FoxO transcription factors: Their roles in the maintenance of skeletal muscle homeostasis

Cellular and Molecular Life Sciences

Volumn 71, Issue 9, 2014, Pages 1657-1671

  Sanchez, Anthony M J ^a,b   Candau, Robin B ^a,b   Bernardi, Henri ^a  

^a University of Montpellier   (France)

^b UNIV MONTPELLIER   (France)

Author keywords

Atrophy; Autophagy; E3 ligase; Forkhead box class O; Metabolism; Mitophagy

Indexed keywords

ANIMALS; AUTOPHAGY; ENERGY METABOLISM; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MITOCHONDRIA; MUSCLE, SKELETAL; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84899450195     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1513-z     Document Type: Review

References (137)

1. Goldberg AL, Etlinger JD, Goldspink DF, Jablecki C (1975) Mechanism of work-induced hypertrophy of skeletal muscle. Med Sci Sports 7(3):185-198
2. Adibi SA, Krzysik BA, Morse EL, Amin PM, Allen ER (1974) Oxidative energy metabolism in the skeletal muscle: biochemical and ultrastructural evidence for adaptive changes. J Lab Clin Med 83(4):548-562
3. Dijkers PF, Medema RH, Pals C, Banerji L, Thomas NS, Lam EW, Burgering BM, Raaijmakers JA, Lammers JW, Koenderman L, Coffer PJ (2000) Forkhead transcription factor FKHR-L1 modulates cytokine-dependent transcriptional regulation of p27(KIP1). Mol Cell Biol 20(24):9138-9148 (Pubitemid 32246103)
4. Medema RH, Kops GJ, Bos JL, Burgering BM (2000) AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404(6779):782-787 (Pubitemid 30212408)
5. Tran H, Brunet A, Grenier JM, Datta SR, Fornace AJ Jr, DiStefano PS, Chiang LW, Greenberg ME (2002) DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296(5567):530-534 (Pubitemid 34408672)
6. Furukawa-Hibi Y, Yoshida-Araki K, Ohta T, Ikeda K, Motoyama N (2002) FOXO forkhead transcription factors induce G(2)-M checkpoint in response to oxidative stress. J Biol Chem 277(30):26729-26732 (Pubitemid 34951676)
7. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Burgering BM (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419(6904):316-321
8. Nemoto S, Finkel T (2002) Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295(5564):2450-2452 (Pubitemid 34270258)
9. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389(6654):994-999 (Pubitemid 27485694)
10. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857-868 (Pubitemid 29165088)
11. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ (2000) Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 10(19):1201-1204
12. Lehmann OJ, Tuft S, Brice G, Smith R, Blixt A, Bell R, Johansson B, Jordan T, Hitchings RA, Khaw PT, John SW, Carlsson P, Bhattacharya SS (2003) Novel anterior segment phenotypes resulting from forkhead gene alterations: evidence for cross-species conservation of function. Invest Ophthalmol Vis Sci 44(6):2627-2633 (Pubitemid 36618423)
13. Nakae J, Cao Y, Daitoku H, Fukamizu A, Ogawa W, Yano Y, Hayashi Y (2006) The LXXLL motif of murine forkhead transcription factor FoxO1 mediates Sirt1-dependent transcriptional activity. J Clin Investig 116(9):2473-2483 (Pubitemid 44330146)
14. Furuyama T, Nakazawa T, Nakano I, Mori N (2000) Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem J 349(Pt 2):629-634 (Pubitemid 30465799)
15. Chung SY, Huang WC, Su CW, Lee KW, Chi HC, Lin CT, Chen ST, Huang KM, Tsai MS, Yu HP, Chen SL (2013) FoxO6 and PGC-1alpha form a regulatory loop in myogenic cells. Biosci Rep 33(3). doi: 10.1042/BSR20130031
16. Salih DA, Rashid AJ, Colas D, de la Torre-Ubieta L, Zhu RP, Morgan AA, Santo EE, Ucar D, Devarajan K, Cole CJ, Madison DV, Shamloo M, Butte AJ, Bonni A, Josselyn SA, Brunet A (2012) FoxO6 regulates memory consolidation and synaptic function. Genes Dev 26(24):2780-2801
17. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA (2003) Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301(5630):215-218 (Pubitemid 36858475)
18. Hosaka T, Biggs WH III, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC (2004) Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 101(9):2975-2980 (Pubitemid 38327721)
19. Ni YG, Berenji K, Wang N, Oh M, Sachan N, Dey A, Cheng J, Lu G, Morris DJ, Castrillon DH, Gerard RD, Rothermel BA, Hill JA (2006) Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation 114(11):1159-1168 (Pubitemid 44386480)
20. Hu P, Geles KG, Paik JH, DePinho RA, Tjian R (2008) Codependent activators direct myoblast-specific MyoD transcription. Dev Cell 15(4):534-546
21. Zhou W, Cao Q, Peng Y, Zhang QJ, Castrillon DH, DePinho RA, Liu ZP (2009) FoxO4 inhibits NF-kappaB and protects mice against colonic injury and inflammation. Gastroenterology 137(4):1403-1414
22. Eijkelenboom A, Burgering BM (2013) FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14(2):83-97
23. Bertaggia E, Coletto L, Sandri M (2012) Posttranslational modifications control FoxO3 activity during denervation. Am J Physiol Cell Physiol 302(3):C587-C596
24. Senf SM, Sandesara PB, Reed SA, Judge AR (2011) p300 Acetyltransferase activity differentially regulates the localization and activity of the FOXO homologues in skeletal muscle. Am J Physiol Cell Physiol 300(6):C1490-C1501
25. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3(11):1014-1019 (Pubitemid 34428747)
26. Dan HC, Sun M, Yang L, Feldman RI, Sui XM, Ou CC, Nellist M, Yeung RS, Halley DJ, Nicosia SV, Pledger WJ, Cheng JQ (2002) Phosphatidylinositol 3-kinase/Akt pathway regulates tuberous sclerosis tumor suppressor complex by phosphorylation of tuberin. J Biol Chem 277(38):35364-35370
27. Inoki K, Li Y, Zhu T, Wu J, Guan KL (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4(9):648-657 (Pubitemid 34993700)
28. Vander Haar E, Lee SI, Bandhakavi S, Griffin TJ, Kim DH (2007) Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat Cell Biol 9(3):316-323 (Pubitemid 46344611)
29. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14(3):395-403 (Pubitemid 38591410)
30. Cahill CM, Tzivion G, Nasrin N, Ogg S, Dore J, Ruvkun G, Alexander-Bridges M (2001) Phosphatidylinositol 3-kinase signaling inhibits DAF-16 DNA binding and function via 14-3-3-dependent and 14-3-3-independent pathways. J Biol Chem 276(16):13402-13410
31. Zhang BH, Tang ED, Zhu T, Greenberg ME, Vojtek AB, Guan KL (2001) Serum- and glucocorticoid-inducible kinase SGK phosphorylates and negatively regulates B-Raf. J Biol Chem 276(34):31620-31626 (Pubitemid 37384806)
32. 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(6728):630-634 (Pubitemid 29183692)
33. Takaishi H, Konishi H, Matsuzaki H, Ono Y, Shirai Y, Saito N, Kitamura T, Ogawa W, Kasuga M, Kikkawa U, Nishizuka Y (1999) Regulation of nuclear translocation of forkhead transcription factor AFX by protein kinase B. Proc Natl Acad Sci USA 96(21):11836-11841 (Pubitemid 29502819)
34. Reynolds THt, Merrell E, Cinquino N, Gaugler M, Ng L (2012) Disassociation of insulin action and Akt/FOXO signaling in skeletal muscle of older Akt-deficient mice. Am J Physiol Regul Integr Comp Physiol 303(11):R1186-R1194
35. Sanchez AM, Candau RB, Csibi A, Pagano AF, Raibon A, Bernardi H (2012) The role of AMP-activated protein kinase in the coordination of skeletal muscle turnover and energy homeostasis. Am J Physiol Cell Physiol 303(5):C475-C485
36. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, Brunet A (2007) The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282(41):30107-30119 (Pubitemid 350035296)
37. Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, Bernardi H, Candau R (2012) AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem 113(2):695-710
38. Tong JF, Yan X, Zhu MJ, Du M (2009) AMP-activated protein kinase enhances the expression of muscle-specific ubiquitin ligases despite its activation of IGF-1/Akt signaling in C2C12 myotubes. J Cell Biochem 108(2):458-468
39. Nakashima K, Yakabe Y (2007) 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(7):1650-1656 (Pubitemid 47358716)
40. Williamson DL, Butler DC, Alway SE (2009) AMPK inhibits myoblast differentiation through a PGC-1alpha-dependent mechanism. Am J Physiol Endocrinol Metab 297(2):E304-E314
41. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458(7241):1056-1060
42. Canto C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, Lagouge M, Zierath JR, Auwerx J (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab 11(3):213-219
43. Nystrom GJ, Lang CH (2008) Sepsis and AMPK Activation by AICAR Differentially Regulate FoxO-1, -3 and -4 mRNA in Striated Muscle. Int J Clin Exp Med 1(1):50-63
44. Schmoll D, Walker KS, Alessi DR, Grempler R, Burchell A, Guo S, Walther R, Unterman TG (2000) Regulation of glucose-6-phosphatase gene expression by protein kinase Balpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and -independent effects of insulin on promoter activity. J Biol Chem 275(46):36324-36333
45. Nakae J, Biggs WH III, Kitamura T, Cavenee WK, Wright CV, Arden KC, Accili D (2002) Regulation of insulin action and pancreatic beta-cell function by mutated alleles of the gene encoding forkhead transcription factor Foxo1. Nat Genet 32(2):245-253
46. Rached MT, Kode A, Silva BC, Jung DY, Gray S, Ong H, Paik JH, DePinho RA, Kim JK, Karsenty G, Kousteni S (2010) FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice. J Clin Investig 120(1):357-368
47. Furuyama T, Kitayama K, Yamashita H, Mori N (2003) Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 375(Pt 2):365-371 (Pubitemid 37315444)
48. Bowker-Kinley MM, Davis WI, Wu P, Harris RA, Popov KM (1998) Evidence for existence of tissue-specific regulation of the mammalian pyruvate dehydrogenase complex. Biochem J 329(Pt 1):191-196 (Pubitemid 28022308)
49. Bastie CC, Nahle Z, McLoughlin T, Esser K, Zhang W, Unterman T, Abumrad NA (2005) FoxO1 stimulates fatty acid uptake and oxidation in muscle cells through CD36-dependent and -independent mechanisms. J Biol Chem 280(14):14222-14229 (Pubitemid 40517324)
50. Constantin-Teodosiu D, Constantin D, Stephens F, Laithwaite D, Greenhaff PL (2012) The role of FOXO and PPAR transcription factors in diet-mediated inhibition of PDC activation and carbohydrate oxidation during exercise in humans and the role of pharmacological activation of PDC in overriding these changes. Diabetes 61(5):1017-1024
51. Rauramaa R, Kuusela P, Hietanen E (1980) Adipose, muscle and lung tissue lipoprotein lipase activities in young streptozotocin treated rats. Horm Metab Res 12(11):591-595 (Pubitemid 11196230)
52. Kamei Y, Mizukami J, Miura S, Suzuki M, Takahashi N, Kawada T, Taniguchi T, Ezaki O (2003) A forkhead transcription factor FKHR up-regulates lipoprotein lipase expression in skeletal muscle. FEBS Lett 536(1-3):232-236 (Pubitemid 36206437)
53. Tsuchida A, Yamauchi T, Ito Y, Hada Y, Maki T, Takekawa S, Kamon J, Kobayashi M, Suzuki R, Hara K, Kubota N, Terauchi Y, Froguel P, Nakae J, Kasuga M, Accili D, Tobe K, Ueki K, Nagai R, Kadowaki T (2004) Insulin/Foxo1 pathway regulates expression levels of adiponectin receptors and adiponectin sensitivity. J Biol Chem 279(29):30817-30822 (Pubitemid 38938015)
