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      Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a.

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      Journal: Science (New York, N.Y.)
      Keywords: Animals, Epididymis, abnormalities, Epigenesis, Genetic, Female, Gene Expression Regulation, Developmental, Histones, metabolism, Jumonji Domain-Containing Histone Demethylases, genetics, Male, Methylation, Mice, Mice, Mutant Strains, Mice, Transgenic, Ovary, enzymology, Protein Processing, Post-Translational, Sex Determination Processes, Testis, Uterus

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          Abstract

          Developmental gene expression is defined through cross-talk between the function of transcription factors and epigenetic status, including histone modification. Although several transcription factors play crucial roles in mammalian sex determination, how epigenetic regulation contributes to this process remains unknown. We observed male-to-female sex reversal in mice lacking the H3K9 demethylase Jmjd1a and found that Jmjd1a regulates expression of the mammalian Y chromosome sex-determining gene Sry. Jmjd1a directly and positively controls Sry expression by regulating H3K9me2 marks. These studies reveal a pivotal role of histone demethylation in mammalian sex determination.

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          G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription.

          Makoto Tachibana, Andrew M. Fukuda, Yoichi Shinkai … (2008)
          Methylation of DNA and lysine 9 of histone H3 (H3K9) are well-conserved epigenetic marks for transcriptional silencing. Although H3K9 methylation directs DNA methylation in filamentous fungi and plants, this pathway has not been corroborated in mammals. G9a and GLP/Eu-HMTase1 are two-related mammalian lysine methyltransferases and a G9a/GLP heteromeric complex regulates H3K9 methylation of euchromatin. To elucidate the function of G9a/GLP-mediated H3K9 methylation in the regulation of DNA methylation and transcriptional silencing, we characterized ES cells expressing catalytically inactive mutants of G9a and/or GLP. Interestingly, in ES cells expressing a G9a-mutant/GLP complex that does not rescue global H3K9 methylation, G9a/GLP-target genes remain silent. The CpG sites of the promoter regions of these genes were hypermethylated in such mutant ES cells, but hypomethylated in G9a- or GLP-KO ES cells. Treatment with a DNA methyltransferase inhibitor reactivates these G9a/GLP-target genes in ES cells expressing catalytically inactive G9a/GLP proteins, but not the wild-type proteins. This is the first clear evidence that G9a/GLP suppresses transcription by independently inducing both H3K9 and DNA methylation.
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            Sry: the master switch in mammalian sex determination.

            Kenichi Kashimada, Peter Koopman (2010)
            SRY, the mammalian Y-chromosomal testis-determining gene, induces male sex determination. Recent studies in mice reveal that the major role of SRY is to achieve sufficient expression of the related gene Sox9, in order to induce Sertoli cell differentiation, which in turn drives testis formation. Here, we discuss the cascade of events triggered by SRY and the mechanisms that reinforce the differentiation of the testes in males while actively inhibiting ovarian development.
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              Functional dynamics of H3K9 methylation during meiotic prophase progression.

              Makoto Tachibana, Masami Nozaki, Naoki Takeda … (2007)
              Histone H3 lysine 9 (H3K9) methylation is a crucial epigenetic mark of heterochromatin formation and transcriptional silencing. G9a is a major mammalian H3K9 methyltransferase at euchromatin and is essential for mouse embryogenesis. Here we describe the roles of G9a in germ cell development. Mutant mice in which G9a is specifically inactivated in the germ-lineage displayed sterility due to a drastic loss of mature gametes. G9a-deficient germ cells exhibited perturbation of synchronous synapsis in meiotic prophase. Importantly, mono- and di-methylation of H3K9 (H3K9me1 and 2) in G9a-deficient germ cells were significantly reduced and G9a-regulated genes were overexpressed during meiosis, suggesting that G9a-mediated epigenetic gene silencing is crucial for proper meiotic prophase progression. Finally, we show that H3K9me1 and 2 are dynamically and sex-differentially regulated during the meiotic prophase. This genetic and biochemical evidence strongly suggests that a specific set of H3K9 methyltransferase(s) and demethylase(s) coordinately regulate gametogenesis.
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                Author and article information

                Journal
                PubMed ID:: 24009392
                DOI:: 10.1126/science.1239864

                ScienceOpen disciplines: Chemistry
                Keywords: Animals,Epididymis,abnormalities,Epigenesis, Genetic,Female,Gene Expression Regulation, Developmental,Histones,metabolism,Jumonji Domain-Containing Histone Demethylases,genetics,Male,Methylation,Mice,Mice, Mutant Strains,Mice, Transgenic,Ovary,enzymology,Protein Processing, Post-Translational,Sex Determination Processes,Testis,Uterus
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                ScienceOpen disciplines: Chemistry
                Keywords: Animals, Epididymis, abnormalities, Epigenesis, Genetic, Female, Gene Expression Regulation, Developmental, Histones, metabolism, Jumonji Domain-Containing Histone Demethylases, genetics, Male, Methylation, Mice, Mice, Mutant Strains, Mice, Transgenic, Ovary, enzymology, Protein Processing, Post-Translational, Sex Determination Processes, Testis, Uterus

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