Perinatal exposure to xenoestrogens affects pain in adult female rats

Neurotoxicology and Teratology

Volumn 31, Issue 4, 2009, Pages 203-209

  Ceccarelli, Ilaria ^a   Fiorenzani, Paolo ^a   Della Seta, Daniele ^a   Massafra, Cosimo ^a   Cinci, Giuliano ^a   Bocci, Anna ^a   Aloisi, Anna Maria ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

Brain development; Experimental pain; Gonadal hormones; Memory; Xenoestrogens

Indexed keywords

ARACHIS OIL; ESTRADIOL; ETHINYLESTRADIOL; FORMALDEHYDE; METHOXYCHLOR; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; FEMALE; HORMONE BLOOD LEVEL; LACTATION; MEMORY; NERVE GROWTH; NONHUMAN; PAIN; PERINATAL DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; RAT;

ANIMALS; CENTRAL NERVOUS SYSTEM; COGNITION; DISEASE MODELS, ANIMAL; ENVIRONMENTAL EXPOSURE; ESTROGENS; ETHINYL ESTRADIOL; FEMALE; LACTATION; MEMORY; MEMORY DISORDERS; METHOXYCHLOR; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 67349086966     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2009.02.004     Document Type: Article

References (57)

1. Abraham G.E. Radioimmunoassay of steroids in biological fluids. J. Steroid Biochem. 6 (1975) 261-270
2. Adriani W., Della Seta D., Dessi-Fulgheri F., Farabollini F., and La Viola G. Altered profiles of spontaneous novelty seeking, impulsive behaviour, and response to D-amphetamine in rats perinatally exposed to bisphenol A. Environ. Health Perspect. 111 (2003) 395-401
3. Akhondzadeh S., and Abbasi S.H. Herbal medicine in the treatment of Alzheimer's disease. Am. J. Alzheimer's Dis. Other Dement. 21 (2006) 113-118
4. Aloisi A.M., and Bonifazi M. Sex hormones, central nervous system and pain. Horm. Behav. 50 (2006) 1-7
5. Aloisi A.M., and Ceccarelli I. Role of gonadal hormones in formalin-induced pain responses of male rats: modulation by estradiol and naloxone administration. Neuroscience 95 (2000) 559-566
6. Aloisi A.M., Albonetti M.E., and Carli G. Sex differences in the behavioural response to persistent pain in rats. Neurosci. Lett. 179 (1994) 79-82
7. Aloisi A.M., Della Seta D., Ceccarelli I., and Farabollini F. Bisphenol A differently affects estrogen receptor-α in estrous-cycling and lactating female rats. Neurosci. Lett. 310 (2001) 49-52
8. Aloisi A.M., Della Seta D., Rendo C., Ceccarelli I., Scaramuzzino A., and Farabollini F. Exposure to the estrogenic pollutant bisphenol A affects pain behavior induced by subcutaneous formalin injection in male and female rats. Brain Res. 937 (2002) 1-7
9. Anway M.D., Cupp A.S., Uzumcu M., and Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308 (2005) 1466-1469
10. Atanassova N., McKinnell C., Walker M., Turner K.J., Fisher J.S., Morley M., Millar M.R., Groome N.P., and Sharpe R.M. Permanent effects of neonatal estrogen exposure in rats on reproductive hormone levels, Sertoli cell number, and the efficiency of spermatogenesis in adulthood. Endocrinology 140 (1999) 5364-5373
11. Becker J.B., Arnold A.P., Berkley K.J., Bluastein J.D., Eckel L.A., Hampson E.H., Herman J.P., Marts S., Sadee W., Steiner M., Taylor J., and Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146 (2005) 1650-1673
12. Bulger W.H., Feil V.J., and Kupfer D. Role of hepatic monooxygenases in generating estrogenic metabolites from methoxychlor and from its identified contaminants. Mol. Pharmacol. 27 (1985) 115-124
13. Capone F., and Aloisi A.M. Refinement of pain evaluation techniques. The formalin test. Ann. Ist. Super. Sanità 40 (2004) 223-229
14. Ceccarelli I., Scaramuzzino A., and Aloisi A.M. Effects of gonadal hormones and persistent pain on non-spatial working memory in male and female rats. Behav. Brain Res. 123 (2001) 65-76