54. Peserico A, Chiacchiera F, Grossi V, Matrone A, Latorre D, Simonatto M, Fusella A, Ryall JG, Finley LW, Haigis MC, Villani G, Puri PL, Sartorelli V, Simone C (2013) A novel AMPK-dependent FoxO3A-SIRT3 intramitochondrial complex sensing glucose levels. Cell Mol Life Sci 70(11):2015-2029
55. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, Yang Y, Chen Y, Hirschey MD, Bronson RT, Haigis M, Guarente LP, Farese RV Jr, Weissman S, Verdin E, Schwer B (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27(24):8807-8814
56. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL (2004) Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117(3):399-412 (Pubitemid 38534545)
57. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6(6):458-471 (Pubitemid 350163055)
58. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294(5547):1704-1708 (Pubitemid 33104839)
59. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98(25):14440-14445 (Pubitemid 33121410)
60. Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, Nishino I, Ezaki O (2004) Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 279(39):41114-41123 (Pubitemid 39287713)
61. Lagirand-Cantaloube J, Cornille K, Csibi A, Batonnet-Pichon S, Leibovitch MP, Leibovitch SA (2009) Inhibition of atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS ONE 4(3):e4973
62. Lagirand-Cantaloube J, Offner N, Csibi A, Leibovitch MP, Batonnet-Pichon S, Tintignac LA, Segura CT, Leibovitch SA (2008) The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J 27(8):1266-1276 (Pubitemid 351574748)
63. Tintignac LA, Lagirand J, Batonnet S, Sirri V, Leibovitch MP, Leibovitch SA (2005) Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J Biol Chem 280(4):2847-2856 (Pubitemid 40189393)
64. Jogo M, Shiraishi S, Tamura TA (2009) Identification of MAFbx as a myogenin-engaged F-box protein in SCF ubiquitin ligase. FEBS Lett 583(17):2715-2719
65. Lokireddy S, Wijesoma IW, Sze SK, McFarlane C, Kambadur R, Sharma M (2012) Identification of atrogin-1-targeted proteins during the myostatin-induced skeletal muscle wasting. Am J Physiol Cell Physiol 303(5):C512-C529
66. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ (2007) The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6(5):376-385 (Pubitemid 350011998)
67. Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E, Goldberg AL (2009) During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185(6):1083-1095
68. Cohen S, Zhai B, Gygi SP, Goldberg AL (2012) Ubiquitylation by Trim32 causes coupled loss of desmin, Z-bands, and thin filaments in muscle atrophy. J Cell Biol 198(4):575-589
69. Kudryashova E, Kudryashov D, Kramerova I, Spencer MJ (2005) Trim32 is a ubiquitin ligase mutated in limb girdle muscular dystrophy type 2H that binds to skeletal muscle myosin and ubiquitinates actin. J Mol Biol 354(2):413-424 (Pubitemid 41579855)
70. Hishiya A, Iemura S, Natsume T, Takayama S, Ikeda K, Watanabe K (2006) A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J 25(3):554-564 (Pubitemid 43237662)
71. Klionsky DJ, Codogno P (2013) The mechanism and physiological function of macroautophagy. J Innate Immun 427-433
72. Codogno P (2004) ATG genes and macroautophagy. Med Sci 20(8-9):734-736
73. Mizushima N, Sugita H, Yoshimori T, Ohsumi Y (1998) A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem 273(51):33889-33892 (Pubitemid 29008848)
74. Mizushima N, Noda T, Ohsumi Y (1999) Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J 18(14):3888-3896 (Pubitemid 29335842)
75. Romanov J, Walczak M, Ibiricu I, Schuchner S, Ogris E, Kraft C, Martens S (2012) Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J 31(22):4304-4317
