Notochord vacuoles absorb compressive bone growth during zebrafish spine formation
The vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single fluid-filled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine kinking. Here, we identified a mutation in the ki...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2020-01-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/51221 |
| _version_ | 1811199420735160320 |
|---|---|
| author | Jennifer Bagwell James Norman Kathryn Ellis Brianna Peskin James Hwang Xiaoyan Ge Stacy V Nguyen Sarah K McMenamin Didier YR Stainier Michel Bagnat |
| author_facet | Jennifer Bagwell James Norman Kathryn Ellis Brianna Peskin James Hwang Xiaoyan Ge Stacy V Nguyen Sarah K McMenamin Didier YR Stainier Michel Bagnat |
| author_sort | Jennifer Bagwell |
| collection | DOAJ |
| description | The vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single fluid-filled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine kinking. Here, we identified a mutation in the kinase gene dstyk that causes fragmentation of notochord vacuoles and a severe congenital scoliosis-like phenotype in zebrafish. Live imaging revealed that Dstyk regulates fusion of membranes with the vacuole. We find that localized disruption of notochord vacuoles causes vertebral malformation and curving of the spine axis at those sites. Accordingly, in dstyk mutants the spine curves increasingly over time as vertebral bone formation compresses the notochord asymmetrically, causing vertebral malformations and kinking of the axis. Together, our data show that notochord vacuoles function as a hydrostatic scaffold that guides symmetrical growth of vertebrae and spine formation. |
| first_indexed | 2024-04-12T01:49:02Z |
| format | Article |
| id | doaj.art-12c8e29646ff4dbe997ba1938d110d88 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T01:49:02Z |
| publishDate | 2020-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-12c8e29646ff4dbe997ba1938d110d882022-12-22T03:53:00ZengeLife Sciences Publications LtdeLife2050-084X2020-01-01910.7554/eLife.51221Notochord vacuoles absorb compressive bone growth during zebrafish spine formationJennifer Bagwell0https://orcid.org/0000-0002-8873-0897James Norman1Kathryn Ellis2Brianna Peskin3James Hwang4Xiaoyan Ge5Stacy V Nguyen6https://orcid.org/0000-0002-2641-3984Sarah K McMenamin7https://orcid.org/0000-0002-1154-5810Didier YR Stainier8https://orcid.org/0000-0002-0382-0026Michel Bagnat9https://orcid.org/0000-0002-3829-0168Department of Cell Biology, Duke University, Durham, United StatesDepartment of Cell Biology, Duke University, Durham, United StatesDepartment of Cell Biology, Duke University, Durham, United StatesDepartment of Cell Biology, Duke University, Durham, United StatesDepartment of Cell Biology, Duke University, Durham, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesBiology Department, Boston College, Boston, United StatesBiology Department, Boston College, Boston, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United States; Max Planck Institute for Heart and Lung Research, Bad Nauheim, GermanyDepartment of Cell Biology, Duke University, Durham, United StatesThe vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single fluid-filled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine kinking. Here, we identified a mutation in the kinase gene dstyk that causes fragmentation of notochord vacuoles and a severe congenital scoliosis-like phenotype in zebrafish. Live imaging revealed that Dstyk regulates fusion of membranes with the vacuole. We find that localized disruption of notochord vacuoles causes vertebral malformation and curving of the spine axis at those sites. Accordingly, in dstyk mutants the spine curves increasingly over time as vertebral bone formation compresses the notochord asymmetrically, causing vertebral malformations and kinking of the axis. Together, our data show that notochord vacuoles function as a hydrostatic scaffold that guides symmetrical growth of vertebrae and spine formation.https://elifesciences.org/articles/51221notochordvacuolated cellsvertebrascoliosisdstykspine |
| spellingShingle | Jennifer Bagwell James Norman Kathryn Ellis Brianna Peskin James Hwang Xiaoyan Ge Stacy V Nguyen Sarah K McMenamin Didier YR Stainier Michel Bagnat Notochord vacuoles absorb compressive bone growth during zebrafish spine formation eLife notochord vacuolated cells vertebra scoliosis dstyk spine |
| title | Notochord vacuoles absorb compressive bone growth during zebrafish spine formation |
| title_full | Notochord vacuoles absorb compressive bone growth during zebrafish spine formation |
| title_fullStr | Notochord vacuoles absorb compressive bone growth during zebrafish spine formation |
| title_full_unstemmed | Notochord vacuoles absorb compressive bone growth during zebrafish spine formation |
| title_short | Notochord vacuoles absorb compressive bone growth during zebrafish spine formation |
| title_sort | notochord vacuoles absorb compressive bone growth during zebrafish spine formation |
| topic | notochord vacuolated cells vertebra scoliosis dstyk spine |
| url | https://elifesciences.org/articles/51221 |
| work_keys_str_mv | AT jenniferbagwell notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT jamesnorman notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT kathrynellis notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT briannapeskin notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT jameshwang notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT xiaoyange notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT stacyvnguyen notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT sarahkmcmenamin notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT didieryrstainier notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation AT michelbagnat notochordvacuolesabsorbcompressivebonegrowthduringzebrafishspineformation |