Effect of Sex Steroids on Gonadal Differentiation and Sex Reversal in the Frog, Rana curtipes

Saidapur, Srinivas K.; Gramapurohit, Narahari P.; Shanbhag, Bhagyashri A.

doi:10.1006/gcen.2001.7699

Cited by 33 publications

(21 citation statements)

References 24 publications

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“…However, when the hormones are applied during sexual differentiation, they cause partial sex reversal and hermaphroditism, but they have no effect when administered later. Similar phenomena were also described for Rana curtipes and Rana pipiens (Saidapur et al 2001, Hogan et al 2008.…”

Section: Introductionsupporting

confidence: 83%

“…Our previous study showed that the first signs of normal sexual differentiation in Bombina appear in male gonads relatively early at Gosner stage 33 when the germ cells translocate from the cortex to the medulla (Piprek et al 2010). Importantly, it has been previously demonstrated that the effect of hormone depends on the timing of administration (Villalpando & Merchant-Larios 1990, Saidapur et al 2001, Hogan et al 2008). Exposure to testosterone or E 2 before sexual differentiation usually causes total sex reversal; exposure beginning during the sexual differentiation results in the formation of ambivalent gonads, whereas exposure after the critical sensitive period of gonad differentiation has no effect (Villalpando & Merchant-Larios 1990).…”

Section: Highly Sensitive Speciesmentioning

confidence: 96%

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Differential effects of testosterone and 17β-estradiol on gonadal development in five anuran species

Piprek

Pecio²,

Kubiak³

et al. 2012

Reproduction

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Sex hormones are essential for sexual differentiation and play a key role in the development of gonads in amphibians. The goal of this study was to evaluate the influence of exogenous sex steroids, testosterone, and 17b-estradiol (E 2 ) on development of gonads in five anuran species differing in their evolutionary positions, sex determination, and mode of gonadogenesis. We found that in two closely related species of fire-bellied toad, Bombina bombina and Bombina variegata, testosterone and E 2 exposure results in sex reversal as well as intersex and undifferentiated gonads. Similarly, sex reversal was observed in Hyla arborea after exposure to male or female sex steroids. Xenopus laevis was sensitive to E 2 but only moderately to testosterone. In Bufo viridis, treatment with either sex hormone provoked a developmental delay in gonads and Bidder's organs. Therefore, susceptibility to hormonal sex reversal appeared species dependent but unrelated to genetic sex determination and the type of gonadogenesis. We also found that the onset of sex steroid exposure influences gonad differentiation and the meiotic status of the germ cells depends on their location within the gonad. Our findings reveal differential sensitivity of amphibians to testosterone and E 2 , establishing a hierarchy of sensitivity to these hormones among different anuran species.

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Section: Introductionsupporting

confidence: 83%

Section: Highly Sensitive Speciesmentioning

confidence: 96%

Differential effects of testosterone and 17β-estradiol on gonadal development in five anuran species

Piprek

Pecio²,

Kubiak³

et al. 2012

Reproduction

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show abstract

“…Moreover, similar polymorphisms in the patterns of gonadal development, with differentiated, undifferentiated and semi-differentiated types, have been described for other species of frogs (e.g. [44,45]). Extending investigations to a wider taxonomic range might provide important insights on the evolution of sex determination in amphibians.…”

Section: Discussionsupporting

confidence: 61%

Sex-chromosome differentiation and ‘sex races’ in the common frog ( Rana temporaria )

et al. 2015

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Sex-chromosome differentiation was recently shown to vary among common frog populations in Fennoscandia, suggesting a trend of increased differentiation with latitude. By rearing families from two contrasted populations (respectively, from northern and southern Sweden), we show this disparity to stem from differences in sex-determination mechanisms rather than in XY-recombination patterns. Offspring from the northern population display equal sex ratios at metamorphosis, with phenotypic sexes that correlate strongly with paternal LG 2 haplotypes (the sex chromosome); accordingly, Y haplotypes are markedly differentiated, with male-specific alleles and depressed diversity testifying to their smaller effective population size. In the southern population, by contrast, a majority of juveniles present ovaries at metamorphosis; only later in development do sex ratios return to equilibrium. Even at these later stages, phenotypic sexes correlate only mildly with paternal LG 2 haplotypes; accordingly, there are no recognizable Y haplotypes. These distinct patterns of gonadal development fit the concept of 'sex races' proposed in the 1930s, with our two populations assigned to the 'differentiated' and 'semi-differentiated' races, respectively. Our results support the suggestion that 'sex races' differ in the genetic versus epigenetic components of sex determination. Analysing populations from the 'undifferentiated race' with high-density genetic maps should help to further test this hypothesis.

