CoChat
Sign Up
Cited by 87Effects and risks of endocrine disrupting chemicalsToxic Organic Pollutants ImpactSexual Differentiation and Disorders

The effects of prenatal PCBs on adult female paced mating reproductive behaviors in rats

Open access
Steinberg, Rebecca M., Juenger, Thomas E., Gore, Andrea C.·2007·Hormones and Behavior
DOI 10.1016/j.yhbeh.2006.12.004PMC PMC2692581
Open this paper in CoChat — free account

Abstract

Polychlorinated biphenyls (PCBs) are a family of toxicants that persist in measurable quantities in human and wildlife tissues, despite their ban in production in 1977. Some PCB mixtures can act as endocrine disrupting chemicals (EDCs) by mimicking or antagonizing the actions of hormones in the brain and periphery. When exposure to hormonally active substances such as PCBs occurs during vulnerable developmental periods, particularly prenatally or in early postnatal life, they can disrupt sex-specific patterning of the brain, inducing permanent changes that can later be manifested as improper sexual behaviors. Here, we investigated the effects of prenatal exposure to the PCB mixture Aroclor (A) 1221 on adult female reproductive behaviors in a dose-response model in the Sprague-Dawley rat. Using a paced mating paradigm that permits the female to set the timing of mating and control contact with the male during copulation, we were able to uncover significant differences in female-typical sexual activities in A1221-exposed females. Specifically, A1221 causes significant effects on mating trial pacing, vocalizations, ambulation and the female's likelihood to mate. The results further demonstrate that the intermediate treatment group has the greatest number of disrupted endpoints, suggestive of non-linear dose responses to A1221. These data demonstrate that the behavioral phenotype in adulthood is disrupted by low, ecologically relevant exposures to PCBs, and the results have implications for reproductive success and health in wildlife and women.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.yhbeh.2006.12.004

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • PCBs including A1221 disrupt sexual behavior in female rats.

    “Polychlorinated biphenyls (PCBs) - including the Aroclor 1221 mixture (A1221) used in the current study – also disrupt sexual behavior in female rats (Chung and Clemens, 1999; Steinberg et al., 2007).”

    From The effects of prenatal PCBs on adult social behavior in rats (2015) · cites this paper as Steinberg et al., 2007

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 87

  1. Aluru N, Vijayan MM. Aryl hydrocarbon receptor activation impairs cortisol response to stress in rainbow trout by disrupting the rate-limiting steps in steroidogenesis. Endocrinology. 2006;147(4):1895–1903. doi: 10.1210/en.2005-1143. [DOI] [PubMed] [Google Scholar] · DOI
  2. Aluru N, Jorgensen EH, Maule AG, Vijayan MM. PCB disruption of the hypothalamus-pituitary-interrenal axis involves brain glucocorticoid receptor downregulation in anadromous Arctic charr. Am. J. Physiol., Regul. Integr. Comp. Physiol. 2004;287(4):R787–R793. doi: 10.1152/ajpregu.00091.2004. [DOI] [PubMed] [Google Scholar] · DOI
  3. Aubert ML, Begeot M, Winiger BP, Morel G, Sizonenko PC, Dubois PM. Ontogeny of hypothalamic luteinizing hormone-releasing hormone (GnRH) and pituitary GnRH receptors in fetal and neonatal rats. Endocrinology. 1985;116(4):1565–1576. doi: 10.1210/endo-116-4-1565. [DOI] [PubMed] [Google Scholar] · DOI
