Neuroprotective and neurotrophic efficacy of phytoestrogens in cultured hippocampal neurons

Experimental Biology and Medicine

Volumn 227, Issue 7, 2002, Pages 509-519

  Zhao, Lixia ^a   Chen, Qi ^a   Brinton, Roberta Diaz ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Daidzein; Daidzin; Equol; Formononetin; Genistein; Genistin; LDH; MTT; Neuroprotection; Neurotrophism; Phytoestrogens

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; AMYLOID BETA PROTEIN; ANTIOXIDANT; DAIDZEIN; DAIDZIN; EQUOL; ESTRADIOL; ESTROGEN; FORMONONETIN; GENISTEIN; GENISTIN; GLUTAMIC ACID; LACTATE DEHYDROGENASE; PHYTOESTROGEN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFICACY; ENZYME RELEASE; FETUS; HIPPOCAMPUS; MEMBRANE DAMAGE; MEMORY; MITOCHONDRION; NERVE CELL; NERVE CELL MEMBRANE; NERVE FIBER GROWTH; NEUROPROTECTION; NONHUMAN; RAT; SYNAPTOGENESIS;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0036655701     PISSN: 00379727     EISSN: None     Source Type: Journal    
DOI: 10.1177/153537020222700716     Document Type: Article

References (70)

