Sub-cellular localization, expression and functions of Sirt6 during the cell cycle in HeLa cells

Nucleus (United States)

Volumn 3, Issue 5, 2012, Pages 442-451

  Ardestani, Pooneh Memar ^a   Liang, Fengyi ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell cycle; Mitosis; Nucleolus; Sirt6; Sirtuin

Indexed keywords

SIRTUIN 6;

ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL NUCLEUS; CELL PROLIFERATION; CHROMOSOME CONDENSATION; CONTROLLED STUDY; HUMAN; INTERPHASE; MITOSIS; MITOSIS SPINDLE; NUCLEOLUS; NUCLEOTIDE SEQUENCE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

MAMMALIA; MUS;

EID: 84866103537     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.21134     Document Type: Article

References (50)

1. Dutnall RN, Pillus L. Deciphering NAD-dependent deacetylases. Cell 2001; 105:161-4; PMID:11336664; http://dx.doi.org/10.1016/S0092-8674(01)00305-1.
2. Blander G, Guarente L. The Sir2 family of protein deacetylases. Annu Rev Biochem 2004; 73:417-35; PMID:15189148; http://dx.doi.org/10.1146/annurev. biochem.73.011303.073651.
3. Gasser SM, Cockell MM. The molecular biology of the SIR proteins. Gene 2001; 279:1-16; PMID:11722841; http://dx.doi.org/10.1016/S0378-1119(01)00741-7.
4. Guarente L. Sir2 links chromatin silencing, metabolism and aging. Genes Dev 2000; 14:1021-6; PMID:10809662.
5. Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000; 403:795-800; PMID:10693811; http://dx.doi. org/10.1038/35001622.
6. Zhang T, Kraus WL. SIRT1-dependent regulation of chromatin and transcription: linking NAD(+) metabolism and signaling to the control of cellular functions. Biochim Biophys Acta 2010; 1804:1666-75; PMID:19879981.
7. Murayama A, Ohmori K, Fujimura A, Minami H, Yasuzawa-Tanaka K, Kuroda T, et al. Epigenetic control of rDNA loci in response to intracellular energy status. Cell 2008; 133:627-39; PMID:18485871; http://dx.doi.org/10.1016/j.cell.2008.03.030.
8. Salminen A, Kaarniranta K. SIRT1 regulates the ribosomal DNA locus: epigenetic candles twinkle longevity in the Christmas tree. Biochem Biophys Res Commun 2009; 378:6-9; PMID:19010308; http://dx.doi.org/10.1016/j.bbrc.2008.11.023.
9. 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; 20:1075-80; PMID:16618798; http://dx.doi. org/10.1101/gad.1399706.
10. Grob A, Roussel P, Wright JE, McStay B, Hernandez-Verdun D, Sirri V. Involvement of SIRT7 in resumption of rDNA transcription at the exit from mitosis. J Cell Sci 2009; 122:489-98; PMID:19174463; http://dx.doi.org/10.1242/jcs.042382.
11. Kaidi A, Weinert BT, Choudhary C, Jackson SP. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 2010; 329:1348-53; PMID:20829486; http://dx.doi.org/10.1126/science. 1192049.
12. Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, Lin M, et al. SIRT6 links histone H3 lysine 9 deacetylation to NFkappaB-dependent gene expression and organismal life span. Cell 2009; 136:62-74; PMID:19135889; http://dx.doi.org/10.1016/j. cell.2008.10.052.
13. Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, Damian M, et al. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 2008; 452:492-6; PMID:18337721; http://dx.doi.org/10.1038/nature06736.
14. Mostoslavsky R, Chua KF, Lombard DB, Pang WW, Fischer MR, Gellon L, et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 2006; 124:315-29; PMID:16439206; http://dx.doi.org/10.1016/j.cell.2005.11.044.
15. Tennen RI, Berber E, Chua KF. Functional dissection of SIRT6: identification of domains that regulate histone deacetylase activity and chromatin localization. Mech Ageing Dev 2010; 131:185-92; PMID:20117128; http://dx.doi.org/10.1016/j.mad.2010.01.006.
