Concerted morphogenesis of genital ridges and nephric ducts in the mouse captured through whole-embryo imaging

Bunce, Corey; McKey, Jennifer; Capel, Blanche

doi:10.1242/dev.199208

Cited by 18 publications

(18 citation statements)

References 46 publications

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“…1I). SLCs express CE-derived somatic cell markers such as Nr5a1 , Wt1 , and Gata4 , but also Pax8 , a marker of cells of the mesonephric tubules, the rete testis, and rete ovarii ( 17 , 25 ). In contrast, SLCs do not express Dmrt1 and Pax2 , a well-known marker of mesonephric tubules (Fig.…”

Section: Resultsmentioning

confidence: 99%

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

et al. 2022

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Gonadal sex determination represents a unique model for studying cell fate decisions. However, a complete understanding of the different cell lineages forming the developing testis and ovary remains elusive. Here, we investigated the origin, specification, and subsequent sex-specific differentiation of a previously uncharacterized population of supporting-like cells (SLCs) in the developing mouse gonads. The SLC lineage is closely related to the coelomic epithelium and specified as early as E10.5, making it the first somatic lineage to be specified in the bipotential gonad. SLC progenitors are localized within the genital ridge at the interface with the mesonephros and initially coexpress Wnt4 and Sox9 . SLCs become sexually dimorphic around E12.5, progressively acquire a more Sertoli- or pregranulosa-like identity and contribute to the formation of the rete testis and rete ovarii. Last, we found that WNT4 is a crucial regulator of the SLC lineage and is required for normal development of the rete testis.

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Section: Resultsmentioning

confidence: 99%

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

et al. 2022

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“…Spearman’s correlation analysis and hierarchical clustering revealed that the transcriptome of the early and late SLC populations share similarities with those of other cell types of the supporting lineage, such as granulosa, pre-supporting and Sertoli cells ( Figure 1I ). SLCs express CE-derived somatic cell markers such as Nr5a1 , Wt1 , and Gata4 , but also Pax8 , a marker of cells of the mesonephric tubules, the rete testis and rete ovarii ( 21, 29 ). In contrast, SLCs do not express Pax2, a well-known marker of mesonephric tubules ( 30 ) ( Figure 1J ).…”

Section: Resultsmentioning

confidence: 99%

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

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Perea-Gómez

et al. 2021

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Gonadal sex determination represents a unique model for studying cell fate decisions. However, a complete understanding of the different cell lineages forming the developing testis and ovary remains elusive. Here, we investigated the origin, specification and subsequent sex-specific differentiation of a previously uncharacterized population of supporting-like cells (SLC) in the developing mouse gonads. The SLC lineage is closely related to the coelomic epithelium and specified as early as E10.5, making it the first somatic lineage to be specified in the bipotential gonad. SLC progenitors are localized within the genital ridge at the interface with the mesonephros and initially co-express Wnt4 and Sox9. SLCs become sexually dimorphic around E12.5, progressively acquire a Sertoli- or granulosa-like identity and contribute to the formation of the rete testis and rete ovarii. Finally, we found that WNT4 is a crucial regulator of the SLC lineage and is required for the formation of the rete testis.

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“…To determine the optimal angles to assess ovary morphology, we first performed immunostaining of whole XX embryos at E14.5 with antibodies against FOXL2, which is expressed in pre-granulosa cells and serves as a marker of the gonadal domain, and antibodies against PAX8, which is expressed in the epithelium of the reproductive ducts and cells of the developing kidney. These samples were cleared using iDISCO and imaged with lightsheet microscopy (Bunce et al, 2021; Renier et al, 2014). We generated 3D models of the labelled structures using isosurface segmentation to provide a morphological view of the urogenital complex in situ (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…1B). A recent study combining contextual 3D images of the developing gonads in the whole embryo with quantitative morphometric analysis showed that the entire genital ridge rotates inward from E10.5 to E12.5 (Bunce et al, 2021), thus by E12.5 the gonads appear on the medial aspect of the mesonephros. Consistent with these observations, at E14.5 the reproductive ducts were located lateral to the gonads, which were oriented towards each other in the medial axis (Fig.…”

Section: S1a Movie S1)mentioning

confidence: 99%

“…Consequently, their impact on ovary morphogenesis has been overlooked. With recent advances in tissue clearing and 3D imaging technology, it is now possible to visualize structural changes at the level of the whole gonad or even the whole embryo (Bunce et al, 2021; Fiorentino et al, 2021; Soygur et al, 2021a; Soygur et al; 2021b). We recently developed a tissue-clearing method that combines CUBIC and iDISCO (McKey et al, 2020; Renier et al, 2014; Susaki et al, 2015), and optimized 3D imaging methods using lightsheet microscopy to visualize the fetal and perinatal ovary in situ , in the context of its surrounding tissues (McKey et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Integration of mouse ovary morphogenesis with developmental dynamics of the oviduct, ovarian ligaments, and rete ovarii

McKey

Bunce

et al. 2021

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The morphogenetic events that occur during fetal development of the mammalian ovary are crucial to the establishment of adult female fertility. While our knowledge of the cellular and molecular aspects of ovary development is increasing, the structural rearrangements that give rise to the cortex and medulla and the relation of other female reproductive tissues to the ovary have not been thoroughly investigated. In this study, we used tissue clearing and lightsheet microscopy to investigate the stepwise morphogenesis of the ovary. We found that the ovary transitioned from an elongated to a crescent-shaped structure, suggestive of a folding mechanism. As this occured, the ovarian surface epithelium wrapped from the ventral to the dorsal side of the ovary, forming the ovarian cortex and engulfing the dorsal face of the ovary to form the medulla. To identify the tissue mechanics that drive ovary folding, we investigated proximate tissues closely associated with the ovary including the M&uumlllerian duct, the cranial suspensory ligament, and the rete ovarii. We found that relocation of the M&uumlllerian duct to the ventral aspect of the ovary was associated with expansion of mesonephric tissue that left the ovary fully encapsulated by birth. The cranial suspensory ligament, which tethers the ovary to the body wall and to the M&uumlllerian duct may exert mechanical tension that triggers ovarian folding. Finally, we found that the rete ovarii, a previously dismissed epithelial appendage of the ovary, significantly expanded during late gestation and may act to anchor the ovary to the mesonephros, leading to integration of extrinsic components into the ovarian medulla. This detailed atlas of ovary morphogenesis reveals novel relationships among the ovary and its surrounding tissues and paves the way towards the functional investigation of the relationship between architecture and differentiation of the mammalian ovary.

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Concerted morphogenesis of genital ridges and nephric ducts in the mouse captured through whole-embryo imaging

Cited by 18 publications

References 46 publications

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

Origin, specification and differentiation of a rare supporting-like lineage in the developing mouse gonad

Integration of mouse ovary morphogenesis with developmental dynamics of the oviduct, ovarian ligaments, and rete ovarii

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