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Retinoic Acid Induces Blood–Brain Barrier Development
Open accessAbstract
The blood–brain barrier (BBB) is crucial in the maintenance of a controlled environment within the brain to safeguard optimal neuronal function. The endothelial cells (ECs) of the BBB possess specific properties that restrict the entry of cells and metabolites into the CNS. The specialized BBB endothelial phenotype is induced during neurovascular development by surrounding cells of the CNS. However, the molecular differentiation of the BBB endothelium remains poorly understood. Retinoic acid (RA) plays a crucial role in the brain during embryogenesis. Because radial glial cells supply the brain with RA during the developmental cascade and associate closely with the developing vasculature, we hypothesize that RA is important for the induction of BBB properties in brain ECs. Analysis of human postmortem fetal brain tissue shows that the enzyme mainly responsible for RA synthesis, retinaldehyde dehydrogenase, is expressed by radial glial cells. In addition, the most important receptor for RA-driven signaling in the CNS, RA-receptor β (RARβ), is markedly expressed by the developing brain vasculature. Our findings have been further corroborated by in vitro experiments showing RA- and RARβ-dependent induction of different aspects of the brain EC barrier. Finally, pharmacologic inhibition of RAR activation during the differentiation of the murine BBB resulted in the leakage of a fluorescent tracer as well as serum proteins into the developing brain and reduced the expression levels of important BBB determinants. Together, our results point to an important role for RA in the induction of the BBB during human and mouse development.
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“RA/RAR signaling is critical for BBB differentiation and integrity90.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [90]
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Mizee, M. R., van Doorn, R., Prat, A., & de Vries, H. E. (2015) · CRC Press eBooks · doi:10.1201/b19299-2 · Cited by 1
Self-citationCells of Cerebrovascular Endothelium and Perivascular Astroglia in the Regulation of Neurogenesis
Тепляшина, Е. А., Gorina, Y. V., Хилажева, Е. Д., Boytsova, E. B., Mosiagina, A. I., Malinovskaya, N. A., Komleva, Y. K., Morgun, A. V., Uspenskaya, Y. A., Shuvaev, А. N., et al. (2022) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093022030097 · Cited by 1
İskemik Beyin Hasarında Reaktif Astrositlerin Fonksiyonları
Akbulut, N. H., Topal, G., & Eyigör, Ö. (2023) · Uludağ Üniversitesi Tıp Fakültesi Dergisi · doi:10.32708/uutfd.1261257 · Cited by 3
Effects of the Ketogenic Diet on the Blood–Brain Barrier
Janigro, D. (2022) · Oxford University Press eBooks · doi:10.1093/med/9780197501207.003.0029 · Cited by 1
Lubin, K. E., & Knipp, G. T. (2021) · Research Square · doi:10.21203/rs.3.rs-592200/v1 · Cited by 1
Computational Drug Repositioning Identifies Potentially Active Therapies for Chordoma
Traylor, J. I., Sheppard, H. E., Ravikumar, V., Breshears, J. D., Raza, S. M., Lin, C. Y., PATEL, S. R., & DeMonte, F. (2021) · Neurosurgery · doi:10.1093/neuros/nyaa398_s099 · Cited by 1
In Vitro Chronic Neurotoxicity Assays: Present and Future Developments
Nagel, D. A., Hill, E. J., Woehrling, E. K., & Coleman, M. D. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.99500-x
Multiple Sclerosis: Impact on Functioning of the Blood–Brain Barrier
Mizee, M. R., Kooij, G., & de Vries, H. E. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1071-7_8
Self-citationKnuesel, I. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800228-5.00004-2
Inflammation at the Blood–Brain Barrier in Multiple Sclerosis