  4. Bansal R, You SH, Herzig CT, Zoeller RT. Maternal thyroid hormone increases HES expression in the fetal rat brain: an effect mimicked by exposure to a mixture of polychlorinated biphenyls (PCBs) Brain Res. Dev. Brain Res. 2005;156(1):13–22. doi: 10.1016/j.devbrainres.2005.01.007. [DOI] [PubMed] [Google Scholar] · DOI
  5. Barfield MA, Lisk RD. Advancement of behavioral estrus by subcutaneous injection of progesterone in the 4-day cyclic rat. Endocrinology. 1970;87(5):1096–1098. doi: 10.1210/endo-87-5-1096. [DOI] [PubMed] [Google Scholar] · DOI
  6. Battershill JM. Review of the safety assessment of polychlorinated biphenyls (PCBs) with particular reference to reproductive toxicity. Hum. Exp. Toxicol. 1994;13(9):581–597. doi: 10.1177/096032719401300901. [DOI] [PubMed] [Google Scholar] · DOI
  7. Becu-Villalobos D, Gonzalez Iglesias A, Diaz-Torga G, Hockl P, Libertun C. Brain sexual differentiation and gonadotropins secretion in the rat. Cell. Mol. Neurobiol. 1997;17(6):699–715. doi: 10.1023/A:1022542221535. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  8. Bowman RE, Heironimus MP, Barsotti DA. Locomotor hyperactivity in PCB-exposed rhesus monkeys. Neurotoxicology. 1981;2(2):251–268. [PubMed] [Google Scholar]
  9. Breedlove SM. Sexual dimorphism in the vertebrate nervous system. J. Neurosci. 1992;12(11):4133–4142. doi: 10.1523/JNEUROSCI.12-11-04133.1992. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  10. Brouwer A, van den Berg KJ. Binding of a metabolite of 3,4,3′,4′-tetrachlorobiphenyl to transthyretin reduces serum vitamin A transport by inhibiting the formation of the protein complex carrying both retinol and thyroxin. Toxicol. Appl. Pharmacol. 1986;85(3):301–312. doi: 10.1016/0041-008x(86)90337-6. [DOI] [PubMed] [Google Scholar] · DOI
  11. Brouwer A, Longnecker MP, Birnbaum LS, Cogliano J, Kostyniak P, Moore J, Schantz S, Winneke G. Characterization of potential endocrine-related health effects at low-dose levels of exposure to PCBs. Environ. Health Perspect. 1999;107(Suppl 4):639–649. doi: 10.1289/ehp.99107s4639. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  12. Brunnberg S, Pettersson K, Rydin E, Matthews J, Hanberg A, Pongratz I. The basic helix-loop-helix-PAS protein ARNT functions as a potent coactivator of estrogen receptor-dependent transcription. Proc. Natl. Acad. Sci. U. S. A. 2003;100(11):6517–6522. doi: 10.1073/pnas.1136688100. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  13. Buitenhuis C, Cenijn PC, van Velzen M, Lilienthal H, Malmberg T, Bergman A, Gutleb AC, Legler J, Brouwer A. Effects of prenatal exposure to hydroxylated PCB metabolites and some brominated flame retardants on the development of rats. Organohalog. Compd. 2004;66:3586–3592. [Google Scholar]
  14. Calabrese EJ, Baldwin LA. U-shaped dose-responses in biology, toxicology, and public health. Annu. Rev. Public Health. 2001;22:15–33. doi: 10.1146/annurev.publhealth.22.1.15. [DOI] [PubMed] [Google Scholar] · DOI
  15. Cassell DL. A randomized-test wrapper for SAS PROCs. SUGI. 2002;27:1–4. [Google Scholar]
  16. Chauhan KR, Kodavanti PR, McKinney JD. Assessing the role of ortho-substitution on polychlorinated biphenyl binding to transthyretin, a thyroxine transport protein. Toxicol. Appl. Pharmacol. 2000;162(1):10–21. doi: 10.1006/taap.1999.8826. [DOI] [PubMed] [Google Scholar] · DOI
