260, 2006.
53. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ. Circulating mitochondrial DAMPs cause inflammatoryresponses to injury. Nature 464: 104–107, 2010.
54. Zhang W, Zhong W, Sun X, Sun Q, Tan X, Li Q, Sun X, Zhou Z. Visceral white adipose tissue is susceptible to alcohol-induced lipodystrophyin rats: role of acetaldehyde. Alcohol Clin Exp Res 39: 416–423, 2015.
55. Zhao L, Zou X, Feng Z, Luo C, Liu J, Li H, Chang L, Wang H, Li Y, Long J, Gao F, Liu J. Evidence for association of mitochondrial metabolismalteration with lipid accumulation in aging rats. Exp Gerontol 56:3–12, 2014.
56. Zhao Q, Wang J, Levichkin IV, Stasinopoulos S, Ryan MT, Hoogenraad NJ. A mitochondrial specific stress response in mammalian cells. EMBO J 21: 4411–4419, 2002.
57. Zhao Y, Zhong W, Sun X, Song Z, Clemens DL, Kang YJ, McClain CJ, Zhou Z. Zinc deprivation mediates alcohol-induced hepatocyte IL-8analog expression in rodents via an epigenetic mechanism. Am J Pathol179: 693–702, 2011.
58. Zhong W, Zhang W, Li Q, Xie G, Sun Q, Sun X, Tan X, Sun X, Jia W, Zhou Z. Pharmacological activation of aldehyde dehydrogenase 2 byAlda-1 reverses alcohol-induced hepatic steatosis and cell death in mice. J Hepatol 62: 1375–1381, 2015.
59. Zhou Z, Wang L, Song Z, Saari JT, McClain CJ, Kang YJ. Zincsupplementation prevents alcoholic liver injury in mice through attenuationof oxidative stress. Am J Pathol 166: 1681–1690, 2005.
60. Zhu H, Li YR. Oxidative stress and redox signaling mechanisms ofinflammatory bowel disease: updated experimental and clinical evidence. Exp Biol Med (Maywood) 237: 474–480, 2012.