Understanding the acetylome: Translating targeted proteomics into meaningful physiology

American Journal of Physiology - Cell Physiology

Volumn 307, Issue 9, 2014, Pages C763-C773

  Philp, Andrew ^a   Rowland, Thomas ^a   Perez Schindler, Joaquin ^a   Schenk, Simon ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adaptation; Exercise; Metabolism; Mitochondria; Muscle

Indexed keywords

ACETYL COENZYME A; ACYLTRANSFERASE; CYTOPLASM PROTEIN; E1A ASSOCIATED P300 PROTEIN; GENERAL CONTROL OF AMINO ACID SYNTHESIS 5; GLUCOSE TRANSPORTER 4; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYOXYLIC ACID; HISTONE ACETYLTRANSFERASE PCAF; LYSINE; MITOCHONDRIAL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MYOCYTE ENHANCER FACTOR 2; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE DEPENDENT DEACETYLASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN; PROTEOME; S6 KINASE; S6 KINASE 1; SIRTUIN 1; SIRTUIN 2; SIRTUIN 3; SIRTUIN 4; SIRTUIN 5; SIRTUIN 6; SIRTUIN 7; STABLE ISOTOPE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; UNINDEXED DRUG; HISTONE ACETYLTRANSFERASE;

ACETYLOME; AEROBIC METABOLISM; ARTICLE; CELL DIFFERENTIATION; CELL METABOLISM; CELLULAR DISTRIBUTION; CITRIC ACID CYCLE; DEACETYLATION; DELETION MUTANT; ENZYME ACTIVITY; ESCHERICHIA COLI; EXTENSOR DIGITORUM LONGUS MUSCLE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; GENE DELETION; GENE ONTOLOGY; GLUCONEOGENESIS; GLYCOGEN METABOLISM; GLYCOLYSIS; HISTONE ACETYLATION; HUMAN; IMMUNOBLOTTING; IMMUNOPRECIPITATION; ISOELECTRIC FOCUSING; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; METABOLIC REGULATION; MUSCLE CONTRACTION; MYOBLAST; NONHUMAN; NUCLEOSOME; PHYLOGENY; PROTEIN ACETYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEOMICS; RNA SPLICING; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TANDEM MASS SPECTROMETRY; TRANSCRIPTION INITIATION; UREA CYCLE; ACETYLATION; ENZYMOLOGY; METABOLISM;

ACETYLATION; ACETYLTRANSFERASES; HISTONE ACETYLTRANSFERASES; HUMANS; LYSINE; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS;

EID: 84908518716     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00399.2013     Document Type: Article

References (81)

