Acknowledgement
This work was supported by grants NRF-2021R1A4A1027355, NRF-2021R1A2C3011919, and NRF-2021R1C1C2009319 from the National Research Foundation of Korea (NRF).
References
- Al Jord, A., Lemaitre, A., Delgehyr, N., Faucourt, M., Spassky, N., and Meunier, A. (2014). Centriole amplification by mother and daughter centrioles differs in multiciliated cells. Nature 516, 104-107. https://doi.org/10.1038/nature13770
- Anderson, R.G. and Brenner, R.M. (1971). The formation of basal bodies (centrioles) in the rhesus monkey oviduct. J. Cell Biol. 50, 10-34. https://doi.org/10.1083/jcb.50.1.10
- Banizs, B., Pike, M.M., Millican, C.L., Ferguson, W.B., Komlosi, P., Sheetz, J., Bell, P.D., Schwiebert, E.M., and Yoder, B.K. (2005). Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 132, 5329-5339. https://doi.org/10.1242/dev.02153
- Bienz, M. (2005). β-Catenin: a pivot between cell adhesion and Wnt signalling. Curr. Biol. 15, R64-R67. https://doi.org/10.1016/j.cub.2004.12.058
- Breslow, D.K. and Holland, A.J. (2019). Mechanism and regulation of centriole and cilium biogenesis. Annu. Rev. Biochem. 88, 691-724. https://doi.org/10.1146/annurev-biochem-013118-111153
- Delgehyr, N., Meunier, A., Faucourt, M., Bosch Grau, M., Strehl, L., Janke, C., and Spassky, N. (2015). Ependymal cell differentiation, from monociliated to multiciliated cells. Methods Cell Biol. 127, 19-35. https://doi.org/10.1016/bs.mcb.2015.01.004
- Dirksen, E.R. (1971). Centriole morphogenesis in developing ciliated epithelium of the mouse oviduct. J. Cell Biol. 51, 286-302. https://doi.org/10.1083/jcb.51.1.286
- Faber, J. and Nieuwkoop, P.D. (1994). Normal Table of Xenopus laevis (Daudin) (New York: Garland Science).
- Fliegauf, M., Benzing, T., and Omran, H. (2007). When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893. https://doi.org/10.1038/nrm2278
- Gomperts, B.N., Gong-Cooper, X., and Hackett, B.P. (2004). Foxj1 regulates basal body anchoring to the cytoskeleton of ciliated pulmonary epithelial cells. J. Cell Sci. 117, 1329-1337. https://doi.org/10.1242/jcs.00978
- Gonzalez-Mariscal, L., Namorado, M.C., Martin, D., Luna, J., Alarcon, L., Islas, S., Valencia, L., Muriel, P., Ponce, L., and Reyes, J.L. (2000). Tight junction proteins ZO-1, ZO-2, and occludin along isolated renal tubules. Kidney Int. 57, 2386-2402. https://doi.org/10.1046/j.1523-1755.2000.00098.x
- Kim, S., Ma, L., Shokhirev, M.N., Quigley, I., and Kintner, C. (2018). Multicilin and activated E2f4 induce multiciliated cell differentiation in primary fibroblasts. Sci. Rep. 8, 12369.
- Klos Dehring, D., Vladar, E., Werner, M., Mitchell, J., Hwang, P., and Mitchell, B. (2013). Deuterosome-mediated centriole biogenesis. Dev. Cell 27, 103-112.
- Labedan, P., Matthews, C., Kodjabachian, L., Cremer, H., Tissir, F., and Boutin, C. (2016). Dissection and staining of mouse brain ventricular wall for the analysis of ependymal cell cilia organization. Bio Protoc. 6, e1757.
- Matsuda, T. and Cepko, C.L. (2007). Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. U. S. A. 104, 1027-1032. https://doi.org/10.1073/pnas.0610155104
- Mercey, O., Al Jord, A., Rostaing, P., Mahuzier, A., Fortoul, A., Boudjema, A., Faucourt, M., Spassky, N., and Meunier, A. (2019a). Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors. Sci. Rep. 9, 13060.
- Mercey, O., Levine, M.S., LoMastro, G.M., Rostaing, P., Brotslaw, E., Gomez, V., Kumar, A., Spassky, N., Mitchell, B.J., Meunier, A., et al. (2019b). Massive centriole production can occur in the absence of deuterosomes in multiciliated cells. Nat. Cell Biol. 21, 1544-1552. https://doi.org/10.1038/s41556-019-0427-x
- Mirvis, M., Stearns, T., and James Nelson, W. (2018). Cilium structure, assembly, and disassembly regulated by the cytoskeleton. Biochem. J. 475, 2329-2353. https://doi.org/10.1042/BCJ20170453
- Mirzadeh, Z., Doetsch, F., Sawamoto, K., Wichterle, H., and Alvarez-Buylla, A. (2010). The subventricular zone en-face: wholemount staining and ependymal flow. J. Vis. Exp. (39), 1938.
