Effects of perinatal administration of bisphenol a on the neuronal nitric oxide synthase expressing system in the hypothalamus and limbic system of CD1 mice

Journal of Neuroendocrinology

Volumn 22, Issue 9, 2010, Pages 1004-1012

  Martini, M ^a   Miceli, D ^a   Gotti, S ^a   Viglietti Panzica, C ^a,b   Fissore, E ^c   Palanza, P ^c   Panzica, G ^a,b,d  

^a UNIVERSITY OF TURIN   (Italy)

^b National Institute of Neuroscience Italy   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

^d Scientific Institute of the Cavalieri Ottolenghi Foundation   (Italy)

Author keywords

Accessory olfactory system; Bed nucleus of the stria terminalis; Endocrine disrupting chemicals; Medial preoptic nucleus; Xenoestrogens

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CD1 ANTIGEN; NEURONAL NITRIC OXIDE SYNTHASE; SEX HORMONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DRUG EFFECT; FEMALE; HYPOTHALAMUS; LIMBIC SYSTEM; MALE; MOUSE; NERVE TRACT; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEXUAL BEHAVIOR;

ANIMALS; ANIMALS, OUTBRED STRAINS; DRUG EVALUATION, PRECLINICAL; FEMALE; HYPOTHALAMUS; LIMBIC SYSTEM; MALE; MICE; NITRIC OXIDE SYNTHASE TYPE I; PARTURITION; PHENOLS; POSTPARTUM PERIOD; PREGNANCY; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; TIME FACTORS; TISSUE DISTRIBUTION;

EID: 77955996394     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02043.x     Document Type: Article

References (69)