  17. Chen RC, Tang SY, Miyata H, Kashimoto T, Chang YC, Chang KJ, Tung TC. Polychlorinated biphenyl poisoning: correlation of sensory and motor nerve conduction, neurologic symptoms, and blood levels of polychlorinated biphenyls, quaterphenyls, and dibenzofurans. Environ. Res. 1985;37(2):340–348. doi: 10.1016/0013-9351(85)90114-8. [DOI] [PubMed] [Google Scholar] · DOI
  18. Chung YW, Clemens LG. Effects of perinatal exposure to polychlorinated biphenyls on development of female sexual behavior. Bull. Environ. Contam. Toxicol. 1999;62(6):664–670. doi: 10.1007/s001289900925. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  19. Chung YW, Nunez AA, Clemens LG. Effects of neonatal polychlorinated biphenyl exposure on female sexual behavior. Physiol. Behav. 2001;74(3):363–370. doi: 10.1016/s0031-9384(01)00579-0. [DOI] [PubMed] [Google Scholar] · DOI
  20. Colciago A, Celotti F, Pravettoni A, Mornati O, Martini L, Negri-Cesi P. Dimorphic expression of testosterone metabolizing enzymes in the hypothalamic area of developing rats. Brain Res. Dev. Brain Res. 2005;155(2):107–116. doi: 10.1016/j.devbrainres.2004.12.003. [DOI] [PubMed] [Google Scholar] · DOI
  21. Connor K, Ramamoorthy K, Moore M, Mustain M, Chen I, Safe S, Zacharewski T, Gillesby B, Joyeux A, Balaguer P. Hydroxylated polychlorinated biphenyls (PCBs) as estrogens and antiestrogens: structure-activity relationships. Toxicol. Appl. Pharmacol. 1997;145(1):111–123. doi: 10.1006/taap.1997.8169. [DOI] [PubMed] [Google Scholar] · DOI
  22. Coopersmith C, Erskine MS. Influence of paced mating and number of intromissions on fertility in the laboratory rat. J. Reprod. Fertil. 1994;102(2):451–458. doi: 10.1530/jrf.0.1020451. [DOI] [PubMed] [Google Scholar] · DOI
  23. Crews D, Lou W, Fleming A, Ogawa S. From gene networks underlying sex determination and gonadal differentiation to the development of neural networks regulating sociosexual behavior. Brain Res. 2006;1126(1):109–121. doi: 10.1016/j.brainres.2006.07.031. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  24. Crofton KM, Kodavanti PR, Derr-Yellin EC, Casey AC, Kehn LS. PCBs, thyroid hormones, and ototoxicity in rats: cross-fostering experiments demonstrate the impact of postnatal lactation exposure. Toxicol. Sci. 2000;57(1):131–140. doi: 10.1093/toxsci/57.1.131. [DOI] [PubMed] [Google Scholar] · DOI
  25. Desaulniers D, Leingartner K, Wade M, Fintelman E, Yagminas A, Foster WG. Effects of acute exposure to PCBs 126 and 153 on anterior pituitary and thyroid hormones and FSH isoforms in adult Sprague Dawley male rats. Toxicol. Sci. 1999;47(2):158–169. doi: 10.1093/toxsci/47.2.158. [DOI] [PubMed] [Google Scholar] · DOI
  26. Dohler KD. The pre- and postnatal influence of hormones and neurotransmitters on sexual differentiation of the mammalian hypothalamus. Int. Rev. Cytol. 1991;131:1–57. doi: 10.1016/s0074-7696(08)62016-1. [DOI] [PubMed] [Google Scholar] · DOI
  27. Durham SK, Brouwer A. 3,4,3′,4′-Tetrachlorobiphenyl distribution and induced effects in the rat adrenal gland. Lab. Invest. 1990;62(2):232–239. [PubMed] [Google Scholar]
  28. Edmonds S, Zoloth SR, Adler NT. Storage of copulatory stimulation in the female rat. Physiol. Behav. 1972;8(2):161–164. doi: 10.1016/0031-9384(72)90354-x. [DOI] [PubMed] [Google Scholar] · DOI
