Mitochondrial acetylome analysis in a mouse model of alcohol-induced liver injury utilizing SIRT3 knockout mice

Journal of Proteome Research

Volumn 11, Issue 3, 2012, Pages 1633-1643

  Fritz, Kristofer S ^a   Galligan, James J ^b   Hirschey, Matthew D ^c   Verdin, Eric ^c   Petersen, Dennis R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

acetylation; alcohol; LC?MS MS; MudPIT; SIRT3; sirtuin

Indexed keywords

ACETIC ACID DERIVATIVE; AMINO ACID; ANTIOXIDANT; FATTY ACID; LIPID; SIRTUIN 3;

ALCOHOL CONSUMPTION; ALCOHOL LIVER DISEASE; AMINO ACID SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONFERENCE PAPER; CONTROLLED STUDY; DEACETYLATION; FATTY ACID METABOLISM; LIPID METABOLISM; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACETYLATION; ACETYLTRANSFERASES; ALDEHYDE DEHYDROGENASE; ANIMALS; DISEASE MODELS, ANIMAL; DRUG-INDUCED LIVER INJURY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ETHANOL; ISOCITRATE DEHYDROGENASE; LIPID METABOLISM; LIVER DISEASES, ALCOHOLIC; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; SIRTUIN 3; SUPEROXIDE DISMUTASE;

MUS;

EID: 84857883360     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2008384     Document Type: Conference Paper

References (58)

