NPTX2 and cognitive dysfunction in Alzheimer’s Disease

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 netwo...

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Bibliographic Details
Published ineLife Vol. 6
Main Authors Xiao, Mei-Fang, Xu, Desheng, Craig, Michael T, Pelkey, Kenneth A, Chien, Chun-Che, Shi, Yang, Zhang, Juhong, Resnick, Susan, Pletnikova, Olga, Salmon, David, Brewer, James, Edland, Steven, Wegiel, Jerzy, Tycko, Benjamin, Savonenko, Alena, Reeves, Roger H, Troncoso, Juan C, McBain, Chris J, Galasko, Douglas, Worley, Paul F
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 23.03.2017
eLife Sciences Publications, Ltd
Subjects
Alzheimer Disease - pathology
Alzheimer Disease - physiopathology
Alzheimer's disease
Amyloidosis
Animals
Brain research
C-Reactive Protein - analysis
C-Reactive Protein - cerebrospinal fluid
Cerebral Cortex - pathology
Cerebrospinal fluid
Cognitive ability
Cognitive Dysfunction - physiopathology
Dementia
Disease Models, Animal
Excitability
Firing pattern
Hippocampus
Hippocampus - pathology
Human subjects
Humans
immediate early gene
inhibitory neuron
Interneurons
Medicine
Memory
Mice
Mice, Knockout
Nerve Tissue Proteins - analysis
Nerve Tissue Proteins - cerebrospinal fluid
Neurodegeneration
Neurodegenerative diseases
Neuroscience
Neurosciences
Parvalbumin
Pyramidal cells
Rodents
Synapses
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
United States > US
California
alzheimer’s disease
mmediate early gene
neuroscience
inhibitory neuron
dementia
immediate early gene
Alzheimer's disease
Online AccessGet full text
ISSN2050-084X
2050-084X
DOI10.7554/eLife.23798

