The Diversity of Histone Versus Nonhistone Sirtuin Substrates

Genes and Cancer

Volumn 4, Issue 3-4, 2013, Pages 148-163

  Martínez Redondo, Paloma ^a   Vaquero, Alejandro ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

Author keywords

deacetylation; epigenetics; genome stability; histones; SIRT1 SIRT7; sirtuins; stress response

Indexed keywords

ACETYL COENZYME A ACYLTRANSFERASE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; HISTONE; HISTONE ACETYLTRANSFERASE; LYSINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NONHISTONE PROTEIN; SIRTUIN; SIRTUIN 2; SIRTUIN 3; SIRTUIN 6; SIRTUIN 7; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FOXO;

DNA DAMAGE; DNA END JOINING REPAIR; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; EXCISION REPAIR; GENETIC CONSERVATION; HISTONE ACETYLATION; HUMAN; INTRACELLULAR SIGNALING; METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSCRIPTION REGULATION;

EID: 84887491976     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601913483767     Document Type: Review

References (201)

1. Sebastian C,Satterstrom FK,Haigis MC,Mostoslavsky R.From sirtuin biology to human diseases: an update.J Biol Chem. 2012;287 (51): 42444-52.
2. Guarente L.Sirtuins in aging and disease.Cold Spring Harb Symp Quant Biol. 2007;72:483-8.
3. Imai S,Johnson FB,Marciniak RA,McVey M,Park PU,Guarente L.Sir2: an NAD-dependent histone deacetylase that connects chromatin silencing, metabolism, and aging.Cold Spring Harb Symp Quant Biol. 2000;65:297-302.
4. Yuan H,Marmorstein R.Structural basis for sirtuin activity and inhibition.J Biol Chem. 2012;287 (51): 42428-35.
5. Hawse WF,Wolberger C.Structure-based mechanism of ADP-ribosylation by sirtuins.J Biol Chem. 2009;284 (48): 33654-61.
6. Du J,Jiang H,Lin H.Investigating the ADP- ribosyltransferase activity of sirtuins with NAD analogues and 32P-NAD.Biochemistry. 2009;48 (13): 2878-90.
7. North BJ,Verdin E.Sirtuins: Sir2-related NAD-dependent protein deacetylases.Genome Biol. 2004;5 (5): 224.
8. Frye RA.Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins.Biochem Biophys Res Commun. 2000;273 (2): 793-8.
9. Bell SD,Botting CH,Wardleworth BN,Jackson SP,White MF.The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation.Science. 2002;296 (5565): 148-51.
10. Jin Q,Yan T,Ge X,Sun C,Shi X,Zhai Q.Cytoplasm-localized SIRT1 enhances apoptosis.J Cell Physiol. 2007;213 (1): 88-97.
11. Tanno M,Sakamoto J,Miura T,Shimamoto K,Horio Y.Nucleocytoplasmic shuttling of the NAD+-dependent histone deacetylase SIRT1.J Biol Chem. 2007;282 (9): 6823-32.
12. Scher MB,Vaquero A,Reinberg D.SirT3 is a nuclear NAD+-dependent histone deacetylase that translocates to the mitochondria upon cellular stress.Genes Dev. 2007;21 (8): 920-8.
13. Michishita E,Park JY,Burneskis JM,Barrett JC,Horikawa I.Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins.Mol Biol Cell. 2005;16 (10): 4623-35.
14. North BJ,Verdin E.Interphase nucleo-cytoplasmic shuttling and localization of SIRT2 during mitosis.PLoS One. 2007;2 (8): e784.
15. Frye RA.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. 1999;260 (1): 273-9.
16. Mead J,McCord R,Youngster L,Sharma M,Gartenberg MR,Vershon AK.Swapping the gene-specific and regional silencing specificities of the Hst1 and Sir2 histone deacetylases.Mol Cell Biol. 2007;27 (7): 2466-75.
17. Zhao K,Chai X,Clements A,Marmorstein R.Structure and autoregulation of the yeast Hst2 homolog of Sir2.Nat Struct Biol. 2003;10 (10): 864-71.
18. Flick F,Luscher B.Regulation of sirtuin function by posttranslational modifications.Front Pharmacol. 2012;3:29.
19. Greiss S,Gartner A.Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation.Mol Cells. 2009;28 (5): 407-15.
20. Finnin MS,Donigian JR,Pavletich NP.Structure of the histone deacetylase SIRT2.Nat Struct Biol. 2001;8 (7): 621-5.
21. Holbert MA,Marmorstein R.Structure and activity of enzymes that remove histone modifications.Curr Opin Struct Biol. 2005;15 (6): 673-80.
22. Sauve AA,Celic I,Avalos J,Deng H,Boeke JD,Schramm VL.Chemistry of gene silencing: the mechanism of NAD+-dependent deacetylation reactions.Biochemistry. 2001;40 (51): 15456-63.
