Planar polarity pathway and Nance-Horan syndrome-like 1b have essential cell-autonomous functions in neuronal migration
Open Access
- 15 July 2011
- journal article
- Published by The Company of Biologists in Development
- Vol. 138 (14), 3033-3042
- https://doi.org/10.1242/dev.063842
Abstract
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.Keywords
This publication has 72 references indexed in Scilit:
- Epidermal Wound Repair Is Regulated by the Planar Cell Polarity Signaling PathwayDevelopmental Cell, 2010
- Prickle1b mediates interpretation of migratory cues during zebrafish facial branchiomotor neuron migrationDevelopmental Dynamics, 2010
- Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanismDevelopmental Biology, 2010
- A quest for the mechanism regulating global planar cell polarity of tissuesTrends in Cell Biology, 2009
- The cell adhesion molecule Tag1, transmembrane protein Stbm/Vangl2, and Lamininα1 exhibit genetic interactions during migration of facial branchiomotor neurons in zebrafishDevelopmental Biology, 2009
- Contact inhibition of locomotion in vivo controls neural crest directional migrationNature, 2008
- Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cellsNature Genetics, 2008
- Planar cell polarity: one or two pathways?Nature Reviews Genetics, 2007
- Identification of Vangl2 and Scrb1 as planar polarity genes in mammalsNature, 2003
- Stages of embryonic development of the zebrafishDevelopmental Dynamics, 1995