The dual role of sirtuins in cancer

Genes and Cancer

Volumn 2, Issue 6, 2011, Pages 648-662

  Bosch Presegué, Laia ^a   Vaquero, Alejandro ^b  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

cancer; deacetylation; DNA damage; DNA repair; genome stability; heterochromatin; SirT1 7; sirtuins

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PROTEIN BCL 6; PROTEIN P53; SIRTUIN; SIRTUIN 1; SIRTUIN 2; SIRTUIN 3; SIRTUIN 4; SIRTUIN 6; TRANSCRIPTION FACTOR FOXO;

APOPTOSIS; CARCINOGENESIS; CELL FUNCTION; CELLULAR STRESS RESPONSE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; GENOMIC INSTABILITY; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 80054782483     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601911417862     Document Type: Review

References (211)

1. Shore D,Squire M,Nasmyth KA.Characterization of two genes required for the position-effect control of yeast mating-type genes.EMBO J. 1984;3:2817-23.
2. Sinclair DA,Guarente L.Extrachromosomal rDNA circles-a cause of aging in yeast.Cell. 1997;91:1033-42.
3. Saunders LR,Verdin E.Sirtuins: critical regulators at the crossroads between cancer and aging.Oncogene. 2007;26:5489-504.
4. Guarente L.Diverse and dynamic functions of the Sir silencing complex.Nat Genet. 1999;23:281-5.
5. Braunstein M,Rose AB,Holmes SG,Allis CD,Broach JR.Transcriptional silencing in yeast is associated with reduced nucleosome acetylation.Genes Dev. 1993;7:592-604.
6. Vaquero A.The conserved role of sirtuins in chromatin regulation.Int J Dev Biol. 2009;53:303-22.
7. 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.
8. Landry J,Sutton A,Tafrov ST, et al.The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases.Proc Natl Acad Sci U S A. 2000;97:5807-11.
9. 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;99:735-45.
10. 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.
11. Frye RA.Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins.Biochem Biophys Res Commun. 2000;273:793-8.
12. Haigis MC,Guarente LP.Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction.Genes Dev. 2006;20:2913-21.
13. Vaquero A,Sternglanz R,Reinberg D.NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs.Oncogene. 2007;26:5505-20.
14. 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.
15. Vaquero A,Reinberg DSirtuins in biology and disease. Boca Raton, FL: CRC Press/Taylor & Francis; 2008:.
16. Wang RH,Sengupta K,Li C, et al.Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice.Cancer Cell. 2008;14:312-23.
17. Mostoslavsky R,Chua KF,Lombard DB, et al.Genomic instability and aging-like phenotype in the absence of mammalian SIRT6.Cell. 2006;124:315-29.
18. Negrini S,Gorgoulis VG,Halazonetis TD.Genomic instability-an evolving hallmark of cancer.Nat Rev Mol Cell Biol. 2010;11:220-8.
19. Peters AH,O'Carroll D,Scherthan H, et al.Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability.Cell. 2001;107:323-37.
20. 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.
21. 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.
22. Jenuwein T,Allis CD.Translating the histone code.Science. 2001;293:1074-80.
23. Murayama A,Ohmori K,Fujimura A, et al.Epigenetic control of rDNA loci in response to intracellular energy status.Cell. 2008;133:627-39.
24. Zhang Y,Wang J,Chen G,Fan D,Deng M.Inhibition of Sirt1 promotes neural progenitors toward motoneuron differentiation from human embryonic stem cells.Biochem Biophys Res Commun. 2011;404:610-4.
25. Ou X,Chae HD,Wang RH, et al.SIRT1 deficiency compromises mouse embryonic stem cell hematopoietic differentiation, and embryonic and adult hematopoiesis in the mouse.Blood. 2011;117:440-50.
26. Saunders LR,Sharma AD,Tawney J, et al.miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues.Aging (Albany NY). 2010;2:415-31.
27. Calvanese V,Lara E,Suarez-Alvarez B, et al.Sirtuin 1 regulation of developmental genes during differentiation of stem cells.Proc Natl Acad Sci U S A. 2010;107:13736-41.