23. Kustatscher G,Hothorn M,Pugieux C,Scheffzek K,Ladurner AG.Splicing regulates NAD metabolite binding to histone macroH2A.Nat Struct Mol Biol. 2005;12 (7): 624-5.
24. Grubisha O,Rafty LA,Takanishi CL,et al.Metabolite of SIR2 reaction modulates TRPM2 ion channel.J Biol Chem. 2006;281 (20): 14057-65.
25. Liou GG,Tanny JC,Kruger RG,Walz T,Moazed D.Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation.Cell. 2005;121 (4): 515-27.
26. Tanny JC,Dowd GJ,Huang J,Hilz H,Moazed D.An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing.Cell. 1999;99 (7): 735-45.
27. Hassa PO,Haenni SS,Elser M,Hottiger MO.Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going?.Microbiol Mol Biol Rev. 2006;70 (3): 789-829.
28. Fahie K,Hu P,Swatkoski S,Cotter RJ,Zhang Y,Wolberger C.Side chain specificity of ADP-ribosylation by a sirtuin.FEBS J. 2009;276 (23): 7159-76.
29. Mao Z,Tian X,Van Meter M,Ke Z,Gorbunova V,Seluanov A.Sirtuin 6 (SIRT6) rescues the decline of homologous recombination repair during replicative senescence.Proc Natl Acad Sci U S A. 2012;109 (29): 11800-5.
30. Du J,Zhou Y,Su X,et al.Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase.Science. 2012;334 (6057): 806-9.
31. French JB,Cen Y,Sauve AA.Plasmodium falciparum Sir2 is an NAD+-dependent deacetylase and an acetyllysine-dependent and acetyllysine-independent NAD+ glycohydrolase.Biochemistry. 2008;47 (38): 10227-39.
32. Tsang AW,Escalante-Semerena JC.CobB, a new member of the SIR2 family of eucaryotic regulatory proteins, is required to compensate for the lack of nicotinate mononucleotide: 5,6-dimethylbenzimidazole phosphoribosyltransferase activity in CobT mutants during cobalamin biosynthesis in Salmonella typhimurium LT2.J Biol Chem. 1998;273 (48): 31788-94.
33. Tsang AW,Escalante-Semerena JC.CobB function is required for catabolism of propionate in Salmonella typhimurium LT2: evidence for existence of a substitute function for CobB within the 1,2-propanediol utilization (pdu) operon.J Bacteriol. 1996;178 (23): 7016-9.
34. Vaziri H,Dessain SK,Ng Eaton E,et al.hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 2001;107 (2): 149-59.
35. Langley E,Pearson M,Faretta M,et al.Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence.EMBO J. 2002;21 (10): 2383-96.
36. Luo J,Nikolaev AY,Imai S,et al.Negative control of p53 by Sir2alpha promotes cell survival under stress.Cell. 2001;107 (2): 137-48.
37. Blander G,Olejnik J,Krzymanska-Olejnik E,et al.SIRT1 shows no substrate specificity in vitro.J Biol Chem. 2005;280 (11): 9780-5.
38. Khan AN,Lewis PN.Unstructured conformations are a substrate requirement for the Sir2 family of NAD-dependent protein deacetylases.J Biol Chem. 2005;280 (43): 36073-8.
39. Kuzmichev A,Margueron R,Vaquero A,et al.Composition and histone substrates of Polycomb repressive group complexes change during cellular differentiation.Proc Natl Acad Sci U S A. 2005;102 (6): 1859-64.
40. Furuyama T,Kitayama K,Shimoda Y,et al.Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice.J Biol Chem. 2004;279 (33): 34741-9.
41. Fulco M,Schiltz RL,Iezzi S,et al.Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state.Mol Cell. 2003;12 (1): 51-62.
42. Picard F,Kurtev M,Chung N,et al.Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature. 2004;429 (6993): 771-6.
43. Zhang F,Wang S,Gan L,et al.Protective effects and mechanisms of sirtuins in the nervous system.Prog Neurobiol. 2011;95 (3): 373-95.
44. Mancio-Silva L,Lopez-Rubio JJ,Claes A,Scherf A.Sir2a regulates rDNA transcription and multiplication rate in the human malaria parasite Plasmodium falciparum.Nat Commun. 2012 1530;4:.
45. Goyal M,Alam A,Iqbal MS,et al.Identification and molecular characterization of an Alba-family protein from human malaria parasite Plasmodium falciparum.Nucleic Acids Res. 2012;40 (3): 1174-90.
46. Kaeberlein M,McVey M,Guarente L.The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms.Genes Dev. 1999;13 (19): 2570-80.
47. Cockell MM,Perrod S,Gasser SM.Analysis of Sir2p domains required for rDNA and telomeric silencing in Saccharomyces cerevisiae.Genetics. 2000;154 (3): 1069-83.
