Maternal exposure to daidzein alters behaviour and oestrogen receptor α expression in adult female offspring

Behavioural Pharmacology

Volumn 21, Issue 4, 2010, Pages 283-291

  Yu, Chengjun ^a,b   Tai, Fadao ^a   Wu, Ruiyong ^a   Song, Zhenzhen ^a   Zhang, Xia ^c   An, Xiaolei ^a  

^a SHAANXI NORMAL UNIVERSITY   (China)

^b NINGXIA NORMAL UNIVERSITY   (China)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

anxiety; daidzein; memory; mouse; oestrogen receptor a; social behaviours; spatial learning

Indexed keywords

DAIDZEIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN; ISOFLAVONE DERIVATIVE;

ADULTHOOD; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CAGE; COMPARATIVE STUDY; CONTROLLED STUDY; DEVELOPMENT; ENVIRONMENTAL EXPOSURE; FEMALE; IMMUNOCYTOCHEMISTRY; LACTATION; MAZE TEST; MEMORY; MOTHER; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; PREGNANCY; PROGENY; PROTEIN EXPRESSION; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SPATIAL MEMORY; STIMULUS RESPONSE; STRIA TERMINALIS; VIRILIZATION; ANIMAL; ANIMAL BEHAVIOR; BAGG ALBINO MOUSE; BIOSYNTHESIS; BRAIN LEVEL; DRUG EFFECTS; EMOTION; HUMAN RELATION; IMMUNOHISTOCHEMISTRY; MALE; SEXUAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; EMOTIONS; ESTROGEN RECEPTOR ALPHA; ESTROGENS, NON-STEROIDAL; FEMALE; IMMUNOHISTOCHEMISTRY; INTERPERSONAL RELATIONS; ISOFLAVONES; MALE; MAZE LEARNING; MICE; MICE, INBRED BALB C; PREGNANCY; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

EID: 77955176439     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/FBP.0b013e32833aec1a     Document Type: Article

References (85)

