Post-translational modifications of FOXO family proteins (Review)
- Authors:
- Ziyao Wang
- Tinghe Yu
- Ping Huang
-
Affiliations: National Key Clinical Department, Department of Hepatobiliary Surgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing 400000, P.R. China, Chongqing Key Medical Laboratory of Obstetrics and Gynecology, The Second Affiliated Hospital of Chongqing Medical University, Chongqing Medical University, Chongqing 400000, P.R. China - Published online on: October 20, 2016 https://doi.org/10.3892/mmr.2016.5867
- Pages: 4931-4941
This article is mentioned in:
Abstract
Weigel D, Jürgens G, Küttner F, Seifert E and Jäckle H: The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell. 57:645–658. 1989. View Article : Google Scholar : PubMed/NCBI | |
Weigel D and Jäckle H: The fork head domain: A novel DNA binding motif of eukaryotic transcription factors? Cell. 63:455–456. 1990. View Article : Google Scholar : PubMed/NCBI | |
Kaufmann E and Knöchel W: Five years on the wings of fork head. Mech Dev. 57:3–20. 1996. View Article : Google Scholar : PubMed/NCBI | |
Furuyama T, Nakazawa T, Nakano I and Mori N: Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem J. 349:629–634. 2000. View Article : Google Scholar : PubMed/NCBI | |
Kaestner KH, Knochel W and Martinez DE: Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14:142–146. 2000.PubMed/NCBI | |
Myatt SS and Lam EW: The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer. 7:847–859. 2007. View Article : Google Scholar : PubMed/NCBI | |
Shen X, Cui J and Gong Q: Fox gene loci in Takifugu rubripes and Tetraodon nigroviridis genomes and comparison with those of medaka and zebrafish genomes. Genome. 54:965–972. 2011. View Article : Google Scholar : PubMed/NCBI | |
Greer EL and Brunet A: FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene. 24:7410–7425. 2005. View Article : Google Scholar : PubMed/NCBI | |
Jacobs FM, van der Heide LP, Wijchers PJ, Burbach JP, Hoekman MF and Smidt MP: FoxO6, a novel member of the FoxO class of transcription factors with distinct shuttling dynamics. J Biol Chem. 278:35959–35967. 2003. View Article : Google Scholar : PubMed/NCBI | |
Hu HJ, Zhang LG, Wang ZH and Guo XX: FoxO6 inhibits cell proliferation in lung carcinoma through up-regulation of USP7. Mol Med Rep. 12:575–580. 2015.PubMed/NCBI | |
Kim DH, Zhang T, Lee S, Calabuig-Navarro V, Yamauchi J, Piccirillo A, Fan Y, Uppala R, Goetzman E and Dong HH: FoxO6 integrates insulin signaling with MTP for regulating VLDL production in the liver. Endocrinology. 155:1255–1267. 2014. View Article : Google Scholar : PubMed/NCBI | |
Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM and Degnan BM: Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol. 25:980–996. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lapierre LR, Kumsta C, Sandri M, Ballabio A and Hansen M: Transcriptional and epigenetic regulation of autophagy in aging. Autophagy. 11:867–880. 2015. View Article : Google Scholar : PubMed/NCBI | |
Edmonds JW, Prasain JK, Dorand D, Yang Y, Hoang HD, Vibbert J, Kubagawa HM and Miller MA: Insulin/FOXO signaling regulates ovarian prostaglandins critical for reproduction. Dev Cell. 19:858–871. 2010. View Article : Google Scholar : PubMed/NCBI | |
Lin L, Hron JD and Peng SL: Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity. 21:203–213. 2004. View Article : Google Scholar : PubMed/NCBI | |
Smith WW, Norton DD, Gorospe M, Jiang H, Nemoto S, Holbrook NJ, Finkel T and Kusiak JW: Phosphorylation of p66Shc and forkhead proteins mediates Abeta toxicity. J Cell Biol. 169:331–339. 2005. View Article : Google Scholar : PubMed/NCBI | |
van der Vos KE and Coffer PJ: The extending network of FOXO transcriptional target genes. Antioxid Redox Signal. 14:579–592. 2011. View Article : Google Scholar : PubMed/NCBI | |
Huang H, Regan KM, Wang F, Wang D, Smith DI, van Deursen JM and Tindall DJ: Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci USA. 102:1649–1654. 2005. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Gan L, Pan H, Guo S, He X, Olson ST, Mesecar A, Adam S and Unterman TG: Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J Biol Chem. 277:45276–45284. 2002. View Article : Google Scholar : PubMed/NCBI | |
