Deconstructing the perineuronal net: Cellular contributions and molecular composition of the neuronal extracellular matrix
Open accessAbstract
Perineuronal nets (PNNs) are lattice-like substructures of the neural extracellular matrix that enwrap particular populations of neurons throughout the central nervous system. Previous work suggests that this structure plays a major role in modulating developmental neural plasticity and brain maturation. Understanding the precise role of these structures has been hampered by incomplete comprehension of their molecular composition and cellular contributions to their formation, which is studied herein using primary cortical cell cultures. By defining culture conditions to reduce (cytosine-β-d-arabinofuranoside/AraC addition) or virtually eliminate (elevated potassium chloride (KCl) and AraC application) glia, PNN components impacted by this cell type were identified. Effects of depolarizing KCl concentrations alone were also assessed. Our work identified aggrecan as the primary neuronal component of the PNN and its expression was dramatically up-regulated by both depolarization and glial cell inhibition and additionally, the development of aggrecan-positive PNNs was accelerated. Surprisingly, most of the other PNN components tested were made in a glial-dependent manner in our culture system. Interestingly, in the absence of these glial-derived components, an aggrecan- and hyaluronan-reactive PNN developed, demonstrating that these two components are sufficient for base PNN assembly. Other components were expressed in a glial-dependent manner. Overall, this work provides deeper insight into the complex interplay between neurons and glia in the formation of the PNN and improves our understanding of the molecular composition of these structures.
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Long hyaluronan chains provide a scaffold for the assembly of CSPGs, hyaluronan, hyaluronin and proteoglycan link proteins (Hapln), and tenascins.
“The long hyaluronan chains provide a scaffold for the assembly of CSPGs, hyaluronan, hyaluronin and proteoglycan link proteins (Hapln), and tenascins [15, 18].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [18]
ACAN+/− mice are aggrecan-deficient.
“heterozygote aggrecan-deficient (ACAN+/−) mice”
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 [43]
Aggrecan is a major component of the brain ECM and of at least a subgroup of PNNs, and contains numerous CS chains with a predominant CS-6 representation.
“Aggrecan is a major component of the brain ECM and of at least a subgroup of PNNs, and contains numerous CS chains with a predominant CS-6 representation.45, 46”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [46]
Reports that aggrecan knockout results in loss of WFA-positive PNNs support the possibility that PNNs may be lost or lack key elements.
“Reports that aggrecan knockout results in loss of WFA-positive PNNs45, 46 support this possibility.”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [46]
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 [20]
Parvalbumin levels and perineuronal net labeling are regulated in an activity-dependent manner.
“Levels of PV (Kinney et al, 2006) and PNN labeling (Dityatev et al, 2007;Giamanco and Matthews, 2012) are regulated in an activity-dependent manner.”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Giamanco and Matthews, 2012
Adamts8 and Adamts15 are two metallopeptidases that could cleave the proteoglycans aggrecan and versican, two major components of the extracellular matrix of the PNN.
“Adamts8 and Adamts15 are two metallopeptidases that could cleave the proteoglycans aggrecan and versican, two major components of the extracellular matrix of the PNN.18, 19”
From Cortical fast-spiking parvalbumin interneurons enwrapped in the perineuronal net express the metallopeptidases Adamts8, Adamts15 and Neprilysin (2015) · cites this paper as [18]
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 Giamanco and Matthews, 2012
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Dubey, D., McRae, P. A., Rankin-Gee, E. K., Baranov, E., Wandrey, L., Rogers, S., & Porter, B. E. (2017) · Epilepsy Research · doi:10.1016/j.eplepsyres.2017.02.021 · Cited by 65 · see citing works
Yamada, J., & Jinno, S. (2017) · Journal of Comparative Neurology · doi:10.1002/cne.24132 · Cited by 59 · see citing works
Hyaluronan synthesis by developing cortical neurons in vitro
Fowke, T. M., Karunasinghe, R. N., Bai, J.-Z., Jordan, S., Gunn, A. J., & Dean, J. M. (2017) · Scientific Reports · doi:10.1038/srep44135 · Cited by 47 · see citing works
Juvenile stress induces behavioral change and affects perineuronal net formation in juvenile mice
Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., Aoki, S., & Ishihara, T. (2018) · BMC Neuroscience · doi:10.1186/s12868-018-0442-z · Cited by 39 · see citing works
- Authors
- Giamanco, K. A., & Matthews, R. T.
- Affiliations
- SUNY Upstate Medical University (US)
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 218
- Pages
- 367-384
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC3400135
- OpenAlex
- W2009062864
- Cited by
- 138
- References
- 61
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 10 · 2023: 8 · 2022: 4 · 2021: 7 · 2020: 14 · 2019: 10 · 2018: 12 · 2017: 13 · 2016: 8 · 2015: 12 · 2014: 6 · 2013: 12 · 2012: 1
- FWCI
- 3.33
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (R01NS069660)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- perineuronal nets, extracellular matrix, aggrecan, hyaluronic acid, glial cells, neuron-glia interactions, potassium chloride depolarization, neuroplasticity, brain maturation
- MeSH terms
- Animals, Cells, Cultured, Cerebral Cortex, Extracellular Matrix, Immunohistochemistry, Neuroglia, Neurons, Blotting, Western, Cell Culture Techniques, Reverse Transcriptase Polymerase Chain Reaction, Mice, Aggrecans, Real-Time Polymerase Chain Reaction
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