Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish

Yan, Yi‐Lin; Desvignes, Thomas; BreMiller, Ruth A.; Wilson, Catherine; Dillon, Danielle; High, Samantha K.; Draper, Bruce W.; Buck, C. Loren; Postlethwait, John H.

doi:10.1002/dvdy.24579

Cited by 78 publications

(76 citation statements)

References 191 publications

(266 reference statements)

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“…It is known that targeted disruption of gsdf in medaka causes abnormal folliculogenesis associated with sterility [56]. 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].…”

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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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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“…We show here that this phenotype correlates with multiple and ectopic Taz expressing MCs. The study of the tight communication established between the oocyte and FCs during the zebrafish folliculogenesis have shed lights into the underlying mechanism regulating oocyte development progression and survival (Li and Ge, 2011;Yan et al, 2017). However, the identification of reciprocal signaling exchange governing micropyle biogenesis has not been reported yet.…”

Section: Taz Functions As a Major Regulator Of The Micropylar Cell Fatementioning

confidence: 99%

The Hippo pathway effector Taz is required for cell fate specification and fertilization in zebrafish

Dingare

Niedzwetzki

Klemmt

et al. 2018

Preprint

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In the last decade, Hippo signaling has emerged as a critical pathway integrating extrinsic and intrinsic mechanical cues to regulate cell proliferation and survival, tissue morphology and organ size in vivo. Despite its essential role in organogenesis, surprisingly much less is known about how it connects biomechanical signals to control of cell fate and cell size during development. Here we unravel a novel and unexpected role of the Hippo pathway effector Taz (wwtr1) in the control of cell size and cell fate specification. In teleosts, fertilization occurs through a specific structure at the animal pole, called the micropyle. This opening in the chorion is formed during oogenesis by a specialized somatic follicle cell, the micropylar cell (MC). The MC has a peculiar shape and is much larger than its neighboring follicle cells but the mechanisms underlying its specification and cell shape acquisition are not known.Here we show that Taz is essential for the specification of the MC and subsequent micropyle formation in zebrafish. We identify Taz as the first bona fide MC marker and show that Taz is specifically and strongly enriched in the MC precursor before the cell can be identified morphologically. Altogether, our genetic data and molecular characterization of the MC lead us to propose that Taz is a key regulator of the MC fate activated by physical cues emanating from the oocyte to initiate the MC morphogenetic program. We describe here for the first time the mechanism underlying the specification of the MC fate. Abstract word count: 248 words Main text word count: 8639 words Bally-Cuif, L., Schatz, W. J. and Ho, R. K. (1998). Characterization of the zebrafish Orb/CPEB-related RNA binding protein and localization of maternal components in the zebrafish oocyte. Mech Dev 77, 31-47. . Cadherin-catenin complexes during zebrafish oogenesis: heterotypic junctions between oocytes and follicle cells. Biol. Reprod. 61, 692-704. . (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39, e82. Chaigne, A., Campillo, C., Gov, N. S., Voituriez, R., Sykes, C., Verlhac, M. H. and Terret, M. E. (2015). A narrow window of cortical tension guides asymmetric spindle positioning in the mouse oocyte. Nat Commun 6, 6027.Compagnon, J., Barone, V., Rajshekar, S., Kottmeier, R., Pranjic-Ferscha, K., Behrndt, M. and Heisenberg, C.-P. (2014). The notochord breaks bilateral symmetry by controlling cell shapes in the zebrafish laterality organ. Dev Cell 31, 774-783.

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“…In this study we found that gsdf is highly expressed in females and males, with specific transcript localization in granulosa and Sertoli cells, respectively. 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].…”

Section: Gsdfmentioning

confidence: 95%

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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Gonadal soma controls ovarian follicle proliferation through Gsdf in zebrafish

Cited by 78 publications

References 191 publications

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

The Hippo pathway effector Taz is required for cell fate specification and fertilization in zebrafish

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

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