Low-dose perinatal diethylstilbestrol exposure affected behaviors and hypothalamic estrogen receptor-α-positive cells in the mouse

Neurotoxicology and Teratology

Volumn 26, Issue 2, 2004, Pages 261-269

  Tanaka, Mika ^a   Ohtani Kaneko, Ritsuko ^b   Yokosuka, Makoto ^b   Watanabe, Chiho ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Aggressive behavior; Central nervous system; CNS; DES; Diethylstilbestrol; EDs; Endocrine disruptors; ER ; Estrogen receptor immunoreactivity; Low dose diethylstilbestrol; Open field activity; Passive avoidance; Sexual behavior

Indexed keywords

CORN OIL; DIETHYLSTILBESTROL; ESTROGEN RECEPTOR ALPHA; TYROSINE 3 MONOOXYGENASE;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BODY WEIGHT; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GESTATION PERIOD; HYPOTHALAMUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; IMMUNOCOMPETENT CELL; MALE; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; PASSIVE AVOIDANCE; PERFORMANCE; PERINATAL DRUG EXPOSURE; PERINATAL PERIOD; PREGNANCY; PRIORITY JOURNAL; SEX DIFFERENCE; SEXUAL BEHAVIOR;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CELL COUNT; DIETHYLSTILBESTROL; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTROGENS, NON-STEROIDAL; EXPLORATORY BEHAVIOR; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REACTION TIME; RECEPTORS, ESTROGEN; SEX FACTORS; SEXUAL BEHAVIOR; TYROSINE 3-MONOOXYGENASE;

ZEA MAYS;

EID: 1542298284     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2003.11.003     Document Type: Article

References (51)

