The Translation Regulatory Subunit EIF3f Controls the Kinase-dependent MTOR Signaling Required for Muscle Differentiation and Hypertrophy in Mouse

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2010 Feb 4

PMID 20126553

Citations 42

Authors

Alfredo Csibi

Karen Cornille

Marie-Pierre Leibovitch

Anne Poupon

Lionel A Tintignac

Anthony M J Sanchez

Serge A Leibovitch

Affiliations

Soon will be listed here.

Abstract

The mTORC1 pathway is required for both the terminal muscle differentiation and hypertrophy by controlling the mammalian translational machinery via phosphorylation of S6K1 and 4E-BP1. mTOR and S6K1 are connected by interacting with the eIF3 initiation complex. The regulatory subunit eIF3f plays a major role in muscle hypertrophy and is a key target that accounts for MAFbx function during atrophy. Here we present evidence that in MAFbx-induced atrophy the degradation of eIF3f suppresses S6K1 activation by mTOR, whereas an eIF3f mutant insensitive to MAFbx polyubiquitination maintained persistent phosphorylation of S6K1 and rpS6. During terminal muscle differentiation a conserved TOS motif in eIF3f connects mTOR/raptor complex, which phosphorylates S6K1 and regulates downstream effectors of mTOR and Cap-dependent translation initiation. Thus eIF3f plays a major role for proper activity of mTORC1 to regulate skeletal muscle size.

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References

Shi J, Hershey J, Nelson M . Phosphorylation of the eukaryotic initiation factor 3f by cyclin-dependent kinase 11 during apoptosis. FEBS Lett. 2009; 583(6):971-7. PMC: 2666973. DOI: 10.1016/j.febslet.2009.02.028. View

Erbay E, Chen J . The mammalian target of rapamycin regulates C2C12 myogenesis via a kinase-independent mechanism. J Biol Chem. 2001; 276(39):36079-82. DOI: 10.1074/jbc.C100406200. View

Luthy R, Bowie J, Eisenberg D . Assessment of protein models with three-dimensional profiles. Nature. 1992; 356(6364):83-5. DOI: 10.1038/356083a0. View

Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W . Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997; 25(17):3389-402. PMC: 146917. DOI: 10.1093/nar/25.17.3389. View

Richardson C, Schalm S, Blenis J . PI3-kinase and TOR: PIKTORing cell growth. Semin Cell Dev Biol. 2004; 15(2):147-59. DOI: 10.1016/j.semcdb.2003.12.023. View

Holz M, Ballif B, Gygi S, Blenis J . mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell. 2005; 123(4):569-80. DOI: 10.1016/j.cell.2005.10.024. View

Coeytaux K, Poupon A . Prediction of unfolded segments in a protein sequence based on amino acid composition. Bioinformatics. 2005; 21(9):1891-900. DOI: 10.1093/bioinformatics/bti266. View

Gingras A, Raught B, Sonenberg N . Regulation of translation initiation by FRAP/mTOR. Genes Dev. 2001; 15(7):807-26. DOI: 10.1101/gad.887201. View

Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, Viereck J . Fast/Glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab. 2008; 7(2):159-72. PMC: 2828690. DOI: 10.1016/j.cmet.2007.11.003. View

10.

Gomes M, Lecker S, Jagoe R, Navon A, GOLDBERG A . Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci U S A. 2001; 98(25):14440-5. PMC: 64700. DOI: 10.1073/pnas.251541198. View

11.

Park I, Chen J . Mammalian target of rapamycin (mTOR) signaling is required for a late-stage fusion process during skeletal myotube maturation. J Biol Chem. 2005; 280(36):32009-17. DOI: 10.1074/jbc.M506120200. View

12.

Csibi A, Tintignac L, Leibovitch M, Leibovitch S . eIF3-f function in skeletal muscles: to stand at the crossroads of atrophy and hypertrophy. Cell Cycle. 2008; 7(12):1698-701. DOI: 10.4161/cc.7.12.6090. View

13.

Ohanna M, Sobering A, Lapointe T, Lorenzo L, Praud C, Petroulakis E . Atrophy of S6K1(-/-) skeletal muscle cells reveals distinct mTOR effectors for cell cycle and size control. Nat Cell Biol. 2005; 7(3):286-94. DOI: 10.1038/ncb1231. View

14.

Csibi A, Leibovitch M, Cornille K, Tintignac L, Leibovitch S . MAFbx/Atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines. J Biol Chem. 2008; 284(7):4413-21. DOI: 10.1074/jbc.M807641200. View

15.

Miyamoto S, Patel P, Hershey J . Changes in ribosomal binding activity of eIF3 correlate with increased translation rates during activation of T lymphocytes. J Biol Chem. 2005; 280(31):28251-64. DOI: 10.1074/jbc.M414129200. View

16.

Lecker S, Jagoe R, Gilbert A, Gomes M, Baracos V, Bailey J . Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 2004; 18(1):39-51. DOI: 10.1096/fj.03-0610com. View

17.

Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg M, Hall A . Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol. 2004; 6(11):1122-8. DOI: 10.1038/ncb1183. View

18.

Reynaud E, Leibovitch M, Tintignac L, Pelpel K, Guillier M, Leibovitch S . Stabilization of MyoD by direct binding to p57(Kip2). J Biol Chem. 2000; 275(25):18767-76. DOI: 10.1074/jbc.M907412199. View

19.

Shi J, Kahle A, Hershey J, Honchak B, Warneke J, Leong S . Decreased expression of eukaryotic initiation factor 3f deregulates translation and apoptosis in tumor cells. Oncogene. 2006; 25(35):4923-36. DOI: 10.1038/sj.onc.1209495. View

20.

Frodin M, Antal T, Dummler B, Jensen C, Deak M, Gammeltoft S . A phosphoserine/threonine-binding pocket in AGC kinases and PDK1 mediates activation by hydrophobic motif phosphorylation. EMBO J. 2002; 21(20):5396-407. PMC: 129083. DOI: 10.1093/emboj/cdf551. View