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Ependymal cells of chordate larvae are stem-like cells that form the adult nervous system

Nature volume 469, pages 525–528 (2011)Cite this article

Abstract

In ascidian tunicates, the metamorphic transition from larva to adult is accompanied by dynamic changes in the body plan. For instance, the central nervous system (CNS) is subjected to extensive rearrangement because its regulating larval organs are lost and new adult organs are created1. To understand how the adult CNS is reconstructed, we traced the fate of larval CNS cells during ascidian metamorphosis by using transgenic animals and imaging technologies with photoconvertible fluorescent proteins2. Here we show that most parts of the ascidian larval CNS, except for the tail nerve cord, are maintained during metamorphosis and recruited to form the adult CNS. We also show that most of the larval neurons disappear and only a subset of cholinergic motor neurons and glutamatergic neurons are retained. Finally, we demonstrate that ependymal cells of the larval CNS contribute to the construction of the adult CNS and that some differentiate into neurons in the adult CNS. An unexpected role of ependymal cells highlighted by this study is that they serve as neural stem-like cells to reconstruct the adult nervous network during chordate metamorphosis. Consequently, the plasticity of non-neuronal ependymal cells and neuronal cells in chordates should be re-examined by future studies3,4.

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Figure 1: Tracing of cells in the larval CNS.
Figure 2: Tracing of larval cholinergic neurons and ependymal cells, and differentiation of larval ependymal cells to adult cholinergic neurons.
Figure 3: Adult CNS is constructed from the larval CNS.

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Acknowledgements

We acknowledge the members of the Shimoda Marine Research Center at the University of Tsukuba for their cooperation with our study. We also thank National Bio-resource Project, Ministry of Education, Culture, Sports, Science and Technology, Japan (MEXT), S. Fujiwara and all members of the Maizuru Fishery Research Station of Kyoto University and the Education and Research Center of Marine Bioresources of Tohoku University for providing us with Ciona adults, and C. Savakis for providing Minos. This study was supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science and MEXT to T.H., T.G.K., N.S. and Y.S. Y.S. was supported by the National Institute of Genetics Cooperative Research Program.

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Authors and Affiliations

  1. Shimoda Marine Research Center, University of Tsukuba, Shimoda, 415-0025, Shizuoka, Japan

    Takeo Horie, Ryoko Shinki, Yosuke Ogura & Yasunori Sasakura

  2. Department of Biology, Konan University, Kobe, 658-8501, Hyogo, Japan

    Takehiro G. Kusakabe

  3. Marine Genomics Unit, Okinawa Institute of Science and Technology Promotion Corporation, Onna, 904-0412, Okinawa, Japan

    Nori Satoh

Authors
  1. Takeo Horie
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  4. Takehiro G. Kusakabe
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  5. Nori Satoh
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  6. Yasunori Sasakura
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Contributions

T.H. and Y.S. designed the experiments. T.H., R.S. and Y.O. performed most of the experiments. T.H. and T.G.K. isolated cis regulatory elements. T.G.K. and N.S. were advisors for the experiments and evaluated the data. T.H., N.S. and Y.S. wrote the manuscript.

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Correspondence to Takeo Horie.

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The authors declare no competing financial interests.

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Horie, T., Shinki, R., Ogura, Y. et al. Ependymal cells of chordate larvae are stem-like cells that form the adult nervous system. Nature 469, 525–528 (2011). https://doi.org/10.1038/nature09631

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