Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain
Summary: Motile cilia defects impair cerebrospinal fluid (CSF) flow and can cause brain and spine disorders. The development of ciliated cells, their impact on CSF flow, and their function in brain and axial morphogenesis are not fully understood. We have characterized motile ciliated cells within t...
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Elsevier
2021-10-01
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Series: | Cell Reports |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124721012298 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Percival P. D’Gama Tao Qiu Mehmet Ilyas Cosacak Dheeraj Rayamajhi Ahsen Konac Jan Niklas Hansen Christa Ringers Francisca Acuña-Hinrichsen Subhra P. Hui Emilie W. Olstad Yan Ling Chong Charlton Kang An Lim Astha Gupta Chee Peng Ng Benedikt S. Nilges Nachiket D. Kashikar Dagmar Wachten David Liebl Kazu Kikuchi Caghan Kizil Emre Yaksi Sudipto Roy Nathalie Jurisch-Yaksi |
spellingShingle |
Percival P. D’Gama Tao Qiu Mehmet Ilyas Cosacak Dheeraj Rayamajhi Ahsen Konac Jan Niklas Hansen Christa Ringers Francisca Acuña-Hinrichsen Subhra P. Hui Emilie W. Olstad Yan Ling Chong Charlton Kang An Lim Astha Gupta Chee Peng Ng Benedikt S. Nilges Nachiket D. Kashikar Dagmar Wachten David Liebl Kazu Kikuchi Caghan Kizil Emre Yaksi Sudipto Roy Nathalie Jurisch-Yaksi Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain Cell Reports cilia multiciliated cells foxj1 gmnc ependymal cell zebrafish |
author_facet |
Percival P. D’Gama Tao Qiu Mehmet Ilyas Cosacak Dheeraj Rayamajhi Ahsen Konac Jan Niklas Hansen Christa Ringers Francisca Acuña-Hinrichsen Subhra P. Hui Emilie W. Olstad Yan Ling Chong Charlton Kang An Lim Astha Gupta Chee Peng Ng Benedikt S. Nilges Nachiket D. Kashikar Dagmar Wachten David Liebl Kazu Kikuchi Caghan Kizil Emre Yaksi Sudipto Roy Nathalie Jurisch-Yaksi |
author_sort |
Percival P. D’Gama |
title |
Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain |
title_short |
Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain |
title_full |
Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain |
title_fullStr |
Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain |
title_full_unstemmed |
Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain |
title_sort |
diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain |
publisher |
Elsevier |
series |
Cell Reports |
issn |
2211-1247 |
publishDate |
2021-10-01 |
description |
Summary: Motile cilia defects impair cerebrospinal fluid (CSF) flow and can cause brain and spine disorders. The development of ciliated cells, their impact on CSF flow, and their function in brain and axial morphogenesis are not fully understood. We have characterized motile ciliated cells within the zebrafish brain ventricles. We show that the ventricles undergo restructuring through development, involving a transition from mono- to multiciliated cells (MCCs) driven by gmnc. MCCs co-exist with monociliated cells and generate directional flow patterns. These ciliated cells have different developmental origins and are genetically heterogenous with respect to expression of the Foxj1 family of ciliary master regulators. Finally, we show that cilia loss from the tela choroida and choroid plexus or global perturbation of multiciliation does not affect overall brain or spine morphogenesis but results in enlarged ventricles. Our findings establish that motile ciliated cells are generated by complementary and sequential transcriptional programs to support ventricular development. |
topic |
cilia multiciliated cells foxj1 gmnc ependymal cell zebrafish |
url |
http://www.sciencedirect.com/science/article/pii/S2211124721012298 |
work_keys_str_mv |