  29. Erskine MS. Effects of paced coital stimulation on estrus duration in intact cycling rats and ovariectomized and ovariectomized-adrenalectomized hormone-primed rats. Behav. Neurosci. 1985;99(1):151–161. doi: 10.1037//0735-7044.99.1.151. [DOI] [PubMed] [Google Scholar] · DOI
  30. Erskine MS. Pelvic and pudendal nerves influence the display of paced mating behavior in response to estrogen and progesterone in the female rat. Behav. Neurosci. 1992;106(4):690–697. doi: 10.1037//0735-7044.106.4.690. [DOI] [PubMed] [Google Scholar] · DOI
  31. Erskine MS, Lehmann ML, Cameron NM, Polston EK. Co-regulation of female sexual behavior and pregnancy induction: an exploratory synthesis. Behav. Brain Res. 2004;153(2):295–315. doi: 10.1016/j.bbr.2004.01.026. [DOI] [PubMed] [Google Scholar] · DOI
  32. Flouriot G, Pakdel F, Ducouret B, Valotaire Y. Influence of xenobiotics on rainbow trout liver estrogen receptor and vitellogenin gene expression. J. Mol. Endocrinol. 1995;15(2):143–151. doi: 10.1677/jme.0.0150143. [DOI] [PubMed] [Google Scholar] · DOI
  33. Frame GM. A collaborative study of 209 PCB congeners and 6 Aroclors on 20 different HRGC columns. Fresenius J. Anal. Chem. 1997;357:714–722. [Google Scholar]
  34. Gillette DM, Corey RD, Lowenstine LJ, Shull LR. Comparative toxicology of tetrachlorobiphenyls in mink and rats. Fundam. Appl. Toxicol. 1987;8(1):15–22. doi: 10.1016/0272-0590(87)90096-0. [DOI] [PubMed] [Google Scholar] · DOI
  35. Gore AC, Wu TJ, Oung T, Lee JB, Woller MJ. A novel mechanism for endocrine-disrupting effects of polychlorinated biphenyls: direct effects on gonadotropin-releasing hormone neurones. J. Neuroendo-crinol. 2002;14(10):814–823. doi: 10.1046/j.1365-2826.2002.00845.x. [DOI] [PubMed] [Google Scholar] · DOI
  36. Gore AC, Heindel JJ, Zoeller RT. Endocrine disruption for endocrinologists (and others) Endocrinology. 2006;147(6 Suppl):S1–S3. doi: 10.1210/en.2005-1367. [DOI] [PubMed] [Google Scholar] · DOI
  37. Gregoraszczuk EL, Zemla M, Ptak A, Grabic R. The action of low- and high-chlorinated biphenyl mixture on prepubertal porcine ovary: steroid secretion and cells apoptosis. Endocr. Regul. 2005;39(2):33–41. [PubMed] [Google Scholar]
  38. Han JS, Bird GC, Li W, Jones J, Neugebauer V. Computerized analysis of audible and ultrasonic vocalizations of rats as a standardized measure of pain-related behavior. J. Neurosci. Methods. 2005;141(2):261–269. doi: 10.1016/j.jneumeth.2004.07.005. [DOI] [PubMed] [Google Scholar] · DOI
  39. Holene E, Nafstad I, Skaare JU, Bernhoft A, Engen P, Sagvolden T. Behavioral effects of prenatal and postnatal exposure to individual polychlorinated biphenyl congeners in rats. Environ. Toxicol. Chem. 1995;14(6):967–976. [Google Scholar]
  40. Kester MH, Bulduk S, Tibboel D, Meinl W, Glatt H, Falany CN, Coughtrie MW, Bergman A, Safe SH, Kuiper GG, Schuur AG, Brouwer A, Visser TJ. Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: a novel pathway explaining the estrogenic activity of PCBs. Endocrinology. 2000;141(5):1897–1900. doi: 10.1210/endo.141.5.7530. [DOI] [PubMed] [Google Scholar] · DOI
  41. Khan IA, Thomas P. Disruption of neuroendocrine control of luteinizing hormone secretion by Aroclor 1254 involves inhibition of hypothalamic tryptophan hydroxylase activity. Biol. Reprod. 2001;64(3):955–964. doi: 10.1095/biolreprod64.3.955. [DOI] [PubMed] [Google Scholar] · DOI