1. Kurzer MS, Xu X. Dietary phytoestrogens. Annu Rev Nutr 17:353-381, 1997.
2. Makela S, Santti R, Salo L, McLachlan JA. Phytoestrogens are partial estrogen agonists in the adult male mouse. Environ Health Perspect 103:123-127, 1995.
3. Stahl S, Chun TY, Gray WG. Phytoestrogens act as estrogen agonists in an estrogen-responsive pituitary cell line. Toxicol Appl Pharmacol 152:41-48, 1998.
4. Bowers JL, Tyulmenkov VV, Jernigan SC, Klinge CM. Resveratrol acts as a mixed agonist/antagonist for estrogen receptors α and β. Endocrinology 141:3657-3667, 2000.
5. Wang C, Kurzer MS. Phytoestrogen concentration determines effects on DNA synthesis in human breast cancer cells. Nutr Cancer 28:236-247, 1997.
6. Zava DT, Duwe G. Estrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr Cancer 27:31-40, 1997.
7. Dixon-Shanies D, Shaikh N. Growth inhibition of human breast cancer cells by herbs and phytoestrogens. Oncol Rep 6:1383-1387, 1999.
8. Balabhadrapathruni S, Thomas TJ, Yurkow EJ, Amenta PS, Thomas T. Effects of genistein and structurally related phytoestrogens on cell cycle kinetics and apoptosis in MDA-MB-468 human breast cancer cells. Oncol Rep 7:3-12, 2000.
9. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139:4252-4263, 1998.
10. Nikov GN, Hopkins NE, Boue S, Alworth WL. Interactions of dietary estrogens with human estrogen receptors and the effect on estrogen receptor-estrogen response element complex formation. Environ Health Perspect 108:867-872, 2000.
11. Jacob DA, Temple JL, Patisaul HB, Young LJ, Rissman EF. Coumestrol antagonizes neuroendocrine actions of estrogen via the estrogen receptor α. Exp Biol Med 226:301-306, 2001.
12. Adlercreutz H, Bannwart C, Wahala K, Makela T, Brunow G, Hase T, Arosemena PJ, Kellis JT Jr, Vickery LE. Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol 44:147-153, 1993.
13. Monti E, Sinha BK. Antiproliferative effect of genistein and adriamycin against estrogen-dependent and -independent human breast carcinoma cell lines. Anticancer Res 14:1221-1226, 1994.
14. Kulling SE, Metzler M. Induction of micronuclei, DNA strand breaks and HPRT mutations in cultured Chinese hamster V79 cells by the phytoestrogen coumoestrol. Food Chem Toxicol 35:605-613, 1997.
15. Harper A, Kerr DJ, Gescher A, Chipman JK. Antioxidant effects of isoflavonoids and lignans, and protection against DNA oxidation. Free Radic Res 31:149-160, 1999.
16. Pino AM, Valladares LE, Palma MA, Mancilla AM, Yanez M, Albala C. Dietary isoflavones affect sex hormone-binding globulin levels in postmenopausal women. J Clin Endocrinol Metab 85:2797-2800, 2000.
17. Brinton RD. Estrogens and Alzheimer's Disease. In: Marwah J, Teitelbaum H, Eds. Advances in Neurodegenerative Disorders. Vol.2: Alzheimer's and Aging. Scottsdale, AZ: Prominent Press, pp 99-130, 1998.
18. Sherwin BB. Oestrogen and cognitive function throughout the female lifespan. Novartis Found Symp 230:188-196; discussion 196-201, 2000.
19. Birge SJ. Is there a role for estrogen replacement therapy in the prevention and treatment of dementia? [see comments]. J Am Geriatr Soc 44:865-870, 1996.
20. Paganini-Hill A, Henderson VW. Estrogen replacement therapy and risk of Alzheimer disease. Arch Intern Med 156:2213-2217, 1996.
21. Tang MX, Jacobs D, Stern Y, Marder K, Schofield P, Gurland B, Andrews H, Mayeux R. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. [see comments]. Lancet 348:429-432, 1996.
22. Kawas C, Resnick S, Morrison A, Brookmeyer R, Corrada M, Zonderman A, Bacal C, Lingle DD, Metter E. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore Longitudinal Study of Aging. [erratum appears in Neurology 1998 Aug;51(2):654]. Neurology 48:1517-1521, 1997.
23. Yaffe K, Sawaya G, Lieberburg I, Grady D. Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. J Am Med Assoc 279:688-695, 1998.
24. Henderson VW. Hormone Therapy and the Brain: A Clinical Perspective on the Role of Estrogen. New York: Parthenon Publishing, 2000.
25. Green PS, Gridley KE, Simpkins JW. Estradiol protects against β-amyloid (25-35)-induced toxicity in SK-N-SH human neuroblastoma cells. Neurosci Lett 218:165-168, 1996.
26. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541, 1997.
27. Brinton RD, Chen S, Montoya M, Hsieh D, Minaya J, Kim J, Chu HP. The women's health initiative estrogen replacement therapy is neurotrophic and neuroprotective. Neurobiol Aging 21:457-496, 2000.
28. Brinton RD. Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease: recent insights and remaining challenges. Learn Mem 8:121-133, 2001.
29. Toran-Allerand CD. On the genesis of sexual differentiation of the general nervous system: morphogenetic consequences of steroidal exposure and possible role of α-fetoprotein. Prog Brain Res 61:63-98, 1984.
30. Brinton RD. 17β-estradiol induction of filopodial growth in cultured hippocampal neurons within minutes of exposure. Mol Cell Neurosci 4:36-46, 1993.
31. Murphy DD, Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059-4068, 1996.
32. Brinton RD, Tran J, Proffitt P, Montoya M. 17β-Estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem Res 22:1339-1351, 1997.
33. Woolley CS. Electrophysiological and cellular effects of estrogen on neuronal function. Crit Rev Neurobiol 13:1-20, 1999.
34. Sandstrom NJ, Williams CL. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115:384-393, 2001.
35. Hammond CB. Women's concerns with hormone replacement therapy-compliance issues. Fertil Steril 62:157S-160S, 1994.
36. Grady D, Gebretsadik T, Kerlikowske K, Ernster V, Fetitti Petitti D. Hormone replacement therapy and endometrial cancer risk: a metaanalysis. Obstet Gynecol 85:304-313, 1995.
37. Anonymous. Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Collaborative Group on Hormonal Factors in Breast Cancer [see comments] [published erratum appears in Lancet 1997 Nov 15;350(9089): 1484]. Lancet 350:1047-1059, 1997.