1. Adlercreutz H, Mazur W (1997). Phyto-oestrogens and western diseases. Ann Med 29:95-120.
2. 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.
3. Arnold AP, Gorski RA (1984). Gonadal steroid induction of structural sex differences in the nervous system. Annu Rev Neurosci 7:413-442.
4. Astur RS, Tropp J, Sava S, Constable RT, Markus EJ (2004). Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behav Brain Res 151:103-115.
5. Badger TM, Ronis MJ, Hakkak R, Rowlands JC, Korourian S (2002). The health consequences of early soy consumption. J Nutr 132:559-565.
6. Bakker J, Honda S, Harada N, Balthazart J (2002). Sexual partner preference requires a functional aromatase(Cyp19) gene in male mice. Horm Behav 42:158-171.
7. Barrett JR (2002). Soy and children's health: a formula for trouble. Environ Health Perspect 110:294-296.
8. Bronson FH, Dagg CP, Snell GD (1975). Reproduction. In: Green EL, editor. Biology of the laboratory mouse. New York: Dover Publ Inc. pp. 187-204.
9. Bu LH, Lephart ED (2005). Soy isoflavones modulate the expression of BAD and neuron-specific beta III tubulin in male rat brain. Neurosci Lett 385:153-157.
10. Choleris E, Ogawa S, Kavaliers M, Gustafsson JA, Korach KS, Muglia LJ, et al. (2006). Involvement of estrogen receptor alpha, beta and oxytocin in social discrimination: a detailed behavioral analysis with knockout female mice. Genes Brain Behav 5:528-539.
11. Cooke B, Hegstrom CD, Villeneuve LS, Breedlove SM (1998). Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 19:323-362.
12. Dalais F, Rice G, Wahlqvist M, Hus-Hage B, Wattanapenpiaboon N (1998). Urinary excretion of isoflavonoid phytoestrogens in Chinese and Anglo-Celtic populations in Australia. Nutr Res 18:1703-1709.
13. Dalery J, Francois R, de Villard R (1981). The role of hormones in the sex differentiation of the central nervous system in animal and man. Critical study. Ann Med Psychol 139:721-740.
14. Daniel JM, Fader AJ, Spencer AL, Dohanich GP (1997). Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225.
15. De Vries GJ, Villalba C (1997). Brain sexual dimorphism and sex differences in parental and other social behaviours. Ann N Y Acad Sci 807:273-286.
16. Dessi-Fulgheri F, Porrini S, Farabollini F (2002). Effects of perinatal exposure to Bisphenol A on play behaviour of female and male juvenile rats. Environ Health Perspect 110:403-407.
17. Dickerson SM, Gore AC (2007). Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev Endocr Metab Disord 8:143-159.
18. Fader AJ, Hendricson AW, Dohanich GP (1998). Estrogen improves performance of reinforced T-maze alternation and prevents the amnestic effects of scopolamine administered systemically or intrahippocampally. Neurobiol Learn Mem 69:225-240.
19. Ferguson JN, Aldag JM, Insel TR, Young LJ (2001). Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21:8278-8285.
20. Fonseca D, Ward EW (2004). Daidzein. Together with high calcium preserve bone mass and biomechanical strength at multiple sites in ovariectomized mice. Bone 35:489-497.
21. Forest MG (1983). Role of androgens in fetal and pubertal development. Horm Res 18:69-83.
22. Goy RW, Deputte BL (1996). The effects of diethylstilbestrol (DES) before birth on the development of masculine behaviour in juvenile female rhesus monkeys. Horm Behav 30:379-386.
23. Gresack JE, Frick KM (2003). Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task. Brain Res 982:98-107.
24. Gustafsson JA (2003). What pharmacologists can learn from recent advances in estrogen signalling. Trends Pharmacol Sci 24:479-485.
25. Han TM, De Vries GJ (2003). Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the striaterminalis. J Neurobiol 54:502-510.
26. Hewitt SC, Korach KS (2003). Oestrogen receptor knockout mice: roles for oestrogen receptors alpha and beta in reproductive tissues. Reproduction 125:143-149.
27. Hines M, Kaufman FR (1994). Androgen and the development of human sex typical behaviour-rough-and-tumble play and sex of preferred playmates in children with congenital adrenal-hyperplasia (CAH). Child Dev 65:1042-1053.
28. Huang Y, Pan L, Xia X, Feng Y, Jiang C, Cui Y (2008). Long-term effects of phytoestrogen daidzein on penile cavernosal structures in adult rats. Urology 72:220-224.
29. Huddleston GG, Michael RP, Zumpe D, Clancy AN (2003). Estradiol in the male rat amygdala facilitates mounting but not ejaculation. Physiol Behav 79:239-246.
30. Hutchison JB (1997). Gender-specific steroid metabolism in neural differentiation. Cell Mol Neurobiol 17:603-626.
31. Jensen EV, Jacobson HI, Walf AA, Frye CA (2010). Estrogen action: a historic perspective on the implications of considering alternative approaches. Physiol Behav 99:151-162.
