Structural changes in gonadal basement membranes during sex differentiation in the frog <i>Rana rugosa</i>

Saotome, Kazuhiro; Isomura, Tomoko; Seki, Tatsunori; Nakamura, Yoriko; Nakamura, Masahisa

doi:10.1002/jez.607

Cited by 18 publications

(34 citation statements)

References 45 publications

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“…The presence of basal laminae enclosing the ovarian follicles was observed in all studied anurans (e.g. Falconi et al, 2004; reviewed in Ogielska and Bartmanska, 2009;Piprek et al, 2010;Saotome et al, 2010).…”

Section: Development Of the Ovarymentioning

confidence: 91%

“…In G. rugosa there is no significant difference in somatic cell number between testes and ovaries at the early phase of sexual differentiation (Saotome et al, 2010). Thus, it is not clear if a cell number increase in testis differentiation is a common mechanism for all vertebrates.…”

Section: Sex-specific Pattern Of Cell Proliferation and Migrationmentioning

confidence: 96%

“…The germ cells were always enclosed by the coelomic-epithelium-derived cells (pre-Sertoli and pre-follicular cells that differentiate into supporting cells), and they never contacted the stroma or the basal lamina. The developing gonads of all studied anuran species contain stroma between cortex and medulla (Falconi et al, 2004;Piprek et al, 2010;Saotome et al, 2010;reviewed in Ogielska, 2009). …”

Section: Stroma Appearance In the Undifferentiated Gonadsmentioning

confidence: 97%

“…In amphibians, the development of gonads has been extensively studied at the light microscopy level (Falconi et al, 2004;Piprek et al, 2010;Saotome et al, 2010;Iwasawa, 1988, 1989;Witschi, 1929). The structure of developing amphibian gonads deviates from that of amniotes, and it is unknown whether the mechanisms responsible for testis and ovary development in amphibians and amniotes are similar.…”

Section: Introductionmentioning

confidence: 99%

“…nigromaculuarus and Glandirana rugosa (Saotome et al, 2010;Tanimura and Iwasawa, 1991). Many studies were focused on the gene expression in developing gonads in G. rugosa because of its unusual mode of sex determination (Kato et al, 2004;Nakamura, 2009;Oike et al, 2016;Oike et al, 2017;Oshima et al, 2005;Yamamura et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Development of Xenopus laevis bipotential gonads into testis or ovary is driven by sex-specific cell-cell interactions, proliferation rate, cell migration and deposition of extracellular matrix

Piprek

Kloc

Tassan

et al. 2017

Developmental Biology

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. Development of Xenopus laevis bipotential gonads into testis or ovary is driven by sex-specific cell-cell interactions, proliferation rate, cell migration and deposition of extracellular matrix. Developmental Biology, Elsevier, 2017, 432 (2) AbstractInformation on the mechanisms orchestrating sexual differentiation of the bipotential gonads into testes or ovaries in amphibians is limited. The aim of this study was to investigate the development of Xenopus laevis gonad, to identify the earliest signs of sexual differentiation, and to describe mechanisms driving these processes. We used light and electron microscopy, immunofluorescence and cell tracing. In order to identify the earliest signs of sexual differentiation the sex of each tadpole was determined using genotyping with the sex markers. Our analysis revealed a series of events participating in the gonadal development, including cell proliferation, migration, cell adhesion, stroma penetration, and basal lamina formation. We found that during the period of sexual differentiation the sites of intensive cell proliferation and migration differ between male and female gonads. In the differentiating ovaries the germ cells remain associated with the gonadal surface epithelium (cortex) and a sterile medulla forms in the ovarian centre, whereas in the differentiating testes the germ cells detach from the surface epithelium, disperse, and the cortex and medulla fuse.Cell junctions that are more abundant in the ovarian cortex possibly can favor the persistence of germ cells in the cortex. Also the stroma penetrates the female and male gonads differently.These finding indicate that the crosstalk between the stroma and the coelomic epitheliumderived cells is crucial for development of male and female gonad.

