Environmental-like exposure to low levels of estrogen affects sexual behavior and physiology of female rats

Endocrinology

Volumn 149, Issue 11, 2008, Pages 5592-5598

  Della Seta, Daniele ^a   Farabollini, Francesca ^a   Dessì Fulgheri, Francesco ^b   Fusani, Leonida ^c  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF FERRARA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN; ETHINYLESTRADIOL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; CONTROLLED STUDY; COPULATION; ENVIRONMENTAL EXPOSURE; ESTRADIOL BLOOD LEVEL; ESTRUS CYCLE; FEMALE; LORDOSIS; NONHUMAN; PRIORITY JOURNAL; RAT; REPRODUCTIVE SUCCESS; SEXUAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; ENVIRONMENTAL EXPOSURE; ESTROGENS; ETHINYL ESTRADIOL; FEMALE; MALE; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; WATER POLLUTANTS, CHEMICAL;

EID: 54349126863     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0113     Document Type: Article

References (74)

1. Arnold AP, Gorski RA 1984 Gonadal steroid induction of structural sex differences in the central nervous system. Ann Rev Neurosci 7:413-442
2. Morris JA, Jordan CL, Breedlove SM 2004 Sexual differentiation of the vertebrate nervous system. Nat Neurosci 7:1034-1039
3. McEwen BS, Lieberburg I, Chaptal C, Krey LC1977 Aromatization: important for sexual differentiation of neonatal rat brain. Horm Behav 9:249-263
4. MacLusky NJ, Naftolin F 1981 Sexual differentiation of the central nervous system. Science 211:1294-1302
5. Gorski RA 1985 Sexual dimorphisms of the brain. J Anim Sci 61:38-61
6. Pereira OC, Carvalho NF, Carlos CP 1997 Perinatal estrogen exposure: later repercussion on the fertility of rats. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 118:241-245
7. Fitch RH, Denenberg VH 1998 A role for ovarian hormones in sexual differentiation of the brain. Behav Brain Sci 21:311-327
8. McEwen BS, Alves SE 1999 Estrogen actions in the central nervous system. Endocrinol Rev 20:279-307
9. MacLusky NJ, Lieberburg I, McEwen BS 1979 The development of estrogen receptor systems in the rat brain: perinatal development. Brain Res 178:129 -142
10. Breedlove SM, Hampson E 2002 Sexual differentiation of the brain and behavior. In: Becker JB, Breedlove SM, Crews D, McCarthy MM, eds. Behavioral endocrinology. Cambridge, MA: MIT Press/Bradford Books; 75-115
11. Bakker J, De Mees C, Douhard Q, Balthazart J, Gabant P, Szpirer J, Szpirer C 2006 α-Fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat Neurosci 9:220-226
12. vom Saal FS 1989 Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero. J Anim Sci 67:1824-1840
13. Colborn T, vom Saal FS, Soto AM 1993 Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101:378-384
14. Davis DL, Bradlow HL, Wolff M, Woodruff T, Hoel DG, Anton-Culver H 1993 Medical hypothesis: xenoestrogens as preventable causes of breast cancer. Environ Health Perspect 101:372-377
15. Welshons WV, Thayer KA, Judy BM, Curran EM, vom Saal FS 2003 Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ Health Perspect 8:994-1006
16. Sharpe RM, Fisher JS, Millar MM, Jobling S, Sumpter JP 1995 Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ Health Perspect 103:1136-1143
17. Newbold RR, Banks EP, Bullock B, Jefferson WN 2001 Uterine adenocarcinoma in mice treated neonatally with genistein. Cancer Res 61:4325-4328
18. Zala SM, Penn DJ 2004 Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Animal Behav 68:649-664
19. vom Saal FS, Nagel SC, Palanza P, Boechler M, Parmigiani S, Welshons WV 1995 Estrogenic pesticides: binding relative to estradiol in MCF-7 cells and effects of exposure during foetal life on subsequent territorial behaviour in male mice. Toxicol Lett 77:343-350
20. McClintock MK 1987 A functional approach to the behavioral endocrinology of rodents. In: Crews D, ed. Psychobiology of reproductive behavior. Englewood Cliffs, NJ: Prentice Hall; 176-203
21. Pfaus JG 1999 Revisiting the concept of sexual motivation. Annu Rev Sex Res 10:120-156
22. Avitsur R, Yirmiya R 1999 The partner preference paradigm: a method to study sexual motivation and performance of female rats. Brain Res Brain Res Protoc 3:320-325
23. Pfaus JG, Kippin TE, Centeno S 2001 Conditioning and sexual behavior: a review. Horm Behav 40:291-321
