Cloning, characterisation, and expression of three oestrogen receptors (ERα, ERβ1 and ERβ2) in the European sea bass, Dicentrarchus labrax

Halm, Silke; Martı́nez-Rodrı́guez, Gonzalo; Rodríguez, Lucinda; Prat, Francisco; Mylonas, Constantinos C.; Carrillo, Manuel; Zanuy, Silvia

doi:10.1016/j.mce.2004.05.009

Cited by 98 publications

(55 citation statements)

References 43 publications

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“…IGF-1, IGF-2; GH-1, GH-2) (Wittbrodt et al, 1998;Palti et al, 2004). With respect to fish ERs, two different isoforms of the ERβ subtype have been reported in several ray-finned fish species (Tchoudakova et al, 1999;Ma et al, 2000;Menuet et al, 2002;Halm et al, 2004;Hawkins and Thomas, 2004;SaboAttwood et al, 2004) presumably because of genome duplication. Since the fish ERβ subtype has been duplicated, it is predicted that the other ER subtype, ERα, should also be found as two isoforms.…”

Section: Introductionmentioning

confidence: 99%

The complete nuclear estrogen receptor family in the rainbow trout: Discovery of the novel ERα2 and both ERβ isoforms

Nagler

Cavileer

Sullivan

et al. 2007

Gene

156

101

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Estrogen hormones interact with cellular ERs to exert their biological effects in vertebrate animals. Similar to other animals, fishes have two distinct ER subtypes, ERalpha (NR3A1) and ERbeta (NR3A2). The ERbeta subtype is found as two different isoforms in several fish species because of a gene duplication event. Although predicted, two different isoforms of ERalpha have not been demonstrated in any fish species. In the rainbow trout (Oncorhynchus mykiss), the only ER described is an isoform of the ERalpha subtype (i.e. ERalpha1, NR3A1a). The purpose of this study was to determine whether the gene for the other ERalpha isoform, ERalpha2 (i.e., NR3A1b), exists in the rainbow trout. A RT-PCR and cloning strategy, followed by screening a rainbow trout BAC library yielded a unique DNA sequence coding for 558 amino acids. The deduced amino acid sequence had a 75.4% overall similarity to ERalpha1. Both the rainbow trout ERbeta subtypes, ERbeta1 [NR3A2a] and ERbeta2, [NR3A2b] which were previously unknown in this species, were also sequenced as part of this study, and the amino acid sequences were found to be very different from the ERalphas (approximately 40% similarity). ERbeta1 and ERbeta2 had 594 and 604 amino acids, respectively, and had 57.6% sequence similarity when compared to one another. This information provides what we expect to be the first complete nuclear ER gene family in a fish. A comprehensive phylogenetic analysis with all other known fish ER gene sequences was undertaken to understand the evolution of fish ERs. The results show a single ERalpha subtype clade, with the closest relative to rainbow trout ERalpha2 being rainbow trout ERalpha1, suggesting a recent, unique duplication event to create these two isoforms. For the ERbeta subtype there are two distinct subclades, one represented by the ERbeta1 isoform and the other by the ERbeta2 isoform. The rainbow trout ERbeta1 and ERbeta2 are not closely associated with each other, but instead fall into their respective ERbeta subclades with other known fish species. Real-time RT-PCR was used to measure the mRNA levels of all four ER isoforms (ERalpha1, ERalpha2, ERbeta1, and ERbeta2) in stomach, spleen, heart, brain, pituitary, muscle, anterior kidney, posterior kidney, liver, gill, testis and ovary samples from rainbow trout. The mRNAs for each of the four ERs were detected in every tissue examined. The liver tended to have the highest ER mRNA levels along with the testes, while the lowest levels were generally found in the stomach or heart. The nuclear ERs have a significant and ubiquitous distribution in the rainbow trout providing the potential for complex interactions that involve the functioning of many organ systems.

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Section: Introductionmentioning

confidence: 99%

The complete nuclear estrogen receptor family in the rainbow trout: Discovery of the novel ERα2 and both ERβ isoforms

Nagler

Cavileer

Sullivan

et al. 2007

Gene

156

101

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“…Three types of ER exist in fish, namely ERa, ERb1 and ERb2 (Hawkins et al 2000, Menuet et al 2002, Choi & Habibi 2003, Halm et al 2004, Filby & Tyler 2005; the types are designated as, (gene/protein) esr1/Esr1, esr2b/Esr2b and esr2a/Esr2a respectively, following the Official Zebrafish Nomenclature Guidelines (http://zfin.org). All types of ER are expressed in testis (Hawkins et al 2000, Menuet et al 2002, Choi & Habibi 2003, Halm et al 2004, Filby & Tyler 2005.…”

Section: Introductionmentioning

confidence: 99%

“…All types of ER are expressed in testis (Hawkins et al 2000, Menuet et al 2002, Choi & Habibi 2003, Halm et al 2004, Filby & Tyler 2005. Studies describing their cellular localization in testis indicate a heterogeneous pattern of mRNA and protein expression, for example, Esr1 protein has been found in the interstitial tissue of rainbow trout (Oncorhynchus mykiss) testis (Bouma & Nagler 2001), esr1 and esr2 mRNA expressions were found in Japanese common goby (Acanthogobius flavimanus) and Japanese eel (Anguilla japonica) Sertoli cells (Miura et al 1999, Ito et al 2007, while Esr1 and Esr2 proteins were produced by meiotic and postmeiotic germ cells in channel catfish (Ictalurus punctatus) testis (Wu et al 2001).…”

