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Cell Cycle Remodeling and Zygotic Gene Activation at the Midblastula Transition

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Vertebrate Development

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 953))

Abstract

Following fertilization, vertebrate embryos delay large-scale activation of the zygotic genome from several hours in fish and amphibians to several days in mammals. Externally developing embryos also undergo synchronous and extraordinarily rapid cell divisions that are accelerated by promiscuous licensing of DNA replication origins, absence of gap phases and cell cycle checkpoints, and preloading of the egg with maternal RNAs and proteins needed to drive early development. After a species-specific number of cell divisions, the cell cycle slows and becomes asynchronous, gap phases appear, checkpoint functions are acquired, and large-scale zygotic gene activation begins. These events, along with clearance of maternal RNAs and proteins, define the maternal to zygotic transition and are coordinated at a developmental milestone termed the midblastula transition (MBT). Despite the relative quiescence of the zygotic genome in vertebrate embryos, genes required for clearance of maternal RNAs and for the initial steps in mesoderm induction are robustly transcribed before MBT. The coordination and timing of the MBT depends on a mechanism that senses the ratio of nuclear to cytoplasmic content as well as mechanisms that are independent of the nuclear–cytoplasm ratio. Changes in chromatin architecture anticipate zygotic gene activation, and maternal transcription factors identified as regulators of pluripotency play critical roles in kick-starting the transition from the proliferative, pluripotent state of the early embryo to the more lineage-committed phase of development after the MBT. This chapter describes the regulation of the cell cycle and the activation of zygotic gene expression before and after the MBT in vertebrate embryos.

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Acknowledgements

We thank Shelby Blythe, Jing Yang, Daniel Kessler, Mary Mullins, Karla Neugebauer, Patricia Heyn, Steven Harvey, and Derek Stemple for helpful discussions. We thank Jing Yang for sharing unpublished data and Karla Neugebauer and Patricia Heyn for permission to reprint their published data. We are indebted to authoritative reviews from many authors, as cited above, and thank Shelby Blythe and Eric Wieschaus for sharing their review prior to publication. M.Z. was supported in part by the Developmental Biology Training Grant at Penn (T32HD007516). J.S. was supported in part by the Cell and Molecular Biology Training Grant at Penn (T32-GM07229). M.A.L. was supported by the NIH (R01GM083988) and a Searle Scholar award. P.S.K. was supported by the NIH (R01HL110806 and R01MH100923) and the Institute for Regenerative Medicine at the University of Pennsylvania.

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    Authors and Affiliations

    1. Department of Biology, University of Pennsylvania, Philadelphia, PA, USA

      Maomao Zhang & Michael A. Lampson

    2. Cell and Molecular Biology Graduate Group, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA

      Maomao Zhang, Jennifer Skirkanich, Michael A. Lampson & Peter S. Klein

    3. Department of Cancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York, NY, USA

      Maomao Zhang

    4. Department of Biology, Bryn Mawr College, Bryn Mawr, PA, USA

      Jennifer Skirkanich

    5. Department of Medicine (Hematology-Oncology), Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, USA

      Peter S. Klein

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    Correspondence to Michael A. Lampson or Peter S. Klein .

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    1. Laboratory of Genetics, University of Wisconsin—Madison, Madison, Wisconsin, USA

      Francisco Pelegri

    2. Department of Integrative Biosciences, Oregon Health & Science University, Portland, Oregon, USA

      Michael Danilchik

    3. Department of Cell Biology, University of Virginia Health System, Charlottesville, Virginia, USA

      Ann Sutherland

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    Zhang, M., Skirkanich, J., Lampson, M.A., Klein, P.S. (2017). Cell Cycle Remodeling and Zygotic Gene Activation at the Midblastula Transition. In: Pelegri, F., Danilchik, M., Sutherland, A. (eds) Vertebrate Development. Advances in Experimental Medicine and Biology, vol 953. Springer, Cham. https://doi.org/10.1007/978-3-319-46095-6_9

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