Brunet A, Park J, Tran H, Hu LS, Hemmings BA and Greenberg ME: Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol Cell Biol. 21:952–965. 2001. View Article : Google Scholar : PubMed/NCBI | |
Brunet A, Kanai F, Stehn J, Xu J, Sarbassova D, Frangioni JV, Dalal SN, DeCaprio JA, Greenberg ME and Yaffe MB: 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol. 156:817–828. 2002. View Article : Google Scholar : PubMed/NCBI | |
Obsilova V, Vecer J, Herman P, Pabianova A, Sulc M, Teisinger J, Boura E and Obsil T: 14-3-3 Protein interacts with nuclear localization sequence of forkhead transcription factor FoxO4. Biochemistry. 44:11608–11617. 2005. View Article : Google Scholar : PubMed/NCBI | |
Rena G, Prescott AR, Guo S, Cohen P and Unterman TG: Roles of the forkhead in rhabdomyosarcoma (FKHR) phosphorylation sites in regulating 14-3-3 binding, transactivation and nuclear targetting. Biochem J. 354:605–612. 2001. View Article : Google Scholar : PubMed/NCBI: | |
Tsai WC, Bhattacharyya N, Han LY, Hanover JA and Rechler MM: Insulin inhibition of transcription stimulated by the forkhead protein Foxo1 is not solely due to nuclear exclusion. Endocrinology. 144:5615–5622. 2003. View Article : Google Scholar : PubMed/NCBI | |
Obsil T, Ghirlando R, Anderson DE, Hickman AB and Dyda F: Two 14-3-3 binding motifs are required for stable association of Forkhead transcription factor FOXO4 with 14-3-3 proteins and inhibition of DNA binding. Biochemistry. 42:15264–15272. 2003. View Article : Google Scholar : PubMed/NCBI | |
Plas DR and Thompson CB: Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J Biol Chem. 278:12361–12366. 2003. View Article : Google Scholar : PubMed/NCBI | |
Aoki M, Jiang H and Vogt PK: Proteasomal degradation of the FoxO1 transcriptional regulator in cells transformed by the P3k and Akt oncoproteins. Proc Natl Acad Sci USA. 101:13613–13617. 2004. View Article : Google Scholar : PubMed/NCBI | |
Matsuzaki H, Daitoku H, Hatta M, Tanaka K and Fukamizu A: Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Proc Natl Acad Sci USA. 100:11285–11290. 2003. View Article : Google Scholar : PubMed/NCBI | |
Santo EE, Stroeken P, Sluis PV, Koster J, Versteeg R and Westerhout EM: FOXO3a is a major target of inactivation by PI3K/AKT signaling in aggressive neuroblastoma. Cancer Res. 73:2189–2198. 2013. View Article : Google Scholar : PubMed/NCBI | |
Alon U: Network motifs: Theory and experimental approaches. Nat Rev Genet. 8:450–461. 2007. View Article : Google Scholar : PubMed/NCBI | |
Zhang W, Hietakangas V, Wee S, Lim SC, Gunaratne J and Cohen SM: ER stress potentiates insulin resistance through PERK-mediated FOXO phosphorylation. Genes Dev. 27:441–449. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mounir Z, Krishnamoorthy JL, Wang S, Papadopoulou B, Campbell S, Muller WJ, Hatzoglou M and Koromilas AE: Akt determines cell fate through inhibition of the PERK-eIF2α phosphorylation pathway. Sci Signal. 4:ra622011. View Article : Google Scholar : PubMed/NCBI | |
Bobrovnikova-Marjon E, Pytel D, Riese MJ, Vaites LP, Singh N, Koretzky GA, Witze ES and Diehl JA: PERK utilizes intrinsic lipid kinase activity to generate phosphatidic acid, mediate Akt activation, and promote adipocyte differentiation. Mol Cell Biol. 32:2268–2278. 2012. View Article : Google Scholar : PubMed/NCBI | |
Xiao L and Yuan Z: Redemystifying MST1/hippo signaling. Protein Cell. 1:706–708. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zeng Q and Hong W: The emerging role of the hippo pathway in cell contact inhibition, organ size control and cancer development in mammals. Cancer Cell. 13:188–192. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villén J, Becker EB, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK and Bonni A: A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell. 125:987–1001. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yuan Z, Lehtinen MK, Merlo P, Villén J, Gygi S and Bonni A: Regulation of neuronal cell death by MST1-FOXO1 signaling. J Biol Chem. 284:11285–11292. 2009. View Article : Google Scholar : PubMed/NCBI | |