32. Jonasson Z (2005). Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci Biobehav Rev 28:811-825.
33. Kelly SJ, Ostrowski NL, Wilson MA (1999). Gender differences in brain and behaviour: hormonal and neural bases. Pharmacol Biochem Behav 64: 655-664.
34. Kendrick KM, Drewett RF (1980). Testosterone-sensitive neurons respond to oestradiol but not to dihydrotestosterone. Nature 286:67-68.
35. Kramer KM, Carr MS, Schmidt JV, Cushing BS (2006). Parental regulation of central patterns of estrogen receptor alpha. Neuroscience 142:165-173.
36. Kudwa AE, Bodo C, Gustafsson JA, Rissman EF (2005). A previously uncharacterized role for estrogen receptor beta: defeminization of male brain and behaviour. Proc Natl Acad Sci USA 102:4608-4612.
37. Kudwa AE, Michopoulos V, Gatewood JD, Rissman EF (2006). Roles of estrogen receptors alpha and beta in differentiation of mouse sexual behaviour. Neuroscience 138:921-928.
38. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA (1996). Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93:5925-5930.
39. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, et al. (1998). Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor b. Endocrinology 139:4252-4263.
40. Latonnelle K, Fostier A, Le Menn F, Bennetau-Pelissero C (2002). Binding affinities of hepatic nuclear estrogen receptors for phytoestrogens in rainbow trout (Oncorhynchus mykiss) and Siberian sturgeon (Acipenser baeri). Gen Comp Endocrinol 129:69-79.
41. Lee YB, Lee HJ, Won MH, Hwang IK, Kang TC, Lee JY, et al. (2004). Soy isoflavones improve spatial delayed matching-to-place performance and reduce cholinergic neuron loss in elderly male rats. J Nutr 134:1827-1831.
42. Lee YB, Lee HJ, Sohn HS (2005). Soy isoflavones and cognitive function. J Nutr Biochem 16:641-649.
43. Leret ML, Molina-Holgado F, Gonzalez MI (1994). The effects of perinatal exposure to estrogens on the sexually dimorphic response to novelty. Physiol Behav 55:371-373.
44. Lo FH, Mak NK, Leung KN (2007). Studies on the anti-tumor activities of the soy isoflavone daidzein on murine neuroblastoma cells. Biomed Pharmacother 61:591-595.
45. Luine V, Attalla S, Mohan G, Costa A, Frankfurt M (2006). Dietary phytoestrogens enhance spatial memory and spine density in the hippocampus and prefrontal cortex of ovariectomized rats. Brain Res 1126:183-187.
46. Luine VN, Jacome LF, Maclusky NJ (2003). Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144:2836-2844.
47. Lund TD, Lephart ED (2001). Dietary soy phytoestrogens produce anxiolytic effects in the elevated plus-maze. Brain Res 913:180-184.
48. Lund TD, Rhees RW, Setchell KD, Lephart ED (2001a). Altered sexually dimorphic nucleus of the preoptic area (SDN-POA) volume in adult Long-Evans rats by dietary soy phytoestrogens. Brain Res 914:92-99.
49. Lund TD, West TW, Tian LY, Bu LH, Simmons DL, Setchell KD, et al. (2001b). Visual spatial memory is enhanced in females rats (but inhibited in males) by dietary soy phytoestrogens. BMC Neurosci 2:20.
50. MacLusky NJ, Naftolin F (1981). Sexual differentiation of the central nervous system. Science 211:1294-1302.
51. Messina M (2000). Soyfoods and soybean phytoestrogens (isoflavones) as possible alternatives to hormone replacement therapy (HRT). J Eur J Cancer 36:71-77.
52. Messina MJ, Persky V, Setchell KD, Barnes S (1994). Soy intake and cancer risk: a review of the in vitro and in vivo data. Nutr Cancer 21:113-131.
53. Moore TO, Karom M, O'Farrell L (2004). The neurobehavioural effects of phytoestrogens in male Syrian hamsters. Brain Res 1016:102-110.
54. Musatov S, Chen W, Pfaff DW, Kaplitt MG, Ogawa S (2006). RNAi-mediated silencing of estrogen receptor a in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc Natl Acad Sci USA 103: 10456-10460.
55. Muthyala RS, Ju YH, Sheng S, Williams LD, Doerge DR, Katzenellenbogen BS, et al. (2004). 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 12:1559-1567.
56. Newman SW (1999). The medial extended amygdala in male reproductive behaviour: a node in the mammalian social behaviour network. Ann N Y Acad Sci 877:242-257.
57. Ogawa S, Lubahn DB, Korach KS, Pfaff DW (1997). Behavioural effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci USA 94:1476-1481.
58. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff PW (1998). Roles of estrogen receptor alpha gene expression in reproduction-related behaviours in female mice. Endocrinology 139:5070-5081.
59. Ogawa S, Chan J, Gustafsson JA, Korach KS, Pfaff DW (2003). Estrogen increases locomotor activity in mice through estrogen receptor a: specificity for the type of activity. Endocrinology 144:230-239.
