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Cited by 88Barrier Structure and Function StudiesCerebrospinal fluid and hydrocephalusIon Transport and Channel Regulation

Heterogeneous vascular permeability and alternative diffusion barrier in sensory circumventricular organs of adult mouse brain

Morita, Shoko, Furube, Eriko, Mannari, Tetsuya, Okuda, Hiroaki, Tatsumi, Kouko, Wanaka, Akio, Miyata, Seiji·2016·Cell and Tissue Research
DOI 10.1007/s00441-015-2207-7
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Abstract

Fenestrated capillaries of the sensory circumventricular organs (CVOs), including the organum vasculosum of the lamina terminalis, the subfornical organ and the area postrema, lack completeness of the blood-brain barrier (BBB) to sense a variety of blood-derived molecules and to convey the information into other brain regions. We examine the vascular permeability of blood-derived molecules and the expression of tight-junction proteins in sensory CVOs. The present tracer assays revealed that blood-derived dextran 10 k (Dex10k) having a molecular weight (MW) of 10,000 remained in the perivascular space between the inner and outer basement membranes, but fluorescein isothiocyanate (FITC; MW: 389) and Dex3k (MW: 3000) diffused into the parenchyma. The vascular permeability of FITC was higher at central subdivisions than at distal subdivisions. Neither FITC nor Dex3k diffused beyond the dense network of glial fibrillar acidic protein (GFAP)-positive astrocytes/tanycytes. The expression of tight-junction proteins such as occludin, claudin-5 and zonula occludens-1 (ZO-1) was undetectable at the central subdivisions of the sensory CVOs but some was expressed at the distal subdivisions. Electron microscopic observation showed that capillaries were surrounded with numerous layers of astrocyte processes and dendrites. The expression of occludin and ZO-1 was also observed as puncta on GFAP-positive astrocytes/tanycytes of the sensory CVOs. Our study thus demonstrates the heterogeneity of vascular permeability and expression of tight-junction proteins and indicates that the outer basement membrane and dense astrocyte/tanycyte connection are possible alternative mechanisms for a diffusion barrier of blood-derived molecules, instead of the BBB.

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Crossref · 10.1007/s00441-015-2207-7

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  • Blood vessels within the choroid plexus and circumventricular organs have endothelia that lack tight junctions and are open to peripheral circulation.

    “Blood vessels within these two structures have endothelia that lack tight junctions and are open to peripheral circulation (25, 26).”

    From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [25]

  • The dura mater, choroid plexus, and CVOs are particularly exposed to the effects of circulating cytokines given their fenestrated blood vessels and relative openness to factors in the blood.

    “The dura mater, choroid plexus, and CVOs are particularly exposed to the effects of circulating cytokines given their fenestrated blood vessels and relative openness to factors in the blood (25).”

    From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [25]

  • CVOs are separated from adjacent neural tissue in the brain parenchyma by tanycytic astrocytes that limit diffusion of solutes from the CVO to the surrounding tissue.

    “CVOs are separated from adjacent neural tissue in the brain parenchyma by tanycytic astrocytes that limit diffusion of solutes from the CVO to the surrounding tissue (25).”

    From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [25]

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Authors
Morita, S., Furube, E., Mannari, T., Okuda, H., Tatsumi, K., Wanaka, A., & Miyata, S.
Affiliations
  • Kyoto Institute of Technology (JP)
  • Nara Medical University (JP)
Corresponding author
Miyata, Seiji
ORCID
Venue
Cell and Tissue Research
Publisher
Springer Science and Business Media LLC
Published
2015-06-06
Volume
363
Issue
2
Pages
497-511
ISSN
  • 0302-766X (ISSN-L)
  • 1432-0878
DOI
10.1007/s00441-015-2207-7
OpenAlex
W600234098
Cited by
88
References
66
Citations by year
2026: 7 · 2025: 9 · 2024: 9 · 2023: 4 · 2022: 7 · 2021: 10 · 2020: 10 · 2019: 8 · 2018: 7 · 2017: 7 · 2016: 7 · 2015: 3
FWCI
4.27
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • Cell and Tissue Research (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • Japan Society for the Promotion of Science (16J10225, 26293039, 15K11352, 15K14354, 26830029)
Topics
  • Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
Keywords
blood-brain barrier, fenestrated capillaries, vascular permeability, tight junction proteins, organum vasculosum of the lamina terminalis, subfornical organ, area postrema, occludin, claudin-5, zonula occludens-1, astrocytes, tanycytes, glial fibrillary acidic protein, basement membrane
MeSH terms
Cadherin 5, Aging, Animals, Blood-Brain Barrier, Capillary Permeability, Diffusion, Male, Mice, Inbred C57BL, Models, Biological, Antigens, CD, Cadherins, Fluorescein-5-isothiocyanate, Claudin-5, Occludin, Zonula Occludens-1 Protein, Circumventricular Organs

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