Puerarin activates endothelial nitric oxide synthase through estrogen receptor-dependent PI3-kinase and calcium-dependent AMP-activated protein kinase

Toxicology and Applied Pharmacology

Volumn 257, Issue 1, 2011, Pages 48-58

  Hwang, Yong Pil ^a   Kim, Hyung Gyun ^a   Hien, Tran Thi ^b   Jeong, Myung Ho ^c   Jeong, Tae Cheon ^d   Jeong, Hye Gwang ^a  

^a Chungnam National University   (South Korea)

^b Chosun University   (South Korea)

^c Chonnam National University Medical School   (South Korea)

^d Yeungnam University   (South Korea)

Author keywords

AMPK; CaMKII; ENOS; PI3K Akt; Puerarin

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTROGEN RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PUERARIN; SERINE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ATTENUATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; INHIBITION KINETICS; INTRACELLULAR SIGNALING; MONOCYTE;

BLOTTING, WESTERN; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE KINASE; CELL LINE; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; ISOFLAVONES; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 81255176611     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.08.017     Document Type: Article

References (58)

1. Atochin D.N., Huang P.L. Endothelial nitric oxide synthase transgenic models of endothelial dysfunction. Pflugers Arch. 2010, 460:965-974.
2. Boué S.M., Wiese T.E., Nehls S., Burow M.E., Elliott S., Carter-Wientjes C.H. Evaluation of the estrogenic effects of legume extracts containing phytoestrogens. J. Agric. Food Chem. 2003, 51:2193-2199.
3. Busse R., Mulsch A. Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Lett. 1990, 265:133-136.
4. Cai H., Liu D., Garcia J.G. CaM Kinase II-dependent pathophysiological signalling in endothelial cells. Cardiovasc. Res. 2008, 77:30-34.
5. Calvert J.W., Gundewar S., Jha S., Greer J.J., Bestermann W.H., Tian R., Lefer D.J. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes 2008, 57:696-705.
6. Chambliss K.L., Shaul P.W. Estrogen modulation of endothelial nitric oxide synthase. Endocr. Rev. 2002, 23:665-686.
7. Chen Z., Peng I.C., Sun W., Su M.I., Hsu P.H., Fu Y., Zhu Y., DeFea K., Pan S., Tsai M.D., Shyy J.Y. AMP-activated protein kinase functionally phosphorylates endothelial nitric oxide synthase Ser633. Circ. Res. 2009, 104:496-505.
8. Chen Z.P., Mitchelhill K.I., Michell B.J., Stapleton D., Rodriguez-Crespo I., Witters L.A., Power D.A., Ortiz de Montellano P.R., Kemp B.E. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999, 443:285-289.
9. Chi Z., Melendez A.J. Role of cell adhesion molecules and immune-cell migration in the initiation, onset and development of atherosclerosis. Cell Adh. Migr. 2007, 1:171-175.
10. Chueh F.S., Chang C.P., Chio C.C., Lin M.T. Puerarin acts through brain serotonergic mechanisms to induce thermal effects. J. Pharmacol. Sci. 2004, 96:420-427.
11. Chung H.T., Pae H.O., Cha Y.N. Role of heme oxygenase-1 in vascular disease. Curr. Pharm. Des. 2008, 14:422-428.
12. De Caterina R., Libby P., Peng H.B., Thannickal V.J., Rajavashisth T.B., Gimbrone M.A., Shin W.S., Liao J.K. Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J. Clin. Investig. 1995, 96:60-68.
13. Matsushita K., Morrell C.N., Cambien B., Yang S.X., Yamakuchi M., Bao C., Hara M.R., Quick R.A., Cao W., O'Rourke B., Lowenstein J.M., Pevsner J., Wagner D.D., Lowenstein C.J. Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor. Cell 2003, 115:139-150.
14. Fang Q. Some current study and research approaches relating to the use of plants in the traditional Chinese medicine. J. Ethnopharmacol. 1980, 2:57-63.
15. Feng Z.Q., Wang Y.Y., Guo Z.R., Chu F.M., Sun P.Y. The synthesis of puerarin derivatives and their protective effect on the myocardial ischemia and reperfusion injury. J. Asian Nat. Prod. Res. 2010, 12:843-850.
16. Fisslthaler B., Fleming I. Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ. Res. 2009, 105:114-127.
