Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats.
Abstract
The upregulation of extracellular matrix components, especially chondroitin sulfate proteoglycans, after brain injury and stroke is known to accompany the glial reaction, forming repellent scars that hinder axonal growth and the reorganization of the injured neuronal networks. The extracellular matrix associated with perineuronal nets (PNs) in the primarily injured and remote regions has not yet been systematically analyzed. We use the model of permanent middle cerebral artery occlusion (MCAO) to investigate the acute and long‐lasting consequences of ischemia for PNs, related to the damage of neurons and reactions of glial cells, in spontaneously hypertensive rats. Extracellular matrix components associated with PNs around cortical interneurons and neurons in thalamic nuclei were characterized 1, 7, 14, and 35 days after MCAO, using Wisteria floribunda agglutinin (WFA) staining and immunocytochemistry. The degradation of PNs in the infarct core was initiated by loss of WFA‐binding matrix components, indicating the cleavage of glycosaminoglycan chains of chondroitin sulfate proteoglycans. Immunostaining showed the subsequent removal of proteoglycan core proteins within the extending microglia/macrophage invasion zone lasting for 2 weeks after MCAO. In the cortical periinfarct region, delineated by an astrocytic scar against the infarct core, the number of WFA‐stained and proteoglycan core protein‐immunoreactive PNs was permanently reduced. In the homolateral ventroposterior thalamus, the delayed decrease in perineuronal matrix was related to the distribution pattern of activated microglia and massive neuronal degeneration. It can be concluded from these results that complementary to the known upregulation of matrix components in the glial scar, deficits in the expression of the neuron‐associated extracellular matrix develop in the periinfarct and remote regions. These deficits may contribute to the long‐lasting functional impairments after stroke. © 2005 Wiley‐Liss, Inc.
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Decrease in inhibitory cell function may underlie epilepsy-like activity following stroke.
“this decrease in inhibitory cell function may underlie epilepsy-like activity following stroke (Hobohm et al., 2005; Xie et al., 2014).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Hobohm et al., 2005
In cortical areas surrounding the infarct and outside of the glial scar, CSPG immunoreactivity is down regulated although it remains detectable up to 14 days post-injury.
“CSPG immunoreactivity is down regulated although they remain detectable up to 14 days post-injury (Hobohm et al., 2005).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Hobohm et al., 2005
Reduced PV-immunoreactivity and PV cell function have been observed following stroke.
“reduced PV-immunoreactivity and PV cell function have also been observed following stroke”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Hobohm et al., 2005
In cortical areas surrounding the infarct and outside of the glial scar, WFA-expressing PNNs are completely degraded by day 7.
“in cortical areas surrounding the infarct and outside of the glial scar, WFA-expressing PNNs are completely degraded by day 7”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Hobohm et al., 2005
Data on changes in PNs after stroke remain rather limited.
“However, data on the changes in PNs after stroke remain rather limited.”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Hobohm et al., 2005
Hobohm et al. (2005) found that 7 days after experimental stroke induced by invasive electrocoagulative occlusion of the middle cerebral artery in rats, PNs were damaged in the primarily affected neocortex and in more distant thalamic nuclei.
“Hobohm et al. (2005) found 7 days after experimental stroke induced by invasive electrocoagulative occlusion of the middle cerebral artery in rats that PNs were damaged in the primarily affected neocortex and in the more distant thalamic nuclei.”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Hobohm et al., 2005
Abolished and decomposed PNs were reported for other animal models of experimentally induced stroke in neocortices of rats.
“Based on WFA staining, abolished and decomposed PNs were also reported for other animal models of experimentally induced stroke in neocortices of rats (Hobohm et al., 2005; Karetko-Sysa et al., 2011; Madinier et al., 2014; Quattromani et al., 2017).”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Hobohm et al., 2005
Metzincin metalloproteases (MMPs, ADAMs, ADAMTS) are the main agents of ECM remodeling and cleave ECM molecules including PNN components.
“The main agents of this remodeling process are three families of metalloproteases collectively known as metzincin family, i.e. ‘matrix metalloproteases’ (MMPs), ‘a disintegrin and matrix metalloproteases’ (ADAMS), and ‘ADAMS with a thrombospondin domain’ (ADAMTS), which cleave ECM molecules, including those that compose PNNs (Fig.2)”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Hobohm et al., 2005
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- Authors
- Hobohm, C., Günther, A., Grosche, J., Roßner, S., Schneider, D., & Brückner, G.
- Affiliations
- Leipzig University (DE)
- Corresponding author
- Brückner, Gert
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2005-04
- Volume
- 80
- Issue
- 4
- Pages
- 539-548
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W2072975935
- Cited by
- 103
- References
- 78
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 8 · 2023: 3 · 2022: 8 · 2021: 5 · 2020: 7 · 2019: 4 · 2018: 8 · 2017: 9 · 2016: 5 · 2015: 8 · 2014: 7 · 2013: 3 · 2012: 3
- FWCI
- 1.09
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroscience Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Neurology › Neurological Disorders and Treatments
- Keywords
- perineuronal nets, extracellular matrix, focal cerebral ischemia, middle cerebral artery occlusion, chondroitin sulfate proteoglycans, glycosaminoglycan degradation, proteoglycan core protein, glial scar, cortical interneurons, stroke, spontaneously hypertensive rats, neurodegeneration
- MeSH terms
- Animals, Cell Count, Cerebral Cortex, Brain Ischemia, Disease Models, Animal, Extracellular Matrix, Gene Expression Regulation, Glial Fibrillary Acidic Protein, Immunohistochemistry, Functional Laterality, Male, Models, Biological, Nerve Net, Parvalbumins, Proteoglycans, Rats, Inbred SHR, Thalamus, Time Factors, Receptors, N-Acetylglucosamine, Plant Lectins, Rats
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