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Presubiculum principal cells are preserved from degeneration in knock-in APP/TAU mouse models of Alzheimer’s disease

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Islam, Anam, Saito, Takashi, Saido, Takaomi, Ali, Afia B.·2023·Seminars in Cell & Developmental Biology
DOI 10.1016/j.semcdb.2022.03.001PMC PMC10439011
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Abstract

The presubiculum (PRS) is an integral component of the perforant pathway that has recently been recognised as a relatively unscathed region in clinical Alzheimer’s disease (AD), despite neighbouring components of the perforant pathway, CA1 and the entorhinal cortex, responsible for formation of episodic memory and storage, showing severe hallmarks of AD including, amyloid-beta (Aβ) plaques, tau tangles and marked gliosis. However, the question remains whether this anatomical resilience translates into functional resilience of the PRS neurons. Using neuroanatomy combined with whole-cell electrophysiological recordings, we investigated whether the unique spatial profile of the PRS was replicable in two knock-in mouse models of AD, APPNL-F/NL-F, and APPNL-F/MAPTHTAU and whether the intrinsic properties and morphological integrity of the PRS principal neurons was maintained compared to the lateral entorhinal cortex (LEC) and hippocampal CA1 principal cells. Our data revealed an age-dependent Aβ and tau pathology with neuroinflammation in the LEC and CA1, but a presence of fleece-like Aβ deposits with an absence of tau tangles and cellular markers of gliosis in the PRS of the mouse models at 11–16 and 18–22 months. These observations were consistent in human post-mortem AD tissue. This spatial profile also correlated with functional resilience of strong burst firing PRS pyramidal cells that showed unaltered sub- and suprathreshold intrinsic biophysical membrane properties and gross morphology in the AD models that were similar to the properties of pyramidal cells recorded in age-matched wild-type mice (11–14 months). This was in contrast to the LEC and CA1 principal cells which showed altered subthreshold intrinsic properties such as a higher input resistance, longer membrane time constants and hyperexcitability in response to suprathreshold stimulation that correlated with atrophied dendrites in both AD models. In conclusion, our data show for the first time that the unique anatomical profile of the PRS constitutes a diffuse AD pathology that is correlated with the preservation of principal pyramidal cell intrinsic biophysical and morphological properties despite alteration of LEC and CA1 pyramidal cells in two distinct genetic models of AD. Understanding the underlying mechanisms of this resilience could be beneficial in preventing the spread of disease pathology before cognitive deficits are precipitated in AD.

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  • Human MAPT KI models exhibit delayed tau pathology, as does a cross between the two KI models.

    “Human MAPT KI models exhibit delayed tau pathology, as does a cross between the two KI models (Saito et al., 2019; Islam et al., 2023).”

    From β-amyloid accumulation enhances microtubule associated protein tau pathology in an APPNL-G-F/MAPTP301S mouse model of Alzheimer’s disease (2024) · cites this paper as Islam et al., 2023

    The Discussion section on spatially distinct pathology reports that mature tau tangles in the APP/MAPT double-knock-in mice were frequent at 18–22 months but virtually absent at 11–16 months, supporting later development of that form of pathology. It also reports elevated hyperphosphorylated tau in the younger mice. The paper does not establish delayed tau pathology in a human MAPT knock-in model studied on its own. (LLM, conf=0.85)

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Authors
Islam, A., Saito, T., Saido, T., & Ali, A. B.
Affiliations
  • UCL School of Pharmacy (GB)
  • Nagoya City University (JP)
  • RIKEN Center for Brain Science (JP)
Corresponding author
Ali, Afia B.
ORCID
Venue
Seminars in Cell & Developmental Biology
Publisher
Elsevier BV
Published
2023-04
Volume
139
Pages
55-72
ISSN
1084-9521 (ISSN-L)
DOI
10.1016/j.semcdb.2022.03.001
PMC
PMC10439011
OpenAlex
W4220678237
Cited by
17
References
16
Citations by year
2026: 1 · 2025: 1 · 2024: 7 · 2023: 5 · 2022: 3
FWCI
2.48
Type
journal article
Language
en
Open access
Licence
Locations
  • Seminars in Cell and Developmental Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • Medical Research Council (GO501263)
  • Alzheimer’s Research UK (ARUK- NC2020-UCL)
  • School of Pharmacy, University College London
  • UCL Institute of Neurology, University College London
  • Wellcome Trust
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
presubiculum, Alzheimer's disease, perforant path, APP knock-in mice, lateral entorhinal cortex, hippocampal CA1, pyramidal neurons, neuronal resilience, amyloid-beta, tau pathology, neuroinflammation, gliosis, intrinsic membrane properties, burst firing, dendritic atrophy
MeSH terms
Alzheimer Disease, Animals, Disease Models, Animal, Gliosis, Humans, Infant, Mice, Transgenic, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, Parahippocampal Gyrus, Mice, Plaque, Amyloid

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