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“…Endocrine disruption has generated increasing public concern because reproductive and physiological effects have been observed in both humans and wildlife, including lowered fertility (Foote, 1999; Gray et al, 1997a; Gray et al, 1997b; Wolf et al, 1999), precocious (Honma et al, 2002) or delayed puberty (Faqi et al, 1998), skewed sex ratios (Bergeron et al, 1994; Saidapur et al, 2001; Willingham and Crews, 1999), gonadal abnormalities (Cook et al, 2003; Roos et al, 2001), and population decline (Cook et al, 2003; Roos et al, 2001). Laboratory studies indicate that long-term exposure to endocrine disrupting chemicals (EDCs) results in an overall desensitization through several different mechanisms, such as transcriptional or post-translational downregulation of receptors (Saceda et al, 1988), a change in steroid clearance rates (Edmunds et al, 1990; Loukovaara et al, 1995; Toscano et al, 1992), and/or an increase or decrease in co-activators and repressors (reviewed in (Shibata et al, 1997)).…”

Section: Introductionmentioning

confidence: 99%

Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific

et al. 2010

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Epidemiological, ecological, and laboratory-based studies support the hypothesis that endocrine disrupting chemicals (EDCs) in the environment are responsible for developmental and reproductive abnormalities. We have previously described a killifish population resident in a highly polluted Superfund site (New Bedford Harbor, NBH) that shows evidence of exposure to an estrogenic environment and endocrine disruption. Here, we compare NBH with a local reference population (Scorton Creek, SC) for developmental patterns and direct effects of exogenous estradiol on the estrogenic markers, brain cytochrome P450 aromatase (CYP19A2 or AroB), hepatic vitellogenin (Vtg), and hepatic estrogen receptor alpha (ERα). In contrast to our previous observation of elevated ERα in NBH embryos, developmental levels of AroB and Vtg mRNAs did not differ between the two sites, demonstrating that not all estrogen-responsive genes are upregulated in NBH embryos. A dose-response experiment showed that NBH larvae are less responsive (lower maximum induction, as measured by ERα) and less sensitive (higher EC50 for induction, as measured by AroB) to estradiol than SC larvae, changes that would be adaptive in an estrogenic environment. In contrast, induction of Vtg mRNA is similar in the two populations, indicating that the adaptive mechanism is target gene-specific. Based on the lower basal levels of ERα mRNA in several tissues from adult NBH fish vs SC fish (Greytak and Callard, 2007), we predicted estrogen hyporesponsiveness; however, induction of ERα by estradiol exposure in reproductively inactive males did not differ between the two sites. Moreover, AroB was more responsive and Vtg induction was greater (2d) or similar (5d) in NBH as compared to SC males. Worth noting is the high inter-individual variability in estrogen responses of gene targets, especially in NBH killifish, which may indicate evolving preadaptive or adaptive mechanisms. In conclusion, although multi-generational exposure to a highly polluted environment is associated with changes in basal levels of ERα mRNA, this is not a simple predictor of estrogen responsiveness. We hypothesize that adaptation of killifish to the estrogenic and polluted environment may be occurring through diverse mechanisms that are gene-, tissue type- and life-stage specific.

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Effect of Sex Steroids on Gonadal Differentiation and Sex Reversal in the Frog, Rana curtipes

Cited by 33 publications

References 24 publications

Differential effects of testosterone and 17β-estradiol on gonadal development in five anuran species

Differential effects of testosterone and 17β-estradiol on gonadal development in five anuran species

Sex-chromosome differentiation and ‘sex races’ in the common frog ( Rana temporaria )

Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific

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