JY-1, an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle.

Laboratory of Mammalian Reproductive Biology and Genomics, and Department of Animal Science, Michigan State University, East Lansing, MI 48824, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 12/2007; 104(45):17602-7. DOI: 10.1073/pnas.0706383104
Source: PubMed

ABSTRACT Oocyte-specific gene products play a key role in regulation of fertility in mammals. Here, we describe the discovery, molecular characterization, and function of JY-1, a bovine oocyte-expressed gene shown to regulate both function of ovarian granulosa cells and early embryogenesis in cattle and characteristics of JY-1 loci in other species. The JY-1 gene encodes for a secreted protein with multiple mRNA transcripts containing an identical ORF but differing lengths of 3' UTR. JY-1 mRNA and protein are oocyte-specific and detectable throughout folliculogenesis. Recombinant JY-1 protein regulates function of follicle-stimulating hormone-treated ovarian granulosa cells, resulting in enhanced progesterone synthesis accompanied by reduced cell numbers and estradiol production. JY-1 mRNA of maternal origin is also present in early bovine embryos, temporally regulated during the window from meiotic maturation through embryonic genome activation, and is required for blastocyst development. The JY-1 gene has three exons and is located on bovine chromosome 29. JY-1-like sequences are present on syntenic chromosomes of other vertebrate species, but lack exons 1 and 2, including the protein-coding region, suggestive of species specificity in evolution and function of this oocyte-specific gene.

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    ABSTRACT: Background The sub-cortical maternal complex (SCMC), located in the subcortex of mouse oocytes and preimplantation embryos, is composed of at least four proteins encoded by maternal effect genes: OOEP, NLRP5/MATER, TLE6 and KHDC3/FILIA. The SCMC assembles during oocyte growth and was seen to be essential for murine zygote progression beyond the first embryonic cell divisions; although roles in chromatin reprogramming and embryonic genome activation were hypothesized, the full range of functions of the complex in preimplantation development remains largely unknown.ResultsHere we report the expression of the SCMC genes in ovine oocytes and pre-implantation embryos, describing for the first time its expression in a large mammalian species.We report sheep-specific patterns of expression and a relationship with the oocyte developmental potential in terms of delayed degradation of maternal SCMC transcripts in pre-implantation embryos derived from developmentally incompetent oocytes.In addition, by determining OOEP full length cDNA by Rapid Amplification of cDNA Ends (RACE) we identified two different transcript variants (OOEP1 and OOEP2), both expressed in oocytes and early embryos, but with different somatic tissue distributions. In silico translation showed that 140 aminoacid peptide OOEP1 shares an identity with orthologous proteins ranging from 95% with the bovine to 45% with mouse. Conversely, OOEP2 contains a premature termination codon, thus representing an alternative noncoding transcript and supporting the existence of aberrant splicing during ovine oogenesis.Conclusions These findings confirm the existence of the SCMC in sheep and its key role for the oocyte developmental potential, deepening our understanding on the molecular differences underlying cytoplasmic vs nuclear maturation of the oocytes.Describing differences and overlaps in transcriptome composition between model organisms advance our comprehension of the diversity/uniformity between mammalian species during early embryonic development and provide information on genes that play important regulatory roles in fertility in nonmurine models, including the human.
    BMC Developmental Biology 11/2014; 14(1). DOI:10.1186/s12861-014-0040-y · 2.75 Impact Factor
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    ABSTRACT: The oocyte is a central regulator of multiple aspects of female fertility, including ovarian follicular development and early embryogenesis. During its prolonged diplotene arrest, the oocyte is subjected to endogenous (i.e., reactive oxygen species from metabolism) and exogenous (i.e., heat stress, malnutrition) sources of damage-inducing factors, which may lead to a progressive deterioration of oocyte quality. A deficit in oocyte competence can lead not only to a failure of fertilization but also to a lower developmental rate after fertilization. Thus, an appropriate environment for growth and maturation of the oocyte, in vivo and in vitro, is critical to ensure optimal oocyte quality. The objectives of the current review are to give an overview of some maternal key factors that influence oocyte quality in cattle and describe some of the findings to date in the hope of obtaining competent oocytes that could be used for clinical and applied purposes. Copyright © 2015. Published by Elsevier B.V.
    Animal Reproduction Science 01/2015; DOI:10.1016/j.anireprosci.2015.01.011 · 1.58 Impact Factor
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    ABSTRACT: Upstream stimulating factor 1 (USF1) is a basic helix loop helix transcription factor that specifically binds to E-box DNA motifs, known cis-elements of key oocyte expressed genes essential for oocyte and early embryo development. However, the functional and regulatory role of USF1 in bovine oocyte and embryo development is not understood. In this study, we demonstrated that USF1 mRNA is maternal in origin and expressed in a stage specific manner during the course of oocyte maturation and preimplantation embryonic development. Immunocytochemical analysis showed detectable USF1 protein during oocyte maturation and early embryonic development with increased abundance in cytoplasm and nucleus at 8-16 cell stage of embryo development, suggesting a potential role in embryonic genome activation. Knockdown of USF1 in germinal vesicle stage oocytes did not impact meiotic maturation or cumulus expansion, but caused significant changes in mRNA abundance for genes associated with oocyte developmental competence. Furthermore, siRNA mediated depletion of USF1 in presumptive zygote stage embryos demonstrated that USF1 is required for early embryonic development to the blastocyst stage. A similar (USF2) yet unique (TWIST2) expression pattern during oocyte and early embryonic development for related E box binding transcription factors known to cooperatively bind USF1 suggest a potential link to USF1 action. This study demonstrates that USF1 is a maternally derived transcription factor required for bovine early embryonic development which also functions in regulation of JY-1 and GDF9 genes associated with oocyte competence.
    Reproduction (Cambridge, England) 11/2014; 149(2). DOI:10.1530/REP-14-0445 · 3.26 Impact Factor


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