Perineuronal nets protect against amyloid β-protein neurotoxicity in cultured cortical neurons
Abstract
Perineuronal nets (PNs) consisting of chondroitin sulfate proteoglycans (CSPGs) and hyaluronic acid are associated with distinct neuronal populations in mammalian brain. Cortical areas abundant in PNs have been known to be less affected by neurotoxicity in human Alzheimer's disease. In the present study, we examined whether PNs protect the neurotoxicity caused by amyloid beta-protein (Abeta), a major constituent of senile plaques in Alzheimer's disease using cortical neurons of dissociated culture. Double labeling experiments using confocal microscopy showed that the neurons associated with PNs were visualized with the anti-CSPG antibody in dissociated cortical culture. The analysis of reverse transcription-polymerase chain reaction revealed that mRNA expression of chondroitin sulfotransferases, CSPG-specific enzymes, was detected in neuronal culture, indicating that cultured cortical neurons are able to synthesize CSPGs and construct PNs structure. The treatment of Abeta1-42 showed significant neurotoxicity on PNs-free cortical neurons, however, it did not reveal neurotoxicity on PNs-associated neurons. Moreover, it was shown that the treatment of Abeta1-42 was able to kill PNs-associated neurons after the removal of chondroitin sulfate (CS) glycosaminoglycans with chondroitinase ABC. The treatment of glutamate killed not only PNs-free cortical neurons but also PNs-associated neurons. These results suggest that CS glycosaminoglycans on PNs are responsible for protecting neurons from Abeta1-42 neurotoxicity.
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PNN prevents Aβ-induced neurotoxicity in cortical neurons.
“PNN prevents Aβ-induced neurotoxicity in cortical neurons (Miyata et al., 2007)”
From Disrupted structural connectivity in ArcAβ mouse model of Aβ amyloidosis (2020) · cites this paper as Miyata et al., 2007
Most previous studies support a beneficial role of PNN in Alzheimer's disease mouse models.
“In summary, most of the previous studies are in support of beneficial role of PNN in AD mouse model.”
From Disrupted structural connectivity in ArcAβ mouse model of Aβ amyloidosis (2020) · cites this paper as Miyata et al., 2007
Microglia-mediated loss of PNNs likely plays an important role in AD pathogenesis.
“As PNNs are implicated in neuronal health and function, protecting cells against neurotoxins such as Aβ1–42 [39] and oxidative stress [65] in addition to modulating neuronal activity [63, 66], the microglia-mediated loss of these structures in disease likely plays an important role in AD pathogenesis.”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [39]
Perineuronal nets protect neurons against tau and amyloid-beta pathology.
“PNNs are reported to protect neurons against tau [37, 38] and Aβ pathology [39]”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [39]
Both neurons and glial cells are involved in the assembly of PNN around neurons.
“It is unclear how these molecules are assembled to form PNN around neurons, but some studies suggest that both neurons and glial cells are involved in the process (Miyata et al., 2007; Pyka et al., 2011).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Miyata et al., 2007
It is unclear how these molecules are assembled to form PNN around neurons.
“It is unclear how these molecules are assembled to form PNN around neurons, but some studies suggest that both neurons and glial cells are involved in the process (Miyata et al., 2007; Pyka et al., 2011).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Miyata et al., 2007
More cells died when pretreated with chABC in rodent cortical neuron experiments.
“More cells died when pretreated with chABC (Miyata et al., 2007).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Miyata et al., 2007
PNN-ensheathed rodent cortical neurons were more resistant to cell death when incubated with exogenous monomeric Aβ1-42 peptide for 48 h.
“PNN-ensheathed cells were more resistant to cell death when neurons were incubated with exogenous monomeric Aβ1-42 peptide for 48 h.”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Miyata et al., 2007
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“For instance, neurons having intact PNN never deposits neurofibrillary tangles (Morawski et al., 2012); PNN prevents Aβ-induced neurotoxicity in cortical neurons (Miyata et al., 2007) and neurons with aggrecan-linked PNN protect tau pathology (Morawski et al., 2010a).”
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- Authors
- Miyata, S., Nishimura, Y., & Nakashima, T.
- Affiliations
- Kyoto Institute of Technology (JP)
- Corresponding author
- Miyata, Seiji
- ORCID
- Miyata, Seiji
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2007-05
- Volume
- 1150
- Pages
- 200-206
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2063629979
- Cited by
- 101
- References
- 39
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 9 · 2022: 11 · 2021: 8 · 2020: 9 · 2019: 6 · 2018: 9 · 2017: 4 · 2016: 3 · 2015: 6 · 2014: 2 · 2013: 2 · 2012: 2
- FWCI
- 2.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- perineuronal nets, amyloid-beta, neuroprotection, chondroitin sulfate proteoglycans, chondroitinase ABC, cortical neurons, Alzheimer's disease, neurotoxicity, glutamate excitotoxicity, hyaluronic acid
- MeSH terms
- Animals, Cells, Cultured, Cerebral Cortex, Dose-Response Relationship, Drug, Embryo, Mammalian, Hyaluronic Acid, Microtubule-Associated Proteins, Neurons, Peptide Fragments, Chondroitin Sulfate Proteoglycans, RNA, Messenger, Time Factors, Sulfotransferases, Amyloid beta-Peptides, Cell Death, Rats, Wistar, Glutamic Acid, Chondroitin ABC Lyase, Reverse Transcriptase Polymerase Chain Reaction, Rats
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