Developmental exposure to polychlorinated biphenyls affects sexual behavior of rats
Introduction
Polychlorinated biphenyls (PCBs) are persistent environmental pollutants because of their chemical stability and ability to accumulate in the food chain. They are detected in the air, water, sediments, wildlife, and human adipose tissue, milk, and serum [1], [2], [3], [4]. PCBs have the potential to disrupt reproduction through various pathways. They are reported to decrease female fertility by reducing implanted ova and increasing the degeneration rate of embryos in mice [5], [6]. A possible mechanism for this effect is through the change of the biochemical environment of the ovaries and uterus during oogenesis or pregnancy [7], [8]. PCBs also affect male fertility by depressing the reproductive organs [9], [10] and by reducing sperm production [9]. Further, androgen metabolism was altered in males [10], [11], [12], and progesterone (P) synthesis was disrupted in female rats [13], following exposure to PCBs.
Perinatal treatment with the PCB mixtures, Aroclor 1221 and Aroclor 1254, has been shown to decrease sexual behavior in female rats [14], [15], [16]. These commercial PCB mixtures are composed of different concentrations of coplanar and noncoplanar PCBs. Therefore, some PCBs, such as the commercial mixture A1221, may act as endocrine disrupters because of their affinity for estrogen receptors [17]. However, other PCB mixtures, such as A1254, exhibit minimal binding to estrogen receptors, and some of their metabolites may even have antiestrogenic activity [4], [17]. In this study, we evaluate the effects of prenatal exposure to the dioxin-like PCB congener 3,4,3′,4′-tetrachlorobiphenyl (PCB 77), and the noncoplanar di-ortho-substituted PCB congener, 2,4,2′,4′-tetrachlorobiphenyl (PCB 47), on the development of sexual behavior in the laboratory rat. Both of these congeners have been shown to alter brain dopamine levels (see [18], [19] for review), a neurotransmitter that plays an important role in mediating male and female sexual behavior [20], [21]. PCB 77 is also reported to have estrogenic and antiestrogenic activity [22], [23].
Section snippets
Methods
Fifty time-mated Long–Evans female rats were purchased from Harlan–Sprague Dawley (Indianapolis, IN). Upon arrival, the rats were randomly divided into five groups and housed individually in plastic cages (50×25×20 cm). There was a minimum of nine dams per experimental treatment. These animals were kept in a colony room at 23±2 °C, under a 12:12 light/dark cycle (lights on at 1900 h) and with a relative humidity of 55%. Food (Harlan Teklad 22/5 rodent diet #8640, Madison, WI) and tap water were
Behavioral results
Prenatal exposure to PCB 77 decreased sexual receptivity in female rats as measured by LQ (χ2=20.365, df=2, P<.001; Fig. 1); however, treatment with PCB 47 had a significant effect only in the 20-mg/kg group (χ2=6.868, df=2, P<.05). Exposure to PCB 77 significantly decreased the AL of the females [F(2,25)=4.905, P<.05] in both the 0.25- and 1-mg/kg groups compared with that of the control group (Fig. 2). Treatment with PCB 47 did not significantly affect AL. MRL, IRL, and PER were not affected
Discussion
Our results demonstrate that prenatal exposure to both the coplanar congener PCB 77 and the ortho-chlorinated congener PCB 47 at subtoxic doses reduces sexual receptivity of female rats as measured by the LQ. This effect was seen at both doses for the coplanar PCB, but only at the relatively high dose in the case of PCB 47. All PCB-treated groups that showed deficits in lordosis also showed a significant increase in anogenital distance. Since PCB 77 has been reported to be estrogenic as well as
Acknowledgements
The work in this manuscript was supported by NIEHS Superfund Grant P42ES049 and NSF Grant IBN9728883 to Lynwood G. Clemens and by a grant from the Sichuan Provincial Education Commission, China to X.Q. Wang.
References (36)
- et al.
PCB and dioxin levels in plasma and human milk of 418 Dutch women and their infants: predictive value of PCB congener levels in maternal plasma for fetal and infant's exposure to PCBs and dioxins
Chemosphere
(1994) - et al.
Antiestrogen activity of hydroxylated polychlorinated biphenyl congeners identified in human serum
Toxicol Appl Pharmacol
(1997) - et al.
Effects of long-term feeding of polychlorinate biphenyls (PCB, clophen a 60) on the length of oestrous cycle and on the frequency of implanted ova in the mouse
Environ Res
(1973) - et al.
Effects of polychlorinated biphenyls (PCBs) on in vitro fertilization in the mouse
Reprod Toxicol
(1994) - et al.
Polychlorinated biphenyls and nutritional restriction: their effects and interaction on endocrine and reproductive characteristics of male and white mice
Toxicol Appl Pharmacol
(1977) - et al.
Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants
Eur J Pharmacol Environ Toxicol Pharmacol
(1995) - et al.
Effects of in utero and lactational exposure of the laboratory rat to 2,4,2′,4′- and 3,4,3′,4′-tetrachlorobiphenyl on dopamine function
Toxicol Appl Pharmacol
(1997) - et al.
Estrogenic and antiestrogenic actions of PCBs in the female rat: in vitro and in vivo studies
Reprod Toxicol
(1993) Sexual attractivity, proceptivity and receptivity in female mammals
Horm Behav
(1976)- et al.
Antisense oligodeoxynucleotides in behavioral neuroscience
Neuroprotocols
(1993)
Paced copulation in rats: effects of intromission frequency and duration on luteal activation and estrous length
Physiol Behav
Behavioral effects following single and combine maternal exposure to PCB 77 (3,4,3′,4′-tetrachlorobiphenyl) and PCB 47 (2,4,2′,4′-tetrachlorobiphenyl) in rats
Neurotoxicol Teratol
3,4,3′,4′-Tetrachlorobiphenyl given to mice prenatally produces long-term decreases in striatal dopamine and receptor binding sites in the caudate nucleus
Toxicol Lett
Polychlorinated biphenyls and the developing nervous system: cross-species comparisons
Neurotoxicol Teratol
The transfer of polycholorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs) across the human placenta and into maternal milk
Am J Public Health
Structures and levels of most chlorobiphenyls in two technical PCB products and in human adipose tissue
Ambio
An assessment of the reproductive toxic potential of Aroclor 1254 in female Sprague–Dawley rats
Bull Environ Contam Toxicol
Delayed pregnancy in NMRI mice treated with PCB: 2,2′dechlorobiphenyl
Bull Environ Contam Toxicol
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2019, Hormones and BehaviorCitation Excerpt :Sexual behavior studies in male rats showed that developmental PCB77 or PCB126 increased numbers of intromissions but did not affect pregnancy outcomes (Faqi et al., 1998). Another report in male rats reported no effect of PCB47 or PCB77 (Wang et al., 2002). By contrast, measures of sexual behavior in females have revealed effects of developmental PCB exposures.