48. Freeman-Cook LL,Gomez EB,Spedale EJ,et al.Conserved locus-specific silencing functions of Schizosaccharomyces pombe sir2+.Genetics. 2005;169 (3): 1243-60.
49. Kyes SA,Kraemer SM,Smith JD.Antigenic variation in Plasmodium falciparum: gene organization and regulation of the var multigene family.Eukaryot Cell. 2007;6 (9): 1511-20.
50. Tonkin CJ,Carret CK,Duraisingh MT,et al.Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum.PLoS Biol. 2009;7 (4): e84.
51. Trojer P,Reinberg D.Facultative heterochromatin: is there a distinctive molecular signature?.Mol Cell. 2007;28 (1): 1-13.
52. Shankaranarayana GD,Motamedi MR,Moazed D,Grewal SI.Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast.Curr Biol. 2003;13 (14): 1240-6.
53. Vaquero A,Scher M,Erdjument-Bromage H,Tempst P,Serrano L,Reinberg D.SIRT1 regulates the histone methyl-transferase SUV39H1 during heterochromatin formation.Nature. 2007;450 (7168): 440-4.
54. Bosch-Presegue L,Vaquero A.The dual role of sirtuins in cancer.Genes Cancer. 2011;2 (6): 648-62.
55. Kruszewski M,Szumiel I.Sirtuins (histone deacetylases III) in the cellular response to DNA damage: facts and hypotheses.DNA Repair (Amst). 2005;4 (11): 1306-13.
56. Vaquero A,Scher M,Lee D,Erdjument-Bromage H,Tempst P,Reinberg D.Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin.Mol Cell. 2004;16 (1): 93-105.
57. Vaquero A.The conserved role of sirtuins in chromatin regulation.Int J Dev Biol. 2009;53 (2-3): 303-22.
58. Megee PC,Morgan BA,Mittman BA,Smith MM.Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation.Science. 1990;247 (4944): 841-5.
59. Bird AW,Yu DY,Pray-Grant MG,et al.Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair.Nature. 2002;419 (6905): 411-5.
60. Schwaiger M,Stadler MB,Bell O,Kohler H,Oakeley EJ,Schubeler D.Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome.Genes Dev. 2009;23 (5): 589-601.
61. Fraga MF,Ballestar E,Villar-Garea A,et al.Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer.Nat Genet. 2005;37 (4): 391-400.
62. Vaquero A,Scher MB,Lee DH,et al.SirT2 is a histone deacetylase with preference for histone H4 Lys 16 during mitosis.Genes Dev. 2006;20 (10): 1256-61.
63. Krauss V.Glimpses of evolution: heterochromatic histone H3K9 methyltransferases left its marks behind.Genetica. 2008;133 (1): 93-106.
64. McCord RA,Michishita E,Hong T,et al.SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair.Aging (Albany NY). 2009;1 (1): 109-21.
65. He W,Newman JC,Wang MZ,Ho L,Verdin E.Mitochondrial sirtuins: regulators of protein acylation and metabolism.Trends Endocrinol Metab. 2012;23 (9): 467-76.
66. Iwahara T,Bonasio R,Narendra V,Reinberg D.SIRT3 functions in the nucleus in the control of stress-related gene expression.Mol Cell Biol. 2012;32 (24): 5022-34.
67. Barber MF,Michishita-Kioi E,Xi Y,et al.SIRT7 links H3K18 deacetylation to maintenance of oncogenic transformation.Nature. 2012;487 (7405): 114-8.
68. Ford E,Voit R,Liszt G,Magin C,Grummt I,Guarente L.Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription.Genes Dev. 2006;20 (9): 1075-80.
69. Armstrong CM,Kaeberlein M,Imai SI,Guarente L.Mutations in Saccharomyces cerevisiae gene SIR2 can have differential effects on in vivo silencing phenotypes and in vitro histone deacetylation activity.Mol Biol Cell. 2002;13 (4): 1427-38.
70. Yuan J,Pu M,Zhang Z,Lou Z.Histone H3-K56 acetylation is important for genomic stability in mammals.Cell Cycle. 2009;8 (11): 1747-53.
71. Michishita E,McCord RA,Boxer LD,et al.Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6.Cell Cycle. 2009;8 (16): 2664-6.
72. Celic I,Masumoto H,Griffith WP,et al.The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation.Curr Biol. 2006;16 (13): 1280-9.
73. Vempati RK,Jayani RS,Notani D,Sengupta A,Galande S,Haldar D.p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals.J Biol Chem. 2010;285 (37): 28553-64.
74. Garcia-Salcedo JA,Gijon P,Nolan DP,Tebabi P,Pays E.A chromosomal SIR2 homologue with both histone NAD-dependent ADP-ribosyltransferase and deacetylase activities is involved in DNA repair in Trypanosoma brucei.EMBO J. 2003;22 (21): 5851-62.
75. Wirth M,Paap F,Fischle W,et al.HIS-24 linker histone and SIR-2.1 deacetylase induce H3K27me3 in the Caenorhabditis elegans germ line.Mol Cell Biol. 2009;29 (13): 3700-9.
