AMP-activated protein kinase conducts the ischemic stress response orchestra

Circulation

Volumn 117, Issue 6, 2008, Pages 832-840

  Young, Lawrence H ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b 333 Cedar St ^*  (United States)

Author keywords

AMP kinase; Fatty acids; Glucose; Ischemia; Signal transduction

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; MITOGEN ACTIVATED PROTEIN KINASE; AMP ACTIVATED PROTEIN KINASES; AMP-ACTIVATED PROTEIN KINASES; MULTIENZYME COMPLEX; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

CARDIOMYOPATHY; CELL ENERGY; CELL ORGANELLE; CELL STRESS; ENZYME ACTIVATION; EXERCISE; GENE MUTATION; HEART MUSCLE ISCHEMIA; HEART STRESS; ISCHEMIC PRECONDITIONING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; HEART DISEASE; HEART INFARCTION PREVENTION; HEART MUSCLE; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

HEART DISEASES; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; MUTATION; MYOCARDIAL ISCHEMIA; MYOCARDIUM; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 39549092137     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.107.713115     Document Type: Review

References (95)

1. Young LH, Li J, Baron SJ, Russell RR. AMP-activated protein kinase: a key stress signaling pathway in the heart. Trends Cardiovasc Med. 2005;15:110-118.
2. Dyck JR, Lopaschuk GD. AMPK alterations in cardiac physiology and pathology: enemy or ally? J Physiol. 2006;574:95-112.
3. Ruderman NB, Cacicedo JM, Itani S, Yagihashi N, Saha AK, Ye JM, Chen K, Zou M, Carling D, Boden G, Cohen RA, Keaney J, Kraegen EW, Ido Y. 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.
4. Motoshima H, Goldstein BJ, Igata M, Araki E. AMPK and cell proliferation: AMPK as a therapeutic target for atherosclerosis and cancer. J Physiol. 2006;574:63-71.
5. Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005;1:15-25.
6. Towler MC, Hardie DG. AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res. 2007;100:328-341.
7. Arad M, Seidman CE, Seidman JG. AMP-activated protein kinase in the heart: role during health and disease. Circ Res. 2007;100:474-488.
8. Hardie DG, Hawley SA, Scott JW. AMP-activated protein kinase: development of the energy sensor concept. J Physiol. 2006;574:7-15.
9. 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.
10. Carling D, Clarke P, Zammit V, Hardie D. Purification and characterization of the AMP-activated protein kinase: copurification of acetyl-CoA carboxylase kinase and 3-hydroxy-3-methylglutaryl-CoA reductase kinase activities. Eur J Biochem. 1989;186:129-136.
11. Kudo N, Barr AJ, Barr RL, Desai S, Lopaschuk GD. 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.
12. Sun W, Lee TS, Zhu M, Gu C, Wang Y, Zhu Y, Shyy JY. Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation. 2006;114:2655-2662.
13. Hardie DG. AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med Sci Sports Exerc. 2004;36:28-34.
14. Wojtaszewski JF, Jorgensen SB, Hellsten Y, Hardie DG, Richter EA. 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.
15. Polekhina G, Gupta A, Michell BJ, van Denderen B, Murthy S, Feil SC, Jennings IG, Campbell DJ, Witters LA, Parker MW, Kemp BE, Stapleton D. AMPK beta subunit targets metabolic stress sensing to glycogen. Curr Biol. 2003;13:867-871.
16. Russell RR, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ, Young LH. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest. 2004;114:495-503.
