Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (<i>Dazl</i>) at the oocyte-to-zygote transition

Chen, Jing; Melton, Collin; Suh, Nayoung; Oh, Jeong Su; Horner, Kathleen; Xie, Fang; Sette, Claudio; Blelloch, Robert; Conti, Marco

doi:10.1101/gad.2028911

Cited by 241 publications

(379 citation statements)

References 57 publications

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“…S1A). Inhibition of translation by MOs is a widely used tool in developmental biology and we routinely apply it to study mouse preimplantation development (Chen et al, 2011;Oh et al, 2011). We note that, unlike in Xenopus (Szenker et al, 2012;Lim et al, 2013), 5Ј UTR sequence divergence in mouse allows us to design MOs expected to target H3.3 but not H3.1 or H3.2.…”

Section: H33 Is Essential For Mouse Preimplantation Developmentmentioning

confidence: 99%

“…In mammals, H3.3 is a maternal factor that can arise from both H3f3a and H3f3b genes and is dynamically distributed during oogenesis (Chen et al, 2011) and through fertilization and cleavage stages to the blastocyst stage (Torres-Padilla et al, 2006). Dramatic epigenetic changes occur during this developmental period, and both DNA demethylation (Gu et al, 2011) and the dynamic regulation of histone marks (Erhardt et al, 2003;Puschendorf et al, 2008) are known to be essential for embryogenesis.…”

Section: Introductionmentioning

confidence: 99%

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Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development

2013

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Histone variants can replace canonical histones in the nucleosome and modify chromatin structure and gene expression. The histone variant H3.3 preferentially associates with active chromatin and has been implicated in the regulation of a diverse range of developmental processes. However, the mechanisms by which H3.3 may regulate gene activity are unclear and gene duplication has hampered an analysis of H3.3 function in mouse. Here, we report that the specific knockdown of H3.3 in fertilized mouse zygotes leads to developmental arrest at the morula stage. This phenotype can be rescued by exogenous H3.3 but not by canonical H3.1 mRNA. Loss of H3.3 leads to over-condensation and mis-segregation of chromosomes as early as the two-cell stage, with corresponding high levels of aneuploidy, but does not appear to affect zygotic gene activation at the two-cell stage or lineage gene transcription at the morula stage. H3.3-deficient embryos have significantly reduced levels of markers of open chromatin, such as H3K36me2 and H4K16Ac. Importantly, a mutation in H3.3K36 that disrupts H3K36 methylation (H3.3K36R) does not rescue the H3.3 knockdown (KD) phenotype. In addition, H3.3 KD embryos have increased incorporation of linker H1. Knockdown of Mof (Kat8), an acetyltransferase specific for H4K16, similarly leads to excessive H1 incorporation. Remarkably, pan-H1 RNA interference (RNAi) partially rescues the chromosome condensation of H3.3 KD embryos and allows development to the blastocyst stage. These results reveal that H3.3 mediates a balance between open and condensed chromatin that is crucial for the fidelity of chromosome segregation during early mouse development.

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Section: H33 Is Essential For Mouse Preimplantation Developmentmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development

2013

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“…Ribosome RIP as a strategy to monitor ribosome loading onto maternal mRNAs and translation in the oocyte A genome-wide analysis of actively translating mRNA during mammalian oocyte maturation provided a first insight into the mechanisms controlling specific translation from transition from prophase I to MI and MII (Chen et al, 2011). However, the large number of oocytes needed for polysome fractionation on a sucrose density gradient limits the temporal resolution of measurements.…”

Section: Resultsmentioning

confidence: 99%

DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

Martins¹,

Liu²,

Oke³

et al. 2016

Development

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Meiotic progression requires exquisitely coordinated translation of maternal messenger (m)RNA that has accumulated during oocyte growth. A major regulator of this program is the cytoplasmic polyadenylation element binding protein 1 (CPEB1). However, the temporal pattern of translation at different meiotic stages indicates the function of additional RNA binding proteins (RBPs). Here, we report that deleted in azoospermia-like (DAZL) cooperates with CPEB1 to regulate maternal mRNA translation. Using a strategy that monitors ribosome loading onto endogenous mRNAs and a prototypic translation target, we show that ribosome loading is induced in a DAZL-and CPEB1-dependent manner, as the oocyte reenters meiosis. Depletion of the two RBPs from oocytes and mutagenesis of the 3′ untranslated regions (UTRs) demonstrate that both RBPs interact with the Tex19.1 3′ UTR and cooperate in translation activation of this mRNA. We observed a synergism between DAZL and cytoplasmic polyadenylation elements (CPEs) in the translation pattern of maternal mRNAs when using a genome-wide analysis. Mechanistically, the number of DAZL proteins loaded onto the mRNA and the characteristics of the CPE might define the degree of cooperation between the two RBPs in activating translation and meiotic progression.

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“…These data strongly suggest that in somatic cells, DAZL participates to the storage of its target mRNAs at specific cytoplasmic sites. In oocyte, DAZL seems to be diffusely distributed throughout the oocyte cytoplasm but is also enriched at the poles of both MI and MII metaphase spindles (Chen et al 2011). A careful simultaneous analysis of DAZL and CPEB1 localization throughout oogenesis remains to be undertaken.…”

Section: Rbps and Translational Controlmentioning

confidence: 99%

“…Then, the newly synthesized DAZL protein increases the translation of its own mRNA. This post-transcriptional regulatory cascade leads to a progressive accumulation of DAZL, which in turn promotes the translation of DAZL target mRNAs, including Tpx2, Tex19.1, and other regulators of the cell cycle necessary for spindle assembly, the MI-MII transition, and early embryonic development (Chen et al 2011). In addition, DAZL is known to interact with several other proteins, including Pumilio2 that may act as a translational repressor (Vasudevan et al 2006, Brook et al 2009, MacNicol & MacNicol 2010.…”

Section: Rbps and Translational Controlmentioning

confidence: 99%

RNA-binding proteins, RNA granules, and gametes: is unity strength?

Nguyen-Chi¹,

Morello²

2011

Reproduction

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Changes in mRNA translation and degradation represent post-transcriptional processes operating during gametogenesis and early embryogenesis to ensure regulated protein synthesis. Numerous mRNA-binding proteins (RBPs) have been described in multiple animal models that contribute to the control of mRNA translation and decay during oogenesis and spermatogenesis. An emerging view from studies performed in germ cells and somatic cells is that RBPs associate with their target mRNAs in RNA-protein (or ribonucleoprotein) complexes (mRNPs) that assemble in various cytoplasmic RNA granules that communicate with the translation machinery and control mRNA storage, triage, and degradation. In comparison with Xenopus, Caenorhabditis elegans, or Drosophila, the composition and role of cytoplasmic RNA-containing granules in mammalian germ cells are still poorly understood. However, regained interest for these structures has emerged with the recent discovery of their role in small RNA synthesis and transposon silencing through DNA methylation. In this review, we will briefly summarize our current knowledge on cytoplasmic RNA granules in murine germ cells and describe the role of some of the RBPs they contain in regulating mRNA metabolism and small RNA processing during gametogenesis.

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Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition

Cited by 241 publications

References 57 publications

Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development

Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development

DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation

RNA-binding proteins, RNA granules, and gametes: is unity strength?

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