76. Jedrusik MA,Schulze E.Linker histone HIS-24 (H1.1) cytoplasmic retention promotes germ line development and influences histone H3 methylation in Caenorhabditis elegans.Mol Cell Biol. 2007;27 (6): 2229-39.
77. Li JY,Patterson M,Mikkola HK,Lowry WE,Kurdistani SK.Dynamic distribution of linker histone H1.5 in cellular differentiation.PLoS Genet. 2012;8 (8): e1002879.
78. Pruitt K,Zinn RL,Ohm JE,et al.Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation.PLoS Genet. 2006;2 (3): e40.
79. Espada J,Ballestar E,Santoro R,et al.Epigenetic disruption of ribosomal RNA genes and nucleolar architecture in DNA methyltransferase 1 (Dnmt1) deficient cells.Nucleic Acids Res. 2007;35 (7): 2191-8.
80. Peng L,Yuan Z,Ling H,et al.SIRT1 deacetylates the DNA methyltransferase 1 (DNMT1) protein and alters its activities.Mol Cell Biol. 2011;31 (23): 4720-34.
81. 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 U S A. 1964;51:786-94.
82. Brownell JE,Allis CD.Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation.Curr Opin Genet Dev. 1996;6 (2): 176-84.
83. Taunton J,Hassig CA,Schreiber SL.A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p.Science. 1996;272 (5260): 408-11.
84. Gu W,Roeder RG.Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain.Cell. 1997;90 (4): 595-606.
85. Glozak MA,Sengupta N,Zhang X,Seto E.Acetylation and deacetylation of non-histone proteins.Gene. 2005;363:15-23.
86. Garcia-Cao M,O'Sullivan R,Peters AH,Jenuwein T,Blasco MA.Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases.Nat Genet. 2004;36 (1): 94-9.
87. Bosch-Presegue L,Raurell-Vila H,Marazuela-Duque A,et al.Stabilization of Suv39H1 by SirT1 is part of oxidative stress response and ensures genome protection.Mol Cell. 2010;42 (2): 210-23.
88. Murayama A,Ohmori K,Fujimura A,et al.Epigenetic control of rDNA loci in response to intracellular energy status.Cell. 2008;133 (4): 627-39.
89. Das C,Lucia MS,Hansen KC,Tyler JK.CBP/p300-mediated acetylation of histone H3 on lysine 56.Nature. 2009;459 (7243): 113-7.
90. Szerlong HJ,Prenni JE,Nyborg JK,Hansen JC.Activator-dependent p300 acetylation of chromatin in vitro: enhancement of transcription by disruption of repressive nucleosome-nucleosome interactions.J Biol Chem. 2010;285 (42): 31954-64.
91. Bouras T,Fu M,Sauve AA,et al.SIRT1 deacetylation and repression of p300 involves lysine residues 1020/1024 within the cell cycle regulatory domain 1.J Biol Chem. 2005;280 (11): 10264-76.
92. Black JC,Mosley A,Kitada T,Washburn M,Carey M.The SIRT2 deacetylase regulates autoacetylation of p300.Mol Cell. 2008;32 (3): 449-55.
93. Albaugh BN,Arnold KM,Lee S,Denu JM.Autoacetylation of the histone acetyltransferase Rtt109.J Biol Chem. 2011;286 (28): 24694-701.
94. Gu W,Szauter P,Lucchesi JC.Targeting of MOF, a putative histone acetyl transferase, to the X chromosome of Drosophila melanogaster.Dev Genet. 1998;22 (1): 56-64.
95. Akhtar A,Becker PB.Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila.Mol Cell. 2000;5 (2): 367-75.
96. Lu L,Li L,Lv X,Wu XS,Liu DP,Liang CC.Modulations of hMOF autoacetylation by SIRT1 regulate hMOF recruitment and activities on the chromatin.Cell Res. 2011;21 (8): 1182-95.
97. Yamagata K,Kitabayashi I.Sirt1 physically interacts with Tip60 and negatively regulates Tip60-mediated acetylation of H2AX.Biochem Biophys Res Commun. 2009;390 (4): 1355-60.
98. Wang J,Chen J.SIRT1 regulates autoacetylation and histone acetyltransferase activity of TIP60.J Biol Chem. 2010;285 (15): 11458-64.
99. Mostoslavsky R,Chua KF,Lombard DB,et al.Genomic instability and aging-like phenotype in the absence of mammalian SIRT6.Cell. 2006;124 (2): 315-29.
100. Kaidi A,Weinert BT,Choudhary C,Jackson SP.Human SIRT6 promotes DNA end resection through CtIP deacetylation.Science. 2010;329 (5997): 1348-53.
101. Religa AA,Waters AP.Sirtuins of parasitic protozoa: in search of function(s).Mol Biochem Parasitol. 2012;185 (2): 71-88.
