Estrogen oversees the maintenance of the female genetic program in terminally differentiated gonochorists

Paul‐Prasanth, Bindhu; Bhandari, Ramji Kumar; Kobayashi, Tohru; Horiguchi, Ryo; Kobayashi, Yasuhisa; Nakamoto, Masatoshi; Shibata, Yasushi; Sakai, Fumie; Nakamura, Masaru; Nagahama, Yoshitaka

doi:10.1038/srep02862

Cited by 93 publications

(61 citation statements)

References 34 publications

(48 reference statements)

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“…It has been recently discovered that mature adult ovaries can be transdifferentiated into functional testes in several teleosts, including medaka [Paul-Prasanth et al, 2013], tilapia [Sun et al, 2014], and zebrafish [Takatsu et al, 2013] by inhibiting estrogen production. Testicular tissues have been suggested to originate from the germinal epithelium of ovaries [Paul-Prasanth et al, 2013], supporting the notion that the testis is an expanded version of the germinal epithelium within which spermatogenesis occurs in an organized manner. In this context, the common unit may also play an important role in the sex reversal process of natural hermaphroditic fish.…”

Section: Resultsmentioning

confidence: 99%

A Structurally and Functionally Common Unit in Testes and Ovaries of Medaka (Oryzias latipes), a Teleost Fish

Nishimura

Nakamura

Tanaka³

2016

Sex Dev

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Testes and ovaries are structurally and functionally different organs, but they originate from the same gonadal primordium. Here, we propose how a tissue composed of germ cells and sox9b-expressing cells underlain by a basement membrane develops a functionally common unit that reserves sexually indifferent or unfixed germline stem cells in both the ovaries and testes of adult medaka. During testicular development, the unit expands and gives rise to lobules where germline stem cells continuously produce a tremendous amount of sperm, while the unit in the female becomes germinal cradles that represent niche areas for neo-oogenesis. A recent finding in female foxl3 mutants demonstrates that the unit can also serve as the niche for germline stem cells continuously producing sperm in the ovary. We hypothesize that this unit in medaka might correspond to the medullary cords of the gonadal primordium in amniotes and that fragmentation of the medullary cords during ovarian development may be related to the absence of germline stem cells.

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Section: Resultsmentioning

confidence: 99%

A Structurally and Functionally Common Unit in Testes and Ovaries of Medaka (Oryzias latipes), a Teleost Fish

Nishimura

Nakamura

Tanaka³

2016

Sex Dev

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“…Repression of aromatase expression and decrease of estrogen level were also observed in female to male sex reversal induced by high rearing temperatures (D'Cotta et al 2001). Long-term treatment of aromatase inhibitor Fadrozole even induced secondary sex reversal of the differentiated ovary into functional testis (Paul-Prasanth et al 2013. However, it is unclear whether sex will still be determined by estrogen if the animals were exposed to an environment with both estrogens and androgens.…”

Section: Discussionmentioning

confidence: 99%

Simultaneous exposure to estrogen and androgen resulted in feminization and endocrine disruption

Chen¹,

Jiang²,

Feng³

et al. 2016

Journal of Endocrinology

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Estrogen, which is synthesized earlier in females than androgen in males, is critical for sex determination in non-mammalian vertebrates. However, it remains unknown that what would happen to the gonadal phenotype if estrogen and androgen were administrated simultaneously. In this study, XY and XX tilapia fry were treated with the same dose of 17a-methyltestosterone (MT) and 17b-estradiol (E 2 ) alone and in combination from 0 to 30 days after hatching. Treatment of XY fish with E 2 resulted in male to female sex reversal, while treatment of XX fish with MT resulted in female to male sex reversal. In contrast, simultaneous treatment of XX and XY fish with MT and E 2 resulted in female, but with cyp11b2 and cyp19a1a co-expressed in the ovary. Serum 11-ketotestosteron level of the MT and E 2 simultaneously treated XX and XY female was similar to that of the XY control, while serum E 2 level of these two groups was similar to that of the XX control. Transcriptomic cluster analysis revealed that the MT and E 2 treated XX and XY gonads clustered into the same branch with the XX control. However a small fraction of genes, which showed disordered expression, may be associated with stress response. These results demonstrated that estrogen could maintain the female phenotype of XX fish and feminize XY fish even in the presence of androgen. Simultaneous treatment with estrogen and androgen up-regulated the endogenous estrogen and androgen synthesis, and resulted in disordered gene expression and endocrine disruption in tilapia.

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“…Sex as a threshold phenotype based on a sex-determining network More and more data reveal that, especially in teleost fishes, sex seems to be a rather plastic phenotype with natural and inducible sex reversal even after the genetic fixation of one sex at fertilization (Paul-Prasanth et al 2013). These results thus question the scenario of a stepwise, hierarchical cascade with a fixed outcome.…”

Section: Classic View On Sexual Developmentmentioning

confidence: 99%

Genetics of Sexual Development: An Evolutionary Playground for Fish

2014

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Teleost fishes are the most species-rich clade of vertebrates and feature an overwhelming diversity of sex-determining mechanisms, classically grouped into environmental and genetic systems. Here, we review the recent findings in the field of sex determination in fish. In the past few years, several new master regulators of sex determination and other factors involved in sexual development have been discovered in teleosts. These data point toward a greater genetic plasticity in generating the male and female sex than previously appreciated and implicate novel gene pathways in the initial regulation of the sexual fate. Overall, it seems that sex determination in fish does not resort to a single genetic cascade but is rather regulated along a continuum of environmental and heritable factors.

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Estrogen oversees the maintenance of the female genetic program in terminally differentiated gonochorists

Cited by 93 publications

References 34 publications

A Structurally and Functionally Common Unit in Testes and Ovaries of Medaka <b><i>(Oryzias latipes)</i></b>, a Teleost Fish

A Structurally and Functionally Common Unit in Testes and Ovaries of Medaka <b><i>(Oryzias latipes)</i></b>, a Teleost Fish

Simultaneous exposure to estrogen and androgen resulted in feminization and endocrine disruption

Genetics of Sexual Development: An Evolutionary Playground for Fish

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