Impact of neonatal exposure to the ERα agonist PPT, bisphenol-A or phytoestrogens on hypothalamic kisspeptin fiber density in male and female rats

NeuroToxicology

Volumn 30, Issue 3, 2009, Pages 350-357

  Patisaul, Heather B ^a   Todd, Karina L ^a   Mickens, Jillian A ^a   Adewale, Heather B ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Bisphenol; Development; Disruption; Equol; Estrogen; Estrogen receptor; Genistein; GnRH; Gonadotropins; KISS; Phytoestrogens; Soy

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; 4,4' ISOPROPYLIDENEDIPHENOL; ANTIESTROGEN; ENDOCRINE DISRUPTOR; EQUOL; ESTRADIOL BENZOATE; ESTROGEN RECEPTOR ALPHA; GENISTEIN; KISSPEPTIN; PHYTOESTROGEN; SESAME SEED OIL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN TOXICITY; BRAIN VENTRICLE; CONTROLLED STUDY; DRUG MEGADOSE; FEMALE; HYPOTHALAMUS; IMMUNOREACTIVITY; LOW DRUG DOSE; MALE; NONHUMAN; OVARIECTOMY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN CONTENT; RAT;

ANIMALS; ANIMALS, NEWBORN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HYPOTHALAMUS; MALE; NERVE FIBERS; OVARIECTOMY; PHENOLS; PHYTOESTROGENS; PROGESTERONE; PROTEINS; PYRAZOLES; RATS; RATS, LONG-EVANS; SEX CHARACTERISTICS;

RATTUS; SESAMUM INDICUM;

EID: 67349205410     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2009.02.010     Document Type: Article

References (66)

