Isoflavone genistein protects human vascular endothelial cells against tumor necrosis factor-a-induced apoptosis through the p38β mitogen-activated protein kinase

Apoptosis

Volumn 14, Issue 1, 2009, Pages 66-76

  Si, Hongwei ^a   Liu, Dongmin ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Endothelial cells; Genistein; P38

Indexed keywords

7 AMINODACTINOMYCIN; 7-AMINOACTINOMYCIN D; ANTINEOPLASTIC AGENT; CASPASE 3; DACTINOMYCIN; DRUG DERIVATIVE; FLUORESCENT DYE; GENISTEIN; ISOFLAVONE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE 11; PROTEIN BCL 2; PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ENZYME ACTIVATION; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ANTICARCINOGENIC AGENTS; APOPTOSIS; CASPASE 3; DACTINOMYCIN; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; FLUORESCENT DYES; GENISTEIN; HUMANS; ISOFLAVONES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 11; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-BCL-2; TUMOR NECROSIS FACTOR-ALPHA;

EID: 58949086523     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-008-0283-9     Document Type: Article

References (82)

1. Kim H, Peterson TG, Barnes S (1998) Mechanisms of action of the soy isoflavone genistein: emerging role for its effects via transforming growth factor beta signaling pathways. Am J Clin Nutr 68:1418S-1425S (Pubitemid 28550923)
2. Kuiper GG, Carlsson B, Grandien K et al (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138:863-870. doi:10.1210/en.138.3.863 (Pubitemid 27089735)
3. Akiyama T, Ishida J, Nakagawa S et al (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262:5592-5595
4. Goodman-Gruen D, Kritz-Silverstein D (2001) Usual dietary isoflavone intake is associated with cardiovascular disease risk factors in postmenopausal women. J Nutr 131:1202-1206 (Pubitemid 32275100)
5. de Kleijn MJ, van der Schouw YT, Wilson PW et al (2001) Intake of dietary phytoestrogens is low in postmenopausal women in the United States: the Framingham study (1-4). J Nutr 131:1826-1832 (Pubitemid 32520453)
6. Zhang X, Shu XO, Gao YT et al (2003) Soy food consumption is associated with lower risk of coronary heart disease in Chinese women. J Nutr 133:2874-2878 (Pubitemid 37099774)
7. Erdman JW Jr. (2000) AHA science advisory: soy protein and cardiovascular disease: a statement for healthcare professionals from the Nutrition Committee of the AHA. Circulation 102: 2555-2559
8. Hale G, Paul-Labrador M, Dwyer JH et al (2002) Isoflavone supplementation and endothelial function in menopausal women. Clin Endocrinol (Oxf) 56:693-701. doi:10.1046/j.1365-2265. 2002.01533.x (Pubitemid 34785900)
9. Anthony MS, Clarkson TB, Williams JK (1998) Effects of soy isoflavones on atherosclerosis: potential mechanisms. Am J Clin Nutr 68:1390S-1393S (Pubitemid 28550918)
10. van der Schouw YT, de Kleijn MJ, Peeters PH et al (2000) Phytooestrogens and cardiovascular disease risk. Nutr Metab Cardiovas 10:154-167
11. Wangen KE, Duncan AM, Xu X et al (2001) Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women. Am J Clin Nutr 73:225-231 (Pubitemid 32109850)
12. Walker HA, Dean TS, Sanders TA et al (2001) The phytoestrogen genistein produces acute nitric oxide-dependent dilation of human forearm vasculature with similar potency to 17ss-estradiol. Circulation 103:258-262 (Pubitemid 32095412)
13. Squadrito F, Altavilla D, Morabito N et al (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. doi:10.1016/S0021-9150(02)00013-8 (Pubitemid 34615825)
14. Squadrito F, Altavilla D, Crisafulli A et al (2003) Effect of genistein on endothelial function in postmenopausal women: a randomized, double-blind, controlled study. Am J Med 114:470-476. doi:10.1016/S0002-9343(03)00059-7 (Pubitemid 36515109)