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doaj-1dd717feda074446b65e421f9b70e01f2021-10-07T04:24:54ZengElsevierCell Reports2211-12472021-10-01371109775Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brainPercival P. D’Gama0Tao Qiu1Mehmet Ilyas Cosacak2Dheeraj Rayamajhi3Ahsen Konac4Jan Niklas Hansen5Christa Ringers6Francisca Acuña-Hinrichsen7Subhra P. Hui8Emilie W. Olstad9Yan Ling Chong10Charlton Kang An Lim11Astha Gupta12Chee Peng Ng13Benedikt S. Nilges14Nachiket D. Kashikar15Dagmar Wachten16David Liebl17Kazu Kikuchi18Caghan Kizil19Emre Yaksi20Sudipto Roy21Nathalie Jurisch-Yaksi22Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Erling Skjalgsons Gate 1, 7491 Trondheim, Norway; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, NorwayInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, SingaporeGerman Center for Neurodegenerative Diseases (DZNE), Helmholtz Association, Tatzberg 41, 01307 Dresden, GermanyInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore; Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, SingaporeKavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, NorwayInstitute of Innate Immunity, Biophysical Imaging, Medical Faculty, University of Bonn, 53127 Bonn, GermanyDepartment of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Erling Skjalgsons Gate 1, 7491 Trondheim, Norway; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, NorwayKavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, NorwayS. N. Pradhan Centre for Neurosciences, University of Calcutta, 35 Ballygunge Circular Road, Kolkata 700 019, IndiaKavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, NorwayInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, SingaporeInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, SingaporeResolve Biosciences GmbH, Creative Campus Monheim, Gebäude A03, Alfred-Nobel-Str.10, 40789 Monheim am Rhein, GermanyA∗STAR Microscopy Platform, Research Support Center, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, SingaporeResolve Biosciences GmbH, Creative Campus Monheim, Gebäude A03, Alfred-Nobel-Str.10, 40789 Monheim am Rhein, GermanyResolve Biosciences GmbH, Creative Campus Monheim, Gebäude A03, Alfred-Nobel-Str.10, 40789 Monheim am Rhein, GermanyInstitute of Innate Immunity, Biophysical Imaging, Medical Faculty, University of Bonn, 53127 Bonn, GermanyA∗STAR Microscopy Platform, Research Support Center, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, SingaporeDepartment of Regenerative Medicine and Tissue Engineering, National Cerebral and Cardiovascular Center Research Institute, 6-1 Kishibe-Shimmachi, Suita, Osaka 564-8565, JapanGerman Center for Neurodegenerative Diseases (DZNE), Helmholtz Association, Tatzberg 41, 01307 Dresden, Germany; Department of Neurology and The Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Vagelos College of Physicians and Surgeons, Columbia University Irving Medical Center, 650 W 168th St, New York, NY 10032, USAKavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, NorwayInstitute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore; Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Singapore; Department of Pediatrics, Yong Loo Lin School of Medicine, National University of Singapore, 1E Kent Ridge Road, Singapore 119288, Singapore; Corresponding authorDepartment of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Erling Skjalgsons Gate 1, 7491 Trondheim, Norway; Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, Norway; Corresponding authorSummary: Motile cilia defects impair cerebrospinal fluid (CSF) flow and can cause brain and spine disorders. The development of ciliated cells, their impact on CSF flow, and their function in brain and axial morphogenesis are not fully understood. We have characterized motile ciliated cells within the zebrafish brain ventricles. We show that the ventricles undergo restructuring through development, involving a transition from mono- to multiciliated cells (MCCs) driven by gmnc. MCCs co-exist with monociliated cells and generate directional flow patterns. These ciliated cells have different developmental origins and are genetically heterogenous with respect to expression of the Foxj1 family of ciliary master regulators. Finally, we show that cilia loss from the tela choroida and choroid plexus or global perturbation of multiciliation does not affect overall brain or spine morphogenesis but results in enlarged ventricles. Our findings establish that motile ciliated cells are generated by complementary and sequential transcriptional programs to support ventricular development.http://www.sciencedirect.com/science/article/pii/S2211124721012298ciliamulticiliated cellsfoxj1gmncependymal cellzebrafish |