28. 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;102:1859-64.
29. Oberdoerffer P,Michan S,McVay M, et al.SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging.Cell. 2008;135:907-18.
30. Palacios JA,Herranz D,De Bonis ML,Velasco S,Serrano M,Blasco MA.SIRT1 contributes to telomere maintenance and augments global homologous recombination.J Cell Biol. 2010;191:1299-313.
31. Bosch-Presegué 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. 2011;42:210-23.
32. 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;37:391-400.
33. 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:e40.
34. Michishita E,McCord RA,Berber E, et al.SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin.Nature. 2008;452:492-6.
35. Michishita E,McCord RA,Boxer LD, et al.Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6.Cell Cycle. 2009;8:2664-6.
36. 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.
37. Tennen RI,Chua KF.Chromatin regulation and genome maintenance by mammalian SIRT6.Trends Biochem Sci. 2011;36:39-46.
38. Das C,Lucia MS,Hansen KC,Tyler JK.CBP/p300-mediated acetylation of histone H3 on lysine 56.Nature. 2009;459:113-7.
39. 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;20:1256-61.
40. Shogren-Knaak M,Ishii H,Sun JM,Pazin MJ,Davie JR,Peterson CL.Histone H4-K16 acetylation controls chromatin structure and protein interactions.Science. 2006;311:844-7.
41. Lombard DB,Alt FW,Cheng HL, et al.Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation.Mol Cell Biol. 2007;27:8807-14.
42. 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;21:920-8.
43. McAinsh AD,Scott-Drew S,Murray JA,Jackson SP.DNA damage triggers disruption of telomeric silencing and Mec1p-dependent relocation of Sir3p.Curr Biol. 1999;9:963-6.
44. 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;97:621-33.
45. Shim EY,Hong SJ,Oum JH,Yanez Y,Zhang Y,Lee SE.RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin.Mol Cell Biol. 2007;27:1602-13.
46. Mills KD,Sinclair DA,Guarente L.MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks.Cell. 1999;97:609-20.
47. Lee SE,Paques F,Sylvan J,Haber JE.Role of yeast SIR genes and mating type in directing DNA double-strand breaks to homologous and non-homologous repair paths.Curr Biol. 1999;9:767-70.
48. Tamburini BA,Tyler JK.Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair.Mol Cell Biol. 2005;25:4903-13.
49. Chen CC,Carson JJ,Feser J, et al.Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair.Cell. 2008;134:231-43.
50. Yuan Z,Zhang X,Sengupta N,Lane WS,Seto E.SIRT1 regulates the function of the Nijmegen breakage syndrome protein.Mol Cell. 2007;27:149-62.
51. Uhl M,Csernok A,Aydin S,Kreienberg R,Wiesmuller L,Gatz SA.Role of SIRT1 in homologous recombination.DNA Repair (Amst). 2010;9:383-93.
52. Li K,Casta A,Wang R, et al.Regulation of WRN protein cellular localization and enzymatic activities by SIRT1-mediated deacetylation.J Biol Chem. 2008;283:7590-8.
53. Jeong J,Juhn K,Lee H, et al.SIRT1 promotes DNA repair activity and deacetylation of Ku70.Exp Mol Med. 2007;39:8-13.
54. Sawada M,Sun W,Hayes P,Leskov K,Boothman DA,Matsuyama S.Ku70 suppresses the apoptotic translocation of Bax to mitochondria.Nat Cell Biol. 2003;5:320-9.
55. Cohen HY,Miller C,Bitterman KJ, et al.Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase.Science. 2004;305:390-2.
56. Sundaresan NR,Samant SA,Pillai VB,Rajamohan SB,Gupta MP.SIRT3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70.Mol Cell Biol. 2008;28:6384-401.
57. Fan W,Luo J.SIRT1 regulates UV-induced DNA repair through deacetylating XPA.Mol Cell. 2010;39:247-58.
58. 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;1:109-21.