1. Bateman H.L., and Patisaul H.B. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology (2008)
2. Boettger-Tong H., Murthy L., Chiappetta C., Kirkland J.L., Goodwin B., Adlercreutz H., et al. A case of a laboratory animal feed with high estrogenic activity and its impact on in vivo responses to exogenously administered estrogens. Environ Health Perspect 106 (1998) 369-373
3. Brown N.M., and Setchell K.D. Animal models impacted by phytoestrogens in commercial chow: implications for pathways influenced by hormones. Lab Invest 81 (2001) 735-747
4. Clarkson J., d'Anglemont de Tassigny X., Moreno A.S., Colledge W.H., and Herbison A.E. Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28 (2008) 8691-8697
5. Clarkson J., and Herbison A.E. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 147 (2006) 5817-5825
6. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., and Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100 (2003) 10972-10976
7. Dixon R.A., Ferreira D., and Genistein. Phytochemistry 60 (2002) 205-211
8. Elkind-Hirsch K., King J.C., Gerall A.A., and Arimura A.A. The luteinizing hormone-releasing hormone (LHRH) system in normal and estrogenized neonatal rats. Brain Res Bull 7 (1981) 645-654
9. Freni-Titulaer L.W., Cordero J.F., Haddock L., Lebron G., Martinez R., and Mills J.L. Premature thelarche in Puerto Rico A search for environmental factors. Am J Dis Child 140 (1986) 1263-1267
10. Gaudette D.C., and Holub B.J. Effect of genistein, a tyrosine kinase inhibitor, on U46619-induced phosphoinositide phosphorylation in human platelets. Biochem Biophys Res Commun 170 (1990) 238-242
11. Gonzalez-Martinez D., De Mees C., Douhard Q., Szpirer C., and Bakker J. Absence of GnRH1 and Kiss1 activation in alpha-fetoprotein knockout mice: prenatal estrogens defeminize the potential to show preovulatory LH surges. Endocrinology (2008)
12. Gorski R.A., Mennin S.P., and Kubo K. The neural and hormonal bases of the reproductive cycle of the rat. Adv Exp Med Biol 54 (1975) 115-153
13. Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145 (2004) 4073-4077
14. Gu G.B., and Simerly R.B. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J Comp Neurol 384 (1997) 142-164
15. Guillette Jr. L.J., and Gunderson M.P. Alterations in development of reproductive and endocrine systems of wildlife populations exposed to endocrine-disrupting contaminants. Reproduction 122 (2001) 857-864
16. Herbison A.E., and Pape J.R. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol 22 (2001) 292-308
17. Howdeshell K.L., Hotchkiss A.K., Thayer K.A., Vandenbergh J.G., and vom Saal F.S. Exposure to bisphenol A advances puberty. Nature 401 (1999) 763-764
18. Hrabovszky E., Shughrue P.J., Merchenthaler I., Hajszan T., Carpenter C.D., Liposits Z., et al. Detection of estrogen receptor-beta messenger ribonucleic acid and 125I-estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 141 (2000) 3506-3509
19. Hrabovszky E., Steinhauser A., Barabas K., Shughrue P.J., Petersen S.L., Merchenthaler I., et al. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 142 (2001) 3261-3264
20. Huang R.Q., Fang M.J., and Dillon G.H. The tyrosine kinase inhibitor genistein directly inhibits GABAA receptors. Brain Res Mol Brain Res 67 (1999) 177-183
21. Irwig M.S., Fraley G.S., Smith J.T., Acohido B.V., Popa S.M., Cunningham M.J., et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80 (2004) 264-272
22. Jefferson W.N., Padilla-Banks E., and Newbold R.R. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol Reprod 73 (2005) 798-806
23. Jefferson W.N., Padilla-Banks E., and Newbold R.R. Studies of the effects of neonatal exposure to genistein on the developing female reproductive system. J AOAC Int 89 (2006) 1189-1196
24. Kauffman A.S., Clifton D.K., and Steiner R.A. Emerging ideas about kisspeptin- GPR54 signaling in the neuroendocrine regulation of reproduction. Trends Neurosci 30 (2007) 504-511
25. Kauffman A.S., Gottsch M.L., Roa J., Byquist A.C., Crown A., Clifton D.K., et al. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148 (2007) 1774-1783
26. Kotani M., Detheux M., Vandenbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276 (2001) 34631-34636
27. Kuiper G.G.J.M., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., Van Der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139 (1998) 4252-4263
28. Lee D.K., Nguyen T., O'Neill G.P., Cheng R., Liu Y., Howard A.D., et al. Discovery of a receptor related to the galanin receptors. FEBS Lett 446 (1999) 103-107
29. Lewis R.W., Brooks N., Milburn G.M., Soames A., Stone S., Hall M., et al. The effects of the phytoestrogen genistein on the postnatal development of the rat. Toxicol Sci 71 (2003) 74-83
30. Lund T.D., Munson D.J., Haldy M.E., Setchell K.D., Lephart E.D., and Handa R.J. Equol is a novel anti-androgen that inhibits prostate growth and hormone feedback. Biol Reprod 70 (2004) 1188-1195
31. Mueller S.O., Kling M., Arifin Firzani P., Mecky A., Duranti E., Shields-Botella J., et al. Activation of estrogen receptor alpha and ERbeta by 4-methylbenzylidene-camphor in human and rat cells: comparison with phyto- and xenoestrogens. Toxicol Lett 142 (2003) 89-101
32. Muir A.I., Chamberlain L., Elshourbagy N.A., Michalovich D., Moore D.J., Calamari A., et al. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276 (2001) 28969-28975
33. Navarro V.M., Fernandez-Fernandez R., Castellano J.M., Roa J., Mayen A., Barreiro M.L., et al. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 561 (2004) 379-386
