PUBLICATION

Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons

Authors
Desban, L., Prendergast, A., Roussel, J., Rosello, M., Geny, D., Wyart, C., Bardet, P.L.
ID
ZDB-PUB-190422-16
Date
2019
Source
PLoS Biology   17: e3000235 (Journal)
Registered Authors
Bardet, Pierre-Luc, Prendergast, Andrew, Wyart, Claire
Keywords
none
MeSH Terms
  • Cerebrospinal Fluid/physiology
  • Spinal Cord/metabolism
  • Cell Differentiation
  • Neurons/physiology
  • Microvilli/physiology*
  • Sensory Receptor Cells/physiology*
  • Zebrafish/metabolism
  • Cell Surface Extensions/physiology
  • Mechanotransduction, Cellular/physiology*
  • Actins/metabolism
  • Morphogenesis/physiology
  • Animals
(all 12)
PubMed
31002663 Full text @ PLoS Biol.
Abstract
Multiple types of microvilliated sensory cells exhibit an apical extension thought to be instrumental in the detection of sensory cues. The investigation of the mechanisms underlying morphogenesis of sensory apparatus is critical to understand the biology of sensation. Most of what we currently know comes from the study of the hair bundle of the inner ear sensory cells, but morphogenesis and function of other sensory microvilliated apical extensions remain poorly understood. We focused on spinal sensory neurons that contact the cerebrospinal fluid (CSF) through the projection of a microvilliated apical process in the central canal, referred to as cerebrospinal fluid-contacting neurons (CSF-cNs). CSF-cNs respond to pH and osmolarity changes as well as mechanical stimuli associated with changes of flow and tail bending. In vivo time-lapse imaging in zebrafish embryos revealed that CSF-cNs are atypical neurons that do not lose their apical attachment and form a ring of actin at the apical junctional complexes (AJCs) that they retain during differentiation. We show that the actin-based protrusions constituting the microvilliated apical extension arise and elongate from this ring of actin, and we identify candidate molecular factors underlying every step of CSF-cN morphogenesis. We demonstrate that Crumbs 1 (Crb1), Myosin 3b (Myo3b), and Espin orchestrate the morphogenesis of CSF-cN apical extension. Using calcium imaging in crb1 and espin mutants, we further show that the size of the apical extension modulates the amplitude of CSF-cN sensory response to bending of the spinal cord. Based on our results, we propose that the apical actin ring could be a common site of initiation of actin-based protrusions in microvilliated sensory cells. Furthermore, our work provides a set of actors underlying actin-based protrusion elongation shared by different sensory cell types and highlights the critical role of the apical extension shape in sensory detection.
Genes / Markers
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Mutations / Transgenics
Allele Construct Type Affected Genomic Region
icm07TgTransgenic Insertion
    icm08TgTransgenic Insertion
      icm10TgTransgenic Insertion
        icm17TgTransgenic Insertion
          icm22TgTransgenic Insertion
            icm26
              Small Deletion
              icm28TgTransgenic Insertion
                icm31
                  Small Deletion
                  icm63TgTransgenic Insertion
                    s1020tEtTransgenic Insertion
                      1 - 10 of 11
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                      Human Disease / Model
                      No data available
                      Sequence Targeting Reagents
                      Target Reagent Reagent Type
                      crb1CRISPR1-crb1CRISPR
                      espnCRISPR3-espnCRISPR
                      1 - 2 of 2
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                      Fish
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                      Orthology
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                      Engineered Foreign Genes
                      Marker Marker Type Name
                      ECFPEFGECFP
                      EGFPEFGEGFP
                      GAL4EFGGAL4
                      GCaMPEFGGCaMP
                      GFPEFGGFP
                      mCherryEFGmCherry
                      TagRFPEFGTagRFP
                      VenusEFGVenus
                      1 - 8 of 8
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                      Mapping
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