Cell Reports (Oct 2021)
Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain
- 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
Affiliations
- Percival P. D’Gama
- Department 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
- Tao Qiu
- Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore
- Mehmet Ilyas Cosacak
- German Center for Neurodegenerative Diseases (DZNE), Helmholtz Association, Tatzberg 41, 01307 Dresden, Germany
- Dheeraj Rayamajhi
- Institute 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
- Ahsen Konac
- Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, Norway
- Jan Niklas Hansen
- Institute of Innate Immunity, Biophysical Imaging, Medical Faculty, University of Bonn, 53127 Bonn, Germany
- Christa Ringers
- Department 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
- Francisca Acuña-Hinrichsen
- Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, Norway
- Subhra P. Hui
- S. N. Pradhan Centre for Neurosciences, University of Calcutta, 35 Ballygunge Circular Road, Kolkata 700 019, India
- Emilie W. Olstad
- Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, Norway
- Yan Ling Chong
- Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore
- Charlton Kang An Lim
- Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore
- Astha Gupta
- Resolve Biosciences GmbH, Creative Campus Monheim, Gebäude A03, Alfred-Nobel-Str.10, 40789 Monheim am Rhein, Germany
- Chee Peng Ng
- A∗STAR Microscopy Platform, Research Support Center, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore
- Benedikt S. Nilges
- Resolve Biosciences GmbH, Creative Campus Monheim, Gebäude A03, Alfred-Nobel-Str.10, 40789 Monheim am Rhein, Germany
- Nachiket D. Kashikar
- Resolve Biosciences GmbH, Creative Campus Monheim, Gebäude A03, Alfred-Nobel-Str.10, 40789 Monheim am Rhein, Germany
- Dagmar Wachten
- Institute of Innate Immunity, Biophysical Imaging, Medical Faculty, University of Bonn, 53127 Bonn, Germany
- David Liebl
- A∗STAR Microscopy Platform, Research Support Center, Agency for Science, Technology and Research, 61 Biopolis Drive, Singapore 138673, Singapore
- Kazu Kikuchi
- Department of Regenerative Medicine and Tissue Engineering, National Cerebral and Cardiovascular Center Research Institute, 6-1 Kishibe-Shimmachi, Suita, Osaka 564-8565, Japan
- Caghan Kizil
- German 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, USA
- Emre Yaksi
- Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Olav Kyrres Gate 9, 7030 Trondheim, Norway
- Sudipto Roy
- Institute 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 author
- Nathalie Jurisch-Yaksi
- Department 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 author
- Journal volume & issue
-
Vol. 37,
no. 1
p. 109775
Abstract
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.
