Trends in Cardiovascular Medicine
Volume 15, Issue 3 , Pages 110-118 , April 2005

AMP-Activated Protein Kinase: A Key Stress Signaling Pathway in the Heart

References 

  1. Altarejos JY, Taniguchi M, Clanachan AS, et al. Myocardial ischemia differentially regulates LKB1 and an alternate 5′-AMP-activated protein kinase kinase. J Biol Chem. 2005;280:183–190
  2. Andersson L. Identification and characterization of AMPK gamma3 mutations in the pig. Biochem Soc Trans. 2003;31:232–235
  3. Andersson U, Filipsson K, Abbott CR, et al. AMP-activated protein kinase plays a role in the control of food intake. J Biol Chem. 2004;279:12005–12008
  4. Arad M, Benson DW, Perez-Atayde AR, et al. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J Clin Invest. 2002;109:357–362
  5. Arad M, Moskowitz IP, Patel VV, et al. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff–Parkinson–White syndrome in glycogen storage cardiomyopathy. Circulation. 2003;107:2850–2856
  6. Baron SJ, Li J, Russell RR, et al. Dual mechanisms regulating AMP-activated protein kinase action in the ischemic heart. Circ Res. 2005;96:337–345
  7. Belke DD, Larsen TS, Gibbs EM, et al. Glucose metabolism in perfused mouse hearts overexpressing human GLUT-4 glucose transporter. Am J Physiol. 2001;280:E420–E427
  8. Bergeron R, Russell RR, Young LH, et al. Effect of AMPK activation on muscle glucose metabolism in conscious rats. Am J Physiol. 1999;276:E938–E944
  9. Blair E, Redwood C, Ashrafian H, et al. Mutations in the gamma2 subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum Mol Genet. 2001;10:1215–1220
  10. Boss O, Hagen T, Lowell BB. Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes. 2000;49:143–156
  11. 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;279:12220–12231
  12. Carling D. The AMP-activated protein kinase cascade—a unifying system for energy control. Trends Biochem Sci. 2004;29:18–24
  13. 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;279:32771–32779
  14. Chen ZP, Mitchelhill KI, Michell BJ, et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999;443:285–289
  15. Cheng SW, Fryer LG, Carling D, et al. Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J Biol Chem. 2004;279:15719–15722
  16. Choi SL, Kim SJ, Lee KT, et al. The regulation of AMP-activated protein kinase by H(2)O(2). Biochem Biophys Res Commun. 2001;287:92–97
  17. Coven DL, Hu X, Cong L, et al. Physiological role of AMP-activated protein kinase in the heart: graded activation during exercise. Am J Physiol. 2003;285:E629–E636
  18. Dagher Z, Ruderman N, Tornheim K, et al. The effect of AMP-activated protein kinase and its activator AICAR on the metabolism of human umbilical vein endothelial cells. (published erratum appears in Biochem Biophys Res Commun 1999 Dec 20;266:615) Biochem Biophys Res Commun. 1999;265:112–115
  19. Dagher Z, Ruderman N, Tornheim K, et al. Acute regulation of fatty acid oxidation and amp-activated protein kinase in human umbilical vein endothelial cells. Circ Res. 2001;88:1276–1282
  20. Daniel T, Carling D. Functional analysis of mutations in the gamma 2 subunit of AMP-activated protein kinase associated with cardiac hypertrophy and Wolff–Parkinson–White syndrome. J Biol Chem. 2002;277:51017–51024
  21. Durante PE, Mustard KJ, Park SH, et al. Effects of endurance training on activity and expression of AMP-activated protein kinase isoforms in rat muscles. Am J Physiol. 2002;283:E178–E186
  22. Dyck JR, Kudo N, Barr AJ, et al. Phosphorylation control of cardiac acetyl-CoA carboxylase by cAMP-dependent protein kinase and 5′-AMP activated protein kinase. Eur J Biochem. 1999;262:184–190
  23. Frederich M, Balschi JA. The relationship between AMP-activated protein kinase activity and AMP concentration in the isolated perfused rat heart. J Biol Chem. 2002;277:1928–1932
  24. Fryer LGD, Parbu-Patel A, Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct pathways. J Biol Chem. 2002;277:25226–25232
  25. Gollob MH, Green MS, Tang AS, et al. Identification of a gene responsible for familial Wolff–Parkinson–White syndrome. N Engl J Med. 2001;344:1823–1831
  26. Gollob MH, Seger JJ, Gollob TN, et al. Novel PRKAG2 mutation responsible for the genetic syndrome of ventricular preexcitation and conduction system disease with childhood onset and absence of cardiac hypertrophy. Circulation. 2001;104:3030–3033
  27. Hallows KR, Raghuram V, Kemp BE, et al. Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J Clin Invest. 2000;105:1711–1721
  28. Hamilton SR, O'Donnell JB, Hammet A, et al. AMP-activated protein kinase kinase: detection with recombinant AMPK alpha1 subunit. Biochem Biophys Res Commun. 2002;293:892–898