1. Bayarsaihan, D. Epigenetic mechanisms in inflammation J. Dent. Res. 2011, 90 (1) 9-17
2. Atadja, P. W. HDAC inhibitors and cancer therapy Prog. Drug Res. 2011, 67, 175-95
3. Sawan, C.; Herceg, Z. Histone modifications and cancer Adv. Genet. 2010, 70, 57-85
4. Ghizzoni, M.; Haisma, H. J.; Maarsingh, H.; Dekker, F. J. Histone acetyltransferases are crucial regulators in NF-kappaB mediated inflammation Drug Discov. Today 2011, 16 (11-12) 504-11
5. Kim, S. C.; Sprung, R.; Chen, Y.; Xu, Y.; Ball, H.; Pei, J.; Cheng, T.; Kho, Y.; Xiao, H.; Xiao, L.; Grishin, N. V.; White, M.; Yang, X. J.; Zhao, Y. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey Mol. Cell 2006, 23 (4) 607-18
6. Hirschey, M. D.; Shimazu, T.; Goetzman, E.; Jing, E.; Schwer, B.; Lombard, D. B.; Grueter, C. A.; Harris, C.; Biddinger, S.; Ilkayeva, O. R.; Stevens, R. D.; Li, Y.; Saha, A. K.; Ruderman, N. B.; Bain, J. R.; Newgard, C. B.; Farese, R. V., Jr.; Alt, F. W.; Kahn, C. R.; Verdin, E. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation Nature 2010, 464 (7285) 121-5
7. Qiu, X.; Brown, K.; Hirschey, M. D.; Verdin, E.; Chen, D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation Cell Metab. 2010, 12 (6) 662-7
8. Schwer, B.; Bunkenborg, J.; Verdin, R. O.; Andersen, J. S.; Verdin, E. Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2 Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (27) 10224-9
9. Nakagawa, T.; Lomb, D. J.; Haigis, M. C.; Guarente, L. SIRT5 Deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle Cell 2009, 137 (3) 560-70
10. Hallows, W. C.; Smith, B. C.; Lee, S.; Denu, J. M. Ure(k)a! Sirtuins Regulate Mitochondria Cell 2009, 137 (3) 404-6
11. Ahn, B. H.; Kim, H. S.; Song, S.; Lee, I. H.; Liu, J.; Vassilopoulos, A.; Deng, C. X.; Finkel, T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (38) 14447-52
12. Schlicker, C.; Gertz, M.; Papatheodorou, P.; Kachholz, B.; Becker, C. F.; Steegborn, C. Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5 J. Mol. Biol. 2008, 382 (3) 790-801
13. Someya, S.; Yu, W.; Hallows, W. C.; Xu, J.; Vann, J. M.; Leeuwenburgh, C.; Tanokura, M.; Denu, J. M.; Prolla, T. A. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction Cell 2010, 143 (5) 802-12
14. Close, P.; Creppe, C.; Gillard, M.; Ladang, A.; Chapelle, J. P.; Nguyen, L.; Chariot, A. The emerging role of lysine acetylation of non-nuclear proteins Cell. Mol. Life Sci. 2010, 67 (8) 1255-64
15. Lavu, S.; Boss, O.; Elliott, P. J.; Lambert, P. D. Sirtuins - novel therapeutic targets to treat age-associated diseases Nat. Rev. Drug Discov. 2008, 7 (10) 841-53
16. Alcain, F. J.; Villalba, J. M. Sirtuin activators Expert Opin. Ther. Pat. 2009, 19 (4) 403-14
17. Alcain, F. J.; Villalba, J. M. Sirtuin inhibitors Expert Opin. Ther. Pat. 2009, 19 (3) 283-94
18. Sauve, A. A. Sirtuin chemical mechanisms Biochim. Biophys. Acta 2010, 8, 1591-603
19. Verdin, E.; Hirschey, M. D.; Finley, L. W.; Haigis, M. C. Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling Trends Biochem. Sci. 2010, 35 (12) 669-75
20. Shimazu, T.; Hirschey, M. D.; Hua, L.; Dittenhafer-Reed, K. E.; Schwer, B.; Lombard, D. B.; Li, Y.; Bunkenborg, J.; Alt, F. W.; Denu, J. M.; Jacobson, M. P.; Verdin, E. SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production Cell Metab. 2010, 12 (6) 654-61
21. Albaugh, B. N.; Arnold, K. M.; Lee, S.; Denu, J. M. Autoacetylation of the histone acetyltransferase Rtt109 J. Biol. Chem. 2011, 286 (28) 24694-701
22. Kuo, M. H.; Allis, C. D. Roles of histone acetyltransferases and deacetylases in gene regulation Bioessays 1998, 20 (8) 615-26
23. Schwer, B.; Verdin, E. Conserved metabolic regulatory functions of sirtuins Cell Metab. 2008, 7 (2) 104-12
24. Huang, J. Y.; Hirschey, M. D.; Shimazu, T.; Ho, L.; Verdin, E. Mitochondrial sirtuins Biochim. Biophys. Acta 2010, 1804 (8) 1645-1651
25. Picklo, M. J., Sr. Ethanol intoxication increases hepatic N-lysyl protein acetylation Biochem. Biophys. Res. Commun. 2008, 376 (3) 615-9
26. Fritz, K. S.; Galligan, J. J.; Smathers, R. L.; Roede, J. R.; Shearn, C. T.; Reigan, P.; Petersen, D. R. 4-Hydroxynonenal inhibits SIRT3 via thiol-specific modification Chem. Res. Toxicol. 2011, 24 (5) 651-62
27. Bailey, S. M.; Cunningham, C. C. Contribution of mitochondria to oxidative stress associated with alcoholic liver disease Free Radic. Biol. Med. 2002, 32 (1) 11-6
28. Mantena, S. K.; King, A. L.; Andringa, K. K.; Eccleston, H. B.; Bailey, S. M. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases Free Radic. Biol. Med. 2008, 44 (7) 1259-72
29. Shepard, B. D.; Tuma, P. L. Alcohol-induced protein hyperacetylation: mechanisms and consequences World J. Gastroenterol. 2009, 15 (10) 1219-30
30. Shepard, B. D.; Tuma, D. J.; Tuma, P. L. Chronic ethanol consumption induces global hepatic protein hyperacetylation Alcohol.: Clin. Exp. Res. 2010, 34 (2) 280-91