  42. Kholkute SD, Rodriguez J, Dukelow WR. Effects of polychlorinated biphenyls (PCBs) on in vitro fertilization in the mouse. Reprod. Toxicol. 1994;8(1):69–73. doi: 10.1016/0890-6238(94)90069-8. [DOI] [PubMed] [Google Scholar] · DOI
  43. Kilic N, Sandal S, Colakoglu N, Kutlu S, Seyran A, Yilmaz B. Endocrine disruptive effects of polychlorinated biphenyls on the thyroid gland in female rats. Tohoku J. Exp. Med. 2005;206(4):327–332. doi: 10.1620/tjem.206.327. [DOI] [PubMed] [Google Scholar] · DOI
  44. Kremer H, Lilienthal H, Hany J, Roth-Harer A, Winneke G. Sex-dependent effects of maternal PCB exposure on the electroretinogram in adult rats. Neurotoxicol. Teratol. 1999;21(1):13–19. doi: 10.1016/s0892-0362(98)00030-0. [DOI] [PubMed] [Google Scholar] · DOI
  45. Kuriyama SN, Chahoud I. In utero exposure to low-dose 2,3′,4,4′,5-pentachlorobiphenyl (PCB 118) impairs male fertility and alters neurobehavior in rat offspring. Toxicology. 2004;202(3):185–197. doi: 10.1016/j.tox.2004.05.006. [DOI] [PubMed] [Google Scholar] · DOI
  46. Lackmann GM. Polychlorinated biphenyls and hexachlorobenzene in full-term neonates. Reference values updated. Biol. Neonate. 2002;81(2):82–85. doi: 10.1159/000047188. [DOI] [PubMed] [Google Scholar] · DOI
  47. Li LA, Wang PW. PCB126 induces differential changes in androgen, cortisol, and aldosterone biosynthesis in human adrenocortical H295R cells. Toxicol. Sci. 2005;85(1):530–540. doi: 10.1093/toxsci/kfi105. [DOI] [PubMed] [Google Scholar] · DOI
  48. Lilienthal H, Neuf M, Munoz C, Winneke G. Behavioral effects of pre- and postnatal exposure to a mixture of low chlorinated PCBs in rats. Fundam. Appl. Toxicol. 1990;15(3):457–467. doi: 10.1016/0272-0590(90)90032-f. [DOI] [PubMed] [Google Scholar] · DOI
  49. Littell RC, Milliken GA, Stroup WW, Wolfinger RD. SAS Systems for Mixed Models. SAS Institute Inc.; Cary, NC.: 1999. [Google Scholar]
  50. Love OP, Shutt LJ, Silfies JS, Bortolotti GR, Smits JE, Bird DM. Effects of dietary PCB exposure on adrenocortical function in captive American kestrels (Falco sparverius) Ecotoxicology. 2003;12(14):199–208. doi: 10.1023/a:1022502826800. [DOI] [PubMed] [Google Scholar] · DOI
  51. Matthews H, Anderson M. Effect of chlorination on the distribution and excretion of polychlorinated biphenyls. Metab. Dispos. 1975;3(5):371–380. [PubMed] [Google Scholar]
  52. Meerts HA, Lilienthal H, Hoving S, vand den Berh JH, Weijers BM, Bergman A, Koeman JH, Brouwer A. Developmental exposure to 4-hydroxy-2,3,3′,4′,5-pentachlorobiphenyl (4-OH-CB107): Long-term effects on brain development, behavior, and brain stem auditory evoked potential in rats. Toxciol. Sci. 2004;82:207–218. doi: 10.1093/toxsci/kfh252. [DOI] [PubMed] [Google Scholar] · DOI
  53. Meredith JM, Moffatt CA, Auger AP, Snyder GL, Greengard P, Blaustein JD. Mating-related stimulation induces phosphorylation of dopamine- and cyclic AMP-regulated phosphoprotein-32 in progestin receptor-containing areas in the female rat brain. J. Neurosci. 1998;18(23):10189–10195. doi: 10.1523/JNEUROSCI.18-23-10189.1998. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  54. Morse DC, Seegal RF, Borsch KO, Brouwer A. Long-term alterations in regional brain serotonin metabolism following maternal polychlorinated biphenyl exposure in the rat. Neurotoxicology. 1996;17(34):631–638. [PubMed] [Google Scholar]