- Mitchell, B., Jacobs, R., Li, J., Chien, S., and Kintner, C. (2007). A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 447, 97-101. https://doi.org/10.1038/nature05771
- Nanjundappa, R., Kong, D., Shim, K., Stearns, T., Brody, S.L., Loncarek, J., and Mahjoub, M.R. (2019). Regulation of cilia abundance in multiciliated cells. Elife 8, e44039.
- Ohata, S., Nakatani, J., Herranz-Perez, V., Cheng, J., Belinson, H., Inubushi, T., Snider, W., Garcia-Verdugo, J., Wynshaw-Boris, A., and Alvarez-Buylla, A. (2014). Loss of Dishevelleds disrupts planar polarity in ependymal motile cilia and results in hydrocephalus. Neuron 83, 558-571. https://doi.org/10.1016/j.neuron.2014.06.022
- Park, S., Lee, H., Lee, J., Park, E., and Park, S. (2019). Ependymal cells require Anks1a for their proper development. Mol. Cells 42, 245-251.
- Redmond, S.A., Figueres-Onate, M., Obernier, K., Nascimento, M.A., Parraguez, J.I., Lopez-Mascaraque, L., Fuentealba, L.C., and Alvarez-Buylla, A. (2019). Development of ependymal and postnatal neural stem cells and their origin from a common embryonic progenitor. Cell Rep. 27, 429-441. e3. https://doi.org/10.1016/j.celrep.2019.01.088
- Revinski, D.R., Zaragosi, L., Boutin, C., Ruiz-Garcia, S., Deprez, M., Thome, V., Rosnet, O., Gay, A., Mercey, O., Paquet, A., et al. (2018). CDC20B is required for deuterosome-mediated centriole production in multiciliated cells. Nat. Commun. 9, 4668.
- Ryu, H., Lee, H., Lee, J., Noh, H., Shin, M., Kumar, V., Hong, S., Kim, J., and Park, S. (2021). The molecular dynamics of subdistal appendages in multi-ciliated cells. Nat. Commun. 12, 612.
- Shahid, U. and Singh, P. (2018). Emerging picture of deuterosome-dependent centriole amplification in MCCs. Cells 7, 152.
- Sir, J.H., Barr, A.R., Nicholas, A.K., Carvalho, O.P., Khurshid, M., Sossick, A., Reichelt, S., D'Santos, C., Woods, C.G., and Gergely, F. (2011). A primary microcephaly protein complex forms a ring around parental centrioles. Nat. Genet. 43, 1147-1153. https://doi.org/10.1038/ng.971
- Spassky, N. and Meunier, A. (2017). The development and functions of multiciliated epithelia. Nat. Rev. Mol. Cell Biol. 18, 423-436. https://doi.org/10.1038/nrm.2017.21
- Spassky, N., Merkle, F.T., Flames, N., Tramontin, A.D., Garcia-Verdugo, J.M., and Alvarez-Buylla, A. (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci. 25, 10-18. https://doi.org/10.1523/JNEUROSCI.1108-04.2005
- Umair, Z., Kumar, V., Goutam, R.S., Kumar, S., Lee, U., and Kim, J. (2021). Goosecoid controls neuroectoderm specification via dual circuits of direct repression and indirect stimulation in Xenopus embryos. Mol. Cells 44, 723-735. https://doi.org/10.14348/molcells.2021.0055
- Vladar, E.K. and Stearns, T. (2007). Molecular characterization of centriole assembly in ciliated epithelial cells. J. Cell Biol. 178, 31-42. https://doi.org/10.1083/jcb.200703064
- Weibel, M., Pettmann, B., Artault, J., Sensenbrenner, M., and Labourdette, G. (1986). Primary culture of rat ependymal cells in serum-free defined medium. Brain Res. 25, 199-209. https://doi.org/10.1016/0165-3806(86)90209-9
- Winey, M. and O'Toole, E. (2014). Centriole structure. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130457.
- Wloga, D., Joachimiak, E., Louka, P., and Gaertig, J. (2017). Posttranslational modifications of tubulin and cilia. Cold Spring Harb. Perspect. Biol. 9, a028159.
- Zhao, H., Chen, Q., Fang, C., Huang, Q., Zhou, J., Yan, X., and Zhu, X. (2019). Parental centrioles are dispensable for deuterosome formation and function during basal body amplification. EMBO Rep. 20, e46735.
- Zhao, H., Zhu, L., Zhu, Y., Cao, J., Li, S., Huang, Q., Xu, T., Huang, X., Yan, X., and Zhu, X. (2013). The Cep63 paralogue Deup1 enables massive de novo centriole biogenesis for vertebrate multiciliogenesis. Nat. Cell Biol. 15, 1434-1444. https://doi.org/10.1038/ncb2880