Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development.
Spontaneous Ca2+ transients of neural cells is a hallmark of the developing nervous system. It is widely accepted that chemical signals, like neurotransmitters, contribute to spontaneous Ca2+ transients in the nervous system. Here, we reveal an additional mechanism of spontaneous Ca2+ transients tha...
| Main Authors: | , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-09-01
|
| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002319&type=printable |
| _version_ | 1797326204340011008 |
|---|---|
| author | Jacob P Brandt Cody J Smith |
| author_facet | Jacob P Brandt Cody J Smith |
| author_sort | Jacob P Brandt |
| collection | DOAJ |
| description | Spontaneous Ca2+ transients of neural cells is a hallmark of the developing nervous system. It is widely accepted that chemical signals, like neurotransmitters, contribute to spontaneous Ca2+ transients in the nervous system. Here, we reveal an additional mechanism of spontaneous Ca2+ transients that is mechanosensitive in the peripheral nervous system (PNS) using intravital imaging of growing dorsal root ganglia (DRG) in zebrafish embryos. GCaMP6s imaging shows that developing DRG satellite glia contain distinct spontaneous Ca2+ transients, classified into simultaneous, isolated, and microdomains. Longitudinal analysis over days in development demonstrates that as DRG satellite glia become more synchronized, isolated Ca2+ transients remain constant. Using a chemical screen, we identify that Ca2+ transients in DRG glia are dependent on mechanical properties, which we confirmed using an experimental application of mechanical force. We find that isolated spontaneous Ca2+ transients of the glia during development is altered by manipulation of mechanosensitive protein Piezo1, which is expressed in the developing ganglia. In contrast, simultaneous Ca2+ transients of DRG satellite glia is not Piezo1-mediated, thus demonstrating that distinct mechanisms mediate subtypes of spontaneous Ca2+ transients. Activating Piezo1 eventually impacts the cell abundance of DRG cells and behaviors that are driven by DRG neurons. Together, our results reveal mechanistically distinct subtypes of Ca2+ transients in satellite glia and introduce mechanobiology as a critical component of spontaneous Ca2+ transients in the developing PNS. |
| first_indexed | 2024-03-08T06:20:05Z |
| format | Article |
| id | doaj.art-1cdc159d09834608aa1c9a00f951053e |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-03-08T06:20:05Z |
| publishDate | 2023-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-1cdc159d09834608aa1c9a00f951053e2024-02-04T05:30:29ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-09-01219e300231910.1371/journal.pbio.3002319Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development.Jacob P BrandtCody J SmithSpontaneous Ca2+ transients of neural cells is a hallmark of the developing nervous system. It is widely accepted that chemical signals, like neurotransmitters, contribute to spontaneous Ca2+ transients in the nervous system. Here, we reveal an additional mechanism of spontaneous Ca2+ transients that is mechanosensitive in the peripheral nervous system (PNS) using intravital imaging of growing dorsal root ganglia (DRG) in zebrafish embryos. GCaMP6s imaging shows that developing DRG satellite glia contain distinct spontaneous Ca2+ transients, classified into simultaneous, isolated, and microdomains. Longitudinal analysis over days in development demonstrates that as DRG satellite glia become more synchronized, isolated Ca2+ transients remain constant. Using a chemical screen, we identify that Ca2+ transients in DRG glia are dependent on mechanical properties, which we confirmed using an experimental application of mechanical force. We find that isolated spontaneous Ca2+ transients of the glia during development is altered by manipulation of mechanosensitive protein Piezo1, which is expressed in the developing ganglia. In contrast, simultaneous Ca2+ transients of DRG satellite glia is not Piezo1-mediated, thus demonstrating that distinct mechanisms mediate subtypes of spontaneous Ca2+ transients. Activating Piezo1 eventually impacts the cell abundance of DRG cells and behaviors that are driven by DRG neurons. Together, our results reveal mechanistically distinct subtypes of Ca2+ transients in satellite glia and introduce mechanobiology as a critical component of spontaneous Ca2+ transients in the developing PNS.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002319&type=printable |
| spellingShingle | Jacob P Brandt Cody J Smith Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development. PLoS Biology |
| title | Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development. |
| title_full | Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development. |
| title_fullStr | Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development. |
| title_full_unstemmed | Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development. |
| title_short | Piezo1-mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development. |
| title_sort | piezo1 mediated spontaneous calcium transients in satellite glia impact dorsal root ganglia development |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002319&type=printable |
| work_keys_str_mv | AT jacobpbrandt piezo1mediatedspontaneouscalciumtransientsinsatellitegliaimpactdorsalrootgangliadevelopment AT codyjsmith piezo1mediatedspontaneouscalciumtransientsinsatellitegliaimpactdorsalrootgangliadevelopment |