AMP-activated protein kinase activation as a strategy for protecting vascular endothelial function

Clinical and Experimental Pharmacology and Physiology

Volumn 35, Issue 5-6, 2008, Pages 535-545

  Zou, Ming Hui ^a   Wu, Yong ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

AMP activated kinase; Atherosclerosis; Diabetes mellitus; Endothelium; Energy metabolism; Hypertension; Nitric oxide; Oxidative stress; Peroxynitrite; Superoxide anions

Indexed keywords

ADENYLATE KINASE; ISOENZYME; METFORMIN; OXIDIZING AGENT; PROTEIN SERINE THREONINE KINASE; ROSIGLITAZONE; STATINE DERIVATIVE;

CARDIOVASCULAR FUNCTION; CELL ENERGY; CELL METABOLISM; ENERGY BALANCE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; EUKARYOTIC CELL; HUMAN; METABOLIC REGULATION; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATION REDUCTION POTENTIAL; REVIEW; SENSOR; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; WEIGHT CONTROL;

ENDOTHELIAL CELLS; ENZYME ACTIVATION; MULTIENZYME COMPLEXES; PROTEIN-SERINE-THREONINE KINASES;

EID: 41749120541     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2007.04851.x     Document Type: Review

References (113)

1. Kemp BE, Stapleton D, Campbell DJ et al. AMP-activated protein kinase, super metabolic regulator. Biochem. Soc. Trans. 2003 31 : 162 8.
2. Winder WW, Hardie DG. AMP-activated protein kinase, a metabolic master switch: Possible roles in type 2 diabetes. Am. J. Physiol. 1999 277 : E1 10.
3. 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 8.
4. Sakamoto K, Goransson O, Hardie DG, Alessi DR. Activity of LKB1 and AMPK-related kinases in skeletal muscle: Effects of contraction, phenformin, and AICAR. Am. J. Physiol. Endocrinol. Metab. 2004 287 : E310 17.
5. Hawley SA, Boudeau J, Reid JL et al. 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.
6. 2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 2005 280 : 29 060 6.
7. Hardie DG, 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 16.
8. Soltoff SP. Evidence that tyrphostins AG10 and AG18 are mitochondrial uncouplers that alter phosphorylation-dependent cell signaling. J. Biol. Chem. 2004 279 : 10 910 18.
9. Kubota N, Yano W, Kubota T et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab. 2007 6 : 55 68.
10. Uotani S, Abe T, Yamaguchi Y. Leptin activates AMP-activated protein kinase in hepatic cells via a JAK2-dependent pathway. Biochem. Biophys. Res. Commun. 2006 351 : 171 5.
11. Hutchinson DS, Chernogubova E, Dallner OS, Cannon B, Bengtsson T. Beta-adrenoceptors, but not alpha-adrenoceptors, stimulate AMP-activated protein kinase in brown adipocytes independently of uncoupling protein-1. Diabetologia 2005 48 : 2386 95.
12. Daval M, Diot-Dupuy F, Bazin R et al. Anti-lipolytic action of AMP-activated protein kinase in rodent adipocytes. J. Biol. Chem. 2005 280 : 25 250 7.
13. An Z, Wang H, Song P, Zhang M, Gong X, Zou MH. Nicotine-induced activation of AMP-activated protein kinase Inhibits fatty acid synthase in 3T3-L1 adipocytes: A role for oxidant stress. J. Biol. Chem. 2007 282 : 26 793 801.
14. Shaw RJ, Lamia KA, Vasquez D et al. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 2005 310 : 1642 6.
15. LeBrasseur NK, Kelly M, Tsao TS et al. Thiazolidinediones can rapidly activate AMP-activated protein kinase in mammalian tissues. Am. J. Physiol. Endocrinol. Metab. 2006 291 : E175 81.
16. Zou MH, Kirkpatrick SS, Davis BJ et al. Activation of the AMP-activated protein kinase by the anti-diabetic drug metformin in vivo. Role of mitochondrial reactive nitrogen species. J. Biol. Chem. 2004 279 : 43 940 51.
17. Xie Z, Dong Y, Zhang M et al. Activation of protein kinase C zeta by peroxynitrite regulates LKB1-dependent AMP-activated protein kinase in cultured endothelial cells. J. Biol. Chem. 2006 281 : 6366 75.
