Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components
Abstract
The decrease in plasticity that occurs in the central nervous system during postnatal development is accompanied by the appearance of perineuronal nets (PNNs) around the cell body and dendrites of many classes of neuron. These structures are composed of extracellular matrix molecules, such as chondroitin sulfate proteoglycans (CSPGs), hyaluronan (HA), tenascin‐R, and link proteins. To elucidate the role played by neurons and glial cells in constructing PNNs, we studied the expression of PNN components in the adult rat cerebellum by immunohistochemistry and in situ hybridization. In the deep cerebellar nuclei, only large excitatory neurons were surrounded by nets, which contained the CSPGs aggrecan, neurocan, brevican, versican, and phosphacan, along with tenascin‐R and HA. Whereas both net‐bearing neurons and glial cells were the sources of CSPGs and tenascin‐R, only the neurons expressed the mRNA for HA synthases (HASs), cartilage link protein, and link protein Bral2. In the cerebellar cortex, Golgi neurons possessed PNNs and also synthesized HASs, cartilage link protein, and Bral2 mRNAs. To see whether HA might link PNNs to the neuronal cell surface by binding to a receptor, we investigated the expression of the HA receptors CD44, RHAMM, and LYVE‐1. No immunolabelling for HA receptors on the membrane of net‐bearing neurons was found. We therefore propose that HASs, which can retain HA on the cell surface, may act as a link between PNNs and neurons. Thus, HAS and link proteins might be key molecules for PNN formation and stability. J. Comp. Neurol. 494:559–577, 2006. © 2005 Wiley‐Liss, Inc.
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Delayed eyeblink conditioning requires neurons in the deep cerebellar nuclei, many of which are surrounded by PNNs.
“Delayed eyeblink conditioning is a type of associative conditioning that requires neurons in the deep cerebellar nuclei (DCN) [76], many of which are surrounded by PNNs [77].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [77]
Perineuronal nets surround both inhibitory and excitatory neurons.
“PNNs enwrap both inhibitory and excitatory neurons (Carulli et al. 2006)”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Carulli et al. 2006
The two link proteins found in perineuronal nets are Hapln1/Crtl1 and Hapln4/Bral2.
“Two are the link proteins found in PNNs: Hapln1/Crtl1 and Hapln4/Bral2.”
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 Carulli et al., 2006
Hapln1/Crtl1 and Hapln4/Bral2 are expressed exclusively in neurons bearing a perineuronal net.
“These Haplns are expressed exclusively in neurons bearing a PNN (Bekku et al., 2003;Carulli et al., 2006;Galtrey et al., 2008;Rauch et al., 2004) and are essential for the proper assembly of the PNN structure.”
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 Carulli et al., 2006
WFA-positive nets are localized around different neuronal types, including parvalbumin-expressing GABAergic neurons in cortical areas, cortical pyramidal neurons, glutamatergic neurons in cerebellar nuclei, and glycinergic neurons of the medial nucleus of the trapezoid body.
“WFA-positive nets are localised around different neuronal types, such as parvalbumin-expressing GABAergic neurons in cortical areas (see above), as well as cortical pyramidal neurons (Alpár et al., 2006;Hartig et al., 2001;Takahashi-Iwanaga et al., 1998;Wegner et al., 2003), glutamatergic neurons in the cerebellar nuclei (Carulli et al., 2006) and glycinergic neurons of the medial nucleus of the”
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 Carulli et al., 2006
All four lecticans are found in perineuronal nets.
“All four lecticans are found in PNNs (Carulli et al., 2006(Carulli et al., , 2010;;Hagihara et al., 1999;Matsui et al., 1998;Zimmermann and Dours-Zimmermann, 2008).”
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 Carulli et al., 2006
Hapln1/Crtl1 and Hapln4/Bral2 are essential for proper assembly of the perineuronal net structure.
“These Haplns are expressed exclusively in neurons bearing a PNN (Bekku et al., 2003;Carulli et al., 2006;Galtrey et al., 2008;Rauch et al., 2004) and are essential for the proper assembly of the PNN structure.”
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 Carulli et al., 2006
Molecules crucial for perineuronal net assembly, namely hyaluronan synthases, link proteins, and aggrecan, are exclusively synthesized by neurons, whereas astrocytes, oligodendrocyte precursors, and oligodendrocytes produce other ECM molecules likely incorporated into the PNN.
“As to the cellular origin of PNN components, molecules that are crucial for PNN assembly, namely HAS, link proteins and aggrecan, are exclusively synthesized by neurons, whereas astrocytes, oligodendrocyte precursors and oligodendrocytes produce other ECM molecules, which are then likely incorporated into the PNN (Carulli et al., 2006(Carulli et al., , 2007;;Lander et al., 1998; see table I).”
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 Carulli et al., 2006
Neurons in the cerebellar nuclei and visual cortex express HAS-2 and HAS-3, while neurons in the spinal cord express HAS-1 and HAS-3.
“Neurons in the cerebellar nuclei and visual cortex express HAS-2 and -3, while neurons in the spinal cord express HAS-1 and -3 (Carulli et al., 2006(Carulli et al., , 2010;;Galtrey et al., 2008).”
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 Carulli et al., 2006
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- Authors
- Carulli, D., Rhodes, K. E., Brown, D. J., Bonnert, T. P., Pollack, S. J., Oliver, K., Strata, P., & Fawcett, J. W.
- Affiliations
- University of Cambridge (GB)
- MSD (UK) Limited (United Kingdom) (GB)
- University of Turin (IT)
- Corresponding author
- Fawcett, James W.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2005-12-22
- Volume
- 494
- Issue
- 4
- Pages
- 559-577
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2125814499
- Cited by
- 341
- References
- 12
- Citations by year
- 2026: 18 · 2025: 17 · 2024: 18 · 2023: 16 · 2022: 18 · 2021: 15 · 2020: 19 · 2019: 18 · 2018: 20 · 2017: 22 · 2016: 15 · 2015: 19 · 2014: 13 · 2013: 22 · 2012: 21
- FWCI
- 5.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion)
- 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, cerebellum, chondroitin sulfate proteoglycans, hyaluronic acid, tenascin-R, link protein, hyaluronan synthase, deep cerebellar nuclei, cerebellar cortex, CD44, RHAMM, LYVE-1, extracellular matrix, glial cells, neuron-glia interactions
- MeSH terms
- Hyaluronan Synthases, Animals, Cerebellum, Extracellular Matrix, Female, Hyaluronic Acid, Nerve Tissue Proteins, Neuroglia, Neuronal Plasticity, Neurons, Chondroitin Sulfate Proteoglycans, Glucuronosyltransferase, Rats, Sprague-Dawley, In Situ Hybridization, Hyaluronan Receptors, Rats
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