Zebrafish cerebrospinal fluid mediates cell survival through a retinoid signaling pathway

Chang, Jessica T.; Lehtinen, Maria K.; Sive, Hazel

doi:10.1002/dneu.22300

Cited by 46Cerebrospinal fluid and hydrocephalusZebrafish Biomedical Research ApplicationsNeurogenesis and neuroplasticity mechanisms

Zebrafish cerebrospinal fluid mediates cell survival through a retinoid signaling pathway

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Chang, Jessica T., Lehtinen, Maria K., Sive, Hazel·2016·Developmental Neurobiology

DOI 10.1002/dneu.22300PMC PMC4644717

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Abstract

Cerebrospinal fluid (CSF) includes conserved factors whose function is largely unexplored. To assess the role of CSF during embryonic development, CSF was repeatedly drained from embryonic zebrafish brain ventricles soon after their inflation. Removal of CSF increased cell death in the diencephalon, indicating a survival function. Factors within the CSF are required for neuroepithelial cell survival as injected mouse CSF but not artificial CSF could prevent cell death after CSF depletion. Mass spectrometry analysis of the CSF identified retinol binding protein 4 (Rbp4), which transports retinol, the precursor to retinoic acid (RA). Consistent with a role for Rbp4 in cell survival, inhibition of Rbp4 or RA synthesis increased neuroepithelial cell death. Conversely, ventricle injection of exogenous human RBP4 plus retinol, or RA alone prevented cell death after CSF depletion. Zebrafish rbp4 is highly expressed in the yolk syncytial layer, suggesting Rbp4 protein and retinol/RA precursors can be transported into the CSF from the yolk. In accord with this suggestion, injection of human RBP4 protein into the yolk prevents neuroepithelial cell death in rbp4 loss-of-function embryos. Together, these data support the model that Rbp4 and RA precursors are present within the CSF and used for synthesis of RA, which promotes embryonic neuroepithelial survival.

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4V ChP fibroblasts expressed high levels of genes encoding signaling molecules with roles in hindbrain development.
“4V ChP fibroblasts also expressed high levels of genes encoding signaling molecules with roles in hindbrain development (e.g., Hhip (Chuang and McMahon, 1999), Ptch1 (Huang et al., 2009), Rbp4 (Chang et al., 2016), and Wisp1 (Lun et al., 2015a, Figure 4B, S4D).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Chang et al., 2016