  29. Hardie D, Carling D, Halford N. Roles of the Snf1/Rkin1/AMP-activated protein kinase family in the response to environmental and nutritional stress. Semin Cell Biol. 1994;5:409–416
  30. Hardie DG. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology. 2003;144:5179–5183
  31. Hardie DG. AMP-activated protein kinase: the guardian of cardiac energy status. J Clin Invest. 2004;114:465–468
  32. Hardie DG, Carling D. The AMP-activated protein kinase–fuel gauge of the mammalian cell?. Eur J Biochem. 1997;246:259–273
  33. Hawley SA, Boudeau J, Reid JL, et al. Complexes between the LKB1 tumor suppressor, STRADalpha/beta and MO25alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol. 2003;2:28
  34. Hawley SA, Selbert MA, Goldstein EG, et al. 5′-AMP activates the AMP-activated protein kinase cascade, and Ca2+/calmodulin activates the calmodulin-dependent protein kinase I cascade, via three independent mechanisms. J Biol Chem. 1995;270:27186–27191
  35. Hayashi T, Hirshman MF, Kurth EJ, et al. Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes. 1998;47:1369–1373
  36. Hong YH, Varanasi US, Yang W, et al. AMP-activated protein kinase regulates HNF4 alpha transcriptional activity by inhibiting dimer formation and decreasing protein stability. J Biol Chem. 2003;278:27495–27501
  37. Hopkins TA, Dyck JR, Lopaschuk GD. AMP-activated protein kinase regulation of fatty acid oxidation in the ischaemic heart. Biochem Soc Trans. 2003;31:207–212
  38. 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;278:41970–41976
  39. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003;115:577–590
  40. Jorgensen SB, Nielsen JN, Birk JB, et al. The alpha2 5′AMP-activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading. Diabetes. 2004;53:3074–3081
  41. Kemp BE. Bateman domains and adenosine derivatives form a binding contract. J Clin Invest. 2004;113:182–184
  42. Kemp BE, Stapleton D, Campbell DJ, et al. AMP-activated protein kinase, super metabolic regulator. Biochem Soc Trans. 2003;31:162–168
  43. Kimura N, Tokunaga C, Dalal S, et al. A possible linkage between AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) signalling pathway. Genes Cells. 2003;8:65–79
  44. Kovacic S, Soltys CL, Barr AJ, et al. Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart. J Biol Chem. 2003;278:39422–39427
  45. Kudo N, Barr AJ, Barr RL, et al. High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5′-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J Biol Chem. 1995;270:17513–17520
  46. 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
  47. Lee M, Hwang JT, Lee HJ, et al. AMP-activated protein kinase activity is critical for hypoxia-inducible factor-1 transcriptional activity and its target gene expression under hypoxic conditions in DU145 cells. J Biol Chem. 2003;278:39653–39661
  48. 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. 2004;287:E834–E841
  49. Light PE, Wallace CH, Dyck JR. Constitutively active adenosine monophosphate-activated protein kinase regulates voltage-gated sodium channels in ventricular myocytes. Circulation. 2003;107:1962–1965
  50. Lizcano JM, Goransson O, Toth R, et al. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 2004;23:833–843
  51. Mangano DT. Effects of acadesine on myocardial infarction, stroke, and death following surgery. JAMA. 1997;277:325–332
  52. 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;10:1247–1255
  53. Merrill GF, Kurth EJ, Hardie DG, et al. AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol. 1997;273:E1107–E1112
  54. Minokoshi Y, Kim YB, Peroni OD, et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature. 2002;415:339–343
  55. Mu J, Brozinick JT, Valladares O, et al. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell. 2001;7:1085–1094
  56. Muoio DM, Seefeld K, Witters LA, et al. AMP-activated kinase reciprocally regulates triacylglycerol synthesis and fatty acid oxidation in liver and muscle: evidence that sn-glycerol-3-phosphate acyltransferase is a novel target. Biochem J. 1999;338:783–791
  57. Nagata D, Takeda R, Sata M, et al. AMP-activated protein kinase inhibits angiotensin II-stimulated vascular smooth muscle cell proliferation. Circulation. 2004;110:441–451
  58. Ojuka EO. Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle. Proc Nutr Soc. 2004;63:275–278
  59. Ouchi N, Kobayashi H, Kihara S, et al. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem. 2004;279:1304–1309
  60. Pelletier A, Joly E, Prentki M, et al. Adenosine 5'–monophosphate–activated protein kinase and p38 mitogen–activated protein kinase participate in the stimulation of glucose uptake by dinitrophenol in adult cardiomyocytes. Endocrinology. 2005;146:2285–2294
