The DOI matches its Crossref record; 86 of the 86 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
Citations
Cites
Chondroitinase ABC promotes functional recovery after spinal cord injury
Bradbury, E. J., Moon, L. D. F., Popat, R. J., King, V. R., Bennett, G. S., Patel, P. N., Fawcett, J. W., & McMahon, S. B. (2002) · Nature · doi:10.1038/416636a · Cited by 2,357
Self-citationHyaluronan: from extracellular glue to pericellular cue
Toole, B. P. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1391 · Cited by 2,125
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679
Self-citationSulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro
Snow, D. M., Lemmon, V., Carrino, D. A., Caplan, A. I., & Silver, J. (1990) · Experimental Neurology · doi:10.1016/s0014-4886(05)80013-5 · Cited by 776
Lecticans: organizers of the brain extracellular matrix
Yamaguchi, Y. (2000) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000690 · Cited by 642
Proteoglycans in the Developing Brain: New Conceptual Insights for Old Proteins
Bandtlow, C. E., & Zimmermann, D. R. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.4.1267 · Cited by 632
Moon, L. D. F., Asher, R. A., Rhodes, K. E., & Fawcett, J. W. (2001) · Nature Neuroscience · doi:10.1038/87415 · Cited by 569
Self-citationHyaluronan-binding Proteins: Tying Up the Giant
Day, A. J., & Prestwich, G. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.r100036200 · Cited by 567
Novel hyaluronidase from streptomyces
Takaichi, O. H. Y. A., & Kaneko, Y. (1970) · Biochimica et Biophysica Acta (BBA) - Enzymology · doi:10.1016/0005-2744(70)90139-7 · Cited by 518
Perineuronal nets: past and present
Celio, M. R., Spreafico, R., De Biasi, S., & Vitellaro-Zuccarello, L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01298-3 · Cited by 497
Flagged first, then by citations
Research works printed but not linked: 1
- Levine, 1996, Perspect. Dev. Neurobiol., 3, 245
Cited by
Sorted by citations
Items 301–369 of 369
Wéber, I., Dakos, A., Mészár, Z., Matesz, C., & Birinyi, A. (2024) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2024.1369103 · Cited by 3
Perineuronal Nets: Old Structures, New Functions
Tewari, B. P., Chaunsali, L., & Sontheimer, H. W. (2026) · The Neuroscientist · doi:10.1177/10738584261421180 · Cited by 3
Post-Stroke Recovery in Relation to Parvalbumin-Positive Interneurons and Perineuronal Nets
Kuhl, L. M., Jeffers, M. S., Hristozov, N., Karthikeyan, S., McDonald, M. W., Hufnagel, A., Carter, A., Dancause, N., & Corbett, D. (2025) · Neurorehabilitation and neural repair · doi:10.1177/15459683241309567 · Cited by 4
Fingolimod increases parvalbumin-positive neurons in adult mice
Ueno, H., Takahashi, Y., Murakami, S., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2022) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2022.06.005 · Cited by 3
Neural extracellular matrix regulates visual sensory motor integration
Reinhard, J., Mueller-Buehl, C., Wiemann, S., Roll, L., Luft, V., Shabani, H., Rathbun, D. L., Gan, L., Kuo, C., Franzen, J., et al. (2024) · iScience · doi:10.1016/j.isci.2024.108846 · Cited by 3
Iwakura, Y., Kobayashi, Y., Namba, H., Nawa, H., & Takei, N. (2024) · Neurochemical Research · doi:10.1007/s11064-024-04122-y · Cited by 3
Descriptive study of perineuronal net in enteric nervous system of humans and mice
da Silva, M. D. V., Bacarin, C. C., Machado, C. C. A., Franciosi, A., Mendes, J. D. D. L., Watanabe, P. D. S., Miqueloto, C. A., Fattori, V., Albarracin, O. Y. E., Verri, W. A., Jr., et al. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16159 · Cited by 3
Molecular mechanisms of spinal cord injury repair across vertebrates: A comparative review
Jiang, Y., Cai, Y., Yang, N., Gao, S., Li, Q., Pang, Y., & Su, P. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16462 · Cited by 3
Eisele, B. S., Wu, A. J., Luka, Z., Hale, A. T., & York, J. D. (2021) · Advances in Biological Regulation · doi:10.1016/j.jbior.2021.100858 · Cited by 3
Liu, J. R., & Modo, M. (2018) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155418771677 · Cited by 3
Fawcett, J. W. (2008) · Elsevier eBooks · doi:10.1016/b978-012373994-0.50016-6 · Cited by 3
Self-citationPerineuronal net receptor PTPσ regulates retention of memoriesPreprint
Lesnikova, A., Casarotto, P. C., Biojone, C., & Ċastrén, E. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.26.433000 · Cited by 3