102. Yuan Z,Seto E.A functional link between SIRT1 deacetylase and NBS1 in DNA damage response.Cell Cycle. 2007;6 (23): 2869-71.
103. Fan W,Luo J.SIRT1 regulates UV-induced DNA repair through deacetylating XPA.Mol Cell. 2010;39 (2): 247-58.
104. Rajamohan SB,Pillai VB,Gupta M,et al.SIRT1 promotes cell survival under stress by deacetylation-dependent deactivation of poly(ADP-ribose) polymerase 1.Mol Cell Biol. 2009;29 (15): 4116-29.
105. Hassa PO,Buerki C,Lombardi C,Imhof R,Hottiger MO.Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1.J Biol Chem. 2003;278 (46): 45145-53.
106. Hassa PO,Haenni SS,Buerki C,et al.Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription.J Biol Chem. 2005;280 (49): 40450-64.
107. Cohen HY,Miller C,Bitterman KJ,et al.Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase.Science. 2004;305 (5682): 390-2.
108. Jeong J,Juhn K,Lee H,et al.SIRT1 promotes DNA repair activity and deacetylation of Ku70.Exp Mol Med. 2007;39 (1): 8-13.
109. Thrower DA,Bloom K.Dicentric chromosome stretching during anaphase reveals roles of Sir2/Ku in chromatin compaction in budding yeast.Mol Biol Cell. 2001;12 (9): 2800-12.
110. Martin SG,Laroche T,Suka N,Grunstein M,Gasser SM.Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast.Cell. 1999;97 (5): 621-33.
111. Tang Y,Zhao W,Chen Y,Zhao Y,Gu W.Acetylation is indispensable for p53 activation.Cell. 2008;133 (4): 612-26.
112. Yi J,Luo J.SIRT1 and p53, effect on cancer, senescence and beyond.Biochim Biophys Acta. 2010;1804 (8): 1684-9.
113. Liu L,Scolnick DM,Trievel RC,et al.p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage.Mol Cell Biol. 1999;19 (2): 1202-9.
114. Wang YH,Tsay YG,Tan BC,Lo WY,Lee SC.Identification and characterization of a novel p300-mediated p53 acetylation site, lysine 305.J Biol Chem. 2003;278 (28): 25568-76.
115. D'Erchia AM,Tullo A,Lefkimmiatis K,Saccone C,Sbisa E.The fatty acid synthase gene is a conserved p53 family target from worm to human.Cell Cycle. 2006;5 (7): 750-8.
116. Cheng HL,Mostoslavsky R,Saito S,et al.Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice.Proc Natl Acad Sci U S A. 2003;100 (19): 10794-9.
117. Peck B,Chen CY,Ho KK,et al.SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2.Mol Cancer Ther. 2010;9 (4): 844-55.
118. Li S,Banck M,Mujtaba S,Zhou MM,Sugrue MM,Walsh MJ.p53-induced growth arrest is regulated by the mitochondrial SirT3 deacetylase.PLoS One. 2010;5 (5): e10486.
119. Wang F,Nguyen M,Qin FX,Tong Q.SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction.Aging Cell. 2007;6 (4): 505-14.
120. Liu L,Arun A,Ellis L,Peritore C,Donmez G.Sirtuin 2 (SIRT2) enhances 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced nigrostriatal damage via deacetylating forkhead box O3a (Foxo3a) and activating Bim protein.J Biol Chem. 2012;287 (39): 32307-11.
121. Daitoku H,Hatta M,Matsuzaki H,et al.Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity.Proc Natl Acad Sci U S A. 2004;101 (27): 10042-7.
122. van der Horst A,Tertoolen LG,de Vries-Smits LM,Frye RA,Medema RH,Burgering BM.FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1).J Biol Chem. 2004;279 (28): 28873-9.
123. Motta MC,Divecha N,Lemieux M,et al.Mammalian SIRT1 represses forkhead transcription factors.Cell. 2004;116 (4): 551-63.
124. Yang Y,Hou H,Haller EM,Nicosia SV,Bai W.Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation.EMBO J. 2005;24 (5): 1021-32.
125. Jing E,Gesta S,Kahn CR.SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation.Cell Metab. 2007;6 (2): 105-14.
126. Jacobs KM,Pennington JD,Bisht KS,et al.SIRT3 interacts with the daf-16 homolog FOXO3a in the mitochondria, as well as increases FOXO3a dependent gene expression.Int J Biol Sci. 2008;4 (5): 291-9.
127. Rodriguez-Colman MJ,Reverter-Branchat G,Sorolla MA,Tamarit J,Ros J,Cabiscol E.The forkhead transcription factor Hcm1 promotes mitochondrial biogenesis and stress resistance in yeast.J Biol Chem. 2010;285 (47): 37092-101.
128. Frescas D,Valenti L,Accili D.Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes.J Biol Chem. 2005;280 (21): 20589-95.