38. Welshons WV, Murphy CS, Koch R, Calaf G, Jordan VC. Stimulation of breast cancer cells in vitro by the environmental estrogen enterolactone and the phytoestrogen equol. Breast Cancer Res Treat 10:169-175, 1987.
39. Peterson G, Barnes S. Genistein inhibition of the growth of human breast cancer cells: independence from estrogen receptors and the multi-drug resistance gene. Biochem Biophys Res Commun 179:661-667, 1991.
40. Matsukawa Y, Marui N, Sakai T, Satomi Y, Yoshida M, Matsumoto K, Nishino H, Aoike A. Genistein arrests cell cycle progression at G2-M. Cancer Res 53:1328-1331, 1993.
41. Clarke R, Hilakivi-Clarke L, Cho E, James MR, Leonessa F. Estrogens, phytoestrogens, and breast cancer. Adv Exp Med Biol 401:63-85, 1996.
42. Barnes S, Sfakianos J, Coward L, Kirk M. Soy isoflavonoids and cancer prevention: underlying biochemical and pharmacological issues. Adv Exp Med Biol 401:87-100, 1996.
43. Ingram D, Sanders K, Kolybaba M, Lopez D. Case-control study of phyto-oestrogens and breast cancer [see comments]. Lancet 350:990-994, 1997.
44. Messina M, Barnes S, Setchell KD. Phyto-oestrogens and breast cancer [comment]. Lancet 350:971-972, 1997.
45. Behl C. Vitamin E and other antioxidants in neuroprotection. Int J Vitam Nutr Res 69:213-219, 1999.
46. Mazur W. Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab 12:729-742, 1998.
47. Henderson VW. Estrogen, cognition, and a woman's risk of Alzheimer's disease. Am J Med 103:11S-18S, 1997.
48. Brinton RD, Proffitt P, Tran J, Luu R. Equilin, a principal component of the estrogen replacement therapy premarin, increases the growth of cortical neurons via an NMDA receptor-dependent mechanism. Exp Neurol 147:211-220, 1997.
49. Singh M, Meyer EM, Millard WJ, Simpkins JW. Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 644:305-312, 1994.
50. Simpkins JW, Green PS, Gridley KE, Singh M, de Fiebre NC, Rajakumar G. Role of estrogen replacement therapy in memory enhancement and the prevention of neuronal loss associated with Alzheimer's disease. Am J Med 103:19S-25S, 1997.
51. Drake EB, Henderson VW, Stanczyk FZ, McCleary CA, Brown WS, Smith CA, Rizzo AA, Murdock GA, Buckwalter JG. Associations between circulating sex steroid hormones and cognition in normal elderly women. Neurology 54:599-603, 2000.
52. Dubal DB, Shughrue PJ, Wilson ME, Merchenthaler I, Wise PM, Kindy MS, Wise PM. Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J Neurosci 19:6385-6393, 1999.
53. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I. Estrogen receptor α not β, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci U S A 98:1952-1957, 2001.
54. Rissman EF, Wersinger SR, Taylor JA, Lubahn DB. Estrogen receptor function as revealed by knockout studies: neuroendocrine and behavioral aspects. Horm Behav 31:232-243, 1997.
55. Racher AJ, Looby D, Griffiths JB. Use of lactate dehydrogenase release to assess changes in culture viability. Cytotechnology 3:301-307, 1990.
56. Legrand C, Bour JM, Jacob C, Capiaumont J, Martial A, Marc A, Wudtke M, Kretzmer G, Demangel C, Duval D. Lactate dehydrogenase (LDH) activity of the cultured eukaryotic cells as marker of the number of dead cells in the medium [corrected] [published erratum appears in J Biotechnol 1993 Nov;31(2):234]. J Biotechnol 25:231-243, 1992.
57. Liu Y, Peterson DA, Kimura H, Schubert D. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 69:581-593, 1997.
58. Morgan DM. Tetrazolium (MTT) assay for cellular viability and activity. Methods Mol Biol 79:179-183, 1998.
59. Arechabala B, Coiffard C, Rivalland P, Coiffard LJ, de Roeck-Holtzhauer Y. Comparison of cytotoxicity of various surfactants tested on normal human fibroblast cultures using the neutral red test, MTT assay and LDH release. J Appl Toxicol 19:163-165, 1999.
60. Lobner D. Comparison of the LDH and MTT assays for quantifying cell death: validity for neuronal apoptosis? J Neurosci Methods 96:147-152, 2000.
61. Ruiz-Larrea MB, Mohan AR, Paganga G, Miller NJ, Bolwell GP, Rice-Evans CA. Antioxidant activity of phytoestrogenic isoflavones. Free Radic Res 26:63-70, 1997.
62. Mitchell JH, Gardner PT, McPhail DB, Morrice PC, Collins AR, Duthie GG. Antioxidant efficacy of phytoestrogens in chemical and biological model systems. Arch Biochem Biophys 360:142-148, 1998.
63. Singh M, Setalo G, Jr, Guan X, Warren M, Toran-Allerand CD. Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 19:1179-1188, 1999.
64. Singer CA, Figueroa-Masot XA, Batchelor RH, Dorsa DM. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci 19:2455-2463, 1999.
65. Singh M. Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of the cerebral cortex. Endocrine 14:407-415, 2001.
66. Pan Y, Anthony M, Watson S, Clarkson TB. Soy phytoestrogens improve radial arm maze performance in ovariectomized retired breeder rats and do not attenuate benefits of 17β-estradiol treatment. [see comments]. Menopause 7:230-235, 2000.
67. Rice M, Graves A, Larson E. Estrogen replacement therapy and cognition: role of phytoestrogens (abstract). Gerontologist 35(Suppl 1):169, 1995.
68. White L, Petrovitch H, Ross G, Masaki K, Hardman J, Nelson J, Davis D, Markesbery W. Brain aging and midlife tofu consumption. J Am Coll Nutr 19:242-255, 2000.
69. Ogura C, Nakamoto H, Uema T, Yamamoto K, Yonemori T, Yoshimura T. Prevalence of senile dementia in Okinawa, Japan. COSEPO Group. Study Group of Epidemiology for Psychiatry in Okinawa. Int J Epidemiol 24:373-380, 1995.
70. Suh GH, Shah A. A review of the epidemiological transition in dementia: cross-national comparisons of the indices related to Alzheimer's disease and vascular dementia. Acta Psychiatr Scand 104:4-11, 2001.