31. Lombard, D. B.; Alt, F. W.; Cheng, H. L.; Bunkenborg, J.; Streeper, R. S.; Mostoslavsky, R.; Kim, J.; Yancopoulos, G.; Valenzuela, D.; Murphy, A.; Yang, Y.; Chen, Y.; Hirschey, M. D.; Bronson, R. T.; Haigis, M.; Guarente, L. P.; Farese, R. V., Jr.; Weissman, S.; Verdin, E.; Schwer, B. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation Mol. Cell. Biol. 2007, 27 (24) 8807-14
32. Lieber, C. S. Metabolism of alcohol Clin. Liver Dis. 2005, 9 (1) 1-35
33. Sastre, J.; Serviddio, G.; Pereda, J.; Minana, J. B.; Arduini, A.; Vendemiale, G.; Poli, G.; Pallardo, F. V.; Vina, J. Mitochondrial function in liver disease Front. Biosci. 2007, 12, 1200-9
34. Lieber, C. S. [Clinical biochemistry of alcohol and its metabolic and hepatic effects] J. Annu. Diabetol. Hotel Dieu. 1992, 183-210
35. Veech, R. L.; Guynn, R.; Veloso, D. The time-course of the effects of ethanol on the redox and phosphorylation states of rat liver Biochem. J. 1972, 127 (2) 387-97
36. Ramaiah, S.; Rivera, C.; Arteel, G. Early-phase alcoholic liver disease: an update on animal models, pathology, and pathogenesis Int. J. Toxicol. 2004, 23 (4) 217-31
37. Ozden, O.; Park, S. H.; Kim, H. S.; Jiang, H.; Coleman, M. C.; Spitz, D. R.; Gius, D. Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress Aging (Albany NY) 2011, 3 (2) 102-7
38. Yang, E. S.; Park, J. W. Regulation of ethanol-induced toxicity by mitochondrial NADP(+)-dependent isocitrate dehydrogenase Biochimie 2009, 91 (8) 1020-8
39. Roede, J. R.; Stewart, B. J.; Petersen, D. R. Decreased expression of peroxiredoxin 6 in a mouse model of ethanol consumption Free Radic. Biol. Med. 2008, 45 (11) 1551-8
40. Roede, J. R.; Carbone, D. L.; Doorn, J. A.; Kirichenko, O. V.; Reigan, P.; Petersen, D. R. In vitro and in silico characterization of peroxiredoxin 6 modified by 4-hydroxynonenal and 4-oxononenal Chem. Res. Toxicol. 2008, 21 (12) 2289-99
41. Choudhary, C.; Kumar, C.; Gnad, F.; Nielsen, M. L.; Rehman, M.; Walther, T. C.; Olsen, J. V.; Mann, M. Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 2009, 325 (5942) 834-40
42. Vidali, M.; Stewart, S. F.; Albano, E. Interplay between oxidative stress and immunity in the progression of alcohol-mediated liver injury Trends Mol. Med. 2008, 14 (2) 63-71
43. Yang, E. S.; Lee, J. H.; Park, J. W. Ethanol induces peroxynitrite- mediated toxicity through inactivation of NADP+-dependent isocitrate dehydrogenase and superoxide dismutase Biochimie 2008, 90 (9) 1316-24
44. Tao, R.; Coleman, M. C.; Pennington, J. D.; Ozden, O.; Park, S. H.; Jiang, H.; Kim, H. S.; Flynn, C. R.; Hill, S.; Hayes McDonald, W.; Olivier, A. K.; Spitz, D. R.; Gius, D. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress Mol. Cell 2010, 40 (6) 893-904
45. Lieber, C. S.; Leo, M. A.; Wang, X.; Decarli, L. M. Alcohol alters hepatic FoxO1, p53, and mitochondrial SIRT5 deacetylation function Biochem. Biophys. Res. Commun. 2008, 373 (2) 246-52
46. Lieber, C. S.; Leo, M. A.; Wang, X.; Decarli, L. M. Effect of chronic alcohol consumption on Hepatic SIRT1 and PGC-1alpha in rats Biochem. Biophys. Res. Commun. 2008, 370 (1) 44-8
47. Niemela, O. Aldehyde-protein adducts in the liver as a result of ethanol-induced oxidative stress Front. Biosci. 1999, 4, 506-13
48. Kendrick, S. F.; OBoyle, G.; Mann, J.; Zeybel, M.; Palmer, J.; Jones, D. E.; Day, C. P. Acetate, the key modulator of inflammatory responses in acute alcoholic hepatitis Hepatology 2010, 51 (6) 1988-97
49. Dormeyer, W.; Ott, M.; Schnolzer, M. Probing lysine acetylation in proteins: strategies, limitations, and pitfalls of in vitro acetyltransferase assays Mol. Cell. Proteomics 2005, 4 (9) 1226-39
50. Albano, E. Alcohol, oxidative stress and free radical damage Proc. Nutr. Soc. 2006, 65 (3) 278-90
51. Das, S. K.; Vasudevan, D. M. Alcohol-induced oxidative stress Life Sci. 2007, 81 (3) 177-87
52. Bell, E. L.; Guarente, L. The SirT3 Divining Rod Points to Oxidative Stress Mol. Cell 2011, 42 (5) 561-8
53. Yang, E. S.; Lee, S. M.; Park, J. W. Silencing of cytosolic NADP+-dependent isocitrate dehydrogenase gene enhances ethanol-induced toxicity in HepG2 cells Arch. Pharm. Res. 2010, 33 (7) 1065-71
54. Wheeler, M. D.; Nakagami, M.; Bradford, B. U.; Uesugi, T.; Mason, R. P.; Connor, H. D.; Dikalova, A.; Kadiiska, M.; Thurman, R. G. Overexpression of manganese superoxide dismutase prevents alcohol-induced liver injury in the rat J. Biol. Chem. 2001, 276 (39) 36664-72
55. Lu, Z.; Bourdi, M.; Li, J. H.; Aponte, A. M.; Chen, Y.; Lombard, D. B.; Gucek, M.; Pohl, L. R.; Sack, M. N. SIRT3-dependent deacetylation exacerbates acetaminophen hepatotoxicity EMBO Rep. 2011, 12 (8) 840-6
56. Shi, T.; Fan, G. Q.; Xiao, S. D. SIRT3 reduces lipid accumulation via AMPK activation in human hepatic cells J. Dig. Dis. 2010, 11 (1) 55-62
57. Hallows, W. C..; Yu, W.; Smith, B. C.; Devries, M. K.; Ellinger, J. J.; Someya, S.; Shortreed, M. R.; Prolla, T.; Markley, J. L.; Smith, L. M.; Zhao, S.; Guan, K. L.; Denu, J. M. Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction Mol. Cell 2011, 41 (2) 139-49
58. Silberman, D. M.; Mostoslavsky, R. SIRT3 deacetylase: the Jekyll and Hyde sirtuin EMBO Rep. 2011, 12 (8) 746-7