Multiple mechanisms of soy isoflavones against oxidative stress-induced endothelium injury

Free Radical Biology and Medicine

Volumn 47, Issue 2, 2009, Pages 167-175

  Xu, Shang Zhong ^a   Zhong, Wenwen ^a   Ghavideldarestani, Maryam ^a   Saurabh, Rahul ^a   Lindow, Steve W ^b   Atkin, Stephen L ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

^b DEPARTMENT OF OBSTETRICS AND GYNAECOLOGY   (United Kingdom)

Author keywords

Endothelial cells; Free radicals; Hyperglycemia; Oxidative stress; Phytoestrogens

Indexed keywords

DAIDZEIN; ESTROGEN RECEPTOR BETA; GENISTEIN; GLUCOSE; HYDROGEN PEROXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; RHO KINASE;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; OXIDATIVE STRESS; PRIORITY JOURNAL; RECEPTOR UPREGULATION; VASCULAR ENDOTHELIUM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ESTRADIOL; ESTROGEN RECEPTOR BETA; GENISTEIN; GLUCOSE; HUMANS; HYDROGEN PEROXIDE; ISOFLAVONES; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SOYBEANS; UMBILICAL VEINS;

EID: 67349247426     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.04.021     Document Type: Article

References (52)

1. Meigs J.B., Larson M.G., Fox C.S., Keaney Jr. J.F., Vasan R.S., and Benjamin E.J. Association of oxidative stress, insulin resistance, and diabetes risk phenotypes: the Framingham Offspring Study. Diabetes Care 30 (2007) 2529-2535
2. Houstis N., Rosen E.D., and Lander E.S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440 (2006) 944-948
3. Allen D.A., Yaqoob M.M., and Harwood S.M. Mechanisms of high glucose-induced apoptosis and its relationship to diabetic complications. J. Nutr. Biochem. 16 (2005) 705-713
4. Song P., Wu Y., Xu J., Xie Z., Dong Y., Zhang M., and Zou M.H. Reactive nitrogen species induced by hyperglycemia suppresses Akt signaling and triggers apoptosis by upregulating phosphatase PTEN (phosphatase and tensin homologue deleted on chromosome 10) in an LKB1-dependent manner. Circulation 116 (2007) 1585-1595
5. Varma S., Lal B.K., Zheng R., Breslin J.W., Saito S., Pappas P.J., Hobson II R.W., and Duran W.N. Hyperglycemia alters PI3k and Akt signaling and leads to endothelial cell proliferative dysfunction. Am. J. Physiol. Heart Circ. Physiol. 289 (2005) H1744-1751
6. Sacks F.M., Lichtenstein A., Van Horn L., Harris W., Kris-Etherton P., and Winston M. Soy protein, isoflavones, and cardiovascular health: an American Heart Association Science Advisory for professionals from the Nutrition Committee. Circulation 113 (2006) 1034-1044
7. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der Burg B., and Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
8. Siow R.C., Li F.Y., Rowlands D.J., de Winter P., and Mann G.E. Cardiovascular targets for estrogens and phytoestrogens: transcriptional regulation of nitric oxide synthase and antioxidant defense genes. Free Radic. Biol. Med. 42 (2007) 909-925
9. Lee Y.S., Chen X.W., and Anderson J.J.B. Physiological concentrations of genistein stimulate the proliferation and protect against free radical-induced oxidative damage of MC3T3-E1 osteoblast-like cells. Nutr. Res. 21 (2001) 1287-1298
10. Exner M., Hermann M., Hofbauer R., Kapiotis S., Quehenberger P., Speiser W., Held I., and Gmeiner B.M. Genistein prevents the glucose autoxidation mediated atherogenic modification of low density lipoprotein. Free Radic. Res. 34 (2001) 101-112
11. Sierens J., Hartley J.A., Campbell M.J., Leathem A.J., and Woodside J.V. Effect of phytoestrogen and antioxidant supplementation on oxidative DNA damage assessed using the comet assay. Mutat. Res. 485 (2001) 169-176
12. Kampkotter A., Wiegand C., Timpel C., Rohrdanz E., Chovolou Y., Kahl R., and Watjen W. Increased expression of catalase in human hepatoma cells by the soy isoflavone, daidzein. Basic Clin. Pharmacol. Toxicol. 102 (2008) 437-442
13. Mezei O., Banz W.J., Steger R.W., Peluso M.R., Winters T.A., and Shay N. Soy isoflavones exert antidiabetic and hypolipidemic effects through the PPAR pathways in obese Zucker rats and murine RAW 264.7 cells. J. Nutr. 133 (2003) 1238-1243
