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
-
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
-
Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase.
Science. 2004 Mar 26;303(5666):2011-5
PMID: 14976264
-
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
-
Sequential changes in the signal transduction responses of skeletal muscle following food deprivation.
FASEB J. 2006 Dec;20(14):2579-81
PMID: 17065218
-
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
-
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
-
Skeletal muscle NAMPT is induced by exercise in humans.
Am J Physiol Endocrinol Metab. 2010 Jan;298(1):E117-26
PMID: 19887595
-
Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1.
Nature. 2005 Mar 3;434(7029):113-8
PMID: 15744310
-
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
-
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
-
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
-
AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol.
Diabetes. 2010 Mar;59(3):554-63
PMID: 19934007
-
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
-
Fuel selection in human skeletal muscle in insulin resistance: a reexamination.
Diabetes. 2000 May;49(5):677-83
PMID: 10905472
-
Hormone-fuel interrelationships during fasting.
J Clin Invest. 1966 Nov;45(11):1751-69
PMID: 5926444
-
Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation.
Nature. 2006 Jan 26;439(7075):484-9
PMID: 16400329
-
Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism.
Endocr Rev. 2006 Dec;27(7):728-35
PMID: 17018837
-
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
-
AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity.
Nature. 2009 Apr 23;458(7241):1056-60
PMID: 19262508
-
The role of FoxO in the regulation of metabolism.
Oncogene. 2008 Apr 7;27(16):2320-36
PMID: 18391974
-
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
-
5'-AMP-activated protein kinase regulates skeletal muscle glycogen content and ergogenics.
FASEB J. 2005 May;19(7):773-9
PMID: 15857891
-
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
-
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
-
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
-
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
-
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
-
Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle.
FASEB J. 2005 Jul;19(9):1146-8
PMID: 15878932
-
AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy.
Nat Rev Mol Cell Biol. 2007 Oct;8(10):774-85
PMID: 17712357
-
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
-
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