Composition of Perineuronal Net Extracellular Matrix in Rat Brain
Open accessAbstract
We developed a method to extract differentially chondroitin sulfate proteoglycans (CSPGs) that are diffusely present in the central nervous system (CNS) matrix and CSPGs that are present in the condensed matrix of perineuronal nets (PNNs). Adult rat brain was sequentially extracted with Tris-buffered saline (TBS), TBS-containing detergent, 1 m NaCl, and 6 m urea. Extracting tissue sections with these buffers showed that the diffuse and membrane-bound CSPGs were extracted in the first three buffers, but PNN-associated CSPGs remained and were only removed by 6 m urea. Most of the CSPGs were extracted to some degree with all the buffers, with neurocan, brevican, aggrecan, and versican particularly associated with the stable urea-extractable PNNs. The CSPGs in stable complexes only extractable in urea buffer are found from postnatal day 7-14 coinciding with PNN formation. Disaccharide composition analysis indicated a different glycosaminoglycan (GAG) composition for PGs strongly associated with extracellular matrix (ECM). For CS/dermatan sulfate (DS)-GAG the content of nonsulfated, 6-O-sulfated, 2,6-O-disulfated, and 4,6-O-disulfated disaccharides were higher and for heparan sulfate (HS)-GAG, the content of 6-O-sulfated, 2-N-, 6-O-disulfated, 2-O-, 2-N-disulfated, and 2-O-, 2-N-, 6-O-trisulfated disaccharides were higher in urea extract compared with other buffer extracts. Digestions with chondroitinase ABC and hyaluronidase indicated that aggrecan, versican, neurocan, brevican, and phosphacan are retained in PNNs through binding to hyaluronan (HA). A comparison of the brain and spinal cord ECM with respect to CSPGs indicated that the PNNs in both parts of the CNS have the same composition.
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PNNs tightly interdigitate with synaptic contacts on the soma and proximal dendrites of neurons.
“the unique, lattice--like structures that wrap around specific neurons in the brain and spinal cord called perineuronal nets (PNNs) that tightly interdigitate with synaptic contacts on the soma and proximal dendrites of neurons (Celio et al., 1998;Deepa et al., 2006;Soleman et al., 2013).”
From Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity (2016) · cites this paper as Deepa et al., 2006
4-O-sulfation becomes dominant in the adult brain to produce C4S, which is the most inhibitory form of CS.
“whereas 4--O--sulfation becomes dominant in the adult brain to produce C4S, which is the most inhibitory form of CS: it inhibits the growth of cerebellar granular neurons in culture and is upregulated in regions that do not support axonal growth after spinal cord injury (Deepa et al., 2006;Wang et al., 2008).”
From Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity (2016) · cites this paper as Deepa et al., 2006
The core structure of PNNs consists of chondroitin sulfate proteoglycans of the lectican family, hyaluronan, tenascins, particularly tenascin-R, and link proteins for stabilization.
“The core structure of PNNs consists of chondroitin sulfate proteoglycans (CSPGs) of the lectican family17,18, hyaluronan19,20, tenascins, particularly tenascin-R (TnR)21,22 and link proteins23,24 for stabilization.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [17]
CSPGs are organizers of the ECM and are highly represented in PNNs, with aggrecan, neurocan, brevican, versican, and phosphacan among the most abundant.
“CSPGs, the organizers of the ECM, are highly represented in PNNs, with aggrecan, neurocan, brevican, versican and phosphacan among the most abundant (Deepa et al., 2006; Giamanco and Matthews, 2012; Yamaguchi, 2000).”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Deepa et al., 2006
PNN components include chondroitin sulfate proteoglycans, hyaluronan, tenascin-R, link proteins, Reelin, and semaphorin 3A.
“Their components include chondroitin sulfate proteoglycans (CSPGs), hyaluronan, tenascin-R, link proteins, Reelin and semaphorin 3A (Carulli et al., 2013b; Deepa et al., 2006; Dick et al., 2013; Matthews et al., 2002; Vo et al., 2013a).”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Deepa et al., 2006
Sema3A binds PNNs via CS-E, which is enriched in PNNs.
“Particularly, Sema3A has been shown to bind PNNs via CS-E (Dick et al., 2013), which is enriched in PNNs (Deepa et al., 2006).”
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 Deepa et al., 2006
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Self-citation
- Authors
- Deepa, S. S., Carulli, D., Galtrey, C., Rhodes, K., Fukuda, J., Mikami, T., Sugahara, K., & Fawcett, J. W.
- Affiliations
- University of Cambridge (GB)
- Kobe Pharmaceutical University (JP)
- Corresponding author
- Fawcett, James W.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2006-06
- Volume
- 281
- Issue
- 26
- Pages
- 17789-17800
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2003726233
- Cited by
- 367
- References
- 86
- Citations by year
- 2026: 14 · 2025: 17 · 2024: 22 · 2023: 20 · 2022: 23 · 2021: 23 · 2020: 34 · 2019: 20 · 2018: 21 · 2017: 25 · 2016: 13 · 2015: 24 · 2014: 23 · 2013: 24 · 2012: 10
- FWCI
- 4.28
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- 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 › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- perineuronal nets, chondroitin sulfate proteoglycans, extracellular matrix, glycosaminoglycan composition, neurocan, brevican, aggrecan, versican, phosphacan, hyaluronic acid, chondroitinase ABC, hyaluronidase, urea extraction, postnatal development, brain, spinal cord
- MeSH terms
- Age Factors, Animals, Biochemistry, Brain Chemistry, Buffers, Detergents, Disaccharides, Hyaluronoglucosaminidase, Nerve Tissue Proteins, Neuronal Plasticity, Chondroitin Sulfate Proteoglycans, Proteoglycans, Spinal Cord, Streptomyces, Extracellular Matrix Proteins, Rats, Sprague-Dawley, Lectins, C-Type, Rats, Aggrecans, Receptor-Like Protein Tyrosine Phosphatases, Class 5, Neurocan, Brevican
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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