Genistein acutely stimulates nitric oxide synthesis in vascular endothelial cells by a cyclic adenosine 5′-monophosphate-dependent mechanism

Endocrinology

Volumn 145, Issue 12, 2004, Pages 5532-5539

  Liu, Dongmin ^a   Homan, Laurie L ^a   Dillon, Joseph S ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GENISTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHYTOESTROGEN; PROTEIN KINASE B; RNA;

ANIMAL CELL; AORTA; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ESTROGEN ACTIVITY; HEART PROTECTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA TRANSCRIPTION; SOYBEAN; VASCULAR ENDOTHELIUM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; AORTA; CATTLE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENISTEIN; HUMANS; MAP KINASE SIGNALING SYSTEM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; UMBILICAL VEINS;

EID: 9444257630     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2004-0102     Document Type: Article

References (67)

1. Wenger NK, Speroff L, Packard B 1993 Cardiovascular health and disease in women. N Engl J Med 329:247-256
2. Scuteri A, Ferrucci L 2003 Blood pressure, arterial function, structure, and aging: the role of hormonal replacement therapy in postmenopausal women. J Clin Hypertens 5:219-225
3. Manson JE, Hsia J, Johnson KC, Rossouw JE, Assaf AR, Lasser NL, Trevisan M, Black HR, Heckbert SR, Detrano R, Strickland OL, Wong ND, Crouse JR, Stein E, Cushman M, Women's Health Initiative I 2003 Estrogen plus progestin and the risk of coronary heart disease. N Engl J Med 349:523-534
4. Cassidy A, Griffin B 1999 Phyto-oestrogens: a potential role in the prevention of CHD? Proc Nutr Soc 58:193-199
5. Setchell KD, Lydeking-Olsen E 2003 Dietary phytoestrogens and their effect on bone: evidence from in vitro and in vivo, human observational, and dietary intervention studies. Am J Clin Nutr 78(3 Suppl):593S-609S
6. Sarkar FH, Li Y 2002 Mechanisms of cancer chemoprevention by soy isoflavone genistein. Cancer Metastasis Rev 21:265-280
7. Kim H, Peterson TG, Barnes S 1998 Mechanisms of action of the soy isoflavone genistein: emerging role for its effects via transforming growth factor β signaling pathways. Am J Clin Nutr 68(6 Suppl):1418S-1425S
8. 2-mediated human platelet responses. Mol Pharmacol 39:475-480
9. Fotsis T, Pepper M, Adlercreutz H, Hase T, Montesano R, Schweigerer L 1995 Genistein, a dietary ingested isoflavonoid, inhibits cell proliferation and in vitro angiogenesis. J Nutr 125(3 Suppl):790S-797S
10. Dubey RK, Gillespie DG, Imthurn B, Rosselli M, Jackson EK, Keller PJ 1999 Phytoestrogens inhibit growth and MAP kinase activity in human aortic smooth muscle cells. Hypertension 33:177-182
11. Honore EK, Williams JK, Anthony MS, Clarkson TB 1997 Soy isoflavones enhance coronary vascular reactivity in atherosclerotic female macaques. Fertil Steril 67:148-154
12. Kapiotis S, Hermann M, Held I, Seelos C, Ehringer H, Gmeiner BM 1997 Genistein, the dietary-derived angiogenesis inhibitor, prevents LDL oxidation and protects endothelial cells from damage by atherogenic LDL. Arterioscler Thromb Vasc Biol 17:2868-2874
13. Katamsetty MR, Klinger JR, Hill NS 2001 Phytoestrogens restore nitric oxide-mediated relaxation in isolated pulmonary arteries from chronically hypoxic rats. J Pharmacol Exp Ther 297:968-974
14. Nevala R, Lassila M, Finckenberg P, Paukku K, Korpela R, Vapaatalo H 2002 Genistein treatment reduces arterial contractions by inhibiting tyrosine kinases in ovariectomized hypertensive rats. Eur J Pharmacol 452:87-96