24. Fadem BH, Barfield RJ, Whalen RE 1979 Dose-response and time-response relationships between progesterone and the display of patterns of receptive and proceptive behavior in the female rat. Horm Behav 13:40-48
25. Erskine MS 1989 Solicitation behavior in the estrus female rat: a review. Horm Behav 23:473-502
26. Farabollini F, Porrini S, Della Seta D, Bianchi F, Dessì-Fulgheri F 2002 Effects of perinatal exposure to bisphenol A on sociosexual behaviour of female and male rats. Environ Health Perspect 110:409-413
27. Gould JC, Leonard LS, Maness SC, Wagner BL, Conner K, Zacharewski T, Safe S, McDonnell DP, Gaido KW 1998 Bisphenol A interacts with the estrogen receptor α in a distinct manner from estradiol. Mol Cell Endocrinol 142:203-214
28. MacLusky NJ, Hajszan T, Leranth C 2005 The environmental estrogen bisphenol A inhibits estradiol-induced hippocampal synaptogenesis. Environ Health Perspect 113:675-679
29. Smithells RW 1981 Oral contraceptives and birth defects. Dev Med Child Neurol 23:369-372
30. Li D, Daling JR, Mueller BA, Hickok DE, Fantel AG, Weiss NS 1995 Oral contraceptive use after conception in relation to the risk of congenital urinary tract anomalies. Teratology 51:30-36
31. Thayer KA, Ruhlen RL, Howdeshell KL, Buchanan DL, Cooke PS, Preziosi D, Welshons WV, Haseman J, vom Saal FS 2001 Altered prostate growth and daily sperm production in male mice exposed prenatally to subclinical doses of 17α-ethinyl oestradiol. Hum Reprod 16:988-996
32. Larsson DGJ, Adolfsson-Erici M, Parkkonen J, Pettersson M, Berg AH, Olsson PE, Forlin L 1999 Ethinylestradiol - an undesired fish contraceptive? Aquatic Toxicol 45:91-97
33. Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT 2002 Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environ Sci Technol 36:1202-1211
34. Pojana G, Bonfa A, Busetti F, Collarin A, Marcomini A 2004 Estrogenic potential of the Venice, Italy, lagoon waters. Environ Toxicol Chem 23:1874-1880
35. Cargouet M, Perdiz D, Mouatassim-Souali A, Tamisier-Karolak S, Levi Y 2004 Assessment of river contamination by estrogenic compounds in Paris area (France). Sci Total Environ 324:55-66
36. Brian JV, Harris CA, Scholze M, Backhaus T, Booy P, Lamoree M, Pojana G, Jonkers N, Runnalls T, Bonfa A, Marcomini A, Sumpter JP 2005 Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals. Environ Health Perspect 113:721-728
37. Yasuda Y, Kihara T, Tanimura T 1985 Effect of ethinylestradiol on the differentiation of mouse fetal testis. Teratology 32:113-118
38. Yasuda Y, Konishi H, Tanimura T 1986 Leydig cell hyperplasia in fetal mice treated transplacentally with ethinyl estradiol. Teratology 33:281-288
39. Yasuda Y, Konish H, Tanimura T 1987 Ovarian follicular cell hyperplasia in fetal mice treated transplacentally with ethinyl estradiol. Teratology 36:35-43
40. Walker AH, Bernstein L, Warren DW, Warner NE, Zheng X, Henderson BE 1990 The effect of in utero ethinyl oestradiol exposure on the risk of cryptorchid testis and testicular teratoma in mice. Br J Cancer 62:599-602
41. Sawaki M, Noda S, Muroi T, Mitoma H, Takakura S, Sakamoto S, Yamasaki K 2003 In utero through lactational exposure to ethinylestradiol induces cleft phallus and delayed ovarian dysfunction in the offspring. Toxicol Sci 75:402- 411
42. Sawaki M, Noda S, Muroi T, Mitoma H, Takakura S, Sakamoto S, Yamasaki K 2003 Evaluation of an in utero through lactational exposure protocol for detection of estrogenic effects of ethinyl estradiol on the offspring of rats: preliminary trial. Reprod Toxicol 17:335-343
43. Dugard ML, Tremblay-Leveau H, Mellier D, Caston J 2001 Prenatal exposure to ethinylestradiol elicits behavioural abnormalities in the rat. Dev Brain Res 129:189-199
44. Ferguson SA, Delclos KB, Newbold RR, Flynn KM 2003 Dietary ethinylestradiol exposure during development causes increased voluntary sodium intake and mild maternal and offspring toxicity in rats. Neurotoxicol Teratol 25:491-501
45. Corrieri L, Della Seta D, Canoine V, Fusani L 2007 Developmental exposure to xenoestrogen enhances spatial learning in male rats. Horm Behav 51:620-625
46. Timms BG, Howdeshell KL, Barton L, Bradley S, Richter CA 2005 Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. Proc Natl Acad Sci USA 102:7014-7019
47. Nash JP, Kime DE, Van der Ven LT, Wester PW, Brion F, Maack G, Stahlschmidt-Allner P, Tyler CR 2004 Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 112:1725-1733
