Skip to main content
Top
Published in: Current Heart Failure Reports 3/2012

01-09-2012 | Investigative Therapies (J.-L. Balligand, Section editor)

AMP-activated Protein Kinase in the Control of Cardiac Metabolism and Remodeling

Authors: Sandrine Horman, Christophe Beauloye, Jean-Louis Vanoverschelde, Luc Bertrand

Published in: Current Heart Failure Reports | Issue 3/2012

Login to get access

Abstract

The AMP-activated protein kinase (AMPK) can be firstly considered as a cellular fuel gauge. AMPK rapidly senses energy deprivation and orchestrates a metabolic response to maintain an acceptable energy level required for cell survival under such adverse condition. Its protective role during myocardial ischemia has been deeply documented. More recently, it has been shown that the role of AMPK extends to several nonmetabolic effects related to other cardiac pathologies comprising diabetic cardiomyopathy, cardiac hypertrophy, and heart failure. Here, we briefly review the different roles played by AMPK in the control of cardiac metabolism and function under normal and pathological conditions. The potential cardioprotective actions of AMPK and the relative importance of its energetic and nonmetabolic effects in these mechanisms are deeply discussed.
Literature
1.
go back to reference Viollet B, Athea Y, Mounier R, et al. AMPK: Lessons from transgenic and knockout animals. Front Biosci. 2009;14:19–44.PubMedCrossRef Viollet B, Athea Y, Mounier R, et al. AMPK: Lessons from transgenic and knockout animals. Front Biosci. 2009;14:19–44.PubMedCrossRef
2.
go back to reference Sakamoto K, Zarrinpashneh E, Budas GR, et al. Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPKalpha2 but not AMPKalpha1. Am J Physiol Endocrinol Metab. 2006;290:E780–8.PubMedCrossRef Sakamoto K, Zarrinpashneh E, Budas GR, et al. Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPKalpha2 but not AMPKalpha1. Am J Physiol Endocrinol Metab. 2006;290:E780–8.PubMedCrossRef
3.
go back to reference Woods A, Dickerson K, Heath R, et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2005;2:21–33.PubMedCrossRef Woods A, Dickerson K, Heath R, et al. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2005;2:21–33.PubMedCrossRef
4.
go back to reference Hawley SA, Pan DA, Mustard KJ, et al. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005;2:9–19.PubMedCrossRef Hawley SA, Pan DA, Mustard KJ, et al. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2005;2:9–19.PubMedCrossRef
5.
go back to reference Beauloye C, Bertrand L, Horman S, et al. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc Res. 2011;90:224–33.PubMedCrossRef Beauloye C, Bertrand L, Horman S, et al. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc Res. 2011;90:224–33.PubMedCrossRef
7.
go back to reference Bertrand L, Horman S, Beauloye C, et al. Insulin signalling in the heart. Cardiovasc Res. 2008;79:238–48.PubMedCrossRef Bertrand L, Horman S, Beauloye C, et al. Insulin signalling in the heart. Cardiovasc Res. 2008;79:238–48.PubMedCrossRef
8.
go back to reference Treebak JT, Glund S, Deshmukh A, et al. AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes. 2006;55:2051–8.PubMedCrossRef Treebak JT, Glund S, Deshmukh A, et al. AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes. 2006;55:2051–8.PubMedCrossRef
9.
go back to reference Kramer HF, Witczak CA, Fujii N, et al. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes. 2006;55:2067–76.PubMedCrossRef Kramer HF, Witczak CA, Fujii N, et al. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes. 2006;55:2067–76.PubMedCrossRef
10.
go back to reference Marsin AS, Bertrand L, Rider MH, et al. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol. 2000;10:1247–55.PubMedCrossRef Marsin AS, Bertrand L, Rider MH, et al. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol. 2000;10:1247–55.PubMedCrossRef
11.
go back to reference Kudo N, Gillespie JG, Kung L, et al. Characterization of 5′AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim Biophys Acta. 1996;1301:67–75.PubMedCrossRef Kudo N, Gillespie JG, Kung L, et al. Characterization of 5′AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim Biophys Acta. 1996;1301:67–75.PubMedCrossRef
12.
go back to reference Dyck JR, Lopaschuk GD. AMPK alterations in cardiac physiology and pathology: enemy or ally? J Physiol. 2006;574:95–112.PubMedCrossRef Dyck JR, Lopaschuk GD. AMPK alterations in cardiac physiology and pathology: enemy or ally? J Physiol. 2006;574:95–112.PubMedCrossRef
13.