15. Kondo K, Suzuki Y, Ikeda Y, Umemura K 2002 Genistein, an isoflavone included in soy, inhibits thrombotic vessel occlusion in the mouse femoral artery and in vitro platelet aggregation. Eur J Pharmacol 455:53-57
16. Anthony MS, Clarkson TB, Bullock BC, Wagner JD 1997 Soy protein versus soy phytoestrogens in the prevention of diet-induced coronary artery atherosclerosis of male cynomolgus monkeys. Arterioscler Thromb Vasc Biol 17: 2524-2531
17. Clarkson TB, Anthony MS, Williams JK, Honore EK, Cline JM 1998 The potential of soybean phytoestrogens for postmenopausal hormone replacement therapy. Proc Soc Exp Biol Med 217:365-368
18. Washburn S, Burke GL, Morgan T, Anthony M 1999 Effect of soy protein supplementation on serum lipoproteins, blood pressure, and menopausal symptoms in perimenopausal women. Menopause 6:7-13
19. Nestel PJ, Yamashita T, Sasahaia T, Pomeroy S, Dart A, Komesarof P, Owen A, Abbey M 1997 Soy isoflavones improve systemic arterial compliance but not plasma lipids in menopausal and perimenopausal women. Arterioscler Thromb Vasc Biol 17:3392-3398
20. Hodgson JM, Puddey IB, Beilin LJ, Mori TA, Croft KD 1998 Supplementation with isoflavonoid phytoestrogens does not alter serum lipid concentrations: a randomized controlled trial in humans. J Nutr 128:728-732
21. Anthony MS, Clarkson TB, Williams JK 1998 Effects of soy isoflavones on atherosclerosis: potential mechanisms. Am J Clin Nutr 68(6 Suppl):1390S-1393S
22. van der Schouw YT, de Kleijn MJ, Peeters PH, Grobbee DE 2000 Phytooestrogens and cardiovascular disease risk. Nutr Metab Cardiovasc Dis 10: 154-167
23. Walker HA, Dean TS, Sanders TA, Jackson G, Ritter JM, Chowienczyk PJ 2001 The phytoestrogen genistein produces acute nitric oxide-dependent dilation of human forearm vasculature with similar potency to 17β-estradiol. Circulation 103:258-262
24. Squadrito F, Altavilla D, Crisafulli A, Saitta A, Cucinotta D, Morabito N, D'Anna R, Corrado F, Ruggeri P, Frisina N, Squadrito G 2003 Effect of genistein on endothelial function in postmenopausal women: a randomized, double-blind, controlled study. Am J Med 114:470-476
25. Dobrydneva Y, Williams RL, Morris GZ, Blackmore PF 2002 Dietary phytoestrogens and their synthetic structural analogues as calcium channel blockers in human platelets. J Cardiovasc Pharmacol 40:399-410
26. Gottstein N, Ewins BA, Eccleston C, Hubbard GP, Kavanagh IC, Minihane AM, Weinberg PD, Rimbach G 2003 Effect of genistein and daidzein on platelet aggregation and monocyte and endothelial function. Br J Nutr 89: 607-616
27. MacRitchie AN, Jun SS, Chen Z, German Z, Yuhanna IS, Sherman TS, Shaul PW 1997 Estrogen upregulates endothelial nitric oxide synthase gene expression in fetal pulmonary artery endothelium. Circ Res 81:355-362
28. Chen Z, Yuhanna IS, Galcheva-Gargova Z, Karas RH, Mendelsohn ME, Shaul PW 1999 Estrogen receptor α mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest 103:401-406
29. Squadrito F, Altavilla D, Morabito N, Crisafulli A, D'Anna R, Corrado F, Ruggeri P, Campo GM, Calapai G, Caputi AP, Squadrito G 2002 The effect of the phytoestrogen genistein on plasma nitric oxide concentrations, endothelin-1 levels and endothelium dependent vasodilation in postmenopausal women. Atherosclerosis 163:339-347
30. Mishra SK, Abbot SE, Choudhury Z, Cheng M, Khatab N, Maycock NJ, Zavery A, Aaronson PI 2000 Endothelium-dependent relaxation of rat aorta and main pulmonary artery by the phytoestrogens genistein and daidzein. Cardiovasc Res 46:539-546
31. Satake N, Shibata S 1999 The potentiating effect of genistein on the relaxation induced by isoproterenol in rat aortic rings. Gen Pharmacol 33:221-227