34. Navarro V.M., Sanchez-Garrido M.A., Castellano J.M., Roa J., Garcia-Galiano D., Pineda R., et al. Persistent impairment of hypothalamic KiSS-1 system following exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology (2008)
35. Nikov G.N., Hopkins N.E., Boue S., and Alworth W.L. Interactions of dietary estrogens with human estrogen receptors and the effect on estrogen receptor-estrogen response element complex formation. Environ Health Perspect 108 (2000) 867-872
36. Orikasa C., Kondo Y., Hayashi S., McEwen B.S., and Sakuma Y. Sexually dimorphic expression of estrogen receptor beta in the anteroventral periventricular nucleus of the rat preoptic area: implication in luteinizing hormone surge. Proc Natl Acad Sci USA 99 (2002) 3306-3311
37. Orikasa C., and Sakuma Y. Possible involvement of preoptic estrogen receptor beta positive cells in luteinizing hormone surge in the rat. Domest Anim Endocrinol 25 (2003) 83-92
38. Patisaul H.B., Fortino A.E., and Polston E.K. Neonatal genistein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol Teratol 28 (2006) 111-118
39. Patisaul H.B., Fortino A.E., and Polston E.K. Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A. Neurotoxicology 28 (2007) 1-12
40. Patisaul H.B., Fortino A.E., and Polston E.K. Sex differences in serotonergic but not gamma-aminobutyric acidergic (GABA) projections to the rat ventromedial nucleus of the hypothalamus. Endocrinology 149 (2008) 397-408
41. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1998), Academic Press, San Diego
42. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates [the new coronal set] (2004), Elsevier Academic, London
43. Perez S.E., Chen E.Y., and Mufson E.J. Distribution of estrogen receptor alpha and beta immunoreactive profiles in the postnatal rat brain. Brain Res Dev Brain Res 145 (2003) 117-139
44. Polston E.K., Gu G., and Simerly R.B. Neurons in the principal nucleus of the bed nuclei of the stria terminalis provide a sexually dimorphic GABAergic input to the anteroventral periventricular nucleus of the hypothalamus. Neuroscience 123 (2004) 793-803
45. Polston E.K., and Simerly R.B. Ontogeny of the projections from the anteroventral periventricular nucleus of the hypothalamus in the female rat. J Comp Neurol 495 (2006) 122-132
46. Roa J., Vigo E., Castellano J.M., Navarro V.M., Fernandez-Fernandez R., Casanueva F.F., et al. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 147 (2006) 2864-2878
47. Rubin B.S., Murray M.K., Damassa D.A., King J.C., and Soto A.M. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ Health Perspect 109 (2001) 675-680
48. Schoental R. Precocious sexual development in Puerto Rico and oestrogenic mycotoxins (zearalenone). Lancet 1 (1983) 537
49. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno Jr. J.S., Shagoury J.K., et al. The GPR54 gene as a regulator of puberty. N Engl J Med 349 (2003) 1614-1627
50. Setchell K.D., Brown N.M., Desai P.B., Zimmer-Nechimias L., Wolfe B., Jakate A.S., et al. Bioavailability, disposition, and dose-response effects of soy isoflavones when consumed by healthy women at physiologically typical dietary intakes. J Nutr 133 (2003) 1027-1035
51. Setchell K.D., Brown N.M., and Lydeking-Olsen E. The clinical importance of the metabolite equol-a clue to the effectiveness of soy and its isoflavones. J Nutr 132 (2002) 3577-3584
52. Setchell K.D.R., Zimmer-Nechemias L., Cai J., and Heubi J.E. Exposure of infants to phyto-oestrogens from soy-based infant formula. Lancet 350 (1997) 23-27
53. Shughrue P.L., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor α and β mRNA in the rat central nervous system. J Comp Neurol 388 (1997) 507-525
54. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25 (2002) 507-536
55. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294 (1990) 76-95
56. Smith J.T., Clifton D.K., and Steiner R.A. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 131 (2006) 623-630
57. Smith J.T., Cunningham M.J., Rissman E.F., Clifton D.K., and Steiner R.A. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146 (2005) 3686-3692
58. Smith J.T., Popa S.M., Clifton D.K., Hoffman G.E., and Steiner R.A. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 26 (2006) 6687-6694
59. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., et al. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 43 (2000) 4934-4947
60. Sun J., Huang Y.R., Harrington W.R., Sheng S., Katzenellenbogen J.A., and Katzenellenbogen B.S. Antagonists selective for estrogen receptor alpha. Endocrinology 143 (2002) 941-947
61. Taylor J.A., Welshons W.V., and Vom Saal F.S. No effect of route of exposure (oral; subcutaneous injection) on plasma bisphenol A throughout 24 h after administration in neonatal female mice. Reprod Toxicol 25 (2008) 169-176
62. Thigpen J.E., Setchell K.D.R., Ahlmark K.B., Locklear J., Spahr T., Caviness G.F., et al. Phytoestrogen content of purified open- and closed-formula laboratory animal diets. Lab Anim Sci 49 (1999) 530-536
63. Todaka E., Sakurai K., Fukata H., Miyagawa H., Uzuki M., Omori M., et al. Fetal exposure to phytoestrogens-the difference in phytoestrogen status between mother and fetus. Environ Res 99 (2005) 195-203
64. vom Saal F.S., and Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect 113 (2005) 926-933
65. Welshons W.V., Nagel S.C., and vom Saal F.S. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 147 (2006) S56-69
66. Wisniewski A.B., Klein S.L., Lakshmanan Y., and Gearhart J.P. Exposure to genistein during gestation and lactation demasculinizes the reproductive system in rats. J Urol 169 (2003) 1582-1586