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Abstract 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.
AbstractList 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.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.
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.
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.DOI: http://dx.doi.org/10.7554/eLife.23798.001
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. DOI: http://dx.doi.org/10.7554/eLife.23798.001
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, 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.
Author Craig, Michael T
Salmon, David
Galasko, Douglas
Savonenko, Alena
McBain, Chris J
Wegiel, Jerzy
Xu, Desheng
Pletnikova, Olga
Worley, Paul F
Edland, Steven
Pelkey, Kenneth A
Shi, Yang
Brewer, James
Zhang, Juhong
Tycko, Benjamin
Reeves, Roger H
Xiao, Mei-Fang
Troncoso, Juan C
Chien, Chun-Che
Resnick, Susan
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  givenname: Mei-Fang
  surname: Xiao
  fullname: Xiao, Mei-Fang
  organization: Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States, Department of Physiology, Johns Hopkins University School of Medicine, Baltimore, United States, Institute for Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 2
  givenname: Desheng
  surname: Xu
  fullname: Xu, Desheng
  organization: Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 3
  givenname: Michael T
  orcidid: 0000-0001-8481-6709
  surname: Craig
  fullname: Craig, Michael T
  organization: Program in Developmental Neurobiology, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, Bethesda, United States
– sequence: 4
  givenname: Kenneth A
  surname: Pelkey
  fullname: Pelkey, Kenneth A
  organization: Program in Developmental Neurobiology, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, Bethesda, United States
– sequence: 5
  givenname: Chun-Che
  surname: Chien
  fullname: Chien, Chun-Che
  organization: Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 6
  givenname: Yang
  surname: Shi
  fullname: Shi, Yang
  organization: Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 7
  givenname: Juhong
  surname: Zhang
  fullname: Zhang, Juhong
  organization: Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 8
  givenname: Susan
  surname: Resnick
  fullname: Resnick, Susan
  organization: Laboratory of Behavioral Neuroscience, National Institute on Aging, Intramural Research Program, Baltimore, United States
– sequence: 9
  givenname: Olga
  surname: Pletnikova
  fullname: Pletnikova, Olga
  organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 10
  givenname: David
  surname: Salmon
  fullname: Salmon, David
  organization: Department of Neurosciences, University of California San Diego Medical Center, San Diego, United States, Shiley-Marcos Alzheimer's Disease Research Center, University of California San Diego Medical Center, San Diego, United States
– sequence: 11
  givenname: James
  surname: Brewer
  fullname: Brewer, James
  organization: Department of Neurosciences, University of California San Diego Medical Center, San Diego, United States, Shiley-Marcos Alzheimer's Disease Research Center, University of California San Diego Medical Center, San Diego, United States
– sequence: 12
  givenname: Steven
  orcidid: 0000-0002-1153-7335
  surname: Edland
  fullname: Edland, Steven
  organization: Shiley-Marcos Alzheimer's Disease Research Center, University of California San Diego Medical Center, San Diego, United States, Division of Biostatistics and Bioinformatics, University of California San Diego, San Diego, United States
– sequence: 13
  givenname: Jerzy
  surname: Wegiel
  fullname: Wegiel, Jerzy
  organization: Institute for Basic Research, New York City, United States
– sequence: 14
  givenname: Benjamin
  surname: Tycko
  fullname: Tycko, Benjamin
  organization: Taub Institute for Research on Alzheimer’s disease and the Aging Brain, Columbia University, New York City, United States
– sequence: 15
  givenname: Alena
  surname: Savonenko
  fullname: Savonenko, Alena
  organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 16
  givenname: Roger H
  surname: Reeves
  fullname: Reeves, Roger H
  organization: Department of Physiology, Johns Hopkins University School of Medicine, Baltimore, United States, Institute for Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 17
  givenname: Juan C
  surname: Troncoso
  fullname: Troncoso, Juan C
  organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, United States, Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, United States
– sequence: 18
  givenname: Chris J
  surname: McBain
  fullname: McBain, Chris J
  organization: Program in Developmental Neurobiology, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, Bethesda, United States
– sequence: 19
  givenname: Douglas
  surname: Galasko
  fullname: Galasko, Douglas
  organization: Department of Neurosciences, University of California San Diego Medical Center, San Diego, United States, Shiley-Marcos Alzheimer's Disease Research Center, University of California San Diego Medical Center, San Diego, United States
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  givenname: Paul F
  orcidid: 0000-0002-5086-614X
  surname: Worley
  fullname: Worley, Paul F
  organization: Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States, Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, United States
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28440221$$D View this record in MEDLINE/PubMed
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Keywords alzheimer’s disease
mmediate early gene
neuroscience
inhibitory neuron
dementia
immediate early gene
Alzheimer's disease
Language English
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– reference: 28440224 - Elife. 2017 Apr 25;6:
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Snippet 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...
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...
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SubjectTerms Alzheimer Disease - pathology
Alzheimer Disease - physiopathology
Alzheimer's disease
Amyloidosis
Animals
Brain research
C-Reactive Protein - analysis
C-Reactive Protein - cerebrospinal fluid
Cerebral Cortex - pathology
Cerebrospinal fluid
Cognitive ability
Cognitive Dysfunction - physiopathology
Dementia
Disease Models, Animal
Excitability
Firing pattern
Hippocampus
Hippocampus - pathology
Human subjects
Humans
immediate early gene
inhibitory neuron
Interneurons
Medicine
Memory
Mice
Mice, Knockout
Nerve Tissue Proteins - analysis
Nerve Tissue Proteins - cerebrospinal fluid
Neurodegeneration
Neurodegenerative diseases
Neuroscience
Neurosciences
Parvalbumin
Pyramidal cells
Rodents
Synapses
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
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Title NPTX2 and cognitive dysfunction in Alzheimer’s Disease
URI https://www.ncbi.nlm.nih.gov/pubmed/28440221
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Volume 6
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