129. Peserico A,Chiacchiera F,Grossi V,et al.A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels.Cell Mol Life Sci. 2013;:.
130. Rizki G,Iwata TN,Li J,et al.The evolutionarily conserved longevity determinants HCF-1 and SIR-2.1/SIRT1 collaborate to regulate DAF-16/FOXO.PLoS Genet. 2011;7 (9): e1002235.
131. Menssen A,Hydbring P,Kapelle K,et al.The c-MYC oncoprotein, the NAMPT enzyme, the SIRT1-inhibitor DBC1, and the SIRT1 deacetylase form a positive feedback loop.Proc Natl Acad Sci U S A. 2012;109 (4): E187-96.
132. Marshall GM,Liu PY,Gherardi S,et al.SIRT1 promotes N-Myc oncogenesis through a positive feedback loop involving the effects of MKP3 and ERK on N-Myc protein stability.PLoS Genet. 2011;7 (6): e1002135.
133. Liu PY,Xu N,Malyukova A,et al.The histone deacetylase SIRT2 stabilizes Myc oncoproteins.Cell Death Differ. 2013;20 (3): 503-14.
134. Zhang R,Chen HZ,Liu JJ,et al.SIRT1 suppresses activator protein-1 transcriptional activity and cyclooxygenase-2 expression in macrophages.J Biol Chem. 2010;285 (10): 7097-110.
135. Mayo MW,Baldwin AS.The transcription factor NF-kappaB: control of oncogenesis and cancer therapy resistance.Biochim Biophys Acta. 2000;1470 (2): M55-62.
136. Karin M,Lin A.NF-kappaB at the crossroads of life and death.Nat Immunol. 2002;3 (3): 221-7.
137. Rothgiesser KM,Erener S,Waibel S,Luscher B,Hottiger MO.SIRT2 regulates NF-kappaB dependent gene expression through deacetylation of p65 Lys310.J Cell Sci. 2010;123 (Pt 24): 4251-8.
138. Rothgiesser KM,Fey M,Hottiger MO.Acetylation of p65 at lysine 314 is important for late NF-kappaB-dependent gene expression.BMC Genomics. 2010;11:22.
139. Lim JH,Lee YM,Chun YS,Chen J,Kim JE,Park JW.Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha.Mol Cell. 2010;38 (6): 864-78.
140. Zhong L,D'Urso A,Toiber D,et al.The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha.Cell. 2009;140 (2): 280-93.
141. Wang C,Chen L,Hou X,et al.Interactions between E2F1 and SirT1 regulate apoptotic response to DNA damage.Nat Cell Biol. 2006;8 (9): 1025-31.
142. Schertel C,Conradt B. C.elegans orthologs of components of the RB tumor suppressor complex have distinct pro-apoptotic functions.Development. 2007;134 (20): 3691-701.
143. de Oliveira RM,Pais TF,Outeiro TF.Sirtuins: common targets in aging and in neurodegeneration.Curr Drug Targets. 2010;11 (10): 1270-80.
144. Starai VJ,Celic I,Cole RN,Boeke JD,Escalante-Semerena JC.Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine.Science. 2002;298 (5602): 2390-2.
145. Gardner JG,Escalante-Semerena JC.In Bacillus subtilis, the sirtuin protein deacetylase, encoded by the srtN gene (formerly yhdZ), and functions encoded by the acuABC genes control the activity of acetyl coenzyme A synthetase.J Bacteriol. 2009;191 (6): 1749-55.
146. Hirschey MD,Shimazu T,Capra JA,Pollard KS,Verdin E.SIRT1 and SIRT3 deacetylate homologous substrates: AceCS1,2 and HMGCS1,2.Aging (Albany NY). 2010;3 (6): 635-42.
147. Starai VJ,Takahashi H,Boeke JD,Escalante-Semerena JC.Short-chain fatty acid activation by acyl-coenzyme A synthetases requires SIR2 protein function in Salmonella enterica and Saccharomyces cerevisiae.Genetics. 2003;163 (2): 545-55.
148. Chan CH,Garrity J,Crosby HA,Escalante-Semerena JC.In Salmonella enterica, the sirtuin-dependent protein acylation/deacylation system (SDPADS) maintains energy homeostasis during growth on low concentrations of acetate.Mol Microbiol. 2011;80 (1): 168-83.
149. Gurd BJ.Deacetylation of PGC-1alpha by SIRT1: importance for skeletal muscle function and exercise-induced mitochondrial biogenesis.Appl Physiol Nutr Metab. 2011;36 (5): 589-97.
150. Rodgers JT,Lerin C,Gerhart-Hines Z,Puigserver P.Metabolic adaptations through the PGC-1 alpha and SIRT1 pathways.FEBS Lett. 2008;582 (1): 46-53.
151. Li X,Zhang S,Blander G,Tse JG,Krieger M,Guarente L.SIRT1 deacetylates and positively regulates the nuclear receptor LXR.Mol Cell. 2007;28 (1): 91-106.
