Planar polarity pathway and Nance-Horan syndrome-like 1b have essential cell-autonomous functions in neuronal migration
Open accessAbstract
Components of the planar cell polarity (PCP) pathway are required for the caudal tangential migration of facial branchiomotor (FBM) neurons, but how PCP signaling regulates this migration is not understood. In a forward genetic screen, we identified a new gene, nhsl1b, required for FBM neuron migration. nhsl1b encodes a WAVE-homology domain-containing protein related to human Nance-Horan syndrome (NHS) protein and Drosophila GUK-holder (Gukh), which have been shown to interact with components of the WAVE regulatory complex that controls cytoskeletal dynamics and with the polarity protein Scribble, respectively. Nhsl1b localizes to FBM neuron membrane protrusions and interacts physically and genetically with Scrib to control FBM neuron migration. Using chimeric analysis, we show that FBM neurons have two modes of migration: one involving interactions between the neurons and their planar-polarized environment, and an alternative, collective mode involving interactions between the neurons themselves. We demonstrate that the first mode of migration requires the cell-autonomous functions of Nhsl1b and the PCP components Scrib and Vangl2 in addition to the non-autonomous functions of Scrib and Vangl2, which serve to polarize the epithelial cells in the environment of the migrating neurons. These results define a role for Nhsl1b as a neuronal effector of PCP signaling and indicate that proper FBM neuron migration is directly controlled by PCP signaling between the epithelium and the migrating neurons.
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Scribble and Vangl have collaborative roles in PCP in diverse other mouse tissues, mediating axon guidance in the hindbrain and heart looping and subsequent cardiac development.
“Subsequently, collaborative roles for Scribble and Vangl in PCP were uncovered in diverse other mouse tissues, mediating axon guidance in the hindbrain (Walsh et al., 2011) and heart looping and subsequent cardiac development (Phillips et al., 2007).”
From Scribble: A master scaffold in polarity, adhesion, synaptogenesis, and proliferation (2019) · cites this paper as Walsh et al., 2011
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- Authors
- Walsh, G. S., Grant, P. K., Morgan, J. A., & Moens, C. B.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Moens, Cecilia B.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2011-07-15
- Volume
- 138
- Issue
- 14
- Pages
- 3033-3042
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC3119310
- OpenAlex
- W2072660071
- Cited by
- 57
- References
- 70
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 5 · 2017: 5 · 2016: 4 · 2015: 3 · 2014: 5 · 2013: 8 · 2012: 7
- FWCI
- 2.85
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Development (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Human Genome Research Institute (R01HG002995)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD037909)
- 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 › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Keywords
- planar cell polarity pathway, Nance-Horan syndrome, neuronal migration, Scribble, Vangl2, WAVE regulatory complex, collective migration, epithelial polarity, chimeric analysis
- MeSH terms
- Animals, Cell Movement, Cells, Cultured, Facial Nerve, Immunohistochemistry, Membrane Proteins, Neurons, Plasmids, Zebrafish, Signal Transduction, Mutagenesis, In Situ Hybridization, Zebrafish Proteins, Animals, Genetically Modified, Immunoprecipitation
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