16. Xiao C, Kim HS, Lahusen T, Wang RH, Xu X, Gavrilova O, et al. SIRT6 deficiency results in severe hypoglycemia by enhancing both basal and insulinstimulated glucose uptake in mice. J Biol Chem 2010; 285:36776-84; PMID:20847051; http://dx.doi. org/10.1074/jbc.M110.168039.
17. Zhong L, D'Urso A, Toiber D, Sebastian C, Henry RE, Vadysirisack DD, et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 2010; 140:280-93; PMID:20141841; http://dx.doi. org/10.1016/j.cell.2009.12.041.
18. Gan L, Mucke L. Paths of convergence: sirtuins in aging and neurodegeneration. Neuron 2008; 58:10-4; PMID:18400158; http://dx.doi.org/10.1016/j.neuron. 2008.03.015.
19. Michishita E, McCord RA, Boxer LD, Barber MF, Hong T, Gozani O, et al. Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 2009; 8:2664-6; PMID:19625767; http://dx.doi.org/10.4161/cc.8.16.9367.
20. Yang B, Zwaans BM, Eckersdorff M, Lombard DB. The sirtuin SIRT6 deacetylates H3 K56Ac in vivo to promote genomic stability. Cell Cycle 2009; 8:2662-3; PMID:19597350; http://dx.doi.org/10.4161/cc.8.16.9329.
21. Liszt G, Ford E, Kurtev M, Guarente L. Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J Biol Chem 2005; 280:21313-20; PMID:15795229; http://dx.doi.org/10.1074/jbc.M413296200.
22. 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; 260:273-9; PMID:10381378; http://dx.doi.org/10.1006/bbrc.1999.0897.
23. 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; 16:4623-35; PMID:16079181; http://dx.doi.org/10.1091/mbc. E05-01-0033.
24. Straight AF, Shou W, Dowd GJ, Turck CW, Deshaies RJ, Johnson AD, et al. Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell 1999; 97:245-56; PMID:10219245; http://dx.doi.org/10.1016/S0092-8674(00)80734-5.
25. Shen HB, Chou KC. Nuc-PLoc: a new web-server for predicting protein subnuclear localization by fusing PseAA composition and PsePSSM. Protein Eng Des Sel 2007; 20:561-7; PMID:17993650; http://dx.doi. org/10.1093/protein/gzm057.
26. Li LH, Wu LJ, Tashiro SI, Onodera S, Uchiumi F, Ikejima T. Activation of the SIRT1 pathway and modulation of the cell cycle were involved in silymarin's protection against UV-induced A375-S2 cell apoptosis. J Asian Nat Prod Res 2007; 9:245-52; PMID:17566917; http://dx.doi.org/10.1080/10286020600604260.
27. Scott MS, Boisvert FM, McDowall MD, Lamond AI, Barton GJ. Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res 2010; 38:7388-99; PMID:20663773; http://dx.doi. org/10.1093/nar/gkq653.
28. Dephoure N, Zhou C, Villén J, Beausoleil SA, Bakalarski CE, Elledge SJ, et al. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 2008; 105:10762-7; PMID:18669648; http://dx.doi. org/10.1073/pnas.0805139105.
29. Okuwaki M, Tsujimoto M, Nagata K. The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol Biol Cell 2002; 13:2016-30; PMID:12058066; http://dx.doi.org/10.1091/mbc.02-03-0036.
30. Hernandez-Verdun D. Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2011; 2:189-94; PMID:21818412; http://dx.doi.org/10.4161/nucl.2.3.16246.
31. Michan S, Sinclair D. Sirtuins in mammals: insights into their biological function. Biochem J 2007; 404:1-13; PMID:17447894; http://dx.doi.org/10.1042/BJ20070140.
32. 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; 450:440-4; PMID:18004385; http://dx.doi.org/10.1038/nature06268.
33. 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; 16:93-105; PMID:15469825; http://dx.doi.org/10.1016/j.molcel. 2004.08.031.
34. Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI. The multifunctional nucleolus. Nat Rev Mol Cell Biol 2007; 8:574-85; PMID:17519961; http://dx.doi.org/10.1038/nrm2184.