14. Lavigne C., Marette A., and Jacques H. Cod and soy proteins compared with casein improve glucose tolerance and insulin sensitivity in rats. Am. J. Physiol. Endocrinol. Metab. 278 (2000) E491-500
15. Jayagopal V., Albertazzi P., Kilpatrick E.S., Howarth E.M., Jennings P.E., Hepburn D.A., and Atkin S.L. Beneficial effects of soy phytoestrogen intake in postmenopausal women with type 2 diabetes. Diabetes Care 25 (2002) 1709-1714
16. Oh H.Y., Kim S.S., Chung H.Y., and Yoon S. Isoflavone supplements exert hormonal and antioxidant effects in postmenopausal Korean women with diabetic retinopathy. J. Med. Food 8 (2005) 1-7
17. Fanti P., Asmis R., Stephenson T.J., Sawaya B.P., and Franke A.A. Positive effect of dietary soy in ESRD patients with systemic inflammation-correlation between blood levels of the soy isoflavones and the acute-phase reactants. Nephrol. Dial. Transplant. 21 (2006) 2239-2246
18. Liu D., Zhen W., Yang Z., Carter J.D., Si H., and Reynolds K.A. Genistein acutely stimulates insulin secretion in pancreatic beta-cells through a cAMP-dependent protein kinase pathway. Diabetes 55 (2006) 1043-1050
19. Cederroth C.R., Vinciguerra M., Gjinovci A., Kuhne F., Klein M., Cederroth M., Caille D., Suter M., Neumann D., James R.W., Doerge D.R., Wallimann T., Meda P., Foti M., Rohner-Jeanrenaud F., Vassalli J.D., and Nef S. Dietary phytoestrogens activate AMP-activated protein kinase with improvement in lipid and glucose metabolism. Diabetes 57 (2008) 1176-1185
20. Lee J.S. Effects of soy protein and genistein on blood glucose, antioxidant enzyme activities, and lipid profile in streptozotocin-induced diabetic rats. Life Sci. 79 (2006) 1578-1584
21. Hwang J.T., Park J., Shin J.I., Lee Y.K., Lee S.K., Baik H.W., Ha J., and Park O.J. Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochem. Biophys. Res. Commun. 338 (2005) 694-699
22. Szkudelski T., Nogowski L., Pruszynska-Oszmalek E., Kaczmarek P., and Szkudelska K. Genistein restricts leptin secretion from rat adipocytes. J. Steroid Biochem. Mol. Biol. 96 (2005) 301-307
23. Hintz K.K., and Ren J. Phytoestrogenic isoflavones daidzein and genistein reduce glucose-toxicity-induced cardiac contractile dysfunction in ventricular myocytes. Endocr. Res. 30 (2004) 215-223
24. Fotsis T., Pepper M., Adlercreutz H., Hase T., Montesano R., and Schweigerer L. Genistein, a dietary ingested isoflavonoid, inhibits cell proliferation and in vitro angiogenesis. J. Nutr. 125 (1995) 790S-797S
25. Baluchnejadmojarad T., and Roghani M. Chronic administration of genistein improves aortic reactivity of streptozotocin-diabetic rats: mode of action. Vasc. Pharmacol. 49 (2008) 1-5
26. Nakajima M., Cooney M.J., Tu A.H., Chang K.Y., Cao J., Ando A., An G.J., Melia M., and de Juan Jr. E. Normalization of retinal vascular permeability in experimental diabetes with genistein. Invest. Ophthalmol. Visual Sci. 42 (2001) 2110-2114
27. Walker H.A., Dean T.S., Sanders T.A., Jackson G., Ritter J.M., and Chowienczyk P.J. The phytoestrogen genistein produces acute nitric oxide-dependent dilation of human forearm vasculature with similar potency to 17beta-estradiol. Circulation 103 (2001) 258-262
28. Knock G.A., Mahn K., Mann G.E., Ward J.P., and Aaronson P.I. Dietary soy modulates endothelium-dependent relaxation in aged male rats: increased agonist-induced endothelium-derived hyperpolarising factor and basal nitric oxide activity. Free Radic. Biol. Med. 41 (2006) 731-739
29. Xu S.Z., Zhong W., Watson N.M., Dickerson E., Wake J., Lindow S., Newton C.J., and Atkin S.L. Fluvastatin reduces oxidative damage in human vascular endothelial cells by upregulating Bcl-2. J. Thromb. Haemostasis 6 (2008) 692-700
30. Xu S.Z., Sukumar P., Zeng F., Li J., Jairaman A., English A., Naylor J., Ciurtin C., Majeed Y., Milligan C.J., Bahnasi Y.M., Al-Shawaf E., Porter K.E., Jiang L.H., Emery P., Sivaprasadarao A., and Beech D.J. TRPC channel activation by extracellular thioredoxin. Nature 451 (2008) 69-72
31. Shaw R.J., and Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441 (2006) 424-430