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BackgroundInfluential
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BackgroundInfluential
Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos
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BackgroundMethodResultInfluential
Retinoid Content, Visual Responses, and Ocular Morphology Are Compromised in the Retinas of Mice Lacking the Retinol-Binding Protein Receptor, STRA6
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Background
Retinoic Acid Functions as a Key GABAergic Differentiation Signal in the Basal Ganglia
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BackgroundInfluential
Retinoic Acid Signaling Identifies a Distinct Precursor Population in the Developing and Adult Forebrain
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Background
Identification and Characterization of a Non-retinoid Ligand for Retinol-binding Protein 4 Which Lowers Serum Retinol-binding Protein 4 Levels in Vivo
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Background
Retinoic Acid Receptor-Dependent Survival of Olfactory Sensory Neurons in Postnatal and Adult Mice
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Epidermal transient down‐regulation of retinol ‐ binding protein 4 and mirror expression of apolipoprotein Eb and estrogen receptor 2a during zebrafish fin and scale development
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Cerebrospinal fluid control of neurogenesis induced by retinoic acid during early brain development
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BackgroundInfluential
The homeobox geneGsh2is required for retinoid production in the embryonic mouse telencephalon
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“Abnormal RA signaling disrupts embryonic patterning, neuronal plasticity, differentiation, regeneration, learning, and memory (Sive et al., 1990; Krezel et al., 1998; Waclaw et al., 2004; Maden, 2007).”
Background
Flat Mount Preparation for Observation and Analysis of Zebrafish Embryo Specimens Stained by Whole Mount In situ Hybridization
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“Stained embryos were flat-mounted as previously described (Cheng et al., 2014) and imaged using the 253 or 633 oil objective on a Zeiss 710 scanning confocal microscope.”
Method
Multiple roles for the Na,K-ATPase subunits, Atp1a1 and Fxyd1, during brain ventricle development
Chang, J. T., Lowery, L. A., & Sive, H. L. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.05.034 · Cited by 46 · cited 1× · see citing works
“The zebrafish is an ideal system to define the mechanisms underlying CSF function during brain development (Lowery and Sive, 2005; Gutzman and Sive, 2009; Chang et al., 2012).”
Background
Embryonic cerebrospinal fluid collaborates with the isthmic organizer to regulate mesencephalic gene expression
Parada, C., Martín, C., Alonso, M. I., Moro, J. A., Bueno, D., & Gato, A. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20618 · Cited by 45 · cited 2× · see citing works
“These studies suggest that secreted factors within the CSF, hydrostatic pressure, or a combination of the two are required for gene expression, cell proliferation, survival, and neurogenesis (Desmond et al., 2005; Gato et al., 2005; Parada et al., 2005; Mashayekhi and Salehi, 2006a,b; Miyan et al., 2006; Salehi and Ma…”
Background
All-trans retinol and retinol-binding protein from embryonic cerebrospinal fluid exhibit dynamic behaviour during early central nervous system development
Parada, C., Gato, A., & Bueno, D. (2008) · Neuroreport · doi:10.1097/wnr.0b013e3283021c94 · Cited by 44 · cited 4× · see citing works
“While Rbp4 and retinol have previously been identified within the CSF (Zappaterra et al., 2007; Parada et al., 2008; Alonso et al., 2011), the source has remained unknown.”
BackgroundInfluential
Localized rbp4expression in the yolk syncytial layer plays a role in yolk cell extension and early liver development
Li, Z., Korzh, V. P., & Gong, Z. (2007) · BMC Developmental Biology · doi:10.1186/1471-213x-7-117 · Cited by 40 · cited 8× · see citing works
“RBP4 can Prevent Neuroepithelial Cell Death after Injection into the Yolk Zebrafish rbp4 is highly expressed at 24 hpf in the yolk syncytial layer, a transient extraembryonic syncytial tissue (Li et al., 2007) but not significantly in the neuroepithelium.”
BackgroundMethodInfluential
Investigation of retinoic acid function during embryonic brain development using retinaldehyde‐rescued Rdh10 knockout mice
Chatzi, C. A., Cunningham, T. J., & Duester, G. (2013) · Developmental Dynamics · doi:10.1002/dvdy.23999 · Cited by 34 · cited 4× · see citing works
“…of RA is from the meninges, which are the protective layers surrounding the brain (Siegenthaler et al., 2009; Siegenthaler and Pleasure, 2011), the choroid plexus (Yamamoto et al., 1996; Lun et al., 2015) or the ventricular cells adjacent to the CSF (Chatzi et al., 2011; Chatzi et al., 2013).”
BackgroundInfluential
A blood–CSF barrier function controls embryonic CSF protein composition and homeostasis during early CNS development
Parvas, M., Parada, C., & Bueno, D. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.05.552 · Cited by 34 · see citing works
Adult cerebrospinal fluid inhibits neurogenesis but facilitates gliogenesis from fetal rat neural stem cells
Buddensiek, J., Dressel, A., Kowalski, M., Storch, A., & Sabolek, M. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22150 · Cited by 32 · cited 1× · see citing works
“This is consistent with in vitro studies where application of CSF to human neural progenitor cell cultures or explanted chick neuroepithelium increased cell survival (Gato et al., 2005; Buddensiek et al., 2009).”
Result
Insulin-like growth factor-1 and insulin-like growth factor binding proteins in cerebrospinal fluid during the development of mouse embryos
Salehi, Z., Mashayekhi, F., Naji, M., & Pandamooz, S. (2009) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2008.09.018 · Cited by 31 · cited 2× · see citing works
“Insulin-like growth factor 2 (IGF2), retinoic acid (RA), fibroblast growth factor 2 (FGF2) and low-density lipoproteins were identified within mouse and/or chick CSF and, when applied to explanted chick or mouse neuroepithelium, could promote neurogenesis and cell proliferation (Martin et al., 2006; Parada et al., 200…”
Background
Low‐density lipoproteins from embryonic cerebrospinal fluid are required for neural differentiation
Parada, C., Escolá‐Gil, J. C., & Bueno, D. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21724 · Cited by 28 · cited 6× · see citing works
“While Rbp4 and retinol have previously been identified within the CSF (Zappaterra et al., 2007; Parada et al., 2008; Alonso et al., 2011), the source has remained unknown.”
BackgroundInfluential
The importance of cerebrospinal fluid on neural cell proliferation in developing chick cerebral cortex
Mashayekhi, F., & Salehi, Z. (2006) · European Journal of Neurology · doi:10.1111/j.1468-1331.2006.01208.x · Cited by 25 · see citing works
Immunodetection of protein composition in cerebral amyloid extracts in Alzheimer's disease: Enrichment of retinol-binding protein
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“…CSF depletion in the intact zebrafish is consistent with Developmental Neurobiology reports of increased cell death after a single CSF drainage from cultured chick embryos (Salehi and Mashayekhi, 2006) or in explanted chick neuroepithelium cultured in minimal growth media (Gato et al., 2005).”
BackgroundMethodInfluential
Cerebrospinal fluid nerve growth factor levels in patients with Alzheimer’s disease
Mashayekhi, F., & Salehi, Z. (2006) · Annals of Saudi Medicine · doi:10.5144/0256-4947.2006.278 · Cited by 17 · see citing works
Manual Drainage of the Zebrafish Embryonic Brain Ventricles
Chang, J. T., & Sive, H. L. (2012) · Journal of Visualized Experiments · doi:10.3791/4243 · Cited by 8 · cited 5× · see citing works
“CSF can be fully replenished after 2–3 hours (Chang and Sive, 2012), therefore, we drained CSF every two hours from 22–36 hpf [Fig.”
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Blood‚ÄìCSF Barrier in Iron Regulation and Manganese-Induced Parkinsonism
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Flagged first, then by citations