32. Duarte J, Ocete MA, Perez-Vizcaino F, Zarzuelo A, Tamargo J 1997 Effect of tyrosine kinase and tyrosine phosphatase inhibitors on aortic contraction and induction of nitric oxide synthase. Eur J Pharmacol 338:25-33
33. Yu J, Rudic RD, Sessa WC 2002 Nitric oxide-releasing aspirin decreases vascular injury by reducing inflammation and promoting apoptosis. Lab Invest 82:825-832
34. Shin WS, Hong YH, Peng HB, De Caterina R, Libby P, Liao JK 1996 Nitric oxide attenuates vascular smooth muscle cell activation by interferon-γ. The role of constitutive NF-κB activity. J Biol Chem 271:11317-11324
35. Alonso D, Radomski MW 2003 Nitric oxide, platelet function, myocardial infarction and reperfusion therapies. Heart Fail Rev 8:47-54
36. Kotamraju S, Hogg N, Joseph J, Keefer LK, Kalyanaraman B 2001 Inhibition of oxidized low-density lipoprotein-induced apoptosis in endothelial cells by nitric oxide. Peroxyl radical scavenging as an antiapoptotic mechanism. J Biol Chem 276:17316-17323
37. Liu D, Dillon J 2004 Dehydroepiandrosterone stimulates nitric oxide release in vascular endothelial cells: evidence for a cell surface receptor. Steroids 69:279-289
38. Hisamoto K, Ohmichi M, Kurachi H, Hayakawa J, Kanda Y, Nishio Y, Adachi K, Tasaka K, Miyoshi E, Fujiwara N, Taniguchi N, Murata Y 2001 Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 276:3459-3467
39. Liu D, Dillon JS 2002 Dehydroepiandrosterone activates endothelial cell nitric-oxide synthase by a specific plasma membrane receptor coupled to Gα(i2,3). J Biol Chem 277:21379-21388
40. Simoncini T, Mannella P, Fornari L, Varone G, Caruso A, Genazzani AR 2003 Dehydroepiandrosterone modulates endothelial nitric oxide synthesis via direct genomic and nongenomic mechanisms. Endocrinology 144:3449-3455
41. Bernier SG, Haldar S, Michel T 2000 Bradykinin-regulated interactions of the mitogen-activated protein kinase pathway with the endothelial nitric-oxide synthase. J Biol Chem 275:30707-30715
42. Igarashi J, Bernier SG, Michel T 2001 Sphingosine 1-phosphate and activation of endothelial nitric-oxide synthase: differential regulation of Akt and MAP kinase pathways by EDG and bradykinin receptors in vascular endothelial cells. J Biol Chem 276:12420-12426
43. Boo YC, Jo HIJH 2003 Flow-dependent regulation of endothelial nitric oxide synthase: role of protein kinases. Am J Physiol 285:C499-C508
44. May MJ, Wheeler-Jones CP, Pearson JD 1996 Effects of protein tyrosine kinase inhibitors on cytokine-induced adhesion molecule expression by human umbilical vein endothelial cells. Br J Pharmacol 118:1761-1771
45. Makela S, Savolainen H, Aavik E, Myllarniemi M, Strauss L, Taskinen E, Gustafsson JA, Hayry P 1999 Differentiation between vasculoprotective and uterotrophic effects of ligands with different binding affinities to estrogen receptors α and β. Proc Natl Acad Sci USA 96:7077-7082
46. Chau CH, Chen KY, Deng HT, Kim KJ, Hosoya K, Terasaki T, Shih HM, Ann DK 2002 Coordinating Etk/Bmx activation and VEGF upregulation to promote cell survival and proliferation. Oncogene 21:8817-8829
47. Boo YC, Sorescu G, Boyd N, Shiojima I, Walsh K, Du J, Jo H 2002 Shear stress stimulates phosphorylation of endothelial nitric-oxide synthase at Ser1179 by Akt-independent mechanisms: role of protein kinase A. J Biol Chem 277:3388-3396
48. Morton MS, Arisaka O, Miyake N, Morgan LD, Evans BA 2002 Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J Nutr 132:3168-3171
49. Linford NJ, Dorsa DM 2002 17β-Estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin. Steroids 67:1029-1040