32. Li X., Liu L., Tupper J.C., Bannerman D.D., Winn R.K., Sebti S.M., Hamilton A.D., and Harlan J.M. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J. Biol. Chem. 277 (2002) 15309-15316
33. Willis S.N., Fletcher J.I., Kaufmann T., van Delft M.F., Chen L., Czabotar P.E., Ierino H., Lee E.F., Fairlie W.D., Bouillet P., Strasser A., Kluck R.M., Adams J.M., and Huang D.C. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315 (2007) 856-859
34. Critchley H.O., Henderson T.A., Kelly R.W., Scobie G.S., Evans L.R., Groome N.P., and Saunders P.T. Wild-type estrogen receptor (ERbeta1) and the splice variant (ERbetacx/beta2) are both expressed within the human endometrium throughout the normal menstrual cycle. J. Clin. Endocrinol. Metab. 87 (2002) 5265-5273
35. Campbell-Thompson M., Lynch I.J., and Bhardwaj B. Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res. 61 (2001) 632-640
36. Toth B., Saadat G., Geller A., Scholz C., Schulze S., Friese K., and Jeschke U. Human umbilical vascular endothelial cells express estrogen receptor beta (ERbeta) and progesterone receptor A (PR-A), but not ERalpha and PR-B. Histochem. Cell Biol. 130 (2008) 399-405
37. Yu T., Robotham J.L., and Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. USA 103 (2006) 2653-2658
38. Busik J.V., Mohr S., and Grant M.B. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes 57 (2008) 1952-1965
39. 2-terminal kinase pathway and prevented by PI3K/Akt/eNOS pathway. Cell Signalling 18 (2006) 391-399
40. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., and Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262 (1987) 5592-5595
41. Pytel D., Sliwinski T., Poplawski T., Ferriola D., and Majsterek I. Tyrosine kinase blockers: new hope for successful cancer therapy. Anticancer Agents Med. Chem. 9 (2009) 66-76
42. Bhakta D., Higgins C.D., Sevak L., Mangtani P., Adlercreutz H., McMichael A.J., and dos Santos Silva I. Phyto-oestrogen intake and plasma concentrations in South Asian and native British women resident in England. Br. J. Nutr. 95 (2006) 1150-1158
43. Uchida S., Watanabe G., Shimada Y., Maeda M., Kawabe A., Mori A., Arii S., Uehata M., Kishimoto T., Oikawa T., and Imamura M. The suppression of small GTPase rho signal transduction pathway inhibits angiogenesis in vitro and in vivo. Biochem. Biophys. Res. Commun. 269 (2000) 633-640
44. Sawada N., Itoh H., Ueyama K., Yamashita J., Doi K., Chun T.H., Inoue M., Masatsugu K., Saito T., Fukunaga Y., Sakaguchi S., Arai H., Ohno N., Komeda M., and Nakao K. Inhibition of rho-associated kinase results in suppression of neointimal formation of balloon-injured arteries. Circulation 101 (2000) 2030-2033
45. Hermenegildo C., Oviedo P.J., Garcia-Perez M.A., Tarin J.J., and Cano A. Effects of phytoestrogens genistein and daidzein on prostacyclin production by human endothelial cells. J. Pharmacol. Exp. Ther. 315 (2005) 722-728
46. Cai H. Hydrogen peroxide regulation of endothelial function: origins, mechanisms, and consequences. Cardiovasc. Res. 68 (2005) 26-36
47. Lu A., Frink M., Choudhry M.A., Schwacha M.G., Hubbard W.J., Rue III L.W., Bland K.I., and Chaudry I.H. Mitochondria play an important role in 17beta-estradiol attenuation of H(2)O(2)-induced rat endothelial cell apoptosis. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E585-593
48. Florian M., and Magder S. Estrogen decreases TNF-alpha and oxidized LDL induced apoptosis in endothelial cells. Steroids 73 (2008) 47-58
49. Wang T.T., Sathyamoorthy N., and Phang J.M. Molecular effects of genistein on estrogen receptor mediated pathways. Carcinogenesis 17 (1996) 271-275
50. Leung Y.K., Mak P., Hassan S., and Ho S.M. Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling. Proc. Natl. Acad. Sci. USA 103 (2006) 13162-13167
51. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Strom A., Treuter E., Warner M., and Gustafsson J.A. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87 (2007) 905-931
52. Mahn K., Borras C., Knock G.A., Taylor P., Khan I.Y., Sugden D., Poston L., Ward J.P., Sharpe R.M., Vina J., Aaronson P.I., and Mann G.E. 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 (2005) 1755-1757