Metformin improves endothelial function in aortic tissue and microvascular endothelial cells subjected to diabetic hyperglycaemic conditions

Biochemical Pharmacology

Volumn 98, Issue 3, 2015, Pages 412-421

  Ghosh, Suparna ^a   Lakshmanan, Arun P ^a   Hwang, Mu Ji ^a   Kubba, Haidar ^a   Mushannen, Ahmed ^a   Triggle, Chris R ^a   Ding, Hong ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (Qatar)

Author keywords

Akt; Aorta; Diabetes; Endothelial cells; eNOS; Metformin

Indexed keywords

ADENYLATE KINASE; BETA ACTIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; INSULIN; METFORMIN; PROTEIN KINASE B; SIRTUIN 1; SMALL INTERFERING RNA; ANTIDIABETIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDIABETIC ACTIVITY; AORTIC TISSUE; ARTICLE; BODY WEIGHT; CAPILLARY ENDOTHELIAL CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; EC50; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; INSULIN TREATMENT; INTRACELLULAR SIGNALING; MALE; MOUSE; MYOGRAPHY; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; THORACIC AORTA; VASCULAR ENDOTHELIUM; VASCULAR RING; VASODILATATION; ANIMAL; AORTA; C57BL MOUSE; COMPLICATION; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENE SILENCING; GENETICS; METABOLISM; MICROVASCULATURE; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION;

ADENYLATE KINASE; ANIMALS; AORTA; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; GENE KNOCKDOWN TECHNIQUES; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; INSULIN; METFORMIN; MICE; MICE, INBRED C57BL; MICROVESSELS; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION;

EID: 84946559701     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2015.10.008     Document Type: Article

References (44)