go back to reference Zarrinpashneh E, Carjaval K, Beauloye C, et al. Role of the alpha2-isoform of AMP-activated protein kinase in the metabolic response of the heart to no-flow ischemia. Am J Physiol Heart Circ Physiol. 2006;291:H2875–83.PubMedCrossRef Zarrinpashneh E, Carjaval K, Beauloye C, et al. Role of the alpha2-isoform of AMP-activated protein kinase in the metabolic response of the heart to no-flow ischemia. Am J Physiol Heart Circ Physiol. 2006;291:H2875–83.PubMedCrossRef
14.
go back to reference Carvajal K, Zarrinpashneh E, Szarszoi O, et al. Dual cardiac contractile effects of the alpha2-AMPK deletion in low-flow ischemia and reperfusion. Am J Physiol Heart Circ Physiol. 2007;292:H3136–47.PubMedCrossRef Carvajal K, Zarrinpashneh E, Szarszoi O, et al. Dual cardiac contractile effects of the alpha2-AMPK deletion in low-flow ischemia and reperfusion. Am J Physiol Heart Circ Physiol. 2007;292:H3136–47.PubMedCrossRef
15.
go back to reference Russell 3rd RR, Li J, Coven DL, et al. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest. 2004;114:495–503.PubMed Russell 3rd RR, Li J, Coven DL, et al. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest. 2004;114:495–503.PubMed
16.
go back to reference •• Gundewar S, Calvert JW, Jha S, et al. Activation of AMP-activated protein kinase by metformin improves left ventricular function and survival in heart failure. Circ Res. 2009;104:403–11. This study demonstrates that low-dose metformin significantly improves left ventricular function and survival via activation of AMPK and its downstream mediators, eNOS and PGC-1alpha, in a model of heart failure. They used an AMPK dominant-negative mouse model to prove the implication of AMPK.PubMedCrossRef •• Gundewar S, Calvert JW, Jha S, et al. Activation of AMP-activated protein kinase by metformin improves left ventricular function and survival in heart failure. Circ Res. 2009;104:403–11. This study demonstrates that low-dose metformin significantly improves left ventricular function and survival via activation of AMPK and its downstream mediators, eNOS and PGC-1alpha, in a model of heart failure. They used an AMPK dominant-negative mouse model to prove the implication of AMPK.PubMedCrossRef
17.
go back to reference • Kim AS, Miller EJ, Wright TM, et al. A small molecule AMPK activator protects the heart against ischemia-reperfusion injury. J Mol Cell Cardiol. 2011;51:24–32. The authors were the first to show that treatment with a direct AMPK-activating molecule, the A-769662, is an effective strategy to protect the heart against ischemia–reperfusion injury. They used an AMPK dominant-negative mouse model to prove the implication of AMPK.PubMedCrossRef • Kim AS, Miller EJ, Wright TM, et al. A small molecule AMPK activator protects the heart against ischemia-reperfusion injury. J Mol Cell Cardiol. 2011;51:24–32. The authors were the first to show that treatment with a direct AMPK-activating molecule, the A-769662, is an effective strategy to protect the heart against ischemia–reperfusion injury. They used an AMPK dominant-negative mouse model to prove the implication of AMPK.PubMedCrossRef
18.
go back to reference Calvert JW, Gundewar S, Jha S, et al. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes. 2008;57:696–705.PubMedCrossRef Calvert JW, Gundewar S, Jha S, et al. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes. 2008;57:696–705.PubMedCrossRef
19.
go back to reference Xing Y, Musi N, Fujii N, et al. Glucose metabolism and energy homeostasis in mouse hearts overexpressing dominant negative alpha2 subunit of AMP-activated protein kinase. J Biol Chem. 2003;278:28372–7.PubMedCrossRef Xing Y, Musi N, Fujii N, et al. Glucose metabolism and energy homeostasis in mouse hearts overexpressing dominant negative alpha2 subunit of AMP-activated protein kinase. J Biol Chem. 2003;278:28372–7.PubMedCrossRef
20.
go back to reference Boudina S, Abel ED. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord. 2010;11:31–9.PubMedCrossRef Boudina S, Abel ED. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord. 2010;11:31–9.PubMedCrossRef
21.
go back to reference Zhou G, Myers R, Li Y, et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest. 2001;108:1167–74.PubMed Zhou G, Myers R, Li Y, et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest. 2001;108:1167–74.PubMed
22.
go back to reference Bertrand L, Ginion A, Beauloye C, et al. AMPK activation restores the stimulation of glucose uptake in an in vitro model of insulin-resistant cardiomyocytes via the activation of protein kinase B. Am J Physiol Heart Circ Physiol. 2006;291:H239–50.PubMedCrossRef Bertrand L, Ginion A, Beauloye C, et al. AMPK activation restores the stimulation of glucose uptake in an in vitro model of insulin-resistant cardiomyocytes via the activation of protein kinase B. Am J Physiol Heart Circ Physiol. 2006;291:H239–50.PubMedCrossRef
