Mitochondrial protein acetylation regulates metabolism

Essays in Biochemistry

Volumn 52, Issue 1, 2012, Pages 23-35

  Anderson, Kristin A ^a   Hirschey, Matthew D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN; SIRTUIN 3;

ACETYLATION; ANIMAL; BIOLOGICAL MODEL; HUMAN; METABOLISM; MITOCHONDRION; REVIEW;

ACETYLATION; ANIMALS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; SIRTUIN 3;

EID: 84867594869     PISSN: 00711365     EISSN: None     Source Type: Journal    
DOI: 10.1042/BSE0520023     Document Type: Article

References (56)

1. Glozak, M.A., Sengupta, N., Zhang, X. and Seto, E. (2005) Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23
2. Kim, S.C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Cheng, T., Kho, Y., Xiao, H., Xiao, L. et al. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 23, 607-618
3. Blander, G. and Guarente, L. (2004) The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73, 417-435
4. North, B.J. and Verdin, E. (2004) Sirtuins: Sir2-related NAD-dependent protein deacetylases. Genome Biol. 5, 224
5. Michishita, E., Park, J.Y., Burneskis, J.M., Barrett, J.C. and Horikawa, I. (2005) Evolutionary conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell 16, 4623-4635
6. Haigis, M.C., Mostoslavsky, R., Haigis, K.M., Fahie, K., Christodoulou, D.C., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Karow, M., Blander, G. et al. (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic β-cells. Cell 126, 941-954
7. Chen, I.Y., Lypowy, J., Pain, J., Sayed, D., Grinberg, S., Alcendor, R.R., Sadoshima, J. and Abdellatif, M. (2006) Histone H2A.z is essential for cardiac myocyte hypertrophy but opposed by silent information regulator 2a. J. Biol. Chem. 281, 19369-19377
8. +-dependent histone deacetylase SIRT1. J. Biol. Chem. 282, 6823-6832
9. Frye, R.A. (1999) Characterization of five human cDNAs with homology to the yeast SIR2 gene: Sir2-like proteins (sirtuins) metabolize NAD and may have protein ADP-ribosyltransferase activity. Biochem. Biophys. Res. Commun. 260, 273-279
10. Frye, R.A. (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem. Biophys. Res. Commun. 273, 793-798
11. Ahuja, N., Schwer, B., Carobbio, S., Waltregny, D., North, B.J., Castronovo, V., Maechler, P. and Verdin, E. (2007) Regulation of insulin secretion by SIRT4, a mitochondrial ADP-ribosyltransferase. J. Biol. Chem. 282, 33583-33592
12. Verdin, E., Dequiedt, F., Fischle, W., Frye, R., Marshall, B. and North, B. (2004) Measurement of mammalian histone deacetylase activity. Methods Enzymol. 377, 180-196
13. Nakagawa, T., Lomb, D.J., Haigis, M.C. and Guarente, L. (2009) SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 137, 560-570
14. Kawahara, T.L.A., Michishita, E., Adler, A.S., Damian, M., Berber, E., Lin, M., McCord, R.A., Ongaigui, K.C.L., Boxer, L.D., Chang, H.Y. and Chua, K.F. (2009) SIRT6 links histone H3 lysine 9 deacetylation to NF-κB-dependent gene expression and organismal life span. Cell 136, 62-74
15. Haigis, M.C. and Sinclair, D.A. (2010) Mammalian sirtuins: biological insights and disease relevance. Annu. Rev. Pathol. 5, 253-295
16. Sauve, A.A., Wolberger, C., Schramm, V.L. and Boeke, J.D. (2006) The biochemistry of sirtuins. Annu. Rev. Biochem. 75, 435-465
17. Denu, J.M. (2005) The Sir 2 family of protein deacetylases. Curr. Opin. Chem. Biol. 9, 431-440
18. Lin, S.J., Defossez, P.A. and Guarente, L. (2000) Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289, 2126-2128
19. Lin, S.J., Kaeberlein, M., Andalis, A.A., Sturtz, L.A., Defossez, P.A., Culotta, V.C., Fink, G.R. and Guarente, L. (2002) Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418, 344-348
20. Lin, J., Wu, P.H., Tarr, P.T., Lindenberg, K.S., St-Pierre, J., Zhang, C.Y., Mootha, V.K., Jager, S., Vianna, C.R., Reznick, R.M. et al. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119, 121-135
21. Bitterman, K.J., Anderson, R.M., Cohen, H.Y., Latorre-Esteves, M. and Sinclair, D.A. (2002) Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J. Biol. Chem. 277, 45099-45107
22. Anderson, R.M., Bitterman, K.J., Wood, J.G., Medvedik, O. and Sinclair, D.A. (2003) Nicotinamide and PNC1 govern lifespan extension by calorie restriction in Saccharomyces cerevisiae. Nature 423, 181-185
23. Finkel, T., Deng, C.X. and Mostoslavsky, R. (2009) Recent progress in the biology and physiology of sirtuins. Nature 460, 587-591
24. Lombard, D.B., Alt, F.W., Cheng, H.L., Bunkenborg, J., Streeper, R.S., Mostoslavsky, R., Kim, J., Yancopoulos, G., Valenzuela, D., Murphy, A. et al. (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol. Cell. Biol. 27, 8807-8814
25. Schwer, B., North, B.J., Frye, R.A., Ott, M. and Verdin, E. (2002) The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase. J. Cell Biol. 158, 647-657
26. Schwer, B., Bunkenborg, J., Verdin, R.O., Andersen, J.S. and Verdin, E. (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U.S.A. 103, 10224-10229