76. Walczak M, Martens S (2013) Dissecting the role of the Atg12-Atg5-Atg16 complex during autophagosome formation. Autophagy 9(3):424-425
77. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19(21):5720-5728
78. Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130(1):165-178 (Pubitemid 47031316)
79. Matsuura A, Tsukada M, Wada Y, Ohsumi Y (1997) Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192(2):245-250 (Pubitemid 27268249)
80. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150(6):1507-1513
81. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T (2001) Beclin- phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2(4):330-335 (Pubitemid 32401529)
82. Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y (2001) The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J 20(21):5971-5981 (Pubitemid 33049272)
83. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6(6):472-483 (Pubitemid 350163056)
84. Yamazaki Y, Kamei Y, Sugita S, Akaike F, Kanai S, Miura S, Hirata Y, Troen BR, Kitamura T, Nishino I, Suganami T, Ezaki O, Ogawa Y (2010) The cathepsin L gene is a direct target of FOXO1 in skeletal muscle. Biochem J 427(1):171-178
85. Reed SA, Sandesara PB, Senf SM, Judge AR (2012) Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB J 26(3):987-1000
86. Raben N, Hill V, Shea L, Takikita S, Baum R, Mizushima N, Ralston E, Plotz P (2008) Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease. Hum Mol Genet 17(24):3897-3908 (Pubitemid 352762852)
87. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27(2):433-446 (Pubitemid 351161653)
88. Lokireddy S, Wijesoma IW, Teng S, Bonala S, Gluckman PD, McFarlane C, Sharma M, Kambadur R (2012) The ubiquitin ligase Mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab 16(5):613-624
89. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141(2):280-289
90. Rathbone CR, Booth FW, Lees SJ (2008) FoxO3a preferentially induces p27Kip1 expression while impairing muscle precursor cell-cycle progression. Muscle Nerve 37(1):84-89
91. Machida S, Spangenburg EE, Booth FW (2003) Forkhead transcription factor FoxO1 transduces insulin-like growth factor's signal to p27Kip1 in primary skeletal muscle satellite cells. J Cell Physiol 196(3):523-531 (Pubitemid 36927747)
92. Shi X, Bowlin KM, Garry DJ (2010) Fhl2 interacts with Foxk1 and corepresses Foxo4 activity in myogenic progenitors. Stem Cells 28(3):462-469
93. Shi X, Wallis AM, Gerard RD, Voelker KA, Grange RW, Depinho RA, Garry MG, Garry DJ (2012) Foxk1 promotes cell proliferation and represses myogenic differentiation by regulating Foxo4 and Mef2. J Cell Sci 125(Pt 22):5329-5337
94. Hribal ML, Nakae J, Kitamura T, Shutter JR, Accili D (2003) Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J Cell Biol 162(4):535-541 (Pubitemid 37022932)
95. Kitamura T, Kitamura YI, Funahashi Y, Shawber CJ, Castrillon DH, Kollipara R, DePinho RA, Kitajewski J, Accili D (2007) A Foxo/Notch pathway controls myogenic differentiation and fiber type specification. J Clin Investig 117(9):2477-2485 (Pubitemid 47494349)
96. Wu AL, Kim JH, Zhang C, Unterman TG, Chen J (2008) Forkhead box protein O1 negatively regulates skeletal myocyte differentiation through degradation of mammalian target of rapamycin pathway components. Endocrinology 149(3):1407-1414 (Pubitemid 351397941)
97. Erbay E, Park IH, Nuzzi PD, Schoenherr CJ, Chen J (2003) IGF-II transcription in skeletal myogenesis is controlled by mTOR and nutrients. J Cell Biol 163(5):931-936 (Pubitemid 37541870)
98. Bois PR, Grosveld GC (2003) FKHR (FOXO1a) is required for myotube fusion of primary mouse myoblasts. EMBO J 22(5):1147-1157 (Pubitemid 36313598)