15. Nestel PJ, Yamashita T, Sasahara T et al (1997) Soy isoflavones improve systemic arterial compliance but not plasma lipids in menopausal and perimenopausal women. Arterioscler Thromb Vasc Biol 17:3392-3398 (Pubitemid 28028547)
16. Makela S, Savolainen H, Aavik E et al (1999) Differentiation between vasculoprotective and uterotrophic effects of ligands with different binding affinities to estrogen receptors alpha and beta. Proc Natl Acad Sci USA 96:7077-7082. doi:10.1073/pnas. 96.12.7077 (Pubitemid 29275012)
17. Anthony MS, Clarkson TB, Hughes CL Jr. et al (1996) Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J Nutr 126:43-50 (Pubitemid 26030632)
18. Honore EK, Williams JK, Anthony MS et al (1997) Soy isoflavones enhance coronary vascular reactivity in atherosclerotic female macaques. Fertil Steril 67:148-154. doi:10.1016/S0015- 0282(97)81872-9 (Pubitemid 26428429)
19. Williams JK, Clarkson TB (1998) Dietary soy isoflavones inhibit in-vivo constrictor responses of coronary arteries to collageninduced platelet activation. Coron Artery Dis 9:759-764 (Pubitemid 29012188)
20. Yamakoshi J, Piskula MK, Izumi T et al (2000) Isoflavone aglycone-rich extract without soy protein attenuates atherosclerosis development in cholesterol-fed rabbits. J Nutr 130: 1887-1893 (Pubitemid 30497517)
21. Karamsetty 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 (Pubitemid 32472493)
22. Nevala R, Lassila M, Finckenberg P et al (2002) Genistein treatment reduces arterial contractions by inhibiting tyrosine kinases in ovariectomized hypertensive rats. Eur J Pharmacol 452:87-96. doi:10.1016/S0014-2999(02)02270-7 (Pubitemid 35248128)
23. Deodato B, Altavilla D, Squadrito G et al (1999) Cardioprotection by the phytoestrogen genistein in experimental myocardial ischaemia-reperfusion injury. Br J Pharmacol 128:1683-1690. doi:10.1038/sj.bjp.0702973 (Pubitemid 30011881)
24. Squadrito F, Altavilla D, Squadrito G et al (2000) Genistein supplementation and estrogen replacement therapy improve endothelial dysfunction induced by ovariectomy in rats. Cardiovasc Res 45:454-462. doi:10.1016/S0008- 6363(99)00359-4 (Pubitemid 30069511)
25. Cassidy A, Hooper L (2006) Phytoestrogens and cardiovascular disease. J Br Menopause Soc 12:49-56. doi:10.1258/13621800 6777525776 (Pubitemid 43881063)
26. Vega-Lopez S, Yeum KJ, Lecker JL et al (2005) Plasma antioxidant capacity in response to diets high in soy or animal protein with or without isoflavones. Am J Clin Nutr 81:43-49 (Pubitemid 43073374)
27. Ruiz-Larrea MB, Mohan AR, Paganga G et al (1997) Antioxidant activity of phytoestrogenic isoflavones. Free Radic Res 26:63-70. doi:10.3109/ 10715769709097785 (Pubitemid 27060130)
28. An J, Tzagarakis-Foster C, Scharschmidt TC et al (2001) Estrogen receptor beta-selective transcriptional activity and recruitment of coregulators by phytoestrogens. J Biol Chem 276:17808-17814. doi:10.1074/jbc.M100953200
29. Sacks FM, Lichtenstein A, Van Horn L et al (2006) Soy protein, isoflavones, and cardiovascular health: an American Heart Association Science Advisory for professionals from the Nutrition Committee. Circulation 113:1034-1044. doi:10.1161/ CIRCULATIONAHA.106.171052 (Pubitemid 43879479)
30. Takenaka T, Takahashi K, Kobayashi T et al (2002) Oxidized low density lipoprotein (Ox-LDL) as a marker of atherosclerosis in hemodialysis (HD) patients. Clin Nephrol 58:33-37 (Pubitemid 34752991)
31. Hulthe J, Fagerberg B (2002) Circulating oxidized LDL is associated with subclinical atherosclerosis development and inflammatory cytokines (AIR Study). Arterioscler Thromb Vasc Biol 22:1162-1167. doi:10.1161/01.ATV.0000021150.63480. CD (Pubitemid 34764868)
