Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos
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 v...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-45251-w |
| _version_ | 1797273917770956800 |
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| author | Ai Kiyomitsu Toshiya Nishimura Shiang Jyi Hwang Satoshi Ansai Masato T. Kanemaki Minoru Tanaka Tomomi Kiyomitsu |
| author_facet | Ai Kiyomitsu Toshiya Nishimura Shiang Jyi Hwang Satoshi Ansai Masato T. Kanemaki Minoru Tanaka Tomomi Kiyomitsu |
| author_sort | Ai Kiyomitsu |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-07T14:52:02Z |
| format | Article |
| id | doaj.art-dc7c8c696f3b4304938aefd2aa89b6fd |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-07T14:52:02Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-dc7c8c696f3b4304938aefd2aa89b6fd2024-03-05T19:41:42ZengNature PortfolioNature Communications2041-17232024-02-0115111910.1038/s41467-024-45251-wRan-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryosAi Kiyomitsu0Toshiya Nishimura1Shiang Jyi Hwang2Satoshi Ansai3Masato T. Kanemaki4Minoru Tanaka5Tomomi Kiyomitsu6Okinawa Institute of Science and Technology Graduate UniversityDivision of Biological Science, Graduate School of Science, Nagoya University, Chikusa-kuOkinawa Institute of Science and Technology Graduate UniversityGraduate School of Life Sciences, Tohoku UniversityDepartment of Chromosome Science, National Institute of Genetics, Research Organization of Information and Systems (ROIS), and Graduate Institute for Advanced StudiesDivision of Biological Science, Graduate School of Science, Nagoya University, Chikusa-kuOkinawa Institute of Science and Technology Graduate UniversityAbstract 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.https://doi.org/10.1038/s41467-024-45251-w |
| spellingShingle | Ai Kiyomitsu Toshiya Nishimura Shiang Jyi Hwang Satoshi Ansai Masato T. Kanemaki Minoru Tanaka Tomomi Kiyomitsu Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos Nature Communications |
| title | Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos |
| title_full | Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos |
| title_fullStr | Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos |
| title_full_unstemmed | Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos |
| title_short | Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos |
| title_sort | ran gtp assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos |
| url | https://doi.org/10.1038/s41467-024-45251-w |
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