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PMID: 16916907 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy.

The Journal of physiology ·Vol. 576 ·No. Pt 3 ·2006-11-01 ·Pages 923-33

Léger B, Cartoni R, Praz M, Lamon S, Dériaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP

Abstract

Skeletal muscle size is tightly regulated by the synergy between anabolic and catabolic signalling pathways which, in humans, have not been well characterized. Akt has been suggested to play a pivotal role in the regulation of skeletal muscle hypertrophy and atrophy in rodents and cells. Here we measured the amount of phospho-Akt and several of its downstream anabolic targets (glycogen synthase kinase-3beta (GSK-3beta), mTOR, p70(s6k) and 4E-BP1) and catabolic targets (Foxo1, Foxo3, atrogin-1 and MuRF1). All measurements were performed in human quadriceps muscle biopsies taken after 8 weeks of both hypertrophy-stimulating resistance training and atrophy-stimulating de-training. Following resistance training a muscle hypertrophy ( approximately 10%) and an increase in phospho-Akt, phospho-GSK-3beta and phospho-mTOR protein content were observed. This was paralleled by a decrease in Foxo1 nuclear protein content. Following the de-training period a muscle atrophy (5%), relative to the post-training muscle size, a decrease in phospho-Akt and GSK-3beta and an increase in Foxo1 were observed. Atrogin-1 and MuRF1 increased after the hypertrophy and decreased after the atrophy phases. We demonstrate, for the first time in human skeletal muscle, that the regulation of Akt and its downstream signalling pathways GSK-3beta, mTOR and Foxo1 are associated with both the skeletal muscle hypertrophy and atrophy processes.

