Potentiation of brain mitochondrial function by S-equol and R/S-equol estrogen receptor β-selective phytoSERM treatments

Brain Research

Volumn 1514, Issue , 2013, Pages 128-141

  Yao, Jia ^a   Zhao, Liqin ^a   Mao, Zisu ^a   Chen, Shuhua ^a   Wong, Karren Carmen ^a   To, Jimmy ^a   Brinton, Roberta Diaz ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Bioenergetics; Equol; Mitochondria; Oxidative stress; PhytoSERM

Indexed keywords

AMYLOID BETA PROTEIN; CHOLESTEROL; DAIDZEIN; EQUOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR BETA SELECTIVE PHYTOESTROGEN; GENISTEIN; GLUCOSE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; BIOENERGY; BRAIN NERVE CELL; DRUG EFFECT; ENERGY YIELD; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GLUCOSE METABOLISM; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; LIPID METABOLISM; LIPID PEROXIDATION; MENOPAUSE RELATED DISORDER; MITOCHONDRION; NEUROPROTECTION; NONHUMAN; OVARIECTOMY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN; UTERUS WEIGHT;

ANIMALS; BRAIN; CELLS, CULTURED; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; EMBRYO, MAMMALIAN; ENERGY METABOLISM; EQUOL; ESTROGEN RECEPTOR BETA; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LIPID PEROXIDATION; MICE; MICE, INBRED C57BL; MITOCHONDRIA; NEURONS; OVARIECTOMY; PHYTOESTROGENS; PREGNANCY; PYRUVATE DEHYDROGENASE COMPLEX; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84878478952     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.02.021     Document Type: Article

References (60)