1. Colborn T, vom Saal FS, Soto AM. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 1993, 101:378-384.
2. McLachlan JA. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev 2001, 22:319-341.
3. Ottinger MA, vom Saal FS. Impact of environmental endocrine disruptors on sexual differentiation in birds and mammals. Hormones and Behavior in Higher Vertebrates 2002, 325-383. Pfaff D, Arnold AEtgen AMRubin R. eds, New York, NY, Academic Press
4. Panzica GC, Viglietti-Panzica C, Mura E, Quinn MJ, Palanza P, Ottinger MA. Effects of xenoestrogens on the differentiation of behaviorally relevant neural circuits. Front Neuroendocrinol 2007, 28:179-200.
5. Davis DL, Bradlow HL, Wolff M, Woodruff T, Hoel DG, Anton-Culver H. Medical hypothesis: xenoestrogens as preventable causes of breast cancer. Environ Health Perspect 1993, 101:372-377.
6. Biles JE, White KD, McNeal TP, Begley TH. Determination of the diglycidyl ether of bisphenol A and its derivatives in canned foods. J Agric Food Chem 1999, 47:1965-1969.
7. Brotons JA, Olea-Serrano FF, Villalobos M, Pedraza V, Olea N. Xenoestrogens released from lacquer coatings in food cans. Environ Health Perspect 1995, 103:608-612.
8. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997, 138:863-870.
9. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
10. Sohoni P, Sumpter JP. Several environmental oestrogens are also anti-androgens. J Endocrinol 1998, 158:327-339.
11. Lee HJ, Chattopadhyay S, Gong EY, Ahn RS, Lee K. Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor. Toxicol Sci 2003, 75:40-46.
12. Sun H, Xu LC, Chen JF, Song L, Wang XR. Effect of bisphenol A, tetrachlorobisphenol A and pentachlorophenol on the transcriptional activities of androgen receptor-mediated reporter gene. Food Chem Toxicol 2006, 44:1916-1921.
13. Kruger T, Long M, Bonefeld-Jorgensen EC. Plastic components affect the activation of the aryl hydrocarbon and the androgen receptor. Toxicology 2008, 246:112-123.
14. Gaido KW, Leonard LS, Lovell S, Gould JC, Babai D, Portier CJ, McDonnell DP. Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay. Toxicol Appl Pharmacol 1997, 143:205-212.
15. McCarthy MM. Estradiol and the developing brain. Physiol Rev 2008, 88:91-134.
16. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, vom Saal FS. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007, 24:199-224.
17. 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 2000, 141:4512-4517.
18. Rubin BS, Lenkowski JR, Schaeberle CM, Vandenberg LN, Ronsheim PM, Soto AM. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 2006, 147:3681-3691.
19. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. Perinatal exposure to low doses of bisphenol-A affects body weight, patterns of estrous cyclicity and plasma LH levels. Environ Health Perspect 2001, 109:675-680.
20. 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 2001, 304:73-76.
21. 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 2003, 45:345-356.
22. vom Saal FS. Bisphenol A eliminates brain and behavior sex dimorphisms in mice: how low can you go? Endocrinology 2006, 147:3679-3680.
23. Gore AC. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol 2008, 29:358-374.
24. Prast H, Philippu A. Nitric oxide releases acetylcholine in the basal forebrain. Eur J Pharmacol 1992, 216:139-140.
25. Stuehr DJ. Structure-function aspects in the nitric oxide synthases. Annu Rev Pharmacol Toxicol 1997, 37:339-359.
26. Mungrue IN, Bredt DS, Stewart DJ, Husain M. From molecules to mammals: what's NOS got to do with it? Acta Physiol Scand 2003, 179:123-135.
27. Hadeishi Y, Wood RI. Nitric oxide synthase in mating behavior circuitry of male Syrian hamster brain. J Neurobiol 1996, 30:480-492.
28. Gotti S, Sica M, Viglietti Panzica C, Panzica GC. The distribution of nitric oxide sythase immunoreactivity in the mouse brain. Microsc Res Tech 2005, 68:13-35.
29. Collado P, Guillamon A, Pinos H, Perez-Izquierdo MA, Garci{dotless}a-Falgueras A, Carrillo B, Rodri{dotless}guez C, Panzica GC. NADPH-diaphorase activity increases during estrous phase in the bed nucleus of the accessory olfactory tract in the female rat. Brain Res 2003, 983:223-229.
30. Sica M, Martini M, Viglietti-Panzica C, Panzica GC. Estrous cycle influences the expression of neuronal nitric oxide synthase in the hypothalamus and limbic system of female mice. BMC Neurosci 2009, 10:78.
31. McDonald AJ, Payne DR, Mascagni F. Identification of putative nitric oxide producing neurons in the rat amygdala using NADPH-diaphorase histochemistry. Neuroscience 1993, 52:97-106.
32. Carrillo B, Pinos H, Guillamon A, Panzica GC, Collado P. Morphometrical and neurochemical changes in the anteroventral subdivision of the rat medial amygdala during estrus cycle. Brain Res 2007, 1150:83-93.
33. Segovia S, Guillamon A. Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res Rev 1993, 18:51-74.
34. Segovia S, Guillamon A. Searching for sex differences in the vomeronasal pathway. Horm Behav 1996, 30:618-626.
35. Okamura H, Yokosuka M, McEwen BS, Hayashi S. Colocalization of NADPH-diaphorase and estrogen receptor immunoreactivity in the rat ventromedial hypothalamic nucleus: stimulatory effect of estrogen on NADPH-diaphorase activity. Endocrinology 1994, 135:1705-1708.
36. Sato S, Braham CS, Putnam SK, Hull EM. Neuronal nitric oxide synthase and gonadal steroid interaction in the MPOA of male rats: co-localization and testosterone-induced restoration of copulation and nNOS-immunoreactivity. Brain Res 2005, 1043:205-213.
37. Scordalakes EM, Shetty SJ, Rissman EF. Roles of estrogen receptor alpha and androgen receptor in the regulation of neuronal nitric oxide synthase. J Comp Neurol 2002, 453:336-344.