Research works printed but not linked: 1

Kimmel CB, Westerfield M. 1990 Primary neurons of the zebrafish. New York: Wiley.

Sorted by citations

Development and functions of the choroid plexus–cerebrospinal fluid system
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Emergence and Developmental Roles of the Cerebrospinal Fluid System
Fame, R. M., & Lehtinen, M. K. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.01.027 · Cited by 201 · see citing works
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The Reissner Fiber in the Cerebrospinal Fluid Controls Morphogenesis of the Body Axis
Cantaut-Belarif, Y., Sternberg, J. R., Thouvenin, O., Wyart, C., & Bardet, P. (2018) · Current Biology · doi:10.1016/j.cub.2018.05.079 · Cited by 134 · see citing works
“Our discovery of a critical role of the Reissner fiber in body morphogenesis provides a mechanistic explanation for the unresolved observation that CSF-drained zebrafish embryos develop a mild curled-down posterior axis [26].”
Progressive Differentiation and Instructive Capacities of Amniotic Fluid and Cerebrospinal Fluid Proteomes following Neural Tube Closure
Chau, K. F., Springel, M. W., Broadbelt, K. G., Park, H., Topal, S., Lun, M. P., Mullan, H., Maynard, T. M., Steen, H., LaMantia, A., et al. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.11.015 · Cited by 101 · see citing works
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D’Gama, P. P., Qiu, T., Coşacak, M. İ., Rayamajhi, D., Konac, A., Hansen, J. N., Ringers, C., Acuña, F., Hui, S. P., Olstad, E. W., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109775 · Cited by 84 · see citing works
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Thouvenin, O., Keiser, L., Cantaut-Belarif, Y., Tano, M. C., Verweij, F. J., Jurisch‐Yaksi, N., Bardet, P., van Niel, G., Gallaire, F., & Wyart, C. (2020) · eLife · doi:10.7554/elife.47699 · Cited by 87 · see citing works
“Bidirectional long-range transport of particles in the CC is accelerated by CSF flow We characterized above the local CSF flow in the CC, but did not investigate its ability to transport particles over long distances, despite its importance for embryonic development (Chang et al., 2016).”
Background
Extracellular Control of Radial Glia Proliferation and Scaffolding During Cortical Development and Pathology
Ferent, J., Zaidi, D., & Francis, F. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.578341 · Cited by 64 · see citing works
Brain Ventricular System and Cerebrospinal Fluid Development and Function: Light at the End of the Tube
Fame, R. M., Cortés‐Campos, C., & Sive, H. L. (2020) · BioEssays · doi:10.1002/bies.201900186 · Cited by 59 · see citing works
AP endonuclease 1 (Apex1) influences brain development linking oxidative stress and DNA repair
Pei, D., Jia, P., Luo, J., Liu, W., & Strauss, P. R. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1578-1 · Cited by 54 · see citing works
Directional cerebrospinal fluid movement between brain ventricles in larval zebrafish
Fame, R. M., Chang, J. T., Hong, A., Aponte-Santiago, N. A., & Sive, H. L. (2016) · Fluids and Barriers of the CNS · doi:10.1186/s12987-016-0036-z · Cited by 49 · see citing works
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Mohanty, R., Das, S. K., & Patri, M. (2017) · Neurotoxicity Research · doi:10.1007/s12640-016-9694-5 · Cited by 49 · see citing works
Choroid Plexus: The Orchestrator of Long-Range Signalling Within the CNS
Kaiser, K., & Bryja, V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134760 · Cited by 38 · see citing works
“A growing list of signalling molecules and growth factors identified in eCSF [5,27], provides compelling evidence explaining the disruption of CNS embryonic development observed as a consequence of CSF removal [28].”
Background
On being the right shape: Roles for motile cilia and cerebrospinal fluid flow in body and spine morphology
Bearce, E. A., & Grimes, D. T. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.07.005 · Cited by 34 · see citing works
Evolutionary development of embryonic cerebrospinal fluid composition and regulation: an open research field with implications for brain development and function
Bueno, D., & García‐Fernàndez, J. (2016) · Fluids and Barriers of the CNS · doi:10.1186/s12987-016-0029-y · Cited by 34 · see citing works
“Interestingly, a parallel situation has been described recently in zebrafish embryos [79].”
Background
New Insights Into the Roles of Retinoic Acid Signaling in Nervous System Development and the Establishment of Neurotransmitter Systems
Zieger, E., & Schubert, M. (2016) · International review of cytology · doi:10.1016/bs.ircmb.2016.09.001 · Cited by 31 · see citing works
Retinoic Acid Is Required for Oligodendrocyte Precursor Cell Production and Differentiation in the Postnatal Mouse Corpus Callosum
Morrison, V. E., Smith, V. N., & Huang, J. K. (2019) · eNeuro · doi:10.1523/eneuro.0270-19.2019 · Cited by 25 · see citing works
“In the CNS, oligodendrocytes (OLs) promote neuronal survival (Wilkins et al., 2003; Chang et al., 2016), regulate neuronal energy metabolism (Saab et al.”
Background
Embryonic cerebrospinal fluid formation and regulation
Bueno, D., Parvas, M., Nabiuni, M., & Miyan, J. A. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.09.006 · Cited by 23 · see citing works
Inhibition of NRF2 signaling and increased reactive oxygen species during embryogenesis in a rat model of retinoic acid-induced neural tube defects
Liu, D., Xue, J., Liu, Y., Gu, H., Wei, X., Ma, W., Luo, W., Ma, L., Jia, S., Dong, N., et al. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.09.005 · Cited by 21 · see citing works
Embryonic Zebrafish as a Model for Investigating the Interaction between Environmental Pollutants and Neurodegenerative Disorders