Valis K, Prochazka L, Boura E, Chladova J, Obsil T, Rohlena J, Truksa J, Dong LF, Ralph SJ and Neuzil J: Hippo/Mst1 stimulates transcription of the proapoptotic mediator NOXA in a FoxO1-dependent manner. Cancer Res. 71:946–954. 2011. View Article : Google Scholar : PubMed/NCBI | |
Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, Bos JL and Burgering BM: FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J. 23:4802–4812. 2004. View Article : Google Scholar : PubMed/NCBI: | |
van den Berg MC, van Gogh IJ, Smits AM, van Triest M, Dansen TB, Visscher M, Polderman PE, Vliem MJ, Rehmann H and Burgering BM: The small GTPase RALA controls c-Jun N-terminal kinase-mediated FOXO activation by regulation of a JIP1 scaffold complex. J Biol Chem. 288:21729–21741. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sunayama J, Tsuruta F, Masuyama N and Gotoh Y: JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3. J Cell Biol. 170:295–304. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kawamori D, Kaneto H, Nakatani Y, Matsuoka TA, Matsuhisa M, Hori M and Yamasaki Y: The forkhead transcription factor Foxo1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J Biol Chem. 281:1091–1098. 2006. View Article : Google Scholar : PubMed/NCBI | |
Song JJ and Lee YJ: Cross-talk between JIP3 and JIP1 during glucose deprivation: SEK1-JNK2 and Akt1 act as mediators. J Biol Chem. 280:26845–26855. 2005. View Article : Google Scholar : PubMed/NCBI | |
Asada S, Daitoku H, Matsuzaki H, Saito T, Sudo T, Mukai H, Iwashita S, Kako K, Kishi T, Kasuya Y and Fukamizu A: Mitogen-activated protein kinases, Erk and p38, phosphorylate and regulate Foxo1. Cell Signal. 19:519–527. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ho KK, McGuire VA, Koo CY, Muir KW, de Olano N, Maifoshie E, Kelly DJ, McGovern UB, Monteiro LJ, Gomes AR, et al: Phosphorylation of FOXO3a on Ser-7 by p38 promotes its nuclear localization in response to doxorubicin. J Biol Chem. 287:1545–1555. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lin A, Yao J, Zhuang L, Wang D, Han J, Lam EW and Gan B: The FoxO-BNIP3 axis exerts a unique regulation of mTORC1 and cell survival under energy stress. Oncogene. 33:3183–3194. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X, Lang JY, Lai CC, Chang CJ, Huang WC, et al: ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol. 10:138–148. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hu Y, Wang X, Zeng L, Cai DY, Sabapathy K, Goff SP, Firpo EJ and Li B: ERK phosphorylates p66shcA on Ser36 and subsequently regulates p27kip1 expression via the Akt-FOXO3a pathway: Implication of p27kip1 in cell response to oxidative stress. Mol Biol Cell. 16:3705–3718. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pramod S and Shivakumar K: Mechanisms in cardiac fibroblast growth: An obligate role for Skp2 and FOXO3a in ERK1/2 MAPK-dependent regulation of p27kip1. Am J Physiol Heart Circ Physiol. 306:H844–H855. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kodiha M, Banski P and Stochaj U: Interplay between MEK and PI3Kinase signaling regulates the subcellular localization of protein kinases ERK1/2 and Akt upon oxidative stress. FEBS Lett. 583:1987–1993. 2009. View Article : Google Scholar : PubMed/NCBI | |
Huang H, Regan KM, Lou Z, Chen J and Tindall DJ: CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage. Science. 314:294–297. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yuan Z, Becker EB, Merlo P, Yamada T, DiBacco S, Konishi Y, Schaefer EM and Bonni A: Activation of FOXO1 by Cdk1 in cycling cells and postmitotic neurons. Science. 319:1665–1668. 2008. View Article : Google Scholar : PubMed/NCBI | |
