Berberine prevents hyperglycemia-induced endothelial injury and enhances vasodilatation via adenosine monophosphate-activated protein kinase and endothelial nitric oxide synthase

Cardiovascular Research

Volumn 82, Issue 3, 2009, Pages 484-492

  Wang, Yiqun ^a   Huang, Yu ^c   Lam, Karen S L ^a,b   Li, Yiming ^d   Wong, Wing Tak ^c   Ye, Hongying ^d   Lau, Chi Wai ^c   Vanhoutte, Paul M ^a,b   Xu, Aimin ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d FUDAN UNIVERSITY   (China)

Author keywords

Endothelium; Hyperglycemia; Nitric oxide; Oxidative stress; Vascular injury

Indexed keywords

BERBERINE; CELL ADHESION MOLECULE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEAT SHOCK PROTEIN 90; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; SERINE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL CULTURE; CELL PROTECTION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM INJURY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VASCULAR RING; VASODILATATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AORTA; APOPTOSIS; BERBERINE; CELL ADHESION; CELL LINE; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; HYPERGLYCEMIA; MALE; MONOCYTES; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; VASODILATION;

EID: 66249092436     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp078     Document Type: Article

References (44)

1. Feletou M, Vanhoutte PM. Endothelial dysfunction: a multifaceted disorder. Am J Physiol Heart Circ Physiol 2006;291:H985-H1002.
2. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 2006;113:1708-1714.
3. Huang PL. Endothelial nitric oxide synthase and endothelial dysfunction. Curr Hypertens Rep 2003;5:473-480.
4. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 2006;113:1888-1904.
5. Rask-Madsen C, King GL Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 2007; 3:46-56.
6. Zhang Y, Li X, Zou D, Liu W, Yang J, Zhu N et al. Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J Clin Endocrinol Metab 2008;93:2559-2565.
7. Turner N, Li JY, Gosby A, To SW, Cheng Z, Miyoshi H et al. Berberine and its more biologically available derivative, dihydroberberine, inhibit mitochondrial respiratory complex I: a mechanism for the action of berberine to activate AMP-activated protein kinase and improve insulin action. Diabetes 2008;57:1414-1418.
8. Yin J, Gao Z, Liu D, Liu Z, Ye J. Berberine improves glucose metabolism through induction of glycolysis. Am J Physiol Endocrinol Metab 2008; 294:E148-E156.
9. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y et al. Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 2006;55:2256-2264.
10. Zeng XH, Zeng XJ, Li YY. Efficacy and safety of berberine for congestive heart failure secondary to ischaemic or idiopathic dilated cardiomyopa-thy. Am J Cardiol 2003;92:173-176.
11. Marin-Neto JA, Maciel BC, Secches AL, Gallo Junior L. Cardiovascular effects of berberine in patients with severe congestive heart failure. Clin Cardiol 1988;11:253-260.
12. Xu MG, Wang JM, Chen L, Wang Y, Yang Z, Tao J. Berberine-induced mobilization of circulating endothelial progenitor cells improves human small artery elasticity. J Hum Hypertens 2008;22:389-393.
13. Liu JC, Chan P, Chen YJ, Tomlinson B, Hong SH, Cheng JT. The antihypertensive effect of the berberine derivative 6-protoberberine in spontaneously hypertensive rats. Pharmacology 1999;59:283-289.
14. Lee S, Lim HJ, Park HY, Lee KS, Park JH, Jang Y. Berberine inhibits rat vascular smooth muscle cell proliferation and migration in vitro and improves neointima formation after balloon injury in vivo. Berberine improves neointima formation in a rat model. Atherosclerosis 2006; 186:29-37.
15. Cheng KK, Lam KS, Wang Y, Huang Y, Carling D, Wu D et al. Adiponectin-induced endothelial nitric oxide synthase activation and nitric oxide production are mediated by APPL1 in endothelial cells. Diabetes 2007;56:1387-1394.
16. Bhunia AK, Arai T, Bulkley G, Chatterjee S. Lactosylceramide mediates tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 (ICAM-1) expression and the adhesion of neutrophil in human umbilical vein endothelial cells. J Biol Chem 1998;273:34349-34357.
17. Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol 2006; 42:271-279.
