Deacetylation of FOXO3 by SIRT1 or SIRT2 leads to Skp2-mediated FOXO3 ubiquitination and degradation

Oncogene

Volumn 31, Issue 12, 2012, Pages 1546-1557

  Wang, F ^a   Chan, C H ^b   Chen, K ^a   Guan, X ^a   Lin, H K ^b   Tong, Q ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

acetylation; E3 ubiquitin ligase; Forkhead transcription factor; proteasomal degradation; sirtuin; ubiquitination

Indexed keywords

ARGININE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; LYSINE; PROTEASOME INHIBITOR; S PHASE KINASE ASSOCIATED PROTEIN 2; SIRTUIN 1; SIRTUIN 2; TRANSCRIPTION FACTOR FKHRL1; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL TISSUE; ARTICLE; CANCER CELL; CONTROLLED STUDY; DEACETYLATION; ENZYME DEGRADATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; RECEPTOR DOWN REGULATION; UBIQUITINATION;

ACETYLATION; CELL LINE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; LYSINE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; S-PHASE KINASE-ASSOCIATED PROTEINS; SIRTUIN 1; SIRTUIN 2; SIRTUINS; TRANSFECTION; UBIQUITINATION;

MUS;

EID: 84858795617     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.347     Document Type: Article

References (66)

