Partial recovery of the damaged rat blood–brain barrier is mediated by adherens junction complexes, extracellular matrix remodeling and macrophage infiltration following focal astrocyte loss
Highlights • Paracellular VE-cadherin and β-catenin maintained in the absence of GFAP-astrocytes. • Demonstrates a different regulation mechanism for adherens and tight junction protein. • Extracellular matrix remodeling and inflammatory response following astrocyte loss. • Size-selective temporary...
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| Published in: | Neuroscience Vol. 250; pp. 773 - 785 |
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| Main Authors: | , , , |
| Format: | Journal Article |
| Language: | English |
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| Abstract | Highlights • Paracellular VE-cadherin and β-catenin maintained in the absence of GFAP-astrocytes. • Demonstrates a different regulation mechanism for adherens and tight junction protein. • Extracellular matrix remodeling and inflammatory response following astrocyte loss. • Size-selective temporary barrier formed in the absence of tight junction proteins. • Represents a new approach to studying BBB integrity loss in demyelinating disorders. |
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| AbstractList | • Paracellular VE-cadherin and β-catenin maintained in the absence of GFAP-astrocytes. • Demonstrates a different regulation mechanism for adherens and tight junction protein. • Extracellular matrix remodeling and inflammatory response following astrocyte loss. • Size-selective temporary barrier formed in the absence of tight junction proteins. • Represents a new approach to studying BBB integrity loss in demyelinating disorders.
Blood–brain barrier (BBB) dysfunction is a feature of many neurodegenerative disorders. The mechanisms and interactions between astrocytes, extracellular matrix and vascular endothelial cells in regulating the mature BBB are poorly understood. We have previously shown that transitory glial fibrillary acidic protein (GFAP)-astrocyte loss, induced by the systemic administration of 3-chloropropanediol, leads to reversible disruption of tight junction complexes and BBB integrity to a range of markers. However, early restoration of BBB integrity to dextran (10–70kDa) and fibrinogen was seen in the absence of paracellular tight junction proteins claudin-5 and occludin. In the present study we show that in the GFAP-astrocyte-lesioned rat inferior colliculus, paracellular expression of adherens junction proteins (vascular endothelial (VE)-cadherin and β-catenin) was maintained in vascular endothelial cells that lacked paracellular claudin-5 expression and which showed reversible post-translational occludin modification. Claudin-1 expression paralleled the loss and recovery of claudin-5, while claudin-3 or -12 immunoreactivity was not detected. In addition, the extracellular matrix, as visualized by laminin and fibronectin, underwent extensive reversible remodeling and perivascular CD169 macrophages become abundant throughout the lesioned inferior colliculus. At a time that GFAP-astrocytes repopulated the lesion area and tight junction proteins were returned to paracellular domains, the extracellular matrix and leukocyte profiles normalized and resembled profiles seen in control tissue. This study supports the hypothesis that a combination of paracellular adherens junctional proteins, remodeled basement membrane and the presence of perivascular leukocytes provide a temporary barrier to limit the extravasation of macromolecules and potentially neurotoxic substances into the brain parenchyma until tight junction proteins are restored to paracellular domains. Blood-brain barrier (BBB) dysfunction is a feature of many neurodegenerative disorders. The mechanisms and interactions between astrocytes, extracellular matrix and vascular endothelial cells in regulating the mature BBB are poorly understood. We have previously shown that transitory GFAP-astrocyte loss, induced by systemic administration of 3-chloropropanediol, leads to reversible disruption of tight junction complexes and BBB integrity to a range of markers. However, early restoration of BBB integrity to dextran (10-70 kDa) and fibrinogen was seen in the absence of paracellular tight junction proteins claudin-5 and occludin. In the present study we show that in the GFAP-astrocyte lesioned rat inferior colliculus, paracellular expression of adherens junction proteins (VE-cadherin and β-catenin) was maintained in vascular endothelial cells that lacked paracellular claudin-5 expression and which showed reversible post-translational occludin modification. Claudin-1 expression paralleled the loss and recovery of claudin-5, while claudin -3 or -12 immunoreactivity was not