32. Simons LA, von Konigsmark M, Simons J et al (2000) Phytoestrogens do not influence lipoprotein levels or endothelial function in healthy, postmenopausal women. Am J Cardiol 85:1297-1301. doi:10.1016/S0002-9149(00)00759-1 (Pubitemid 30314660)
33. Patel RP, Boersma BJ, Crawford JH et al (2001) Antioxidant mechanisms of isoflavones in lipid systems: paradoxical effects of peroxyl radical scavenging. Free Radic Biol Med 31:1570-1581. doi:10.1016/S0891-5849(01)00737-7 (Pubitemid 34024979)
34. Chacko BK, Chandler RT, Mundhekar A et al (2005) Revealing anti-inflammatory mechanisms of soy isoflavones by flow: modulation of leukocyte-endothelial cell interactions. Am JPhysiol Heart Circ Physiol 289:H908-H915. doi:10.1152/ ajpheart.00781.2004 (Pubitemid 41129409)
35. Wei H, Wei L, Frenkel K et al (1993) Inhibition of tumor promoter- induced hydrogen peroxide formation in vitro and in vivo by genistein. Nutr Cancer 20:1-12 (Pubitemid 23225362)
36. Kapiotis S, Hermann M, Held I et al (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 (Pubitemid 28016034)
37. Tikkanen MJ, Vihma V, Hockerstedt A et al (2002) Lipophilic oestrogen derivatives contained in lipoprotein particles. Acta Physiol Scand 176:117-121. doi:10.1046/j.1365-201X.2002. 01022.x (Pubitemid 35216288)
38. Liu D, Homan LL, Dillon JS (2004) Genistein acutely stimulates nitric oxide synthesis in vascular endothelial cells by a cyclic adenosine 50-monophosphate-dependent mechanism. Endocrinology 145:5532-5539. doi:10.1210/en.2004-0102 (Pubitemid 39564593)
39. Liu D, Jiang H, Grange RW (2005) Genistein activates the 3', 5'-cyclic adenosine monophosphate signaling pathway in vascular endothelial cells and protects endothelial barrier function. Endocrinology 146:1312-1320. doi:10.1210/en.2004-1221 (Pubitemid 40289318)
40. Mahn K, Borras C, Knock GA et al (2005) Dietary soy isoflavone induced increases in antioxidant and eNOS gene expression lead to improved endothelial function and reduced blood pressure in vivo. FASEB J 19:1755-1757 (Pubitemid 41429553)
41. Asai K, Kudej RK, Shen YT et al (2000) Peripheral vascular endothelial dysfunction and apoptosis in old monkeys. Arterioscler Thromb Vasc Biol 20:1493-1499 (Pubitemid 30353879)
42. Mallat Z, Hugel B, Ohan J et al (1999) Shed membrane microparticles with procoagulant potential in human atherosclerotic plaques: a role for apoptosis in plaque thrombogenicity. Circulation 99:348-353 (Pubitemid 29051259)
43. Lecoeur H, Ledru E, Prevost MC et al (1997) Strategies for phenotyping apoptotic peripheral human lymphocytes comparing ISNT, annexin-V and 7-AAD cytofluorometric staining methods. J Immunol Methods 209:111-123. doi:10.1016/S0022-1759 (97)00138-5 (Pubitemid 28055701)
44. Liu D, Si H, Reynolds KA et al (2007) Dehydroepiandrosterone protects vascular endothelial cells against apoptosis through a Galphai protein-dependent activation of phosphatidylinositol 3-kinase/Akt and regulation of antiapoptotic Bcl-2 expression. Endocrinology 148:3068-3076. doi:10.1210/en. 2006-1378 (Pubitemid 46996987)
45. Schmid I, Uittenbogaart CH, Keld B et al (1994) A rapid method for measuring apoptosis and dual-color immunofluorescence by single laser flow cytometry. J Immunol Methods 170:145-157. doi:10.1016/0022-1759(94)90390-5 (Pubitemid 24122504)
46. Shi Y (2002) Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 9:459-470. doi:10.1016/S1097-2765 (02)00482-3 (Pubitemid 34273778)
47. Ling S, Zhou L, Li H et al (2006) Effects of 17beta-estradiol on growth and apoptosis in human vascular endothelial cells: influence of mechanical strain and tumor necrosis factor-alpha. Steroids 71:799-808. doi:10.1016/j.steroids.2006.05.010 (Pubitemid 44062602)