59. Kaidi A,Weinert BT,Choudhary C,Jackson SP.Human SIRT6 promotes DNA end resection through CtIP deacetylation.Science. 2010;329:1348-53.
60. Stunkel W,Peh BK,Tan YC, et al.Function of the SIRT1 protein deacetylase in cancer.Biotechnol J. 2007;2:1360-8.
61. Chua KF,Mostoslavsky R,Lombard DB, et al.Mammalian SIRT1 limits replicative life span in response to chronic genotoxic stress.Cell Metab. 2005;2:67-76.
62. Allison SJ,Milner J.SIRT3 is pro-apoptotic and participates in distinct basal apoptotic pathways.Cell Cycle. 2007;6:2669-77.
63. Wang F,Nguyen M,Qin FX,Tong Q.SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction.Aging Cell. 2007;6:505-14.
64. Langley E,Pearson M,Faretta M, et al.Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence.EMBO J. 2002;21:2383-96.
65. Sasaki T,Maier B,Bartke A,Scrable H.Progressive loss of SIRT1 with cell cycle withdrawal.Aging Cell. 2006;5:413-22.
66. Ota H,Tokunaga E,Chang K, et al.Sirt1 inhibitor, Sirtinol, induces senescence-like growth arrest with attenuated Ras-MAPK signaling in human cancer cells.Oncogene. 2006;25:176-85.
67. Luo J,Nikolaev AY,Imai S, et al.Negative control of p53 by Sir2alpha promotes cell survival under stress.Cell. 2001;107:137-48.
68. Vaziri H,Dessain SK,Ng Eaton E, et al.hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase.Cell. 2001;107:149-59.
69. Hollstein M,Sidransky D,Vogelstein B,Harris CC.p53 mutations in human cancers.Science. 1991;253:49-53.
70. Vogelstein B,Lane D,Levine AJ.Surfing the p53 network.Nature. 2000;408:307-10.
71. Lain S,Lane D.Improving cancer therapy by non-genotoxic activation of p53.Eur J Cancer. 2003;39:1053-60.
72. 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;100:10794-9.
73. Chen WY,Wang DH,Yen RC,Luo J,Gu W,Baylin SB.Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses.Cell. 2005;123:437-48.
74. Kim JE,Chen J,Lou Z.DBC1 is a negative regulator of SIRT1.Nature. 2008;451:583-6.
75. Zhao W,Kruse JP,Tang Y,Jung SY,Qin J,Gu W.Negative regulation of the deacetylase SIRT1 by DBC1.Nature. 2008;451:587-90.
76. Lim CS.SIRT1: tumor promoter or tumor suppressor?.Med Hypotheses. 2006;67:341-4.
77. Han MK,Song EK,Guo Y,Ou X,Mantel C,Broxmeyer HE.SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization.Cell Stem Cell. 2008;2:241-51.
78. Kamel C,Abrol M,Jardine K,He X,McBurney MW.SirT1 fails to affect p53-mediated biological functions.Aging Cell. 2006;5:81-8.
79. Matsushita N,Takami Y,Kimura M, et al.Role of NAD-dependent deacetylases SIRT1 and SIRT2 in radiation and cisplatin-induced cell death in vertebrate cells.Genes Cells. 2005;10:321-32.
80. 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;16:34-45.
81. 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:e10486.
82. Talos F,Petrenko O,Mena P,Moll UM.Mitochondrially targeted p53 has tumor suppressor activities in vivo.Cancer Res. 2005;65:9971-81.
83. Greer EL,Brunet A.FOXO transcription factors at the interface between longevity and tumor suppression.Oncogene. 2005;24:7410-25.
84. Burgering BM,Kops GJ.Cell cycle and death control: long live Forkheads.Trends Biochem Sci. 2002;27:352-60.
85. Accili D,Arden KC.FoxOs at the crossroads of cellular metabolism, differentiation, and transformation.Cell. 2004;117:421-6.
86. Furukawa-Hibi Y,Kobayashi Y,Chen C,Motoyama N.FOXO transcription factors in cell-cycle regulation and the response to oxidative stress.Antioxid Redox Signal. 2005;7:752-60.
