Extracellular matrix modulation is driven by experience-dependent plasticity during stroke recovery.
Open accessAbstract
Following stroke, complete cellular death in the ischemic brain area may ensue, with remaining brain areas undergoing tissue remodelling to various degrees. Experience-dependent brain plasticity exerted through an enriched environment (EE) promotes remodelling after central nervous system injury, such as stroke. Post-stroke tissue reorganization is modulated by growth inhibitory molecules differentially expressed within the ischemic hemisphere, like chondroitin sulfate proteoglycans found in perineuronal nets (PNNs). PNNs in the neocortex predominantly enwrap parvalbumin-containing GABAergic (PV/GABA) neurons, important in sensori-information processing. Here, we investigate how extracellular matrix (ECM) proteases and their inhibitors may participate in the regulation of PNN integrity during stroke recovery. Rats were subjected to photothrombotic stroke in the motor cortex, and functional deficits were assessed at 7 days of recovery. Sham and stroked rats were housed in either standard or EE conditions for 5 days, and infarct volumes were calculated. PNNs were visualized by immunohistochemistry and counted in the somatosensory cortex of both hemispheres. mRNA expression levels of ECM proteases and protease inhibitors were assessed by RT-qPCR and their activity analyzed by gel zymography. PNNs and protease activity were also studied in brains from stroke patients where similar results were observed. EE starting 2 days after stroke and continuing for 5 days stimulated behavioral recovery of limb-placement ability without affecting infarct size. EE promoted a decrease of PNNs around PV/GABA neurons and a concomitant modulation of the proteolytic activity and mRNA expression of ECM proteases and protease inhibitors in the somatosensory cortex. This study provides molecular targets for novel therapies that could support rehabilitation of stroke patients.
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Rats housed in enriched environments following ischemic damage exhibited faster neurological recovery compared to rats placed in standard housing.
“recent findings in rodent stroke models indicate that rats housed in enriched environments following ischemic damage exhibited faster neurological recovery compared to rats placed in standard housing (Madinier et al., 2014; Quattromani et al., 2018).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Quattromani et al., 2018
Ischemia-induced damage of PNs in rat neocortices was analyzed by Bidmon et al. (1998) and by Wieloch's research group using a similar animal model.
“Using a similar animal model, ischemia-induced damage of PNs in rat neocortices was analyzed by Bidmon et al. (1998) and by Wieloch’s research group (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 Quattromani et al., 2017
Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction modulated activity and mRNA expression of extracellular matrix proteases and their inhibitors.
“Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced PNs, modulated activity and mRNA expression of ECM proteases and their inhibitors, accompanied by enhanced recovery of limb placement ability (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 Quattromani et al., 2017
Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced perineuronal nets.
“Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced PNs, modulated activity and mRNA expression of ECM proteases and their inhibitors, accompanied by enhanced recovery of limb placement ability (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 Quattromani et al., 2017
Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction was accompanied by enhanced recovery of limb placement ability.
“Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced PNs, modulated activity and mRNA expression of ECM proteases and their inhibitors, accompanied by enhanced recovery of limb placement ability (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 Quattromani et al., 2017
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- Authors
- Quattromani, M. J., Pruvost, M., Guerreiro, C., Backlund, F., Englund, E., Aspberg, A., Jaworski, T., Hakon, J., Ruscher, K., Kaczmarek, L., Vivien, D., & Wieloch, T.
- Affiliations
- Lund University (SE)
- Inserm (FR)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- Corresponding author
- Quattromani, Miriana Jlenia
- ORCID
- Venue
- Molecular Neurobiology
- Published
- 2017-03-13
- Volume
- 55
- Issue
- 3
- Pages
- 2196-2213
- ISSN
- 0893-7648 (ISSN-L)
- 1559-1182
- PMC
- PMC5840227
- OpenAlex
- W2597229620
- Cited by
- 39
- References
- 78
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 4 · 2021: 2 · 2020: 6 · 2019: 4 · 2018: 8 · 2017: 3
- FWCI
- 5.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Molecular Neurobiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- Vetenskapsrådet (2011-2652, 2014-3802)
- Hans-Gabriel and Alice Trolle-Wachtmeister Foundation
- Strategic Research Area MultiPark
- Pia Ståhl Foundation
- Kungliga Fysiografiska Sällskapet i Lund
- STROKE-Riksförbundet
- Topics
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Keywords
- stroke recovery, extracellular matrix, perineuronal nets, chondroitin sulfate proteoglycans, experience-dependent plasticity, environmental enrichment, protease inhibitors, parvalbumin interneurons, GABAergic neurons, somatosensory cortex, photothrombotic stroke, stroke rehabilitation, tissue remodeling
- MeSH terms
- Stroke Rehabilitation, Aged, Aged, 80 and over, Animals, Environment, Extracellular Matrix, Female, Humans, Male, Middle Aged, Neuronal Plasticity, Inflammation Mediators, Recovery of Function, Stroke, Rats
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