Post-transcriptional regulation of autophagy in C2C12 myotubes following starvation and nutrient restoration

International Journal of Biochemistry and Cell Biology

Volumn 54, Issue , 2014, Pages 208-216

  Desgeorges, Marine Maud ^a   Freyssenet, Damien ^a   Chanon, Stéphanie ^c   Castells, Josiane ^a   Pugnière, Pascal ^d   Béchet, Daniel ^e   Peinnequin, André ^d   Devillard, Xavier ^a   Defour, Aurélia ^a,b  

^a UNIVERSITÉ JEAN MONNET   (France)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^c UNIVERSITÉ LYON 1   (France)

^d CENTRE DE RECHERCHES   (France)

^e INRA and University of Auvergne   (France)

Author keywords

Autophagy lysosome; Proteolysis; Skeletal muscle; Ubiquitin proteasome

Indexed keywords

ADENYLATE KINASE; ATG12 PROTEIN; ATROGIN 1; AUTOPHAGY PROTEIN 5; CATHEPSIN B; CATHEPSIN L; CELL NUCLEUS DNA; HISTONE H3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MUSCLE RING FINGER 1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASOME; PROTEIN; PROTEIN BNIP3; PROTEIN KINASE B; PROTEIN S6; S6 KINASE; TRANSCRIPTION FACTOR FKHRL1; UBIQUITIN; ULK1 PROTEIN; UNCLASSIFIED DRUG; ATG5 PROTEIN, MOUSE; BNIP3 PROTEIN, MOUSE; GABARAPL1 PROTEIN, MOUSE; MAP1LC3 PROTEIN, MOUSE; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL PROTEIN; MTOR PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TARGET OF RAPAMYCIN KINASE; ULK1 PROTEIN, MOUSE; AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 13; GABARAPL1 PROTEIN; LC3B PROTEIN; PEPTIDES AND PROTEINS;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BINDING SITE; C2C12 MYOTUBE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; IMAGE ANALYSIS; MUSCLE ATROPHY; MYOTUBE; NUTRIENT; PROMOTER REGION; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STARVATION; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; NUTRITION; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; PROTEIN BINDING;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIAL PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SIGNAL TRANSDUCTION; STARVATION; TOR SERINE-THREONINE KINASES;

EID: 84907331118     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2014.07.008     Document Type: Article

References (30)