  61. Peralta C, Bartrons R, Serafin A, et al. Adenosine monophosphate-activated protein kinase mediates the protective effects of ischemic preconditioning on hepatic ischemia–reperfusion injury in the rat. Hepatology. 2001;34:1164–1173
  62. Polekhina G, Gupta A, Michell BJ, et al. AMPK beta subunit targets metabolic stress sensing to glycogen. Curr Biol. 2003;13:867–871
  63. Ruderman NB, Cacicedo JM, Itani S, et al. Malonyl-CoA and AMP-activated protein kinase (AMPK): possible links between insulin resistance in muscle and early endothelial cell damage in diabetes. Biochem Soc Trans. 2003;31:202–206
  64. Russell RR, Bergeron R, Shulman GI, et al. Translocation of myocardial GLUT4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol. 1999;277:H643–H649
  65. Russell 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
  66. Saha AK, Schwarsin AJ, Roduit R, et al. Activation of malonyl-CoA decarboxylase in rat skeletal muscle by contraction and the AMP-activated protein kinase activator 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside. J Biol Chem. 2000;275:24279–24283
  67. Sakamoto K, Goransson O, Hardie DG, et al. Activity of LKB1 and AMPK-related kinases in skeletal muscle; effects of contraction, phenformin and AICAR. Am J Physiol. 2004;287:E310–E317
  68. Salt I, Celler JW, Hawley SA, et al. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem J. 1998;334:177–187
  69. Scott JW, Hawley SA, Green KA, et al. CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest. 2004;113:274–284
  70. Shaw RJ, Kosmatka M, Bardeesy N, et al. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A. 2004;101:3329–3335
  71. Sidhu JS, Rajawat YS, Rami TG, et al. Transgenic mouse model of ventricular preexcitation and atrioventricular reentrant tachycardia induced by an AMP-activated protein kinase loss-of-function mutation responsible for Wolff–Parkinson–White syndrome. Circulation. 2005;111:21–29
  72. Spicer J, Ashworth A. LKB1 kinase: master and commander of metabolism and polarity. Curr Biol. 2004;14:R383–R385
  73. Stein SC, Woods A, Jones NA, et al. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J. 2000;345:437–443
  74. Thelander M, Olsson T, Ronne H. Snf1-related protein kinase 1 is needed for growth in a normal day–night light cycle. EMBO J. 2004;23:1900–1910
  75. 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;104:1664–1669
  76. Wang W, Fan J, Yang X, et al. AMP-activated kinase regulates cytoplasmic HuR. Mol Cell Biol. 2002;22:3425–3436
  77. Warden SM, Richardson C, O'Donnell J, et al. Post-translational modifications of the beta-1 subunit of AMP-activated protein kinase affect enzyme activity and cellular localization. Biochem J. 2001;354:275–283
  78. Winder WW, Hardie DG. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol. 1996;270:E299–E304
  79. Wojtaszewski JF, Jorgensen SB, Hellsten Y, et al. Glycogen-dependent effects of 5-aminoimidazole-4-carboxamide (AICA)-riboside on AMP-activated protein kinase and glycogen synthase activities in rat skeletal muscle. Diabetes. 2002;51:284–292
  80. Woods A, Johnstone SR, Dickerson K, et al. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol. 2003;13:2004–2008
  81. Wright DC, Hucker KA, Holloszy JO, et al. Ca2+ and AMPK both mediate stimulation of glucose transport by muscle contractions. Diabetes. 2004;53:330–335
  82. 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;278:28372–28377
  83. Yamauchi T, Kamon J, Minokoshi Y, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med. 2002;8:1288–1295
  84. Yin W, Mu J, Brinbaum MJ. Role of AMP-activated protein kinase in cyclic AMP-dependent lipolysis in 3T3-L1 adipocytes. J Biol Chem. 2003;278:43074–43080
  85. Young LH, Renfu Y, Russell RR, et al. Low-flow ischemia leads to translocation of canine heart GLUT-4 and GLUT-1 glucose transporters to the sarcolemma in vivo. Circulation. 1997;95:415–422
  86. Young LH, Russell RR, Yin R, et al. Regulation of myocardial glucose uptake and transport during ischemia and energetic stress. Am J Cardiol. 1999;83:25H–30H
  87. Zhou G, Myers R, Li Y, et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest. 2001;108:1167–1174
  88. Zhou M, Lin BZ, Coughlin S, et al. UCP-3 expression in skeletal muscle: effects of exercise, hypoxia, and AMP-activated protein kinase. Am J Physiol. 2000;279:E622–E629
  89. Zong H, Ren JM, Young LH, et al. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA. 2002;99:15983–15987

PII: S1050-1738(05)00038-1

doi: 10.1016/j.tcm.2005.04.005

Trends in Cardiovascular Medicine
Volume 15, Issue 3 , Pages 110-118 , April 2005