15. Ceccarelli I., Della Seta D., Fiorenzani P., Farabollini F., and Aloisi A.M. Estrogenic chemicals at puberty change ER-α in the hypothalamus of male and female rats. Neurotoxicol. Teratol. 29 (2007) 108-115
16. Corrieri L., Della Seta D., Canoine V., and Fusani L. Developmental exposure to xenoestrogen enhances spatial learning in male rats. Horm. Behav. 51 (2007) 620-625
17. Craft R.M., Mogil J.S., and Aloisi A.M. Sex differences in pain and analgesia: the role of gonadal hormones. Eur. J. Pain 8 (2004) 397-411
18. Cromer B.A. Menstrual cycle and bone health in adolescents. Ann. N.Y. Acad. Sci. 1135 (2008) 196-203
19. Cummings A.M., and Gray Jr. L.E. Methoxychlor affects the decidual cell responses of the uterus but not other progestational parameters in female rats. Toxicol. Appl. Pharmacol. 90 (1987) 330-336
20. Delemarre E.M., Felius B., and Delemarre-van de Waal H.A. Inducing puberty. Eur. J. Endocrinol. 159 (2008) S9-S15
21. Della Seta D., Farabollini F., Dessì-Fulgheri F., and Fusani L. Environmental-like exposure to low levels of estrogen affects sexual behavior and physiology of female rats. Endocrinology 149 (2008) 5592-5598
22. Farabollini F., Porrini S., and Dessì-Fulgheri F. Perinatal exposure to the estrogenic pollutant bisphenol A affects behaviour in male and female rats. Pharmacol. Biochem. Behav. 64 (1999) 687-694
23. Fillingim R.B., and Ness T.J. Sex-related hormonal influences on pain and analgesic responses. Neurosci. Biobehav. Rev. 24 (2000) 485-501
24. Fisher J.S. Are all EDC effects mediated via steroid hormone receptors?. Toxicology 205 (2004) 33-41
25. Gaido K.W., Leonard L.S., Maness S.C., Hall J.M., McDonnell D.P., Saville B., and Safe S. Differential interaction of the methoxychlor metabolite 2,2-bis-(p-hydroxyphenyl)-1,1,1-trichloroethane with estrogen receptors alpha and beta. Endocrinology 140 (1999) 5746-5753
26. Gould E., Woolley C.S., Frankfurt M., and McEwen B.S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10 (1990) 1286-1291
27. Gray L.E., Ostby J., Cooper R.L., and Kelce W.R. The estrogenic and androgenic pesticide methoxychlor alters the reproductive tract and behavior without affecting pituitary size or LH and prolactin secretion in male rats. Toxicol. Ind. Health 15 (1999) 37-47
28. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
29. Hillebrand U., Hausberg M., Lang D.D., Stock C., Riethmuller C., Callies C., and Bussemaker E. How steroid hormones act on the endothelium-insight by atomic force microscopy. Pflugers Arch. 456 (2008) 51-60
30. Howdeshell K.L., Furr J., Lambright C.R., Wilson V.S., Ryan B.C., and Gray Jr. L.E. Gestational and lactational exposure to ethinyl estradiol, but not bisphenol A, decrease androgen-dependent reproductive organ weights and epididymal sperm abundance in the male Long Evans hooded rat. Toxicol. Sci. 102 (2008) 371-382
31. Jacobson J.L., and Jacobson S.W. Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N. Engl. J. Med. 335 (1996) 783-789
32. Lephart E.D., Setchell K.D.R., Handa R.J., and Lund T.D. Behavioral effects of endocrine disrupting substances: phytoestrogens. ILAR J. 45 (2004) 443-454
33. Li D., Daling J.R., Mueller B.A., Hickok D.E., Fantel A.G., and Weiss N.S. Oral contraceptive use after conception in relation to the risk of congenital urinary tract anomalies. Teratology 51 (1995) 30-36
34. Lieben C.K., Blokland A., Şi{dotless}k A., Sung E., van Nieuwenhuizen P., and Schreiber R. The selective 5-HT6 receptor antagonist Ro4368554 restores memory performance in cholinergic and serotonergic models of memory deficiency in the rat. Neuropsychopharmacology 30 (2005) 2169-2179
35. Luine V.N. Sex steroids and cognitive function. J. Endocrinol. 20 (2008) 866-872
36. McEwen B.S. Estrogen actions throughout the brain. Recent Prog. Horm. Res. 57 (2002) 357-384
