Proteomic Investigations of Lysine Acetylation Identify Diverse Substrates of Mitochondrial Deacetylase Sirt3

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Sol, Eri Maria ^a   Wagner, Sebastian A ^a   Weinert, Brian T ^a   Kumar, Amit ^a   Kim, Hyun Seok ^b,c   Deng, Chu Xia ^b   Choudhary, Chunaram ^a   Imhof, Axel ^d  

^a University of Copenhagen   (Denmark)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c Ewha Womans University   (South Korea)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED CHAIN AMINO ACID; FATTY ACID; HYDROLASE; LYSINE DEACETYLASE; SHORT HAIRPIN RNA; SIRTUIN 3; TRICARBOXYLIC ACID; UNCLASSIFIED DRUG;

ACETYLATION; AMINO ACID METABOLISM; ANIMAL CELL; ARTICLE; CELL FUNCTION; CITRIC ACID CYCLE; CONTROLLED STUDY; EMBRYO; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; FATTY ACID METABOLISM; FUNCTIONAL PROTEOMICS; GENE INACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; METABOLIC REGULATION; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; QUANTITATIVE ANALYSIS;

ACETYLATION; ANIMALS; CELL LINE; FIBROBLASTS; HUMANS; LYSINE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; PROTEOMICS; SIRTUIN 3;

MURINAE;

EID: 84870880080     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050545     Document Type: Article

References (51)

1. Yang XJ, Seto E, (2008) Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 31: 449-461.
2. Huang JY, Hirschey MD, Shimazu T, Ho L, Verdin E, (2010) Mitochondrial sirtuins. Biochim Biophys Acta 1804: 1645-1651.
3. Yang XJ, Seto E, (2007) HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 26: 5310-5318.
4. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, et al. (2010) SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17: 41-52.
5. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, et al. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325: 834-840.
6. Gnad F, Forner F, Zielinska DF, Birney E, Gunawardena J, et al. (2010) Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria. Mol Cell Proteomics 9: 2642-2653.
7. Weinert BT, Wagner SA, Horn H, Henriksen P, Liu WR, et al. (2011) Proteome-wide mapping of the Drosophila acetylome demonstrates a high degree of conservation of lysine acetylation. Sci Signal 4: ra48.
8. Yang XJ, Seto E, (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9: 206-218.
9. Schwer B, Verdin E, (2008) Conserved metabolic regulatory functions of sirtuins. Cell Metab 7: 104-112.
10. Haigis MC, Sinclair DA, (2010) Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5: 253-295.
11. Finkel T, Deng CX, Mostoslavsky R, (2009) Recent progress in the biology and physiology of sirtuins. Nature 460: 587-591.
12. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, et al. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464: 121-125.
13. Someya S, Yu W, Hallows WC, Xu J, Vann JM, et al. (2010) Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143: 802-812.
14. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, et al. (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40: 893-904.
15. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, et al. (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27: 8807-8814.
16. Ahn BH, Kim HS, Song S, Lee IH, Liu J, et al. (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A 105: 14447-14452.
17. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D, (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12: 662-667.
18. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, et al. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1: 376-386.
19. Michalski A, Damoc E, Hauschild JP, Lange O, Wieghaus A, et al. (2011) Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol Cell Proteomics 10: M111 011015.
20. Olsen JV, Schwartz JC, Griep-Raming J, Nielsen ML, Damoc E, et al. (2009) A dual pressure linear ion trap Orbitrap instrument with very high sequencing speed. Mol Cell Proteomics 8: 2759-2769.
21. Olsen JV, Macek B, Lange O, Makarov A, Horning S, et al. (2007) Higher-energy C-trap dissociation for peptide modification analysis. Nat Methods 4: 709-712.
22. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372.
23. Elias JE, Gygi SP, (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214.
24. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, et al. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23: 607-618.
25. Zhao S, Xu W, Jiang W, Yu W, Lin Y, et al. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327: 1000-1004.
26. Chegary M, Brinke H, Ruiter JP, Wijburg FA, Stoll MS, et al. (2009) Mitochondrial long chain fatty acid beta-oxidation in man and mouse. Biochim Biophys Acta 1791: 806-815.
27. Cimen H, Han MJ, Yang Y, Tong Q, Koc H, et al. (2010) Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 49: 304-311.
28. Finley LW, Haas W, Desquiret-Dumas V, Wallace DC, Procaccio V, et al. (2011) Succinate dehydrogenase is a direct target of sirtuin 3 deacetylase activity. PLoS One 6: e23295.
29. Haberland M, Montgomery RL, Olson EN, (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10: 32-42.
30. Bolden JE, Peart MJ, Johnstone RW, (2006) Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784.
31. Kim JY, Kim KW, Kwon HJ, Lee DW, Yoo JS, (2002) Probing lysine acetylation with a modification-specific marker ion using high-performance liquid chromatography/electrospray-mass spectrometry with collision-induced dissociation. Anal Chem 74: 5443-5449.
32. Choudhary C, Mann M, (2010) Decoding signalling networks by mass spectrometry-based proteomics. Nat Rev Mol Cell Biol 11: 427-439.
33. Wallace DC, (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39: 359-407.
34. Hallows WC, Yu W, Smith BC, Devires MK, Ellinger JJ, et al. (2011) Sirt3 Promotes the Urea Cycle and Fatty Acid Oxidation during Dietary Restriction. Mol Cell 41: 139-149.
35. Shimazu T, Hirschey MD, Hua L, Dittenhafer-Reed KE, Schwer B, et al. (2010) SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab 12: 654-661.
36. Brummelkamp TR, Bernards R, Agami R, (2002) Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2: 243-247.
37. Morita S, Kojima T, Kitamura T, (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 7: 1063-1066.
38. Choudhary C, Brandts C, Schwable J, Tickenbrock L, Sargin B, et al. (2007) Activation mechanisms of STAT5 by oncogenic Flt3-ITD. Blood 110: 370-374.
39. Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, et al. (2005) The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17: 331-339.
40. Nielsen ML, Vermeulen M, Bonaldi T, Cox J, Moroder L, et al. (2008) Iodoacetamide-induced artifact mimics ubiquitination in mass spectrometry. Nat Methods 5: 459-460.
41. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648.
42. Horth P, Miller CA, Preckel T, Wenz C, (2006) Efficient fractionation and improved protein identification by peptide OFFGEL electrophoresis. Mol Cell Proteomics 5: 1968-1974.
43. Hubner NC, Ren S, Mann M, (2008) Peptide separation with immobilized pI strips is an attractive alternative to in-gel protein digestion for proteome analysis. Proteomics 8: 4862-4872.
44. Rappsilber J, Ishihama Y, Mann M, (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 75: 663-670.
45. Wisniewski JR, Zougman A, Mann M, (2009) Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J Proteome Res 8: 5674-5678.
46. Rappsilber J, Mann M, Ishihama Y, (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896-1906.
47. Kelstrup CD, Young C, Lavallee R, Nielsen ML, Olsen JV, (2012) Optimized Fast and Sensitive Acquisition Methods for Shotgun Proteomics on a Quadrupole Orbitrap Mass Spectrometer. J Proteome Res.
48. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, et al. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 4: 2010-2021.
49. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, et al. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794-1805.
50. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
51. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, et al. (2012) eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40: D284-289.