Perineuronal nets provide a polyanionic, glia‐associated form of microenvironment around certain neurons in many parts of the rat brain
Abstract
The nature and function of previously described perineuronal nets are still obscure. In the present study their polyanionic components were demonstrated in the rat brain using colloidal iron hydroxide (CIH) staining. In subcortical regions, such as the red nucleus, cerebellar, and vestibular nuclei, most neurons were ensheathed by CIH‐binding material. In the cerebral cortex perineuronal nets were seen around numerous nonpyramidal neurons. Biotinylated hyaluronectin revealed that hyaluronan occurs in perineuronal nets. Two plant lectins [ Wisteria floribunda agglutinin (WFA) and Vicia villosa agglutinin (VVA)] with affinity for N‐acetylgalactosamine visualized perineuronal nets similar to those rich in anionic components. Glutamic acid decarboxylase (GAD)‐immunoreactive synaptic boutons were shown to occupy numerous meshes of perineuronal VVA‐positive nets. Electron microscopically, VVA binding sites were scattered throughout perisynaptic profiles, but accumulated at membranes and in the extra‐cellular space except not in synaptic clefts. To investigate the spatial relationship between glial cell processes and perineuronal nets, two astrocytic markers (S100‐protein and glutamine synthetase) were visualized at the light and electron microscopic level. Two methods to detect microglia by the use of Griffonia simplicifolia agglutinin (GSA I‐B 4 ) and the monoclonal antibody, OX‐42, were also applied. Labelled structures forming perineuronal nets were observed with both astrocytic, but not with microglial, markers. It is concluded that perineuronal nets are composed of a specialized type of glia‐associated extracellular matrix rich in polyanionic groups and N‐acetylgalactosamine. The net‐like appearance is due to perisynaptic arrangement of the astrocytic processes and these extracellular components. Similar to the ensheathment of nodes of Ranvier, perineuronal nets may provide a special ion buffering capacity required around various, perhaps highly active, types of neurons. © 1993 Wiley‐Liss, Inc.
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Sulphate groups on GAGs together with negatively charged hyaluronic acid generate a highly polyanionic microenvironment around PN-ensheathed neurons.
“Sulphate groups attached to these GAGs in concert with the negatively charged hyaluronic acid generate a highly polyanionic microenvironment around PN-ensheathed neurons.20, 21”
From Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress (2014) · cites this paper as [20]
Iron ions are involved in generating oxidative stress.
“the polyanionic components might also interact with ions of potential pathophysiological relevance such as iron ions involved in generating oxidative stress.20, 22, 26, 27”
From Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress (2014) · cites this paper as [20]
Astrocytes extend their processes into PNNs localized near the synapse.
“Astrocytes extend their processes into PNNs localized near the synapse (Brückner et al., 1993; Blümcke et al., 1995), suggesting a tetrapartite synaptic organization involving ECM, pre/post synaptic sites and astrocytes (Dityatev and Rusakov, 2011; Smith et al., 2015) whose synergistic functions remain unexplored.”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Brückner et al., 1993
Perineuronal nets carry a high degree of negative charge and may function as cation sinks.
“First, PNNs carry a high degree of negative charge and may function as cation sinks (Bruckner et al, 1993).”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Bruckner et al, 1993
Perineuronal nets (PNs) are polyanionic, chondroitin sulfate proteoglycan (CSPG)-rich coatings of certain neurons.
“As part of the extracellular matrix (ECM), perineuronal nets (PNs) are polyanionic, chondroitin sulfate proteoglycan (CSPG)-rich coatings of certain neurons, known to be affected in various neural diseases.”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Brückner et al., 1993
PNs are composed of chondroitin sulfate proteoglycans (CSPGs) and their glycosaminoglycans, hyaluronic acid and tenascins, produced by various neural cell types.
“They are composed of chondroitin sulfate proteoglycans (CSPGs) and their glycosaminoglycans, hyaluronic acid and tenascins, produced by various neural cell types (Brückner et al., 1993).”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Brückner et al., 1993
WFA-labeled PNNs are associated with more heterogeneous neuronal phenotypes than previously thought, including several subgroups of interneurons, a small subset of cortico-cortical pyramidal cells, spinal cord motor neurons, and cerebellum Purkinje cells.
“More recent evidence indicates that WFA-labeled PNNs are associated with more heterogeneous neuronal phenotypes than previously thought, including several subgroups of interneurons, a small subset of cortico-cortical pyramidal cells, spinal cord motor neurons and cerebellum Purkinje cells (Ajmo et al., 2008; Brauer et al., 1995; Bruckner et al., 1993; Gati and Lendvai, 2013; Hartig et al., 1995;”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Bruckner et al., 1993
Evidence links PNNs to ion homeostasis near neurons with high activity.