18. 2. Biochem. Biophys. Res. Commun. 2001 287 : 92 7.
19. Iseli TJ, Walter M, van Denderen BJ et al. AMP-activated protein kinase beta subunit tethers alpha and gamma subunits via its C-terminal sequence (186-270). J. Biol. Chem. 2005 280 : 13 395 400.
20. Gao G, Widmer J, Stapleton D et al. Catalytic subunits of the porcine and rat 5′-AMP-activated protein kinase are members of the SNF1 protein kinase family. Biochim. Biophys. Acta 1995 1266 : 73 82.
21. 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 12.
22. Ruderman NB, Park H, Kaushik VK et al. AMPK as a metabolic switch in rat muscle, liver and adipose tissue after exercise. Acta Physiol. Scand. 2003 178 : 435 42.
23. Chen ZP, Mitchelhill KI, Michell BJ et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999 443 : 285 9.
24. Winder WW, Holmes BF, Rubink DS, Jensen EB, Chen M, Holloszy JO. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 2000 88 : 2219 26.
25. Brauner P, Kopecky P, Flachs P et al. Expression of uncoupling protein 3 and GLUT4 gene in skeletal muscle of preterm newborns: Possible control by AMP-activated protein kinase. Pediatr. Res. 2006 60 : 569 75.
26. Woods A, Azzout-Marniche D, Foretz M et al. 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 20 : 6704 11.
27. Hubert A, Husson A, Chedeville A, Lavoinne A. AMP-activated protein kinase counteracted the inhibitory effect of glucose on the phosphoenolpyruvate carboxykinase gene expression in rat hepatocytes. FEBS Lett. 2000 481 : 209 12.
28. Steinberg HO, Paradisi G, Hook G, Crowder K, Cronin J, Baron AD. Free fatty acid elevation impairs insulin-mediated vasodilation and nitric oxide production. Diabetes 2000 49 : 1231 8.
29. Artwohl M, Roden M, Waldhausl W, Freudenthaler A, Baumgartner-Parzer SM. Free fatty acids trigger apoptosis and inhibit cell cycle progression in human vascular endothelial cells. FASEB J. 2004 18 : 146 8.
30. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am. J. Cardiol. 2003 91 : A7 11.
31. Libby P. Current concepts of the pathogenesis of the acute coronary syndromes. Circulation 2001 104 : 365 72.
32. Ido Y, Carling D, Ruderman N. Hyperglycemia-induced apoptosis in human umbilical vein endothelial cells: Inhibition by the AMP-activated protein kinase activation. Diabetes 2002 51 : 159 67.
33. Nishikawa T, Edelstein D, Du XL et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000 404 : 787 90.
34. Inoguchi T, Li P, Umeda F et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000 49 : 1939 45.
35. Pieper GM, Riaz Ul H. Activation of nuclear factor-kappaB in cultured endothelial cells by increased glucose concentration: Prevention by calphostin C. J. Cardiovasc. Pharmacol. 1997 30 : 528 32.
36. Cheung PC, Salt IP, Davies SP, Hardie DG, Carling D. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem. J. 2000 346 : 659 69.
37. Kemp BE, Mitchelhill KI, Stapleton D, Michell BJ, Chen ZP, Witters LA. Dealing with energy demand: The AMP-activated protein kinase. Trends Biochem. Sci. 1999 24 : 22 5.
38. Dyck JR, Gao G, Widmer J et al. Regulation of 5′-AMP-activated protein kinase activity by the noncatalytic beta and gamma subunits. J. Biol. Chem. 1996 271 : 17 798 803.
39. Stapleton D, Mitchelhill KI, Gao G et al. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 1996 271 : 611 14.
40. Lihn AS, Jessen N, Pedersen SB, Lund S, Richelson B. AICAR stimulates adiponectin and inhibits cytokines in adipose tissue. Biochem. Biophys. Res. Commun. 2004 316 : 853 8.
41. Woods A, Salt I, Scott J, Hardie DG, Carling D. The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Lett. 1996 397 : 347 51.
42. 2+ signalling mechanisms in oxygen-sensing cells. Novartis Found. Symp. 2006 272 : 234 52.
