Loss of Gsdf leads to a dysregulation of Igf2bp3-mediated oocyte development in medaka

Wu, Xiaowen; Zhang, Yingqing; Xu, Sihua; Chang, Yuyang; Yang, Yong; Guo, Anning; Yi, Kang; Guo, Haiyan; Xu, Hongyan; Chen, Liangbiao; Zhao, Xiaomiao; Guan, Guijun

doi:10.1016/j.ygcen.2019.04.001

Cited by 16 publications

(17 citation statements)

References 28 publications

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“…Germ cells have a feminizing effect, which has been demonstrated by a series of XX mutants in different stages of gametogenesis (15), indicating that the identity of an XX germ cell is distinct from that of an XY germ cell. We have reported that two kinds of germ cells, those with positive or negative expression of Igf2bp3 and H3K27me3, were located in the same cyst of a gsdf KO XY ovary in the early pachytene stage of meiosis I, but not in normal XX ovaries or normal XY testes (16). These results suggest that XY germ cells may have become heterogeneous in response to a Gsdf signal due to incomplete mitotic division.…”

Section: Introductionmentioning

confidence: 93%

“…Mature gonads of wild-type XX females, XY males, gsdf-deficient XY females and Sissy intersex were pooled as a single biologic sample per group to minimize the the influence of individual variants. Label-free proteomic analysis was performed in biologic triplicate described previously (16). Briefly, enzyme specificity was set as trypsin whereas a maximum of 2 missed cleavages were allowed.…”

Section: Label-free Proteomic Analysismentioning

confidence: 99%

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A Potential Role for the Gsdf–eEF1α Complex in Inhibiting Germ Cell Proliferation: A Protein-Interaction Analysis in Medaka (Oryzias latipes) From a Proteomics Perspective

Zhang

Chang

Zhai

et al. 2021

Molecular & Cellular Proteomics

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Gonadal soma–derived factor ( gsdf ) has been demonstrated to be essential for testicular differentiation in medaka ( Oryzias latipes ). To understand the protein dynamics of Gsdf in spermatogenesis regulation, we used a His-tag “pull-down” assay coupled with shotgun LC-MS/MS to identify a group of potential interacting partners for Gsdf, which included cytoplasmic dynein light chain 2, eukaryotic polypeptide elongation factor 1 alpha (eEF1α), and actin filaments in the mature medaka testis. As for the interaction with transforming growth factor β–dynein being critical for spermatogonial division in Drosophila melanogaster , the physical interactions of Gsdf–dynein and Gsdf–eEF1α were identified through a yeast 2-hybrid screening of an adult testis cDNA library using Gsdf as bait, which were verified by a paired yeast 2-hybrid assay. Coimmunoprecipitation of Gsdf and eEF1α was defined in adult testes as supporting the requirement of a Gsdf and eEF1α interaction in testis development. Proteomics analysis (data are available via ProteomeXchange with identifier PXD022153) and ultrastructural observations showed that Gsdf deficiency activated eEF1α-mediated protein synthesis and ribosomal biogenesis, which in turn led to the differentiation of undifferentiated germ cells. Thus, our results provide a framework and new insight into the coordination of a Gsdf (transforming growth factor β) and eEF1α complex in the basic processes of germ cell proliferation, transcriptional and translational control of sexual RNA, which may be fundamentally conserved across the phyla during sexual differentiation.

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Section: Introductionmentioning

confidence: 93%

Section: Label-free Proteomic Analysismentioning

confidence: 99%

A Potential Role for the Gsdf–eEF1α Complex in Inhibiting Germ Cell Proliferation: A Protein-Interaction Analysis in Medaka (Oryzias latipes) From a Proteomics Perspective

Zhang

Chang

Zhai

et al. 2021

Molecular & Cellular Proteomics

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“…In zebrafish, Gsdf may have a role in regulating ovarian follicle maturation and expression of genes involved in steroid biosynthesis, obesity, diabetes, and female fertility [57]. Lack of Gsdf in medaka has been linked to a dysregulation of oocyte development [58]. In coho salmon (Oncorhynchus kisutch) ovarian tissue, gsdf transcript levels are significantly increased during early secondary growth.…”

