Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis
Open accessAbstract
The endothelial cell monolayer of cerebral vessels and its basement membrane (BM) are ensheathed by the astrocyte endfeet, the leptomeningeal cells, and their associated parenchymal BM, all of which contribute to establishment of the blood–brain barrier (BBB). As a consequence of this unique structure, leukocyte penetration of cerebral vessels is a multistep event. In mouse experimental autoimmune encephalomyelitis (EAE), a widely used central nervous system inflammatory model, leukocytes first penetrate the endothelial cell monolayer and underlying BM using integrin β1-mediated processes, but mechanisms used to penetrate the second barrier defined by the parenchymal BM and glia limitans remain uninvestigated. We show here that macrophage-derived gelatinase (matrix metalloproteinase [MMP]-2 and MMP-9) activity is crucial for leukocyte penetration of the parenchymal BM. Dystroglycan, a transmembrane receptor that anchors astrocyte endfeet to the parenchymal BM via high affinity interactions with laminins 1 and 2, perlecan and agrin, is identified as a specific substrate of MMP-2 and MMP-9. Ablation of both MMP-2 and MMP-9 in double knockout mice confers resistance to EAE by inhibiting dystroglycan cleavage and preventing leukocyte infiltration. This is the first description of selective in situ proteolytic damage of a BBB-specific molecule at sites of leukocyte infiltration.
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Metalloproteinases selectively cleave dystroglycan, which tethers astrocytic foot processes to the basement membrane, allowing penetration of effector T cells and myeloid cells into the CNS parenchyma in the MOG35-55 EAE model.
“The metalloproteinases selectively cleave dystroglycan, which tethers astrocytic foot processes to the basement membrane (Fig. 3), allowing penetration of effector T cells and myeloid cells into the CNS parenchyma in the MOG35-55 EAE model (121).”
From The anatomy and immunology of vasculature in the central nervous system (2019) · cites this paper as [121]
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- Authors
- Agrawal, S., Anderson, P., Durbeej, M., van Rooijen, N., Ivars, F., Opdenakker, G., & Sorokin, L. M.
- Affiliations
- 1Experimental Pathology
- 2Immunology,
- Lund University (SE)
- 4Vrije Universiteit, Molecular Cell Biology, 1081 BT Amsterdam, Netherlands
- Rega Institute for Medical Research (BE)
- University of Münster (DE)
- Venue
- The Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 2006-04-03
- Volume
- 203
- Issue
- 4
- Pages
- 1007-1019
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC2118280
- OpenAlex
- W2154793195
- Cited by
- 559
- References
- 49
- Citations by year
- 2026: 11 · 2025: 22 · 2024: 33 · 2023: 22 · 2022: 23 · 2021: 29 · 2020: 19 · 2019: 18 · 2018: 31 · 2017: 31 · 2016: 37 · 2015: 30 · 2014: 31 · 2013: 38 · 2012: 37
- FWCI
- 17.77
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Experimental Medicine (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Institutional Repository of the University of Granada (University of Granada) (submittedVersion, cc-by-nc-nd)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- Multiple Sclerosis Society
- Fondation Charcot
- Vlaamse regering
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- dystroglycan, experimental autoimmune encephalomyelitis, leukocyte transmigration, blood-brain barrier, MMP-2, MMP-9, astrocyte endfeet, laminin, perlecan, agrin, beta1 integrin, leukocyte infiltration
- MeSH terms
- Animals, Astrocytes, Basement Membrane, Cells, Cultured, Encephalomyelitis, Autoimmune, Experimental, Hydrolysis, Leukocytes, Macrophages, Mice, Inbred C57BL, Gelatinases, Mice, Knockout, Matrix Metalloproteinase 2, Matrix Metalloproteinase 9, Leukocyte Rolling, Dystroglycans, Mice
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