Liu P, Kao TP and Huang H: CDK1 promotes cell proliferation and survival via phosphorylation and inhibition of FOXO1 transcription factor. Oncogene. 27:4733–4744. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zhou J, Li H, Li X, Zhang G, Niu Y, Yuan Z, Herrup K, Zhang YW, Bu G, Xu H and Zhang J: The roles of Cdk5-mediated subcellular localization of FOXO1 in neuronal death. J Neurosci. 35:2624–2635. 2015. View Article : Google Scholar : PubMed/NCBI | |
Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP and Brunet A: The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem. 282:30107–30119. 2007. View Article : Google Scholar : PubMed/NCBI | |
Chiacchiera F, Matrone A, Ferrari E, Ingravallo G, Lo Sasso G, Murzilli S, Petruzzelli M, Salvatore L, Moschetta A and Simone C: p38alpha blockade inhibits colorectal cancer growth in vivo by inducing a switch from HIF1alpha- to FoxO-dependent transcription. Cell Death Differ. 16:1203–1214. 2009. View Article : Google Scholar : PubMed/NCBI | |
Yun H, Park S, Kim MJ, Yang WK, Im DU, Yang KR, Hong J, Choe W, Kang I, Kim SS and Ha J: AMP-activated protein kinase mediates the antioxidant effects of resveratrol through regulation of the transcription factor FoxO1. FEBS J. 281:4421–4438. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chiacchiera F and Simone C: The AMPK-FoxO3A axis as a target for cancer treatment. Cell Cycle. 9:1091–1096. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nakashima K and Yakabe Y: AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem. 71:1650–1656. 2007. View Article : Google Scholar : PubMed/NCBI | |
Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, Simonatto M, Fusella A, Ryall JG, Finley LW, Haigis MC, et al: A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci. 70:2015–2029. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li XN, Song J, Zhang L, LeMaire SA, Hou X, Zhang C, Coselli JS, Chen L, Wang XL, Zhang Y and Shen YH: Activation of the AMPK-FOXO3 pathway reduces fatty acid-induced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes. 58:2246–2257. 2009. View Article : Google Scholar : PubMed/NCBI | |
Sengupta A, Molkentin JD, Paik JH, DePinho RA and Yutzey KE: FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem. 286:7468–7478. 2011. View Article : Google Scholar : PubMed/NCBI | |
Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP and Brunet A: An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol. 17:1646–1656. 2007. View Article : Google Scholar : PubMed/NCBI | |
Tullet JM, Araiz C, Sanders MJ, Au C, Benedetto A, Papatheodorou I, Clark E, Schmeisser K, Jones D, Schuster EF, et al: DAF-16/FoxO directly regulates an atypical AMP-activated protein kinase gamma isoform to mediate the effects of insulin/IGF-1 signaling on aging in Caenorhabditis elegans. PLoS Genet. 10:e10041092014. View Article : Google Scholar : PubMed/NCBI | |
Eijkelenboom A, Mokry M, de Wit E, Smits LM, Polderman PE, van Triest MH, van Boxtel R, Schulze A, de Laat W, Cuppen E and Burgering BM: Genome-wide analysis of FOXO3 mediated transcription regulation through RNA polymerase II profiling. Mol Syst Biol. 9:6382013. View Article : Google Scholar : PubMed/NCBI | |
Lützner N, De-Castro Arce J and Rösl F: Gene expression of the tumour suppressor LKB1 is mediated by Sp1, NF-Y and FOXO transcription factors. PLoS One. 7:e325902012. View Article : Google Scholar : PubMed/NCBI | |
Cantó C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P and Auwerx J: AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature. 458:1056–1060. 2009. View Article : Google Scholar : PubMed/NCBI | |
Tezil T, Bodur C, Kutuk O and Basaga H: IKK-β mediates chemoresistance by sequestering FOXO3; a critical factor for cell survival and death. Cell Signal. 24:1361–1368. 2012. View Article : Google Scholar : PubMed/NCBI | |
Shen RR and Hahn WC: Emerging roles for the non-canonical IKKs in cancer. Oncogene. 30:631–641. 2011. View Article : Google Scholar : PubMed/NCBI | |
Guo JP, Tian W, Shu S, Xin Y, Shou C and Cheng JQ: IKBKE phosphorylation and inhibition of FOXO3a: A mechanism of IKBKE oncogenic function. PLoS One. 8:e636362013. View Article : Google Scholar : PubMed/NCBI | |