detected. In addition, the extracellular matrix, as visualized by laminin and fibronectin, underwent extensive reversible remodeling and perivascular CD169 macrophages become abundant throughout the lesioned inferior colliculus. At a time that GFAP-astrocytes repopulated the lesion area and tight junction proteins were returned to paracellular domains, the extracellular matrix and leukocyte profiles normalized and resembled profiles seen in control tissue. This study supports the hypothesis that a combination of paracellular adherens junctional proteins, remodeled basement membrane and the presence perivascular leukocytes provide a temporary barrier to limit extravasation of macromolecules and potentially neurotoxic substances into the brain parenchyma until tight junction proteins are restored to paracellular domains. Blood-brain barrier (BBB) dysfunction is a feature of many neurodegenerative disorders. The mechanisms and interactions between astrocytes, extracellular matrix and vascular endothelial cells in regulating the mature BBB are poorly understood. We have previously shown that transitory glial fibrillary acidic protein (GFAP)-astrocyte loss, induced by the systemic administration of 3-chloropropanediol, leads to reversible disruption of tight junction complexes and BBB integrity to a range of markers. However, early restoration of BBB integrity to dextran (10-70kDa) and fibrinogen was seen in the absence of paracellular tight junction proteins claudin-5 and occludin. In the present study we show that in the GFAP-astrocyte-lesioned rat inferior colliculus, paracellular expression of adherens junction proteins (vascular endothelial (VE)-cadherin and beta -catenin) was maintained in vascular endothelial cells that lacked paracellular claudin-5 expression and which showed reversible post-translational occludin modification. Claudin-1 expression paralleled the loss and recovery of claudin-5, while claudin-3 or -12 immunoreactivity was not detected. In addition, the extracellular matrix, as visualized by laminin and fibronectin, underwent extensive reversible remodeling and perivascular CD169 macrophages become abundant throughout the lesioned inferior colliculus. At a time that GFAP-astrocytes repopulated the lesion area and tight junction proteins were returned to paracellular domains, the extracellular matrix and leukocyte profiles normalized and resembled profiles seen in control tissue. This study supports the hypothesis that a combination of paracellular adherens junctional proteins, remodeled basement membrane and the presence of perivascular leukocytes provide a temporary barrier to limit the extravasation of macromolecules and potentially neurotoxic substances into the brain parenchyma until tight junction proteins are restored to paracellular domains. Highlights • Paracellular VE-cadherin and β-catenin maintained in the absence of GFAP-astrocytes. • Demonstrates a different regulation mechanism for adherens and tight junction protein. • Extracellular matrix remodeling and inflammatory response following astrocyte loss. • Size-selective temporary barrier formed in the absence of tight junction proteins. • Represents a new approach to studying BBB integrity loss in demyelinating disorders. Blood-brain barrier (BBB) dysfunction is a feature of many neurodegenerative disorders. The mechanisms and interactions between astrocytes, extracellular matrix and vascular endothelial cells in regulating the mature BBB are poorly understood. We have previously shown that transitory glial fibrillary acidic protein (GFAP)-astrocyte loss, induced by the systemic administration of 3-chloropropanediol, leads to reversible disruption of tight junction complexes and BBB integrity to a range of markers. However, early restoration of BBB integrity to dextran (10-70 kDa) and fibrinogen was seen in the absence of paracellular tight junction proteins claudin-5 and occludin. In the present study we show that in the GFAP-astrocyte-lesioned rat inferior colliculus, paracellular expression of adherens junction proteins (vascular endothelial (VE)-cadherin and β-catenin) was maintained in vascular endothelial cells that lacked paracellular claudin-5 expression and which showed reversible post-translational occludin modification. Claudin-1 expression paralleled the loss and recovery of claudin-5, while claudin-3 or -12 immunoreactivity was not detected. In addition, the extracellular matrix, as visualized by laminin and fibronectin, underwent extensive reversible remodeling and perivascular CD169 macrophages become abundant throughout the lesioned inferior colliculus. At a time that GFAP-astrocytes repopulated the lesion area and tight junction proteins were returned to paracellular domains, the extracellular matrix and leukocyte profiles normalized and resembled profiles seen in control tissue. This study supports the hypothesis that a combination of paracellular adherens junctional proteins, remodeled basement membrane and the presence of perivascular leukocytes provide a temporary barrier to limit the extravasation of macromolecules and potentially neurotoxic substances into the brain parenchyma until tight junction proteins are restored to paracellular domains. |