17. Formoso G., Chen H., Kim J.A., Montagnani M., Consoli A., Quon M.J. Dehydroepiandrosterone mimics acute actions of insulin to stimulate production of both nitric oxide and endothelin 1 via distinct phosphatidylinositol 3-kinase- and mitogen-activated protein kinase-dependent pathways in vascular endothelium. Mol. Endocrinol. 2006, 20:1153-1163.
18. Fulton D., Gratton J.P., McCabe T.J., Fontana J., Fujio Y., Walsh K., Franke T.F., Papapetropoulos A., Sessa W.C. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999, 399:597-601.
19. Gao Q., Yang B., Ye Z.G., Wang J., Bruce I.C., Xia Q. Opening the calcium-activated potassium channel participates in the cardioprotective effect of puerarin. Eur. J. Pharmacol. 2007, 574:179-184.
20. Grossini E., Molinari C., Caimmi P.P., Uberti F., Vacca G. Levosimendan induces NO production through p38 MAPK, ERK and Akt in porcine coronary endothelial cells: role for mitochondrial K(ATP) channel. Br. J. Pharmacol. 2009, 156:250-261.
21. Hattori Y., Kasai K., Gross S.S. NO suppresses while peroxynitrite sustains NF-kappaB: a paradigm to rationalize cytoprotective and cytotoxic actions attributed to NO. Cardiovasc. Res. 2004, 63:31-40.
22. Hien T.T., Kim H.G., Han E.H., Kang K.W., Jeong H.G. Molecular mechanism of suppression of MDR1 by puerarin from Pueraria lobata via NF-kappaB pathway and cAMP-responsive element transcriptional activity-dependent up-regulation of AMP-activated protein kinase in breast cancer MCF-7/adr cells. Mol. Nutr. Food Res. 2010, 54:918-928.
23. Hsu F.L., Liu I.M., Kuo D.H., Chen W.C., Su H.C., Cheng J.T. Antihyperglycemic effect of puerarin in streptozotocin-induced diabetic rats. J. Nat. Prod. 2003, 66:788-792.
24. Hu W., Zhang Q., Yang X., Wang Y., Sun L. Puerarin inhibits adhesion molecule expression in tnf-alpha-stimulated human endothelial cells via modulation of the nuclear factor kappaB pathway. Pharmacology 2010, 85:27-35.
25. 2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 2005, 280:29060-29066.
26. Hwang Y.P., Choi C.Y., Chung Y.C., Jeon S.S., Jeong H.G. Protective effects of puerarin on carbon tetrachloride-induced hepatotoxicity. Arch. Pharm. Res. 2007, 30:1309-1317.
27. Hwang Y.P., Jeong H.G. Mechanism of phytoestrogen puerarin-mediated cytoprotection following oxidative injury: estrogen receptor-dependent up-regulation of PI3K/Akt and HO-1. Toxicol. Appl. Pharmacol. 2008, 233:371-381.
28. Johnson M.R., Wang K., Smith J.B., Heslin M.J., Diasio R.B. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal. Biochem. 2000, 278:175-184.
29. Kim K.H., Moriarty K., Bender J.R. Vascular cell signaling by membrane estrogen receptors. Steroids 2008, 73:864-869.
30. Kim K.M., Jung D.H., Jang D.S., Kim Y.S., Kim J.M., Kim H.N., Surh Y.J., Kim J.S. Puerarin suppresses AGEs-induced inflammation in mouse mesangial cells: a possible pathway through the induction of heme oxygenase-1 expression. Toxicol. Appl. Pharmacol. 2010, 244:106-113.
31. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg B., Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
32. Lee M., Hwang J.T., Lee H.J., Jung S.N., Kang I., Chi S.G., Kim S.S., Ha J. 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.
33. Leikert J.F., Rathel T.R., Muller C., Vollmar A.M., Dirsch V.M. Reliable in vitro measurement of nitric oxide released from endothelial cells using low concentrations of the fluorescent probe 4,5-diaminofluorescein. FEBS Lett. 2001, 506:131-134.
34. Martin D., Song J., Mark C., Eyster K. Understanding the cardiovascular actions of soy isoflavones: potential novel targets for antihypertensive drug development. Cardiovasc. Hematol. Disord. Drug Targets 2008, 8:297-312.
35. Meezan E., Meezan E.M., Jones K., Moore R., Barnes S., Prasain J.K. Contrasting effects of puerarin and daidzin on glucose homeostasis in mice. J. Agric. Food Chem. 2005, 53:8760-8767.
