1DUMMY Estrogen receptor and PI3K/Akt signaling pathway involvement in S-(-)equol-induced activation of Nrf2/ARE in endothelial cells

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Zhang, Ting ^a   Liang, Xinyu ^a   Shi, Linying ^a   Wang, Li ^a   Chen, Junli ^a   Kang, Chao ^a   Zhu, Jundong ^a   Mi, Mantian ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EQUOL; ESTROGEN RECEPTOR BETA; HEME OXYGENASE 1; HMOX1 PROTEIN, HUMAN; HYDROGEN PEROXIDE; NFE2L2 PROTEIN, HUMAN; NQO1 PROTEIN, HUMAN; OXIDIZING AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PHYTOESTROGEN; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); TRANSCRIPTION FACTOR NRF2;

ARTICLE; BIOSYNTHESIS; CARDIOVASCULAR DISEASE; CLINICAL TRIAL; DNA RESPONSIVE ELEMENT; DRUG EFFECT; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

CARDIOVASCULAR DISEASES; EQUOL; ESTROGEN RECEPTOR BETA; FEMALE; HEME OXYGENASE-1; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; MALE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; OXIDANTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHYTOESTROGENS; PROTO-ONCOGENE PROTEINS C-AKT; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION;

EID: 84894261945     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079075     Document Type: Article

References (54)