23.
go back to reference • Ginion A, Auquier J, Benton CR, et al. Inhibition of the mTOR/p70S6K pathway is not involved in the insulin-sensitizing effect of AMPK on cardiac glucose uptake. Am J Physiol Heart Circ Physiol. 2011;301:H469–77. In contrast to a commonly accepted notion, the authors showed that the insulin-sensitizing effect of AMPK on insulin-mediated glucose uptake is not due to the AMPK-induced inhibition of the mTOR/p70S6K-dependent negative feedback loop.PubMedCrossRef • Ginion A, Auquier J, Benton CR, et al. Inhibition of the mTOR/p70S6K pathway is not involved in the insulin-sensitizing effect of AMPK on cardiac glucose uptake. Am J Physiol Heart Circ Physiol. 2011;301:H469–77. In contrast to a commonly accepted notion, the authors showed that the insulin-sensitizing effect of AMPK on insulin-mediated glucose uptake is not due to the AMPK-induced inhibition of the mTOR/p70S6K-dependent negative feedback loop.PubMedCrossRef
24.
go back to reference Longnus SL, Segalen C, Giudicelli J, et al. Insulin signalling downstream of protein kinase B is potentiated by 5′AMP-activated protein kinase in rat hearts in vivo. Diabetologia. 2005;48:2591–601.PubMedCrossRef Longnus SL, Segalen C, Giudicelli J, et al. Insulin signalling downstream of protein kinase B is potentiated by 5′AMP-activated protein kinase in rat hearts in vivo. Diabetologia. 2005;48:2591–601.PubMedCrossRef
25.
go back to reference Yang J, Holman GD. Long-term metformin treatment stimulates cardiomyocyte glucose transport through an AMP-activated protein kinase-dependent reduction in GLUT4 endocytosis. Endocrinology. 2006;147:2728–36.PubMedCrossRef Yang J, Holman GD. Long-term metformin treatment stimulates cardiomyocyte glucose transport through an AMP-activated protein kinase-dependent reduction in GLUT4 endocytosis. Endocrinology. 2006;147:2728–36.PubMedCrossRef
26.
go back to reference Tremblay F, Marette A. Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J Biol Chem. 2001;276:38052–60.PubMed Tremblay F, Marette A. Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J Biol Chem. 2001;276:38052–60.PubMed
27.
go back to reference Boura-Halfon S, Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab. 2009;296:E581–91.PubMedCrossRef Boura-Halfon S, Zick Y. Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab. 2009;296:E581–91.PubMedCrossRef
28.
go back to reference Habegger KM, Hoffman NJ, Ridenour CM, et al. AMPK enhances insulin-stimulated GLUT4 regulation via lowering membrane cholesterol. Endocrinology. 2012;153:2130–41.PubMedCrossRef Habegger KM, Hoffman NJ, Ridenour CM, et al. AMPK enhances insulin-stimulated GLUT4 regulation via lowering membrane cholesterol. Endocrinology. 2012;153:2130–41.PubMedCrossRef
29.
go back to reference Xie Z, He C, Zou MH. AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy. 2011;7:1254–5.PubMedCrossRef Xie Z, He C, Zou MH. AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy. 2011;7:1254–5.PubMedCrossRef
30.
go back to reference Matsumoto T, Noguchi E, Ishida K, et al. Metformin normalizes endothelial function by suppressing vasoconstrictor prostanoids in mesenteric arteries from OLETF rats, a model of type 2 diabetes. Am J Physiol Heart Circ Physiol. 2008;295:H1165–76.PubMedCrossRef Matsumoto T, Noguchi E, Ishida K, et al. Metformin normalizes endothelial function by suppressing vasoconstrictor prostanoids in mesenteric arteries from OLETF rats, a model of type 2 diabetes. Am J Physiol Heart Circ Physiol. 2008;295:H1165–76.PubMedCrossRef
31.
go back to reference Wang Y, Huang Y, Lam KS, et al. Berberine prevents hyperglycemia-induced endothelial injury and enhances vasodilatation via adenosine monophosphate-activated protein kinase and endothelial nitric oxide synthase. Cardiovasc Res. 2009;82:484–92.PubMedCrossRef Wang Y, Huang Y, Lam KS, et al. Berberine prevents hyperglycemia-induced endothelial injury and enhances vasodilatation via adenosine monophosphate-activated protein kinase and endothelial nitric oxide synthase. Cardiovasc Res. 2009;82:484–92.PubMedCrossRef
32.
go back to reference Paiva MA, Rutter-Locher Z, Goncalves LM, et al. Enhancing AMPK activation during ischemia protects the diabetic heart against reperfusion injury. Am J Physiol Heart Circ Physiol. 2011;300:H2123–34.PubMedCrossRef Paiva MA, Rutter-Locher Z, Goncalves LM, et al. Enhancing AMPK activation during ischemia protects the diabetic heart against reperfusion injury. Am J Physiol Heart Circ Physiol. 2011;300:H2123–34.PubMedCrossRef
33.