36. Meng X.H., Ni C., Zhu L., Shen Y.L., Wang L.L., Chen Y.Y. Puerarin protects against high glucose-induced acute vascular dysfunction: role of heme oxygenase-1 in rat thoracic aorta. Vascul. Pharmacol. 2009, 50:110-115.
37. Michel T., Vanhoutte P.M. Cellular signaling and NO production. Pflugers Arch. 2010, 459:807-816.
38. Michell B.J., Chen Z.P., Tiganis T., Stapleton D., Katsis F., Power D.A., Sim A.T., Kemp B.E. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem. 2001, 276:17625-17628.
39. Morrow V.A., Foufelle F., Connell J.M., Petrie J.R., Gould G.W., Salt I.P. Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. J. Biol. Chem. 2003, 278:31629-31639.
40. Murphy E., Steenbergen C. Cardioprotection in females: a role for nitric oxide and altered gene expression. Heart Fail. Rev. 2007, 12:293-300.
41. Namkoong S., Kim C.K., Cho Y.L., Kim J.H., Lee H., Ha K.S., Choe J., Kim P.H., Won M.H., Kwon Y.G., Shim E.B., Kim Y.M. Forskolin increases angiogenesis through the coordinated cross-talk of PKA-dependent VEGF expression and Epac-mediated PI3K/Akt/eNOS signaling. Cell. Signal. 2009, 21:906-915.
42. Napoli C., de Nigris F., Williams-Ignarro S., Pignalosa O., Sica V., Ignarro L.J. Nitric oxide and atherosclerosis: an update. Nitric Oxide 2006, 15:265-279.
43. Otani H. The role of nitric oxide in myocardial repair and remodeling. Antioxid. Redox Signal. 2009, 11:1913-1928.
44. Peterson S.J., Frishman W.H., Abraham N.G. Targeting heme oxygenase: therapeutic implications for diseases of the cardiovascular system. Cardiol. Rev. 2009, 17:99-111.
45. Sessa W. Regulation of endothelial derived nitric oxide in health and disease. Mem. Inst. Oswaldo Cruz 2005, 100(Suppl 1):15-18.
46. Shiojima I., Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 2002, 90:1243-1250.
47. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., Liao J. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 2000, 407:538-541.
48. Vanhoutte P.M., Shimokawa H., Tang E.H., Feletou M. Endothelial dysfunction and vascular disease. Acta Physiol (Oxf.) 2009, 196:193-222.
49. Viollet B., Mounier R., Leclerc J., Yazigi A., Foretz M., Andreelli F. Targeting AMP-activated protein kinase as a novel therapeutic approach for the treatment of metabolic disorders. Diabetes Metab. 2007, 33:395-402.
50. 2+/calmodulin-dependent protein kinase kinase-β acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab. 2005, 2:21-33.
51. Wu B., Liu M., Liu H., Li W., Tan S., Zhang S., Fang Y. Meta-analysis of traditional Chinese patent medicine for ischemic stroke. Stroke 2007, 38:1973-1979.
52. Wyckoff M.H., Chambliss K.L., Mineo C., Yuhanna I.S., Mendelsohn M.E., Mumby S.M., Shaul P.W. Plasma membrane estrogen receptors are coupled to endothelial nitricoxide synthase through Galpha(i). J. Biol. Chem. 2001, 276:27071-27076.
53. Xiong F.L., Sun X.H., Gan L., Yang X.L., Xu H.B. Puerarin protects rat pancreatic islets from damage by hydrogen peroxide. Eur. J. Pharmacol. 2006, 529:1-7.
54. Xu Q., Hao X., Yang Q., Si L. Resveratrol prevents hyperglycemia-induced endothelial dysfunction via activation of adenosine monophosphate-activated protein kinase. Biochem. Biophys. Res. Commun. 2009, 388:389-394.
55. Yan L.P., Zhuang Y.L., Chan S.W., Chen S.L., Shi G.G. Analysis of the mechanisms underlying the endothelium-dependent antivasoconstriction of puerarin in rat aorta. Naunyn Schmiedebergs Arch. Pharmacol. 2009, 379:587-597.
56. Yu Z., Li W. Induction of apoptosis by puerarin in colon cancer HT-29 cells. Cancer Lett. 2005, 238:53-60.
57. Yue H.W., Hu X.Q. Pharmacologic value of radix Puerariae and puerarine on cardiovascular system. Zhongguo Zhong Xi Yi Jie He Za Zhi 1996, 16:382-384.
58. Zhang S.Y., Chen G., Wei P.F., Huang X.S., Dai Y., Shen Y.J., Chen S.L., Sun-Chi C.A., Xu H.X. The effect of puerarin on serum nitric oxide concentration and myocardial eNOS expression in rats with myocardial infarction. J. Asian Nat. Prod. Res. 2008, 10:373-381.