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Fundulus Heteroclitus): Diverences in Populations from Polluted and Reference Environments

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Fundulus Heteroclitus): Diverences in Populations from Polluted and Reference Environments General and Comparative Endocrinology 150 (2007) 174–188 www.elsevier.com/locate/ygcen Communications in Genomics and Proteomics Cloning of three estrogen receptors (ER) from killiWsh (Fundulus heteroclitus): DiVerences in populations from polluted and reference environments Sarah R. Greytak, Gloria V. Callard ¤ Department of Biology, Boston University, Boston, MA 02215, USA Received 13 March 2006; revised 10 June 2006; accepted 26 July 2006 Available online 8 September 2006 Abstract Epidemiological, wildlife, and laboratory studies support the hypothesis that chemicals released into the environment through anthro- pogenic activities are responsible for abnormalities of reproduction and development. Although the New Bedford Harbor (NBH) killiWsh population has survived and reproduced successfully for >50 yr (»20 generations), Wsh have high body burdens of the major NBH con- taminants (polychlorinated biphenyls); elevated levels of P450 aromatase B and vitellogenin mRNA (markers of estrogen eVect); and evi- dence of endocrine disruption. To investigate possible adaptive changes in the estrogen response system of NBH killiWsh, we cloned the estrogen receptors (ER) from killiWsh populations resident in NBH and a relatively unpolluted reference site (Scorton Creek MA, SC). ER, -a, and -b cDNAs encoding full-length polypeptides of 620, 543, and 672 amino acids, respectively, were identiWed. Each ER sub- type had multiple splice variants, single nucleotide polymorphisms (SNPs), and a characteristic tissue distribution and developmental proWle. As measured by real-time quantitative RT-PCR analysis, the overall tissue distribution of each ER was similar in NBH and SC Wsh, implying that the regulatory pathways which maintain tissue-speciWc expression are largely unchanged by long term pollutant expo- sure. Nonetheless, a striking diVerence was seen in the quantity of mRNA of the estrogen-inducible gene ER, which was signiWcantly lower in brain, liver and ovaries of reproductively active NBH as compared to SC females. Paradoxically, despite the “estrogenic” NBH environment, ER mRNA levels did not diVer in reproductively inactive NBH and SC females, or in males at the two sites at any time of year. We interpret results in NBH Wsh as due in part to a deWcit of circulating estrogen, and in part to pollutant-mediated hyporesponsive- ness of the ER gene. In marked contrast to adult Wsh, ER was elevated »5-fold in NBH as compared to SC embryos/larvae, perhaps indicative of estrogenic chemicals in yolk. We conclude that contaminants in the NBH environment impact molecular components of the estrogen signaling pathways in resident killiWsh populations. Whether these changes are transient or heritable requires further study. © 2006 Elsevier Inc. All rights reserved. Keywords: Estrogen receptor; ER; PCBs; KilliWsh; New Bedford Harbor Superfund Site; Molecular markers; Endocrine disruption; Reproduction 1. Introduction in the environment, have the potential to disrupt critical hormone-regulated processes of reproduction and develop- In addition to their toxic and teratogenic eVects, which ment, even at low concentrations and transient exposures generally result from high dose exposures, halogenated aro- (reviewed in Phillips and Harrison, 1999; Sumpter and matic hydrocarbons (HAH) including polychlorinated dib- Johnson, 2005). Although the “endocrine disruptor hypoth- enzodioxins (PCDDs), dibenzofurans (PCDFs), and esis” is still a matter of debate (Safe, 2005), strong theoreti- polychlorinated biphenyls (PCBs), pesticides, plasticizers, cal support comes from laboratory studies, which show drugs, heavy metals, and other chemicals that accumulate that these chemicals can mimic or block hormone-receptor interactions or otherwise aVect signal transduction path- * Corresponding author. Fax: +1 617 353 2923. ways (Crisp et al., 1998; Phillips and Harrison, 1999). Addi- E-mail address: [email protected] (G.V. Callard). tional evidence is based on epidemiological and wildlife 0016-6480/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.ygcen.2006.07.017 S.R. Greytak, G.V. Callard / General and Comparative Endocrinology 150 (2007) 174–188 175 studies which report an increased incidence, or geographi- (Zhu and Conney, 1998) or production (Baba et al., 2005) cal clusters, of reproductive and developmental abnormali- of endogenous estrogens. In addition to dioxin-like PCBs, a ties in the natural environment (Crisp et al., 1998; Phillips subset of PCB congeners and in vivo metabolites can aVect and Harrison, 1999; Mills and Chichester, 2005). Nonethe- reproductive processes by virtue of their ability to bind to