17. Coven DL, Hu X, Cong L, Bergeron R, Shulman GI, Hardie DG, Young LH. Physiological role of AMP-activated protein kinase in the heart: graded activation during exercise. Am J Physiol. 2003;285:E629-E636.
18. Kemp BE. Bateman domains and adenosine derivatives form a binding contract. J Clin Invest. 2004;113:182-184.
19. Hardie DG. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology. 2003;144:5179-5183.
20. Li J, Coven DL, Miller EJ, Hu X, Young ME, Carling D, Sinusas AJ, Young LH. Activation of AMPK alpha- and gamma-isoform complexes in the intact ischemic rat heart. Am J Physiol. 2006;291:H1927-H1934.
21. Salt I, Celler JW, Hawley SA, Prescott A, Woods A, Carling D, Hardie DG. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem J. 1998;334:177-187.
22. Musi N, Hirshman MF, Arad M, Xing Y, Fujii N, Pomerleau J, Ahmad F, Berul CI, Seidman JG, Tian R, Goodyear LJ. Functional role of AMP-activated protein kinase in the heart during exercise. FEBS Lett. 2005;579:2045-2050.
23. Kudo N, Gillespie JG, Kung L, Witters LA, Schulz R, Clanachan AS, Lopaschuk GD. 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.
24. Baron S, Li J, Russell RR, Neumann D, Miller EJ, Tuerk R, Walliman T, Hurley R, Witters LA, Young LH. Dual mechanisms regulating AMP-activated protein kinase action in the ischemic heart. Circ Res. 2005;96:337-345.
25. Hawley SA, Selbert MA, Goldstein EG, Edelman AM, Carling D, Hardie DG. 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.
26. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem. 1996;271:27879-27887.
27. Stein SC, Woods A, Jones NA, Davison MD, Carling D. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J. 2000;345:437-443.
28. Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, Neumann D. Dissecting the role of 5′-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem. 2006;281:32207-32216.
29. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D. Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J. 2007;403:139-148.
30. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol. 2003;2:28.
31. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol. 2003;13:2004-2008.
32. Hemminki A, Markie D, Tomlinson I, Avizienyte E, Roth S, Loukola A, Bignell G, Warren W, Aminoff M, Hoglund P, Jarvinen H, Kristo P, Pelin K, Ridanpaa M, Salovaara R, Toro T, Bodmer W, Olschwang S, Olsen AS, Stratton MR, de la Chapelle A, Aaltonen LA. A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature. 1998;391:184-187.
33. Carretero J, Medina PP, Blanco R, Smit L, Tang M, Roncador G, Maestre L, Conde E, Lopez-Rios F, Clevers HC, Sanchez-Cespedes M. Dysfunctional AMPK activity, signaling through mTOR and survival in response to energetic stress in LKB1-deficient lung cancer. Oncogene. 2007;26:1616-1625.
34. Spicer J, Ashworth A. LKB1 kinase: master and commander of metabolism and polarity. Curr Biol. 2004;14:R383-R385.
35. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC. 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.
36. Sakamoto K, Zarrinpashneh E, Budas GR, Pouleur AC, Dutta A, Prescott AR, Vanoverschelde JL, Ashworth A, Jovanovic A, Alessi DR, Bertrand L. Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPK alpha2 but not AMPK alpha1. Am J Physiol. 2006;290:E780-E788.
37. Shibata R, Sato K, Pimentel DR, Takemura Y, Kihara S, Ohashi K, Funahashi T, Ouchi N, Walsh K. Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat Med. 2005;11:1096-1103.
38. Gamble J, Lopaschuk GD. Insulin inhibition of 5′ adenosine monophosphate-activated protein kinase in the heart results in activation of acetyl coenzyme A carboxylase and inhibition of fatty acid oxidation. Metabolism. 1997;46:1270-1274.