152. Kemper JK,Xiao Z,Ponugoti B,et al.FXR acetylation is normally dynamically regulated by p300 and SIRT1 but constitutively elevated in metabolic disease states.Cell Metab. 2009;10 (5): 392-404.
153. You M,Cao Q,Liang X,Ajmo JM,Ness GC.Mammalian sirtuin 1 is involved in the protective action of dietary saturated fat against alcoholic fatty liver in mice.J Nutr. 2008;138 (3): 497-501.
154. Lan F,Cacicedo JM,Ruderman N,Ido Y.SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1: possible role in AMP-activated protein kinase activation.J Biol Chem. 2008;283 (41): 27628-35.
155. Jiang W,Wang S,Xiao M,et al.Acetylation regulates gluconeogenesis by promoting PEPCK1 degradation via recruiting the UBR5 ubiquitin ligase.Mol Cell. 2011;43 (1): 33-44.
156. Giralt A,Villarroya F.SIRT3, a pivotal actor in mitochondrial functions: metabolism, cell death and aging.Biochem J. 2012;444 (1): 1-10.
157. Tao R,Coleman MC,Pennington JD,et al.Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress.Mol Cell. 2010;40 (6): 893-904.
158. Hallows WC,Lee S,Denu JM.Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases.Proc Natl Acad Sci U S A. 2006;103 (27): 10230-5.
159. Lombard DB,Alt FW,Cheng HL,et al.Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation.Mol Cell Biol. 2007;27 (24): 8807-14.
160. Ahn BH,Kim HS,Song S,et al.A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis.Proc Natl Acad Sci U S A. 2008;105 (38): 14447-52.
161. Cimen H,Han MJ,Yang Y,Tong Q,Koc H,Koc EC.Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria.Biochemistry. 2010;49 (2): 304-11.
162. Lu Z,Bourdi M,Li JH,et al.SIRT3-dependent deacetylation exacerbates acetaminophen hepatotoxicity.EMBO Rep. 2011;12 (8): 840-6.
163. Nakagawa T,Lomb DJ,Haigis MC,Guarente L.SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle.Cell. 2009;137 (3): 560-70.
164. North BJ,Marshall BL,Borra MT,Denu JM,Verdin E.The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase.Mol Cell. 2003;11 (2): 437-44.
165. Du J,Zhou Y,Su X,et al.Sirt5 is a NAD- dependent protein lysine demalonylase and desuccinylase.Science. 2011;334 (6057): 806-9.
166. Zhang Z,Tan M,Xie Z,Dai L,Chen Y,Zhao Y.Identification of lysine succinylation as a new post-translational modification.Nat Chem Biol. 2011;7 (1): 58-63.
167. Peng C,Lu Z,Xie Z,et al.The first identification of lysine malonylation substrates and its regulatory enzyme.Mol Cell Proteomics. 2011;10 (12): M111.012658.
168. Ahuja N,Schwer B,Carobbio S,et al.Regulation of insulin secretion by SIRT4, a mitochondrial ADP-ribosyltransferase.J Biol Chem. 2007;282 (46): 33583-92.
169. Haigis MC,Mostoslavsky R,Haigis KM,et al.SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells.Cell. 2006;126 (5): 941-54.
170. Nasrin N,Wu X,Fortier E,et al.SIRT4 regulates fatty acid oxidation and mitochondrial gene expression in liver and muscle cells.J Biol Chem. 2010;285 (42): 31995-2002.
171. Fakhrai-Rad H,Nikoshkov A,Kamel A,et al.Insulin-degrading enzyme identified as a candidate diabetes susceptibility gene in GK rats.Hum Mol Genet. 2000;9 (14): 2149-58.
172. Li Y,Matsumori H,Nakayama Y,et al.SIRT2 down-regulation in HeLa can induce p53 accumulation via p38 MAPK activation-dependent p300 decrease, eventually leading to apoptosis.Genes Cells. 2011;16 (1): 34-45.
173. Kim HS,Vassilopoulos A,Wang RH,et al.SIRT2 maintains genome integrity and suppresses tumorigenesis through regulating APC/C activity.Cancer Cell. 2011;20 (4): 487-99.
174. Firestein R,Blander G,Michan S,et al.The SIRT1 deacetylase suppresses intestinal tumorigenesis and colon cancer growth.PLoS One. 2008;3 (4): e2020.
175. Narayan N,Lee IH,Borenstein R,et al.The NAD-dependent deacetylase SIRT2 is required for programmed necrosis.Nature. 2012;492 (7428): 199-204.
176. Shulga N,Wilson-Smith R,Pastorino JG.Sirtuin-3 deacetylation of cyclophilin D induces dissociation of hexokinase II from the mitochondria.J Cell Sci. 2010;123 (Pt 6): 894-902.