48. Parrott JL, Blunt BR 2005 Life-cycle exposure of fathead minnows (Pimephales promelas) to an ethinylestradiol concentration below 1 ng/L reduces egg fertilization success and demasculinizes males. Environ Toxicol 20:131-141
49. Lange R, Hutchinson TH, Croudace CP, Siegmund F 2001 Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20:1216-1227
50. Skillman AD, Nagler JJ, Hook SE, Small JA, Schultz IR 2006 Dynamics of 17α-ethynylestradiol exposure in rainbow trout (Oncorhynchus mykiss): absorption, tissue distribution, and hepatic gene expression pattern. Environ Toxicol Chem 25:2997-3005
51. Kuch HM, Ballschmiter K 2001 Determination of endocrine-disrupting phenolic compounds and estrogens in surface and drinking water by HRGC-(NCI)-MS in the picogram per liter range. Environ Sci Technol 35:3201-3206
52. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, Herman JP, Marts S, Sadee W, Steiner M, Taylor J, Young E 2005 Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146:1650-1673
53. Jenkins WJ, Becker JB 2005 Sex. In: Whishaw IQ, Kolb B, eds. The behavior of the laboratory rat. A handbook with tests. New York: Oxford University Press; 307-320
54. Zar JH 1984 Biostatistical analysis. London: Prentice-Hall International
55. Fusani L, Della Seta D, Dessi-Fulgheri F, Farabollini F 2007 Altered reproductive success in rat pairs after environmental-like exposure to xenoestrogen. Proc R Soc Lond B Biol Sci 274:1631-1636
56. Nass TE, Matt DW, Judd HL, Lu JKH 1984 Prepubertal treatment with estrogen or testosterone precipitates the loss of regular estrous cyclicity and normal gonadotropin secretion in adult female rats. Biol Rep 31:723-731
57. Romeo, RD 2003 Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J Neuroendocrinol 15:1185-1192
58. Sisk CL, Zehr JL 2005 Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 26:163-174
59. Borchardt CM, Lehman JR, Hendricks SE 1980 Sexual behavior and some of its physiological consequences in persistently estrous aged female rats. Age 3:59-63
60. Grant EC, Mackintosh JH 1963 A comparison of social postures of some common laboratory rodents. Behaviour 21:246-259
61. Dickey RP 2000 Managing contraceptive pill patients. Dallas: EMIS
62. Gilman DP, Mercer LF, Hitt JC 1979 Influence of female copulatory behavior on the induction of pseudopregnancy in the female rat. Physiol Behav 22:675-678
63. Erskine MS, Kornberg E, Cherry JA 1989 Paced copulation in rats: effects of intromission frequency and duration on luteal activation and estrus length. Physiol Behav 45:33-39
64. Adler NT 1969 Effects of the male's copulatory behavior on successful pregnancy of the female rat. J Comp Physiol Psychol 69:613-622
65. Beach FA 1976 Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105-138
66. Hoshina Y, Takeo T, Nakano K, Sato T, Sakuma Y 1994 Axon-sparing lesion of the preoptic area enhances receptivity and diminishes proceptivity among components of female rat sexual behavior. Behav Brain Res 61:197-204
67. Pfaff D, Keiner M 1973 Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151:121-158
68. Xiao L, Becker JB 1997 Hormonal activation of the striatum and the nucleus accumbens modulates paced mating behavior in the female rat. Horm Behav 32:114-124
69. McCarthy MM, Becker JB 2002 Neuroendocrinology of sexual behavior in the female. In: Becker JB, Breedlove SM, Crews D, McCarthy MM, eds. Behavioral endocrinology. 2nd ed. Cambridge, MA: MIT Press/Bradford Books; 117-151
70. Ceccarelli I, Della Seta D, Fiorenzani P, Farabollini F, Aloisi AM 2007 Estrogenic chemicals at puberty change ER-α in the hypothalamus of male and female rats. Neurotoxicol Teratol 29:108-115
71. Della Seta D, Minder I, Dessì-Fulgheri F, Farabollini F 2002 Bisphenol-A exposure during pregnancy and lactation affects maternal behavior in rats. Brain Res Bull 65:255-260
72. McClintock MK 1981 Social control of the ovarian cycle. Am Zool 21:243-256
73. Palanza P, Della Seta D, Ferrari PF, Parmigiani S 2005 Female competition in wild house mice depends upon timing of female/male settlement and kinship between females. Animal Behav 69:1259-1271
74. Pfaus JG, Kippin TE, Coria-Avila G 2003 What can animal models tell us about human sexual response? Annu Rev Sex Res 14:1-63