99. Liu CM, Yang Z, Liu CW, Wang R, Tien P, Dale R, Sun LQ (2007) Effect of RNA oligonucleotide targeting Foxo-1 on muscle growth in normal and cancer cachexia mice. Cancer Gene Ther 14(12):945-952 (Pubitemid 350115358)
100. Allen DL, Unterman TG (2007) Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors. Am J Physiol Cell Physiol 292(1):C188-C199
101. Baehr LM, Furlow JD, Bodine SC (2011) Muscle sparing in muscle RING finger 1 null mice: response to synthetic glucocorticoids. J Physiol 589(Pt 19):4759-4776
102. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Del Piccolo P, Foretz M, Scorrano L, Rudolf R, Sandri M (2010) Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 29(10):1774-1785
103. McLoughlin TJ, Smith SM, DeLong AD, Wang H, Unterman TG, Esser KA (2009) FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am J Physiol Cell Physiol 297(3):C548-C555
104. Siu PM, Pistilli EE, Butler DC, Alway SE (2005) Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am J Physiol Cell Physiol 288(2):C338-C349
105. Siu PM, Alway SE (2005) Id2 and p53 participate in apoptosis during unloading-induced muscle atrophy. Am J Physiol Cell Physiol 288(5):C1058-C1073
106. Adhihetty PJ, O'Leary MF, Chabi B, Wicks KL, Hood DA (2007) Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J Appl Physiol 102(3):1143-1151 (Pubitemid 46377042)
107. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, Mukku V, Edgerton VR (1997) Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol 273(2 Pt 1):C579-C587
108. Vande Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S, Hakem R, Greenberg AH (2000) BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 20(15):5454-5468 (Pubitemid 30482883)
109. Chipuk JE, Fisher JC, Dillon CP, Kriwacki RW, Kuwana T, Green DR (2008) Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad Sci USA 105(51):20327-20332
110. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL (2004) Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18(1):39-51 (Pubitemid 38076464)
111. Schakman O, Dehoux M, Bouchuari S, Delaere S, Lause P, Decroly N, Shoelson SE, Thissen JP (2012) Role of IGF-I and the TNFalpha/NF-kappaB pathway in the induction of muscle atrogenes by acute inflammation. Am J Physiol Endocrinol Metab 303(6):E729-E739
112. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303(5666):2011-2015 (Pubitemid 38393275)
113. Greer EL, Brunet A (2005) FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24(50):7410-7425 (Pubitemid 41637981)
114. Sandri M, Barberi L, Bijlsma AY, Blaauw B, Dyar KA, Milan G, Mammucari C, Meskers CG, Pallafacchina G, Paoli A, Pion D, Roceri M, Romanello V, Serrano AL, Toniolo L, Larsson L, Maier AB, Munoz-Canoves P, Musaro A, Pende M, Reggiani C, Rizzuto R, Schiaffino S (2013) Signalling pathways regulating muscle mass in ageing skeletal muscle. The role of the IGF1-Akt-mTOR-FoxO pathway. Biogerontology 14(3):303-323
115. Whitman SA, Wacker MJ, Richmond SR, Godard MP (2005) Contributions of the ubiquitin-proteasome pathway and apoptosis to human skeletal muscle wasting with age. Pflugers Arch 450(6):437-446 (Pubitemid 41380702)
116. Pardo PS, Lopez MA, Boriek AM (2008) FOXO transcription factors are mechanosensitive and their regulation is altered with aging in the respiratory pump. Am J Physiol Cell Physiol 294(4):C1056-C1066
117. Edstrom E, Altun M, Hagglund M, Ulfhake B (2006) Atrogin-1/MAFbx and MuRF1 are downregulated in aging-related loss of skeletal muscle. J Gerontol Ser A Biol Sci Med Sci 61(7):663-674 (Pubitemid 44148351)