177. Dryden SC,Nahhas FA,Nowak JE,Goustin AS,Tainsky MA.Role for human SIRT2 NAD-dependent deacetylase activity in control of mitotic exit in the cell cycle.Mol Cell Biol. 2003;23 (9): 3173-85.
178. Inoue T,Hiratsuka M,Osaki M,et al.SIRT2, a tubulin deacetylase, acts to block the entry to chromosome condensation in response to mitotic stress.Oncogene. 2007;26 (7): 945-57.
179. Suzuki K,Koike T.Mammalian Sir2-related protein (SIRT) 2-mediated modulation of resistance to axonal degeneration in slow Wallerian degeneration mice: a crucial role of tubulin deacetylation.Neuroscience. 2007;147 (3): 599-612.
180. Bobrowska A,Donmez G,Weiss A,Guarente L,Bates G.SIRT2 ablation has no effect on tubulin acetylation in brain, cholesterol biosynthesis or the progression of Huntington's disease phenotypes in vivo.PLoS One. 2012;7 (4): e34805.
181. Hubbert C,Guardiola A,Shao R,et al.HDAC6 is a microtubule-associated deacetylase.Nature. 2002;417 (6887): 455-8.
182. Zhang Y,Zhang M,Dong H,et al.Deacetylation of cortactin by SIRT1 promotes cell migration.Oncogene. 2009;28 (3): 445-60.
183. Bonda DJ,Lee HG,Camins A,et al.The sirtuin pathway in ageing and Alzheimer disease: mechanistic and therapeutic considerations.Lancet Neurol. 2011;10 (3): 275-9.
184. Min SW,Cho SH,Zhou Y,et al.Acetylation of tau inhibits its degradation and contributes to tauopathy.Neuron. 2010;67 (6): 953-66.
185. Luijsterburg MS,White MF,van Driel R,Dame RT.The major architects of chromatin: architectural proteins in bacteria, archaea and eukaryotes.Crit Rev Biochem Mol Biol. 2008;43 (6): 393-418.
186. Aravind L,Iyer LM,Anantharaman V.The two faces of Alba: the evolutionary connection between proteins participating in chromatin structure and RNA metabolism.Genome Biol. 2003;4 (10): R64.
187. Verdin E,Hirschey MD,Finley LW,Haigis MC.Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling.Trends Biochem Sci. 2010;35 (12): 669-75.
188. Ammar R,Torti D,Tsui K,et al.Chromatin is an ancient innovation conserved between Archaea and Eukarya.Elife. 2012;1:e00078.
189. Guan KL,Xiong Y.Regulation of intermediary metabolism by protein acetylation.Trends Biochem Sci. 2010;36 (2): 108-16.
190. Lundby A,Lage K,Weinert BT,et al.Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns.Cell Rep. 2012;2 (2): 419-31.
191. Greer EL,Shi Y.Histone methylation: a dynamic mark in health, disease and inheritance.Nat Rev Genet. 2012;13 (5): 343-57.
192. Jeninga EH,Schoonjans K,Auwerx J.Reversible acetylation of PGC-1: connecting energy sensors and effectors to guarantee metabolic flexibility.Oncogene. 2010;29 (33): 4617-24.
193. Giandomenico V,Simonsson M,Gronroos E,Ericsson J.Coactivator-dependent acetylation stabilizes members of the SREBP family of transcription factors.Mol Cell Biol. 2003;23 (7): 2587-99.
194. 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. 2012;443 (3): 655-61.
195. Al-Bassam J,Corbett KD.alpha-tubulin acetylation from the inside out.Proc Natl Acad Sci U S A. 2012;109 (48): 19515-6.
196. Patel JH,Du Y,Ard PG,et al.The c-MYC oncoprotein is a substrate of the acetyltransferases hGCN5/PCAF and TIP60.Mol Cell Biol. 2004;24 (24): 10826-34.
197. Faiola F,Liu X,Lo S,et al.Dual regulation of c-Myc by p300 via acetylation-dependent control of Myc protein turnover and coactivation of Myc-induced transcription.Mol Cell Biol. 2005;25 (23): 10220-34.
198. Van Den Broeck A,Nissou D,Brambilla E,Eymin B,Gazzeri S.Activation of a Tip60/E2F1/ERCC1 network in human lung adenocarcinoma cells exposed to cisplatin.Carcinogenesis. 2011;33 (2): 320-5.
199. Vries RG,Prudenziati M,Zwartjes C,Verlaan M,Kalkhoven E,Zantema A.A specific lysine in c-Jun is required for transcriptional repression by E1A and is acetylated by p300.EMBO J. 2001;20 (21): 6095-103.
200. Geng H,Liu Q,Xue C,et al.HIF1alpha protein stability is increased by acetylation at lysine 709.J Biol Chem. 2012;287 (42): 35496-505.
201. Cohen HY,Lavu S,Bitterman KJ,et al.Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis.Mol Cell. 2004;13 (5): 627-38.