Building an Ovary: Insights into Establishment of Somatic Cell Lineages in the Mouse

Nicol, Barbara; Yao, Hisayuki

doi:10.1159/000358072

Cited by 35 publications

(23 citation statements)

References 90 publications

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“…However, the identity and similarity scores for the entire protein sequence across the four species were lower than those for the FOXL2 sequence (Table 1). FOXL2 is related to ovarian development in mammals 14 and teleosts, 15 and in chickens, foxl2 mRNA is highly expressed in female gonads in eggs incubated for 5.7 days, with the timing of expression similar to that of the aromatase gene. This finding was consistent with results from previous studies showing an absence of foxl3 in amphibians and placental mammals.…”

Section: Discussionmentioning

confidence: 99%

Comparison of sex determination mechanism of germ cells between birds and fish: Cloning and expression analyses of chicken forkhead box L3‐like gene

Ichikawa

Ezaki

Furusawa

et al. 2019

Developmental Dynamics

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Background Birds harbor specific sex determination and differentiation mechanisms. Although the molecular mechanisms associated with sex determination in somatic cells have been elucidated, those for germ cells remain unclear. Results Here, we characterized the chicken forkhead box L3 (foxl3)‐like gene as a sex‐determination factor in sexually indifferent medaka germline stem cells. The foxl3‐like gene was cloned by rapid amplification of cDNA ends, and the nucleotide sequence was analyzed. The deduced amino acid sequence was compared with FOXL3 sequences from other species, revealing low identity and similarity scores. Expression analysis of foxl3‐like mRNA during gonadogenesis showed female left‐gonad‐specific temporal expression in an egg incubated from 10 to 16 days, as well as low general expression in certain hatched female chicken organs. Moreover, the amino acid sequence deduced for the FOXL3‐like protein displayed low identity with medaka FOXL3, with the FOXL3‐like protein specifically localized in the oogonia, whereas medaka FOXL3 was found in sexually indifferent germline stem cells. Furthermore, the timing of expression differed between the foxl3‐like gene and that of medaka foxl3. Conclusions These results suggest that chicken FOXL3‐like protein and medaka FOXL3 differ in terms of their functions as female sex‐determination factors.

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Section: Discussionmentioning

confidence: 99%

Comparison of sex determination mechanism of germ cells between birds and fish: Cloning and expression analyses of chicken forkhead box L3‐like gene

Ichikawa

Ezaki

Furusawa

et al. 2019

Developmental Dynamics

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“…In the absence of the Y chromosome (XX genetic background) or Sry gene (XY genetic background with Sry mutations), the supporting cell linages of the bipotential gonad commit to the ovary-specific granulosa cell fate (for a review, see [13]). In XX mouse embryos, global loss of Wnt4 [14,15], Rspo1 [16,17], or targeted loss of their downstream effector bcatenin in the somatic cells of the fetal gonad [18,19] results in a partial ovary-to-testis sex-reversal characterized by the presence of a testis-specific coelomic vessel and steroidogenic cells.…”

Section: Introductionmentioning

confidence: 99%

Gonadal Identity in the Absence of Pro-Testis Factor SOX9 and Pro-Ovary Factor Beta-Catenin in Mice1

Nicol

Yao

2015

Biology of Reproduction

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Sex-reversal cases in humans and genetic models in mice have revealed that the fate of the bipotential gonad hinges upon the balance between pro-testis SOX9 and pro-ovary beta-catenin pathways. Our central query was: if SOX9 and beta-catenin define the gonad's identity, then what do the gonads become when both factors are absent? To answer this question, we developed mouse models that lack either Sox9, beta-catenin, or both in the somatic cells of the fetal gonads and examined the morphological outcomes and transcriptome profiles. In the absence of Sox9 and beta-catenin, both XX and XY gonads progressively lean toward the testis fate, indicating that expression of certain pro-testis genes requires the repression of the beta-catenin pathway, rather than a direct activation by SOX9. We also observed that XY double knockout gonads were more masculinized than their XX counterpart. To identify the genes responsible for the initial events of masculinization and to determine how the genetic context (XX vs. XY) affects this process, we compared the transcriptomes of Sox9/beta-catenin mutant gonads and found that early molecular changes underlying the XY-specific masculinization involve the expression of Sry and 21 SRY direct target genes, such as Sox8 and Cyp26b1. These results imply that when both Sox9 and beta-catenin are absent, Sry is capable of activating other pro-testis genes and drive testis differentiation. Our findings not only provide insight into the mechanism of sex determination, but also identify candidate genes that are potentially involved in disorders of sex development.

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“…Among all these genes, Foxl2 has attracted particular attention during the last 15 years as a key player due to its involvement in sex differentiation and oogenesis [Baron et al, 2005;Benayoun et al, 2009;Veitia, 2010;Boulanger et al, 2014;Georges et al, 2014a;Nicol and Yao, 2014]. A substantial amount of information on FOXL2 action was initially acquired from studies in humans and other mammals, and many excellent reviews have already been published, most centered on the roles of FOXL2 in normal or pathological female development in mammals and/or vertebrates [Fuhrer, 2002;Baron et al, 2005;De Baere et al, 2005;Benayoun et al, 2009Benayoun et al, , 2010Beysen et al, 2009;Kobel et al, 2009;Pisarska et al, 2011;Uhlenhaut and Treier, 2011;Biason-Lauber, 2012;Caburet et al, 2012;Verdin and De Baere, 2012;Takahashi et al, 2013;Georges et al, 2014a;Rosario et al, 2014;Leung et al, 2016].…”

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confidence: 99%

Foxl2 and Its Relatives Are Evolutionary Conserved Players in Gonadal Sex Differentiation

Bertho

Pasquier

Pan

et al. 2016

Sex Dev

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Foxl2 is a member of the large family of Forkhead Box (Fox) domain transcription factors. It emerged during the last 15 years as a key player in ovarian differentiation and oogenesis in vertebrates and especially mammals. This review focuses on Foxl2 genes in light of recent findings on their evolution, expression, and implication in sex differentiation in animals in general. Homologs of Foxl2 and its paralog Foxl3 are found in all metazoans, but their gene evolution is complex, with multiple gains and losses following successive whole genome duplication events in vertebrates. This review aims to decipher the evolutionary forces that drove Foxl2/3 gene specialization through sub- and neo-functionalization during evolution. Expression data in metazoans suggests that Foxl2/3 progressively acquired a role in both somatic and germ cell gonad differentiation and that a certain degree of sub-functionalization occurred after its duplication in vertebrates. This generated a scenario where Foxl2 is predominantly expressed in ovarian somatic cells and Foxl3 in male germ cells. To support this hypothesis, we provide original results showing that in the pea aphid (insects) foxl2/3 is predominantly expressed in sexual females and showing that in bovine ovaries FOXL2 is specifically expressed in granulosa cells. Overall, current results suggest that Foxl2 and Foxl3 are evolutionarily conserved players involved in somatic and germinal differentiation of gonadal sex.

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Building an Ovary: Insights into Establishment of Somatic Cell Lineages in the Mouse

Cited by 35 publications

References 90 publications

Comparison of sex determination mechanism of germ cells between birds and fish: Cloning and expression analyses of chicken forkhead box L3‐like gene

Comparison of sex determination mechanism of germ cells between birds and fish: Cloning and expression analyses of chicken forkhead box L3‐like gene

Gonadal Identity in the Absence of Pro-Testis Factor SOX9 and Pro-Ovary Factor Beta-Catenin in Mice1

Foxl2 and Its Relatives Are Evolutionary Conserved Players in Gonadal Sex Differentiation

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