  55. Murugesan P, Kanagaraj P, Yuvaraj S, Balasubramanian K, Aruldhas MM, Arunakaran J. The inhibitory effects of polychlorinated biphenyl Aroclor 1254 on Leydig cell LH receptors, steroidogenic enzymes and antioxidant enzymes in adult rats. Reprod. Toxicol. 2005;20(1):117–126. doi: 10.1016/j.reprotox.2004.11.011. [DOI] [PubMed] [Google Scholar] · DOI
  56. Oskam I, Ropstad E, Lie E, Derocher A, Wiig O, Dahl E, Larsen S, Skaare JU. Organochlorines affect the steroid hormone cortisol in free-ranging polar bears (Ursus maritimus) at Svalbard, Norway. J. Toxicol. Environ. Health, A. 2004;67(12):959–977. doi: 10.1080/15287390490443731. [DOI] [PubMed] [Google Scholar] · DOI
  57. Paredes RG, Vazquez B. What do female rats like about sex? Paced mating. Behav. Brain Res. 1999;105(1):117–127. doi: 10.1016/s0166-4328(99)00087-x. [DOI] [PubMed] [Google Scholar] · DOI
  58. Pasterkamp RJ, Yuri K, Visser DT, Hayashi S, Kawata M. The perinatal ontogeny of estrogen receptor-immunoreactivity in the developing male and female rat hypothalamus. Brain Res. Dev. Brain Res. 1996;91(2):300–303. doi: 10.1016/0165-3806(95)00185-9. [DOI] [PubMed] [Google Scholar] · DOI
  59. Patisaul HB, Fortino AE, Polston EK. Neonatal genistein or bisphenol-A exposure alters sexual differentiation of the AVPV. Neurotoxicol. Teratol. 2006;28:111–118. doi: 10.1016/j.ntt.2005.11.004. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  60. Pearce ST, Liu H, Radhakrishnan I, Abdelrahim M, Safe S, Jordan VC. Interaction of the aryl hydrocarbon receptor ligand 6-methyl-1,3,8-trichlorodibenzofuran with estrogen receptor alpha. Cancer Res. 2004;64(8):2889–2897. doi: 10.1158/0008-5472.can-03-1770. [DOI] [PubMed] [Google Scholar] · DOI
  61. Pellis SM, Pellis VC. The prejuvenile onset of play fighting in laboratory rats (Rattus norvegicus) Dev. Psychobiol. 1997;31(3):193–205. [PubMed] [Google Scholar]
  62. Perakis A, Stylianopoulou F. Effects of a prenatal androgen peak on rat brain sexual differentiation. J. Endocrinol. 1986;108(2):281–285. doi: 10.1677/joe.0.1080281. [DOI] [PubMed] [Google Scholar] · DOI
  63. Pravettoni A, Colciago A, Negri-Cesi P, Villa S, Celotti F. Ontogenetic development, sexual differentiation, and effects of Aroclor 1254 exposure on expression of the arylhydrocarbon receptor and of the arylhydrocarbon receptor nuclear translocator in the rat hypothalamus. Reprod. Toxicol. 2005;20(4):521–530. doi: 10.1016/j.reprotox.2005.03.008. [DOI] [PubMed] [Google Scholar] · DOI
  64. Primus RJ, Kellogg CK. Gonadal hormones during puberty organize environment-related social interaction in the male rat. Horm. Behav. 1990;24(3):311–323. doi: 10.1016/0018-506x(90)90012-m. [DOI] [PubMed] [Google Scholar] · DOI
  65. Ptak A, Ludewig G, Lehmler HJ, Wojtowicz AK, Robertson LW, Gregoraszczuk EL. Comparison of the actions of 4-chlorobiphenyl and its hydroxylated metabolites on estradiol secretion by ovarian follicles in primary cells in culture. Reprod. Toxicol. 2005;20(1):57–64. doi: 10.1016/j.reprotox.2004.12.003. [DOI] [PubMed] [Google Scholar] · DOI
  66. Quadros PS, Pfau JL, Goldstein AY, De Vries GJ, Wagner CK. Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology. 2002;143(10):3727–3739. doi: 10.1210/en.2002-211438. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  67. Rhees RW, Shryne JE, Gorski RA. Onset of the hormone-sensitive perinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats. J. Neurobiol. 1990;21(5):781–786. doi: 10.1002/neu.480210511. [DOI] [PubMed] [Google Scholar] · DOI