38. Bhat GK, Mahesh VB, Lamar CA, Ping L, Aguan K, Brann DW. Histochemical localization of nitric oxide neurons in the hypothalamus: association with gonadotropin-releasing hormone neurons and co-localization with N-methyl-D-aspartate receptors. Neuroendocrinology 1995, 62:187-197.
39. d'Anglemont de Tassigny X, Campagne C, Dehouck B, Leroy D, Holstein GR, Beauvillain JC, Buee-Scherrer V, Prevot V. Coupling of neuronal nitric oxide synthase to NMDA receptors via postsynaptic density-95 depends on estrogen and contributes to the central control of adult female reproduction. J Neurosci 2007, 27:6103-6114.
40. d'Anglemont de Tassigny X, Campagne C, Steculorum S, Prevot V. Estradiol induces physical association of neuronal nitric oxide synthase with NMDA receptor and promotes nitric oxide formation via estrogen receptor activation in primary neuronal cultures. J Neurochem 2009, 109:214-224.
41. Panzica GC, Viglietti-Panzica C, Sica M, Gotti S, Martini M, Pinos H, Carrillo B, Collado P. Effects of gonadal hormones on central nitric oxide producing systems. Neuroscience 2006, 138:987-995.
42. http://www.epa.gov/iris/subst/0356.htm, Washington, DC, Environmental Protection Agency, Available: [accessed 10 November 2006]. 1988
43. Morrissey RE, George JD, Price CJ, Tyl RW, Marr MC, Kimmel CA. The developmental toxicity of bisphenol A in rats and mice. Fundam Appl Toxicol 1987, 8:571-582.
44. Franklin KBJ, Paxinos G. The mouse brain in stereotaxic coordinates 1997, New York, NY, Academic Press
45. Watson RE, Wiegand SJ, Clough RW, Hoffman GE. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 1986, 7:155-159.
46. Streefkerk JG. Inhibition of erythrocyte peroxidase activity by treatment with hydrogen peroxide following methanol. J Histochem Cytochem 1972, 20:829-831.
47. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 1991, 88:7797-7801.
48. Eliasson MJ, Blackshaw S, Schell MJ, Snyder SH. Neuronal nitric oxide synthase alternatively spliced forms: prominent functional localizations in the brain. Proc Natl Acad Sci USA 1997, 94:3396-3401.
49. Kriegsfeld LJ, Eliasson MJ, Demas GE, Blackshaw S, Dawson TM, Nelson RJ, Snyder SH. Nocturnal motor coordination deficits in neuronal nitric oxide synthase knock-out mice. Neuroscience 1999, 89:311-315.
50. Martini M, Di Sante G, Collado P, Pinos H, Guillamon A, Panzica GC. Androgen receptors are required for full masculinization of nitric oxide synthase system in rat limbic-hypothalamic region. Horm Behav 2008, 54:557-564.
51. Claro F, Segovia S, Guilamón A, Del Abril A. Lesions in the medial posterior region of the BST impair sexual behavior in sexually experienced and inexperienced male rats. Brain Res Bull 1995, 36:1-10.
52. Coolen LM, Peters HJPW, Veening JG. Anatomical interrelationships of the medial preoptic area and other brain regions activated following male sexual behavior: a combined Fos and tract-tracing study. J Comp Neurol 1998, 397:421-435.
53. Veening JG, Coolen LM. Neural activation following sexual behavior in the male and female rat brain. Behav Brain Res 1998, 92:181-193.
54. Welshons WV, Nagel SC, vom Saal FS. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 2006, 147:S56-S69.
55. Monje L, Varayoud J, Luque EH, Ramos JG. Neonatal exposure to bisphenol A modifies the abundance of estrogen receptor alpha transcripts with alternative 5'-untranslated regions in the female rat preoptic area. J Endocrinol 2007, 194:201-212.
56. Kawai K, Murakami S, Senba E, Yamanaka T, Fujiwara Y, Arimura C, Nozaki T, Takii M, Kubo C. Changes in estrogen receptors alpha and beta expression in the brain of mice exposed prenatally to bisphenol A. Regul Toxicol Pharmacol 2007, 47:166-170.
57. Zsarnovszky A, Le HH, Wang HS, Belcher SM. Ontogeny of rapid estrogen-mediated extracellular signal-regulated kinase signaling in the rat cerebellar cortex: potent non-genomic agonist and endocrine disrupting activity of the xenoestrogen bisphenol A. Endocrinology 2005, 146:5388-5396.
58. Simerly RB, Zee MC, Pendleton JW, Lubhan DB, Korach KS. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci USA 1997, 94:14077-14082.
59. vom Saal FS, Cooke PS, Buchanan DL, Palanza P, Thayer KA, Nagel SC, Parmigiani S, Welshons WV. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol Ind Health 1998, 14:239-260.
60. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, vom Saal FS. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ Health Perspect 2003, 111:994-1006.
61. vom Saal FS, Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect 2005, 113:926-933.
62. 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 2002, 110(Suppl 3):409-414.
63. Gioiosa L, Fissore E, Ghirardelli G, Parmigiani S, Palanza P. Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice. Horm Behav 2007, 52:307-316.
64. Nelson RJ, Kriegsfeld LJ, Dawson VL, Dawson TM. Effects of nitric oxide on neuroendocrine function and behavior. Front Neuroendocrinol 1997, 18:463-491.
65. Ponzi D, Palanza P, Maruniak JA, Parmigiani S, Vom Saal FS. Sexual dimorphism in the number of TH-immunostained neurons in the Locus Coeruleus of young mice is eliminated by prenatal exposure to Bisphenol A. Fifth Forum of European Neuroscience 2006, Abstract A008.21
66. Patisaul HB, Fortino AE, Polston EK. Neonatal genistein or bisphenol-A expose alters sexual differentiation of the AVPV. Neurotoxicol Teratol 2006, 28:111-118.
67. Patisaul HB, Fortino AE, Polston EK. Differential disruption of nuclear volume and neuronal phenotype in the preoptic area by neonatal exposure to genistein and bisphenol-A. Neurotoxicology 2007, 28:1-12.
68. Panzica GC, Viglietti Panzica C, Ottinger MA. Introduction: neurobiological impact of environmental estrogens. Brain Res Bull 2005, 65:187-191.
69. Patisaul HB, Polston EK. Influence of endocrine active compounds on the developing rodent brain. Brain Res Rev 2008, 57:352-362.