1. H. Akaza, N. Miyanaga, N. Takashima, S. Naito, Y. Hirao, T. Tsukamoto, T. Fujioka, M. Mori, W.J. Kim, J.M. Song, and A.J. Pantuck Comparisons of percent equol producers between prostate cancer patients and controls: case-controlled studies of isoflavones in Japanese, Korean and American residents Jpn. J. Clin Oncol. 34 2004 86 89
2. S. Asthana, R.D. Brinton, V.W. Henderson, B.S. McEwen, J.H. Morrison, and P.J. Schmidt Frontiers proposal. National Institute on Aging bench to bedside: estrogen as a case study Age (Dordr) 31 2009 199 210
3. C. Atkinson, C.L. Frankenfeld, and J.W. Lampe Gut bacterial metabolism of the soy isoflavone daidzein: exploring the relevance to human health Exp. Biol. Med. (Maywood) 230 2005 155 170
4. M.F. Beal Mitochondria take center stage in aging and neurodegeneration Ann. Neurol. 58 2005 495 505
5. R.D. Brinton The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications Trends Neurosci. 31 2008 529 537
6. R.D. Brinton Estrogen-induced plasticity from cells to circuits: predictions for cognitive function Trends Pharmacol. Sci. 30 2009 212 222
7. N.M. Brown, C.A. Belles, S.L. Lindley, L.D. Zimmer-Nechemias, X. Zhao, D.P. Witte, M.O. Kim, and K.D. Setchell The chemopreventive action of equol enantiomers in a chemically induced animal model of breast cancer Carcinogenesis 31 2010 886 893
8. R.A. Dixon Phytoestrogens Annu. Rev. Plant Biol. 55 2004 225 261
9. G.E. Gibson, H.L. Chen, H. Xu, L. Qiu, Z. Xu, T.T. Denton, and Q. Shi Deficits in the mitochondrial enzyme alpha-ketoglutarate dehydrogenase lead to Alzheimer's disease-like calcium dysregulation Neurobiol. Aging 33 1121 2012 e13 e24
10. E.R. Gilbert, and D. Liu Anti-diabetic functions of soy isoflavone genistein: mechanisms underlying its effects on pancreatic beta-cell function Food Funct 2012
11. M.A. Goetzl, P.J. Van Veldhuizen, and J.B. Thrasher Effects of soy phytoestrogens on the prostate Prostate Cancer Prostatic. Dis. 10 2007 216 223
12. R. Gopaul, H.E. Knaggs, and E.D. Lephart Biochemical investigation and gene analysis of equol: a plant and soy-derived isoflavonoid with antiaging and antioxidant properties with potential human skin applications Biofactors 38 2012 44 52
13. M.K. Hagen, A. Ludke, A.S. Araujo, R.H. Mendes, T.G. Fernandes, J.M. Mandarino, S. Llesuy, E. Vogt de Jong, and A. Bello-Klein Antioxidant characterization of soy derived products in vitro and the effect of a soy diet on peripheral markers of oxidative stress in a heart disease model Can. J. Physiol. Pharmacol. 90 2012 1095 1103
14. C.B. Hammond Women's concerns with hormone replacement therapy - compliance issues Fertil. Steril. 62 1994 157S 160S
15. R.W. Irwin, J. Yao, R.T. Hamilton, E. Cadenas, R.D. Brinton, and J. Nilsen Progesterone and estrogen regulate oxidative metabolism in brain mitochondria Endocrinology 149 2008 3167 3175
16. N. Ishiwata, M.K. Melby, S. Mizuno, and S. Watanabe New equol supplement for relieving menopausal symptoms: randomized, placebo-controlled trial of Japanese women Menopause 16 2009 141 148
17. R.L. Jackson, J.S. Greiwe, P.B. Desai, and R.J. Schwen Single-dose and steady-state pharmacokinetic studies of S-equol, a potent nonhormonal, estrogen receptor β-agonist being developed for the treatment of menopausal symptoms Menopause 1 2010
18. H.J. Jou, S.C. Wu, F.W. Chang, P.Y. Ling, K.S. Chu, and W.H. Wu Effect of intestinal production of equol on menopausal symptoms in women treated with soy isoflavones Int. J. Gynaecol. Obstet. 102 2008 44 49
19. J.C. Lai, and A.J. Cooper Brain alpha-ketoglutarate dehydrogenase complex: kinetic properties, regional distribution, and effects of inhibitors J. Neurochem. 47 1986 1376 1386
20. A. Lateef, A.Q. Khan, M. Tahir, R. Khan, M.U. Rehman, F. Ali, O.O. Hamiza, and S. Sultana Androgen deprivation by flutamide modulates uPAR, MMP-9 expressions, lipid profile, and oxidative stress: amelioration by daidzein Mol. Cell Biochem. 2012