Section: Gsdfmentioning

confidence: 99%

Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon

et al. 2020

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Background: Sustainability challenges are currently hampering an increase in salmon production. Using sterile salmon can solve problems with precocious puberty and genetic introgression from farmed escapees to wild populations. Recently sterile salmon was produced by knocking out the germ cell-specific dead end (dnd). Several approaches may be applied to inhibit Dnd function, including gene knockout, knockdown or immunization. Since it is challenging to develop a successful treatment against a gene product already existing in the body, alternative targets are being explored. Germ cells are surrounded by, and dependent on, gonadal somatic cells. Targeting genes essential for the survival of gonadal somatic cells may be good alternative targets for sterility treatments. Our aim was to identify and characterize novel germ cell and gonadal somatic factors in Atlantic salmon. Results: We have for the first time analysed RNA-sequencing data from germ cell-free (GCF)/dnd knockout and wild type (WT) salmon testis and searched for genes preferentially expressed in either germ cells or gonadal somatic cells. To exclude genes with extra-gonadal expression, our dataset was merged with available multi-tissue transcriptome data. We identified 389 gonad specific genes, of which 194 were preferentially expressed within germ cells, and 11 were confined to gonadal somatic cells. Interestingly, 5 of the 11 gonadal somatic transcripts represented genes encoding secreted TGF-β factors; gsdf, inha, nodal and two bmp6-like genes, all representative vaccine targets. Of these, gsdf and inha had the highest transcript levels. Expression of gsdf and inha was further confirmed to be gonad specific, and their spatial expression was restricted to granulosa and Sertoli cells of the ovary and testis, respectively. Finally, we show that inha expression increases with puberty in both ovary and testis tissue, while gsdf expression does not change or decreases during puberty in ovary and testis tissue, respectively. Conclusions: This study contributes with transcriptome data on salmon testis tissue with and without germ cells. We provide a list of novel and known germ cell-and gonad somatic specific transcripts, and show that the expression of two highly active gonadal somatic secreted TGF-β factors, gsdf and inha, are located within granulosa and Sertoli cells.

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“…Likewise, expression of gsdf in the same cell types has been observed in several fish species including rainbow trout (Oncorhynchus mykiss), medaka In zebrafish, Gsdf may have a role in regulating ovarian follicle maturation and expression of genes involved in steroid biosynthesis, obesity, diabetes, and female fertility [57]. Lack of Gsdf in medaka has been linked to a dysregulation of oocyte development [58]. In coho salmon (Oncorhynchus kisutch) ovarian tissue, gsdf transcript levels are significantly increased during early secondary growth.…”

Section: Gsdfmentioning

confidence: 96%

Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon

Kleppe

Edvardsen

Furmanek

et al. 2020

Preprint

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Background Sustainability challenges are currently hampering an increase in salmon production. Using sterile salmon can solve problems with precocious puberty and genetic introgression from farmed escapees to wild populations. Recently sterile salmon was produced by knocking out the germ cell-specific dead end (dnd). Several approaches may be applied to inhibit Dnd function, including gene knockout, knockdown or immunization. Since it is challenging to develop a successful treatment against a gene product already existing in the body, alternative targets are being explored. Germ cells are surrounded by, and dependent on, gonadal somatic cells. Targeting genes essential for the survival of gonadal somatic cells may be good alternative targets for sterility treatments. Our aim was to identify and characterize novel germ cell and gonadal somatic factors in Atlantic salmon.Results We have for the first time analysed RNA-sequencing data from germ cell-free (GCF)/dnd knockout and wild type (WT) salmon testis and searched for genes preferentially expressed in either germ cells or gonadal somatic cells. To exclude genes with extra-gonadal expression, our dataset was merged with available multi-tissue transcriptome data. We identified 389 gonad specific genes, of which 194 were preferentially expressed within germ cells, and 11 were confined to gonadal somatic cells. Interestingly, 5 of the 11 gonadal somatic transcripts represented genes encoding secreted TGF-β factors; gsdf, inha, nodal and two bmp6-like genes, all representative vaccine targets. Of these, gsdf and inha had the highest transcript levels. Expression of gsdf and inha was further confirmed to be gonad specific, and their spatial expression was restricted to granulosa and Sertoli cells of the ovary and testis, respectively. Finally, we show that inha expression increases with puberty in both ovary and testis tissue, while gsdf expression does not change or decreases during puberty in ovary and testis tissue, respectively.Conclusions This study contributes with transcriptome data on salmon testis tissue with and without germ cells. We provide a list of novel and known germ cell- and gonad somatic specific transcripts, and show that the expression of two highly active gonadal somatic secreted TGF-β factors, gsdf and inha, are located within granulosa and Sertoli cells.

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Loss of Gsdf leads to a dysregulation of Igf2bp3-mediated oocyte development in medaka

Cited by 16 publications

References 28 publications

A Potential Role for the Gsdf–eEF1α Complex in Inhibiting Germ Cell Proliferation: A Protein-Interaction Analysis in Medaka (Oryzias latipes) From a Proteomics Perspective

A Potential Role for the Gsdf–eEF1α Complex in Inhibiting Germ Cell Proliferation: A Protein-Interaction Analysis in Medaka (Oryzias latipes) From a Proteomics Perspective

Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon

Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon

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