Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer’s disease

Takahashi, Hisaaki; Brasnjevic, Ivona; Rutten, Bart P. F.; Van Der Kolk, Nicolien; Perl, Daniel P.; Bouras, Constantin; Steinbusch, Harry W. M.; Schmitz, Christoph; Hof, Patrick R.; Dickstein, Dara L.

doi:10.1007/s00429-010-0242-4

Cited by 124Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroscience and Neuropharmacology Research

Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer’s disease

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Takahashi, Hisaaki, Brasnjevic, Ivona, Rutten, Bart P. F., Van Der Kolk, Nicolien, Perl, Daniel P., Bouras, Constantin, Steinbusch, Harry W. M., Schmitz, Christoph +2 more·2010·Brain Structure and Function

DOI 10.1007/s00429-010-0242-4PMC PMC3038332

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Abstract

Hippocampal atrophy and neuron loss are commonly found in Alzheimer's disease (AD). However, the underlying molecular mechanisms and the fate in the AD hippocampus of subpopulations of interneurons that express the calcium-binding proteins parvalbumin (PV) and calretinin (CR) has not yet been properly assessed. Using quantitative stereologic methods, we analyzed the regional pattern of age-related loss of PV- and CR-immunoreactive (ir) neurons in the hippocampus of mice that carry M233T/L235P knocked-in mutations in presenilin-1 (PS1) and overexpress a mutated human beta-amyloid precursor protein (APP), namely, the APP(SL)/PS1 KI mice, as well as in APP(SL) mice and PS1 KI mice. We found a loss of PV-ir neurons (40-50%) in the CA1-2, and a loss of CR-ir neurons (37-52%) in the dentate gyrus and hilus of APP(SL)/PS1 KI mice. Interestingly, comparable PV- and CR-ir neuron losses were observed in the dentate gyrus of postmortem brain specimens obtained from patients with AD. The loss of these interneurons in AD may have substantial functional repercussions on local inhibitory processes in the hippocampus.

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In APP/PS1KI mice, significantly reduced CR- and PV-positive neuron numbers were found in the hippocampus, while no changes were detected in layers V and VI of the frontal cortex despite significantly reduced pyramidal neurons and massive thioflavin S-positive extracellular amyloid deposits.
“A related finding was reported in APP/PS1KI mice, which presented with significantly reduced CR- and PV-positive neuron numbers in the hippocampus [125]. Interestingly, no changes were detected in layers V and VI of the frontal cortex in this model, although pyramidal neurons were significantly reduced and massive thioflavin S-positive extracellular amyloid deposits were present [129].”
From Neuron Loss in Alzheimer’s Disease: Translation in Transgenic Mouse Models (2020) · cites this paper as [125]
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Most available studies report a loss of CR- and PV-positive interneurons in the hippocampal formation in AD transgenic mice.
“Quantitative studies investigating interneuron populations in transgenic AD mouse models yielded more conclusive results, with most of the available studies reporting a loss of CR- and PV-positive interneurons in the hippocampal formation in AD transgenic mice [59,122,123,124,125,126].”
From Neuron Loss in Alzheimer’s Disease: Translation in Transgenic Mouse Models (2020) · cites this paper as [125]
In Alzheimer's disease patients, PV-INs are decreased in the dentate gyrus.
“In AD patients, however, a decrease in PV-INs was reported in the dentate gyrus, and an increase in PV-INs was reported in the piriform cortex [34,37,38].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [34]
In Alzheimer's disease patients, PV-INs are increased in the piriform cortex.
“In AD patients, however, a decrease in PV-INs was reported in the dentate gyrus, and an increase in PV-INs was reported in the piriform cortex [34,37,38].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [34]
Hippocampal PV-IN numbers are decreased in two mouse models of Alzheimer's disease.
“For example, decreases in the number of PV-INs in the hippocampus were observed in two mouse models of AD [33,34], while an increase in hippocampal PV immunoreactivity was observed in another [35], and no change in the number of hippocampal PV-positive interneurons was observed in yet another model [36].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [34]

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“A related finding was reported in APP/PS1KI mice, which presented with significantly reduced CR- and PV-positive neuron numbers in the hippocampus [125].”
Background
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Self-citation
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Authors: Takahashi, H., Brasnjevic, I., Rutten, B. P. F., Van Der Kolk, N., Perl, D. P., Bouras, C., Steinbusch, H. W. M., Schmitz, C., Hof, P. R., & Dickstein, D. L.
Affiliations: Maastricht University (NL)
Icahn School of Medicine at Mount Sinai (US)
University of Geneva (CH)
Corresponding author: Dickstein, Dara L.
ORCID: Rutten, Bart P. F.
Perl, Daniel P.
Steinbusch, Harry W. M.
Schmitz, Christoph
Hof, Patrick R.
Dickstein, Dara L.
Venue: Brain Structure and Function
Publisher: Springer Science and Business Media LLC
Published: 2010-03
Volume: 214
Issue: 2-3
Pages: 145-160
ISSN: 1863-2653 (ISSN-L)
1863-2661
DOI: 10.1007/s00429-010-0242-4
PMC: PMC3038332
OpenAlex: W2132816327
Cited by: 124
References: 80
Citations by year: 2026: 7 · 2025: 9 · 2024: 7 · 2023: 5 · 2022: 7 · 2021: 6 · 2020: 11 · 2019: 9 · 2018: 9 · 2017: 6 · 2016: 5 · 2015: 6 · 2014: 9 · 2013: 6 · 2012: 12
FWCI: 6.07
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Brain Structure and Function (publishedVersion)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion)
PubMed Central (acceptedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Archive ouverte UNIGE (University of Geneva) (submittedVersion)
Research Publications (Maastricht University) (submittedVersion)
Funders: National Institute on Aging (AG-02219, AG 05138, P50AG005138, P01AG002219)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: Alzheimer's disease, hippocampal interneurons, parvalbumin, calretinin, presenilin 1, neuronal loss, dentate gyrus, inhibitory interneurons, calcium-binding proteins, postmortem brain
MeSH terms: Aged, Aged, 80 and over, Alzheimer Disease, Animals, Cell Count, Female, Hippocampus, Humans, Interneurons, Male, Nerve Degeneration, Neural Inhibition, Parvalbumins, Biomarkers, Amyloid beta-Protein Precursor, Dentate Gyrus, Mice, Presenilin-1, Gene Knock-In Techniques, S100 Calcium Binding Protein G, Calbindin 2

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Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer’s disease

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