“PNNs have been implicated in ion homeostasis around highly active neurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Bruckner et al., 1993
PNNs can potentially act as a buffering system for calcium, potassium, and sodium around highly active neurons, although direct evidence is lacking.
“They can thus potentially act as a buffering system for physiologically relevant ions such as calcium, potassium, and sodium around highly active types of neurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Bruckner et al., 1993
Perineuronal nets are most prominently displayed around GABAergic interneurons, with parvalbumin-expressing cells showing the highest level of colocalization.
“The PNN is a unique ECM structure that is most prominently displayed around GABAergic interneurons, with parvalbumin expressing cells having the highest level of colocalization (Brückner et al., 1993;Celio and Chiquet-Ehrismann, 1993;Morris and Henderson, 2000).”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Brückner et al., 1993
Perineuronal nets are extracellular matrix structures which surround synapses of highly active neuronal subtypes and are associated with microglia.
“Perineuronal nets are extracellular matrix structures which surround synapses of highly active neuronal subtypes and are associated with microglia [156].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [156]
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Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease
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Self-citationThe perineuronal net component of the extracellular matrix in plasticity and epilepsy
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Aggrecan: Beyond cartilage and into the brain
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Self-citationCollagens in the developing and diseased nervous system
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Self-citationCell-Mediated Neuroprotection in a Mouse Model of Human Tauopathy
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An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity
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Versican V2 Assembles the Extracellular Matrix Surrounding the Nodes of Ranvier in the CNS
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Morawski, M., Reinert, T., Meyer-Klaucke, W., Wagner, F. E., Tröger, W., Reinert, A., Jäger, C., Brückner, G., & Arendt, T. (2015) · Scientific Reports · doi:10.1038/srep16471 · Cited by 116 · see citing works
Self-citationShi, W., Wei, X., Wang, X., Du, S., Liu, W., Song, J., & Wang, Y. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1902680116 · Cited by 122 · see citing works
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Axon initial segment ensheathed by extracellular matrix in perineuronal nets
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Self-citationIn Sickness and in Health: Perineuronal Nets and Synaptic Plasticity in Psychiatric Disorders
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Protective Properties of Neural Extracellular Matrix
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Self-citationNeurons Produce a Neuronal Cell Surface-Associated Chondroitin Sulfate Proteoglycan
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Self-citationPerineuronal net degradation in epilepsy
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Perineuronal nets protect against amyloid β-protein neurotoxicity in cultured cortical neurons
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Perineuronal nets and schizophrenia: The importance of neuronal coatings
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Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat
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The crosstalk of hyaluronan-based extracellular matrix and synapses
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- Authors
- Brückner, G., Brauer, K., Härtig, W., Wolff, J. R., Rickmann, M. J., Derouiche, A., Delpech, B., Girard, N., Oertel, W. H., & Reichenbach, A.
- Affiliations
- Leipzig University (DE)
- University of Göttingen (DE)
- Goethe University Frankfurt (DE)
- Centre Henri Becquerel (FR)
- Ludwig-Maximilians-Universität München (DE)
- Corresponding author
- Brückner, Gert
- Venue
- Glia
- Publisher
- Wiley
- Published
- 1993-07
- Volume
- 8
- Issue
- 3
- Pages
- 183-200
- ISSN
- 0894-1491 (ISSN-L)
- 1098-1136
- OpenAlex
- W2099040370
- Cited by
- 358
- References
- 74
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 7 · 2023: 9 · 2022: 17 · 2021: 13 · 2020: 16 · 2019: 13 · 2018: 25 · 2017: 19 · 2016: 17 · 2015: 10 · 2014: 10 · 2013: 13 · 2012: 14
- FWCI
- 2.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Glia (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- perineuronal nets, N-acetylgalactosamine, hyaluronic acid, astrocytes, microglia, glutamine synthetase, S-100 protein, glutamic acid decarboxylase, synaptic boutons, red nucleus, cerebellar nuclei, vestibular nuclei, cerebral cortex, lectin binding
- MeSH terms
- Acetylgalactosamine, Animals, Anions, Brain, Brain Chemistry, Colloids, Cytoplasm, Extracellular Matrix, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Glutamate-Ammonia Ligase, Hyaluronic Acid, Hydroxides, S100 Proteins, Neuroglia, Neurons, Organic Chemicals, Staining and Labeling, Synapses, Biomarkers, Rats, Sprague-Dawley, Rats, Wistar, Microglia, Lectins, Rats, Iron Compounds
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