| Author | Willis, C.L Brule, S.A Camire, R.B Ray, D.E |
| AuthorAffiliation | 1 Department of Biomedical Sciences, College of Osteopathic Medicine, University of New England, 11 Hills Beach Road. Biddeford, ME 04005, USA 2 MRC Applied Neuroscience Group, School of Biomedical Sciences, Queen’s Medical Centre, University of Nottingham NG7 2UH, UK |
| AuthorAffiliation_xml | – name: 2 MRC Applied Neuroscience Group, School of Biomedical Sciences, Queen’s Medical Centre, University of Nottingham NG7 2UH, UK – name: 1 Department of Biomedical Sciences, College of Osteopathic Medicine, University of New England, 11 Hills Beach Road. Biddeford, ME 04005, USA |
| Author_xml | – sequence: 1 fullname: Willis, C.L – sequence: 2 fullname: Camire, R.B – sequence: 3 fullname: Brule, S.A – sequence: 4 fullname: Ray, D.E |
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| Keywords | PBS PECAM-1 BBB phosphate-buffered saline Tris–Tween-buffered saline GFAP VE vascular endothelial blood–brain barrier fibronectin basal lamina TTBS platelet endothelial cell adhesion molecule-1 VE-cadherin laminin tight junctions GAPDH glial fibrillary acidic protein glyceraldehyde 3-phosphate dehydrogenase neurovascular unit Rat Neuroglia Rodentia Central nervous system Cell junction Astrocyte Cadherin Blood brain barrier Fibronectin Encephalon Vertebrata Mammalia Laminin Animal Tight junction Extracellular matrix Macrophage |
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310 Huber (10.1016/j.neuroscience.2013.06.061_b0085) 2002; 283 Gonzalez-Mariscal (10.1016/j.neuroscience.2013.06.061_b0065) 2008; 1778 Vos (10.1016/j.neuroscience.2013.06.061_b0215) 2005; 20 Lampugnani (10.1016/j.neuroscience.2013.06.061_b0100) 2007; 120 Willis (10.1016/j.neuroscience.2013.06.061_b0235) 2007; 150 Hassel (10.1016/j.neuroscience.2013.06.061_b0075) 1994; 167 Barnett (10.1016/j.neuroscience.2013.06.061_b0025) 2012; 18 Sakurai (10.1016/j.neuroscience.2013.06.061_b0175) 2003; 44 Willis (10.1016/j.neuroscience.2013.06.061_b0225) 2004; 45 Harris (10.1016/j.neuroscience.2013.06.061_b0070) 2010; 22 Szabo (10.1016/j.neuroscience.2013.06.061_b0185) 2004; 30 Dejana (10.1016/j.neuroscience.2013.06.061_b0050) 2008; 121 Milner (10.1016/j.neuroscience.2013.06.061_b0130) 2008; 39 Carmeliet (10.1016/j.neuroscience.2013.06.061_b0040) 1999; 98 Bazzoni (10.1016/j.neuroscience.2013.06.061_b0030) 2004; 84 Wingerchuk (10.1016/j.neuroscience.2013.06.061_b0245) 2007; 6 Yurchenco (10.1016/j.neuroscience.2013.06.061_b0260) 2009; 15 Manoonkitiwongsa (10.1016/j.neuroscience.2013.06.061_b0120) 2001; 21 |
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| Snippet | Highlights • Paracellular VE-cadherin and β-catenin maintained in the absence of GFAP-astrocytes. • Demonstrates a different regulation mechanism for adherens... • Paracellular VE-cadherin and β-catenin maintained in the absence of GFAP-astrocytes. • Demonstrates a different regulation mechanism for adherens and tight... Blood-brain barrier (BBB) dysfunction is a feature of many neurodegenerative disorders. The mechanisms and interactions between astrocytes, extracellular... |
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| SubjectTerms | Adherens Junctions - physiology Animals Antigens, CD - biosynthesis Astrocytes - physiology basal lamina beta Catenin - biosynthesis Biological and medical sciences Blood-Brain Barrier - physiology Blotting, Western Cadherins - biosynthesis Cerebral circulation. Blood-brain barrier. Choroid plexus. Cerebrospinal fluid. Circumventricular organ. Meninges Claudin-5 - biosynthesis Electrophoresis, Polyacrylamide Gel Extracellular Matrix - physiology fibronectin Fibronectins - biosynthesis Fluorescent Antibody Technique Fundamental and applied biological sciences. Psychology Inferior Colliculi - cytology laminin Laminin - biosynthesis Macrophages - physiology Male Microscopy, Confocal Microscopy, Electron Neurology neurovascular unit Occludin - biosynthesis Rats Rats, Inbred F344 Sialic Acid Binding Ig-like Lectin 1 - biosynthesis tight junctions Tight Junctions - physiology VE-cadherin Vertebrates: nervous system and sense organs |
| Title | Partial recovery of the damaged rat blood–brain barrier is mediated by adherens junction complexes, extracellular matrix remodeling and macrophage infiltration following focal astrocyte loss |
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