go back to reference Krause U, Bertrand L, Hue L. Control of p70 ribosomal protein S6 kinase and acetyl-CoA carboxylase by AMP-activated protein kinase and protein phosphatases in isolated hepatocytes. Eur J Biochem. 2002;269:3751–9.PubMedCrossRef Krause U, Bertrand L, Hue L. Control of p70 ribosomal protein S6 kinase and acetyl-CoA carboxylase by AMP-activated protein kinase and protein phosphatases in isolated hepatocytes. Eur J Biochem. 2002;269:3751–9.PubMedCrossRef
34.
go back to reference Horman S, Browne G, Krause U, et al. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol. 2002;12:1419–23.PubMedCrossRef Horman S, Browne G, Krause U, et al. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol. 2002;12:1419–23.PubMedCrossRef
35.
go back to reference Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003;115:577–90.PubMedCrossRef Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003;115:577–90.PubMedCrossRef
36.
go back to reference Gwinn DM, Shackelford DB, Egan DF, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214–26.PubMedCrossRef Gwinn DM, Shackelford DB, Egan DF, et al. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214–26.PubMedCrossRef
37.
go back to reference Browne GJ, Finn SG, Proud CG. Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem. 2004;279:12220–31.PubMedCrossRef Browne GJ, Finn SG, Proud CG. Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem. 2004;279:12220–31.PubMedCrossRef
38.
go back to reference Horman S, Beauloye C, Vertommen D, et al. Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J Biol Chem. 2003;278:41970–6.PubMedCrossRef Horman S, Beauloye C, Vertommen D, et al. Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J Biol Chem. 2003;278:41970–6.PubMedCrossRef
39.
go back to reference Crozier SJ, Vary TC, Kimball SR, et al. Cellular energy status modulates translational control mechanisms in ischemic-reperfused rat hearts. Am J Physiol Heart Circ Physiol. 2005;289:H1242–50.PubMedCrossRef Crozier SJ, Vary TC, Kimball SR, et al. Cellular energy status modulates translational control mechanisms in ischemic-reperfused rat hearts. Am J Physiol Heart Circ Physiol. 2005;289:H1242–50.PubMedCrossRef
40.
go back to reference Chan AY, Soltys CL, Young ME, et al. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J Biol Chem. 2004;279:32771–9.PubMedCrossRef Chan AY, Soltys CL, Young ME, et al. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J Biol Chem. 2004;279:32771–9.PubMedCrossRef
41.
go back to reference Chan AY, Dolinsky VW, Soltys CL, et al. Resveratrol inhibits cardiac hypertrophy via AMP-activated protein kinase and Akt. J Biol Chem. 2008;283:24194–201.PubMedCrossRef Chan AY, Dolinsky VW, Soltys CL, et al. Resveratrol inhibits cardiac hypertrophy via AMP-activated protein kinase and Akt. J Biol Chem. 2008;283:24194–201.PubMedCrossRef
42.
go back to reference • Dolinsky VW, Morton JS, Oka T, et al. Calorie restriction prevents hypertension and cardiac hypertrophy in the spontaneously hypertensive rat. Hypertension. 2010;56:412–21. The authors showed that short-term calorie restriction exerts beneficial effects in hypertensive rats via stimulation of an adiponectin/AMPK/eNOS signaling axis. PubMedCrossRef • Dolinsky VW, Morton JS, Oka T, et al. Calorie restriction prevents hypertension and cardiac hypertrophy in the spontaneously hypertensive rat. Hypertension. 2010;56:412–21. The authors showed that short-term calorie restriction exerts beneficial effects in hypertensive rats via stimulation of an adiponectin/AMPK/eNOS signaling axis. PubMedCrossRef
43.
go back to reference Zarrinpashneh E, Beauloye C, Ginion A, et al. AMPKalpha2 counteracts the development of cardiac hypertrophy induced by isoproterenol. Biochem Biophys Res Commun. 2008;376:677–81.PubMedCrossRef Zarrinpashneh E, Beauloye C, Ginion A, et al. AMPKalpha2 counteracts the development of cardiac hypertrophy induced by isoproterenol. Biochem Biophys Res Commun. 2008;376:677–81.PubMedCrossRef
44.
go back to reference Zhang P, Hu X, Xu X, et al. AMP activated protein kinase-alpha2 deficiency exacerbates pressure-overload-induced left ventricular hypertrophy and dysfunction in mice. Hypertension. 2008;52:918–24.PubMedCrossRef Zhang P, Hu X, Xu X, et al. AMP activated protein kinase-alpha2 deficiency exacerbates pressure-overload-induced left ventricular hypertrophy and dysfunction in mice. Hypertension. 2008;52:918–24.PubMedCrossRef
45.