87. Barreyro FJ,Kobayashi S,Bronk SF,Werneburg NW,Malhi H,Gores GJ.Transcriptional regulation of Bim by FoxO3A mediates hepatocyte lipoapoptosis.J Biol Chem. 2007;282:27141-54.
88. Dehan E,Pagano M.Skp2, the FoxO1 hunter.Cancer Cell. 2005;7:209-10.
89. Fu Z,Tindall DJ.FOXOs, cancer and regulation of apoptosis.Oncogene. 2008;27:2312-9.
90. Galili N,Davis RJ,Fredericks WJ, et al.Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma.Nat Genet. 1993;5:230-5.
91. Parry P,Wei Y,Evans G.Cloning and characterization of the t(X;11) breakpoint from a leukemic cell line identify a new member of the forkhead gene family.Genes Chromosomes Cancer. 1994;11:79-84.
92. Borkhardt A,Repp R,Haas OA, et al.Cloning and characterization of AFX, the gene that fuses to MLL in acute leukemias with a t(X;11) (q13;q23).Oncogene. 1997;14:195-202.
93. Anderson MJ,Viars CS,Czekay S,Cavenee WK,Arden KC.Cloning and characterization of three human forkhead genes that comprise an FKHR-like gene subfamily.Genomics. 1998;47:187-99.
94. Brunet A,Sweeney LB,Sturgill JF, et al.Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase.Science. 2004;303:2011-5.
95. Kobayashi Y,Furukawa-Hibi Y,Chen C, et al.SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress.Int J Mol Med. 2005;16:237-43.
96. 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;279:28873-9.
97. Matsuzaki H,Daitoku H,Hatta M,Aoyama H,Yoshimochi K,Fukamizu A.Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation.Proc Natl Acad Sci U S A. 2005;102:11278-83.
98. Motta MC,Divecha N,Lemieux M, et al.Mammalian SIRT1 represses forkhead transcription factors.Cell. 2004;116:551-63.
99. 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;101:10042-7.
100. Yang Y,Hou H,Haller EM,Nicosia SV,Bai W.Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation.EMBO J. 2005;24:1021-32.
101. Kuma A,Hatano M,Matsui M, et al.The role of autophagy during the early neonatal starvation period.Nature. 2004;432:1032-6.
102. Zhao Y,Yang J,Liao W, et al.Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity.Nat Cell Biol. 2010;12:665-75.
103. Levine B.Cell biology: autophagy and cancer.Nature. 2007;446:745-7.
104. Levine B,Kroemer G.Autophagy in the pathogenesis of disease.Cell. 2008;132:27-42.
105. 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;4:291-9.
106. Ford J,Jiang M,Milner J.Cancer-specific functions of SIRT1 enable human epithelial cancer cell growth and survival.Cancer Res. 2005;65:10457-63.
107. Barnes PJ,Karin M.Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases.N Engl J Med. 1997;336:1066-71.
108. Pikarsky E,Porat RM,Stein I, et al.NF-kappaB functions as a tumour promoter in inflammation-associated cancer.Nature. 2004;431:461-6.
109. Yeung F,Hoberg JE,Ramsey CS, et al.Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase.EMBO J. 2004;23:2369-80.
110. Chen J,Zhou Y,Mueller-Steiner S, et al.SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling.J Biol Chem. 2005;280:40364-74.
111. Kiernan R,Bres V,Ng RW, et al.Post-activation turn-off of NF-kappa B-dependent transcription is regulated by acetylation of p65.J Biol Chem. 2003;278:2758-66.
112. 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;123:4251-8.
113. Kawahara TL,Michishita E,Adler AS, et al.SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span.Cell. 2009;136:62-74.