Guo JP, Coppola D and Cheng JQ: IKBKE protein activates Akt independent of phosphatidylinositol 3-kinase/PDK1/mTORC2 and the pleckstrin homology domain to sustain malignant transformation. J Biol Chem. 286:37389–37398. 2011. View Article : Google Scholar : PubMed/NCBI | |
Luron L, Saliba D, Blazek K, Lanfrancotti A and Udalova IA: FOXO3 as a new IKK-ε-controlled check-point of regulation of IFN-β expression. Eur J Immunol. 42:1030–1037. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chapuis N, Park S, Leotoing L, Tamburini J, Verdier F, Bardet V, Green AS, Willems L, Agou F, Ifrah N, et al: IkB kinase overcomes PI3K/Akt and ERK/MAPK to control FOXO3a activity in acute myeloid leukemia. Blood. 116:4240–4250. 2010. View Article : Google Scholar : PubMed/NCBI | |
Wilson MK, McWhirter SM, Amin RH, Huang D and Schlissel MS: Abelson virus transformation prevents TRAIL expression by inhibiting FoxO3a and NF-kappaB. Mol Cells. 29:333–341. 2010. View Article : Google Scholar : PubMed/NCBI | |
Li Z, Zhang H, Chen Y, Fan L and Fang J: Forkhead transcription factor FOXO3a protein activates nuclear factor kB through B-cell lymphoma/leukemia 10 (BCL10) protein and promotes tumor cell survival in serum deprivation. J Biol Chem. 287:17737–17745. 2012. View Article : Google Scholar : PubMed/NCBI | |
West AC and Johnstone RW: New and emerging HDAC inhibitors for cancer treatment. J Clin Invest. 124:30–39. 2014. View Article : Google Scholar : PubMed/NCBI | |
Auburger G, Gispert S and Jendrach M: Mitochondrial acetylation and genetic models of Parkinson's disease. Prog Mol Biol Transl Sci. 127:155–182. 2014. View Article : Google Scholar : PubMed/NCBI | |
Khongkow M, Olmos Y, Gong C, Gomes AR, Monteiro LJ, Yagüe E, Cavaco TB, Khongkow P, Man EP, Laohasinnarong S, et al: SIRT6 modulates paclitaxel and epirubicin resistance and survival in breast cancer. Carcinogenesis. 34:1476–1486. 2013. View Article : Google Scholar : PubMed/NCBI | |
Beharry AW, Sandesara PB, Roberts BM, Ferreira LF, Senf SM and Judge AR: HDAC1 activates FoxO and is both sufficient and required for skeletal muscle atrophy. J Cell Sci. 127:1441–1453. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, Downes M, Evans RM, Montminy M and Shaw RJ: Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell. 145:607–621. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bertaggia E, Coletto L and Sandri M: Posttranslational modifications control FoxO3 activity during denervation. Am J Physiol Cell Physiol. 302:C587–C596. 2012. View Article : Google Scholar : PubMed/NCBI | |
Senf SM, Sandesara PB, Reed SA and Judge AR: p300 Acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol. 300:C1490–C1501. 2011. View Article : Google Scholar : PubMed/NCBI | |
Salminen A, Kaarniranta K and Kauppinen A: Crosstalk between oxidative stress and SIRT1: Impact on the aging process. Int J Mol Sci. 14:3834–3859. 2013. View Article : Google Scholar : PubMed/NCBI | |
Xiong S, Salazar G, Patrushev N and Alexander RW: FoxO1 mediates an autofeedback loop regulating SIRT1 expression. J Biol Chem. 286:5289–5299. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wang YQ, Cao Q, Wang F, Huang LY, Sang TT, Liu F and Chen SY: SIRT1 protects against oxidative stress-induced endothelial progenitor cells apoptosis by inhibiting FOXO3a via FOXO3a ubiquitination and degradation. J Cell Physiol. 230:2098–2107. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wang F, Chan CH, Chen K, Guan X, Lin HK and Tong Q: Deacetylation of FOXO3 by SIRT1 or SIRT2 leads to Skp2-mediated FOXO3 ubiquitination and degradation. Oncogene. 31:1546–1557. 2012. View Article : Google Scholar : PubMed/NCBI | |
Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, Gu W, Bultsma Y, McBurney M and Guarente L: Mammalian SIRT1 represses forkhead transcription factors. Cell. 116:551–563. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kitamura YI, Kitamura T, Kruse JP, Raum JC, Stein R, Gu W and Accili D: FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab. 2:153–163. 2005. View Article : Google Scholar : PubMed/NCBI | |