go back to reference • Shimano M, Ouchi N, Shibata R, et al. Adiponectin deficiency exacerbates cardiac dysfunction following pressure overload through disruption of an AMPK-dependent angiogenic response. J Mol Cell Cardiol. 2010;49:210–20. The authors showed that adiponectin deficiency accelerates the transition from cardiac hypertrophy to heart failure during pressure overload through disruption of AMPK-dependent angiogenic regulatory axis.PubMedCrossRef • Shimano M, Ouchi N, Shibata R, et al. Adiponectin deficiency exacerbates cardiac dysfunction following pressure overload through disruption of an AMPK-dependent angiogenic response. J Mol Cell Cardiol. 2010;49:210–20. The authors showed that adiponectin deficiency accelerates the transition from cardiac hypertrophy to heart failure during pressure overload through disruption of AMPK-dependent angiogenic regulatory axis.PubMedCrossRef
46.
go back to reference Ikeda Y, Sato K, Pimentel DR, et al. Cardiac-specific deletion of LKB1 leads to hypertrophy and dysfunction. J Biol Chem. 2009;284:35839–49.PubMedCrossRef Ikeda Y, Sato K, Pimentel DR, et al. Cardiac-specific deletion of LKB1 leads to hypertrophy and dysfunction. J Biol Chem. 2009;284:35839–49.PubMedCrossRef
47.
go back to reference Meng R, Pei Z, Zhang A, et al. AMPK activation enhances PPARalpha activity to inhibit cardiac hypertrophy via ERK1/2 MAPK signaling pathway. Arch Biochem Biophys. 2011;511:1–7.PubMedCrossRef Meng R, Pei Z, Zhang A, et al. AMPK activation enhances PPARalpha activity to inhibit cardiac hypertrophy via ERK1/2 MAPK signaling pathway. Arch Biochem Biophys. 2011;511:1–7.PubMedCrossRef
48.
go back to reference Li HL, Yin R, Chen D, et al. Long-term activation of adenosine monophosphate-activated protein kinase attenuates pressure-overload-induced cardiac hypertrophy. J Cell Biochem. 2007;100:1086–99.PubMedCrossRef Li HL, Yin R, Chen D, et al. Long-term activation of adenosine monophosphate-activated protein kinase attenuates pressure-overload-induced cardiac hypertrophy. J Cell Biochem. 2007;100:1086–99.PubMedCrossRef
49.
go back to reference Chen BL, Ma YD, Meng RS, et al. Activation of AMPK inhibits cardiomyocyte hypertrophy by modulating of the FOXO1/MuRF1 signaling pathway in vitro. Acta Pharmacol Sin. 2010;31:798–804.PubMedCrossRef Chen BL, Ma YD, Meng RS, et al. Activation of AMPK inhibits cardiomyocyte hypertrophy by modulating of the FOXO1/MuRF1 signaling pathway in vitro. Acta Pharmacol Sin. 2010;31:798–804.PubMedCrossRef
50.
go back to reference Meng RS, Pei ZH, Yin R, et al. Adenosine monophosphate-activated protein kinase inhibits cardiac hypertrophy through reactivating peroxisome proliferator-activated receptor-alpha signaling pathway. Eur J Pharmacol. 2009;620:63–70.PubMedCrossRef Meng RS, Pei ZH, Yin R, et al. Adenosine monophosphate-activated protein kinase inhibits cardiac hypertrophy through reactivating peroxisome proliferator-activated receptor-alpha signaling pathway. Eur J Pharmacol. 2009;620:63–70.PubMedCrossRef
51.
go back to reference Opie LH, Commerford PJ, Gersh BJ, et al. Controversies in ventricular remodelling. Lancet. 2006;367:356–67.PubMedCrossRef Opie LH, Commerford PJ, Gersh BJ, et al. Controversies in ventricular remodelling. Lancet. 2006;367:356–67.PubMedCrossRef
52.
go back to reference Knoll R, Iaccarino G, Tarone G, et al. Towards a re-definition of ‘cardiac hypertrophy’ through a rational characterization of left ventricular phenotypes: a position paper of the Working Group ‘Myocardial Function’ of the ESC. Eur J Heart Fail. 2011;13:811–9.PubMedCrossRef Knoll R, Iaccarino G, Tarone G, et al. Towards a re-definition of ‘cardiac hypertrophy’ through a rational characterization of left ventricular phenotypes: a position paper of the Working Group ‘Myocardial Function’ of the ESC. Eur J Heart Fail. 2011;13:811–9.PubMedCrossRef
53.
go back to reference Frey N, Olson EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol. 2003;65:45–79.PubMedCrossRef Frey N, Olson EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol. 2003;65:45–79.PubMedCrossRef
54.
go back to reference Baudino TA, Carver W, Giles W, et al. Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol. 2006;291:H1015–26.PubMedCrossRef Baudino TA, Carver W, Giles W, et al. Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol. 2006;291:H1015–26.PubMedCrossRef
55.
go back to reference Eckhouse SR, Spinale FG. Changes in the myocardial interstitium and contribution to the progression of heart failure. Heart Fail Clin. 2012;8:7–20.PubMedCrossRef Eckhouse SR, Spinale FG. Changes in the myocardial interstitium and contribution to the progression of heart failure. Heart Fail Clin. 2012;8:7–20.PubMedCrossRef
56.
go back to reference Takeda N, Manabe I, Uchino Y, et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest. 2010;120:254–65.PubMedCrossRef Takeda N, Manabe I, Uchino Y, et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest. 2010;120:254–65.PubMedCrossRef
57.