Yin, J., & Horzmann, K. A. (2024) · Biomedicines · doi:10.3390/biomedicines12071559 · Cited by 20 · see citing works
“At 48 hpf, the zebrafish brain ventricle forms [53].”
Background
Systematic Quantification of Neurotrophic Adipokines RBP4, PEDF, and Clusterin in Human Cerebrospinal Fluid and Serum
Höpfinger, A., Berghoff, M., Karrasch, T., Schmid, A., & Schäffler, A. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa983 · Cited by 19 · see citing works
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“For example, the HBV are cavities that contain cerebrospinal fluid, rich in hormones, proteoglycans, and ions (Lowery and Sive, 2005; Chang et al., 2016; Fame et al., 2016), the PVS is a sandwiched, avascular region between two malleable membranes surrounding the yolk (Nicoli and Presta, 2007), and the CHT is a compac…”
Background
Hedgehog Signaling in Cortical Development
Cai, E., Barba, M. G., & Ge, X. (2023) · Cells · doi:10.3390/cells13010021 · Cited by 13 · see citing works
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“Its traditionally assigned roles include providing a buoyant ﬂ uid cushion and pH and ion balance for the CNS. CSF also plays critical roles in regulating the CNS throughout life, including the distribution of essential health and growth-promotingfactors 42 – 47 .”
Dietary Zinc Intake Affects the Association Between Dietary Vitamin A and Depression: A Cross-Sectional Study
Hu, B., Lin, Z., Zou, R.-P., Gan, Y.-W., Ji, J., Guo, J.-X., Li, W., Guo, Y.-J., Xu, H.-Q., Sun, D., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.913132 · Cited by 7 · see citing works
“RBP4 can be transferred from the circulation system to the cerebro-spinal fluid and bind to retinol, thus facilitating the metabolism of retinol to retinoic acid in neuroepithelial cells (29).”
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Expression profiles of RA synthases and catabolic enzymes in newly hatched and metamorphosing larvae of Japanese flounder, Paralichthys olivaceus
Chen, Q., Yokoi, H., & Suzuki, T. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.08.015 · Cited by 3 · see citing works
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“…and other signaling molecules that regulate cell proliferation, differentiation, and survival in the developing nervous system. eCSF is also important for regulating the size and shape of the developing brain ventricles (Gato et al., 2014; Bueno and Garcia-Fernàndez, 2016; Chang et al., 2016).”
Background
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Sivaji, K., Kannan, R. R., Soundharapandiyan, N., Alphonse, C. R. W., & Saleem, S. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-04948-8 · Cited by 2 · see citing works
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Additional file 1 of Uncovering the role of the subcommissural organ in early brain development through transcriptomic analysis
González, M., Maurelia, F., Aguayo, J., Amigo, R., Arrué, R., Gutiérrez, J. L., Torrejón, M., Farkas, C., & Caprile, T. (2024) · Figshare · doi:10.6084/m9.figshare.26754355
Additional file 2 of Uncovering the role of the subcommissural organ in early brain development through transcriptomic analysis
González, M., Maurelia, F., Aguayo, J., Amigo, R., Arrué, R., Gutiérrez, J. L., Torrejón, M., Farkas, C., & Caprile, T. (2024) · Figshare · doi:10.6084/m9.figshare.26754358
Additional file 3 of Uncovering the role of the subcommissural organ in early brain development through transcriptomic analysis
González, M., Maurelia, F., Aguayo, J., Amigo, R., Arrué, R., Gutiérrez, J. L., Torrejón, M., Farkas, C., & Caprile, T. (2024) · Figshare · doi:10.6084/m9.figshare.26754361
Additional file 5 of Uncovering the role of the subcommissural organ in early brain development through transcriptomic analysis
González, M., Maurelia, F., Aguayo, J., Amigo, R., Arrué, R., Gutiérrez, J. L., Torrejón, M., Farkas, C., & Caprile, T. (2024) · Figshare · doi:10.6084/m9.figshare.26754367
Additional file 4 of Uncovering the role of the subcommissural organ in early brain development through transcriptomic analysis
González, M., Maurelia, F., Aguayo, J., Amigo, R., Arrué, R., Gutiérrez, J. L., Torrejón, M., Farkas, C., & Caprile, T. (2024) · Figshare · doi:10.6084/m9.figshare.26754364
Additional file 6 of Uncovering the role of the subcommissural organ in early brain development through transcriptomic analysis
González, M., Maurelia, F., Aguayo, J., Amigo, R., Arrué, R., Gutiérrez, J. L., Torrejón, M., Farkas, C., & Caprile, T. (2024) · Figshare · doi:10.6084/m9.figshare.26754370
Roles of retinoic acid signaling in regulating nervous system development in the cephalochordate amphioxus (Branchiostoma lanceolatum)
Zieger, E. (2016) · doi:10.70675/afdccbe5z278dz4cf0zabccze0a8df30916f
Identification and characterisation of loss of function mutations in KIF14 leading to syndromic renal hypodysplasia
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Interoceptive chemosensory functions of neurons in contact with the cerebrospinal fluid
Marnas, H. (2021) · doi:10.70675/090bfaa3zfeccz45fezbaadz4bb15ac06dd4
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Lopez, N., Zhang, B., Shuken, S. R., Zhou, Y., Payzin‐Dogru, D., Paoli, J. C., Striker, A. E., Wu, S. Y. C., Patel, T. S., Chan, K., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.27.747356
Brain defence by the extracellular matrix protein Cochlin
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“Immuno ﬂ uorescence with an antibody raised against the C-terminus of the protein 11 indicates that Cochlin is distributed in a ﬁ brillar pattern on thesurfaceinthelateralfore-andmidbrainmeninges(Fig.1m,n).”