43. Davis BJ, Xie Z, Viollet B, Zou MH. Activation of the AMP-activated kinase by antidiabetes drug metformin stimulates nitric oxide synthesis in vivo by promoting the association of heat shock protein 90 and endothelial nitric oxide synthase. Diabetes 2006 55 : 496 505.
44. 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 : 31 000 6.
45. 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 87.
46. Dagher Z, Ruderman N, Tornheim K, Ido Y. The effect of AMP-activated protein kinase and its activator AICAR on the metabolism of human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 1999 265 : 112 15.
47. Zhang Y, Lee TS, Kolb EM et al. AMP-activated protein kinase is involved in endothelial NO synthase activation in response to shear stress. Arterioscler. Thromb. Vasc. Biol. 2006 26 : 1281 7.
48. Ouchi N, Shibata R, Walsh K. AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ. Res. 2005 96 : 838 46.
49. 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. USA 2004 101 : 3329 35.
50. Boudeau J, Sapkota G, Alessi DR. LKB1, a protein kinase regulating cell proliferation and polarity. FEBS Lett. 2003 546 : 159 65.
51. 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 43.
52. 2+/calmodulin activates the calmodulin-dependent protein kinase I cascade, via three independent mechanisms. J. Biol. Chem. 1995 270 : 27 186 91.
53. 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 : 25 226 32.
54. Hong SP, Leiper FC, Woods A, Carling D, Carlson M. Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc. Natl Acad. Sci. USA 2003 100 : 8839 43.
55. Sutherland CM, Hawley SA, McCartney RR et al. Elm1p is one of three upstream kinases for the Saccharomyces cerevisiae SNF1 complex. Curr. Biol. 2003 13 : 1299 305.
56. 2+/calmodulin-dependent protein kinase kinase beta. Mol. Cell. Biol. 2006 26 : 5933 45.
57. Wu Y, Song P, Xu J, Zhang M, Zou MH. Activation of protein phosphatase 2A by palmitate inhibits AMP-activated protein kinase. J. Biol. Chem. 2007 282 : 9777 88.
58. Zou MH, Hou XY, Shi CM et al. Activation of 5′-AMP-activated kinase is mediated through c-Src and phosphoinositide 3-kinase activity during hypoxia-reoxygenation of bovine aortic endothelial cells. Role of peroxynitrite. J. Biol. Chem. 2003 278 : 34 003 10.
59. Zou MH, Hou XY, Shi CM, Nagata D, Walsh K, Cohen RA. Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. J. Biol. Chem. 2002 277 : 32 552 7.
60. 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 9.
61. Schulz E, Anter E, Zou MH, Keaney JF, Jr. Estradiol-mediated endothelial nitric oxide synthase association with heat shock protein 90 requires adenosine monophosphate-dependent protein kinase. Circulation 2005 111 : 3473 80.
62. Mount PF, Hill RE, Fraser SA et al. Acute renal ischemia rapidly activates the energy sensor AMPK but does not increase phosphorylation of eNOS-Ser1177. Am. J. Physiol. Renal Physiol. 2005 289 : F1103 15.
63. Thors B, Halldorsson H, Thorgeirsson G. Thrombin and histamine stimulate endothelial nitric-oxide synthase phosphorylation at Ser1177 via an AMPK mediated pathway independent of PI3K-Akt. FEBS Lett. 2004 573 : 175 80.
64. Sakamoto K, McCarthy A, Smith D et al. Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J. 2005 24 : 1810 20.
65. Puceat M, Vassort G. Signalling by protein kinase C isoforms in the heart. Mol. Cell. Biochem. 1996 157 : 65 72.
66. Forcet C, Etienne-Manneville S, Gaude H et al. Functional analysis of Peutz-Jeghers mutations reveals that the LKB1 C-terminal region exerts a crucial role in regulating both the AMPK pathway and the cell polarity. Hum. Mol. Genet. 2005 14 : 1283 92.
67. Farese RV. Function and dysfunction of aPKC isoforms for glucose transport in insulin-sensitive and insulin-resistant states. Am. J. Physiol. Endocrinol. Metab. 2002 283 : E1 11.
68. Carling D. AMP-activated protein kinase: Balancing the scales. Biochimie 2005 87 : 87 91.