1. Arden KC. (2008). FOXO animal models reveal a variety of diverse roles for FOXO transcription factors. Oncogene 27: 2345-2350. (Pubitemid 351501785)
2. Biggs III WH, Meisenhelder J, Hunter T, Cavenee WK, Arden KC. (1999). Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA 96: 7421-7426. (Pubitemid 29299677)
3. Borra MT, O'Neill FJ, Jackson MD, Marshall B, Verdin E, Foltz KR et al. (2002). Conserved enzymatic production and biological effect of O-acetyl-ADP-ribose by silent information regulator 2-like NAD+-dependent deacetylases. J Biol Chem 277: 12632-12641. (Pubitemid 34952622)
4. Brummelkamp TR, Bernards R, Agami R. (2002). A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553. (Pubitemid 34408678)
5. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS et al. (1999). Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868. (Pubitemid 29165088)
6. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y et al. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303: 2011-2015. (Pubitemid 38393275)
7. Chan CH, Lee SW, Wang J, Lin HK. (2010). Regulation of Skp2 expression and activity and its role in cancer progression. ScientificWorldJournal 10: 1001-1015.
8. Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P et al. (2003). Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci USA 100: 10794-10799. (Pubitemid 37140107)
9. Cohen HY, Miller C, Bitterman KJ, Wall NR, Hekking B, Kessler B et al. (2004). Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305: 390-392. (Pubitemid 38938153)
10. Daitoku H, Hatta M, Matsuzaki H, Aratani S, Ohshima T, Miyagishi M et al. (2004). Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci USA 101: 10042-10047. (Pubitemid 38891191)
11. Dansen TB, Burgering BM. (2008). Unravelling the tumor-suppressive functions of FOXO proteins. Trends Cell Biol 18: 421-429.
12. Deng CX. (2009). SIRT1, is it a tumor promoter or tumor suppressor? Int J Biol Sci 5: 147-152.
13. Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, Bos JL et al. (2004). FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23: 4802-4812. (Pubitemid 40069710)
14. Finnin MS, Donigian JR, Pavletich NP. (2001). Structure of the histone deacetylase SIRT2. Nat Struct Biol 8: 621-625. (Pubitemid 32613012)
15. Fu W, Ma Q, Chen L, Li P, Zhang M, Ramamoorthy S et al. (2009). MDM2 acts downstream of p53 as an E3 ligase to promote FOXO ubiquitination and degradation. J Biol Chem 284: 13987-14000.
16. Fu Z, Tindall DJ. (2008). FOXOs, cancer and regulation of apoptosis. Oncogene 27: 2312-2319. (Pubitemid 351501782)
17. Fukuoka M, Daitoku H, Hatta M, Matsuzaki H, Umemura S, Fukamizu A. (2003). Negative regulation of forkhead transcription factor AFX (Foxo4) by CBP-induced acetylation. Int J Mol Med 12: 503-508.
18. Gross DN, van den Heuvel AP, Birnbaum MJ. (2008). The role of FoxO in the regulation of metabolism. Oncogene 27: 2320-2336. (Pubitemid 351501783)
19. Haigis MC, Guarente LP. (2006). Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev 20: 2913-2921. (Pubitemid 44771725)
20. Hiratsuka M, Inoue T, Toda T, Kimura N, Shirayoshi Y, Kamitani H et al. (2003). Proteomics-based identification of differentially expressed genes in human gliomas: down-regulation of SIRT2 gene. Biochem Biophys Res Commun 309: 558-566. (Pubitemid 37083288)
21. Ho KK, Myatt SS, Lam EW. (2008). Many forks in the path: cycling with FoxO. Oncogene 27: 2300-2311. (Pubitemid 351501781)
22. Hu MC, Lee DF, Xia W, Golfman LS, Ou-Yang F, Yang JY et al. (2004). IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117: 225-237. (Pubitemid 38496242)
23. Huang H, Regan KM, Wang F, Wang D, Smith DI, van Deursen JM et al. (2005). Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci USA 102: 1649-1654. (Pubitemid 40209222)
24. Jing E, Gesta S, Kahn CR. (2007). SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab 6: 105-114. (Pubitemid 47163621)
25. Jordan M, Schallhorn A, Wurm FM. (1996). Transfecting mammalian cells: optimization of critical parameters affecting calcium-phosphate precipitate formation. Nucleic Acids Res 24: 596-601. (Pubitemid 26085833)
26. Kabra N, Li Z, Chen L, Li B, Zhang X, Wang C et al. (2009). SirT1 is an inhibitor of proliferation and tumor formation in colon cancer. J Biol Chem 284: 18210-18217.
27. Kaeberlein M, Hu D, Kerr EO, Tsuchiya M, Westman EA, Dang N et al. (2005). Increased life span due to calorie restriction in respiratory-deficient yeast. PLoS Genet 1: e69.
28. Kaeberlein M, Kirkland KT, Fields S, Kennedy BK. (2004). Sir2-independent life span extension by calorie restriction in yeast. PLoS Biol 2: E296.
29. Kitamura YI, Kitamura T, Kruse JP, Raum JC, Stein R, Gu W et al. (2005). FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab 2: 153-163.
30. Kojima K, Ohhashi R, Fujita Y, Hamada N, Akao Y, Nozawa Y et al. (2008). A role for SIRT1 in cell growth and chemoresistance in prostate cancer PC3 and DU145 cells. Biochem Biophys Res Commun 373: 423-428.
31. Kops GJ, de Ruiter ND, De Vries-Smits AM, Powell DR, Bos JL, Burgering BM. (1999). Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398: 630-634. (Pubitemid 29183692)
32. Lamming DW, Latorre-Esteves M, Medvedik O, Wong SN, Tsang FA, Wang C et al. (2005). HST2 mediates SIR2-independent lifespan extension by calorie restriction. Science 309: 1861-1864. (Pubitemid 41325097)
33. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB et al. (2006). A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001. (Pubitemid 43795191)
34. Libina N, Berman JR, Kenyon C. (2003). Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489-502. (Pubitemid 37456810)
35. Liu T, Liu PY, Marshall GM. (2009). The critical role of the class III histone deacetylase SIRT1 in cancer. Cancer Res 69: 1702-1705.
36. Makarova O, Kamberov E, Margolis B. (2000). Generation of deletion and point mutations with one primer in a single cloning step. Biotechniques 29: 970-972.
37. Matsuzaki H, Daitoku H, Hatta M, Aoyama H, Yoshimochi K, Fukamizu A. (2005). Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc Natl Acad Sci USA 102: 11278-11283. (Pubitemid 41153811)
38. Matsuzaki H, Daitoku H, Hatta M, Tanaka K, Fukamizu A. (2003). Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Proc Natl Acad Sci USA 100: 11285-11290. (Pubitemid 37205927)
39. Modur V, Nagarajan R, Evers BM, Milbrandt J. (2002). FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem 277: 47928-47937. (Pubitemid 36159321)
40. Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, Gu W et al. (2004). Mammalian SIRT1 represses forkhead transcription factors. Cell 116: 551-563. (Pubitemid 38264432)
41. Obsil T, Obsilova V. (2008). Structure/function relationships underlying regulation of FOXO transcription factors. Oncogene 27: 2263-2275. (Pubitemid 351501778)
42. Oh SW, Mukhopadhyay A, Svrzikapa N, Jiang F, Davis RJ, Tissenbaum HA. (2005). JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc Natl Acad Sci USA 102: 4494-4499. (Pubitemid 40397140)
43. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, Ding Z et al. (2007). FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128: 309-323. (Pubitemid 46123514)
44. Perrot V, Rechler MM. (2005). The coactivator p300 directly acetylates the forkhead transcription factor Foxo1 and stimulates Foxo1-induced transcription. Mol Endocrinol 19: 2283-2298. (Pubitemid 41258099)
45. Pickart CM. (2001). Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533. (Pubitemid 32663902)
46. Plas DR, Thompson CB. (2003). Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J Biol Chem 278: 12361-12366. (Pubitemid 36800220)
47. Ravid T, Hochstrasser M. (2007). Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat Cell Biol 9: 422-427. (Pubitemid 46511075)
48. Rena G, Guo S, Cichy SC, Unterman TG, Cohen P. (1999). Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J Biol Chem 274: 17179-17183.
49. Schwer B, Verdin E. (2008). Conserved metabolic regulatory functions of sirtuins. Cell Metab 7: 104-112. (Pubitemid 351168554)
50. Sedding DG. (2008). FoxO transcription factors in oxidative stress response and ageing-a new fork on the way to longevity? Biol Chem 389: 279-283. (Pubitemid 351329031)
51. Strohmaier H, Spruck CH, Kaiser P, Won KA, Sangfelt O, Reed SI. (2001). Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413: 316-322. (Pubitemid 32905853)
52. Sun Y. (2006). E3 ubiquitin ligases as cancer targets and biomarkers. Neoplasia 8: 645-654. (Pubitemid 44379791)
53. Sung JY, Kim R, Kim JE, Lee J. (2010). Balance between SIRT1 and DBC1 expression is lost in breast cancer. Cancer Sci 101: 1738-1744.
54. Takaishi H, Konishi H, Matsuzaki H, Ono Y, Shirai Y, Saito N et al. (1999). Regulation of nuclear translocation of forkhead transcription factor AFX by protein kinase B. Proc Natl Acad Sci USA 96: 11836-11841. (Pubitemid 29502819)
55. Tedesco D, Lukas J, Reed SI. (2002). The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the proteinubiquitin ligase SCF(Skp2). Genes Dev 16: 2946-2957. (Pubitemid 35334742)
56. Tissenbaum HA, Guarente L. (2001). Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410: 227-230. (Pubitemid 32216597)
57. van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, Colland F et al. (2006). FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol 8: 1064-1073. (Pubitemid 44473601)
58. van der Horst A, Tertoolen LG, de Vries-Smits LM, Frye RA, Medema RH, Burgering BM. (2004). FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(-SIRT1). J Biol Chem 279: 28873-28879. (Pubitemid 38915754)
59. Verdin E. (2007). AROuSing SIRT1: identification of a novel endogenous SIRT1 activator. Mol Cell 28: 354-356. (Pubitemid 350030567)
60. Wang F, Nguyen M, Qin FX, Tong Q. (2007). SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction. Aging Cell 6: 505-514. (Pubitemid 47087055)
61. Wang F, Tong Q. (2009). SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1's repressive interaction with PPARgamma. Mol Biol Cell 20: 801-808.
62. Wang J, Chen J. (2010). SIRT1 regulates autoacetylation and histone acetyltransferase activity of TIP60. J Biol Chem 285: 11458-11464.
63. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X et al. (2008). ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 10: 138-148. (Pubitemid 351194043)
64. Yang WL, Wang J, Chan CH, Lee SW, Campos AD, Lamothe B et al. (2009). The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science 325: 1134-1138.
65. Yang Y, Hou H, Haller EM, Nicosia SV, Bai W. (2005). Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J 24: 1021-1032. (Pubitemid 40470150)
66. Zou Y, Tsai WB, Cheng CJ, Hsu C, Chung YM, Li PC et al. (2008). Forkhead box transcription factor FOXO3a suppresses estrogendependent breast cancer cell proliferation and tumorigenesis. Breast Cancer Res 10: R21.