114. Kaeberlein M,Kapahi P.The hypoxic response and aging.Cell Cycle. 2009;8:2324.
115. Denko NC.Hypoxia, HIF1 and glucose metabolism in the solid tumour.Nat Rev Cancer. 2008;8:705-13.
116. Zhong L,D'Urso A,Toiber D, et al.The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha.Cell. 2010;140:280-93.
117. Singh KK.Mitochondria damage checkpoint, aging, and cancer.Ann N Y Acad Sci. 2006;1067:182-90.
118. Kim SC,Sprung R,Chen Y, et al.Substrate and functional diversity of lysine acetylation revealed by a proteomics survey.Mol Cell. 2006;23:607-18.
119. Onyango P,Celic I,McCaffery JM,Boeke JD,Feinberg AP.SIRT3, a human SIR2 homologue, is an NAD-dependent deacetylase localized to mitochondria.Proc Natl Acad Sci U S A. 2002;99:13653-8.
120. Schwer B,North BJ,Frye RA,Ott M,Verdin E.The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase.J Cell Biol. 2002;158:647-57.
121. Kim HS,Patel K,Muldoon-Jacobs K, et al.SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress.Cancer Cell. 2010;17:41-52.
122. Dimova DK,Dyson NJ.The E2F transcriptional network: old acquaintances with new faces.Oncogene. 2005;24:2810-26.
123. Wong S,Weber JD.Deacetylation of the retinoblastoma tumour suppressor protein by SIRT1.Biochem J. 2007;407:451-60.
124. Logan CY,Nusse R.The Wnt signaling pathway in development and disease.Annu Rev Cell Dev Biol. 2004;20:781-810.
125. Korinek V,Barker N,Morin PJ, et al.Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma.Science. 1997;275:1784-7.
126. Morin PJ,Sparks AB,Korinek V, et al.Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC.Science. 1997;275:1787-90.
127. Brack AS,Conboy MJ,Roy S, et al.Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis.Science. 2007;317:807-10.
128. Liu H,Fergusson MM,Castilho RM, et al.Augmented Wnt signaling in a mammalian model of accelerated aging.Science. 2007;317:803-6.
129. Firestein R,Blander G,Michan S, et al.The SIRT1 deacetylase suppresses intestinal tumorigenesis and colon cancer growth.PLoS One. 2008;3:e2020.
130. Wang RH,Zheng Y,Kim HS, et al.Interplay among BRCA1, SIRT1, and Survivin during BRCA1-associated tumorigenesis.Mol Cell. 2008;32:11-20.
131. Niu H.The proto-oncogene BCL-6 in normal and malignant B cell development.Hematol Oncol. 2002;20:155-66.
132. Heltweg B,Gatbonton T,Schuler AD, et al.Antitumor activity of a small-molecule inhibitor of human silent information regulator 2 enzymes.Cancer Res. 2006;66:4368-77.
133. Bradbury CA,Khanim FL,Hayden R, et al.Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors.Leukemia. 2005;19:1751-9.
134. Hida Y,Kubo Y,Murao K,Arase S.Strong expression of a longevity-related protein, SIRT1, in Bowen's disease.Arch Dermatol Res. 2007;299:103-6.
135. Huffman DM,Grizzle WE,Bamman MM, et al.SIRT1 is significantly elevated in mouse and human prostate cancer.Cancer Res. 2007;67:6612-8.
136. Ashraf N,Zino S,Macintyre A, et al.Altered sirtuin expression is associated with node-positive breast cancer.Br J Cancer. 2006;95:1056-61.
137. Hiratsuka M,Inoue T,Toda T, et al.Proteomics-based identification of differentially expressed genes in human gliomas: down-regulation of SIRT2 gene.Biochem Biophys Res Commun. 2003;309:558-66.
138. 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;26:945-57.
139. Lennerz V,Fatho M,Gentilini C, et al.The response of autologous T cells to a human melanoma is dominated by mutated neoantigens.Proc Natl Acad Sci U S A. 2005;102:16013-8.
140. 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;23:3173-85.
141. Inoue T,Hiratsuka M,Osaki M,Oshimura M.The molecular biology of mammalian SIRT proteins: SIRT2 in cell cycle regulation.Cell Cycle. 2007;6:1011-8.