60. Packard MG, Kohlmaier JR, Alexander GM (1996). Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: interaction with cholinergic systems. Behav Neurosci 110:626-632.
61. Palanza P, Gioiosa L, vom Saal FS, Parmigiani S (2008). Effects of developmental exposure to bisphenol A on brain and behaviour in mice. Environ Res 108:150-157.
62. Pan Y, Anthony M, Watson S, Clarkson TB (2000). Soy phytoestrogens improve radial arm maze performance in ovariectomized retired breeder rats and do not attenuate benefits of 17beta-estradiol treatment. Menopause 7:230-235.
63. Patisaul HB, Bateman HL (2008). Neonatal exposure to endocrine active compounds or an ERb agonist increases adult anxiety and aggression in gonadally intact male rats. Horm Behav 53:580-588.
64. Patisaul HB, Fortino AE, Polston EK (2007). Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A. Neurotoxicology 28:1-12.
65. Ranney A, Petro MS (2009). Resveratrol protects spatial learning in middle-aged C57BL/6 mice from effects of ethanol. Behav Pharmacol 20:330-336.
66. Rasia-Filho AA, Londero RG, Achaval M (2000). Functional activities of the amygdala: an overview. J Psychiatry Neurosci 25:14-23.
67. Ren MQ, Kuhn G, Wegner J, Nurnberg G, Chen J, Ender K (2001). Feeding daidzein to late pregnant sows influences the estrogen receptor beta and type 1 insulin-like growth factor receptor mRNA expression in newborn piglets. J Endocrinol 170:129-135.
68. Rissman EF, Wersinger SR, Fugger HN, Foster TC (1999). Sex with knockout models: behavioural studies of estrogen receptor alpha. Brain Res 835:80-90.
69. Rissman EF, Heck AL, Leonard JE, Shupnik MA, Gustafsson JA (2002). Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc Natl Acad Sci USA 99:3996-4001.
70. Roselli CE, Chambers K (1999). Sex differences in male-typical behaviours in response to androgen and estrogen treatment in rats. Neuroendocrinology 69:290-298.
71. Scordalakes EM, Rissman EF (2004). Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha. Genes Brain Behav 3:20-26.
72. Scordalakes EM, Imwalle DB, Rissman EF (2002). Estrogen's masculine side: mediation of mating in male mice. Reproduction 124:331-338.
73. Setchell KD, Brown NM, Lydeking-Olsen E (2002). The clinical importance of the metabolite equol\a clue to the effectiveness of soy and its isoflavones. J Nutr 132:3577-3584.
74. Setchell KD, Clerici C, Lephart ED, Cole SJ, Heenan C, Castellani D, et al. (2005). S-Equol, a potent ligand for estrogen receptor beta, is the exclusive enantiomeric form of the soy isoflavone metabolite produced by the human bacterial flora. Am J Clin Nutr 81:1072-1079.
75. Shughrue PJ, Lane MV, Merchenthaler I (1997). Comparative distribution of estrogen receptor-alpha and-beta mRNA in the rat central nervous system. J Comp Neurol 388:507-525.
76. Todaka E, Sakurai K, Fukata H, Miyagawa H, Uzuki M, Omori M, et al. (2005). Fetal exposure to phytoestrogens-The difference in phytoestrogen status between mother and fetus. Environ Res 99:195-203.
77. Walf AA, Frye CA (2008). Rapid and estrogen receptor b mediated actions in the hippocampus mediate some functional effects of estrogen. Steroids 73:997-1007.
78. Wang ZX, De Vries GJ (1993). Testosterone effects on paternal behaviour and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res 631:156-160.
79. Wang ZX, Bullock NA, De Vries GJ (1993). Sexual differentiation of vasopressin projections of the bed nucleus of the stria terminalis and medial amygdaloid nucleus in rats. Endocrinology 132:2299-2306.
80. Welshons WV, Nagel SC, vom Saal FS (2006). Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 147:56-69.
81. Wersinger SR, Rissman EF (2000). Estrogen receptor alpha is essential for female-directed chemo-investigatory behaviour but is not required for the pheromone-induced luteinizing hormone surge in male mice. Neuroendocrinol 12:103-110.
82. Wisniewski AB, Cernetich A, Gearhart JP, Klein SL (2005). Perinatal exposure to genistein alters reproductive development and aggressive behaviour in male mice. Physiol Behav 84:327-334.
83. Wood RI (1996). Estradiol, but not dihydrotestosterone, in the medial amygdala facilitates male hamster sex behaviour. Physiol Behav 59:833-841.
84. Zhao R, Wang Y, Zhou Y, Ni Y, Lu L, Grossmann R, et al. (2004). Dietary daidzein influences laying performance of ducks (Anas platyrhynchos) and early post-hatch growth of their hatchlings by modulating gene expression. Comp Biochem Physiol A: Mol Integr Physiol 138:459-466.
85. Ziegler DR, Gallagher M (2005). Spatial memory in middle-aged female rats: assessment of estrogen replacement after ovariectomy. Brain Res 1052:163-173.