Neurochemical mapping of the human hippocampus reveals perisynaptic matrix around functional synapses in Alzheimer’s disease.
Open accessAbstract
Perineuronal matrix is an extracellular protein scaffold to shape neuronal responsiveness and survival. Whilst perineuronal nets engulf the somatodendritic axis of neurons, axonal coats are focal extracellular protein aggregates surrounding individual synapses. Here, we addressed the chemical identity and subcellular localization of both perineuronal and perisynaptic matrices in the human hippocampus, whose neuronal circuitry is progressively compromised in Alzheimer's disease. We hypothesized that (1) the cellular expression sites of chondroitin sulphate proteoglycan-containing extracellular matrix associate with specific neuronal identities, reflecting network dynamics, and (2) the regional distribution and molecular composition of axonal coats must withstand Alzheimer's disease-related modifications to protect functional synapses. We show by epitope-specific antibodies that the perineuronal protomap of the human hippocampus is distinct from other mammals since pyramidal cells but not calretinin(+) and calbindin(+) interneurons, neurochemically classified as novel neuronal subtypes, lack perineuronal nets. We find that cartilage link protein-1 and brevican-containing matrices form isolated perisynaptic coats, engulfing both inhibitory and excitatory terminals in the dentate gyrus and entorhinal cortex. Ultrastructural analysis revealed that presynaptic neurons contribute components of perisynaptic coats via axonal transport. We demonstrate, by combining biochemical profiling and neuroanatomy in Alzheimer's patients and transgenic (APdE9) mice, the preserved turnover and distribution of axonal coats around functional synapses along dendrite segments containing hyperphosphorylated tau and in amyloid-β-laden hippocampal microdomains. We conclude that the presynapse-driven formation of axonal coats is a candidate mechanism to maintain synapse integrity under neurodegenerative conditions.
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Post-mortem brains of AD patients exhibit reduced expression of PNNs, particularly in the hippocampus.
“Post-mortem brains of AD patients exhibit reduced expression of PNNs, particularly in the hippocampus (Baig et al., 2005; Lendvai et al., 2013).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Lendvai et al., 2013
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- Authors
- Lendvai, D., Morawski, M., Négyessy, L., Gáti, G., Jäger, C., Baksa, G., Glasz, T., Attems, J., Tanila, H., Arendt, T., Harkany, T., & Alpár, A.
- Affiliations
- Semmelweis University (HU)
- SUNY Upstate Medical University (US)
- Institute for Particle and Nuclear Physics (HU)
- Leipzig University (DE)
- Newcastle University (GB)
- University of Eastern Finland (FI)
- University of Aberdeen (GB)
- Corresponding author
- Arendt, Thomas
- Alpár, Alán
- ORCID
- Venue
- Acta Neuropathologica
- Published
- 2012-09-09
- Volume
- 125
- Issue
- 2
- Pages
- 215-229
- ISSN
- 0001-6322 (ISSN-L)
- 1432-0533
- PMC
- PMC6485544
- OpenAlex
- W2020761647
- Cited by
- 93
- References
- 74
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 8 · 2023: 7 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 5 · 2018: 11 · 2017: 5 · 2016: 4 · 2015: 5 · 2014: 16 · 2013: 4
- FWCI
- 5.36
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Acta Neuropathologica (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Semmelweis University Repository (Semmelweis University) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- Medical Research Council (MR/L016451/1)
- NIHR Newcastle Biomedical Research Centre (BH111030)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Keywords
- perineuronal nets, extracellular matrix, Alzheimer's disease, human hippocampus, chondroitin sulfate proteoglycans, brevican, presynaptic neurons, axonal transport, hyperphosphorylated tau, amyloid-beta, dentate gyrus, entorhinal cortex, interneurons, pyramidal neurons
- MeSH terms
- Proteoglycan Link Protein, Alzheimer Disease, Animals, Axons, Brain Mapping, Calcium-Binding Proteins, Dendrites, Extracellular Matrix, Female, Hippocampus, Humans, Immunohistochemistry, Male, Mice, Transgenic, Microscopy, Electron, Microscopy, Fluorescence, Proteoglycans, Synapses, Blotting, Western, Cohort Studies, Amyloid beta-Peptides, Extracellular Matrix Proteins, tau Proteins, Microscopy, Confocal, Vesicular Neurotransmitter Transport Proteins, Mice, Aggrecans, 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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