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Early and protective microglial activation in Alzheimer’s disease: a prospective study using18F-DPA-714 PET imaging
Open accessAbstract
While emerging evidence suggests that neuroinflammation plays a crucial role in Alzheimer's disease, the impact of the microglia response in Alzheimer's disease remains a matter of debate. We aimed to study microglial activation in early Alzheimer's disease and its impact on clinical progression using a second-generation 18-kDa translocator protein positron emission tomography radiotracer together with amyloid imaging using Pittsburgh compound B positron emission tomography. We enrolled 96 subjects, 64 patients with Alzheimer's disease and 32 controls, from the IMABio3 study, who had both (11)C-Pittsburgh compound B and (18)F-DPA-714 positron emission tomography imaging. Patients with Alzheimer's disease were classified as prodromal Alzheimer's disease (n = 38) and Alzheimer's disease dementia (n = 26). Translocator protein-binding was measured using a simple ratio method with cerebellar grey matter as reference tissue, taking into account regional atrophy. Images were analysed at the regional (volume of interest) and at the voxel level. Translocator protein genotyping allowed the classification of all subjects in high, mixed and low affinity binders. Thirty high+mixed affinity binders patients with Alzheimer's disease were dichotomized into slow decliners (n = 10) or fast decliners (n = 20) after 2 years of follow-up. All patients with Alzheimer's disease had an amyloid positive Pittsburgh compound B positron emission tomography. Among controls, eight had positive amyloid scans (n = 6 high+mixed affinity binders), defined as amyloidosis controls, and were analysed separately. By both volumes of interest and voxel-wise comparison, 18-kDa translocator protein-binding was higher in high affinity binders, mixed affinity binders and high+mixed affinity binders Alzheimer's disease groups compared to controls, especially at the prodromal stage, involving the temporo-parietal cortex. Translocator protein-binding was positively correlated with Mini-Mental State Examination scores and grey matter volume, as well as with Pittsburgh compound B binding. Amyloidosis controls displayed higher translocator protein-binding than controls, especially in the frontal cortex. We found higher translocator protein-binding in slow decliners than fast decliners, with no difference in Pittsburgh compound B binding. Microglial activation appears at the prodromal and possibly at the preclinical stage of Alzheimer's disease, and seems to play a protective role in the clinical progression of the disease at these early stages. The extent of microglial activation appears to differ between patients, and could explain the overlap in translocator protein binding values between patients with Alzheimer's disease and amyloidosis controls.
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“Aβ itself acts as a proinflammatory agent, activating many inflammatory components.”
From Clinical trials of new drugs for Alzheimer disease (2020) · cites this paper as [26]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“In the early stages of AD, initial microglial activation may serve a protective role (anti-neuroinflammatory), whereby it tries to clear the amyloid and release nerve growth factors. However, when Aβ or other toxic products over-accumulate, proinflammatory phenotypes are activated, which damage the neurons [26].”
From Clinical trials of new drugs for Alzheimer disease (2020) · cites this paper as [26]
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“Furthermore, the brains of patients with AD exhibited evidence of sustained inflammation.”
From Clinical trials of new drugs for Alzheimer disease (2020) · cites this paper as [26]
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“[18F]DPA-714 was extensively studied in preclinical and clinical models [58–61], as a biomarker of neuroinflammation in various human CNS disorders [58].”
From Neuron secrete exosomes containing miR-9-5p to promote polarization of M1 microglia in depression (2022) · cites this paper as [58]
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“Furthermore, early neuroinflammation has been shown to be an adaptive mechanism by microglia that protects against AD pathology by reducing the levels of Aβ and tau.118–120”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [120]
In the citing paper
“In vivo imaging shows that microglia activation precedes the onset of AD (100) and is paralleled by increased levels of inflammatory markers in the cerebrospinal fluid (101)”
From Microglia in Alzheimer's disease (2017) · cites this paper as [100]
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“in MCI, microglial activation was positively correlated with cognition and gray matter volume, suggesting that microglial activation plays a protective role in the early phase of clinically apparent disease (100).”
From Microglia in Alzheimer's disease (2017) · cites this paper as [100]
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“Of relevance, PET studies have indicated increased microglia activation in the precuneus and parietal cortex in AD.47,48”
From CSF biomarkers of neuroinflammation and cerebrovascular dysfunction in early Alzheimer disease (2018) · cites this paper as [48]
In the citing paper
“Another study that divided AD subjects into fast decliners and slow decliners measured a higher TSPO signal in the brains of slow decliners, consistent with a protective role for microglial activation even in stages of AD when dementia is evident (Hamelin et al., 2016).”
From Microglia in Alzheimer’s disease (2018) · cites this paper as Hamelin et al., 2016
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“This is consistent with the finding that early microglial activation in response to amyloid plaques, as assessed by in vivo microglial imaging studies, is correlated with increased grey matter volume and reduced rate of cognitive decline46,47.”
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“Methods to image microglia exist and are being used to test the effect of treatments on microglia205–210.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [209]
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Metadata
- Authors
- Hamelin, L., Lagarde, J., Dorothée, G., Leroy, C., Labit, M., Comley, R. A., de Souza, L. C., Corne, H., Dauphinot, L., Bertoux, M., Dubois, B., Gervais, P., Colliot, O., Potier, M. C., Bottlaender, M., Sarazin, M., & the Clinical IMABio3 team
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Centre d'Acquisition et de Traitement des Images (FR)
- F. Hoffmann-La Roche AG (CH)
- Assistance Publique – Hôpitaux de Paris (FR)
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-03-15
- Volume
- 139
- Issue
- 4
- Pages
- 1252-1264
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2298656843
- Cited by
- 519
- References
- 41
- Citations by year
- 2026: 38 · 2025: 48 · 2024: 71 · 2023: 59 · 2022: 47 · 2021: 47 · 2020: 51 · 2019: 51 · 2018: 57 · 2017: 39 · 2016: 10
- FWCI
- 28.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- Funders
- European Commission (2007–2013, FP7 2007-2013, FP7/2007, 278850)
- Université Paris Descartes
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- Alzheimer's disease, microglial activation, translocator protein (TSPO), [18F]DPA-714, neuroinflammation, prodromal Alzheimer's disease, amyloid imaging, Pittsburgh compound B, clinical progression, amyloidosis, gray matter volume, temporoparietal cortex, frontal cortex, cognitive decline
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Brain, Female, Fluorine Radioisotopes, Follow-Up Studies, Humans, Longitudinal Studies, Male, Middle Aged, Prospective Studies, Pyrazoles, Pyrimidines, Cohort Studies, Microglia, Positron-Emission Tomography
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