Cerebrospinal fluid control of neurogenesis induced by retinoic acid during early brain development
Alonso, M. I., Martín, C., Carnicero, E., Bueno, D., & Gato, A. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22657 · Cited by 50 · see citing works
All-trans retinol and retinol-binding protein from embryonic cerebrospinal fluid exhibit dynamic behaviour during early central nervous system development
Parada, C., Gato, A., & Bueno, D. (2008) · Neuroreport · doi:10.1097/wnr.0b013e3283021c94 · Cited by 44 · see citing works
All-trans retinol and retinol-binding protein from embryonic cerebrospinal £uid exhibit dynamic behaviour during early central nervous system development
Parada, C., Casado, Á. L. G., & Torrens, D. B. I. (2008) · UVaDOC UVaDOC University of Valladolid Documentary Repository (University of Valladolid)
Embryonic cerebrospinal fluid regulates neuroepithelial survival, proliferation, and neurogenesis in chick embryos
Gato, A., Moro, J. A., Alonso, M. I., Bueno, D., la Mano, A. D., & Martín, C. (2005) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20185 · Cited by 109 · see citing works
Manual Drainage of the Zebrafish Embryonic Brain Ventricles
Chang, J. T., & Sive, H. L. (2012) · Journal of Visualized Experiments · doi:10.3791/4243-v · Cited by 1 · see citing works