48. Spyridopoulos I, Sullivan AB, Kearney M et al (1997) Estrogenreceptor- mediated inhibition of human endothelial cell apoptosis estradiol as a survival factor. Circulation 95:1505-1514 (Pubitemid 27142809)
49. Polte T, Schroder H (1998) Cyclic AMP mediates endothelial protection by nitric oxide. Biochem Biophys Res Commun 251:460-465. doi:10.1006/bbrc.1998.9486 (Pubitemid 28505045)
50. Schildberg FA, Schulz S, Dombrowski F et al (2005) Cyclic AMP alleviates endoplasmic stress and programmed cell death induced by lipopolysaccharides in human endothelial cells. Cell Tissue Res 320:91-98. doi:10.1007/s00441-004-1066- 4 (Pubitemid 40543765)
51. Gupta K, Kshirsagar S, Li W et al (1999) VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp Cell Res 247:495-504. doi:10.1006/excr.1998.4359 (Pubitemid 29394787)
52. Joy S, Siow RC, Rowlands DJ et al (2006) The isoflavone Equol mediates rapid vascular relaxation: Ca2?-independent activation of endothelial nitric-oxide synthase/Hsp90 involving ERK1/2 and Akt phosphorylation in human endothelial cells. J Biol Chem 281:27335-27345. doi:10.1074/jbc.M602803200 (Pubitemid 44401761)
53. Silva G, Cunha A, Gregoire IP et al (2006) The antiapoptotic effect of heme oxygenase-1 in endothelial cells involves the degradation of p38 alpha MAPK isoform. J Immunol 177:1894-1903 (Pubitemid 44092529)
54. Frey RS, Singletary KW (2003) Genistein activates p38 mitogenactivated protein kinase, inactivates ERK1/ERK2 and decreases Cdc25C expression in immortalized human mammary epithelial cells. J Nutr 133:226-231 (Pubitemid 36070605)
55. Hale KK, Trollinger D, Rihanek M et al (1999) Differential expression and activation of p38 mitogen-activated protein kinase alpha, beta, gamma, and delta in inflammatory cell lineages. J Immunol 162:4246-4252 (Pubitemid 29314814)
56. Nemoto S, Xiang J, Huang S et al (1998) Induction of apoptosis by SB202190 through inhibition of p38beta mitogen-activated protein kinase. J Biol Chem 273:16415-16420. doi:10.1074/jbc. 273.26.16415 (Pubitemid 28311422)
57. Das S, Fraga CG, Das DK (2006) Cardioprotective effect of resveratrol via HO-1 expression involves p38 map kinase and PI- 3-kinase signaling, but does not involve NFkappaB. Free Radic Res 40:1066-1075. doi:10.1080/10715760600833085 (Pubitemid 44480547)
58. Norata GD, Tonti L, Roma P et al (2002) Apoptosis and proliferation of endothelial cells in early atherosclerotic lesions: possible role of oxidised LDL. Nutr Metab Cardiovasc Dis 12:297-305 (Pubitemid 135713574)
59. Piro S, Spampinato D, Spadaro L et al (2007) Direct apoptotic effects of free fatty acids on human endothelial cells. Nutr Metab Cardiovasc Dis
60. Picchi A, Gao X, Belmadani S et al (2006) Tumor necrosis factor- alpha induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res 99:69-77. doi:10.1161/01.RES. 0000229685.37402.80 (Pubitemid 44297057)
61. Makino N, Maeda T, Sugano M et al (2005) High serum TNFalpha level in Type 2 diabetic patients with microangiopathy is associated with eNOS down-regulation and apoptosis in endothelial cells. J Diabetes Complications 19:347-355. doi:10.1016/ j.jdiacomp.2005.04.002 (Pubitemid 41563018)
62. Sharma S, Adrogue JV, Golfman L et al (2004) Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J 18:1692-1700. doi:10.1096/fj.04- 2263com (Pubitemid 39463708)
63. Winn RK, Harlan JM (2005) The role of endothelial cell apoptosis in inflammatory and immune diseases. J Thromb Haemost 3:1815-1824. doi:10.1111/j.1538-7836.2005.01378.x (Pubitemid 41716568)
64. Li Y, Upadhyay S, Bhuiyan M et al (1999) Induction of apoptosis in breast cancer cells MDA-MB-231 by genistein. Oncogene 18:3166-3172. doi:10.1038/sj.onc.1202650 (Pubitemid 29261238)