go back to reference Bishop SP, Powell PC, Hasebe N, et al. Coronary vascular morphology in pressure-overload left ventricular hypertrophy. J Mol Cell Cardiol. 1996;28:141–54.PubMedCrossRef Bishop SP, Powell PC, Hasebe N, et al. Coronary vascular morphology in pressure-overload left ventricular hypertrophy. J Mol Cell Cardiol. 1996;28:141–54.PubMedCrossRef
58.
go back to reference Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev. 2009;89:481–534.PubMedCrossRef Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev. 2009;89:481–534.PubMedCrossRef
59.
go back to reference Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285–342.PubMedCrossRef Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285–342.PubMedCrossRef
60.
go back to reference Banerjee I, Fuseler JW, Price RL, et al. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol. 2007;293:H1883–91.PubMedCrossRef Banerjee I, Fuseler JW, Price RL, et al. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol. 2007;293:H1883–91.PubMedCrossRef
61.
go back to reference Sugihara N, Genda A, Shimizu M, et al. Diastolic dysfunction and its relation to myocardial fibrosis in essential hypertension. J Cardiol. 1988;18:353–61.PubMed Sugihara N, Genda A, Shimizu M, et al. Diastolic dysfunction and its relation to myocardial fibrosis in essential hypertension. J Cardiol. 1988;18:353–61.PubMed
63.
go back to reference Kuwahara K, Saito Y, Harada M, et al. Involvement of cardiotrophin-1 in cardiac myocyte-nonmyocyte interactions during hypertrophy of rat cardiac myocytes in vitro. Circulation. 1999;100:1116–24.PubMedCrossRef Kuwahara K, Saito Y, Harada M, et al. Involvement of cardiotrophin-1 in cardiac myocyte-nonmyocyte interactions during hypertrophy of rat cardiac myocytes in vitro. Circulation. 1999;100:1116–24.PubMedCrossRef
64.
go back to reference Harada M, Itoh H, Nakagawa O, et al. Significance of ventricular myocytes and nonmyocytes interaction during cardiocyte hypertrophy: evidence for endothelin-1 as a paracrine hypertrophic factor from cardiac nonmyocytes. Circulation. 1997;96:3737–44.PubMedCrossRef Harada M, Itoh H, Nakagawa O, et al. Significance of ventricular myocytes and nonmyocytes interaction during cardiocyte hypertrophy: evidence for endothelin-1 as a paracrine hypertrophic factor from cardiac nonmyocytes. Circulation. 1997;96:3737–44.PubMedCrossRef
65.
go back to reference Sano M, Fukuda K, Kodama H, et al. Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J Biol Chem. 2000;275:29717–23.PubMedCrossRef Sano M, Fukuda K, Kodama H, et al. Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J Biol Chem. 2000;275:29717–23.PubMedCrossRef
66.
go back to reference Shiojima I, Sato K, Izumiya Y, et al. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005;115:2108–18.PubMedCrossRef Shiojima I, Sato K, Izumiya Y, et al. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest. 2005;115:2108–18.PubMedCrossRef
67.
go back to reference Kazakov A, Muller P, Jagoda P, et al. Endothelial nitric oxide synthase of the bone marrow regulates myocardial hypertrophy, fibrosis, and angiogenesis. Cardiovasc Res. 2012;93:397–405.PubMedCrossRef Kazakov A, Muller P, Jagoda P, et al. Endothelial nitric oxide synthase of the bone marrow regulates myocardial hypertrophy, fibrosis, and angiogenesis. Cardiovasc Res. 2012;93:397–405.PubMedCrossRef
68.
go back to reference Ventura-Clapier R, Garnier A, Veksler V. Energy metabolism in heart failure. J Physiol. 2004;555:1–13.PubMedCrossRef Ventura-Clapier R, Garnier A, Veksler V. Energy metabolism in heart failure. J Physiol. 2004;555:1–13.PubMedCrossRef
69.
go back to reference Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev. 2005;85:1093–129.PubMedCrossRef Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev. 2005;85:1093–129.PubMedCrossRef
70.
go back to reference Turer AT, Malloy CR, Newgard CB, et al. Energetics and metabolism in the failing heart: important but poorly understood. Curr Opin Clin Nutr Metab Care. 2010;13:458–65.PubMedCrossRef Turer AT, Malloy CR, Newgard CB, et al. Energetics and metabolism in the failing heart: important but poorly understood. Curr Opin Clin Nutr Metab Care. 2010;13:458–65.PubMedCrossRef
71.
go back to reference Ashrafian H, Frenneaux MP, Opie LH. Metabolic mechanisms in heart failure. Circulation. 2007;116:434–48.PubMedCrossRef Ashrafian H, Frenneaux MP, Opie LH. Metabolic mechanisms in heart failure. Circulation. 2007;116:434–48.PubMedCrossRef
72.
go back to reference Beer M, Seyfarth T, Sandstede J, et al. Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with (31)P-SLOOP magnetic resonance spectroscopy. J Am Coll Cardiol. 2002;40:1267–74.PubMedCrossRef Beer M, Seyfarth T, Sandstede J, et al. Absolute concentrations of high-energy phosphate metabolites in normal, hypertrophied, and failing human myocardium measured noninvasively with (31)P-SLOOP magnetic resonance spectroscopy. J Am Coll Cardiol. 2002;40:1267–74.PubMedCrossRef
