Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development
In many animal species, the body axis is determined by the relocalization of maternal determinants, organelles, or unique cell populations in a cytoskeleton-dependent manner. In the ascidian first cell cycle, the myoplasm, including mitochondria, endoplasmic reticulum (ER), and maternal mRNAs, move...
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MDPI AG
2022-02-01
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| author | Toshiyuki Goto Shuhei Torii Aoi Kondo Kazumasa Kanda Junji Kawakami Yosky Kataoka Takahito Nishikata |
| author_facet | Toshiyuki Goto Shuhei Torii Aoi Kondo Kazumasa Kanda Junji Kawakami Yosky Kataoka Takahito Nishikata |
| author_sort | Toshiyuki Goto |
| collection | DOAJ |
| description | In many animal species, the body axis is determined by the relocalization of maternal determinants, organelles, or unique cell populations in a cytoskeleton-dependent manner. In the ascidian first cell cycle, the myoplasm, including mitochondria, endoplasmic reticulum (ER), and maternal mRNAs, move to the future posterior side concomitantly (called ooplasmic segregation or cytoplasmic and cortical reorganization). This translocation consists of first and second phases depending on the actin and microtubule, respectively. However, the transition from first to second phase, that is, translocation of myoplasmic components from microfilaments to microtubules, has been poorly investigated. In this study, we analyzed the relationship between these cytoskeletons and myoplasmic components during the first cell cycle and their role in morphogenesis by inhibitor experiments. Owing to our improved visualization techniques, there was unexpected F-actin accumulation at the vegetal pole during this transition period. When this F-actin was depolymerized, the microtubule structure was strongly affected, the myoplasmic components, including maternal mRNA, were mislocalized, and the anteroposterior axis formation was disordered. These results suggested the importance of F-actin during the first cell cycle and the existence of interactions between microfilaments and microtubules, implying the enigmatic mechanism of ooplasmic segregation. Solving this mystery leads us to an improved understanding of ascidian early development. |
| first_indexed | 2024-03-09T19:36:45Z |
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| id | doaj.art-9fdd5237136a4990b4dbb078d0b02b9e |
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| issn | 2221-3759 |
| language | English |
| last_indexed | 2024-03-09T19:36:45Z |
| publishDate | 2022-02-01 |
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| series | Journal of Developmental Biology |
| spelling | doaj.art-9fdd5237136a4990b4dbb078d0b02b9e2023-11-24T01:53:06ZengMDPI AGJournal of Developmental Biology2221-37592022-02-011011010.3390/jdb10010010Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian DevelopmentToshiyuki Goto0Shuhei Torii1Aoi Kondo2Kazumasa Kanda3Junji Kawakami4Yosky Kataoka5Takahito Nishikata6Frontiers of Innovative Research in Science and Technology (FIRST), Konan University, 7-1-20 Minatojima-Minamimachi, Chuo-k, Kobe 650-0047, JapanFrontiers of Innovative Research in Science and Technology (FIRST), Konan University, 7-1-20 Minatojima-Minamimachi, Chuo-k, Kobe 650-0047, JapanFrontiers of Innovative Research in Science and Technology (FIRST), Konan University, 7-1-20 Minatojima-Minamimachi, Chuo-k, Kobe 650-0047, JapanFrontiers of Innovative Research in Science and Technology (FIRST), Konan University, 7-1-20 Minatojima-Minamimachi, Chuo-k, Kobe 650-0047, JapanFrontiers of Innovative Research in Science and Technology (FIRST), Konan University, 7-1-20 Minatojima-Minamimachi, Chuo-k, Kobe 650-0047, JapanLaboratory for Cellular Function Imaging, RIKEN Center for Biosystems Dynamics Research, Kobe 650-0047, JapanFrontiers of Innovative Research in Science and Technology (FIRST), Konan University, 7-1-20 Minatojima-Minamimachi, Chuo-k, Kobe 650-0047, JapanIn many animal species, the body axis is determined by the relocalization of maternal determinants, organelles, or unique cell populations in a cytoskeleton-dependent manner. In the ascidian first cell cycle, the myoplasm, including mitochondria, endoplasmic reticulum (ER), and maternal mRNAs, move to the future posterior side concomitantly (called ooplasmic segregation or cytoplasmic and cortical reorganization). This translocation consists of first and second phases depending on the actin and microtubule, respectively. However, the transition from first to second phase, that is, translocation of myoplasmic components from microfilaments to microtubules, has been poorly investigated. In this study, we analyzed the relationship between these cytoskeletons and myoplasmic components during the first cell cycle and their role in morphogenesis by inhibitor experiments. Owing to our improved visualization techniques, there was unexpected F-actin accumulation at the vegetal pole during this transition period. When this F-actin was depolymerized, the microtubule structure was strongly affected, the myoplasmic components, including maternal mRNA, were mislocalized, and the anteroposterior axis formation was disordered. These results suggested the importance of F-actin during the first cell cycle and the existence of interactions between microfilaments and microtubules, implying the enigmatic mechanism of ooplasmic segregation. Solving this mystery leads us to an improved understanding of ascidian early development.https://www.mdpi.com/2221-3759/10/1/10axis determinationERactinmicrotubulematernal mRNA |
| spellingShingle | Toshiyuki Goto Shuhei Torii Aoi Kondo Kazumasa Kanda Junji Kawakami Yosky Kataoka Takahito Nishikata Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development Journal of Developmental Biology axis determination ER actin microtubule maternal mRNA |
| title | Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development |
| title_full | Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development |
| title_fullStr | Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development |
| title_full_unstemmed | Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development |
| title_short | Actin Filament in the First Cell Cycle Contributes to the Determination of the Anteroposterior Axis in Ascidian Development |
| title_sort | actin filament in the first cell cycle contributes to the determination of the anteroposterior axis in ascidian development |
| topic | axis determination ER actin microtubule maternal mRNA |
| url | https://www.mdpi.com/2221-3759/10/1/10 |
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