35. Carmo-Fonseca M, Mendes-Soares L, Campos I. To be or not to be in the nucleolus. Nat Cell Biol 2000; 2:107-12; PMID:10854340; http://dx.doi. org/10.1038/35014078.
36. Cioci F, Vogelauer M, Camilloni G. Acetylation and accessibility of rDNA chromatin in Saccharomyces cerevisiae in (Delta)top1 and (Delta)sir2 mutants. J Mol Biol 2002; 322:41-52; PMID:12215413; http://dx.doi.org/10.1016/S0022-2836(02)00749-0.
37. Shou W, Seol JH, Shevchenko A, Baskerville C, Moazed D, Chen ZW, et al. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 1999; 97:233-44; PMID:10219244; http://dx.doi. org/10.1016/S0092-8674(00)80733-3.
38. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, Lamond AI, et al. Nucleolar proteome dynamics. Nature 2005; 433:77-83; PMID:15635413; http://dx.doi.org/10.1038/nature03207.
39. Espada J, Ballestar E, Santoro R, Fraga MF, Villar-Garea A, Németh A, et al. Epigenetic disruption of ribosomal RNA genes and nucleolar architecture in DNA methyltransferase 1 (Dnmt1) deficient cells. Nucleic Acids Res 2007; 35:2191-8; PMID:17355984; http://dx.doi.org/10.1093/nar/gkm118.
40. Gonugunta VK, Nair BC, Rajhans R, Sareddy GR, Nair SS, Vadlamudi RK. Regulation of rDNA transcription by proto-oncogene PELP1. PLoS One 2011; 6:21095; PMID:21695158; http://dx.doi.org/10.1371/journal. pone.0021095.
41. Kobayashi T. How does genome instability affect lifespan?: roles of rDNA and telomeres. Genes Cells 2011; 16:617-24; PMID:21605287; http://dx.doi. org/10.1111/j.1365-2443.2011.01519.x.
42. Lempiäinen H, Shore D. Growth control and ribosome biogenesis. Curr Opin Cell Biol 2009; 21:855-63; PMID:19796927; http://dx.doi.org/10.1016/j. ceb.2009.09.002.
43. Visintin R, Amon A. The nucleolus: the magician's hat for cell cycle tricks. Curr Opin Cell Biol 2000; 12:752; PMID:11063944; http://dx.doi.org/10.1016/S0955-0674(00)00165-4.
44. Shandilya J, Swaminathan V, Gadad SS, Choudhari R, Kodaganur GS, Kundu TK. Acetylated NPM1 localizes in the nucleoplasm and regulates transcriptional activation of genes implicated in oral cancer manifestation. Mol Cell Biol 2009; 29:5115-27; PMID:19581289; http://dx.doi.org/10.1128/MCB.01969-08.
45. North BJ, Verdin E. Interphase nucleo-cytoplasmic shuttling and localization of SIRT2 during mitosis. PLoS One 2007; 2:784; PMID:17726514; http://dx.doi.org/10.1371/journal.pone.0000784.
46. Dryden SC, Nahhas FA, Nowak JE, Goustin AS, Tainsky MA. Role for human SIRT2 NADdependent deacetylase activity in control of mitotic exit in the cell cycle. Mol Cell Biol 2003; 23:3173-85; PMID:12697818; http://dx.doi.org/10.1128/MCB.23.9.3173-85.2003.
47. Kim HS, Vassilopoulos A, Wang RH, Lahusen T, Xiao Z, Xu X, et al. SIRT2 maintains genome integrity and suppresses tumorigenesis through regulating APC/C activity. Cancer Cell 2011; 20:487-99; PMID:22014574; http://dx.doi.org/10.1016/j. ccr.2011.09.004.
48. Fatoba ST, Okorokov AL. Human SIRT1 associates with mitotic chromatin and contributes to chromosomal condensation. Cell Cycle 2011; 10:2317-22; PMID:21636977; http://dx.doi.org/10.4161/cc.10.14.15913.
49. Manser E, Huang HY, Loo TH, Chen XQ, Dong JM, Leung T, et al. Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol Cell Biol 1997; 17:1129-43; PMID:9032240.
50. Liang F, Hatanaka Y, Saito H, Yamamori T, Hashikawa T. Differential expression of gamma-aminobutyric acid type B receptor-1a and-1b mRNA variants in GABA and non-GABAergic neurons of the rat brain. J Comp Neurol 2000; 416:475-95; PMID:10660879; http://dx.doi.org/10.1002/(SICI)1096-9861(20000124)416:4<475::AIDCNE5> 3.0.CO;2-V.