Aquilano K, Baldelli S, Pagliei B and Ciriolo MR: Extranuclear localization of SIRT1 and PGC-1α: An insight into possible roles in diseases associated with mitochondrial dysfunction. Curr Mol Med. 13:140–154. 2013. View Article : Google Scholar : PubMed/NCBI | |
Morselli E, Mariño G, Bennetzen MV, Eisenberg T, Megalou E, Schroeder S, Cabrera S, Bénit P, Rustin P, Criollo A, et al: Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome. J Cell Biol. 192:615–629. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ng F and Tang BL: Sirtuins' modulation of autophagy. J Cell Physiol. 228:2262–2270. 2013. View Article : Google Scholar : PubMed/NCBI | |
Yun JM, Chien A, Jialal I and Devaraj S: Resveratrol up-regulates SIRT1 and inhibits cellular oxidative stress in the diabetic milieu: Mechanistic insights. J Nutr Biochem. 23:699–705. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sin TK, Yung BY and Siu PM: Modulation of SIRT1-Foxo1 signaling axis by resveratrol: Implications in skeletal muscle aging and insulin resistance. Cell Physiol Biochem. 35:541–552. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yang Y, Hou H, Haller EM, Nicosia SV and Bai W: Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J. 24:1021–1032. 2005. View Article : Google Scholar : PubMed/NCBI | |
Liu X, Greer C and Secombe J: KDM5 interacts with Foxo to modulate cellular levels of oxidative stress. PLoS Genet. 10:e10046762014. View Article : Google Scholar : PubMed/NCBI | |
Wang F, Nguyen M, Qin FX and Tong Q: SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction. Aging Cell. 6:505–514. 2007. View Article : Google Scholar : PubMed/NCBI | |
Wang F and Tong Q: SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1's repressive interaction with PPARgamma. Mol Biol Cell. 20:801–808. 2009. View Article : Google Scholar : PubMed/NCBI | |
Jing E, Gesta S and Kahn CR: SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab. 6:105–114. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, et al: Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol. 27:8807–8814. 2007. View Article : Google Scholar : PubMed/NCBI | |
Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD, van der Meer R, Nguyen P, Savage J, Owens KM, et al: SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell. 17:41–52. 2010. View Article : Google Scholar : PubMed/NCBI | |
Jia G, Su L, Singhal S and Liu X: Emerging roles of SIRT6 on telomere maintenance, DNA repair, metabolism and mammalian aging. Mol Cell Biochem. 364:345–350. 2012. View Article : Google Scholar : PubMed/NCBI | |
Matsuzaki H, Daitoku H, Hatta M, Aoyama H, Yoshimochi K and Fukamizu A: Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc Natl Acad Sci USA. 102:11278–11283. 2005. View Article : Google Scholar : PubMed/NCBI | |
Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, et al: Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 303:2011–2015. 2004. View Article : Google Scholar : PubMed/NCBI | |
Fukuoka M, Daitoku H, Hatta M, Matsuzaki H, Umemura S and Fukamizu A: Negative regulation of forkhead transcription factor AFX (Foxo4) by CBP-induced acetylation. Int J Mol Med. 12:503–508. 2003.PubMed/NCBI | |
van der Horst A, Tertoolen LG, de Vries-Smits LM, Frye RA, Medema RH and Burgering BM: FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J Biol Chem. 279:28873–28879. 2004. View Article : Google Scholar : PubMed/NCBI | |
Qiang L, Banks AS and Accili D: Uncoupling of acetylation from phosphorylation regulates FoxO1 function independent of its subcellular localization. J Biol Chem. 285:27396–27401. 2010. View Article : Google Scholar : PubMed/NCBI | |
Perrot V and Rechler MM: The coactivator p300 directly acetylates the forkhead transcription factor Foxo1 and stimulates Foxo1-induced transcription. Mol Endocrinol. 19:2283–2298. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pramanik KC, Fofaria NM, Gupta P and Srivastava SK: CBP-mediated FOXO-1 acetylation inhibits pancreatic tumor growth by targeting SirT. Mol Cancer Ther. 13:687–698. 2014. View Article : Google Scholar : PubMed/NCBI | |