118. Furuyama T, Yamashita H, Kitayama K, Higami Y, Shimokawa I, Mori N (2002) Effects of aging and caloric restriction on the gene expression of Foxo1, 3, and 4 (FKHR, FKHRL1, and AFX) in the rat skeletal muscles. Microsc Res Tech 59(4):331-334 (Pubitemid 35332954)
119. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92(6):829-839 (Pubitemid 28155321)
120. Goto M, Terada S, Kato M, Katoh M, Yokozeki T, Tabata I, Shimokawa T (2000) cDNA Cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats. Biochem Biophys Res Commun 274(2):350-354 (Pubitemid 30614322)
121. Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen M, Kelly DP, Holloszy JO (2002) Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 16(14):1879-1886 (Pubitemid 35462607)
122. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418(6899):797-801
123. Russell AP, Feilchenfeldt J, Schreiber S, Praz M, Crettenand A, Gobelet C, Meier CA, Bell DR, Kralli A, Giacobino JP, Deriaz O (2003) Endurance training in humans leads to fiber type-specific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferator-activated receptor-alpha in skeletal muscle. Diabetes 52(12):2874-2881 (Pubitemid 37466855)
124. Daitoku H, Yamagata K, Matsuzaki H, Hatta M, Fukamizu A (2003) Regulation of PGC-1 promoter activity by protein kinase B and the forkhead transcription factor FKHR. Diabetes 52(3):642-649 (Pubitemid 36323569)
125. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103(44):16260-16265 (Pubitemid 44715184)
126. Brault JJ, Jespersen JG, Goldberg AL (2010) Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 285(25):19460-19471
127. Yuan Y, Shi XE, Liu YG, Yang GS (2011) FoxO1 regulates muscle fiber-type specification and inhibits calcineurin signaling during C2C12 myoblast differentiation. Mol Cell Biochem 348(1-2):77-87
128. Naya FJ, Mercer B, Shelton J, Richardson JA, Williams RS, Olson EN (2000) Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J Biol Chem 275(7):4545-4548 (Pubitemid 30108834)
129. Nagatomo F, Fujino H, Kondo H, Suzuki H, Kouzaki M, Takeda I, Ishihara A (2011) PGC-1alpha and FOXO1 mRNA levels and fiber characteristics of the soleus and plantaris muscles in rats after hindlimb unloading. Histol Histopathol 26(12):1545-1553
130. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA (2005) Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J 19(11):1498-1500 (Pubitemid 41279010)
131. Marfe G, Tafani M, Pucci B, Di Stefano C, Indelicato M, Andreoli A, Russo MA, Sinibaldi-Salimei P, Manzi V (2010) The effect of marathon on mRNA expression of anti-apoptotic and pro-apoptotic proteins and sirtuins family in male recreational long-distance runners. BMC Physiol 10:7
132. Jamart C, Francaux M, Millet GY, Deldicque L, Frere D, Feasson L (2012) Modulation of autophagy and ubiquitin-proteasome pathways during ultra-endurance running. J Appl Physiol 112(9):1529-1537
133. Pasiakos SM, McClung HL, McClung JP, Urso ML, Pikosky MA, Cloutier GJ,
134. Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103(5):1744-1751 (Pubitemid 350033861)
135. Jamart C, Naslain D, Gilson H, Francaux M (2013) Higher activation of autophagy in skeletal muscle of mice during endurance exercise in the fasted state. Am J Physiol Endocrinol Metab 305(8):E964-974
136. Goodman CA, Frey JW, Mabrey DM, Jacobs BL, Lincoln HC, You JS, Hornberger TA (2011) The role of skeletal muscle mTOR in the regulation of mechanical load-induced growth. J Physiol 589(Pt 22):5485-5501
137. He C, Bassik MC, Moresi V, Sun K, Wei Y, Zou Z, An Z, Loh J, Fisher J, Sun Q, Korsmeyer S, Packer M, May HI, Hill JA, Virgin HW, Gilpin C, Xiao G, Bassel-Duby R, Scherer PE, Levine B (2012) Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 481(7382):511-515