39. Beauloye C, Marsin AS, Bertrand L, Krause U, Hardie DG, Vanoverschelde JL, Hue L. Insulin antagonizes AMP-activated protein kinase activation by ischemia or anoxia in rat hearts without affecting total adenine nucleotides. FEBS Lett. 2001;505:348-352.
40. Hue L, Beauloye C, Marsin AS, Bertrand L, Horman S, Rider MH. Insulin and ischemia stimulate glycolysis by acting on the same targets through different and opposing signaling pathways. J Mol Cell Cardiol. 2002;34:1091-1097.
41. Russell RR, Bergeron R, Shulman GI, Young LH. Translocation of myocardial GLUT4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol. 1999;277:H643-H649.
42. Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, Van den Berghe G, Carling D, Hue L. 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.
43. Chen ZP, McConell GK, Michell BJ, Snow RJ, Canny BJ, Kemp BE. AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am J Physiol. 2000;279:E1202-E1206.
44. Li J, Hu X, Selvakumar P, Russell RR, Cushman SW, Holman GD, Young LH. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am J Physiol. 2004;287:E834-E841.
45. Young LH, Renfu Y, Russell RR, Hu X, Caplan MJ, Ren J, Shulman GI, Sinusas AJ. 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.
46. Tian R, Abel ED. Responses of GLUT4-deficient hearts to ischemia underscore the importance of glycolysis. Circulation. 2001;103:2961-2966.
47. Xing Y, Musi N, Fujii N, Zou L, Luptak I, Hirshman MF, Goodyear LJ, Tian R. 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.
48. Li J, Miller EJ, Ninomiya-Tsuji J, Russell RR, Young LH. AMP-activated protein kinase activates p38 mitogen-activated protein kinase by increasing recruitment of p38 MAPK to TAB1 in the ischemic heart. Circ Res. 2005;97:872-879.
49. Yang J, Holman GD. Insulin and contraction stimulate exocytosis, but increased AMP-activated protein kinase activity resulting from oxidative metabolism stress slows endocytosis of GLUT4 in cardiomyocytes. J Biol Chem. 2005;280:4070-4078.
50. Luiken JJ, Coort SL, Willems J, Coumans WA, Bonen A, van der Vusse GJ, Glatz JF. Contraction-induced fatty acid translocase/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling. Diabetes. 2003;52:1627-1634.
51. An D, Pulinilkunnil T, Qi D, Ghosh S, Abrahani A, Rodrigues B. The metabolic "switch" AMPK regulates cardiac heparin-releasable lipoprotein lipase. Am J Physiol. 2005;288:E246-E253.
52. Augustus AS, Buchanan J, Park TS, Hirata K, Noh HL, Sun J, Homma S, D'Armiento J, Abel ED, Goldberg IJ. Loss of lipoprotein lipase-derived fatty acids leads to increased cardiac glucose metabolism and heart dysfunction. J Biol Chem. 2006;281:8716-8723.
53. Hardie DG. AMP-activated protein kinase: the guardian of cardiac energy status. J Clin Invest. 2004;114:465-468.
54. Horman S, Beauloye C, Vertommen D, Vanoverschelde JL, Hue L, Rider MH. Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J Biol Chem. 2003;278:41970-41976.
55. Chan AY, Soltys CL, Young ME, Proud CG, Dyck JR. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J Biol Chem. 2004;279:32771-32779.
56. 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.
57. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003;115:577-590.
58. Carvajal K, Zarrinpashneh E, Szarszoi O, Joubert F, Athea Y, Mateo P, Gillet B, Vaulont S, Viollet B, Bigard X, Bertrand L, Ventura-Clapier R, Hoerter JA. Dual cardiac contractile effects of the alpha2-AMPK deletion in low-flow ischemia and reperfusion. Am J Physiol. 2007;292:H3136-H3147.