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Section: Development Of the Ovarymentioning

confidence: 91%

Section: Sex-specific Pattern Of Cell Proliferation and Migrationmentioning

confidence: 96%

Section: Stroma Appearance In the Undifferentiated Gonadsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Development of Xenopus laevis bipotential gonads into testis or ovary is driven by sex-specific cell-cell interactions, proliferation rate, cell migration and deposition of extracellular matrix

Piprek

Kloc

Tassan

et al. 2017

Developmental Biology

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Molecular cloning and characterization of oocyte-specific Pat1a inRana rugosafrogs

et al. 2015

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The Pat1 gene is expressed in the immature oocytes of Xenopus, and is reportedly involved in regulating the translation of maternal mRNAs required for oocyte-maturation. However, it is still unknown when Pat1a first appears in the differentiating ovary of amphibians. To address this issue, we isolated the full-length Pat1a cDNA from the frog Rana rugosa and examined its expression in the differentiating ovary of this frog. Among eight different tissues examined, the Pat1a mRNA was detectable in only the ovary. When frozen sections from the ovaries of tadpoles at various stages of development were immunostained for Vasa-a germ cell-specific protein-and Pat1a, Vasa-immunopositive signals were observed in all of the germ cells, whereas Pat1a signals were confined to the growing oocytes (50-200 μm in diameter), and absent from small germ cells (<50 μm in diameter). Forty days after testosterone injection into tadpoles to induce female-to-male sex-reversal, Pat1a-immunoreactive oocytes had disappeared completely from the sex-reversed gonad, but Vasa-positive small germ cells persisted. Thus, Pat1a would be a good marker for identifying the sexual status of the sex-reversing gonad in amphibians. In addition, fluorescence in situ hybridization analysis showed Pat1a to have an autosomal locus, suggesting that Pat1a transcription is probably regulated by a tissue-specific transcription factor in R. rugosa.

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Structural changes in female‐to‐male sex‐reversing gonads of Rana RUGOSA

et al. 2016

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The phenotypic sex of many species of amphibians is subject to reversal by steroid hormones. The mechanism of this process, however, still remains largely unknown. As a step toward understanding the histological changes during sex reversal in amphibians, we analyzed two- and three-dimensional (2D and 3D) structures of sex-reversing gonads in Rana rugosa frogs. 2D views revealed that many oocytes in the wild-type ovary disappeared during female-to-male sex-reversal concomitant with the emergence of Vasa-positive small germ cells. Some of the germ cells were labeled with BrdU. BrdU-positive germ cells were few in the testosterone (T) treated ovaries at days 8 and 16, which resembled wild-type ovaries. Basement membranes became disrupted by day 24 in T-treated ovaries. However, the membranes were later reconfigured into testis-like gonadal structures 40 days after T treatment. 3D imaging of the sex-reversing gonad using serial immunostained sections showed that germ cells were organized in linear fashion extending out from where the sex-reversing gonad attached to the mesorchium 24 days after T treatment. Germ cells were increased in number by 40 days and were localized to the cortex of the gonads. In a T-untreated testis at day 24, many germ cells were distributed throughout the cortex except in the central space, while the efferent duct ran between two sheets of the mesorchium. These results, taken together, suggest that the mesorchium plays an important role in the organization of testicular structure. This is the first report showing germ cell ontogeny and organization in the female-to-male sex-reversing gonad in a vertebrate species.

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Structural changes in gonadal basement membranes during sex differentiation in the frog Rana rugosa

Cited by 18 publications

References 45 publications

Development of Xenopus laevis bipotential gonads into testis or ovary is driven by sex-specific cell-cell interactions, proliferation rate, cell migration and deposition of extracellular matrix

Development of Xenopus laevis bipotential gonads into testis or ovary is driven by sex-specific cell-cell interactions, proliferation rate, cell migration and deposition of extracellular matrix

Molecular cloning and characterization of oocyte-specific Pat1a inRana rugosafrogs

Structural changes in female‐to‐male sex‐reversing gonads of Rana RUGOSA

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