Differential expression patterns of three aromatase genes and of four estrogen receptors genes in the testes of trout (Oncorhynchus mykiss)

Abstract

Estrogens are implicated in male gonad function, although their physiological roles remain uncertain. In the present study, we take advantage of the original model of spatio-temporal organization of trout spermatogenesis to revisit the synthesis and action sites of estrogens in fish testis. Within this system, somatic cell and germ cell development are synchronized due to a strict seasonal spermatogenetic cycle and the cystic organization of gonads. We evaluated the expression patterns and regulation of three aromatase isoforms (cyp19a, cyp19b-I, and cyp19b-II) and four estrogen receptors (esr1a, esr1b, esr2a, and esr2b) by quantitative reverse-transcriptase PCR during testicular maturation and in isolated germ cell populations. Our data demonstrated a reciprocal relationship between cyp19a and cyp19b (I and II) expression during testicular development (cyp19a decreased while cyp19b increased with maturation). Furthermore, cyp19b is significantly expressed in late germ cells. At the protein level, aromatase was immunohistochemically identified in interstitial tissue and in germ cells. Remarkable elevation of esr1a and esr2a was observed during the final stage of spermiation, while esr1b was expressed in an early stage of spermatogenetic development. Estrogen implants reduced testicular cyp19a transcript abundance while up-regulating cyp19b levels, whereas androgens up-regulated testicular esr1a, esr2a, and esr2b. Together, the distinct spatio-temporal expression profiles and regulation of aromatases and estrogen receptors suggest that estrogens have discrete physiological functions during an early step of spermatogenesis and in the final stages of germ cell maturation and/or excretion.

Large-scale transcriptome sequencing reveals novel expression patterns for key sex-related genes in a sex-changing fish

“…Such male-biased expression of estrogen receptors has been shown during late sexual differentiation for Nile tilapia (70dah) [ 49 ] and rainbow trout (60-110dpf) [ 110 ]. A recent study on rainbow trout also showed significantly elevated testicular expression of esr1a and esr2a during the final stage of spermiation, while esr1b and esr2b were expressed at early stages of testicular development [ 111 ]. In the same study, androgen implants up-regulated testicular esr1a , esr2a , and esr2b expression but down-regulated cyp19a1a expression, whereas estrogens reduced testicular cyp19a1a expression but increased the expression of cyp19a1b and esr1b .…”

P450 aromatase: a key enzyme in the spermatogenesis of the Italian wall lizard, Podarcis sicula

“…Indeed, it is well known that P450 aromatase controls the synthesis of 17β-estradiol, one of the most relevant factors that locally controls spermatogenesis in non-mammalian (Cardone et al, 2002;Lance, 2009;Urbatzka et al, 2007;Burrone et al, 2012;Peñaranda et al, 2014;Delalande et al, 2015) and mammalian (O'Donnell et al, 2001;Carreau et al, 2007) vertebrates. In P. sicula, it is well known that high titres of 17β-estradiol are responsible for the spermatogenesis block (Angelini and Botte, 1992) and that 17β-estradiol production is under the control of VIP (Rosati et al, 2015) and PACAP , two neuropeptides involved in the control of lizard spermatogenesis (Agnese et al, 2010(Agnese et al, ,b,c, 2016Rosati et al, 2014aRosati et al, ,b, 2016.…”

“…In non-mammalian vertebrate testes, investigations on P450 aromatase are limited to a few species: the trout Oncorhynchus mykiss (Delalande et al, 2015), the eel Anguilla anguilla (Peñaranda et al, 2014), the frogs Xenopus laevis (Urbatzka et al, 2007) and Pelophylax esculenta (Burrone et al, 2012), and the lizard Podarcis sicula (Cardone et al, 2002;Lance, 2009). In particular, in P. sicula, our experimental model, the partial coding sequence of P450 aromatase is known (gi 257359521), and it has been shown that the P450 aromatase inhibition by fadrozole modifies spermatogenesis, as well as the epididymis morphology (Cardone et al, 2002).…”

Initiation of sex change and gonadal gene expression in black sea bass (Centropristis striata) exposed to exemestane, an aromatase inhibitor

“…Gonadal estrogens are likely important in black sea bass testes, as both cyp19a1a and estrogen receptor beta (esr2b) were upregulated. Estrogen receptor alpha (esr1) was only slightly elevated, but may exhibit greater upregulation later during spermiation, as in rainbow trout (Oncorhynchus mykiss) (Bouma and Nagler, 2001;Delalande et al, 2015).…”