59. Eefting F, Rensing B, Wigman J, Pannekoek WJ, Liu WM, Cramer MJ, Lips DJ, Doevendans PA. Role of apoptosis in reperfusion injury. Cardiovasc Res. 2004;61:414-426.
60. Nishino Y, Miura T, Miki T, Sakamoto J, Nakamura Y, Ikeda Y, Kobayashi H, Shimamoto K. Ischemic preconditioning activates AMPK in a PKC-dependent manner and induces GLUT4 up-regulation in the late phase of cardioprotection. Cardiovasc Res. 2004;61:610-619.
61. + channels. J Cell Physiol. 2007;210:224-236.
62. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res. 2004;95:957-970.
63. Kitsis RN, Mann DL. Apoptosis and the heart: a decade of progress. J Mol Cell Cardiol. 2005;38:1-2.
64. Terai K, Hiramoto Y, Masaki M, Sugiyama S, Kuroda T, Hori M, Kawase I, Hirota H. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol Cell Biol. 2005;25:9554-9575.
65. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6:463-477.
66. Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, Polyakova V, Bauer EP, Klovekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation. 2003;107:984-991.
67. Yan L, Vatner DE, Kim SJ, Ge H, Masurekar M, Massover WH, Yang G, Matsui Y, Sadoshima J, Vatner SF. Autophagy in chronically ischemic myocardium. Proc Natl Acad Sci U S A. 2005;102:13807-13812.
68. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and beclin 1 in mediating autophagy. Circ Res. 2007;100:914-922.
69. Mangano DT. Effects of acadesine on myocardial infarction, stroke, and death following surgery. JAMA. 1997;277:325-332.
70. Cool B, Zinker B, Chiou W, Kifle L, Cao N, Perham M, Dickinson R, Adler A, Gagne G, Iyengar R, Zhao G, Marsh K, Kym P, Jung P, Camp HS, Frevert E. Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab. 2006;3:403-416.
71. Gollob MH, Green MS, Tang AS, Gollob T, Karibe A, Ali Hassan AS, Ahmad F, Lozado R, Shah G, Fananapazir L, Bachinski LL, Roberts R, Hassan AS. Identification of a gene responsible for familial Wolff-Parkinson-White syndrome. N Engl J Med. 2001;344:1823-1831.
72. Gollob MH, Seger JJ, Gollob TN, Tapscott T, Gonzales O, Bachinski L, Roberts R. 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.
73. Arad M, Benson DW, Perez-Atayde AR, McKenna WJ, Sparks EA, Kanter RJ, McGarry K, Seidman JG, Seidman CE. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J Clin Invest. 2002;109:357-362.
74. Arad M, Maron BJ, Gorham JM, Johnson WH Jr, Saul JP, Perez-Atayde AR, Spirito P, Wright GB, Kanter RJ, Seidman CE, Seidman JG. Glycogen storage diseases presenting as hypertrophic cardiomyopathy. N Engl J Med. 2005;352:362-372.
75. Murphy RT, Mogensen J, McGarry K, Bahl A, Evans A, Osman E, Syrris P, Gorman G, Farrell M, Holton JL, Hanna MG, Hughes S, Elliott PM, Macrae CA, McKenna WJ. Adenosine monophosphate-activated protein kinase disease mimics hypertrophic cardiomyopathy and Wolff-Parkinson-White syndrome: natural history. J Am Coll Cardiol. 2005;45:922-930.
76. Arad M, Moskowitz IP, Patel VV, Ahmad F, Perez-Atayde AR, Sawyer DB, Walter M, Li GH, Burgon PG, Maguire CT, Stapleton D, Schmitt JP, Guo XX, Pizard A, Kupershmidt S, Roden DM, Berul CI, Seidman CE, Seidman JG. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation. 2003;107:2850-2856.
77. Zou L, Shen M, Arad M, He H, Lofgren B, Ingwall JS, Seidman CE, Seidman JG, Tian R. N488I mutation of the gamma2-subunit results in bidirectional changes in AMP-activated protein kinase activity. Circ Res. 2005;97:323-328.