1. Adler AJ, Fasman GD, Wangh LJ, Allfrey VG. Altered conformational effects of naturally acetylated histone f2al (IV) in f2al-deoxyribonucleic acid complexes. Circular dichroism studies. J Biol Chem 249: 2911-2914, 1974.
2. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates Pgc-1 transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593, 2005.
3. Alamdari N, Aversa Z, Castillero E, Hasselgren PO. Acetylation and deacetylation—novel factors in muscle wasting. Metab Clin Exp 62: 1-11, 2013.
4. Alamdari N, Smith IJ, Aversa Z, Hasselgren PO. Sepsis and glucocor-ticoids upregulate p300 and downregulate HDAC6 expression and activity in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 299: R509-R520, 2010.
5. Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci USA 51: 786-794, 1964.
6. Arany Z, Sellers WR, Livingston DM, Eckner R. E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators. Cell 77: 799-800, 1994.
7. Bedford MT, Clarke SG. Protein arginine methylation in mammals: who, what, and why. Mol Cell 33: 1-13, 2009.
8. Bouras T, Fu M, Sauve AA, Wang F, Quong AA, Perkins ND, Hay RT, Gu W, Pestell RG. SIRT1 deacetylation and repression of p300 involves lysine residues 1020/1024 within the cell cycle regulatory domain 1. J Biol Chem 280: 10264-10276, 2005.
9. Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84: 843-851, 1996.
10. Cano A, Pestana A. Purification and properties of a histone acetyltransferase from Artemia salina, highly efficient with H1 histone. Eur J Biochem 97: 65-72, 1979.
11. Chen Y, Zhao W, Yang JS, Cheng Z, Luo H, Lu Z, Tan M, Gu W, Zhao Y. Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways. Mol Cell Proteomics 11: 1048-1062, 2012.
12. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325: 834-840, 2009.
13. Coste A, Louet JF, Lagouge M, Lerin C, Antal MC, Meziane H, Schoonjans K, Puigserver P, O’Malley BW, Auwerx J. The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1. Proc Natl Acad Sci USA 105: 17187-17192, 2008.
14. Dominy JE, Jr., Lee Y, Gerhart-Hines Z, Puigserver P. Nutrient-dependent regulation of PGC-1 ’s acetylation state and metabolic function through the enzymatic activities of Sirt1/GCN5. Biochim Biophys Acta 1804: 1676-1683, 2010.
15. Dominy JE, Jr., Lee Y, Jedrychowski MP, Chim H, Jurczak MJ, Camporez JP, Ruan HB, Feldman J, Pierce K, Mostoslavsky R, Denu JM, Clish CB, Yang X, Shulman GI, Gygi SP, Puigserver P. The deacetylase Sirt6 activates the acetyltransferase GCN5 and suppresses hepatic gluconeogenesis. Mol Cell 48: 900-913, 2012.
16. Eckner R, Ewen ME, Newsome D, Gerdes M, DeCaprio JA, Lawrence JB, Livingston DM. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev 8: 869-884, 1994.
17. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, Milne JC, Lambert PD, Mataki C, Elliott PJ, Auwerx J. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab 8: 347-358, 2008.
18. Fenton TR, Gwalter J, Cramer R, Gout IT. S6K1 is acetylated at lysine 516 in response to growth factor stimulation. Biochem Biophys Res Commun 398: 400-405, 2010.
19. Fenton TR, Gwalter J, Ericsson J, Gout IT. Histone acetyltransferases interact with and acetylate p70 ribosomal S6 kinases in vitro and in vivo. Int J Biochem Cell Biol 42: 359-366, 2010.
20. Fernandez-Marcos PJ, Jeninga EH, Canto C, Harach T, de Boer VC, Andreux P, Moullan N, Pirinen E, Yamamoto H, Houten SM, Schoonjans K, Auwerx J. Muscle or liver-specific Sirt3 deficiency induces hyperacetylation of mitochondrial proteins without affecting global metabolic homeostasis. Sci Rep 2: 425, 2012.
21. Finkel T, Deng CX, Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 460: 587-591, 2009.
22. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1 EMBO J 26: 1913-1923, 2007.
23. Gnad F, Ren S, Cox J, Olsen JV, Macek B, Oroshi M, Mann M. PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biol 8: R250, 2007.
24. Guarente L. Franklin H. Epstein lecture: Sirtuins, aging, and medicine. N Engl J Med 364: 2235-2244, 2011.
25. Guarente L. The logic linking protein acetylation and metabolism. Cell Metab 14: 151-153, 2011.
26. Guarente L. Sirtuins as potential targets for metabolic syndrome. Nature 444: 868-874, 2006.
27. Gupta MP, Samant SA, Smith SH, Shroff SG. HDAC4 and PCAF bind to cardiac sarcomeres and play a role in regulating myofilament contractile activity. J Biol Chem 283: 10135-10146, 2008.
28. Gusterson RJ, Jazrawi E, Adcock IM, Latchman DS. The transcriptional co-activators CREB-binding protein (CBP) and p300 play a critical role in cardiac hypertrophy that is dependent on their histone acetyltransferase activity. J Biol Chem 278: 6838-6847, 2003.