50. Gao S, Liu GZ, Wang Z 2004 Modulation of androgen receptor-dependent transcription by resveratrol and genistein in prostate cancer cells. Prostate 59:214-225
51. Fleming I, Busse R 2003 Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol 284:R1-R12
52. Cai H, Li Z, Davis ME, Kanner W, Harrison DG, Dudley Jr SC 2003 Akt-dependent phosphorylation of serine 1179 and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase 1/2 cooperatively mediate activation of the endothelial nitric-oxide synthase by hydrogen peroxide. Mol Pharmacol 63:325-331
53. Frey RS, Singletary KW 2003 Genistein activates p38 mitogen-activated protein kinase, inactivates ERK1/ERK2 and decreases Cdc25C expression in immortalized human mammary epithelial cells. J Nutr 133:226-231
54. Gong L, Li Y, Nedeljkovic-Kurepa A, Sarkar FH 2003 Inactivation of NF-κB by genistein is mediated via Akt signaling pathway in breast cancer cells. Oncogene 22:4702-4709
55. Berk BC, Corson MA, Peterson TE, Tseng H 1995 Protein kinases as mediators of fluid shear stress stimulated signal transduction in endothelial cells: a hypothesis for calcium-dependent and calcium-independent events activated by flow. J Biomech 28:1439-1450
56. D'Angelo G, Lee H, Weiner RI 1997 cAMP-dependent protein kinase inhibits the mitogenic action of vascular endothelial growth factor and fibroblast growth factor in capillary endothelial cells by blocking Raf activation. J Cell Biochem 67:353-366
57. Indolfi C, Avvedimento EV, Di Lorenzo E, Esposito G, Rapacciuolo A, Giuliano P, Grieco D, Cavuto L, Stingone AM, Ciullo I, Condorelli G, Chiariello M 1997 Activation of cAMP-PKA signaling in vivo inhibits smooth muscle cell proliferation induced by vascular injury. Nat Med 3:775-779
58. Morandini R, Ghanem G, Portier-Lemarie A, Robaye B, Renaud A, Boeynaems JM 1996 Action of cAMP on expression and release of adhesion molecules in human endothelial cells. Am J Physiol 270:H807-H816
59. Moy AB, Bodmer JE, Blackwell K, Shasby S, Shasby DM 1998 cAMP protects endothelial barrier function independent of inhibiting MLC20-dependent tension development. Am J Physiol 274:L1024-L1029
60. Peterson G, Barnes S 1996 Genistein inhibits both estrogen and growth factor-stimulated proliferation of human breast cancer cells. Cell Growth Differ 7:1345-1351
61. Vissac-Sabatier C, Bignon YJ, Bernard-Gallon DJ 2003 Effects of the phytoestrogens genistein and daidzein on BRCA2 tumor suppressor gene expression in breast cell lines. Nutr Cancer 45:247-255
62. Murota K, Shimizu S, Miyamoto S, Izumi T, Obata A, Kikuchi M, Terao J 2002 Unique uptake and transport of isoflavone aglycones by human intestinal caco-2 cells: comparison of isoflavonoids and flavonoids. J Nutr 132:1956-1961
63. Nichols MR, Morimoto BH 2000 Differential inhibition of multiple cAMP phosphodiesterase isozymes by isoflavones and tyrphostins. Mol Pharmacol 57:738-745
64. Santell RC, Chang YC, Nair MG, Helferich WG 1997 Dietary genistein exerts estrogenic effects upon the uterus, mammary gland and the hypothalamic/ pituitary axis in rats. J Nutr 127:263-269
65. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA 1997 Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 138: 863-870
66. Simoncini T, Rabkin E, Liao JK 2003 Molecular basis of cell membrane estrogen receptor interaction with phosphatidylinositol 3-kinase in endothelial cells. Arterioscler Thromb Vasc Biol 23:198-203
67. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B 2000 Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor α and estrogen receptor β. Proc Natl Acad Sci USA 97:11603-11608