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Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos

Author

Listed:
  • Ai Kiyomitsu

    (Okinawa Institute of Science and Technology Graduate University)

  • Toshiya Nishimura

    (Nagoya University, Chikusa-ku
    Hokkaido University Fisheries Sciences)

  • Shiang Jyi Hwang

    (Okinawa Institute of Science and Technology Graduate University)

  • Satoshi Ansai

    (Tohoku University
    Kyoto University, Sakyo-ku)

  • Masato T. Kanemaki

    (Research Organization of Information and Systems (ROIS), and Graduate Institute for Advanced Studies
    The University of Tokyo)

  • Minoru Tanaka

    (Nagoya University, Chikusa-ku)

  • Tomomi Kiyomitsu

    (Okinawa Institute of Science and Technology Graduate University)

Abstract

Despite drastic cellular changes during cleavage, a mitotic spindle assembles in each blastomere to accurately segregate duplicated chromosomes. Mechanisms of mitotic spindle assembly have been extensively studied using small somatic cells. However, mechanisms of spindle assembly in large vertebrate embryos remain little understood. Here, we establish functional assay systems in medaka (Oryzias latipes) embryos by combining CRISPR knock-in with auxin-inducible degron technology. Live imaging reveals several unexpected features of microtubule organization and centrosome positioning that achieve rapid, accurate cleavage. Importantly, Ran-GTP assembles a dense microtubule network at the metaphase spindle center that is essential for chromosome segregation in early embryos. This unique spindle structure is remodeled into a typical short, somatic-like spindle after blastula stages, when Ran-GTP becomes dispensable for chromosome segregation. We propose that despite the presence of centrosomes, the chromosome-derived Ran-GTP pathway has essential roles in functional spindle assembly in large, rapidly dividing vertebrate early embryos, similar to acentrosomal spindle assembly in oocytes.

Suggested Citation

  • Ai Kiyomitsu & Toshiya Nishimura & Shiang Jyi Hwang & Satoshi Ansai & Masato T. Kanemaki & Minoru Tanaka & Tomomi Kiyomitsu, 2024. "Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45251-w
    DOI: 10.1038/s41467-024-45251-w
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    References listed on IDEAS

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    1. Daigo Inoue & Manuel Stemmer & Thomas Thumberger & Thomas Ruppert & Felix Bärenz & Joachim Wittbrodt & Oliver J. Gruss, 2017. "Expression of the novel maternal centrosome assembly factor Wdr8 is required for vertebrate embryonic mitoses," Nature Communications, Nature, vol. 8(1), pages 1-12, April.
    2. Petr Kaláb & Arnd Pralle & Ehud Y. Isacoff & Rebecca Heald & Karsten Weis, 2006. "Analysis of a RanGTP-regulated gradient in mitotic somatic cells," Nature, Nature, vol. 440(7084), pages 697-701, March.
    3. Ravindra D. Makde & Joseph R. England & Hemant P. Yennawar & Song Tan, 2010. "Structure of RCC1 chromatin factor bound to the nucleosome core particle," Nature, Nature, vol. 467(7315), pages 562-566, September.
    4. Janko Kajtez & Anastasia Solomatina & Maja Novak & Bruno Polak & Kruno Vukušić & Jonas Rüdiger & Gheorghe Cojoc & Ana Milas & Ivana Šumanovac Šestak & Patrik Risteski & Federica Tavano & Anna H. Klemm, 2016. "Overlap microtubules link sister k-fibres and balance the forces on bi-oriented kinetochores," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
    5. Rafael E. Carazo-Salas & Giulia Guarguaglini & Oliver J. Gruss & Alexandra Segref & Eric Karsenti & Iain W. Mattaj, 1999. "Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation," Nature, Nature, vol. 400(6740), pages 178-181, July.
    6. Masahiro Kasahara & Kiyoshi Naruse & Shin Sasaki & Yoichiro Nakatani & Wei Qu & Budrul Ahsan & Tomoyuki Yamada & Yukinobu Nagayasu & Koichiro Doi & Yasuhiro Kasai & Tomoko Jindo & Daisuke Kobayashi & , 2007. "The medaka draft genome and insights into vertebrate genome evolution," Nature, Nature, vol. 447(7145), pages 714-719, June.
    7. Aisha Yesbolatova & Yuichiro Saito & Naomi Kitamoto & Hatsune Makino-Itou & Rieko Ajima & Risako Nakano & Hirofumi Nakaoka & Kosuke Fukui & Kanae Gamo & Yusuke Tominari & Haruki Takeuchi & Yumiko Saga, 2020. "The auxin-inducible degron 2 technology provides sharp degradation control in yeast, mammalian cells, and mice," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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