  68. Romeo RD. Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J. Neuroendocrinol. 2003;15(12):1185–1192. doi: 10.1111/j.1365-2826.2003.01106.x. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  69. Salama J, Chakraborty TR, Ng L, Gore AC. Effects of polychlorinated biphenyls on estrogen receptor-beta expression in the anteroventral periventricular nucleus. Environ. Health Perspect. 2003;111(10):1278–1282. doi: 10.1289/ehp.6126. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  70. Schrader TJ, Cooke GM. Effects of Aroclors and individual PCB congeners on activation of the human androgen receptor in vitro. Reprod. Toxicol. 2003;17(1):15–23. doi: 10.1016/s0890-6238(02)00076-x. [DOI] [PubMed] [Google Scholar] · DOI
  71. Seegal RF, Bush B, Brosch KO. Polychlorinated biphenyls induce regional changes in brain norepinephrine concentrations in adult rats. Neurotoxicology. 1985;6(3):13–23. [PubMed] [Google Scholar]
  72. Seegal RF, Bush B, Shain W. Lightly chlorinated ortho-substituted PCB congeners decrease dopamine in nonhuman primate brain and in tissue culture. Toxicol. Appl. Pharmacol. 1990;106(1):136–144. doi: 10.1016/0041-008x(90)90113-9. [DOI] [PubMed] [Google Scholar] · DOI
  73. Seegal RF, Okoniewski RJ, Brosch KO, Bemis JC. Polychlorinated biphenyls alter extraneuronal but not tissue dopamine concentrations in adult rat striatum: an in vivo microdialysis study. Environ. Health Perspect. 2002;110(11):1113–1117. doi: 10.1289/ehp.021101113. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  74. Sharpe RM. The influence of the sex of litter-mates on subsequent maternal behaviour in Rattus norvegicus. Anim. Behav. 1975;23(3):551–559. doi: 10.1016/0003-3472(75)90132-3. [DOI] [PubMed] [Google Scholar] · DOI
  75. Shekhar PV, Werdell J, Basrur VS. Environmental estrogen stimulation of growth and estrogen receptor function in preneoplastic and cancerous human breast cell lines. J. Natl. Cancer Inst. 1997;89(23):1774–1782. doi: 10.1093/jnci/89.23.1774. [DOI] [PubMed] [Google Scholar] · DOI
  76. Stellman SD, Djordjevic MV, Muscat JE, Gong L, Bernstein D, Citron ML, White A, Kemeny M, Busch E, Nafziger AN. Relative abundance of organochlorine pesticides and polychlorinated biphenyls in adipose tissue and serum of women in Long Island, New York. Cancer Epidemiol., Biomarkers Prev. 1998;7(6):489–496. [PubMed] [Google Scholar]
  77. Takagi Y, Aburada S, Hashimoto K, Kitaura T. Transfer and distribution of accumulated (14C)polychlorinated biphenyls from maternal to fetal and suckling rats. Arch. Environ. Contam. Toxicol. 1986;15(6):709–715. doi: 10.1007/BF01054917. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  78. Tanabe S, Nakagawa Y, Tatsukawa R. Absorption efficiency and biological half-life of individual chlorobiphenyls in rats treated with kanechlor products. Agric. Biol. Chem. 1981;45(3):717–726. [Google Scholar]
  79. Thomas G, Sweetman AJ, Ockenden WA, Mackay D, Jones KC. Air-pasture transfer of PCBs. Environ. Sci. Technol. 1998;32:936–942. [Google Scholar]