29. Gut P, Verdin E. The nexus of chromatin regulation and intermediary metabolism. Nature 502: 489-498, 2013.
30. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10: 32-42, 2009.
31. Haigis MC, Sinclair DA. Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5: 253-295, 2010.
32. Hebbes TR, Thorne AW, Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 7: 1395-1402, 1988.
33. Hecht A, Laroche T, Strahl-Bolsinger S, Gasser SM, Grunstein M. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80: 583-592, 1995.
34. Hirschey MD, Shimazu T, Jing E, Grueter CA, Collins AM, Aouizerat B, Stancakova A, Goetzman E, Lam MM, Schwer B, Stevens RD, Muehlbauer MJ, Kakar S, Bass NM, Kuusisto J, Laakso M, Alt FW, Newgard CB, Farese RV, Jr., Kahn CR, Verdin E. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell 44: 177-190, 2011.
35. Hunter T. The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell 28: 730-738, 2007.
36. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, Villen J, Haas W, Sowa ME, Gygi SP. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143: 1174-1189, 2010.
37. Kalkhoven E. CBP and p300: HATs for different occasions. Biochem Pharmacol 68: 1145-1155, 2004.
38. Kelly TJ, Lerin C, Haas W, Gygi SP, Puigserver P. GCN5-mediated transcriptional control of the metabolic coactivator PGC-1 through lysine acetylation. J Biol Chem 284: 19945-19952, 2009.
39. Kim JW, Jang SM, Kim CH, An JH, Kang EJ, Choi KH. Tip60 regulates myoblast differentiation by enhancing the transcriptional activity of MyoD via their physical interactions. FEBS J 278: 4394-4404, 2011.
40. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23: 607-618, 2006.
41. Kiran S, Chatterjee N, Singh S, Kaul SC, Wadhwa R, Ramakrishna G. Intracellular distribution of human SIRT7 and mapping of the nuclear/ nucleolar localization signal. FEBS J 280: 3451-3466, 2013.
42. Koltai E, Szabo Z, Atalay M, Boldogh I, Naito H, Goto S, Nyakas C, Radak Z. Exercise alters SIRT1, SIRT6, NAD and NAMPT levels in skeletal muscle of aged rats. Mech Ageing Dev 131: 21-28, 2010.
43. Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370: 223-226, 1994.
44. Lahue RS, Frizzell A. Histone deacetylase complexes as caretakers of genome stability. Epigenetics 7: 806-810, 2012.
45. Lee KK, Workman JL. Histone acetyltransferase complexes: one size doesn’t fit all. Nat Rev Mol Cell Biol 8: 284-295, 2007.
46. Lerin C, Rodgers JT, Kalume DE, Kim SH, Pandey A, Puigserver P. GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1. Cell Metab 3: 429-438, 2006.
47. Lundby A, Lage K, Weinert BT, Bekker-Jensen DB, Secher A, Skovgaard T, Kelstrup CD, Dmytriyev A, Choudhary C, Lundby C, Olsen JV. Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep 2: 419-431, 2012.
48. Lundby A, Secher A, Lage K, Nordsborg NB, Dmytriyev A, Lundby C, Olsen JV. Quantitative maps of protein phosphorylation sites across 14 different rat organs and tissues. Nat Commun 3: 876, 2012.
49. Malik R, Nigg EA, Korner R. Comparative conservation analysis of the human mitotic phosphoproteome. Bioinformatics 24: 1426-1432, 2008.
50. McGee SL, Hargreaves M. Histone modifications and exercise adaptations. J Appl Physiol 110: 258-263, 2011.
51. McKinsey TA, Zhang CL, Olson EN. Control of muscle development by dueling HATs and HDACs. Curr Opin Genet Dev 11: 497-504, 2001.
52. Meissner JD, Freund R, Krone D, Umeda PK, Chang KC, Gros G, Scheibe RJ. Extracellular signal-regulated kinase 1/2-mediated phosphorylation of p300 enhances myosin heavy chain I/ gene expression via acetylation of nuclear factor of activated T cells c1. Nucleic Acids Res 39: 5907-5925, 2011.
53. Meissner JD, Umeda PK, Chang KC, Gros G, Scheibe RJ. Activation of the-myosin heavy chain promoter by MEF-2D, MyoD, p300, and the calcineurin/NFATc1 pathway. J Cell Physiol 211: 138-148, 2007.
54. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, Boss O, Perni RB, Vu CB, Bemis JE, Xie R, Disch JS, Ng PY, Nunes JJ, Lynch AV, Yang H, Galonek H, Israelian K, Choy W, Iffland A, Lavu S, Medvedik O, Sinclair DA, Olefsky JM, Jirousek MR, Elliott PJ, Westphal CH. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450: 712-716, 2007.
55. Nagy Z, Tora L. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26: 5341-5357, 2007.
56. Nogueiras R, Habegger KM, Chaudhary N, Finan B, Banks AS, Dietrich MO, Horvath TL, Sinclair DA, Pfluger PT, Tschop MH. Sirtuin 1 and sirtuin 3: physiological modulators of metabolism. Physiol Rev 92: 1479-1514, 2012.
57. Norvell A, McMahon SB. Cell biology. Rise of the rival. Science 327: 964-965, 2010.