142. Wales MM,Biel MA,el Deiry W, et al.p53 activates expression of HIC-1, a new candidate tumour suppressor gene on 17p13.3.Nat Med. 1995;1:570-7.
143. Chen W,Cooper TK,Zahnow CA, et al.Epigenetic and genetic loss of Hic1 function accentuates the role of p53 in tumorigenesis.Cancer Cell. 2004;6:387-98.
144. Chen WY,Zeng X,Carter MG, et al.Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors.Nat Genet. 2003;33:197-202.
145. Stankovic-Valentin N,Deltour S,Seeler J, et al.An acetylation/deacetylation-SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity.Mol Cell Biol. 2007;27:2661-75.
146. Caballero R,Setien F,Lopez-Serra L, et al.Combinatorial effects of splice variants modulate function of Aiolos.J Cell Sci. 2007;120:2619-30.
147. Nemoto S,Fergusson MM,Finkel T.Nutrient availability regulates SIRT1 through a forkhead-dependent pathway.Science. 2004;306:2105-8.
148. Lynch CJ,Shah ZH,Allison SJ, et al.SIRT1 undergoes alternative splicing in a novel auto-regulatory loop with p53.PLoS One. 2010;5:e13502.
149. Ambros V.The functions of animal microRNAs.Nature. 2004;431:350-5.
150. Bartel DP.MicroRNAs: genomics, biogenesis, mechanism, and function.Cell. 2004;116:281-97.
151. Caldas C,Brenton JD.Sizing up miRNAs as cancer genes.Nat Med. 2005;11:712-4.
152. Calin GA,Croce CM.MicroRNA signatures in human cancers.Nat Rev Cancer. 2006;6:857-66.
153. Cho WC.MicroRNAs: potential biomarkers for cancer diagnosis, prognosis and targets for therapy.Int J Biochem Cell Biol. 2010;42:1273-81.
154. Esquela-Kerscher A,Slack FJ.Oncomirs-microRNAs with a role in cancer.Nat Rev Cancer. 2006;6:259-69.
155. Wittmann J,Jack HM.Serum microRNAs as powerful cancer biomarkers.Biochim Biophys Acta. 2010;1806:200-7.
156. Bommer GT,Gerin I,Feng Y, et al.p53-mediated activation of miRNA34 candidate tumor-suppressor genes.Curr Biol. 2007;17:1298-307.
157. He L,He X,Lim LP, et al.A microRNA component of the p53 tumour suppressor network.Nature. 2007;447:1130-4.
158. Raver-Shapira N,Marciano E,Meiri E, et al.Transcriptional activation of miR-34a contributes to p53-mediated apoptosis.Mol Cell. 2007;26:731-43.
159. Tarasov V,Jung P,Verdoodt B, et al.Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest.Cell Cycle. 2007;6:1586-93.
160. Tazawa H,Tsuchiya N,Izumiya M,Nakagama H.Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells.Proc Natl Acad Sci U S A. 2007;104:15472-7.
161. Yamakuchi M,Ferlito M,Lowenstein CJ.miR-34a repression of SIRT1 regulates apoptosis.Proc Natl Acad Sci U S A. 2008;105:13421-6.
162. Chang TC,Wentzel EA,Kent OA, et al.Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis.Mol Cell. 2007;26:745-52.
163. Fujita Y,Kojima K,Hamada N, et al.Effects of miR-34a on cell growth and chemoresistance in prostate cancer PC3 cells.Biochem Biophys Res Commun. 2008;377:114-9.
164. Kojima K,Ohhashi R,Fujita Y, et al.A role for SIRT1 in cell growth and chemoresistance in prostate cancer PC3 and DU145 cells.Biochem Biophys Res Commun. 2008;373:423-8.
165. Akao Y,Noguchi S,Iio A,Kojima K,Takagi T,Naoe T.Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells.Cancer Lett. 2011;300:197-204.
166. Xiong S,Salazar G,Patrushev N,Alexander RW.FoxO1 mediates an auto-feedback loop regulating SIRT1 expression.J Biol Chem. 2011;286:5289-99.