21. M.T. Lin, and M.F. Beal Alzheimer's APP mangles mitochondria Nat. Med. 12 2006 1241 1243
22. Y. Ma, J.C. Sullivan, and D.A. Schreihofer Dietary genistein and equol (4′,7-isoflavandiol) reduce oxidative stress and protect rats against focal cerebral ischemia Am. J. Physiol. Regul. Integr. Comp. Physiol. 299 2010 R871 R877
23. P.J. Magee, M. Raschke, C. Steiner, J.G. Duffin, B.L. Pool-Zobel, T. Jokela, K. Wahala, and I.R. Rowland Equol: a comparison of the effects of the racemic compound with that of the purified S-enantiomer on the growth, invasion, and DNA integrity of breast and prostate cells in vitro Nutr. Cancer 54 2006 232 242
24. P.I. Moreira, P.L. Harris, X. Zhu, M.S. Santos, C.R. Oliveira, M.A. Smith, and G. Perry Lipoic acid and N-acetyl cysteine decrease mitochondrial-related oxidative stress in Alzheimer disease patient fibroblasts J. Alzheimer's Dis. 12 2007 195 206
25. R.S. Muthyala, Y.H. Ju, S. Sheng, L.D. Williams, D.R. Doerge, B.S. Katzenellenbogen, W.G. Helferich, and J.A. Katzenellenbogen Equol, a natural estrogenic metabolite from soy isoflavones: convenient preparation and resolution of R- and S-equols and their differing binding and biological activity through estrogen receptors alpha and beta Bioorg. Med. Chem. 12 2004 1559 1567
26. J. Nilsen, R.W. Irwin, T.K. Gallaher, and R.D. Brinton Estradiol in vivo regulation of brain mitochondrial proteome J. Neurosci. 27 2007 14069 14077
27. A. Nunomura, G. Perry, G. Aliev, K. Hirai, A. Takeda, E.K. Balraj, P.K. Jones, H. Ghanbari, T. Wataya, S. Shimohama, S. Chiba, C.S. Atwood, R.B. Petersen, and M.A. Smith Oxidative damage is the earliest event in Alzheimer disease J. Neuropathol. Exp. Neurol. 60 2001 759 767
28. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 2003 409 421
29. L. Packer, and E. Cadenas Oxidants and antioxidants revisited. New concepts of oxidative stress Free Radical Res. 41 2007 951 952
30. P.M. Ravdin, K.A. Cronin, N. Howlader, C.D. Berg, R.T. Chlebowski, E.J. Feuer, B.K. Edwards, and D.A. Berry The decrease in breast-cancer incidence in 2003 in the United States N. Engl. J. Med. 356 2007 1670 1674
31. T.E. Richardson, and J.W. Simpkins R- and S-Equol have equivalent cytoprotective effects in Friedreich's ataxia. BMC Pharmacol. Toxicol. 13 2012 12
32. D.F. Romagnolo, and O.I. Selmin Flavonoids and cancer prevention: a review of the evidence J. Nutr. Gerontol. Geriatr. 31 2012 206 238
33. D.A. Schreihofer, and L. Redmond Soy phytoestrogens are neuroprotective against stroke-like injury in vitro Neuroscience 158 2009 602 609
34. K.D. Setchell, S.P. Borriello, P. Hulme, D.N. Kirk, and M. Axelson Nonsteroidal estrogens of dietary origin: possible roles in hormone-dependent disease Am. J. Clin Nutr. 40 1984 569 578
35. K.D. Setchell Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones Am. J. Clin Nutr. 68 1998 1333S 1346S
36. K.D. Setchell, N.M. Brown, and E. Lydeking-Olsen The clinical importance of the metabolite equol-a clue to the effectiveness of soy and its isoflavones J. Nutr. 132 2002 3577 3584
37. K.D. Setchell, C. Clerici, E.D. Lephart, S.J. Cole, C. Heenan, D. Castellani, B.E. Wolfe, L. Nechemias-Zimmer, N.M. Brown, T.D. Lund, R.J. Handa, and J.E. Heubi S-equol, a potent ligand for estrogen receptor beta, is the exclusive enantiomeric form of the soy isoflavone metabolite produced by human intestinal bacterial flora Am. J. Clin Nutr. 81 2005 1072 1079
38. K.D. Setchell, and S.J. Cole Method of defining equol-producer status and its frequency among vegetarians J. Nutr. 136 2006 2188 2193
39. K.D. Setchell, X. Zhao, P. Jha, J.E. Heubi, and N.M. Brown 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 2009 1029 1037
40. K.D. Setchell, and C. Clerici Equol: history, chemistry, and formation J. Nutr. 140 2010 1355S 1362S