MeSH Terms
Adaptor Proteins, Signal Transducing/genetics,metabolism Adult Atrophy/genetics,metabolism,pathology Cell Cycle Proteins Forkhead Box Protein O1 Forkhead Box Protein O3 Forkhead Transcription Factors/genetics,metabolism Gene Expression Regulation/physiology Glycogen Synthase Kinase 3/genetics,metabolism Glycogen Synthase Kinase 3 beta Humans Hypertrophy/genetics,metabolism,pathology Male Muscle Proteins/genetics,metabolism Muscle, Skeletal/metabolism,pathology Phosphoproteins/genetics,metabolism Protein Kinases/genetics,metabolism Proto-Oncogene Proteins c-akt/genetics,metabolism RNA, Messenger/genetics,metabolism Ribosomal Protein S6 Kinases, 70-kDa/genetics,metabolism SKP Cullin F-Box Protein Ligases/genetics,metabolism Signal Transduction/genetics,physiology TOR Serine-Threonine Kinases Tripartite Motif Proteins Ubiquitin-Protein Ligases/genetics,metabolism
Chemicals
Adaptor Proteins, Signal Transducing Cell Cycle Proteins EIF4EBP1 protein, human FOXO1 protein, human FOXO3 protein, human Forkhead Box Protein O1 Forkhead Box Protein O3 Forkhead Transcription Factors Muscle Proteins Phosphoproteins RNA, Messenger Tripartite Motif Proteins FBXO32 protein, human SKP Cullin F-Box Protein Ligases TRIM63 protein, human Ubiquitin-Protein Ligases Protein Kinases MTOR protein, human GSK3B protein, human Glycogen Synthase Kinase 3 beta Proto-Oncogene Proteins c-akt Ribosomal Protein S6 Kinases, 70-kDa TOR Serine-Threonine Kinases Glycogen Synthase Kinase 3
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Léger Bertrand
School of Exercise and Nutrition Sciences, Deakin University, 221 Burwood Highway 3125, Australia.
Cartoni Romain
Praz Manu
Lamon Séverine
Dériaz Olivier
Crettenand Antoinette
Gobelet Charles
Rohmer Paul
Konzelmann Michel
Luthi François
Russell Aaron P
References (52)
52 references, click to expand
  1. Cellular survival: a play in three Akts.
    Genes Dev. 1999 Nov 15;13(22):2905-27 PMID: 10579998
  2. Skeletal muscle fiber area alterations in two opposing modes of resistance-exercise training in the same individual.
    Eur J Appl Physiol Occup Physiol. 1990;61(1-2):37-41 PMID: 2149702
  3. Control of the translational regulators PHAS-I and PHAS-II by insulin and cAMP in 3T3-L1 adipocytes.
    J Biol Chem. 1996 Nov 22;271(47):30199-204 PMID: 8939971
  4. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway.
    N Engl J Med. 1996 Dec 19;335(25):1897-905 PMID: 8948566
  5. Activation of translation initiation factor eIF2B by insulin requires phosphatidyl inositol 3-kinase.
    FEBS Lett. 1997 Jun 30;410(2-3):418-22 PMID: 9237674
  6. Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients.
    Am J Physiol. 1997 Sep;273(3 Pt 2):R1072-9 PMID: 9321888
  7. Muscle atrophy is prevented in patients with acute spinal cord injury using functional electrical stimulation.
    Spinal Cord. 1998 Jul;36(7):463-9 PMID: 9670381
  8. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states.
    J Nutr. 1999 Jan;129(1S Suppl):227S-237S PMID: 9915905
  9. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor.
    Cell. 1999 Mar 19;96(6):857-68 PMID: 10102273
  10. Glycogen synthase kinase-3 is the predominant insulin-regulated eukaryotic initiation factor 2B kinase in skeletal muscle.
    Int J Biochem Cell Biol. 1999 Jan;31(1):191-200 PMID: 10216953
  11. Translational homeostasis: eukaryotic translation initiation factor 4E control of 4E-binding protein 1 and p70 S6 kinase activities.
    Mol Cell Biol. 1999 Jun;19(6):4302-10 PMID: 10330171
  12. Signal transduction pathways that regulate eukaryotic protein synthesis.
    J Biol Chem. 1999 Oct 22;274(43):30337-40 PMID: 10521405
  13. Resistance training in the early postoperative phase reduces hospitalization and leads to muscle hypertrophy in elderly hip surgery patients--a controlled, randomized study.
    J Am Geriatr Soc. 2004 Dec;52(12):2016-22 PMID: 15571536
  14. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway.
    J Biol Chem. 2005 Jan 28;280(4):2737-44 PMID: 15550386
  15. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle.
    FASEB J. 2005 Mar;19(3):362-70 PMID: 15746179
  16. Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation.
    FASEB J. 2005 May;19(7):786-8 PMID: 15716393
  17. Response of the ubiquitin-proteasome pathway to changes in muscle activity.
    Am J Physiol Regul Integr Comp Physiol. 2005 Jun;288(6):R1423-31 PMID: 15886351
  18. The ubiquitin-proteasome pathway as a therapeutic target for muscle wasting.
    J Support Oncol. 2005 May-Jun;3(3):209-17 PMID: 15915823
  19. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise.
    J Physiol. 2005 Aug 15;567(Pt 1):349-58 PMID: 15961417
  20. Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise.
    J Physiol. 2005 Sep 15;567(Pt 3):1021-33 PMID: 16002437