69. Shaw RJ, Bardeesy N, Manning BD et al. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell 2004 6 : 91 9.
70. Luo Z, Saha AK, Xiang X, Ruderman NB. AMPK, the metabolic syndrome and cancer. Trends Pharmacol. Sci. 2005 26 : 69 76.
71. Davies SP, Helps NR, Cohen PT, Hardie DG. 5′-AMP inhibits dephosphorylation, as well as promoting phosphorylation, of the AMP-activated protein kinase. Studies using bacterially expressed human protein phosphatase-2C alpha and native bovine protein phosphatase-2AC. FEBS Lett. 1995 377 : 421 5.
72. Ingebritsen TS, Stewart AA, Cohen P. The protein phosphatases involved in cellular regulation. 6. Measurement of type-1 and type-2 protein phosphatases in extracts of mammalian tissues: An assessment of their physiological roles. Eur. J. Biochem. 1983 132 : 297 307.
73. Wang MY, Unger RH. Role of PP2C in cardiac lipid accumulation in obese rodents and its prevention by troglitazone. Am. J. Physiol. Endocrinol. Metab. 2005 288 : E216 21.
74. 2+-dependent enzyme. Methods Enzymol. 1988 159 : 416 26.
75. McGowan CH, Cohen P. Identification of two isoenzymes of protein phosphatase 2C in both rabbit skeletal muscle and liver. Eur. J. Biochem. 1987 166 : 713 21.
76. 2+: Stimulation by unsaturated fatty acids. FEBS Lett. 1998 437 : 229 32.
77. Lifschitz-Mercer B, Sheinin Y, Ben-Meir D et al. Protein phosphatase 2Calpha expression in normal human tissues: An immunohistochemical study. Histochem. Cell Biol. 2001 116 : 31 9.
78. Marley AE, Sullivan JE, Carling D et al. Biochemical characterization and deletion analysis of recombinant human protein phosphatase 2C alpha. Biochem. J. 1996 320 : 801 6.
79. Dobrowsky RT, Kamibayashi C, Mumby MC, Hannun YA. Ceramide activates heterotrimeric protein phosphatase 2A. J. Biol. Chem. 1993 268 : 15 523 30.
80. Gabel S, Benefield J, Meisinger J, Petruzzelli GJ, Young M. Protein phosphatases 1 and 2A maintain endothelial cells in a resting state, limiting the motility that is needed for the morphogenic process of angiogenesis. Otolaryngol. Head Neck Surg. 1999 121 : 463 8.
81. Tar K, Csortos C, Czikora I et al. Role of protein phosphatase 2A in the regulation of endothelial cell cytoskeleton structure. J. Cell Biochem. 2006 98 : 931 53.
82. Urbich C, Reissner A, Chavakis E et al. Dephosphorylation of endothelial nitric oxide synthase contributes to the anti-angiogenic effects of endostatin. FASEB J. 2002 16 : 706 8.
83. Gimeno-Alcaniz JV, Sanz P. Glucose and type 2A protein phosphatase regulate the interaction between catalytic and regulatory subunits of AMP-activated protein kinase. J. Mol. Biol. 2003 333 : 201 9.
84. Ravnskjaer K, Boergesen M, Dalgaard LT, Mandrup S. Glucose-induced repression of PPARalpha gene expression in pancreatic beta-cells involves PP2A activation and AMPK inactivation. J. Mol. Endocrinol. 2006 36 : 289 99.
85. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: From marvel to menace. Circulation 2006 113 : 1708 14.
86. Stuehr DJ. Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1999 1411 : 217 30.
87. Kawashima S, Yokoyama M. Dysfunction of endothelial nitric oxide synthase and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2004 24 : 998 1005.
88. Jeremy JY, Rowe D, Emsley AM, Newby AC. Nitric oxide and the proliferation of vascular smooth muscle cells. Cardiovasc. Res. 1999 43 : 580 94.
89. Napoli C, de Nigris F, Palinski W. Multiple role of reactive oxygen species in the arterial wall. J. Cell Biochem. 2001 82 : 674 82.
90. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am. J. Physiol. Cell Physiol. 2001 280 : C719 41.
91. Ugochukwu NH, Figgers CL. Attenuation of plasma dyslipidemia and oxidative damage by dietary caloric restriction in streptozotocin-induced diabetic rats. Chem. Biol. Interact. 2007 169 : 32 41.
