Temporal Differences in Granulosa Cell Specification in the Ovary Reflect Distinct Follicle Fates.

Mork, Lindsey; Maatouk, Danielle M.; Guo, Jin; Zhang, Pumin; McMahon, Andrew; McMahon, Jill A.; Capel, Blanche

doi:10.1093/biolreprod/87.s1.128

Cited by 72 publications

(139 citation statements)

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“…We have previously shown that FoxL2 and aromatase genes are not induced until day 3 of the shift to a female-producing temperature (Rhen et al 2007). Granulosa cells, which derive from the coelomic epithelium in other species (Sawyer et al 2002;Mork et al 2012), are critical for steroid production and normal ovary development. We detected a significant genetic correlation between CIRBP expression and sex ratio in siblings briefly exposed to 31°( Figure 3B).…”

Section: Discussionmentioning

confidence: 99%

A Novel Candidate Gene for Temperature-Dependent Sex Determination in the Common Snapping Turtle

et al. 2016

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Temperature-dependent sex determination (TSD) was described nearly 50 years ago. Researchers have since identified many genes that display differential expression at male-vs. female-producing temperatures. Yet, it is unclear whether these genes (1) are involved in sex determination per se, (2) are downstream effectors involved in differentiation of ovaries and testes, or (3) are thermo-sensitive but unrelated to gonad development. Here we present multiple lines of evidence linking CIRBP to sex determination in the snapping turtle, Chelydra serpentina. We demonstrate significant associations between a single nucleotide polymorphism (SNP) (c63A . C) in CIRBP, transcript levels in embryonic gonads during specification of gonad fate, and sex in hatchlings from a thermal regime that produces mixed sex ratios. The A allele was induced in embryos exposed to a female-producing temperature, while expression of the C allele did not differ between female-and male-producing temperatures. In accord with this pattern of temperaturedependent, allele-specific expression, AA homozygotes were more likely to develop ovaries than AC heterozygotes, which, in turn, were more likely to develop ovaries than CC homozygotes. Multiple regression using SNPs in CIRBP and adjacent loci suggests that c63A . C may be the causal variant or closely linked to it. Differences in CIRBP allele frequencies among turtles from northern Minnesota, southern Minnesota, and Texas reflect small and large-scale latitudinal differences in TSD pattern. Finally, analysis of CIRBP protein localization reveals that CIRBP is in a position to mediate temperature effects on the developing gonads. Together, these studies strongly suggest that CIRBP is involved in determining the fate of the bipotential gonad.KEYWORDS genetics of sex; cold-inducible RNA-binding protein; temperature-dependent sex determination; genetic association S EX determination in vertebrates is divided into two broad categories, either genotypic or environmental. Genotypic sex determination (GSD) occurs at fertilization and is governed by an individual's genotype. GSD species often, but not always, display morphologically distinct sex chromosomes, as observed in mammals, birds, snakes, some lizards, and some turtles. While some GSD systems are monogenic, other GSD systems involve two or more genes (Moore and Roberts 2013; Bachtrog et al. 2014). Environmental sex determination occurs when extrinsic factors influence whether an embryo develops into a female or a male. Various abiotic and biotic factors determine sex in metazoans, but temperature is the only environmental factor known to influence sex determination in amniotes (Bull 1983;Janes et al. 2010;Merchant-Larios and Díaz-Hernández 2013). This phenomenon is referred to as temperature-dependent sex determination (TSD) and is observed in many lizards, numerous turtles, and all crocodilians studied to date (Ewert et al. , 2004Lang and Andrews 1994;Viets et al. 1994;Deeming 2004;Harlow 2004). However, GSD and TSD are not as distinct as ...

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Section: Discussionmentioning

confidence: 99%

A Novel Candidate Gene for Temperature-Dependent Sex Determination in the Common Snapping Turtle

et al. 2016

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“…[16][17][18][19] However, the factors responsible for the initiation of growth remain to be determined. In a classic review, Peters et al summarized several key concepts concerning follicular development in mammals.…”

Section: Ovarian Follicular Development: Basic Conceptsmentioning

confidence: 99%

Oocyte-Somatic Cell Interactions and Ovulation Rate: Effects on Oocyte Quality and Embryo Yield

McNatty¹,

Juengel²,

Pitman³

2014

Reproductive Biology Insights

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ABSTRACT:The use of exogenous gonadotropins to increase oocyte yields for better pregnancy outcomes remains unpredictable and inefficient. The objectives of this review are to address two questions concerning this issue: (1) are there any alternatives for improving consistency in oocyte yields? (2) is it possible to develop a molecular diagnostic test for oocytes with blastocyst potential? Studies in sheep with a heterozygous inactivating mutation in the oocyte-derived growth factor, bone morphogenetic protein 15 (BMP15), report increased oocyte yields and significantly more offspring. Moreover, partial immuno-neutralization of BMP15 bioactivity increases oocyte yield without modifying gonadotropin or ovarian steroid secretion. Therefore, it is hypothesized that the development of BMP15 antagonists may prove them to be suitable alternatives to exogenous gonadotropins. Recent evidence from analyses of candidate gene expression in human cumulus cells separated from individual oocytes before IVF indicates a potential non-invasive molecular screen for oocytes with improved blastocyst and live-birth outcomes.

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“…To confirm the conclusions drawn above, we also traced oocyte development by labeling the surrounding somatic cells of all existing oocytes in the initial follicle pool with the Forkhead box L2 (Foxl2)-CreER T2 ;mT/mG mouse model (23). Foxl2 is expressed in follicular somatic cells in the mouse ovary (24) but not in the progenitors of follicular somatic cells in the ovarian epithelium (25). This makes Foxl2 a good marker for tracing the recruitment of nascent somatic cells to form follicles with any de novo-regenerated oocytes (23).…”

Section: There Is No Recruitment Of Nascent Somatic Cells To Form Folmentioning

confidence: 94%

Life-long in vivo cell-lineage tracing shows that no oogenesis originates from putative germline stem cells in adult mice

Zhang

Liu

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Whether or not oocyte regeneration occurs in adult life has been the subject of much debate. In this study, we have traced germcell lineages over the life spans of three genetically modified mouse models and provide direct evidence that oogenesis does not originate from any germline stem cells (GSCs) in adult mice. By selective ablation of all existing oocytes in a Gdf9-Cre;iDTR mouse model, we have demonstrated that no new germ cells were ever regenerated under pathological conditions. By in vivo tracing of oocytes and follicles in the Sohlh1-CreER T2 ;R26R and Foxl2-CreER T2 ;mT/mG mouse models, respectively, we have shown that the initial pool of oocytes is the only source of germ cells throughout the life span of the mice and that no adult oogenesis ever occurs under physiological conditions. Our findings clearly show that there are no GSCs that contribute to adult oogenesis in mice and that the initial pool of oocytes formed in early life is the only source of germ cells throughout the entire reproductive life span.genetically modified mouse models | oocyte tracing | follicle tracing | life-long observations | no postnatal oocyte regeneration

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Temporal Differences in Granulosa Cell Specification in the Ovary Reflect Distinct Follicle Fates.

Cited by 72 publications

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A Novel Candidate Gene for Temperature-Dependent Sex Determination in the Common Snapping Turtle

A Novel Candidate Gene for Temperature-Dependent Sex Determination in the Common Snapping Turtle

Oocyte-Somatic Cell Interactions and Ovulation Rate: Effects on Oocyte Quality and Embryo Yield

Life-long in vivo cell-lineage tracing shows that no oogenesis originates from putative germline stem cells in adult mice

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