Grødem, S., Thompson, E. H., Røe, M. B., Vatne, G. H., Nymoen, I., Buccino, A. P., Madland, T., Hafting, T., Fyhn, M., & Lensjø, K. K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.20.585910 · Cited by 3
New routes to the neuroendocrine hypothalamus: the extracellular space
Nicolas, J. C., Huwart, S. J. P., Ziemens, D., Freire-Agulleiro, Ó., Lee, T. H.-Y., Mattot, V., & Quarta, C. (2025) · European Journal of Endocrinology · doi:10.1093/ejendo/lvaf197 · Cited by 2
PTSD and appetite dysregulation: mTOR-dependent modulation of fear memory and satiety circuits
Krattli, S. N., Li, A. S., & McLachlan, C. S. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106495 · Cited by 2
Gómez, A., Tran, U. T., Grozdanov, P. N., & Cornwall, G. A. (2026) · Journal of Neuroscience Research · doi:10.1002/jnr.70113 · Cited by 2
Huang, Y.-F., Liu, C., Liu, Z., Zhuang, X., Chen, J.-H., Zhang, Z.-N., Shen, C., & Hu, Y. (2026) · Brain · doi:10.1093/brain/awag058 · Cited by 3
Ma, D., & Gu, C. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105897 · Cited by 2
Axon Regeneration in the Lamprey Spinal Cord
Shifman, M. I., & Selzer, M. E. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801732-6.00004-5 · Cited by 2
Neural extracellular matrix regulates visual sensory motor integrationPreprint
Reinhard, J., Mueller-Buehl, C., Wiemann, S., Roll, L., Luft, V., Shabani, H., Rathbun, D. L., Gan, L., Kuo, C., Franzen, J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.17.537074 · Cited by 2
Blanco, I., Chen, S., Yeo, E., Reasonover, S. R., & Santisteban, M. M. (2025) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-025-01628-z · Cited by 1
Proteoglycans of the Central Nervous System
Gupta, G. (2012) · Springer eBooks · doi:10.1007/978-3-7091-1065-2_38 · Cited by 1
Chondroitinase Gene Therapy for Spinal Cord Injury
Hu, J., Curinga, G., & Smith, G. M. (2014) · Neuromethods · doi:10.1007/978-1-4939-2083-9_12 · Cited by 1
Spatial computations in entorhinal cortex after degradation of perineuronal nets
Kvello, A. M. S. (2014) · NORA - Norwegian Open Research Archives · Cited by 1
The Role of Perineuronal Nets in Regulating Barrel Cortex Physiology
Chu, P. (2015) · CUNY Academic Works (City University of New York) · Cited by 1
Tobacco pharming. A quest to turn the killer crop into a treatment for cancer.
Powledge, T. M. (2001) · PubMed · Cited by 1
Gibel-Russo, R., & Nardo, A. A. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.04.578782 · Cited by 1
Unravelling the Roles of Proteinases in Cell Migration In Vitro and In Vivo
Gavrilović, J., & Scott, X. (2008) · Springer eBooks · doi:10.1007/978-0-387-69057-5_18
Plasticity after injury to the central nervous system
Selzer, M. A., Clarke, S., Cohen, L. G., Kwakkel, G., & Miller, R. H. (2014) · Cambridge University Press eBooks · doi:10.1017/cbo9780511995583.014
Araujo, O. A. D., & Folha, C. (2013)
Lanton, R. A. (2015) · NORA - Norwegian Open Research Archives
Investigating chondroitin sulphate proteoglycans as a therapeutic target for Parkinson's disease
Fletcher, E. J. R. (2017) · Research Portal (King's College London)
Regulation of glycosaminoglycan biogenesis is critical for sensitive‐period‐dependent vocal ontogeny
Mencio, C. P., Tran, V. M., Quintero, M. V., Koketsu, M., Goller, F., & Kuberan, B. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22547
In vivo and in vitro guidance of developing neurons by mechanical cues
Thompson, A. J. (2018) · Apollo (University of Cambridge) · doi:10.17863/cam.26465
Versican Expression During Embryonic Development in the Mouse
Snyder, J. M. (2014) · ResearchWorks at the University of Washington (University of Washington)
Perineuronal nets in memory processing and behavior
Thompson, E. H. (2020) · NORA - Norwegian Open Research Archives
Interaction between perineuronal nets and ketamine in antidepressant actionPreprint
Young, C. K., Kinley, K. G., & McNaughton, N. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.30.446326
Structural and Functional Remodeling of the Extracellular Matrix during Brain Development and Aging
Miyata, S. (2021) · Trends in Glycoscience and Glycotechnology · doi:10.4052/tigg.2003.1e
Structural and Functional Remodeling of the Extracellular Matrix during Brain Development and Aging
Miyata, S. (2021) · Trends in Glycoscience and Glycotechnology · doi:10.4052/tigg.2003.1j
Identification of novel intracellular mechanisms in developmental spine pruning through Ankyrin B.