73.
go back to reference Starling RC, Hammer DF, Altschuld RA. Human myocardial ATP content and in vivo contractile function. Mol Cell Biochem. 1998;180:171–7.PubMedCrossRef Starling RC, Hammer DF, Altschuld RA. Human myocardial ATP content and in vivo contractile function. Mol Cell Biochem. 1998;180:171–7.PubMedCrossRef
74.
75.
go back to reference Hue L, Taegtmeyer H. The Randle cycle revisited: a new head for an old hat. Am J Physiol Endocrinol Metab. 2009;297:E578–91.PubMedCrossRef Hue L, Taegtmeyer H. The Randle cycle revisited: a new head for an old hat. Am J Physiol Endocrinol Metab. 2009;297:E578–91.PubMedCrossRef
76.
go back to reference Lopaschuk GD, Ussher JR, Folmes CD, et al. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90:207–58.PubMedCrossRef Lopaschuk GD, Ussher JR, Folmes CD, et al. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90:207–58.PubMedCrossRef
78.
go back to reference Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res. 2008;79:208–17.PubMedCrossRef Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res. 2008;79:208–17.PubMedCrossRef
79.
go back to reference Arany Z, He H, Lin J, et al. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005;1:259–71.PubMedCrossRef Arany Z, He H, Lin J, et al. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005;1:259–71.PubMedCrossRef
80.
go back to reference Arany Z, Novikov M, Chin S, et al. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci U S A. 2006;103:10086–91.PubMedCrossRef Arany Z, Novikov M, Chin S, et al. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci U S A. 2006;103:10086–91.PubMedCrossRef
81.
go back to reference Leone TC, Lehman JJ, Finck BN, et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005;3:e101.PubMedCrossRef Leone TC, Lehman JJ, Finck BN, et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005;3:e101.PubMedCrossRef
82.
go back to reference Tian R, Musi N, D’Agostino J, et al. Increased adenosine monophosphate-activated protein kinase activity in rat hearts with pressure-overload hypertrophy. Circulation. 2001;104:1664–9.PubMedCrossRef Tian R, Musi N, D’Agostino J, et al. Increased adenosine monophosphate-activated protein kinase activity in rat hearts with pressure-overload hypertrophy. Circulation. 2001;104:1664–9.PubMedCrossRef
83.
go back to reference Jessen N, Koh HJ, Folmes CD, et al. Ablation of LKB1 in the heart leads to energy deprivation and impaired cardiac function. Biochim Biophys Acta. 2010;1802:593–600.PubMedCrossRef Jessen N, Koh HJ, Folmes CD, et al. Ablation of LKB1 in the heart leads to energy deprivation and impaired cardiac function. Biochim Biophys Acta. 2010;1802:593–600.PubMedCrossRef
84.
go back to reference Thomson DM, Hancock CR, Evanson BG, et al. Skeletal muscle dysfunction in muscle-specific LKB1 knockout mice. J Appl Physiol. 2010;108:1775–85.PubMedCrossRef Thomson DM, Hancock CR, Evanson BG, et al. Skeletal muscle dysfunction in muscle-specific LKB1 knockout mice. J Appl Physiol. 2010;108:1775–85.PubMedCrossRef
85.
go back to reference Ahluwalia A. Tarnawski AS: Activation of the metabolic sensor-AMP activated protein kinase reverses impairment of angiogenesis in aging myocardial microvascular endothelial cells. Implications for the aging heart. J Physiol Pharmacol. 2011;62:583–7.PubMed Ahluwalia A. Tarnawski AS: Activation of the metabolic sensor-AMP activated protein kinase reverses impairment of angiogenesis in aging myocardial microvascular endothelial cells. Implications for the aging heart. J Physiol Pharmacol. 2011;62:583–7.PubMed
86.
go back to reference Nagata D, Mogi M, Walsh K. AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem. 2003;278:31000–6.PubMedCrossRef Nagata D, Mogi M, Walsh K. AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem. 2003;278:31000–6.PubMedCrossRef
87.
go back to reference Ohashi K, Ouchi N, Higuchi A, et al. LKB1 deficiency in Tie2-Cre-expressing cells impairs ischemia-induced angiogenesis. J Biol Chem. 2010;285:22291–8.PubMedCrossRef Ohashi K, Ouchi N, Higuchi A, et al. LKB1 deficiency in Tie2-Cre-expressing cells impairs ischemia-induced angiogenesis. J Biol Chem. 2010;285:22291–8.PubMedCrossRef
88.
go back to reference Li J, Hu X, Selvakumar P, et al. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am J Physiol Endocrinol Metab. 2004;287:E834–41.PubMedCrossRef Li J, Hu X, Selvakumar P, et al. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am J Physiol Endocrinol Metab. 2004;287:E834–41.PubMedCrossRef
89.