167. Wang C,Chen L,Hou X, et al.Interactions between E2F1 and SirT1 regulate apoptotic response to DNA damage.Nat Cell Biol. 2006;8:1025-31.
168. Martinez-Balbas MA,Bauer UM,Nielsen SJ,Brehm A,Kouzarides T.Regulation of E2F1 activity by acetylation.EMBO J. 2000;19:662-71.
169. Yuan J,Minter-Dykhouse K,Lou Z.A c-Myc-SIRT1 feedback loop regulates cell growth and transformation.J Cell Biol. 2009;185:203-11.
170. Abdelmohsen K,Pullmann R,Lal A, et al.Phosphorylation of HuR by Chk2 regulates SIRT1 expression.Mol Cell. 2007;25:543-57.
171. Wang W,Yang X,Cristofalo VJ,Holbrook NJ,Gorospe M.Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence.Mol Cell Biol. 2001;21:5889-98.
172. Varambally S,Dhanasekaran SM,Zhou M, et al.The polycomb group protein EZH2 is involved in progression of prostate cancer.Nature. 2002;419:624-9.
173. Kleer CG,Cao Q,Varambally S, et al.EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells.Proc Natl Acad Sci U S A. 2003;100:11606-11.
174. Kim EJ,Kho JH,Kang MR,Um SJ.Active regulator of SIRT1 cooperates with SIRT1 and facilitates suppression of p53 activity.Mol Cell. 2007;28:277-90.
175. Li Z,Chen L,Kabra N,Wang C,Fang J,Chen J.Inhibition of SUV39H1 methyltransferase activity by DBC1.J Biol Chem. 2009;284:10361-6.
176. Radvanyi L,Singh-Sandhu D,Gallichan S, et al.The gene associated with trichorhinophalangeal syndrome in humans is overexpressed in breast cancer.Proc Natl Acad Sci U S A. 2005;102:11005-10.
177. Trauernicht AM,Kim SJ,Kim NH,Boyer TG.Modulation of estrogen receptor alpha protein level and survival function by DBC-1.Mol Endocrinol. 2007;21:1526-36.
178. Fu J,Jiang J,Li J, et al.Deleted in breast cancer 1, a novel androgen receptor (AR) coactivator that promotes AR DNA-binding activity.J Biol Chem. 2009;284:6832-40.
179. Lee H,Kim KR,Noh SJ, et al.Expression of DBC1 and SIRT1 is associated with poor prognosis for breast carcinoma.Hum Pathol. 2011;42:204-13.
180. Sung JY,Kim R,Kim JE,Lee J.Balance between SIRT1 and DBC1 expression is lost in breast cancer.Cancer Sci. 2010;101:1738-44.
181. Yang T,Sauve AA.NAD metabolism and sirtuins: metabolic regulation of protein deacetylation in stress and toxicity.Aaps J. 2006;8:E632-43.
182. Revollo JR,Grimm AA,Imai S.The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells.J Biol Chem. 2004;279:50754-63.
183. van der Veer E,Ho C,O'Neil C, et al.Extension of human cell lifespan by nicotinamide phosphoribosyltransferase.J Biol Chem. 2007;282:10841-5.
184. Wang B,Hasan MK,Alvarado E,Yuan H,Wu H,Chen WY.NAMPT overexpression in prostate cancer and its contribution to tumor cell survival and stress response.Oncogene. 2011;30:907-21.
185. McLure KG,Takagi M,Kastan MB.NAD+ modulates p53 DNA binding specificity and function.Mol Cell Biol. 2004;24:9958-67.
186. Zhang J.Are poly(ADP-ribosyl)ation by PARP-1 and deacetylation by Sir2 linked?.Bioessays. 2003;25:808-14.
187. Byles V,Chmilewski LK,Wang J, et al.Aberrant cytoplasm localization and protein stability of SIRT1 is regulated by PI3K/IGF-1R signaling in human cancer cells.Int J Biol Sci. 2010;6:599-612.
188. Herranz D,Munoz-Martin M,Canamero M, et al.Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer.Nat Commun. 2010;1:1-8.
