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PMID: 20197054 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle.

Cell metabolism ·Vol. 11 ·No. 3 ·2010-03-03 ·Pages 213-9

Cantó C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, Lagouge M, Zierath JR, Auwerx J

Abstract

During fasting and after exercise, skeletal muscle efficiently switches from carbohydrate to lipid as the main energy source to preserve glycogen stores and blood glucose levels for glucose-dependent tissues. Skeletal muscle cells sense this limitation in glucose availability and transform this information into transcriptional and metabolic adaptations. Here we demonstrate that AMPK acts as the prime initial sensor that translates this information into SIRT1-dependent deacetylation of the transcriptional regulators PGC-1alpha and FOXO1, culminating in the transcriptional modulation of mitochondrial and lipid utilization genes. Deficient AMPK activity compromises SIRT1-dependent responses to exercise and fasting, resulting in impaired PGC-1alpha deacetylation and blunted induction of mitochondrial gene expression. Thus, we conclude that AMPK acts as the primordial trigger for fasting- and exercise-induced adaptations in skeletal muscle and that activation of SIRT1 and its downstream signaling pathways are improperly triggered in AMPK-deficient states.

MeSH Terms
AMP-Activated Protein Kinases/genetics,metabolism Animals Cells, Cultured Energy Metabolism Fasting/metabolism Forkhead Box Protein O1 Forkhead Transcription Factors/genetics,metabolism Genes, Mitochondrial/genetics Glucose/metabolism Lipids/genetics Male Mice Mice, Inbred C57BL Mice, Knockout Muscle, Skeletal/metabolism Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha Physical Conditioning, Animal/physiology Signal Transduction Sirtuin 1/genetics,metabolism Trans-Activators/genetics,metabolism Transcription Factors Up-Regulation/genetics
Chemicals
Forkhead Box Protein O1 Forkhead Transcription Factors Foxo1 protein, mouse Lipids Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha Ppargc1a protein, mouse Trans-Activators Transcription Factors AMPK alpha1 subunit, mouse Prkag3 protein, mouse AMP-Activated Protein Kinases Sirt1 protein, mouse Sirtuin 1 Glucose
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Cantó Carles
Ecole Polytechnique Fédérale de Lausanne, Switzerland.
Jiang Lake Q
Deshmukh Atul S
Mataki Chikage
Coste Agnes
Lagouge Marie
Zierath Juleen R
Auwerx Johan
References (31)
31 references, click to expand
  1. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt.
    Dev Cell. 2008 May;14(5):661-73 PMID: 18477450
  2. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase.
    Science. 2004 Mar 26;303(5666):2011-5 PMID: 14976264
  3. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):15983-7 PMID: 12444247
  4. Sequential changes in the signal transduction responses of skeletal muscle following food deprivation.
    FASEB J. 2006 Dec;20(14):2579-81 PMID: 17065218
  5. Selective suppression of AMP-activated protein kinase in skeletal muscle: update on 'lazy mice'.
    Biochem Soc Trans. 2003 Feb;31(Pt 1):236-41 PMID: 12546693
  6. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress.
    Cell Metab. 2007 Oct;6(4):280-93 PMID: 17908557
  7. Skeletal muscle NAMPT is induced by exercise in humans.
    Am J Physiol Endocrinol Metab. 2010 Jan;298(1):E117-26 PMID: 19887595
  8. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1.
    Nature. 2005 Mar 3;434(7029):113-8 PMID: 15744310
  9. The 5'-AMP-activated protein kinase gamma3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle.
    J Biol Chem. 2004 Sep 10;279(37):38441-7 PMID: 15247217
  10. PGC-1alpha is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle.
    Am J Physiol Endocrinol Metab. 2008 Feb;294(2):E463-74 PMID: 18073319
  11. Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase.
    Mol Cell Biol. 2000 Sep;20(18):6704-11 PMID: 10958668
  12. AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol.
    Diabetes. 2010 Mar;59(3):554-63 PMID: 19934007
  13. AMP-activated protein kinase in contraction regulation of skeletal muscle metabolism: necessary and/or sufficient?
    Acta Physiol (Oxf). 2009 May;196(1):155-74 PMID: 19243572
  14. Fuel selection in human skeletal muscle in insulin resistance: a reexamination.
    Diabetes. 2000 May;49(5):677-83 PMID: 10905472
  15. Hormone-fuel interrelationships during fasting.
    J Clin Invest. 1966 Nov;45(11):1751-69 PMID: 5926444
  16. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation.
    Nature. 2006 Jan 26;439(7075):484-9 PMID: 16400329
  17. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism.
    Endocr Rev. 2006 Dec;27(7):728-35 PMID: 17018837
  18. Expression profiling of the gamma-subunit isoforms of AMP-activated protein kinase suggests a major role for gamma3 in white skeletal muscle.
    Am J Physiol Endocrinol Metab. 2004 Feb;286(2):E194-200 PMID: 14559719
  19. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity.
    Nature. 2009 Apr 23;458(7241):1056-60 PMID: 19262508
  20. The role of FoxO in the regulation of metabolism.
    Oncogene. 2008 Apr 7;27(16):2320-36 PMID: 18391974
  21. Role of AMP-activated protein kinase in the coordinated expression of genes controlling glucose and lipid metabolism in mouse white skeletal muscle.
    Diabetologia. 2005 Nov;48(11):2354-64 PMID: 16237515
  22. 5'-AMP-activated protein kinase regulates skeletal muscle glycogen content and ergogenics.
    FASEB J. 2005 May;19(7):773-9 PMID: 15857891
  23. Changes in exercise-induced gene expression in 5'-AMP-activated protein kinase gamma3-null and gamma3 R225Q transgenic mice.
    Diabetes. 2005 Dec;54(12):3484-9 PMID: 16306365
  24. Role of AMP-activated protein kinase in exercise capacity, whole body glucose homeostasis, and glucose transport in skeletal muscle -insight from analysis of a transgenic mouse model-.
    Diabetes Res Clin Pract. 2007 Sep;77 Suppl 1:S92-8 PMID: 17452058
  25. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha.
    EMBO J. 2007 Apr 4;26(7):1913-23 PMID: 17347648
  26. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system.
    Hum Mol Genet. 2005 Jun 1;14(11):1405-15 PMID: 15829499
  27. The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans.
    Genes Dev. 2004 Dec 15;18(24):3004-9 PMID: 15574588
  28. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle.
    FASEB J. 2005 Jul;19(9):1146-8 PMID: 15878932
  29. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy.
    Nat Rev Mol Cell Biol. 2007 Oct;8(10):774-85 PMID: 17712357
  30. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle.
    Mol Cell. 2001 May;7(5):1085-94 PMID: 11389854
  31. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha.
    Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12017-22 PMID: 17609368
Article Info
Journal
Cell metabolism
Abbr.
Cell Metab
ISSN
1932-7420
Published
2010-03-03
Pages
213-9
Language
English
Region
United States
NLM ID
101233170
PMCID
PMC3616265
Subset
IM
Grants
European Research Council · 231138 · International
NIDDK NIH HHS · P01 DK059820 · United States
NIDDK NIH HHS · DK59820 · United States
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