Mizee, M. R., van Doorn, R., Prat, A., & de Vries, H. E. (2013) · Topics in medicinal chemistry · doi:10.1007/7355_2013_21
Self-citationЭндотелиальные прогениторные клетки в развитии и восстановлении церебрального Эндотелия (обзор)
Salmina, B., Владимирович, М. В., Solonchuk, R., & Lopatina, L. (2014)
In Vitro Models of the Blood–Brain Barrier to Better Understand the Pathophysiology of Brain Edema
Al-Ahmad, A. J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803196-4.00005-9
Zhou, Y., Zheng, B., Ye, L., Zhang, H., Zhu, S., Zheng, X., Xia, Q.-H., He, Z., Wang, Q., Xiao, J., et al. (2020) · Neurochemical Research · doi:10.1007/s11064-020-03149-1
RetractedBonney, S. K., Mishra, S., Pleasure, S. J., & Siegenthaler, J. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814405-3.00043-6
Effects of the Ketogenic Diet on the Blood-Brain Barrier
Banjara, M., & Janigro, D. (2016) · doi:10.1093/med/9780190497996.003.0030
The Antioxidant Vitamins A, C, and E and the Developing Brain
(2016) · CRC Press eBooks · doi:10.1201/9781315372402-5
Neurovascular mitochondrial susceptibility impacts blood-brain barrier function and behaviorPreprint
Crockett, A. M., Kébir, H., Colόn, M. C. V., Iascone, D. M., Cielieski, B., Rossano, A. J., Sehgal, A., Anderson, S. A., & Alvarez, J. I. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.15.580544
“As retinoic acid is known to induce BBB properties ( 66, 67 ), this is consistent with our findings that BBB integrity is improved by bezafibrate.”
ResultJezierski, A., Huang, J., Haqqani, A. S., Haukenfrers, J., Liu, Z., Baumann, E., Sodja, C., Charlebois, C., Delaney, C. E., Star, A. T., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26592191
Shi, Y., Kim, H., Hamann, C. A., Rhea, E. M., Brunger, J. M., & Lippmann, E. S. (2022) · Figshare · doi:10.6084/m9.figshare.21184245
Jezierski, A., Huang, J., Haqqani, A. S., Haukenfrers, J., Liu, Z., Baumann, E., Sodja, C., Charlebois, C., Delaney, C. E., Star, A. T., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26592188
Tamhankar, S., Ding, Y., Hashjin, F. Y., Boutom, S., Daneman, R., Palecek, S. P., & Shusta, E. V. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.02.699492
Metadata
- Authors
- Mizee, M. R., Wooldrik, D., Lakeman, K. A. M., van het Hof, B., Drexhage, J. A. R., Geerts, D., Bugiani, M., Aronica, E., Mebius, R. E., Prat, A., de Vries, H. E., & Reijerkerk, A.
- Affiliations
- Amsterdam Neuroscience (NL)
- Erasmus MC (NL)
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Amsterdam UMC Location University of Amsterdam (NL)
- Hôpital Notre-Dame (CA)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-01-23
- Volume
- 33
- Issue
- 4
- Pages
- 1660-1671
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6618717
- OpenAlex
- W1985474890
- Cited by
- 203
- References
- 60
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 13 · 2023: 13 · 2022: 19 · 2021: 19 · 2020: 18 · 2019: 11 · 2018: 17 · 2017: 15 · 2016: 16 · 2015: 26 · 2014: 14 · 2013: 7
- FWCI
- 11.79
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Top Institute Pharma
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- retinoic acid, blood-brain barrier development, brain endothelial cells, retinoic acid receptor beta, retinaldehyde dehydrogenase, radial glia, neurovascular development, endothelial barrier function, fetal brain
- MeSH terms
- Animals, Blood-Brain Barrier, Cell Differentiation, Cell Line, Fetus, Humans, Immunohistochemistry, Mice, Inbred C57BL, Neuroglia, Tretinoin, Blotting, Western, Signal Transduction, Gene Expression Regulation, Developmental, Endothelial Cells, Mice, Real-Time Polymerase Chain Reaction
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