78. Sidhu JS, Rajawat YS, Rami TG, Gollob MH, Wang Z, Yuan R, Marian AJ, DeMayo FJ, Weilbacher D, Taffet GE, Davies JK, Carling D, Khoury DS, Roberts R. 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.
79. Davies JK, Wells DJ, Liu K, Whitrow HR, Daniel TD, Grignani R, Lygate CA, Schneider JE, Noel G, Watkins H, Carling D. Characterization of the role of gamma 2 R531G mutation in AMP-activated protein kinase in cardiac hypertrophy and Wolff-Parkinson-White syndrome. Am J Physiol. 2006;290:H1942-H1951.
80. Ahmad F, Arad M, Musi N, He H, Wolf C, Branco D, Perez-Atayde AR, Stapleton D, Bali D, Xing Y, Tian R, Goodyear LJ, Berul CI, Ingwall JS, Seidman CE, Seidman JG. Increased alpha2 subunit-associated AMPK activity and PRKAG2 cardiomyopathy. Circulation. 2005;112:3140-3148.
81. Luptak I, Shen M, He H, Hirshman MF, Musi N, Goodyear LJ, Yan J, Wakimoto H, Morita H, Arad M, Seidman CE, Seidman JG, Ingwall JS, Balschi JA, Tian R. Aberrant activation of AMP-activated protein kinase remodels metabolic network in favor of cardiac glycogen storage. J Clin Invest. 2007;117:1432-1439.
82. Dagher Z, Ruderman N, Tornheim K, Ido Y. Acute regulation of fatty acid oxidation and AMP-activated protein kinase in human umbilical vein endothelial cells. Circ Res. 2001;88:1276-1282.
83. Guo D, Chien S, Shyy JY. Regulation of endothelial cell cycle by laminar versus oscillatory flow: distinct modes of interactions of AMP-activated protein kinase and Akt pathways. Circ Res. 2007;100:564-571.
84. Nagata D, Takeda R, Sata M, Satonaka H, Suzuki E, Nagano T, Hirata Y. AMP-activated protein kinase inhibits angiotensin II-stimulated vascular smooth muscle cell proliferation. Circulation. 2004;110:444-451.
85. Igata M, Motoshima H, Tsuruzoe K, Kojima K, Matsumura T, Kondo T, Taguchi T, Nakamaru K, Yano M, Kukidome D, Matsumoto K, Toyonaga T, Asano T, Nishikawa T, Araki E. Adenosine monophosphate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ Res. 2005;97:837-844.
86. 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;278:31000-31006.
87. Yun H, Lee M, Kim SS, Ha J. Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J Biol Chem. 2005;280:9963-9972.
88. Hayashi T, Hirshman MF, Kurth EJ, Winder WW, Goodyear LJ. Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport. Diabetes. 1998;47:1369-1373.
89. Lochhead PA, Salt IP, Walker KS, Hardie DG, Sutherland C. 5-Aminoimidazole-4-carboxamide riboside mimics the effects of insulin on the expression of the 2 key gluconeogenic genes PEPCK and glucose-6-phosphatase. Diabetes. 2000;49:896-903.
90. Wang C, Mao X, Wang L, Liu M, Wetzel MD, Guan KL, Dong LQ, Liu F. Adiponectin sensitizes insulin signaling by reducing p70 S6 kinase-mediated serine phosphorylation of IRS-1. J Biol Chem. 2007;22:3425-3436.
91. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest. 2001;108:1167-1174.
92. Hardie DG. Neither LKB1 nor AMPK are the direct targets of metformin. Gastroenterology. 2006;131:973.
93. Fryer LG, Parbu-Patel A, Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J Biol Chem. 2002;277:25226-25232.
94. Saha AK, Avilucea PR, Ye JM, Assifi MM, Kraegen EW, Ruderman NB. Pioglitazone treatment activates AMP-activated protein kinase in rat liver and adipose tissue in vivo. Biochem Biophys Res Commun. 2004;314:580-585.
95. Andersson U, Filipsson K, Abbott CR, Woods A, Smith K, Bloom SR, Carling D, Small CJ. AMP-activated protein kinase plays a role in the control of food intake. J Biol Chem. 2004;279:12005-12008.