189. Banks AS,Kon N,Knight C, et al.SirT1 gain of function increases energy efficiency and prevents diabetes in mice.Cell Metab. 2008;8:333-41.
190. Pfluger PT,Herranz D,Velasco-Miguel S,Serrano M,Tschop MH.Sirt1 protects against high-fat diet-induced metabolic damage.Proc Natl Acad Sci U S A. 2008;105:9793-8.
191. Zhang QJ,Wang Z,Chen HZ, et al.Endothelium-specific overexpression of class III deacetylase SIRT1 decreases atherosclerosis in apolipoprotein E-deficient mice.Cardiovasc Res. 2008;80:191-9.
192. Chu F,Chou PM,Zheng X,Mirkin BL,Rebbaa A.Control of multidrug resistance gene mdr1 and cancer resistance to chemotherapy by the longevity gene sirt1.Cancer Res. 2005;65:10183-7.
193. Harper CE,Patel BB,Wang J,Arabshahi A,Eltoum IA,Lamartiniere CA.Resveratrol suppresses prostate cancer progression in transgenic mice.Carcinogenesis. 2007;28:1946-53.
194. Li T,Fan GX,Wang W,Li T,Yuan YK.Resveratrol induces apoptosis, influences IL-6 and exerts immunomodulatory effect on mouse lymphocytic leukemia both in vitro and in vivo.Int Immunopharmacol. 2007;7:1221-31.
195. Aziz MH,Afaq F,Ahmad N.Prevention of ultraviolet-B radiation damage by resveratrol in mouse skin is mediated via modulation in survivin.Photochem Photobiol. 2005;81:25-31.
196. Whitsett T,Carpenter M,Lamartiniere CA.Resveratrol, but not EGCG, in the diet suppresses DMBA-induced mammary cancer in rats.J Carcinog. 2006;5:15.
197. Potente M,Ghaeni L,Baldessari D, et al.SIRT1 controls endothelial angiogenic functions during vascular growth.Genes Dev. 2007;21:2644-58.
198. Furuyama T,Kitayama K,Shimoda Y, et al.Abnormal angiogenesis in Foxo1 (Fkhr)- deficient mice.J Biol Chem. 2004;279:34741-9.
199. Hosaka T,Biggs WH,Tieu D, et al.Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification.Proc Natl Acad Sci U S A. 2004;101:2975-80.
200. Potente M,Urbich C,Sasaki K, et al.Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization.J Clin Invest. 2005;115:2382-92.
201. Paik JH,Kollipara R,Chu G, et al.FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis.Cell. 2007;128:309-23.
202. Daly C,Wong V,Burova E, et al.Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1).Genes Dev. 2004;18:1060-71.
203. Mattagajasingh I,Kim CS,Naqvi A, et al.SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase.Proc Natl Acad Sci U S A. 2007;104:14855-60.
204. Dimmeler S,Haendeler J,Nehls M,Zeiher AM.Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases.J Exp Med. 1997;185:601-7.
205. Potente M,Dimmeler S.Emerging roles of SIRT1 in vascular endothelial homeostasis.Cell Cycle. 2008;7:2117-22.
206. Aicher A,Heeschen C,Mildner-Rihm C, et al.Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells.Nat Med. 2003;9:1370-6.
207. Moncada S,Higgs A.The L-arginine-nitric oxide pathway.N Engl J Med. 1993;329:2002-12.
208. Rodriguez RM,Fraga MF.Aging.and cancer: are sirtuins the link? Future Oncol. 2010;6:905-15.
209. Mahlknecht U,Ho AD,Voelter-Mahlknecht S.Chromosomal organization and fluorescence in situ hybridization of the human Sirtuin 6 gene.Int J Oncol. 2006;28:447-56.
210. 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.
211. Vakhrusheva O,Smolka C,Gajawada P, et al.Sirt7 increases stress resistance of cardiomyocytes and prevents apoptosis and inflammatory cardiomyopathy in mice.Circ Res. 2008;102:703-10.