1. S.M. Grundy, B. Howard, S. Smith Jr., R. Eckel, R. Redberg, and R.O. Bonow Prevention conference VI: diabetes and cardiovascular disease: executive summary conference proceeding for healthcare professionals from a special writing group of the American Heart Association Circulation 105 2002 2231 2239
2. DCCT: The Diabetes Control and Complications Trial Research Group The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus N. Engl. J. Med. 329 1993 977 986
3. UKPDS 28: a randomized trial of efficacy of early addition of metformin in sulfonylurea-treated type 2 diabetes, U.K. Prospective Diabetes Study Group, Diabetes Care, 21 (1998) 87-92.
4. H. Ding, and C.R. Triggle Glycaemic control and protection of the vasculature from glucose toxicity C. Croniger, Medical Complications of Type 2 Diabetes vol. 6 2011 InTech - Open Access Publisher 87 110
5. M. Coutinho, H.C. Gerstein, Y. Wang, and S. Yusuf The relationship between glucose and incident cardiovascular events. A metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years Diabetes Care 22 1999 233 240
6. S. Verma, and T.J. Anderson Fundamentals of endothelial function for the clinical cardiologist Circulation 105 2002 546 549
7. M. Pannirselvam, S. Verma, T.J. Anderson, and C.R. Triggle Cellular basis of endothelial dysfunction in small mesenteric arteries from spontaneously diabetic (db/db-/-) mice: role of decreased tetrahydrobiopterin bioavailability Br. J. Pharmacol. 136 2002 255 263
8. S. Verma, F. Lovren, A.S. Dumont, K.J. Mather, A. Maitland, T.M. Kieser, C.R. Triggle, and T.J. Anderson Tetrahydrobiopterin improves endothelial function in human saphenous veins J. Thorac. Cardiovasc. Surg. 120 2000 668 671
9. C.R. Triggle, and H. Ding A review of endothelial dysfunction in diabetes: a focus on the contribution of a dysfunctional eNOS J. Am. Soc. Hypertens. 4 2010 102 115
10. E. Bosi Metformin - the gold standard in type 2 diabetes: what does the evidence tell us Diabetes Obes. Metab. 2 Suppl 2009 3 8
11. M. Kinaan, H. Ding, and C.R. Triggle Metformin: an old drug for the treatment of diabetes but a new drug for the protection of the endothelium Med. Princ. Pract. 24 2015 401 415
12. K.J. Mather, S. Verma, and T.J. Anderson Improved endothelial function with metformin in type 2 diabetes mellitus J. Am. Coll. Cardiol. 375 2001 1344 1350
13. C. Vitale, G. Mercuro, A. Cornoldi, M. Fini, M. Volterrani, and G.M. Rosano Metformin improves endothelial function in patients with metabolic syndrome J. Intern. Med. 258 2005 250 256
14. M.P. De Boer, R.I. Meijer, N.J. Wijnstok, A.M. Jonk, A.J. Houben, C.D. Stehouwer, Y.M. Smulders, E.C. Eringa, and E.H. Serné Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension Microcirculation 19 2012 5 18
15. H. Ding, M. Aljofan, and C.R. Triggle Oxidative stress and increased eNOS and NADPH oxidase expression in mouse microvessel endothelial cells J. Cell. Physiol. 212 2007 682 689
16. M. Aljofan, and H. Ding High glucose increases expression of cyclooxygenase-2, increases oxidative stress and decreases the generation of nitric oxide in mouse microvessel endothelial cells J. Cell. Physiol. 222 2010 669 675
17. A.K. Madiraju, D.M. Erion, Y. Rahimi, X.M. Zhang, D.T. Braddock, R.A. Albright, B.J. Prigaro, J.L. Wood, S. Bhanot, M.J. MacDonald, M.J. Jurczak, J.P. Camporez, H.Y. Lee, G.W. Cline, V.T. Samuel, R.G. Kibbey, and G.I. Shulman Metformin suppresses gluconeogenesis by inhibiting mitochondrial glycerophosphate dehydrogenase Nature 510 2014 542 546
18. C.R. Triggle, and H. Ding Cardiovascular impact of drugs used in the treatment of diabetes Ther. Adv. Chronic Dis. 5 2014 245 268
19. G. Arunachalam, S.M. Samuel, I. Marei, H. Ding, and C.R. Triggle Metformin modulates hyperglycaemia-induced endothelial senescence and apoptosis through SIRT1 Br. J. Pharmacol. 171 2014 523 535
20. I. Mattagajasingh, C.S. Kim, A. Naqvi, T. Yamamori, T.A. Hoffman, S.B. Jung, J. DeRicco, K. Kasuno, and K. Irani SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase Proc. Natl. Acad. Sci. U. S. A. 104 2007 14855 14860
21. G.T. Tucker, C. Casey, P.J. Phillips, H. Connor, J.D. Ward, and H.F. Woods Metformin kinetics in healthy subjects and in patients with diabetes mellitus Br. J. Clin. Pharmacol. 12 1981 235 246
22. P.V. Katakam, M.R. Ujhelyi, M. Hoenig, and A.W. Miller Metformin improves vascular function in insulin-resistant rats Hypertension 35 2000 108 112