1. Arnold A.P., Breedlove S.M. Organizational and activational effects of sex steroids on brain behaviour: a reanalysis. Horm. Behav. 19:1985;469-498.
2. Arnold R.A., Gorski A.P. Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7:1984;413-442.
3. Ashby J., Tinwell H., Lefevre P.A., Odum J., Paton D., Millward S.W., Tittensor S., Brooks A.N. Normal sexual development of rats exposed to butyl benzyl phthalate from conception to weaning. Regul. Toxicol. Pharmacol. 26:1997;102-118.
4. Atanassova N., McKinnell C., Turner K.J., Walker M., Fisher J.S., Morley M., Millar M.R., Groome N.P., Sharpe R.M. Comparative effects of neonatal exposure of male rats to potent and weak (environmental) estrogens on spermatogenesis at puberty and the relationship to adult testis size and fertility: evidence for stimulatory effects of low estrogen levels. Endocrinology. 141:2000;3898-3907.
5. Bannai M., Ichikawa M., Nishihara M., Takahashi M. Effect of injection of antisense oligodeoxynucleotides of GAD isozymes into rat ventromedial hypothalamus on food intake and locomotor activity. Brain Res. 784:1998;305-315.
6. Behrens G.H., Petersen P.M., Grotmol T., Sorensen D.R., Torjesen P., Tretlin S., Haugen T.B. Reproductive function in male rats after brief in utero exposure to diethylstilboestrol. Int. J. Androl. 23:2000;366-371.
7. Beyer C. Estrogen and the developing mammalian brain. Anat. Embryol. (Berl.). 199:1999;379-390.
8. Blizard D.A., Lippman H.R., Chen J.J. Sex differences in open-field behavior in the rat: the inductive and activational role of gonadal hormones. Physiol. Behav. 14:1975;601-608.
9. Bronson F.H., Desjardins C. Aggression in adult mice: modification by neonatal injections of gonadal hormones. Science. 161:1968;705-706.
10. Cagen S.Z., Waechter J.M. Jr., Diamond S.S., Breslin W.J., Butala J.H., Jekat F.W., Joiner R.L., Shiotsuka R.N., Veenstra G.E., Harris L.R. Normal reproductive organ development in CF-1 mice following prenatal exposure to bispherol A. Toxicol. Sci. 50:1999;36-44.
11. Christensen L.W., Nance D.M., Gorski R.A. Effects of hypothalamic and preoptic lesions on reproductive behavior in male rats. Brain Res. Bull. 2:1977;137-141.
12. Christian M., Gillies G. Developing hypothalamic dopaminergic neurones as potential targets for environmental estrogens. J. Endocrinol. 160:1999;R1-R6.
13. Csaba G., Dobozy O., Dallo J. Influence of neonatal steroid (diethylstilbestrol, allylestrenol) treatment on the sexual behaviour of the adult rat. Med. Biol. 64:1986;193-195.
14. Dohler K.D., Coquelin A., Davis F., Hines M., Shryne J.E., Gorski R.A. Pre- and postnatal influence of testosterone propionate and diethylstilbestrol on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats. Brain Res. 302:1984;291-295.
15. Ema M., Fujii S., Furukawa M., Kiguchi M., Ikka T., Harazono A. Rat two-generation reproductive toxicity study of bisphenol A. Reprod. Toxicol. 15:2001;505-523.
16. Faber K.A., Hughes C.L. Jr. The effect of neonatal exposure to diethystilbestrol, genistein, and zearalenone on pituitary responsiveness and sexually dimorphic nucleus volume in the castrated adult rat. Biol. Reprod. 45:1991;649-653.
17. Faber K.A., Hughes C.L. Jr. The effect of neonatal diethystilbestrol exposure on luteinizing hormone secretion following ketamine anesthesia and gonadotropin-releasing hormone in castrated postpubertal rats. Biol. Reprod. 48:1993;828-832.
18. Farabollini F., Porrini S., Della Seta D., Bianchi F., Dessi-Fulgheri F. Effects of perinatal exposure to bisphenol A on sociosexual behavior of female and male rats. Environ. Health Perspect. 110:2002;409-414.
19. Ferguson S.A., Flynn K.M., Declos K.B., Newbold R.R. Maternal and offspring toxicity but few sexual dimorphic behaviral alterations results from nonylphenol exposure. Neurotoxic. Teratol. 22:2000;583-591.
20. Franklin K., Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 1997;Academic Press, San Diego, CA.
21. Gupta C. Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals. Proc. Soc. Exp. Biol. Med. 224:2000;61-68.
22. Kaada B.R. Brain mechanism related to aggressive behavior. Clemente C.D., Lindsley D.B. Aggression and Defense: Neural Mechanism and Social Patterns. 1967;95-133 University of California Press, Los Angeles CA.
23. Khurana S., Ranmal S., Ben-Jonathan N. Exposure of newborn male and female rats to environmental estrogens: delayed and sustained hyperprolactinemia and alterations in estrogen receptor expression. Endocrinology. 141:2000;4512-4517.
24. Kubo K., Arai O., Ogata R., Omura M., Hori T., Aou S. Exposure to bisphenol A during the fetal and suckling periods disrupts sexual differentiation of the locus coeruleus and of behavior in the rat. Neurosci. Lett. 304:2001;73-76.
25. Kubo K., Arai O., Omura M., Watanabe R., Ogata R., Aou S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci. Res. 45:2003;345-356.