go back to reference Gschwend S, Henning RH, Pinto YM, et al. Myogenic constriction is increased in mesenteric resistance arteries from rats with chronic heart failure: instantaneous counteraction by acute AT1 receptor blockade. Br J Pharmacol. 2003;139:1317–25.PubMedCrossRef Gschwend S, Henning RH, Pinto YM, et al. Myogenic constriction is increased in mesenteric resistance arteries from rats with chronic heart failure: instantaneous counteraction by acute AT1 receptor blockade. Br J Pharmacol. 2003;139:1317–25.PubMedCrossRef
90.
go back to reference Horman S, Morel N, Vertommen D, et al. AMP-activated protein kinase phosphorylates and desensitizes smooth muscle myosin light chain kinase. J Biol Chem. 2008;283:18505–12.PubMedCrossRef Horman S, Morel N, Vertommen D, et al. AMP-activated protein kinase phosphorylates and desensitizes smooth muscle myosin light chain kinase. J Biol Chem. 2008;283:18505–12.PubMedCrossRef
91.
go back to reference Zannad F, Alla F, Dousset B, et al. Limitation of excessive extracellular matrix turnover may contribute to survival benefit of spironolactone therapy in patients with congestive heart failure: insights from the randomized aldactone evaluation study (RALES). Rales Investigators. Circulation. 2000;102:2700–6.PubMedCrossRef Zannad F, Alla F, Dousset B, et al. Limitation of excessive extracellular matrix turnover may contribute to survival benefit of spironolactone therapy in patients with congestive heart failure: insights from the randomized aldactone evaluation study (RALES). Rales Investigators. Circulation. 2000;102:2700–6.PubMedCrossRef
92.
go back to reference Webb CS, Bonnema DD, Ahmed SH, et al. Specific temporal profile of matrix metalloproteinase release occurs in patients after myocardial infarction: relation to left ventricular remodeling. Circulation. 2006;114:1020–7.PubMedCrossRef Webb CS, Bonnema DD, Ahmed SH, et al. Specific temporal profile of matrix metalloproteinase release occurs in patients after myocardial infarction: relation to left ventricular remodeling. Circulation. 2006;114:1020–7.PubMedCrossRef
93.
go back to reference Morizane Y, Thanos A, Takeuchi K, et al. AMP-activated protein kinase suppresses matrix metalloproteinase-9 expression in mouse embryonic fibroblasts. J Biol Chem. 2011;286:16030–8.PubMedCrossRef Morizane Y, Thanos A, Takeuchi K, et al. AMP-activated protein kinase suppresses matrix metalloproteinase-9 expression in mouse embryonic fibroblasts. J Biol Chem. 2011;286:16030–8.PubMedCrossRef
94.
go back to reference Mishra R, Cool BL, Laderoute KR, et al. AMP-activated protein kinase inhibits transforming growth factor-beta-induced Smad3-dependent transcription and myofibroblast transdifferentiation. J Biol Chem. 2008;283:10461–9.PubMedCrossRef Mishra R, Cool BL, Laderoute KR, et al. AMP-activated protein kinase inhibits transforming growth factor-beta-induced Smad3-dependent transcription and myofibroblast transdifferentiation. J Biol Chem. 2008;283:10461–9.PubMedCrossRef
95.
go back to reference Zheng B, Cantley LC. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci U S A. 2007;104:819–22.PubMedCrossRef Zheng B, Cantley LC. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc Natl Acad Sci U S A. 2007;104:819–22.PubMedCrossRef
96.
go back to reference Zhang L, Li J, Young LH, et al. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci U S A. 2006;103:17272–7.PubMedCrossRef Zhang L, Li J, Young LH, et al. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc Natl Acad Sci U S A. 2006;103:17272–7.PubMedCrossRef
Metadata
Title
AMP-activated Protein Kinase in the Control of Cardiac Metabolism and Remodeling
Authors
Sandrine Horman
Christophe Beauloye
Jean-Louis Vanoverschelde
Luc Bertrand
Publication date
01-09-2012
Publisher
Current Science Inc.
Published in
Current Heart Failure Reports / Issue 3/2012
Print ISSN: 1546-9530
Electronic ISSN: 1546-9549
DOI
https://doi.org/10.1007/s11897-012-0102-z

Other articles of this Issue 3/2012

Current Heart Failure Reports 3/2012 Go to the issue

Decompensated Heart Failure (MM Givertz, Section editor)

Mechanical Circulatory Support in Children: Bridge to Transplant Versus Recovery

Investigative Therapies (J.-L. Balligand, Section editor)

Cardiac Side Effects of Anticancer Treatments: New Mechanistic Insights

Decompensated Heart Failure (MM Givertz, Section editor)

Management of Acute Right Ventricular Failure in the Intensive Care Unit

Investigative Therapies (J.-L. Balligand, Section editor)

New Treatment Options for Late Na Current, Arrhythmias, and Diastolic Dysfunction

Decompensated Heart Failure (MM Givertz, Section editor)

Congestion Is the Driving Force Behind Heart Failure

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.