37. Micevych P.E., Eckersell C.B., Brecha N., and Holland K.L. Estrogen modulation of opioid and cholecystokinin systems in the limbic-hypothalamic circuit. Brain Res. Bull. 44 (1997) 335-343
38. Morvay J., Altorjay I., and Sas M. Serum and placenta levels of ethynylestradiol in presence of ethynodiol diacetate after oral administration. Horm. Res. 16 (1982) 237-243
39. Nash J.P., Kime D.E., Van der Ven L.T., Wester P.W., Brion F., Maack G., Stahlschmidt-Allner P., and Tyler C.R. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 112 (2004) 1725-1733
40. Nilsson S., Nygren K.G., and Johansson D.B. Ethynyl estradiol in human milk and plasma after oral administration. Contraception 17 (1978) 131-139
41. Palanza P., Morellini F., Parmigiani S., and vom Saal F.S. Prenatal exposure to endocrine disrupting chemicals: effects on behavioral development. Neurosci. Biobehav. Rev. 23 (1999) 1011-1027
42. Palanza P., Morellini F., Parmigiani S., and vom Saal F. Ethological methods to study the effects of maternal exposure to estrogenic endocrine disrupters: a study with methoxychlor. Neurotoxicol. Teratol. 24 (2002) 55-69
43. Parmigiani S., Palanza P., and vom Saal F.S. Ethotoxicology: an evolutionary approach to the study of environmental endocrine-disrupting chemicals. Toxicol. Ind. Health 14 (1998) 333-339
44. Patchev A.V., Gotz F., and Rhode W. Differential role of estrogen receptor isoforms in sex-specific brain organization. FASEB J. 18 (2004) 1568-1570
45. Przyembel H., Heinrich-Hirsch B., and Vieth B. Exposition to and health effects of residues in human milk. Adv. Exp. Med. Biol. 478 (2000) 307-325
46. Rudick C.N., and Woolley C.S. Estradiol induces a phasic Fos response in the hippocampal CA1 and CA3 regions of adult female rats. Hippocampus 10 (2000) 274-283
47. Ryan G.M., and Vanderbergh J.G. Developmental exposure to environmental estrogens alters anxiety and spatial memory in female mice. Horm. Behav. 50 (2006) 85-93
48. Sato K., Akaishi T., Matsuki N., Ohno Y., and Nakazawa K. Beta-Estradiol induces synaptogenesis in the hippocampus by enhancing brain-derived neurotrophic factor release from dentate gyrus cells. Brain Res. 1150 (2007) 108-120
49. Shen H., Main K.M., Virtanen H.E., Damggard I.N., Haavisto A.M., Kaleva M., Boisen K.A., Schmidt I.M., Chellakooty M., Skakkebaek N.E., Toppari J., and Schramm K. From mother to child: investigation of prenatal and postnatal exposure to persistent bioaccumulating toxicants using breast milk and placenta biomonitoring. Chemosphere 67 (2007) S256-S262
50. Sisk C.L., and Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26 (2005) 163-174
51. Slane McQuade J.M., Vorhees C.V., Xu M., and Zhang J. J. DNA fragmentation factor 45 knockout mice exhibit longer memory retention in the novel object recognition task compared to wild-type mice. Physiol. Behav. 76 (2002) 315-320
52. Smithells R.W. Oral contraceptives and birth defects. Dev. Med. Child Neurol. 23 (1981) 369-372
53. Thayer K.A., Ruhlen R.L., Howdeshell K.L., Buchanan D.L., Cooke P.S., Preziosi D., Welshons W.V., Haseman J., and vom Saal F.S. Altered prostate growth and daily sperm production in male mice exposed prenatally to subclinical doses of 17alpha-ethynyl oestradiol. Hum. Reprod. 16 (2001) 988-996
54. Wallen K. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front. Neuroendocrinol. 26 (2005) 7-26
55. Woolley C.S., and McEwen B.S. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336 (1993) 293-306
56. Woolley C.S., and Schwartzkroin P.A. Hormonal effects on the brain. Epilepsia 39 (1998) S2-S8
57. Zimmermann M. Ethical guidelines for investigation of experimental pain in conscious animals. Pain 16 (1983) 109-110