Nakae J, Cao Y, Hakuno F, Takemori H, Kawano Y, Sekioka R, Abe T, Kiyonari H, Tanaka T, Sakai J, et al: Novel repressor regulates insulin sensitivity through interaction with Foxo1. EMBO J. 31:2275–2295. 2012. View Article : Google Scholar : PubMed/NCBI | |
Li F, Xie P, Fan Y, Zhang H, Zheng L, Gu D, Patterson C and Li H: C terminus of Hsc70-interacting protein promotes smooth muscle cell proliferation and survival through ubiquitin-mediated degradation of FoxO1. J Biol Chem. 284:20090–20098. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kato S, Ding J, Pisck E, Jhala US and Du K: COP1 functions as a FoxO1 ubiquitin E3 ligase to regulate FoxO1-mediated gene expression. J Biol Chem. 283:35464–35473. 2008. View Article : Google Scholar : PubMed/NCBI | |
Hu MC, Lee DF, Xia W, Golfman LS, Ou-Yang F, Yang JY, Zou Y, Bao S, Hanada N, Saso H, et al: IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell. 117:225–237. 2004. View Article : Google Scholar : PubMed/NCBI | |
Brenkman AB, de Keizer PL, van den Broek NJ, Jochemsen AG and Burgering BM: Mdm2 induces mono-ubiquitination of FOXO4. PLoS One. 3:e28192008. View Article : Google Scholar : PubMed/NCBI | |
van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, Colland F, Maurice MM and Burgering BM: FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol. 8:1064–1073. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hall JA, Tabata M, Rodgers JT and Puigserver P: USP7 attenuates hepatic gluconeogenesis through modulation of FoxO1 gene promoter occupancy. Mol Endocrinol. 28:912–924. 2014. View Article : Google Scholar : PubMed/NCBI | |
Li HH, Willis MS, Lockyer P, Miller N, McDonough H, Glass DJ and Patterson C: Atrogin-1 inhibits Akt-dependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of Forkhead proteins. J Clin Invest. 117:3211–3223. 2007. View Article : Google Scholar : PubMed/NCBI | |
Ratti F, Ramond F, Moncollin V, Simonet T, Milan G, Méjat A, Thomas JL, Streichenberger N, Gilquin B, Matthias P, et al: Histone deacetylase 6 is a FoxO transcription factor-dependent effector in skeletal muscle atrophy. J Biol Chem. 290:4215–4224. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yamagata K, Daitoku H, Takahashi Y, Namiki K, Hisatake K, Kako K, Mukai H, Kasuya Y and Fukamizu A: Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol Cell. 32:221–231. 2008. View Article : Google Scholar : PubMed/NCBI | |
Huang J and Berger SL: The emerging field of dynamic lysine methylation of non-histone proteins. Curr Opin Genet Dev. 18:152–158. 2008. View Article : Google Scholar : PubMed/NCBI | |
Xie Q, Hao Y, Tao L, Peng S, Rao C, Chen H, You H, Dong MQ and Yuan Z: Lysine methylation of FOXO3 regulates oxidative stress-induced neuronal cell death. EMBO Rep. 13:371–377. 2012. View Article : Google Scholar : PubMed/NCBI | |
Calnan DR, Webb AE, White JL, Stowe TR, Goswami T, Shi X, Espejo A, Bedford MT, Gozani O, Gygi SP and Brunet A: Methylation by Set9 modulates FoxO3 stability and transcriptional activity. Aging (Albany NY). 4:462–479. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kuo M, Zilberfarb V, Gangneux N, Christeff N and Issad T: O-glycosylation of FoxO1 increases its transcriptional activity towards the glucose 6-phosphatase gene. FEBS Lett. 582:829–834. 2008. View Article : Google Scholar : PubMed/NCBI | |
Housley MP, Rodgers JT, Udeshi ND, Kelly TJ, Shabanowitz J, Hunt DF, Puigserver P and Hart GW: O-GlcNAc regulates FoxO activation in response to glucose. J Biol Chem. 283:16283–16292. 2008. View Article : Google Scholar : PubMed/NCBI | |
Butt AM, Feng D, Idrees M, Tong Y and Lu J: Computational identification and modeling of crosstalk between phosphorylation, O-β-glycosylation and methylation of FoxO3 and implications for cancer therapeutics. Int J Mol Sci. 13:2918–2938. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ho SR, Wang K, Whisenhunt TR, Huang P, Zhu X, Kudlow JE and Paterson AJ: O-GlcNAcylation enhances FOXO4 transcriptional regulation in response to stress. FEBS Lett. 584:49–54. 2010. View Article : Google Scholar : PubMed/NCBI |