Zygotic Nuclear F-Actin Safeguards Embryonic Development
Summary: After fertilization, sperm and oocyte nuclei are rapidly remodeled to form swollen pronuclei (PN) in mammalian zygotes, and the proper formation and function of PN are key to producing totipotent zygotes. However, how mature PN are formed has been unclear. We find that filamentous actin (F-...
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2020-06-01
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doaj-8968abae7ec4417b850cf1095a860c292020-11-25T03:06:43ZengElsevierCell Reports2211-12472020-06-013113107824Zygotic Nuclear F-Actin Safeguards Embryonic DevelopmentTomomi Okuno0Wayne Yang Li1Yu Hatano2Atsushi Takasu3Yuko Sakamoto4Mari Yamamoto5Zenki Ikeda6Taiki Shindo7Matthias Plessner8Kohtaro Morita9Kazuya Matsumoto10Kazuo Yamagata11Robert Grosse12Kei Miyamoto13Graduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanInstitute of Experimental and Clinical Pharmacology and Toxicology, Albert-Ludwigs-University Freiburg, Albertstrasse 25, 79104 Freiburg, GermanyGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, JapanInstitute of Experimental and Clinical Pharmacology and Toxicology, Albert-Ludwigs-University Freiburg, Albertstrasse 25, 79104 Freiburg, Germany; CIBSS–Centre for Integrative Biological Signalling Studies, Albert-Ludwigs-University Freiburg, Schänzlestr. 18, 79104 Freiburg, GermanyGraduate School of Biology-Oriented Science and Technology, Kindai University, Kinokawa-shi, Wakayama 649-6493, Japan; Corresponding authorSummary: After fertilization, sperm and oocyte nuclei are rapidly remodeled to form swollen pronuclei (PN) in mammalian zygotes, and the proper formation and function of PN are key to producing totipotent zygotes. However, how mature PN are formed has been unclear. We find that filamentous actin (F-actin) assembles in the PN of mouse zygotes and is required for fully functional PN. The perturbation of nuclear actin dynamics in zygotes results in the misregulation of genes related to genome integrity and abnormal development of mouse embryos. We show that nuclear F-actin ensures DNA damage repair, thus preventing the activation of a zygotic checkpoint. Furthermore, optogenetic control of cofilin nuclear localization reveals the dynamically regulated F-actin nucleoskeleton in zygotes, and its timely disassembly is needed for developmental progression. Nuclear F-actin is a hallmark of totipotent zygotic PN, and the temporal regulation of its polymerized state is necessary for normal embryonic development.http://www.sciencedirect.com/science/article/pii/S2211124720308056nuclear actinpronucleuszygoteDNA repairtranscriptionchromatin |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Tomomi Okuno Wayne Yang Li Yu Hatano Atsushi Takasu Yuko Sakamoto Mari Yamamoto Zenki Ikeda Taiki Shindo Matthias Plessner Kohtaro Morita Kazuya Matsumoto Kazuo Yamagata Robert Grosse Kei Miyamoto |
spellingShingle |
Tomomi Okuno Wayne Yang Li Yu Hatano Atsushi Takasu Yuko Sakamoto Mari Yamamoto Zenki Ikeda Taiki Shindo Matthias Plessner Kohtaro Morita Kazuya Matsumoto Kazuo Yamagata Robert Grosse Kei Miyamoto Zygotic Nuclear F-Actin Safeguards Embryonic Development Cell Reports nuclear actin pronucleus zygote DNA repair transcription chromatin |
author_facet |
Tomomi Okuno Wayne Yang Li Yu Hatano Atsushi Takasu Yuko Sakamoto Mari Yamamoto Zenki Ikeda Taiki Shindo Matthias Plessner Kohtaro Morita Kazuya Matsumoto Kazuo Yamagata Robert Grosse Kei Miyamoto |
author_sort |
Tomomi Okuno |
title |
Zygotic Nuclear F-Actin Safeguards Embryonic Development |
title_short |
Zygotic Nuclear F-Actin Safeguards Embryonic Development |
title_full |
Zygotic Nuclear F-Actin Safeguards Embryonic Development |
title_fullStr |
Zygotic Nuclear F-Actin Safeguards Embryonic Development |
title_full_unstemmed |
Zygotic Nuclear F-Actin Safeguards Embryonic Development |
title_sort |
zygotic nuclear f-actin safeguards embryonic development |
publisher |
Elsevier |
series |
Cell Reports |
issn |
2211-1247 |
publishDate |
2020-06-01 |
description |
Summary: After fertilization, sperm and oocyte nuclei are rapidly remodeled to form swollen pronuclei (PN) in mammalian zygotes, and the proper formation and function of PN are key to producing totipotent zygotes. However, how mature PN are formed has been unclear. We find that filamentous actin (F-actin) assembles in the PN of mouse zygotes and is required for fully functional PN. The perturbation of nuclear actin dynamics in zygotes results in the misregulation of genes related to genome integrity and abnormal development of mouse embryos. We show that nuclear F-actin ensures DNA damage repair, thus preventing the activation of a zygotic checkpoint. Furthermore, optogenetic control of cofilin nuclear localization reveals the dynamically regulated F-actin nucleoskeleton in zygotes, and its timely disassembly is needed for developmental progression. Nuclear F-actin is a hallmark of totipotent zygotic PN, and the temporal regulation of its polymerized state is necessary for normal embryonic development. |
topic |
nuclear actin pronucleus zygote DNA repair transcription chromatin |
url |
http://www.sciencedirect.com/science/article/pii/S2211124720308056 |
work_keys_str_mv |
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