Section: Introductionmentioning

confidence: 99%

Oestrogen-induced androgen insufficiency results in a reduction of proliferation and differentiation of spermatogonia in the zebrafish testis

Waal¹,

Leal²,

García-López³

et al. 2009

Journal of Endocrinology

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Androgens can induce complete spermatogenesis in immature or prepubertal teleost fish. However, many aspects of the role of androgens in adult teleost spermatogenesis have remained elusive. Since oestrogens inhibit androgen synthesis, we used an oestrogen-induced androgen depletion model to identify androgen-dependent stages during adult zebrafish spermatogenesis. Exposure to 10 nM 17b-oestradiol (E 2 ) in vivo at least halved the mass of differentiating germ cells (from type B spermatogonia to spermatids), while type A spermatogonia accumulated. Studies on the cellular dynamics revealed that a reduction of spermatogonial proliferation together with an inhibition of their differentiation to type B spermatogonia were the basis for the oestrogen-mediated disturbance of spermatogenesis. The capacity of the zebrafish testis to produce 11-ketotestosterone as well as the expression of steroidogenesis-related genes was markedly decreased after in vivo oestrogen exposure. Moreover, the androgen-release response to recombinant zebrafish Lh was lost after oestrogen exposure. We conclude that oestrogen exposure caused a state of androgen insufficiency in adult male zebrafish. Since the downregulation of the steroidogenic system as well as the disturbance of spermatogenesis in testicular explants exposed to E 2 ex vivo was much less severe than after in vivo exposure, the main inhibitory effect appears to be exerted via feedback inhibition of gonadotropin release. This experimental set-up helped to identify spermatogonial proliferation and their differentiation as androgen targets in adult zebrafish spermatogenesis.

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“…The first histological signs of ovarian and testicular differentiation appear when fish reach 79-90 and 83-95 mm standard length (SL), respectively ($150-200 days post fertilization (dpf)) (Saillant et al, 2003), but depending on growth rates some fish can remain sexually undifferentiated until they reach 120 mm (Saillant et al, 2003;Piferrer et al, 2005). Several genes related with sex differentiation have been characterized and their expression profiles studied including cyp19a1a (Dalla Valle et al, 2002;Blázquez et al, 2008), cyp19a1b (Blázquez and Piferrer, 2004;Blázquez et al, 2008), amh (Halm et al, 2007), dax1 , estrogen receptors (ers) (Halm et al, 2004;Blázquez et al, 2008), androgen receptor b, arb , cyp11b (Socorro et al, 2007). Moreover, HTs affect aromatase catalytic activity (González and Piferrer, 2002) and promote male development (Pavlidis et al, 2000;Koumoundouros et al, 2002).…”

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confidence: 99%

Expression profiles of sex differentiation‐related genes during ontogenesis in the European sea bass acclimated to two different temperatures

2009

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The European sea bass is a teleost fish that lacks sex chromosomes and for which temperature influences sex ratios. However, correlation between temperature, developmental stage at a given age and sex-specific gene expression is hampered by the lack of sex markers. To study this correlation, fish were exposed to feminizing (15 degrees C) or masculinizing temperature (21 degrees C) from 0-120 days post fertilization, throughout the thermosensitive period (TSP). Aromatase (cyp19a1a), 11beta-hydroxylase (cyp11b), androgen receptor (arb) and estrogen receptors (era, erb1 and erb2) were assessed by qPCR prior and during sex differentiation. Canonical discriminant analysis (CDA), with length--as proxy for developmental stage--and cyp19a1a expression as predictors, was validated and used to reliably assign gonadal sex to fish sampled within and outside the TSP. Differences in cyp19a1a and cyp11b expression could be detected 1-month before the first signs of histological sex differentiation. Cyp19a1a and cyp11b were significantly higher in future females and males, respectively, and revealed as robust molecular markers to predict future ovarian and testicular differentiation. In contrast, no association between phenotypic sex and arb, era, erb1 and erb2 expression was found, suggesting that these genes do not contribute to the differentiation of a particular sex. The CDA-based approach implemented here could be used to sex undifferentiated animals in species where genetic sex cannot be known owing to the lack of simple sex determining systems, as it is the case of many fish and reptiles with or without temperature-dependent sex determination, and provide a useful tool to relate gene expression and phenotypic sex.

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Cloning, characterisation, and expression of three oestrogen receptors (ERα, ERβ1 and ERβ2) in the European sea bass, Dicentrarchus labrax

Cited by 98 publications

References 43 publications

The complete nuclear estrogen receptor family in the rainbow trout: Discovery of the novel ERα2 and both ERβ isoforms

The complete nuclear estrogen receptor family in the rainbow trout: Discovery of the novel ERα2 and both ERβ isoforms

Oestrogen-induced androgen insufficiency results in a reduction of proliferation and differentiation of spermatogonia in the zebrafish testis

Expression profiles of sex differentiation‐related genes during ontogenesis in the European sea bass acclimated to two different temperatures

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