65. Chodon D, Ramamurty N, Sakthisekaran D (2007) Preliminary studies on induction of apoptosis by genistein on HepG2 cell line. Toxicol In Vitro 21:887-891. doi:10.1016/j.tiv.2007.01.023 (Pubitemid 46603234)
66. Fuchs D, Dirscherl B, Schroot JH et al (2006) Soy extract has different effects compared with the isolated isoflavones on the proteome of homocysteine-stressed endothelial cells. Mol Nutr Food Res 50:58-69. doi:10.1002/mnfr.200500133 (Pubitemid 43155096)
67. Fuchs D, Dirscherl B, Schroot JH et al (2007) Proteome analysis suggests that mitochondrial dysfunction in stressed endothelial cells is reversed by a soy extract and isolated isoflavones. J Proteome Res 6:2132-2142. doi:10.1021/pr060547y (Pubitemid 46985099)
68. Nakashima S, Koike T, Nozawa Y (1991) Genistein, a protein tyrosine kinase inhibitor, inhibits thromboxane A2-mediated human platelet responses. Mol Pharmacol 39:475-480
69. Atluru D, Jackson TM, Atluru S (1991) Genistein, a selective protein tyrosine kinase inhibitor, inhibits interleukin-2 and leukotriene B4 production from human mononuclear cells. Clin Immunol Immunopathol 59:379-387. doi:10.1016/0090-1229 (91)90033-7
70. Adlercreutz CH, Goldin BR, Gorbach SL et al (1995) Soybean phytoestrogen intake and cancer risk. J Nutr 125:757S-770S
71. Xu X, Harris KS, Wang HJ et al (1995) Bioavailability of soybean isoflavones depends upon gut microflora in women. J Nutr 125:2307-2315
72. Chang HC, Churchwell MI, Delclos KB et al (2000) Mass spectrometric determination of genistein tissue distribution in diet-exposed sprague-dawley rats. J Nutr 130:1963-1970 (Pubitemid 30497528)
73. Zhang Y, Hendrich S, Murphy PA (2003) Glucuronides are the main isoflavone metabolites in women. J Nutr 133:399-404 (Pubitemid 36172890)
74. Zhang Y, Song TT, Cunnick JE et al (1999) Daidzein and genistein glucuronides in vitro are weakly estrogenic and activate human natural killer cells at nutritionally relevant concentrations. J Nutr 129:399-405 (Pubitemid 29072127)
75. Ji ES, Yue H, Wu YM et al (2004) Effects of phytoestrogen genistein on myocardial ischemia/reperfusion injury and apoptosis in rabbits. Acta Pharmacol Sin 25:306-312 (Pubitemid 38316040)
76. Latti S, Leskinen M, Shiota N et al (2003) Mast cell-mediated apoptosis of endothelial cells in vitro: a paracrine mechanism involving TNF-alpha-mediated down-regulation of bcl-2 expression. J Cell Physiol 195:130-138. doi:10.1002/jcp.10235 (Pubitemid 36292767)
77. Badrichani AZ, Stroka DM, Bilbao G et al (1999) Bcl-2 and Bcl- XL serve an anti-inflammatory function in endothelial cells through inhibition of NF-kappaB. J Clin Invest 103:543-553. doi:10.1172/JCI2517 (Pubitemid 29094055)
78. Nakagami H, Morishita R, Yamamoto K et al (2001) Phosphorylation of p38 mitogen-activated protein kinase downstream of bax-caspase-3 pathway leads to cell death induced by high Dglucose in human endothelial cells. Diabetes 50:1472-1481. doi:10.2337/diabetes.50.6.1472 (Pubitemid 32500182)
79. Razandi M, Pedram A, Levin ER (2000) Estrogen signals to the preservation of endothelial cell form and function. J Biol Chem 275:38540-38546. doi:10.1074/jbc.M007555200 (Pubitemid 32009181)
80. Luschen S, Scherer G, Ussat S et al (2004) Inhibition of p38 mitogen-activated protein kinase reduces TNF-induced activation of NF-kappaB, elicits caspase activity, and enhances cytotoxicity. Exp Cell Res 293:196-206. doi:10.1016/j.yexcr.2003.10.009 (Pubitemid 38083209)
81. Wang Y, Huang S, Sah VP et al (1998) Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem 273:2161-2168. doi:10.1074/jbc.273.4.2161 (Pubitemid 28069266)
82. Porras A, Zuluaga S, Black E et al (2004) P38 alpha mitogenactivated protein kinase sensitizes cells to apoptosis induced by different stimuli. Mol Biol Cell 15:922-933. doi:10.1091/ mbc.E03-08-0592 (Pubitemid 38146504)