1. Siow RC, Li FY, Rowlands DJ, de Winter P, Mann GE (2007) Cardiovascular targets for estrogens and phytoestrogens: transcriptional regulation of nitric oxide synthase and antioxidant defense genes. Free Radic Biol Med 42: 909-925. (Pubitemid 46356896)
2. Setchell KD, Clerici C (2010) Equol: pharmacokinetics and biological actions. J Nutr 140: 1363S-368S.
3. Setchell KD, Clerici C (2010) Equol: history, chemistry, and formation. J Nutr 140: 1355S-1362S.
4. Jackson RL, Greiwe JS, Schwen RJ (2011) Emerging evidence of the health benefits of S-equol, an estrogen receptor beta agonist. Nutr Rev 69: 432-448.
5. Clerici C, Setchell KD, Battezzati PM, Pirro M, Giuliano V, et al. (2007) Pasta naturally enriched with isoflavone aglycons from soy germ reduces serum lipids and improves markers of cardiovascular risk. J Nutr 137: 2270-2278. (Pubitemid 47529589)
6. McMahon M, Itoh K, Yamamoto M, Hayes JD (2003) Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem 278: 21592-21600. (Pubitemid 36792558)
7. Mann GE, Bonacasa B, Ishii T, Siow RC (2009) Targeting the redox sensitive Nrf2-Keap1 defense pathway in cardiovascular disease: protection afforded by dietary isoflavones. Curr Opin Pharmacol 9: 139-145.
8. Anwar AA, Li FY, Leake DS, Ishii T, Mann GE, et al. (2005) Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: role of mitogen-activated protein kinases and Nrf2. Free Radic Biol Med 39: 227-236. (Pubitemid 40814548)
9. Froyen EB, Steinberg FM (2011) Soy isoflavones increase quinone reductase in hepa-1c1c7 cells via estrogen receptor beta and nuclear factor erythroid 2-related factor 2 binding to the antioxidant response element. J Nutr Biochem. 22: 843-848.
10. Joy S, Siow RC, Rowlands DJ, Becker M, Wyatt AW, 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. (Pubitemid 44401761)
11. Hwang J, Sevanian A, Hodis HN, Ursini F (2000) Synergistic inhibition of LDL oxidation by phytoestrogens and ascorbic acid. Free Radic Biol Med 29: 79-89. (Pubitemid 30658140)
12. Hwang J, Wang J, Morazzoni P, Hodis HN, Sevanian A (2003) The phytoestrogen equol increases nitric oxide availability by inhibiting superoxide production: an antioxidant mechanism for cell-mediated LDL modification. Free Radic Biol Med 34: 1271-1282. (Pubitemid 36513970)
13. Kamiyama M, Kishimoto Y, Tani M, Utsunomiya K, Kondo K (2009) Effects of equol on oxidized low-density lipoprotein-induced apoptosis in endothelial cells. J Atheroscler Thromb 16: 239-249.
14. Siow RC, Mann GE (2010) Dietary isoflavones and vascular protection: activation of cellular antioxidant defenses by SERMs or hormesis? Mol Aspects Med 31: 468-477.
15. Wondrak GT, Cabello CM, Villeneuve NF, Zhang S, Ley S, et al. (2008) Cinnamoyl-based Nrf2-activators targeting human skin cell photo-oxidative stress. Free Radic Biol Med 45: 385-395.
16. Zhang DD (2006) Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 38: 769-789.
17. Cheng C, Wang X, Weakley SM, Kougias P, Lin PH, et al. (2010) The soybean isoflavonoid equol blocks ritonavir-induced endothelial dysfunction in porcine pulmonary arteries and human pulmonary artery endothelial cells. J Nutr 140: 12-17.
18. Gimenez I, Lou M, Vargas F, Alvarez-Guerra M, Mayoral JA, et al. (1997) Renal and vascular actions of equol in the rat. J Hypertens 15: 1303-1308. (Pubitemid 27453183)
19. Chin-Dusting JP FL, Lewis TV, Piekarska A, Nestel PJ, Husband A (2001) The vascular avtivity of some isoflavone metabolities: implications for a cardioprotective role. Br J Pharmacol 133: 595-605. (Pubitemid 32591926)
20. Walker HA, Dean TS, Sanders TA, Jackson G, Ritter JM, et al. (2001) The phytoestrogen genistein produces acute nitric oxide-dependent dilation of human forearm vasculature with similar potency to 17beta-estradiol. Circulation 103: 258-262. (Pubitemid 32095412)
21. Mahn K, Borras C, Knock GA, Taylor P, Khan IY, 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)
22. Jackman KA, Woodman OL, Chrissobolis S, Sobey CG (2007) Vasorelaxant and antioxidant activity of the isoflavone metabolite equol in carotid and cerebral arteries. Brain Res 1141: 99-107. (Pubitemid 46365641)
23. Tormala R, Appt S, Clarkson TB, Groop PH, Ronnback M, et al. (2008) Equol production capability is associated with favorable vascular function in postmenopausal women using tibolone; no effect with soy supplementation. Atherosclerosis 198: 174-178. (Pubitemid 351419209)
24. Tormala RM, Appt S, Clarkson TB, Tikkanen MJ, Ylikorkala O, et al. (2007) Individual differences in equol production capability modulate blood pressure in tibolone-treated postmenopausal women: lack of effect of soy supplementation. Climacteric 10: 471-479. (Pubitemid 350211298)
25. Du Y, Villeneuve NF, Wang XJ, Sun Z, Chen W, et al. (2008) Oridonin confers protection against arsenic-induced toxicity through activation of the Nrf2-mediated defensive response. Environ Health Perspect 116: 1154-1161.
26. Zhang T, Wang F, Xu HX, Yi L, Qin Y, et al. Activation of nuclear factor erythroid 2-related factor 2 and PPARgamma plays a role in the genistein-mediated attenuation of oxidative stress-induced endothelial cell injury. Br J Nutr: 1-13.
27. Blair RM, Appt SE, Franke AA, Clarkson TB (2003) Treatment with antibiotics reduces plasma equol concentration in cynomolgus monkeys (Macaca fascicularis). J Nutr 133: 2262-2267. (Pubitemid 36841551)
