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NPTX2 and cognitive dysfunction in Alzheimer’s Disease
Open accessAbstract
Memory loss in Alzheimer’s disease (AD) is attributed to pervasive weakening and loss of synapses. Here, we present findings supporting a special role for excitatory synapses connecting pyramidal neurons of the hippocampus and cortex with fast-spiking parvalbumin (PV) interneurons that control network excitability and rhythmicity. Excitatory synapses on PV interneurons are dependent on the AMPA receptor subunit GluA4, which is regulated by presynaptic expression of the synaptogenic immediate early gene NPTX2 by pyramidal neurons. In a mouse model of AD amyloidosis, Nptx2-/- results in reduced GluA4 expression, disrupted rhythmicity, and increased pyramidal neuron excitability. Postmortem human AD cortex shows profound reductions of NPTX2 and coordinate reductions of GluA4. NPTX2 in human CSF is reduced in subjects with AD and shows robust correlations with cognitive performance and hippocampal volume. These findings implicate failure of adaptive control of pyramidal neuron-PV circuits as a pathophysiological mechanism contributing to cognitive failure in AD.
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In the citing paper
“Thus, they might be a good candidate biomarker for disease staging and cognitive prognosis (Galasko et al. 2019; Libiger et al. 2021; Nilsson et al. 2021; Swanson et al. 2016; Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTXs might be a selective marker for the imbalance of pyramidal neuron-interneuron microcircuits, thought to underlie cognitive impairment in AD (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“Deregulation of neuronal activity could explain changes in NPTXs and drive neurogenerative processes (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“The receiver operating characteristic (ROC) analysis concluded a similar test performance to distinguish AD from controls than that of the classical AD biomarkers (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“The subunit of AMPAR, GluA4, was also reduced in this study (both in the precuneus and medial frontal gyri) and correlated with NPTX2 in both control and AD group (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“CSF NPTXR levels, both the full length protein and the peptides resulting from TACE cleavage, were reduced in AD in comparison with controls (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“This was further sustained by studies that found NPTX2 correlating with medial temporal atrophy, hippocampal volume and cognitive impairment (Nilsson et al. 2021; Swanson et al. 2016; Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“Consequently, the reduction of NPTX2 could be linked to the disruption of pyramidal neuron-PV interneuron microcircuit, contributing to cognitive failure in AD (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTX2 was also decreased in post-mortem cortex from AD patients (hippocampus not analysed) (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTX2 exhibited a weak correlation with p-tau181 and total tau (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTX1 and NPTXR did not correlate with Aβ42, but did weakly correlate with total tau and p-tau181 (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTX1 and NPTXR did not correlate with Aβ42, but did weakly correlate with total tau and p-tau181 (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“Finally, CSF levels of the different NPTXs strongly correlated with each other in both AD and genetic FTLD, indicating an overall reduction of these proteins in CSF (Nilsson et al. 2021; van der Ende et al. 2020; Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“Some authors described a weak correlation with Aβ42, mainly in MCI (Galasko et al. 2019; Nilsson et al. 2021), whereas others found no correlation (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTXs may contribute to the cognitive decline in neurodegeneration and other diseases of the CNS by modifying the excitatory synaptic drive onto fast-spiking PV interneurons which leads to E/I imbalance.”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“This might promote or accelerate disease progression by increasing the demand in other compensatory mechanisms (Hu et al. 2010; Shepherd et al. 2006; Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“NPTXs also showed an added role when combined with core AD biomarkers in predicting the progression from MCI to AD dementia and in discriminating AD and healthy controls, e.g., NPTX2 in ratio with either total tau or p-tau (Galasko et al. 2019; Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“Unlike core biomarkers such as Aβ (Williams et al. 2011), CSF NPTXs levels correlated with cognitive scores in AD patients, even in the absence of brain pathology.”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
In the citing paper
“In the pre-symptomatic stage, NPTXs may act as a resilience factor keeping the integrity of the synapses, as previously hypothesised (Xiao et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Xiao et al. 2017
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Metadata
- Authors
- Xiao, M.-F., Xu, D., Craig, M. T., Pelkey, K. A., Chien, C.-C., Shi, Y., Zhang, J., Resnick, S., Pletnikova, O., Salmon, D., Brewer, J., Edland, S., Wegiel, J., Tycko, B., Savonenko, A., Reeves, R. H., Troncoso, J. C., McBain, C. J., Galasko, D., & Worley, P. F.
- Affiliations
- Johns Hopkins University (US)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (US)
- National Institute on Aging (US)
- Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, United States
- University of California San Diego (US)
- Institute for Basic Research, New York City, United States
- Columbia University (US)
- Corresponding author
- Worley, Paul F
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2017-03-23
- Volume
- 6
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5404919
- OpenAlex
- W2606988847
- Cited by
- 316
- References
- 91
- Citations by year
- 2026: 26 · 2025: 35 · 2024: 43 · 2023: 28 · 2022: 27 · 2021: 49 · 2020: 49 · 2019: 37 · 2018: 18 · 2017: 4
- FWCI
- 14.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Open Research Exeter (University of Exeter) (submittedVersion, cc-by)
- Funders
- LuMind Research Down Syndrome Foundation
- National Institute on Aging (AG05131)
- National Institute of Mental Health (P50 AG005146-27, MH100024, R35 NS-097966)
- Alzheimer’s drug discovery foundation (20021106)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- 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
- NPTX2, Alzheimer's disease, cognitive impairment, GluA4, AMPA receptors, parvalbumin interneurons, fast-spiking interneurons, pyramidal neurons, hippocampus, cortical excitability, neural oscillations, amyloidosis, memory loss, cerebrospinal fluid biomarkers, hippocampal volume, synaptogenesis
- MeSH terms
- Pentraxins, Alzheimer Disease, Animals, C-Reactive Protein, Cerebral Cortex, Disease Models, Animal, Hippocampus, Humans, Nerve Tissue Proteins, Mice, Knockout, Mice, Cognitive Dysfunction
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