27. Paik, W.K., Pearson, D., Lee, H.W. and Kim, S. (1970) Nonenzymatic acetylation of histones with acetyl-CoA. Biochim. Biophys. Acta 213, 513-522
28. Schwer, B., Eckersdorff, M., Li, Y., Silva, J., Fermin, D., Kurtev, M., Giallourakis, C., Comb, M., Alt, F. and Lombard, D. (2009) Calorie restriction alters mitochondrial protein acetylation. Aging Cell 8, 604-606
29. Hirschey, M., Aouizerat, B., Jing, E., Shimazu, T., Grueter, C., Collins, A., Stevens, R., Lam, M., Muehlbauer, M., Schwer, B. et al. (2011) SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol. Cell 44, 177-190
30. Kendrick, A.A., Choudhury, M., Rahman, S.M., McCurdy, C.E., Friederich, M., Van Hove, J.L.K., Watson, P.A., Birdsey, N., Bao, J., Gius, D. et al. (2011) Fatty liver is associated with reduced SIRT3 activity and mitochondrial protein hyperacetylation. Biochem. J. 433, 505-514
31. Picklo, M.J. (2008) Ethanol intoxication increases hepatic N-lysyl protein acetylation. Biochem. Biophys. Res. Commun. 376, 615-619
32. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M., Rehman, M., Walther, T., Olsen, J. and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
33. Wang, Q., Zhang, Y., Yang, C., Xiong, H., Lin, Y., Yao, J., Li, H., Xie, L., Zhao, W., Yao, Y. et al. (2010) Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327, 1004-1007
34. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H. et al. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327, 1000-1004
35. Pagliarini, D.J., Calvo, S.E., Chang, B., Sheth, S.A., Vafai, S.B., Ong, S.-E., Walford, G.A., Sugiana, C., Boneh, A., Chen, W.K. et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123
36. Huang, D.W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
37. Thomas, P.D., Kejariwal, A., Campbell, M.J., Mi, H., Diemer, K., Guo, N., Ladunga, I., Ulitsky-Lazareva, B., Muruganujan, A., Rabkin, S. et al. (2003) PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res. 31, 334-341
38. Ahn, B.H., Kim, H.S., Song, S., Lee, I.H., Liu, J., Vassilopoulos, A., Deng, C.X. and Finkel, T. (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. U.S.A. 105, 14447-14452
39. Cimen, H., Han, M.-J., Yang, Y., Tong, Q., Koc, H. and Koc, E.C. (2009) Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 49, 304-311
40. Finley, L.W.S., Haas, W., Desquiret-Dumas, V.R., Wallace, D.C., Procaccio, V., Gygi, S.P. and Haigis, M.C. (2011) Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity. PLoS ONE 6, e23295
41. Hirschey, M., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D., Grueter, C., Harris, C., Biddinger, S., Ilkayeva, O. et al. (2010) SIRT3 regulates mitochondrial fatty acid oxidation via reversible enzyme deacetylation. Nature 464, 121-125
42. Beal, M.F. (2005) Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 58, 495-505
43. Bubber, P., Haroutunian, V., Fisch, G., Blass, J.P. and Gibson, G.E. (2005) Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann. Neurol. 57, 695-703
44. Calvo, S.E. and Mootha, V.K. (2010) The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 11, 25-44
45. Hallows, W.C., Lee, S. and Denu, J.M. (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U.S.A. 103, 10230-10235
46. Schwer, B., Bunkenborg, J., Verdin, R.O., Andersen, J.S. and Verdin, E. (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U.S.A. 103, 10224-10229
47. Shimazu, T., Hirschey, M., Hua, L., Dittenhafer-Reed, K.E., Schwer, B., Lombard, D., Li, Y., Bunkenborg, J., Alt, F.W., Denu, J.M. et al. (2010) SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2, increases its enzymatic activity and regulates ketone body production. Cell Metab. 12, 654-661
48. Schlicker, C., Gertz, M., Papatheodorou, P., Kachholz, B., Becker, C.F.W. and Steegborn, C. (2008) Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J. Mol. Biol. 382, 790-801
49. Hallows, W.C., Yu, W., Smith, B.C., Devires, M.K., Ellinger, J.J., Someya, S., Shortreed, M.R., Prolla, T., Markley, J.L., Smith, L.M. et al. (2011) Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol. Cell 41, 139-149
50. Qiu, X., Brown, K., Hirschey, M.D., Verdin, E. and Chen, D. (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metabol. 12, 662-667
51. 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. et al. (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 40, 893-904
52. Mootha, V.K., Bunkenborg, J., Olsen, J.V., Hjerrild, M., Wisniewski, J.R., Stahl, E., Bolouri, M.S., Ray, H.N., Sihag, S., Kamal, M. et al. (2003) Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115, 629-640
53. McBride, H.M., Neuspiel, M. and Wasiak, S. (2006) Mitochondria: more than just a powerhouse. Curr. Biol. 16, R551-R560
54. Chan, D.C. (2006) Mitochondria: dynamic organelles in disease, aging, and development. Cell 125, 1241-1252
55. 2+ uptake in apoptosis. Cell Calcium 40, 553-560
56. Hausenloy, D.J. and Ruiz-Meana, M. (2010) Not just the powerhouse of the cell: emerging roles for mitochondria in the heart. Cardiovasc. Res. 88, 5-6