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Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish

BACKGROUND: Cerebrospinal fluid (CSF) contained within the brain ventricles contacts neuroepithelial progenitor cells during brain development. Dynamic properties of CSF movement may limit locally produced factors to specific regions of the developing brain. However, there is no study of in vivo CSF...

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Autores principales: Fame, Ryann M., Chang, Jessica T., Hong, Alex, Aponte-Santiago, Nicole A., Sive, Hazel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915066/
https://www.ncbi.nlm.nih.gov/pubmed/27329482
http://dx.doi.org/10.1186/s12987-016-0036-z
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author Fame, Ryann M.
Chang, Jessica T.
Hong, Alex
Aponte-Santiago, Nicole A.
Sive, Hazel
author_facet Fame, Ryann M.
Chang, Jessica T.
Hong, Alex
Aponte-Santiago, Nicole A.
Sive, Hazel
author_sort Fame, Ryann M.
collection PubMed
description BACKGROUND: Cerebrospinal fluid (CSF) contained within the brain ventricles contacts neuroepithelial progenitor cells during brain development. Dynamic properties of CSF movement may limit locally produced factors to specific regions of the developing brain. However, there is no study of in vivo CSF dynamics between ventricles in the embryonic brain. We address CSF movement using the zebrafish larva, during the major period of developmental neurogenesis. METHODS: CSF movement was monitored at two stages of zebrafish development: early larva [pharyngula stage; 27–30 h post-fertilization (hpf)] and late larva (hatching period; 51–54 hpf) using photoactivatable Kaede protein to calculate average maximum CSF velocity between ventricles. Potential roles for heartbeat in early CSF movement were investigated using tnnt2a mutant fish (tnnt2a(−/−)) and chemical [2,3 butanedione monoxime (BDM)] treatment. Cilia motility was monitored at these stages using the Tg(βact:Arl13b–GFP) transgenic fish line. RESULTS: In wild-type early larva there is net CSF movement from the telencephalon to the combined diencephalic/mesencephalic superventricle. This movement directionality reverses at late larval stage. CSF moves directionally from diencephalic to rhombencephalic ventricles at both stages examined, with minimal movement from rhombencephalon to diencephalon. Directional movement is partially dependent on heartbeat, as indicated in assays of tnnt2a(−/−) fish and after BDM treatment. Brain cilia are immotile at the early larval stage. CONCLUSION: These data demonstrate directional movement of the embryonic CSF in the zebrafish model during the major period of developmental neurogenesis. A key conclusion is that CSF moves preferentially from the diencephalic into the rhombencephalic ventricle. In addition, the direction of CSF movement between telencephalic and diencephalic ventricles reverses between the early and late larval stages. CSF movement is partially dependent on heartbeat. At early larval stage, the absence of motile cilia indicates that cilia likely do not direct CSF movement. These data suggest that CSF components may be compartmentalized and could contribute to specialization of the early brain. In addition, CSF movement may also provide directional mechanical signaling. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12987-016-0036-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-49150662016-06-22 Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish Fame, Ryann M. Chang, Jessica T. Hong, Alex Aponte-Santiago, Nicole A. Sive, Hazel Fluids Barriers CNS Research BACKGROUND: Cerebrospinal fluid (CSF) contained within the brain ventricles contacts neuroepithelial progenitor cells during brain development. Dynamic properties of CSF movement may limit locally produced factors to specific regions of the developing brain. However, there is no study of in vivo CSF dynamics between ventricles in the embryonic brain. We address CSF movement using the zebrafish larva, during the major period of developmental neurogenesis. METHODS: CSF movement was monitored at two stages of zebrafish development: early larva [pharyngula stage; 27–30 h post-fertilization (hpf)] and late larva (hatching period; 51–54 hpf) using photoactivatable Kaede protein to calculate average maximum CSF velocity between ventricles. Potential roles for heartbeat in early CSF movement were investigated using tnnt2a mutant fish (tnnt2a(−/−)) and chemical [2,3 butanedione monoxime (BDM)] treatment. Cilia motility was monitored at these stages using the Tg(βact:Arl13b–GFP) transgenic fish line. RESULTS: In wild-type early larva there is net CSF movement from the telencephalon to the combined diencephalic/mesencephalic superventricle. This movement directionality reverses at late larval stage. CSF moves directionally from diencephalic to rhombencephalic ventricles at both stages examined, with minimal movement from rhombencephalon to diencephalon. Directional movement is partially dependent on heartbeat, as indicated in assays of tnnt2a(−/−) fish and after BDM treatment. Brain cilia are immotile at the early larval stage. CONCLUSION: These data demonstrate directional movement of the embryonic CSF in the zebrafish model during the major period of developmental neurogenesis. A key conclusion is that CSF moves preferentially from the diencephalic into the rhombencephalic ventricle. In addition, the direction of CSF movement between telencephalic and diencephalic ventricles reverses between the early and late larval stages. CSF movement is partially dependent on heartbeat. At early larval stage, the absence of motile cilia indicates that cilia likely do not direct CSF movement. These data suggest that CSF components may be compartmentalized and could contribute to specialization of the early brain. In addition, CSF movement may also provide directional mechanical signaling. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12987-016-0036-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-21 /pmc/articles/PMC4915066/ /pubmed/27329482 http://dx.doi.org/10.1186/s12987-016-0036-z Text en © The Author(s) 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Fame, Ryann M.
Chang, Jessica T.
Hong, Alex
Aponte-Santiago, Nicole A.
Sive, Hazel
Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
title Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
title_full Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
title_fullStr Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
title_full_unstemmed Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
title_short Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
title_sort directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915066/
https://www.ncbi.nlm.nih.gov/pubmed/27329482
http://dx.doi.org/10.1186/s12987-016-0036-z
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