FOXO transcription factors: Key regulators of cellular quality control

Trends in Biochemical Sciences

Volumn 39, Issue 4, 2014, Pages 159-169

  Webb, Ashley E ^a   Brunet, Anne ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Aging; Cellular quality control; FOXO transcription factors; Proteostasis

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PROTEASOME; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; FORKHEAD TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE;

AGING; AUTOPHAGY; CELL METABOLISM; CELL TYPE; DEGENERATIVE DISEASE; GENE EXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; LIPOPHAGOCYTOSIS; LONGEVITY; MALIGNANT NEOPLASTIC DISEASE; METABOLIC REGULATION; MITOPHAGY; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; METABOLISM; PATHOLOGY; PROTEIN DEGRADATION; CELL DIFFERENTIATION; CELLULAR QUALITY CONTROL; CYTOLOGY; GENE EXPRESSION REGULATION; MUSCLE; NERVE CELL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; UPREGULATION;

AGING; ANIMALS; AUTOPHAGY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84897414264     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.02.003     Document Type: Review

References (127)

1. Maiese K., et al. OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol. Med. 2008, 14:219-227.
2. Greer E.L., Brunet A. FOXO transcription factors in ageing and cancer. Acta Physiol. (Oxf.) 2008, 192:19-28.
3. Kenyon C.J. The genetics of ageing. Nature 2010, 464:504-512.
4. Kaestner K.H., et al. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 2000, 14:142-146.
5. Brunet A., et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999, 96:857-868.
6. Brunet A., et al. Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 2001, 21:952-965.
7. Kops G.J., et al. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 1999, 398:630-634.
8. Biggs W.H., et al. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:7421-7426.
9. Tran H., et al. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 2002, 296:530-534.
10. Nemoto S., Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002, 295:2450-2452.
11. Altomonte J., et al. Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice. Am. J. Physiol. Endocrinol. Metab. 2003, 285:E718-E728.
12. Ren H., et al. FoxO1 target Gpr17 activates AgRP neurons to regulate food intake. Cell 2012, 149:1314-1326.
13. Yeo H., et al. FoxO3 coordinates metabolic pathways to maintain redox balance in neural stem cells. EMBO J. 2013, 32:2589-2602.
14. Calnan D.R., Brunet A. The FoxO code. Oncogene 2008, 27:2276-2288.
15. Greer E.L., et al. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem. 2007, 282:30107-30119.
16. Essers M.A., et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J. 2004, 23:4802-4812.
17. Oh S.W., et al. JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4494-4499.
18. Lehtinen M.K., et al. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 2006, 125:987-1001.
19. Yang J.Y., et al. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat. Cell Biol. 2008, 10:138-148.
20. Asada S., et al. Mitogen-activated protein kinases, Erk and p38, phosphorylate and regulate Foxo1. Cell. Signal. 2007, 19:519-527.
21. Brunet A., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004, 303:2011-2015.
22. van der Horst A., et al. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J. Biol. Chem. 2004, 279:28873-28879.
23. Calnan D.R., et al. Methylation by Set9 modulates FoxO3 stability and transcriptional activity. Aging (Albany NY) 2012, 4:462-479.
24. Yamagata K., et al. Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol. Cell 2008, 32:221-231.
25. Kikis E.A., et al. Protein homeostasis in models of aging and age-related conformational disease. Adv. Exp. Med. Biol. 2010, 694:138-159.
26. Demontis F., Perrimon N. FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 2010, 143:813-825.
27. Mammucari C., et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007, 6:458-471.
28. Mammucari C., et al. Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 2008, 4:524-526.
29. van der Vos K.E., et al. Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat. Cell Biol. 2012, 14:829-837.
30. Xiong X., et al. The autophagy-related gene 14 (Atg14) is regulated by Forkhead box O transcription factors and circadian rhythms and plays a critical role in hepatic autophagy and lipid metabolism. J. Biol. Chem. 2012, 287:39107-39114.
31. Xu P., et al. JNK regulates FoxO-dependent autophagy in neurons. Genes Dev. 2011, 25:310-322.
32. Zhao J., et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6:472-483.
33. Kume S., et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 2010, 120:1043-1055.
34. Toth M.L., et al. Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy 2008, 4:330-338.
35. Lee J.H., et al. Sestrin as a feedback inhibitor of TOR that prevents age-related pathologies. Science 2010, 327:1223-1228.
36. Simonsen A., et al. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 2008, 4:176-184.
37. Pickford F., et al. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J. Clin. Invest. 2008, 118:2190-2199.
38. Komatsu M., et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006, 441:880-884.
39. Hara T., et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441:885-889.
