Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons.
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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-04-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3000235 |
| _version_ | 1818936447151898624 |
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| author | Laura Desban Andrew Prendergast Julian Roussel Marion Rosello David Geny Claire Wyart Pierre-Luc Bardet |
| author_facet | Laura Desban Andrew Prendergast Julian Roussel Marion Rosello David Geny Claire Wyart Pierre-Luc Bardet |
| author_sort | Laura Desban |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-20T05:36:12Z |
| format | Article |
| id | doaj.art-f2c9f5fa740348fca1b34a0afe9efcee |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-20T05:36:12Z |
| publishDate | 2019-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-f2c9f5fa740348fca1b34a0afe9efcee2022-12-21T19:51:37ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-04-01174e300023510.1371/journal.pbio.3000235Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons.Laura DesbanAndrew PrendergastJulian RousselMarion RoselloDavid GenyClaire WyartPierre-Luc BardetMultiple 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.https://doi.org/10.1371/journal.pbio.3000235 |
| spellingShingle | Laura Desban Andrew Prendergast Julian Roussel Marion Rosello David Geny Claire Wyart Pierre-Luc Bardet Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons. PLoS Biology |
| title | Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons. |
| title_full | Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons. |
| title_fullStr | Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons. |
| title_full_unstemmed | Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons. |
| title_short | Regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons. |
| title_sort | regulation of the apical extension morphogenesis tunes the mechanosensory response of microvilliated neurons |
| url | https://doi.org/10.1371/journal.pbio.3000235 |
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