Autosomal gsdf acts as a male sex initiator in the fish medaka

Zhang, Xi; Guan, Guijun; Li, Mingyou; Zhu, Feng; Liu, Qizhi; Naruse, Kiyoshi; Herpin, Amaury; Nagahama, Yoshitaka; Li, Jiale; Hong, Yunhan

doi:10.1038/srep19738

Cited by 99 publications

(105 citation statements)

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“…In addition, in two fish (three‐spot wrasse and rice field eel) that are sequential protogynous hermaphrodites, gsdf expression is up‐regulated as ovaries transform to testes (Horiguchi et al, ; Zhu et al, ). Although gsdf is not the primary genetic sex determinant in O. latipes (Japanese medaka), forced expression of gsdf on an autosome causes XX females to become males (Zhang et al, ) and gsdf knockout causes XY O. latipes to become phenotypic females, demonstrating that gsdf is strongly male determining in this species (Imai et al, ; Zhang et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…In Japanese medaka ( Oryzias latipes ), gsdf is expressed weakly in gonads of both XX and XY embryos, then increases in males in somatic cells that express dmy/dmrt1by (Shibata et al, ). In Japanese medaka, gsdf initiates but does not maintain male fate (Imai et al, ; Zhang et al, ); in contrast, in tilapia gsdf does not initiate, but maintains dmrt1 expression and testis development (Jiang et al, ). In medaka, dmrt1by activates gsdf (Zhang et al, ) and suppresses expression of rspo1 and the female pathway, and gsdf activity can rescue sex reversal caused by loss of dmrt1by (Chakraborty et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…In Japanese medaka, gsdf initiates but does not maintain male fate (Imai et al, ; Zhang et al, ); in contrast, in tilapia gsdf does not initiate, but maintains dmrt1 expression and testis development (Jiang et al, ). In medaka, dmrt1by activates gsdf (Zhang et al, ) and suppresses expression of rspo1 and the female pathway, and gsdf activity can rescue sex reversal caused by loss of dmrt1by (Chakraborty et al, ). Another Oryzias species eliminates the upstream factor ( dmrt1by ) and uses gsdf directly as a sex determinant (Myosho et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish

Yan

Desvignes

BreMiller

et al. 2017

Developmental Dynamics

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Background Aberrant signaling between germ cells and somatic cells can lead to reproductive disease and depends on diffusible signals, including TGFB-family proteins. The TGFB-family protein Gsdf (gonadal soma derived factor) controls sex determination in some fish and is a candidate for mediating germ cell/soma signaling. Results Zebrafish expressed gsdf in somatic cells of bipotential gonads and expression continued in ovarian granulosa cells and testicular Sertoli cells. Homozygous gsdf knockout mutants delayed leaving the bipotential gonad state, but then became a male or a female. Mutant females ovulated a few oocytes, then became sterile, accumulating immature follicles. Female mutants stored excess lipid and down-regulated aromatase, gata4, insulin receptor, estrogen receptor, and genes for lipid metabolism, vitellogenin, and steroid biosynthesis. Mutant females contained less estrogen and more androgen than wild types. Mutant males were fertile. Genomic analysis suggests that Gsdf, Bmp15, and Gdf9, originated as paralogs in vertebrate genome duplication events. Conclusions In zebrafish, gsdf regulates ovarian follicle maturation and expression of genes for steroid biosynthesis, obesity, diabetes, and female fertility, leading to ovarian and extra-ovarian phenotypes that mimic human polycystic ovarian syndrome (PCOS), suggesting a role for a related TGFB signaling molecule in the etiology of PCOS.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish

Yan

Desvignes

BreMiller

et al. 2017

Developmental Dynamics

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“…gsdf is a member of the TGF-β family, that is conserved and upregulated during testicular development in teleosts but is not found in mammals [36][37][38][39]. In medaka, strong expression of gsdf is observed in male gonadal somatic cells, and it co-localizes in the cells expressing DMY/dmrt1bY [37] and is one downstream target of DMY/dmrt1bY [40]. dmrt1 is a masculinizing factor conserved among animals and expressed in male gonads [1].…”