Wyatt, E. V. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/nv7d-dp91
Alba, N. A. (2013) · D-Scholarship@Pitt (University of Pittsburgh)
Minnick, C. (2017) · Wiley eBooks · doi:10.1002/9781394406418.part4
Wéber, I., Dakos, A., Mészár, Z., Matesz, C., & Birinyi, A. (2023) · Research Square · doi:10.21203/rs.3.rs-3184150/v1
Dzyubenko, E., Willig, K. I., Yin, D., Sardari, M., Tokmak, E., Labus, P., Schmermund, B., & Hermann, D. M. (2023) · Figshare · doi:10.6084/m9.figshare.24076907
Dzyubenko, E., Willig, K. I., Yin, D., Sardari, M., Tokmak, E., Labus, P., Schmermund, B., & Hermann, D. M. (2023) · Figshare · doi:10.6084/m9.figshare.24076901
Dzyubenko, E., Willig, K. I., Yin, D., Sardari, M., Tokmak, E., Labus, P., Schmermund, B., & Hermann, D. M. (2023) · Figshare · doi:10.6084/m9.figshare.24076904
Benacom, D., Chataing, C., Prochiantz, A., & Nardo, A. A. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.31.596849
Activity-dependent extracellular proteolytic cascade remodels ECM to promote structural plasticityPreprint
Singh, J. B., Perelló‐Amorós, B., Schneeberg, J., Seidenbecher, C. I., Fejtová, A., Dityatev, A. E., & Frischknecht, R. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.28.620597
Zhang, H., Cicvaric, A., Bassett, T. E., Wood, E. M., Petrovic, Z., & Radulović, J. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00066-3
Fernandez-Ballester, M., Ardaya, M., Dutheil, N., Largitte, L.-A., Martín, A., & Soria, F. N. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.31.635882
Dzyubenko, E., Willig, K. I., Yin, D., Sardari, M., Tokmak, E., Labus, P., Schmermund, B., & Hermann, D. M. (2023) · Figshare · doi:10.6084/m9.figshare.24076910
del Campo, I. S. F., Cebrián-León, A., Caño, C. H.-D., Varela-Andrés, N., Plaza, I., Deogracias, R., & Merchán, M. Á. (2026) · Hearing Research · doi:10.1016/j.heares.2026.109580
Sepulveda-Diaz, J. E. (2013) · theses.fr (ABES) · doi:10.70675/56c42bcbz41dfz432bzbb78z77110b373285
Synaptic changes upon removal of extracellular perineuronal nets in adult mouse visual cortex
Faini, G. (2017) · theses.fr (ABES) · doi:10.70675/7b38d504z7edfz47dezbf9az0a8668ae448a
Devienne, G. F. (2019) · theses.fr (ABES) · doi:10.70675/453418efzc908z49e0zba6fz71fefaa50691
Etude du rôle du Syndécan à la jonction neuromusculaire de Caenorhabditis elegans
Vachon, C. (2020) · theses.fr (ABES) · doi:10.70675/4f34af1dzeed7z426dzbab2zb1e21a201491
ECM remodeling in the mPFC exacerbates cocaine-induced hyperactivity and impairs threat vigilance
Lin, X., Huo, Y., Wang, X., Yu, J., Liu, Z., Fan, X., Guo, S., Ye, X., Zhang, X., Li, Y., et al. (2026) · Translational Psychiatry · doi:10.1038/s41398-026-04014-5
Douceau, S. (2020) · theses.fr (ABES) · doi:10.70675/6f1007f2z8468z4365zb07dz7d863bf32cd5
Molecular mechanisms underlying the surface organization of the NMDA receptors during development
Bénac, N. (2024) · theses.fr (ABES) · doi:10.70675/e3508a2ezb62ez4f99zb27bz156201271974
Gomez, A., Logsdon, A. F., Bailoo, J. D., & Cornwall, G. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.27.728219
Bhuiyan, M. H., Smith, M. J., Hinkley, S. F. R., & Clarkson, A. N. (2026) · Neuroprotection/Neuroprotection (Chichester, England. Print) · doi:10.1002/nep3.70043
Perineuronal Nets in Neuropsychiatric Disorders
Sikder, S., & Bozdagi-Gunal, O. (2026) · Brain Science Advances · doi:10.26599/bsa.2026.905017
Tanaka, T., Kerever, A., Suzuki, Y., Kunitomi, T., Kato, K., Yamashita, Y., Higashi, K., Akazawa, C., Saitow, F., Suzuki, H., et al. (2026) · Glia · doi:10.1002/glia.70188
The role of nervous system extracellular matrix remodeling in chronic pain
Alhamwi, A., Anits, E., & Krock, E. (2026) · Pain · doi:10.1097/j.pain.0000000000004089
Letko-Khait, N., Li, D. X., Guo, K., Cui, H., Sirianni, Q. E. A., Abdo, D., Morshead, C. M., & Shoichet, M. S. (2026) · Advanced Science · doi:10.1002/advs.202522499
Extracellular matrix and perineuronal nets in neural plasticity, memory, and epileptogenesis
Zhu, H., Li, Q., Li, Y., & Wang, W. (2026) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2026.1945520
Metadata
- 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 ›
Are you an author, or do you see a problem with this page? Request a review