less, neither laboratory nor observational approaches per se ER directly and exert agonist or antagonist eVects, depend- reveal the biological consequences of chronic, multigenera- ing on their aYnity and concentration relative to endoge- tional exposures to complex chemical mixtures, and only nous ligand (Connor et al., 1997; Lind et al., 1999). rarely have physiological or genetic mechanisms that per- Our knowledge of the biological activities of NBH pollu- mit or promote survival and reproductive success of tants is far from complete; however, results of our earlier exposed populations been investigated. study show that the NBH environment is “estrogenic”, as To address these issues, killiWsh (Fundulus heteroclitus) measured by increased mRNA levels of hepatic vitellogenin at the New Bedford Harbor MA (NBH) Superfund site, (vtg) and brain P450 aromatase B (P450aromB) in NBH when compared to killiWsh at a relatively unpolluted site males and reproductively inactive females (Greytak et al., (Scorton Creek MA, SC), are an extremely valuable 2005). In the same study, we obtained evidence of endocrine resource. NBH is one of the most extensively PCB-contam- disruption. In reproductively active NBH females, gonado- inated sites in the United States (Weaver, 1983). The history somatic index, hepatosomatic index, plasma estrogen, and of pollution in NBH indicates that the resident killiWsh expression of hepatic vtg and brain P450aromB were sig- population has been exposed to complex mixtures of PCBs, niWcantly lower than in NBH females (Greytak et al., 2005). heavy metals, and other pollutants for >50 yr (»20 genera- The data are consistent with an impact of NBH contami- tions). Despite high body burdens of contaminants (Black nants at one or more levels of the hypothalamic–pituitary– et al., 1998), NBH killiWsh continue to survive and repro- gonadal (HPG) axis. Nonetheless, the seasonal onset and duce (Black et al., 1998). Indeed, killiWsh are highly abun- regression of reproductive condition occur at essentially the dant in NBH (D. Nacci, personal communication). Survival same time in SC and NBH Wsh (Greytak et al., 2005); males of the NBH killiWsh population has been ascribed to and females display a semilunar spawning cycle at both acquired resistance to the toxic eVects of dioxin and dioxin- sites (Black et al., 1998); and viable embryos can be like PCBs (Nacci et al., 1999; Bello et al., 2001). Toxicity of obtained after natural spawning or in vitro fertilization dioxin-like chemicals (DLC) is mediated mainly by arylhy- (Black et al., 1998; Powell et al., 2000). drocarbon receptors (AHR) (Schmidt and BradWeld, 1996). By analogy to acquired resistance to AHR-mediated Although the mechanism of resistance is unclear, compari- toxicity, we postulated that changes in ER-mediated signal- son of NBH and SC killiWsh shows diVerences in tissue-spe- ing pathways of NBH killiWsh could attenuate or neutralize ciWc expression and induction of AHR1 and CYP1A1 eVects of excess environmental estrogen, and thereby con- mRNAs (Powell et al., 2000; Bello et al., 2001), and site-spe- tribute to the reproductive success of the NBH population. ciWc single nucleotide polymorphisms (SNPs) in AHR1 In mammals, the diversity and complexity of estrogen sig- (Hahn et al., 2004). Some but not all of these traits are heri- naling systems is accomplished by two distinct ER genes ( table, indicating that NBH killiWsh reXect current as well as and ) and multiple splice variants (Hall et al., 2001). By historical population exposures to PCBs and other contam- contrast, teleost Wsh have one ER and two ER-subtypes inants. (Hawkins et al., 2000; Menuet et al., 2002; Sabo-Attwood AHR are expressed in many reproductively relevant tis- et al., 2004), termed ERa and ERb (Hawkins and sues (Hahn, 1998) and, in addition to their role in toxicity, Thomas, 2004). Each Wsh ER has one or more splice vari- activation of AHR can impact reproduction by altering the ants (Tchoudakova et al., 1999; Pakdel et al., 2000; Menuet estrogen signaling pathway (reviewed in Safe et al., 2000). et al., 2001) and a characteristic ligand binding proWle, tis- Estrogen receptors (ER) are ligand-activated transcription sue distribution, and regulation (Hawkins and Thomas, factors, which bind to estrogen response elements (ERE) in 2004; Menuet et al., 2004). Interestingly, the teleostean ER regulatory regions of target genes. Like all members of the gene itself is highly estrogen inducible, at least in liver, steroid/thyroid hormone /retinoic acid receptor superfam- indicative of a physiologically relevant autoregulatory ily, ER have a prototypical nuclear receptor structure with mechanism (Urushitani et al., 2003; Menuet et al., 2004). In conserved functional domains designated A–F (AB, activa- theory, therefore, chronic multigenerational exposure to tion function1; C, DNA binding domain; D,
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