41. K.D. Setchell, and C. Clerici Equol: pharmacokinetics and biological actions J. Nutr. 140 2010 1363S 1368S
42. Q. Shi, H. Xu, H. Yu, N. Zhang, Y. Ye, A.G. Estevez, H. Deng, and G.E. Gibson Inactivation and reactivation of the mitochondrial alpha-ketoglutarate dehydrogenase complex J. Biol. Chem. 286 2011 17640 17648
43. S. Shinkaruk, C. Carreau, G. Flouriot, C. Bennetau-Pelissero, and M. Potier Comparative effects of R- and S-equol and implication of transactivation functions (AF-1 and AF-2) in estrogen receptor-induced transcriptional activity Nutrients 2 2010 340 354
44. N.A.M. Society The role of soy isoflavones in menopausal health: report of the North American Menopause Society/Wulf H. Utian Translational Science Symposium in Chicago, IL (October 2010) Menopause 18 2011 732 753
45. F.Z. Stanczyk, J.P. Hapgood, S. Winer, and D.R. Mishell Jr. Progestogens used in postmenopausal hormone therapy: differences in their pharmacological properties, intracellular actions, and clinical effects Endocr. Rev 2012
46. S. Uchiyama, T. Ueno, K. Masaki, S. Shimizu, T. Aso, and T. Shirota The cross-sectional study of the relationship between soy isoflavones, equol and the menopausal symptoms in Japanese women J. Jpn. Menopause Soc. 15 2007 28 37
47. H. Vatanparast, and P.D. Chilibeck Does the effect of soy phytoestrogens on bone in postmenopausal women depend on the equol-producing phenotype? Nutr. Rev. 65 2007 294 299
48. J. Vina, C. Borras, J. Gambini, J. Sastre, and F.V. Pallardo Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds FEBS Lett. 579 2005 2541 2545
49. D.C. Vitale, C. Piazza, B. Melilli, F. Drago, and S. Salomone Isoflavones: estrogenic activity, biological effect and bioavailability Eur. J. Drug Metab Pharmacokinet. 2012
50. J. Yao, R.W. Irwin, L. Zhao, J. Nilsen, R.T. Hamilton, and R.D. Brinton Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease Proc. Nat. Acad. Sci. U.S.A. 106 2009 14670 14675
51. J. Yao, S. Chen, Z. Mao, E. Cadenas, and R.D. Brinton 2-Deoxy-d-glucose treatment induces ketogenesis, sustains mitochondrial function, and reduces pathology in female mouse model of Alzheimer's disease PLoS One 6 2011 e21788
52. J. Yao, R. Irwin, S. Chen, R. Hamilton, E. Cadenas, and R.D. Brinton Ovarian hormone loss induces bioenergetic deficits and mitochondrial beta-amyloid Neurobiol. Aging 33 2012 1507 1521
53. S. Yee, G.A. Burdock, Y. Kurata, Y. Enomoto, K. Narumi, S. Hamada, T. Itoh, Y. Shimomura, and T. Ueno Acute and subchronic toxicity and genotoxicity of SE5-OH, an equol-rich product produced by Lactococcus garvieae Food Chem. Toxicol. 46 2008 2713 2720
54. F. Yin, H. Sancheti, and E. Cadenas Silencing of nicotinamide nucleotide transhydrogenase impairs cellular redox homeostasis and energy metabolism in PC12 cells Biochim. Biophys. Acta 1817 2012 401 409
55. L. Zhao, and R.D. Brinton WHI and WHIMS follow-up and human studies of soy isoflavones on cognition Expert. Rev. Neurother. 7 2007 1549 1564
56. L. Zhao, Z. Mao, and R.D. Brinton A select combination of clinically relevant phytoestrogens enhances estrogen receptor beta-binding selectivity and neuroprotective activities in vitro and in vivo Endocrinology 150 2009 770 783
57. L. Zhao, Z. Mao, L.S. Schneider, and R.D. Brinton Estrogen receptor beta-selective phytoestrogenic formulation prevents physical and neurological changes in a preclinical model of human menopause Menopause 18 2011 1131 1142
58. L. Zhao, T.E. Morgan, Z. Mao, S. Lin, E. Cadenas, C.E. Finch, C.J. Pike, W.J. Mack, and R.D. Brinton Continuous versus cyclic progesterone exposure differentially regulates hippocampal gene expression and functional profiles PLoS One 7 2012 e31267
59. W. Zheng, Z.Y. Ma, F. Li, and G. Wang [Anti-invasion effects of R- and S-enantiomers of equol on prostate cancer PC3, DU145 cells] Wei Sheng Yan Jiu 40 423-425 2011 430
60. R.G. Ziegler Phytoestrogens and breast cancer Am. J. Clin. Nutr. 79 2004 183 184