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Severe alterations of endothelial and glial cells in the blood‐brain barrier of dystrophic mdx mice
Open accessAbstract
In this study, we investigated the involvement of the blood‐brain barrier (BBB) in the brain of the dystrophin‐deficient mdx mouse, an experimental model of Duchenne muscular dystrophy (DMD). To this purpose, we used two tight junction markers, the Zonula occludens (ZO‐1) and claudin‐1 proteins, and a glial marker, the aquaporin‐4 (AQP4) protein, whose expression is correlated with BBB differentiation and integrity. Results showed that most of the brain microvessels in mdx mice were lined by altered endothelial cells that showed open tight junctions and were surrounded by swollen glial processes. Moreover, 18% of the perivascular glial endfeet contained electron‐dense cellular debris and were enveloped by degenerating microvessels. Western blot showed a 60% reduction in the ZO‐1 protein content in mdx mice and a similar reduction in AQP4 content compared with the control brain. ZO‐1 immunocytochemistry and claudin‐1 immunofluorescence in mdx mice revealed a diffuse staining of microvessels as compared with the control ones, which displayed a banded staining pattern. ZO‐1 immunogold electron microscopy showed unlabeled tight junctions and the presence of gold particles scattered in the endothelial cytoplasm in the mdx mice, whereas ZO‐1 gold particles were exclusively located at the endothelial tight junctions in the controls. Dual immunofluorescence staining of α‐actin and ZO‐1 revealed colocalization of these proteins. As in ZO‐1 staining, the pattern of immunolabeling with anti–α‐actin antibody was diffuse in the mdx vessels and pointed or banded in the controls. α‐actin immunogold electron microscopy showed gold particles in the cytoplasms of endothelial cells and pericytes in the mdx mice, whereas α‐actin gold particles were revealed on the endothelial tight junctions and the cytoskeletal microfilaments of pericytes in the controls. Perivascular glial processes of the mdx mice appeared faintly stained by anti‐AQP4 antibody, while in the controls a strong AQP4 labeling of glial processes was detected at light and electron microscope level. The vascular permeability of the mdx brain microvessels was investigated by means of the horseradish peroxidase (HRP). After HRP injection, extensive perivascular areas of marker escape were observed in mdx mice, whereas HRP was exclusively intravascularly localized in the controls. Inflammatory cells, CD4‐, CD8‐, CD20‐, and CD68‐positive cells, were not revealed in the perivascular stroma of the mdx brain. These findings indicate that dystrophin deficiency in the mdx brain leads to severe injury of the endothelial and glial cells with disturbance in α‐actin cytoskeleton, ZO‐1, claudin‐1, and AQP4 assembly, as well as BBB breakdown. The BBB alterations suggest that changes in vascular permeability are involved in the pathogenesis of the neurological dysfunction associated with DMD. GLIA 42:235–251, 2003. © 2003 Wiley‐Liss, Inc.
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“Dystrophin knockout mice exhibit a notable brain microvascular phenotype with disrupted endothelial TJs, swollen perivascular glial endfeet, and degenerating microvessels (433).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [433]
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Metadata
- Authors
- Nico, B., Frigeri, A., Nicchia, G. P., Corsi, P., Ribatti, D., Quondamatteo, F., Herken, R., Girolamo, F., Marzullo, A., Svelto, M., & Roncali, L.
- Affiliations
- University of Bari Aldo Moro (IT)
- University of Göttingen (DE)
- Corresponding author
- Nico, Beatrice
- ORCID
- Venue
- Glia
- Publisher
- Wiley
- Published
- 2003-03-18
- Volume
- 42
- Issue
- 3
- Pages
- 235-251
- ISSN
- 0894-1491 (ISSN-L)
- 1098-1136
- OpenAlex
- W2001178402
- Cited by
- 172
- References
- 93
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 5 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 4 · 2019: 12 · 2018: 5 · 2017: 1 · 2016: 10 · 2015: 7 · 2014: 9 · 2013: 8 · 2012: 8
- FWCI
- 7.07
- Type
- journal article
- Language
- en
- Open access
- Locations
- Glia (publishedVersion)
- PubMed (publishedVersion)
- GRO (submittedVersion, cc-by)
- CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Keywords
- blood-brain barrier, Duchenne muscular dystrophy, mdx mice, dystrophin deficiency, endothelial cells, astrocytes, tight junctions, ZO-1, claudin-1, aquaporin-4, alpha-actin, pericytes
- MeSH terms
- Actins, Animals, Antigens, Surface, Astrocytes, Blood-Brain Barrier, Brain, Disease Models, Animal, Endothelium, Vascular, Female, Horseradish Peroxidase, Immunohistochemistry, Membrane Proteins, Microscopy, Electron, Phosphoproteins, Biomarkers, Down-Regulation, Mice, Inbred mdx, Tight Junctions, Aquaporins, Muscular Dystrophy, Duchenne, Mice, Aquaporin 4, Claudin-1, Zonula Occludens-1 Protein
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