23. H. Kawano, T. Motoyama, O. Hirashima, N. Hirai, Y. Miyao, T. Sakamoto, K. Kugiyama, H. Ogawa, and H. Yasue Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery J. Am. Coll. Cardiol. 34 1999 146 154
24. N. Ihlemann, C. Rask-Madsen, A. Perner, H. Dominguez, T. Hermann, L. Køber, and C. Torp-Pedersen Tetrahydrobiopterin restores endothelial dysfunction induced by an oral glucose challenge in healthy subjects Am. J. Physiol. Heart Circ. Physiol. 285 2003 H875 H882
25. T.X. Zhang, J.X. Xu, F. Peng, D.J. Chai, and J.X. Lin Metformin reduces vascular endothelial dysfunction caused by an acute glucose load in patients with hypertension Blood Press. 22 2013 106 113
26. G.J. Waldron, H. Ding, F. Lovren, P. Kubes, and C.R. Triggle Acetylcholine-induced relaxation of peripheral arteries isolated from mice lacking endothelial nitric oxide synthase Br. J. Pharmacol. 128 1999 653 658
27. A. El-Osta, D. Brasacchio, D. Yao, A. Pocai, P.L. Jones, R.G. Roeder, M.E. Cooper, and M. Brownlee Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia J. Exp. Med. 205 2008 2409 2417
28. S. Dimmeler, I. Fleming, B. Fisslthaler, C. Hermann, R. Busse, and A.M. Zeiher Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation Nature 399 6736 1999 601 605
29. B.D. Manning, and L.C. Cantley AKT/PKB signaling: navigating downstream Cell 129 2007 1261 1274
30. D.D. Sarbassov, D.A. Guertin, S.M. Ali, and D.M. Sabatini Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 2005 1098 1101
31. B.C. Melnik, and G. Scmitz Metformin: an inhibitor of mTOC1 signaling J. Endocrinol. Diabetes Obes. 2 2 2014 1029
32. J. Li, Z. Xu, L. Jiang, J. Mao, Z. Zeng, L. Fang, W. He, W. Yuan, J. Yang, and C. Dai Rictor/mTORC2 protects against cisplatin-induced tubular cell death and acute kidney injury Kidney Int. 86 2014 86 102
33. M.Y. El-Mir, V. Nogueira, E. Fontaine, N. Avéret, M. Rigoulet, and X. Leverve Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I J. Biol. Chem. 275 2000 223 228
34. M.R. Owen, E. Doran, and A.P. Halestrap Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain Biochem. J. 348 2000 607 614
35. S. Schuhmacher, E. Schulz, M. Hortmann, P. Wenzel, M. Oelze, A. Daiber, and H. Munzel Knockout of vascular AMPK leads to increased mitochondrial stress and decreased vasodilator sensitivity towards organic nitrates Circulation 2007 116 II-26. Abstract 233
36. S.L. Colombo, and S. Moncada AMPKalpha1 regulates the antioxidant status of vascular endothelial cells Biochem. J. 42 2009 163 169
37. D. Pitocco, F. Zaccardi, P. Tarzia, M. Milo, G. Scavone, P. Rizzo, F. Pagliaccia, R. Nerla, A. Di Franco, A. Manto, B. Rocca, G.A. Lanza, F. Crea, and G. Ghirlanda Metformin improves endothelial function in type 1 diabetic subjects: a pilot, placebo-controlled randomized study Diabetes Obes. Metab. 15 2013 427 431
38. W.S. Cheang, X.Y. Tian, W.T. Wong, C.W. Lau, S.S. Lee, Z.Y. Chen, X. Yao, N. Wang, and Y. Huang Metformin protects endothelial function in diet-induced obese mice by inhibition of endoplasmic reticulum stress through 5′ adenosine monophosphate-activated protein kinase-peroxisome proliferator-activated receptor δ pathway Arterioscler. Thromb. Vasc. Biol. 34 2014 830 836
39. G. Zhou, R. Myers, Y. Li, Y. Chen, X. Shen, J. Fenyk-Melody, M. Wu, J. Ventre, T. Doebber, N. Fujii, N. Musi, M.F. Hirshman, L.J. Goodyear, and D.E. Moller Role of AMP-activated protein kinase in mechanism of metformin action J. Clin. Investig. 108 2001 1167 1174
40. M. Foretz, S. Hébrard, J. Leclerc, E. Zarrinpashneh, M. Soty, G. Mithieux, K. Sakamoto, F. Andreelli, and B. Viollet Metformin inhibits hepatic gluconeogenesis in mice independently of the LKB1/AMPK pathway via a decrease in hepatic energy state J. Clin. Investig. 120 2010 2355 2369
41. H. Shimokawa, H. Yasutake, K. Fujii, M.K. Owada, R. Nakaike, Y. Fukumoto, T. Takayanagi, T. Nagao, K. Egashira, M. Fujishima, and A. Takeshita The importance of the hyperpolarizing mechanism increases as the vessel size decreases in endothelium-dependent relaxations in rat mesenteric circulation J. Cardiovasc. Pharmacol. 28 1996 703 711
42. M. Pannirselvam, S. Verma, T.J. Anderson, and C.R. Triggle Cellular basis of endothelial dysfunction in small mesenteric arteries from spontaneously diabetic (db/db-/-) mice: role of decreased tetrahydrobiopterin bioavailability Br. J. Pharmacol. 136 2002 255 263
43. D.G. Hardie AMPK - sensing energy while talking to other signaling pathways Cell Metab. 20 2014 939 952
44. M.J. Mulvany, and W. Halpern Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normaotensive rats Circ. Res. 41 1977 19 26