Section: By Gonadal Somatic Cellsmentioning

confidence: 98%

The Mechanism of Germline Sex Determination in Vertebrates

Nishimura

Tanaka

2016

Biology of Reproduction

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Germ cells are the common cells of origin for the two different types of gametes, sperm and eggs. In vertebrates so far examined, the sex of germ cells is determined by gonadal somatic cells. However, influenced by the somatic cells, how germ cells adopt their sexual fates by intrinsic factors has long been unclear in vertebrates. We recently identified forkhead box L3 (FOXL3) as a germ cell-intrinsic factor involved in the sperm-egg fate decision in the teleost fish medaka (Oryzias latipes). On the basis of the results obtained by the analysis of foxl3/FOXL3 expression and loss-of-function mutants, we review when and how germ cell sex is regulated non-cell-autonomously and cell-autonomously. We then discuss the fact that the germline sex determination pathway is genetically distinct from other essential gametogenic pathways such as meiotic entry and the establishment of germline stem cells. Another extraordinary finding in the foxl3 mutant is that functional sperm can be produced in the ovary, which provides a new notion that gametogenesis can proceed regardless of the sex of the surrounding somatic cells once the sexual identity of germ cells is established in medaka.

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“…They are liable to sex exchange in response to environmental elements, such as temperature, sex hormones, or chemical contaminants, even their sex is largely determined genetically(Bachtrog et al, 2014). In medaka ( Oryzias latipes ), male sex is determined under the influence of d oublesex- m ab3 domain gene on Y chromosome ( dmy gene) (Matsuda et al, 2002), but can be turnover by targeted disruption of other genes such as gonadal soma-derived factor ( gsdf ) which is important for testis development(Imai et al, 2015; Zhang et al, 2016). Medaka sex can also be artificially altered by steroid hormones, or by manipulating the number of germ cells (Nagahama et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

A compromised gsdf signaling leads to gamatogenesis confusion and subfertility in medaka

Guan

Guo

et al. 2018

Preprint

Self Cite

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Summary statementGsdf signals trigger the gamatogenesis, alter the somatic expression of Fsh/Lh receptors and brain type aromatase in medaka brain and gonad.AbstractGonadal soma-derived factor (gsdf) and anti-Mullerian hormone (amh) are somatic male determinants in several species of teleosts, although the mechanisms by which they trigger the indifferent germ cells into the male pathway remain unknown. This study aimed to decipher the roles of gsdf/amh in directing the sexual fate of germ cells using medaka as a model. Transgenic lines (TgcryG) that restrictively and persistently express a Gsdf-Gfp fusion protein in the lens and the hypothalamus-pituitary-gonad (HPG) axis, were generated under the control of a mouse γF-crystallin promoter. A high frequency (44.4%) of XX male sex reversals was obtained in TgcryG lines, indicating that signals of gsdf-expressing cells in HPG were enough for the spermatogenesis activation in the genetic females. Furthermore, all TgcryG XY individuals with endogenous gsdf depletion (named Sissy) displayed intersex (100%) with enlarged ovotestis in contrast to a giant ovary developed in XY gsdf deficiency. The heterogeneous expression of gsdf led to the confusion of gamatogenesis and ovotestis development, similar to some hotei (amhr2) mutants, suggests that the signaling balance of gsdf/amh is essential for proper gamatogenesis, maintaining sex steroid production and gonadotropin secretion, which are evolutionarily conserved across phyla.

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Autosomal gsdf acts as a male sex initiator in the fish medaka

Cited by 99 publications

References 65 publications

Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish

Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish

The Mechanism of Germline Sex Determination in Vertebrates

A compromised gsdf signaling leads to gamatogenesis confusion and subfertility in medaka

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