40. Masiero E., et al. Autophagy is required to maintain muscle mass. Cell Metab. 2009, 10:507-515.
41. Jung H.S., et al. Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab. 2008, 8:318-324.
42. Codogno P., et al. Canonical and non-canonical autophagy: variations on a common theme of self-eating?. Nat. Rev. Mol. Cell Biol. 2012, 13:7-12.
43. Mizushima N., et al. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011, 27:107-132.
44. Wei B., et al. MST1, a key player, in enhancing fast skeletal muscle atrophy. BMC Biol. 2013, 11:12.
45. Liesa M., Shirihai O.S. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013, 17:491-506.
46. Chen H., et al. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 2003, 160:189-200.
47. Lokireddy S., et al. The ubiquitin ligase mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab. 2012, 16:613-624.
48. Pino E., et al. FOXO3 determines the accumulation of α-synuclein and controls the fate of dopaminergic neurons in the substantia nigra. Hum. Mol. Genet. 2014, 10.1093/hmg/ddt530.
49. Koh H., et al. Silent information regulator 2 (Sir2) and Forkhead box O (FOXO) complement mitochondrial dysfunction and dopaminergic neuron loss in Drosophila PTEN-induced kinase 1 (PINK1) null mutant. J. Biol. Chem. 2012, 287:12750-12758.
50. Mei Y., et al. FOXO3a-dependent regulation of Pink1 (Park6) mediates survival signaling in response to cytokine deprivation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5153-5158.
51. Hwang S., et al. Drosophila DJ-1 decreases neural sensitivity to stress by negatively regulating Daxx-like protein through dFOXO. PLoS Genet. 2013, 9:e1003412.
52. Singh R., Cuervo A.M. Lipophagy: connecting autophagy and lipid metabolism. Int. J. Cell Biol. 2012, 2012:282041.
53. Kamei Y., et al. A forkhead transcription factor FKHR up-regulates lipoprotein lipase expression in skeletal muscle. FEBS Lett. 2003, 536:232-236.
54. Sengupta A., et al. FoxO transcription factors promote autophagy in cardiomyocytes. J. Biol. Chem. 2009, 284:28319-28331.
55. Warr M.R., et al. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 2013, 494:323-327.
56. Jia K., et al. Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signaling-regulated pathogen resistance. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14564-14569.
57. McColl G., et al. Insulin-like signaling determines survival during stress via posttranscriptional mechanisms in C. elegans. Cell Metab. 2010, 12:260-272.
58. Hansen M., et al. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 2008, 4:e24.
59. Melendez A., et al. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 2003, 301:1387-1391.
60. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
61. Hosokawa N., et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol. Biol. Cell 2009, 20:1981-1991.
62. Jung C.H., et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol. Biol. Cell 2009, 20:1992-2003.
63. Bjedov I., et al. Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab. 2010, 11:35-46.
64. Harrison D.E., et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009, 460:392-395.
65. Kaeberlein M., et al. Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 2005, 310:1193-1196.
66. Jia K., et al. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 2004, 131:3897-3906.
67. Powers R.W., et al. Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 2006, 20:174-184.
68. Tothova Z., et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007, 128:325-339.
69. Miyamoto K., et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 2007, 1:101-112.
70. Lee J.Y., et al. mTOR activation induces tumor suppressors that inhibit leukemogenesis and deplete hematopoietic stem cells after Pten deletion. Cell Stem Cell 2010, 7:593-605.
71. Chen C., et al. mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Sci. Signal. 2009, 2:ra75.
72. Vellai T., et al. Genetics: influence of TOR kinase on lifespan in C. elegans. Nature 2003, 426:620.
73. Meissner B., et al. Deletion of the intestinal peptide transporter affects insulin and TOR signaling in Caenorhabditis elegans. J. Biol. Chem. 2004, 279:36739-36745.
74. Kenyon C., et al. A C. elegans mutant that lives twice as long as wild type. Nature 1993, 366:461-464.
75. Lapierre L.R., et al. Autophagy and lipid metabolism coordinately modulate life span in germline-less C. elegans. Curr. Biol. 2011, 21:1507-1514.
76. Wang M.C., et al. Fat metabolism links germline stem cells and longevity in C. elegans. Science 2008, 322:957-960.
77. Fu L.L., et al. Beclin-1: autophagic regulator and therapeutic target in cancer. Int. J. Biochem. Cell Biol. 2013, 45:921-924.
78. Wang R.C., et al. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 2012, 338:956-959.
79. Mizushima N., Klionsky D.J. Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 2007, 27:19-40.
80. Low P. The role of ubiquitin-proteasome system in ageing. Gen. Comp. Endocrinol. 2011, 172:39-43.
81. Gidalevitz T., et al. Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 2006, 311:1471-1474.
82. Taylor R.C., Dillin A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 2011, 3:a004440.
83. Shibatani T., et al. Alteration of rat liver 20S proteasome activities by age and food restriction. J. Gerontol. A: Biol. Sci. Med. Sci. 1996, 51:B316-B322.
