Zebrafish neural tube morphogenesis requires Scribble-dependent oriented cell divisions
Open accessAbstract
How control of subcellular events in single cells determines morphogenesis on the scale of the tissue is largely unresolved. The stereotyped cross-midline mitoses of progenitors in the zebrafish neural keel provide a unique experimental paradigm for defining the role and control of single-cell orientation for tissue-level morphogenesis in vivo. We show here that the coordinated orientation of individual progenitor cell division in the neural keel is the cellular determinant required for morphogenesis into a neural tube epithelium with a single straight lumen. We find that Scribble is required for oriented cell division and that its function in this process is independent of canonical apicobasal and planar polarity pathways. We identify a role for Scribble in controlling clustering of α-catenin foci in dividing progenitors. Loss of either Scrib or N-cadherin results in abnormally oriented mitoses, reduced cross-midline cell divisions, and similar neural tube defects. We propose that Scribble-dependent nascent cell-cell adhesion clusters between neuroepithelial progenitors contribute to define orientation of their cell division. Finally, our data demonstrate that while oriented mitoses of individual cells determine neural tube architecture, the tissue can in turn feed back on its constituent cells to define their polarization and cell division orientation to ensure robust tissue morphogenesis.
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In zebrafish, most cell divisions are parallel to the epithelial sheet, but during the neural keel/rod phase, mitotic spindles rotate 90° to be perpendicular to it.
“Most cell divisions are parallel to the epithelial sheet, but during the neural keel/rod phase, this changes (Geldmacher-Voss et al., 2003; Žigman et al., 2011). Mitotic spindles set up parallel to the epithelial sheet, but then rotate 90° to be perpendicular to it.”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Žigman et al., 2011
Spindle orientation becomes randomized in scribble mutants, and bilateral positioning of daughter cells is lost.
“Spindle orientation becomes randomized in scribble mutants, and thus bilateral positioning of daughter cells is lost (Žigman et al., 2011).”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Žigman et al., 2011
Scribble is required for cortical localization of the cadherin-catenin complex, and N-cadherin knockdown phenocopies Scribble loss.
“Instead, Scribble is required for cortical localization of the cadherin–catenin complex, and N-cadherin knockdown phenocopies Scribble loss.”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Žigman et al., 2011
This spindle orientation role does not require PCP or apical PAR proteins.
“Surprisingly, this does not require PCP or apical PAR proteins, both partners in other Scribble-mediated events.”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Žigman et al., 2011
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“Spindle orientation becomes randomized in scribble mutants, and thus bilateral positioning of daughter cells is lost (Žigman et al., 2011).”
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Scrib organizes cortical actomyosin clusters to maintain adherens junctions and angiogenic sprouting
Mayo, L. N., Duong, F. H. T., Mompeón, A., Jacobs, K. A., Iruela‐Arispe, M. L., & Kutys, M. L. (2026) · The Journal of Cell Biology · doi:10.1083/jcb.202503146 · Cited by 5 · see citing works
Viral subversion of the cell polarity regulator Scribble
Javorsky, A., Humbert, P. O., & Kvansakul, M. (2023) · Biochemical Society Transactions · doi:10.1042/bst20221067 · Cited by 5 · see citing works
Chann, A. S., Chen, Y., Kinwel, T., Humbert, P. O., & Russell, S. M. (2023) · Journal of Cell Science · doi:10.1242/jcs.260547 · Cited by 5 · see citing works
Stepwise modulation of apical orientational cell adhesions for vertebrate neurulation
Zhang, L., & Wei, X. (2023) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.13006 · Cited by 5 · see citing works
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Using Optogenetics to Investigate the Shared Mechanisms of Apical-Basal Polarity and Mitosis
Crellin, H. A., & Buckley, C. E. (2023) · Cells Tissues Organs · doi:10.1159/000528796 · Cited by 3 · see citing works
Planar Cell Polarity Pathway in Kidney Development and Function
Rocque, B., & Torban, E. (2015) · Advances in Nephrology · doi:10.1155/2015/764682 · Cited by 3 · see citing works
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A Scribble-E-cadherin complex controls daughter cell patterning by multiple mechanismsPreprint
Chann, A. S., Chen, Y., Kinwel, T., Humbert, P. O., & Russell, S. M. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.15.440081
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Rôle de la protéine tyrosine kinase 7 dans le cancer colorectal et la polarité planaire cellulaire
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The Scrib1 Interactome and its relevance for synaptic plasticity & neurodevelopmental disorders
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Dynein-microtubule forces drive nucleokinesis and transmigration in T cellsPreprint
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- Authors
- Žigman, M., Trinh, L. A., Fraser, S. E., & Moens, C. B.
- Affiliations
- Howard Hughes Medical Institute (US)
- California Institute of Technology (US)
- Corresponding author
- Žigman, Mihaela
- Moens, Cecilia B.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 21
- Issue
- 1
- Pages
- 79-86
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4308621
- OpenAlex
- W2051363634
- Cited by
- 71
- References
- 52
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 5 · 2022: 5 · 2021: 1 · 2019: 3 · 2018: 4 · 2017: 7 · 2016: 4 · 2015: 8 · 2014: 8 · 2013: 7 · 2012: 10
- FWCI
- 2.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Human Genome Research Institute (P50HG004071)
- National Institute of Neurological Disorders and Stroke (R01NS082567)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD37909, R01HD037909, R01HD076585)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Keywords
- neural tube morphogenesis, Scribble, oriented cell division, cell-cell adhesion, alpha-catenin, N-cadherin, cell polarity, tissue morphogenesis, zebrafish
- MeSH terms
- Animals, Membrane Proteins, Mitosis, Zebrafish, Gene Expression Regulation, Developmental, Zebrafish Proteins, Neural Tube
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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