26. Kwon S., Stedman D.B., Elswick B.A., Cattley R.C., Welsch F. Pubertal development and reproductive functions of Crl:CD BR Sprague-Dawley rats exposed to bisphenol A during prenatal and postnatal development. Toxicol. Sci. 55:2000;399-406.
27. Le Moal M., Simon H. Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiol. Rev. 71:1991;155-234.
28. Lustig R.H. Sex hormone modulation of neural development in vitro. Horm. Behav. 28:1994;383-395.
29. Maeda H., Maki S. Dopaminergic facilitation of recovery from amygdaloid lesions which affect hypothalamic defensive attack in cats. Brain Res. 363:1986;135-140.
30. Maeda H., Sato T., Maki S. Effects of dopamine agonists on hypothalamic defensive attack in cats. Physiol. Behav. 35:1985;89-92.
31. McGill T.E., Ransom T.W. Genotypic change affecting conclusions regarding the mode of inheritance of elements of behaviour. Anim. Behav. 16:1968;88-91.
32. McLachlan J.A., Newbold R.R. Estrogens and development. Environ. Health Perspect. 75:1987;25-27.
33. Meisel R.L., Joppa M.A. Conditioned place preference in female hamsters following aggressive or sexual encounters. Physiol. Behav. 56:1994;1115-1118.
34. Miczek K.A., O'Donnell J.M. Intruder-evoked aggression in isolated and nonisolated mice: effects of psychomotor stimulants and L-dopa. Psychopharmacology (Berl.). 57:1978;47-55.
35. Miranda R.C., Sohrabji F., Toran-Allerand D. Interactions of estrogen with the neurotrophins and their receptors during neural development. Horm. Behav. 28:1994;367-375.
36. Nagao T., Saito Y., Usumi K., Kuwagata M., Imai K. Reproductive function in rats exposed neonatally to bisphenol A and estradiol benzoate. Reprod. Toxicol. 13:1999;303-311.
37. Nagao T., Wada K., Marumo H., Yoshimura S., Ono H. Reproductive effects of nonylphenol in rats after gavage administration: a two-generation study. Reprod. Toxicol. 15:2001;293-315.
38. Odum J., Lefevre P.A., Tinwell H., Van Miller J.P., Joiner R.L., Chapin R.E., Wallis N.T., Ashby J. Comparison of the developmental and reproductive toxicity of diethylstilbestrol administered to rats in utero, lactationally, preweaning, or postweaning. Toxicol. Sci. 68:2002;147-163.
39. Palanza P., Parmigiani S., Liu H., vom Saal F.S. Prenatal exposure to low doses of the estrogenic chemicals diethylstilbestrol and o, p'-DDT alters aggressive behavior of male and female house mice. Pharmacol. Biochem. Behav. 64:1999;665-672.
40. Quadagno D.M., Shyrne J., Anderson C., Gorski R.A. Influence of gonadal hormones on social, sexual, emergence, and open field behaviour in the rat (Rattus norvegicus). Anim. Behav. 20:1972;732-740.
41. Roeling T.A., Veening J.G., Kruk M.R., Peters J.P., Vermelis M.E., Nieuwenhuys R. Efferent connections of the hypothalamic "aggression area" in the rat. Neuroscience. 59:1994;1001-1024.
42. Siegel A., Roeling T.A., Gregg T.R., Kruk M.R. Neuropharmacology of brain-stimulation-evoked aggression. Neurosci. Biobehav. Rev. 23:1999;359-389.
43. Simon N.G., Whalen R.E. Sexual differentiation of androgen-sensitive and estrogen-sensitive regulatory systems for aggressive behavior. Horm. Behav. 21:1987;493-500.
44. Steward J., Cygan D. Ovarian hormones act early in development to feminize adult open-field behavior in the rat. Horm. Behav. 14:1980;20-32.
45. Takahama K., Matsukizono N., Okada Y., Sigemi A., Hirata A., Shiosaka A., Ishibashi H. Learning impairment by diethylstilbestrol (DES) exposure during fatal stage in mice. Jpn. J. Pharmacol. 82:2000;23.
46. Vancutsem P.M., Roessler M.L. Neonatal treatment with tamoxifen causes immediate alterations of the sexually dimorphic nucleus of the preoptic area and medial preoptic area male rats. Teratology. 56:1997;220-228.
47. vom Saal F.S., Quadagno D.M., Even M.D., Keisler L.W., Keisler D.H., Khan S. Paradoxical effects of maternal stress on fetal steroids and postnatal reproductive traits in female mice from different intrauterine positions. Biol. Reprod. 43:1990;751-761.
48. Vom Saal F.S., Nagel S.C., Palanza P., Boechler M., Parmigiani S., Welshons W.V. Estrogenic pesticides: binding relative to estradiol in MCF-7 cells and effect of exposure during fetal life on subsequent territorial behaviour in male mice. Toxicol. Lett. 77:1995;343-350.
49. Vom Saal F.S., Timms B.G., Montano M.M., Palanza P., Thayer K.A., Nagel S.C., Dhar M.D., Ganjam V.K., Parmigiani S., Welshons W.V. Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc. Natl. Acad. Sci. U. S. A. 94:1997;2056-2061.
50. Yoshimura H., Kimura N. Ethopharmacology of copulatory disorder induced by chronic social conflict in male mice. Neurosci. Biobehav. Rev. 15:1991;497-500.
51. Yoshimura H., Yoshida H., Ogawa N. Neonatal gonadal hormone treatment and adult open-field behavior in female rats. Yajubutsu Seishin Kodo. 2:1982;81-85.