Authors: Chang, J. T., Lehtinen, M. K., & Sive, H.
Affiliations: Whitehead Institute for Biomedical Research (US)
Boston Children's Hospital (US)
Corresponding author: Sive, Hazel
ORCID: Lehtinen, Maria K.
Sive, Hazel
Venue: Developmental Neurobiology
Publisher: Wiley
Published: 2015-06-08
Volume: 76
Issue: 1
Pages: 75-92
ISSN: 1932-8451 (ISSN-L)
1932-846X
DOI: 10.1002/dneu.22300
PMC: PMC4644717
OpenAlex: W1597383969
Cited by: 42
References: 68
Citations by year: 2026: 2 · 2025: 2 · 2024: 6 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 7 · 2019: 4 · 2018: 5 · 2017: 1 · 2016: 5 · 2015: 2
FWCI: 2.01
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Developmental Neurobiology (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
Wiley eBooks
Funders: National Institute for Mental Health, the Alfred P. Sloan Foundation
National Science Foundation
NINDS (R01 NS088566)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: cerebrospinal fluid, retinol-binding protein 4, retinoic acid signaling, cell death, embryonic brain development, zebrafish, yolk syncytiotrophoblast, retinol transport, diencephalon
MeSH terms: Animals, Cell Survival, Cerebral Ventricles, Retinoids, Tretinoin, Zebrafish, Signal Transduction, Cell Death, Zebrafish Proteins, Retinol-Binding Proteins, Plasma

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Zebrafish cerebrospinal fluid mediates cell survival through a retinoid signaling pathway

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