92. Kitayama J, Faraci FM, Lentz SR, Heistad DD. Cerebral vascular dysfunction during hypercholesterolemia. Stroke 2007 38 : 2136 41.
93. Xu J, Xie Z, Reece R, Pimental D, Zou MH. Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: Role of NAD(P)H oxidase-derived superoxide and peroxynitrite. Arterioscler. Thromb. Vasc. Biol. 2006 26 : 2688 95.
94. Xu J, Wu Y, Song P, Zhang M, Wang S, Zou MH. Proteasome-dependent degradation of guanosine 5′-triphosphate cyclohydrolase I causes tetrahydrobiopterin deficiency in diabetes mellitus. Circulation 2007 116 : 944 53.
95. Ouslimani N, Peynet J, Bonnefont-Rousselot D, Therond P, Legrand A, Beaudeux JL. Metformin decreases intracellular production of reactive oxygen species in aortic endothelial cells. Metabolism 2005 54 : 829 34.
96. Kukidome D, Nishikawa T, Sonoda K et al. Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells. Diabetes 2006 55 : 120 7.
97. 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 82.
98. 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 6.
99. Lee TS, Saltsman KA, Ohashi H, King GL. Activation of protein kinase C by elevation of glucose concentration: Proposal for a mechanism in the development of diabetic vascular complications. Proc. Natl Acad. Sci. USA 1989 86 : 5141 5.
100. Michell BJ, Chen Z, Tiganis T et al. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem. 2001 276 : 17 625 8.
101. Park JY, Kim YM, Song HS et al. Oleic acid induces endothelin-1 expression through activation of protein kinase C and NF-kappa B. Biochem. Biophys. Res. Commun. 2003 303 : 891 5.
102. Lee WJ, Lee IK, Kim HS et al. Alpha-lipoic acid prevents endothelial dysfunction in obese rats via activation of AMP-activated protein kinase. Arterioscler. Thromb. Vasc. Biol. 2005 25 : 2488 94.
103. Clark H, Carling D, Saggerson D. Covalent activation of heart AMP-activated protein kinase in response to physiological concentrations of long-chain fatty acids. Eur. J. Biochem. 2004 271 : 2215 24.
104. Suchankova G, Tekle M, Saha AK, Ruderman NB, Clarke SD, Gettys TW. Dietary polyunsaturated fatty acids enhance hepatic AMP-activated protein kinase activity in rats. Biochem. Biophys. Res. Commun. 2005 326 : 851 8.
105. Kelley DE, Simoneau JA. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J. Clin. Invest. 1994 94 : 2349 56.
106. Muse ED, Obici S, Bhanot S et al. Role of resistin in diet-induced hepatic insulin resistance. J. Clin. Invest. 2004 114 : 232 9.
107. Wilkes JJ, Nguyen MT, Bandyopadhyay GK, Nelson E, Olefsky JM. Topiramate treatment causes skeletal muscle insulin sensitization and increased Acrp30 secretion in high-fat-fed male Wistar rats. Am. J. Physiol. Endocrinol. Metab. 2005 289 : E1015 22.
108. McCarty MF. AMPK activation as a strategy for reversing the endothelial lipotoxicity underlying the increased vascular risk associated with insulin resistance syndrome. Med. Hypotheses 2005 64 : 1211 15.
109. Chen H, Montagnani M, Funahashi T, Shimomura I, Quon MJ. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J. Biol. Chem. 2003 278 : 45 021 6.
110. Park H, Kaushik VK, Constant S et al. Coordinate regulation of malonyl-CoA decarboxylase, sn-glycerol-3-phosphate acyltransferase, and acetyl-CoA carboxylase by AMP-activated protein kinase in rat tissues in response to exercise. J. Biol. Chem. 2002 277 : 32 571 7.
111. Kobayashi H, Ouchi N, Kihara S, Ruderman NB, Ido Y. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ. Res. 2004 94 : E27 31.
112. Cacicedo JM, Yagihashi N, Keaney Jr. JF, Ruderman NB, Ido Y. AMPK inhibits fatty acid-induced increases in NF-kappaB transactivation in cultured human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 2004 324 : 1204 9.
113. Hattori Y, Suzuki K, Hattori S, Kasai K. Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells. Hypertension 2006 47 : 1183 8.