58. Philp A, Chen A, Lan D, Meyer GA, Murphy AN, Knapp AE, Olfert IM, McCurdy CE, Marcotte GR, Hogan MC, Baar K, Schenk S. Sirtuin 1 (SIRT1) deacetylase activity is not required for mitochondrial biogenesis or peroxisome proliferator-activated receptorcoactivator-1 (PGC-1) deacetylation following endurance exercise. J Biol Chem 286: 30561-30570, 2011.
59. Philp A, Schenk S. Unraveling the complexities of SIRT1-mediated mitochondrial regulation in skeletal muscle. Exerc Sport Sci Rev 41: 174-181, 2013.
60. Potthoff MJ, Wu H, Arnold MA, Shelton JM, Backs J, McAnally J, Richardson JA, Bassel-Duby R, Olson EN. Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J Clin Invest 117: 2459-2467, 2007.
61. Puigserver P, Adelmant G, Wu Z, Fan M, Xu J, O’Malley B, Spiegelman BM. Activation of PPAR coactivator-1 through transcription factor docking. Science 286: 1368-1371, 1999.
62. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem 70: 81-120, 2001.
63. Ruiz-Carrillo A, Wangh LJ, Allfrey VG. Processing of newly synthesized histone molecules. Science 190: 117-128, 1975.
64. Sartorelli V, Huang J, Hamamori Y, Kedes L. Molecular mechanisms of myogenic coactivation by p300: direct interaction with the activation domain of MyoD and with the MADS box of MEF2C. Mol Cell Biol 17: 1010-1026, 1997.
65. Scott I, Webster BR, Li JH, Sack MN. Identification of a molecular component of the mitochondrial acetyltransferase programme: a novel role for GCN5L1. Biochem J 443: 655-661, 2012.
66. Senf SM, Sandesara PB, Reed SA, Judge AR. p300 Acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol 300: C1490-C1501, 2011.
67. Sol EM, Wagner SA, Weinert BT, Kumar A, Kim HS, Deng CX, Choudhary C. Proteomic investigations of lysine acetylation identify diverse substrates of mitochondrial deacetylase sirt3. PLos One 7: e50545, 2012.
68. Still AJ, Floyd BJ, Hebert AS, Bingman CA, Carson JJ, Gunderson DR, Dolan BK, Grimsrud PA, Dittenhafer-Reed KE, Stapleton DS, Keller MP, Westphall MS, Denu JM, Attie AD, Coon JJ, Pagliarini DJ. Quantification of mitochondrial acetylation dynamics highlights prominent sites of metabolic regulation. J Biol Chem 288: 26209-26219, 2013.
69. Sutendra G, Kinnaird A, Dromparis P, Paulin R, Stenson TH, Haromy A, Hashimoto K, Zhang N, Flaim E, Michelakis ED. A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 158: 84-97, 2014.
70. Thai MV, Guruswamy S, Cao KT, Pessin JE, Olson AL. Myocyte enhancer factor 2 (MEF2)-binding site is required for GLUT4 gene expression in transgenic mice. Regulation of MEF2 DNA binding activity in insulin-deficient diabetes. J Biol Chem 273: 14285-14292, 1998.
71. Tse C, Sera T, Wolffe AP, Hansen JC. Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol Cell Biol 18: 4629-4638, 1998.
72. Wagner GR, Payne RM. Widespread and enzyme-independent Nε-acetylation and Nε-succinylation of proteins in the chemical conditions of the mitochondrial matrix. J Biol Chem 288: 29036-29045, 2013.
73. Wallberg AE, Yamamura S, Malik S, Spiegelman BM, Roeder RG. Coordination of p300-mediated chromatin remodeling and TRAP/ mediator function through coactivator PGC-1. Mol Cell 12: 1137-1149, 2003.
74. Wang L, Tang Y, Cole PA, Marmorstein R. Structure and chemistry of the p300/CBP and Rtt109 histone acetyltransferases: implications for histone acetyltransferase evolution and function. Curr Opin Struct Biol 18: 741-747, 2008.
75. Wang Q, Zhang Y, Yang C, Xiong H, Lin Y, Yao J, Li H, Xie L, Zhao W, Yao Y, Ning ZB, Zeng R, Xiong Y, Guan KL, Zhao S, Zhao GP. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327: 1004-1007, 2010.
76. Wangh L, Ruiz-Carrillo A, Allfrey VG. Separation and analysis of histone subfractions differing in their degree of acetylation: some correlations with genetic activity in development. Arch Biochem Biophys 150: 44-56, 1972.
77. Weinert BT, Iesmantavicius V, Wagner SA, Scholz C, Gummesson B, Beli P, Nystrom T, Choudhary C. Acetyl-phosphate is a critical determinant of lysine acetylation in E. coli. Mol Cell 51: 265-272, 2013.
78. Yang L, Vaitheesvaran B, Hartil K, Robinson AJ, Hoopmann MR, Eng JK, Kurland IJ, Bruce JE. The fasted/fed mouse metabolic acetylome: N6-acetylation differences suggest acetylation coordinates organspecific fuel switching. J Proteome Res 10: 4134-4149, 2011.
79. Yang XJ, Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol Cell 31: 449-461, 2008.
80. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, Yao J, Zhou L, Zeng Y, Li H, Li Y, Shi J, An W, Hancock SM, He F, Qin L, Chin J, Yang P, Chen X, Lei Q, Xiong Y, Guan KL. Regulation of cellular metabolism by protein lysine acetylation. Science 327: 1000-1004, 2010.
81. Zhao X, Sternsdorf T, Bolger TA, Evans RM, Yao TP. Regulation of MEF2 by histone deacetylase 4-and SIRT1 deacetylase-mediated lysine modifications. Mol Cell Biol 25: 8456-8464, 2005.