84. Conconi M., et al. Age-related decline of rat liver multicatalytic proteinase activity and protection from oxidative inactivation by heat-shock protein 90. Arch. Biochem. Biophys. 1996, 331:232-240.
85. Petropoulos I., et al. Increase of oxidatively modified protein is associated with a decrease of proteasome activity and content in aging epidermal cells. J. Gerontol. A: Biol. Sci. Med. Sci. 2000, 55:B220-B227.
86. Bulteau A.L., et al. Age-dependent declines in proteasome activity in the heart. Arch. Biochem. Biophys. 2002, 397:298-304.
87. Husom A.D., et al. Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 2004, 421:67-76.
88. Ciechanover A., Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003, 40:427-446.
89. Gumucio J.P., Mendias C.L. Atrogin-1, MuRF-1, and sarcopenia. Endocrine 2013, 43:12-21.
90. Sandri M., et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004, 117:399-412.
91. Stitt T.N., et al. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 2004, 14:395-403.
92. Sandri M., et al. PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:16260-16265.
93. Bodine S.C., et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001, 294:1704-1708.
94. Vilchez D., et al. Increased proteasome activity in human embryonic stem cells is regulated by PSMD11. Nature 2012, 489:304-308.
95. Vilchez D., et al. FOXO4 is necessary for neural differentiation of human embryonic stem cells. Aging Cell 2013, 12:518-522.
96. Vilchez D., et al. RPN-6 determines C. elegans longevity under proteotoxic stress conditions. Nature 2012, 489:263-268.
97. Santamaria P.G., et al. Rpn6p, a proteasome subunit from Saccharomyces cerevisiae, is essential for the assembly and activity of the 26 S proteasome. J. Biol. Chem. 2003, 278:6687-6695.
98. Honda Y., Honda S. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J. 1999, 13:1385-1393.
99. Hsu A.L., et al. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003, 300:1142-1145.
100. Lopez-Otin C., et al. The hallmarks of aging. Cell 2013, 153:1194-1217.
101. Son J.H., et al. Neuronal autophagy and neurodegenerative diseases. Exp. Mol. Med. 2012, 44:89-98.
102. Lecker S.H., et al. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J. Am. Soc. Nephrol. 2006, 17:1807-1819.
103. Micel L.N., et al. Role of ubiquitin ligases and the proteasome in oncogenesis: novel targets for anticancer therapies. J. Clin. Oncol. 2013, 31:1231-1238.
104. Anselmi C.V., et al. Association of the FOXO3A locus with extreme longevity in a southern Italian centenarian study. Rejuvenation Res. 2009, 12:95-104.
105. Flachsbart F., et al. Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2700-2705.
106. Li Y., et al. Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum. Mol. Genet. 2009, 18:4897-4904.
107. Pawlikowska L., et al. Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 2009, 8:460-472.
108. Willcox B.J., et al. FOXO3A genotype is strongly associated with human longevity. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13987-13992.
109. Lee J.C., et al. Human SNP links differential outcomes in inflammatory and infectious disease to a FOXO3-regulated pathway. Cell 2013, 155:57-69.
110. Donlon T.A., et al. FOXO3 gene variants and human aging: coding variants may not be key players. J. Gerontol. A: Biol. Sci. Med. Sci. 2012, 67:1132-1139.
111. Pyo J.O., et al. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat. Commun. 2013, 4:2300.
112. Morley J.F., et al. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:10417-10422.
113. Parker J.A., et al. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat. Genet. 2005, 37:349-350.
114. Cohen E., et al. Opposing activities protect against age-onset proteotoxicity. Science 2006, 313:1604-1610.
115. Boccitto M., et al. Daf-2 signaling modifies mutant SOD1 toxicity in C. elegans. PLoS ONE 2012, 7:e33494.
116. Cohen E., et al. Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 2009, 139:1157-1169.
117. Bhutia S.K., et al. Autophagy: cancer's friend or foe?. Adv. Cancer Res. 2013, 118:61-95.
118. Hu M.C., et al. IκB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 2004, 117:225-237.
119. Paik J.H., et al. FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 2007, 128:309-323.
120. Sykes S.M., et al. AKT/FOXO signaling enforces reversible differentiation blockade in myeloid leukemias. Cell 2011, 146:697-708.
121. Brady C.A., et al. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 2011, 145:571-583.
122. Dobrowolny G., et al. Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab. 2008, 8:425-436.
123. Shin D.J., et al. Genome-wide analysis of FoxO1 binding in hepatic chromatin: potential involvement of FoxO1 in linking retinoid signaling to hepatic gluconeogenesis. Nucleic Acids Res. 2012, 40:11499-11509.
124. Lin Y.C., et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 2010, 11:635-643.
125. Litvak V., et al. A FOXO3-IRF7 gene regulatory circuit limits inflammatory sequelae of antiviral responses. Nature 2012, 490:421-425.
126. reg cell function. Nature 2012, 491:554-559.
127. Webb A.E., et al. FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. Cell Rep. 2013, 4:477-491.