The cerebrospinal fluid provides a proliferative niche for neural progenitor cells
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Cortical development depends on the active integration of cell-autonomous and extrinsic cues, but the coordination of these processes is poorly understood. Here, we show that the apical complex protein Pals1 and Pten have opposing roles in localizing the Igf1R to the apical, ventricular domain of cerebral cortical progenitor cells. We found that the cerebrospinal fluid (CSF), which contacts this apical domain, has an age-dependent effect on proliferation, much of which is attributable to Igf2, but that CSF contains other signaling activities as well. CSF samples from patients with glioblastoma multiforme show elevated Igf2 and stimulate stem cell proliferation in an Igf2-dependent manner. Together, our findings demonstrate that the apical complex couples intrinsic and extrinsic signaling, enabling progenitors to sense and respond appropriately to diffusible CSF-borne signals distributed widely throughout the brain. The temporal control of CSF composition may have critical relevance to normal development and neuropathological conditions.
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Essentially all major choroid plexus cell types, and in particular choroid plexus fibroblasts, expressed many secreted factors found in cerebrospinal fluid, including Igf2.
“Essentially all major ChP cell types, and in particular ChP fibroblasts, also expressed many secreted factors found in CSF, including Igf2 (Lehtinen et al., 2011).”
From A cellular and spatial map of the choroid plexus across brain ventricles and ages (2021) · cites this paper as Lehtinen et al., 2011
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Petrik, D., Myoga, M. H., Grade, S., Gerkau, N. J., Pusch, M., Rose, C. R., Grothe, B., & Götz, M. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.04.016 · Cited by 104 · see citing works
Sonic hedgehog signaling in the postnatal brain
Álvarez-Buylla, A., & Ihrie, R. A. (2014) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2014.05.008 · Cited by 100 · see citing works
Ford, M. J., Yeyati, P. L., Mali, G. R., Keighren, M. A., Waddell, S. H., Mjoseng, H. K., Douglas, A. T., Hall, E. A., Sakaue-Sawano, A., Miyawaki, A., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.10.027 · Cited by 89 · see citing works
Neuropoietic cytokines in normal brain development and neurodevelopmental disorders
Stolp, H. B. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.08.009 · Cited by 70 · see citing works
BMP9 ameliorates amyloidosis and the cholinergic defect in a mouse model of Alzheimer’s disease
Burke, R. M., Norman, T. A., Haydar, T. F., Slack, B. E., Leeman, S. E., Blusztajn, J. K., & Mellott, T. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319297110 · Cited by 59 · see citing works
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Self-citationZebrafish cerebrospinal fluid mediates cell survival through a retinoid signaling pathway
Chang, J. T., Lehtinen, M. K., & Sive, H. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22300 · Cited by 42 · see citing works
“…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 Mashayekhi, 2006; Lehtinen et al., 2011).”
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Fitzgerald, G. S., Chuchta, T. G., & McNay, E. C. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14160 · Cited by 22 · see citing works
- Authors
- Lehtinen, M. K., Zappaterra, M. W., Chen, X., Yang, Y. J., Hill, A. D., Lun, M., Maynard, T., Gonzalez, D., Kim, S., Ye, P., D'Ercole, A. J., Wong, E. T., LaMantia, A. S., & Walsh, C. A.
- Affiliations
- Broad Institute (US)
- George Washington University (US)
- The University of Texas Health Science Center at Houston (US)
- University of North Carolina at Chapel Hill (US)
- Beth Israel Deaconess Medical Center (US)
- Corresponding author
- Walsh, Christopher A.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-03
- Volume
- 69
- Issue
- 5
- Pages
- 893-905
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3085909
- OpenAlex
- W1967611229
- Cited by
- 648
- References
- 74
- Citations by year
- 2026: 24 · 2025: 34 · 2024: 29 · 2023: 40 · 2022: 42 · 2021: 39 · 2020: 65 · 2019: 50 · 2018: 54 · 2017: 38 · 2016: 43 · 2015: 41 · 2014: 48 · 2013: 42 · 2012: 43
- FWCI
- 15.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- Howard Hughes Medical Institute
- Child Neurology Foundation
- National Institutes of Health
- University of North Carolina at Chapel Hill
- Manton Center for Orphan Disease Research, Boston Children's Hospital
- National Institute of General Medical Sciences (T32GM007753)
- National Institute of Neurological Disorders and Stroke (R01NS048868, P30NS045892, R01NS035129, RO1 NS032457, K99NS072192, R01NS032457, R37NS035129)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD029178, R01HD029178, P30HD018655, R29HD029178, R01HD008299, R01HD042182)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
- Keywords
- cerebrospinal fluid, neural progenitor cells, cortical development, PALS1, PTEN, IGF-1 receptor, insulin-like growth factor II, apical complex, ventricular zone, cell proliferation, glioblastoma, extrinsic signaling, stem cell proliferation
- MeSH terms
- Analysis of Variance, Animals, Brain Neoplasms, Cerebral Cortex, Cerebrospinal Fluid, Glioblastoma, Humans, Insulin-Like Growth Factor II, Membrane Proteins, Neurons, Nucleoside-Phosphate Kinase, Receptor, IGF Type 1, Statistics, Nonparametric, Cell Proliferation, PTEN Phosphohydrolase, Mice, Neural Stem Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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