  80. Tobet SA, Fox TO. Sex- and hormone-dependent antigen immunoreactivity in developing rat hypothalamus. Proc. Natl. Acad. Sci. U. S. A. 1989;86(1):382–386. doi: 10.1073/pnas.86.1.382. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  81. Tsai ML, Webb RC, Loch-Caruso R. Increase of oxytocin-induced oscillatory contractions by 4-hydroxy-2′,4′,6′-trichlorobiphenyl is estrogen receptor mediated. Biol. Reprod. 1997;56(2):341–347. doi: 10.1095/biolreprod56.2.341. [DOI] [PubMed] [Google Scholar] · DOI
  82. Wagner CK, Nakayama AY, De Vries GJ. Potential role of maternal progesterone in the sexual differentiation of the brain. Endocrinology. 1998;139(8):3658–3661. doi: 10.1210/endo.139.8.6223. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  83. Wang XQ, Fang J, Nunez AA, Clemens LG. Developmental exposure to polychlorinated biphenyls affects sexual behavior of rats. Physiol. Behav. 2002;75(5):689–696. doi: 10.1016/s0031-9384(02)00673-x. [DOI] [PubMed] [Google Scholar] · DOI
  84. Weltje L, vom Saal FS, Oehlmann J. Reproductive stimulation by low doses of xenoestrogens contrasts with the view of hormesis as an adaptive response. Hum. Exp. Toxicol. 2005;24(9):431–437. doi: 10.1191/0960327105ht551oa. [DOI] [PubMed] [Google Scholar] · DOI
  85. Wersinger SR, Baum MJ, Erskine MS. Mating-induced FOS-like immunoreactivity in the rat forebrain: a sex comparison and a dimorphic effect of pelvic nerve transection. J. Neuroendocrinol. 1993;5(5):557–568. doi: 10.1111/j.1365-2826.1993.tb00522.x. [DOI] [PubMed] [Google Scholar] · DOI
  86. Woodhouse AJ, Cooke GM. Suppression of aromatase activity in vitro by PCBs 28 and 105 and Aroclor 1221. Toxicol. Lett. 2004;152(1):91–100. doi: 10.1016/j.toxlet.2004.04.009. [DOI] [PubMed] [Google Scholar] · DOI
  87. Yamane T, Fukuda N, Inaba J, Nishimura Y. Effect of polychlorinated biphenyls (PCB) on metabolism of thyroid hormone in Wistar rats. Nippon Eiseigaku Zasshi. 1975;30(4):497–502. doi: 10.1265/jjh.30.497. [DOI] [PubMed] [Google Scholar] · DOI

Cited by

Sorted by citations

Authors
Steinberg, R. M., Juenger, T. E., & Gore, A. C.
Affiliations
The University of Texas at Austin (US)
Corresponding author
Gore, Andrea C.
ORCID
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2007-03
Volume
51
Issue
3
Pages
364-372
ISSN
0018-506X (ISSN-L)
DOI
10.1016/j.yhbeh.2006.12.004
PMC
PMC2692581
OpenAlex
W1968260268
Cited by
87
References
2
Citations by year
2024: 4 · 2023: 1 · 2022: 4 · 2021: 7 · 2020: 5 · 2019: 1 · 2018: 8 · 2017: 5 · 2016: 4 · 2015: 9 · 2014: 2 · 2013: 6 · 2012: 4
FWCI
2.28
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Hormones and Behavior (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Pharmaceutical Research and Manufacturers of America Foundation
  • National Institute of Environmental Health Sciences (#ES07784, ES12272, R21ES012272, P30ES007784)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Keywords
polychlorinated biphenyls, Aroclor 1221, prenatal exposure, endocrine disruptors, female reproductive behavior, mating behavior, dose-response relationship, vocalizations, ambulation, reproductive success
MeSH terms
Animals, Aroclors, Dose-Response Relationship, Drug, Female, Humans, Male, Polychlorinated Biphenyls, Pregnancy, Pregnancy, Animal, Prenatal Exposure Delayed Effects, Reproduction, Sexual Behavior, Animal, Time Factors, Rats, Sprague-Dawley, Models, Animal, Rats, Endocrine Disruptors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review