18. Ko WH, Yao XQ, Lau CW, Law WI, Chen ZY, Kwok W et al. Vasorelaxant and antiproliferative effects of berberine. Eur J Pharmacol 2000;399: 187-196.
19. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, Depinho RA et al. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 2005;310:1642-1646.
20. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001;108:1167-1174.
21. Zou MH, Wu Y. AMP-activated protein kinase activation as a strategy for protecting vascular endothelial function. Clin Exp Pharmacol Physiol 2008;35:535-545.
22. Sun W, Lee TS, Zhu M, Gu C, Wang Y, Zhu Y et al. Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 2006; 114:2655-2662.
23. Zang M, Xu S, Maitland-Toolan KA, Zuccollo A, Hou X, Jiang B et al. Polyphenols stimulate AMP-activated protein kinase, lower lipids, and inhibit accelerated atherosclerosis in diabetic LDL receptor-deficient mice. Diabetes 2006;55:2180-2191.
24. 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.
25. LeBrasseur NK, Kelly M, Tsao TS, Farmer SR, Saha AK, Ruderman NB et al. Thiazolidinediones can rapidly activate AMP-activated protein kinase in mammalian tissues. Am J Physiol Endocrinol Metab 2006;291 :E175-E181.
26. Murakami H, Murakami R, Kambe F, Cao X, Takahashi R, Asai T et al. Fenofibrate activates AMPK and increases eNOS phosphorylation in HUVEC. Biochem Biophys Res Commun 2006;341:973-978.
27. 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: 3473-3480.
28. Lee WJ, Lee IK, Kim HS, Kim YM, Koh EH, Won JC et al. Alpha-lipoic acid prevents endothelial dysfunction in obese rats via activation of AMP-activated protein kinase. Arterioscler Thromb Vasc Biol 2005;25: 2488-2494.
29. Drew BG, Fidge NH, Gallon-Beaumier G, Kemp BE, Kingwell BA. High-density lipoprotein and apolipoprotein AI increase endothelial NO synthase activity by protein association and multisite phosphorylation. Proc Natl Acad Sci USA 2004;101:6999-7004.
30. Chen H, Montagnani M, Funahashi T, Shimomura I, Quon MJ. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem 2003;278:45021-45026.
31. Kobayashi H, Ouchi N, Kihara S, Walsh K, Kumada M, Abe Y et al. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ Res 2004;94:e27-e31.
32. Levine YC, Li GK, Michel T. Agonist-modulated regulation of AMP-activated protein kinase (AMPK) in endothelial cells. Evidence for an AMPK → Rad → Akt → endothelial nitric-oxide synthase pathway. J Biol Chem 2007;282:20351-20364.
33. Reihill JA, Ewart MA, Hardie DG, Salt IP. AMP-activated protein kinase mediates VEGF-stimulated endothelial NO production. Biochem Biophys Res Commun 2007;354:1084-1088.
34. Kukidome D, Nishikawa T, Sonoda K, Imoto K, Fujisawa K, Yano M 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;55:120-127.
35. Ceolotto G, Gallo A, Papparella I, Franco L, Murphy E, Iori E et al. Rosi-glitazone reduces glucose-induced oxidative stress mediated by NAD(P)H oxidase via AMPK-dependent mechanism. Arterioscler Thromb Vasc Biol 2007;27:2627-2633.
36. 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;64:1211-1215.
37. 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;47:1183-1188.
38. 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;51:159-167.
39. Mattiasson G, Sullivan PG. The emerging functions of UCP2 in health, disease, and therapeutics. Antioxid Redox Signal 2006;8:1-38.
40. Xie Z, Zhang J, Wu J, Viollet B, Zou MH. Up-regulation of mitochondrial uncoupling protein-2 by the AMP-activated protein kinase in endothelial cells attenuates oxidative stress in diabetes. Diabetes 2008;57: 3222-3330.
41. Zou MH, Kirkpatrick SS, Davis BJ, Nelson JS, Wiles WG, Schlattner U 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;279:43940-43951.
42. Boyle JG, Logan PJ, Ewart MA, Reihill JA, Ritchie SA, Connell JM et al. Rosiglitazone stimulates nitric oxide synthesis in human aortic endothelial cells via AMP-activated protein kinase. J Biol Chem 2008;283: 11210-11217.
43. Sukhodub A, Jovanovic S, Du Q, Budas G, Clelland AK, Shen M et al. AMP-activated protein kinase mediates preconditioning in cardiomyo-cytes by regulating activity and trafficking of sarcolemmal ATP-sensitive K(p) channels. J Cell Physiol 2007;210:224-236.
44. Kong W, Wei J, Abidi P, Lin M, Inaba S, Li C et al. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 2004;10:1344-1351.