1. S. Alers, A.S. Löffler, S. Wesselborg, and B. Stork Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks Mol Cell Biol 32 2012 2 11
2. P. Berthon, S. Duguez, F.B. Favier, A. Amirouche, L. Feasson, and L. Vico et al. Regulation of ubiquitin-proteasome system, caspase enzyme activities, and extracellular proteinases in rat soleus muscle in response to unloading Pflügers Arch 454 2007 625 633 (Pubitemid 46872895)
3. S.C. Bodine, E. Latres, S. Baumhueter, V.K. Lai, L. Nunez, and B.A. Clarke et al. Identification of ubiquitin ligases required for skeletal muscle atrophy Science (New York, N.Y.) 294 2001 1704 1708 (Pubitemid 33104839)
4. J.M. Bogenberger, and P.J. Laybourn Human T lymphotropic virus type 1 protein tax reduces histone levels Retrovirology 5 2008 9
5. P. Bonaldo, and M. Sandri Cellular and molecular mechanisms of muscle atrophy Dis Model Mech 6 2013 25 39
6. S. Duchêne, S. Métayer, E. Audouin, K. Bigot, J. Dupont, and S. Tesseraud Refeeding and insulin activate the AKT/p70S6 kinase pathway without affecting IRS1 tyrosine phosphorylation in chicken muscle Domest Anim Endocrinol 34 2008 1 13 (Pubitemid 350087611)
7. D.F. Egan, D.B. Shackelford, M.M. Mihaylova, S. Gelino, R.A. Kohnz, and W. Mair et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy Science 331 2011 456 461
8. I.G. Ganley, H. Lam du, J. Wang, X. Ding, S. Chen, and X. Jiang ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy J Biol Chem 284 2009 12297 12305
9. A.V. Gomes, D.S. Waddell, R. Siu, M. Stein, S. Dewey, and J.D. Furlow et al. Upregulation of proteasome activity in muscle RING finger 1-null mice following denervation FASEB J 26 2012 2986 2999
10. M.D. Gomes, S.H. Lecker, R.T. Jagoe, A. Navon, and A.L. Goldberg Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy Proc Natl Acad Sci U S A 98 2001 14440 14445 (Pubitemid 33121410)
11. B.S. Gordon, A.R. Kelleher, and S.R. Kimball Regulation of muscle protein synthesis and the effects of catabolic states Int J Biochem Cell Biol 45 2013 2147 2157
12. N. Hosokawa, T. Hara, T. Kaizuka, C. Kishi, A. Takamura, and Y. Miura et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy Mol Biol Cell 20 2009 1981 1991
13. C.H. Jung, C.B. Jun, S.H. Ro, Y.M. Kim, N.M. Otto, and J. Cao et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery Mol Biol Cell 20 2009 1992 2003
14. B. Khambu, M. Uesugi, and Y. Kawazoe Translational repression stabilizes messenger RNA of autophagy-related genes Genes Cells 16 2011 857 867
15. J. Kim, M. Kundu, B. Viollet, and K.-L. Guan AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1 Nat Cell Biol 13 2011 132 141
16. S.R. Kimball, and L.S. Jefferson Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis J Nutr 136 2006 227S 231S (Pubitemid 43156513)
17. A. Kuma, M. Hatano, M. Matsui, A. Yamamoto, H. Nakaya, and T. Yoshimori et al. The role of autophagy during the early neonatal starvation period Nature 432 2004 1032 1036 (Pubitemid 40052234)
18. S.H. Lecker, R.T. Jagoe, A. Gilbert, M. Gomes, V. Baracos, and J. Bailey et al. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression FASEB J 18 2004 39 51 (Pubitemid 38076464)
19. S.H. Lecker, A.L. Goldberg, and W.E. Mitch Protein degradation by the ubiquitin-proteasome pathway in normal and disease states J Am Soc Nephrol 17 2006 1807 1819 (Pubitemid 44036165)
20. C. Mammucari, G. Milan, V. Romanello, E. Masiero, R. Rudolf, and P. Del Piccolo et al. FoxO3 controls autophagy in skeletal muscle in vivo Cell Metab 6 2007 458 471 (Pubitemid 350163055)
21. N. Mizushima Autophagy: process and function Genes Dev 21 2007 2861 2873 (Pubitemid 350133435)
22. S. Mordier, C. Deval, D. Béchet, A. Tassa, and M. Ferrara Leucine limitation induces autophagy and activation of lysosome-dependent proteolysis in C2C12 myotubes through a mammalian target of rapamycin-independent signaling pathway J Biol Chem 275 2000 29900 29906 (Pubitemid 32043876)
23. S.H. Park, S.R. Gammon, J.D. Knippers, S.R. Paulsen, D.S. Rubink, and W.W. Winder Phosphorylation-activity relationships of AMPK and acetyl-CoA carboxylase in muscle J Appl Physiol 92 2002 2475 2482 (Pubitemid 34666373)
24. J.M. Sacheck, A. Ohtsuka, S.C. McLary, and A.L. Goldberg IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 Am J Physiol Endocrinol Metab 287 2004 E591 E601
25. M. Sandri Autophagy in skeletal muscle FEBS Lett 584 2010 1411 1416
26. M. Sandri Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome Int J Biochem Cell Biol 45 2013 2121 2129
27. M. Sandri, C. Sandri, A. Gilbert, C. Skurk, E. Calabria, and A. Picard et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy Cell 117 2004 399 412 (Pubitemid 38534545)
28. T.N. Stitt, D. Drujan, B.A. Clarke, F. Panaro, Y. Timofeyva, and W.O. Kline et al. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors Mol Cell 14 2004 395 403 (Pubitemid 38591410)
29. J. Vandesompele, K.D. Preter, F. Pattyn, B. Poppe, N.V. Roy, and A.D. Paepe et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol 3 2002 research0034
30. J. Zhao, J.J. Brault, A. Schild, P. Cao, M. Sandri, and S. Schiaffino et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells Cell Metab 6 2007 472 483 (Pubitemid 350163056)