28. Yuan JP, Wang JH, Liu X (2007) Metabolism of dietary soy isoflavones to equol by human intestinal microflora-implications for health. Mol Nutr Food Res 51: 765-781.
29. Adlercreutz H, Yamada T, Wahala K, Watanabe S (1999) Maternal and neonatal phytoestrogens in Japanese women during birth. Am J Obstet Gynecol 180: 737-743. (Pubitemid 29149155)
30. Setchell KD, Cassidy A (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129: 758S-767S.
31. Adlercreutz H, Mazur W (1997) Phyto-oestrogens and Western diseases. Ann Med 29: 95-120. (Pubitemid 27226319)
32. Nishinaka T, Ichijo Y, Ito M, Kimura M, Katsuyama M, et al. (2007) Curcumin activates human glutathione S-transferase P1 expression through antioxidant response element. Toxicol Lett 170: 238-247. (Pubitemid 46710275)
33. Wiegand H, Wagner AE, Boesch-Saadatmandi C, Kruse HP, Kulling S, et al. (2009) Effect of dietary genistein on Phase II and antioxidant enzymes in rat liver. Cancer Genomics Proteomics 6: 85-92.
34. Hernandez-Montes E, Pollard SE, Vauzour D, Jofre-Montseny L, Rota C, et al. (2006) Activation of glutathione peroxidase via Nrf1 mediates genisteiǹs protection against oxidative endothelial cell injury. Biochem Biophys Res Commun 346: 851-859.
35. Russell KS HM, Sinha D, Clerisme E, Bender JR (2000) Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci U S A 23: 5930-5935. (Pubitemid 30367501)
36. Toth B, Scholz C, Saadat G, Geller A, Schulze S, et al. (2009) Estrogen receptor modulators and estrogen receptor beta immunolabelling in human umbilical vein endothelial cells. Acta Histochem 111: 508-519.
37. Xu SZ, Zhong W, Ghavideldarestani M, Saurabh R, Lindow SW, et al. (2009) Multiple mechanisms of soy isoflavones against oxidative stress-induced endothelium injury. Free Radic Biol Med 47: 167-175.
38. Duncan AM, Merz-Demlow BE, Xu X, Phipps WR, Kurzer MS (2000) Premenopausal equol excretors show plasma hormone profiles associated with lowered risk of breast cancer. Cancer Epidemiol Biomarkers Prev 9: 581-586. (Pubitemid 30396180)
39. Montano MM, Jaiswal AK, Katzenellenbogen BS (1998) Transcriptional regulation of the human quinone reductase gene by antiestrogen-liganded estrogen receptor-alpha and estrogen receptor-beta. J Biol Chem 273: 25443-25449. (Pubitemid 28443313)
40. Yao Y, Brodie AMH, Davidson NE, Kensler TW, Zhou Q (2010) Inhibition of estrogen signaling activates the NRF2 pathway in breast cancer. Breast Cancer Res Treat 124: 585-591.
41. Zhou W Lo SC, Liu JH, Hannink M, Lubahn DB (2007) ERRbeta: a potent inhibitor of Nrf2 transcriptional activity. Mol Cell Endocrinol 278 52-62. (Pubitemid 350183944)
42. Iwasaki K MY, Haneda M, Uchida K, Nakao A, Kobayashi T (2010) Significance of HLA class I antibody-induced antioxidant gene expression for endothelial cell protection against complement attack. Biochem Biophys Res Commun 391: 1210-1215.
43. Langston W, Circu ML, Aw TY (2008) Insulin stimulation of gamma-glutamylcysteine ligase catalytic subunit expression increases endothelial GSH during oxidative stress: influence of low glucose. Free Radic Biol Med 45: 1591-1599.
44. Park SS, Kim YN, Jeon YK, Kim YA, Kim JE, et al. (2005) Genistein-induced apoptosis via Akt signaling pathway in anaplastic large-cell lymphoma. Cancer Chemother Pharmacol 56: 271-278. (Pubitemid 40941797)
45. Heiss EH, Schachner D, Werner ER, Dirsch VM (2009) Active NF-E2-related factor (Nrf2) contributes to keep endothelial NO synthase (eNOS) in the coupled state: role of reactive oxygen species (ROS), eNOS, and heme oxygenase (HO-1) levels. J Biol Chem 284: 31579-31586.
46. Rowlands DJ, Chappel S, Siow RC, Mann GE (2011) Equol-stimulated mitochondrial reactive oxygen species activate endothelial nitric oxide synthase and redox signaling in endothelial cells: roles for F-actin and GPR30. Hypertension 57: 833-840.
47. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, et al. (2000) Membrane Estrogen Receptor Engagement Activates Endothelial Nitric Oxide Synthase via the PI3-Kinase-Akt Pathway in Human Endothelial Cells. Circ Res 87: 677-682.
48. Chung JE, Kim SY, Jo HH, Hwang SJ, Chae B, et al. (2008) Antioxidant effects of equol on bovine aortic endothelial cells. Biochem Biophys Res Commun 375: 420-424.
49. Arora A, Nair MG, Strasburg GM (1998) Antioxidant activities of isoflavones and their biological metabolites in a liposomal system. Arch Biochem Biophys 356: 133-141. (Pubitemid 28387717)
50. Mitchell JH, Gardner PT, McPhail DB, Morrice PC, Collins AR, et al. (1998) Antioxidant efficacy of phytoestrogens in chemical and biological model systems. Arch Biochem Biophys 360: 142-148. (Pubitemid 29010923)
51. Choi EJ (2009) Evaluation of equol function on anti- or prooxidant status in vivo. J Food Sci 74: H65-71.
52. Setchell KD, Zhao X, Jha P, Heubi JE, Brown NM (2009) The pharmacokinetic behavior of the soy isoflavone metabolite S-(-)equol and its diastereoisomer R-(+)equol in healthy adults determined by using stable-isotope-labeled tracers. Am J Clin Nutr 90: 1029-1037.
53. Setchell KD, Zhao X, Shoaf SE, Ragland K (2009) The pharmacokinetics of S-(-)equol administered as SE5-OH tablets to healthy postmenopausal women. J Nutr 139: 2037-2043.
54. Yee S, Burdock GA, Kurata Y, Enomoto Y, Narumi K, et al. (2008) Acute and subchronic toxicity and genotoxicity of SE5-OH, an equol-rich product produced by Lactococcus garvieae. Food Chem Toxicol 46: 2713-2720.