  21. Human skeletal muscle atrophy in amyotrophic lateral sclerosis reveals a reduction in Akt and an increase in atrogin-1.
    FASEB J. 2006 Mar;20(3):583-5 PMID: 16507768
  22. Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans.
    FASEB J. 2001 Feb;15(2):475-82 PMID: 11156963
  23. Force/velocity and power/velocity relationships in squat exercise.
    Eur J Appl Physiol. 2001 Mar;84(3):227-32 PMID: 11320640
  24. Therapies for improving muscle function in neuromuscular disorders.
    Exerc Sport Sci Rev. 2001 Oct;29(4):141-8 PMID: 11688785
  25. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways.
    Nat Cell Biol. 2001 Nov;3(11):1009-13 PMID: 11715022
  26. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo.
    Nat Cell Biol. 2001 Nov;3(11):1014-9 PMID: 11715023
  27. Identification of ubiquitin ligases required for skeletal muscle atrophy.
    Science. 2001 Nov 23;294(5547):1704-8 PMID: 11679633
  28. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14440-5 PMID: 11717410
  29. The phosphatidylinositol 3-Kinase AKT pathway in human cancer.
    Nat Rev Cancer. 2002 Jul;2(7):489-501 PMID: 12094235
  30. A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification.
    Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9213-8 PMID: 12084817
  31. A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR.
    Cancer Cell. 2002 Jul;2(1):81-91 PMID: 12150827
  32. Muscular adaptations in response to three different resistance-training regimens: specificity of repetition maximum training zones.
    Eur J Appl Physiol. 2002 Nov;88(1-2):50-60 PMID: 12436270
  33. Combined endurance/resistance training reduces plasma TNF-alpha receptor levels in patients with chronic heart failure and coronary artery disease.
    Eur Heart J. 2002 Dec;23(23):1854-60 PMID: 12445534
  34. Effects of exercise on canine skeletal muscle proteolysis: an investigation of the ubiquitin-proteasome pathway and other metabolic markers.
    Vet Ther. 2002 Fall;3(3):215-25 PMID: 12447828
  35. Exercise treatment to counteract protein wasting of chronic diseases.
    Curr Opin Clin Nutr Metab Care. 2003 Jan;6(1):87-93 PMID: 12496685
  36. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy.
    Nat Cell Biol. 2003 Feb;5(2):87-90 PMID: 12563267
  37. Mitogen-activated protein kinase (MAPK) pathway activation: effects of age and acute exercise on human skeletal muscle.
    J Physiol. 2003 Mar 15;547(Pt 3):977-87 PMID: 12562918
  38. Decisions on life and death: FOXO Forkhead transcription factors are in command when PKB/Akt is off duty.
    J Leukoc Biol. 2003 Jun;73(6):689-701 PMID: 12773501
  39. Lipid peroxidation in skeletal muscle of obese as compared to endurance-trained humans: a case of good vs. bad lipids?
    FEBS Lett. 2003 Sep 11;551(1-3):104-6 PMID: 12965212
  40. 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. 2003 Dec;52(12):2874-81 PMID: 14633846
  41. Constitutive activation of MAPK cascade in acute quadriplegic myopathy.
    Ann Neurol. 2004 Feb;55(2):195-206 PMID: 14755723
  42. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy.
    Cell. 2004 Apr 30;117(3):399-412 PMID: 15109499
  43. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors.
    Mol Cell. 2004 May 7;14(3):395-403 PMID: 15125842
  44. Regulation of muscle protein degradation: coordinated control of apoptotic and ubiquitin-proteasome systems by phosphatidylinositol 3 kinase.
    J Am Soc Nephrol. 2004 Jun;15(6):1537-45 PMID: 15153564
  45. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass.
    FASEB J. 2004 Jun;18(9):1025-7 PMID: 15084522
  46. Mechanical stimuli regulate rapamycin-sensitive signalling by a phosphoinositide 3-kinase-, protein kinase B- and growth factor-independent mechanism.
    Biochem J. 2004 Jun 15;380(Pt 3):795-804 PMID: 15030312
  47. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise.
    Am J Physiol Endocrinol Metab. 2004 Jul;287(1):E1-7 PMID: 14998784
  48. The role of resistance exercise intensity on muscle fibre adaptations.
    Sports Med. 2004;34(10):663-79 PMID: 15335243
  49. Myosin isoform expression and MAFbx mRNA levels in hibernating golden-mantled ground squirrels (Spermophilus lateralis).
    Physiol Biochem Zool. 2004 Jul-Aug;77(4):582-93 PMID: 15449229
  50. Effects of three resistance training programs on muscular strength and absolute and relative endurance.
    Res Q Exerc Sport. 1982 Mar;53(1):1-7 PMID: 7079558
  51. Electromyographic changes during strength training and detraining.
    Med Sci Sports Exerc. 1983;15(6):455-60 PMID: 6656553
  52. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11477-81 PMID: 7972087
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2006-11-01
Epub
2006-00-17
Pages
923-33
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1890416
Subset
IM
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