Synaptic proteins associated with cognitive performance and neuropathology in older humans revealed by multiplexed fractionated proteomics

•Proteomics linked 123 proteins to AD pathology and cognitive performance•Proteins involved in glucose metabolism are altered in cognitive impairment•Frail individuals show pathway dysregulation in absence of AD pathology Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β...

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Veröffentlicht in:Neurobiology of aging Jg. 105; H. C; S. 99 - 114
Hauptverfasser: Carlyle, Becky C., Kandigian, Savannah E., Kreuzer, Johannes, Das, Sudeshna, Trombetta, Bianca A., Kuo, Yikai, Bennett, David A., Schneider, Julie A., Petyuk, Vladislav A., Kitchen, Robert R., Morris, Robert, Nairn, Angus C., Hyman, Bradley T., Haas, Wilhelm, Arnold, Steven E.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: United States Elsevier Inc 01.09.2021
Elsevier
Schlagworte:
60 APPLIED LIFE SCIENCES
Aged
Aged, 80 and over
Aging
Aging - pathology
Aging - psychology
Alzheimer Disease - diagnosis
Alzheimer Disease - genetics
Alzheimer Disease - pathology
Alzheimer Disease - psychology
Alzheimer's disease
Angular gyrus
Chromatography, Liquid
Cognition
Cognition - physiology
Cognitive resilience
Female
Geriatrics & Gerontology
Glycolysis
Humans
Independent Living
Male
Mass Spectrometry
Neuroproteomics
Neurosciences & Neurology
Parietal Lobe - metabolism
Phosphorylation
Proteasome Endopeptidase Complex - metabolism
Proteomics - methods
Serotonin - metabolism
Synapses - metabolism
Synapses - pathology
FDG-PET
LC-MS3
Neuroproteomics
AD
Angular gyrus
SPS-MS3
GSEA
SPE
Cognition
ROSMAP
MS1, MS2, MS3
Aβ
MMSE
Cognitive resilience
Aging
TMT11
m/z
BA39
bRPLC
Alzheimer's disease
AGC
HPLC
ISSN:0197-4580, 1558-1497, 1558-1497
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Abstract •Proteomics linked 123 proteins to AD pathology and cognitive performance•Proteins involved in glucose metabolism are altered in cognitive impairment•Frail individuals show pathway dysregulation in absence of AD pathology Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis, it is not sufficient for causing cognitive impairment. Up to one third of community dwelling older adults harbor intermediate to high levels of AD neuropathology at death yet demonstrate no significant cognitive impairment. Conversely, there are individuals who exhibit dementia with no gross explanatory neuropathology. In prior studies, synapse loss correlated with cognitive impairment. To understand how synaptic composition changes in relation to neuropathology and cognition, multiplexed liquid chromatography mass-spectrometry was used to quantify enriched synaptic proteins from the parietal association cortex of 100 subjects with contrasting levels of AD pathology and cognitive performance. 123 unique proteins were significantly associated with diagnostic category. Functional analysis showed enrichment of serotonin release and oxidative phosphorylation categories in normal (cognitively unimpaired, low neuropathology) and "resilient" (unimpaired despite AD pathology) individuals. In contrast, frail individuals, (low pathology, impaired cognition) showed a metabolic shift towards glycolysis and increased presence of proteasome subunits.
AbstractList •Proteomics linked 123 proteins to AD pathology and cognitive performance•Proteins involved in glucose metabolism are altered in cognitive impairment•Frail individuals show pathway dysregulation in absence of AD pathology Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis, it is not sufficient for causing cognitive impairment. Up to one third of community dwelling older adults harbor intermediate to high levels of AD neuropathology at death yet demonstrate no significant cognitive impairment. Conversely, there are individuals who exhibit dementia with no gross explanatory neuropathology. In prior studies, synapse loss correlated with cognitive impairment. To understand how synaptic composition changes in relation to neuropathology and cognition, multiplexed liquid chromatography mass-spectrometry was used to quantify enriched synaptic proteins from the parietal association cortex of 100 subjects with contrasting levels of AD pathology and cognitive performance. 123 unique proteins were significantly associated with diagnostic category. Functional analysis showed enrichment of serotonin release and oxidative phosphorylation categories in normal (cognitively unimpaired, low neuropathology) and "resilient" (unimpaired despite AD pathology) individuals. In contrast, frail individuals, (low pathology, impaired cognition) showed a metabolic shift towards glycolysis and increased presence of proteasome subunits.
Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis, it is not sufficient for causing cognitive impairment. Up to one third of community dwelling older adults harbor intermediate to high levels of AD neuropathology at death yet demonstrate no significant cognitive impairment. Conversely, there are individuals who exhibit dementia with no gross explanatory neuropathology. In prior studies, synapse loss correlated with cognitive impairment. To understand how synaptic composition changes in relation to neuropathology and cognition, multiplexed liquid chromatography mass-spectrometry was used to quantify enriched synaptic proteins from the parietal association cortex of 100 subjects with contrasting levels of AD pathology and cognitive performance. 123 unique proteins were significantly associated with diagnostic category. Functional analysis showed enrichment of serotonin release and oxidative phosphorylation categories in normal (cognitively unimpaired, low neuropathology) and "resilient" (unimpaired despite AD pathology) individuals. In contrast, frail individuals, (low pathology, impaired cognition) showed a metabolic shift towards glycolysis and increased presence of proteasome subunits.
Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis, it is not sufficient for causing cognitive impairment. Up to one third of community dwelling older adults harbor intermediate to high levels of AD neuropathology at death yet demonstrate no significant cognitive impairment. Conversely, there are individuals who exhibit dementia with no gross explanatory neuropathology. In prior studies, synapse loss correlated with cognitive impairment. To understand how synaptic composition changes in relation to neuropathology and cognition, multiplexed liquid chromatography mass-spectrometry was used to quantify enriched synaptic proteins from the parietal association cortex of 100 subjects with contrasting levels of AD pathology and cognitive performance. 123 unique proteins were significantly associated with diagnostic category. Functional analysis showed enrichment of serotonin release and oxidative phosphorylation categories in normal (cognitively unimpaired, low neuropathology) and "resilient" (unimpaired despite AD pathology) individuals. In contrast, frail individuals, (low pathology, impaired cognition) showed a metabolic shift towards glycolysis and increased presence of proteasome subunits.Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis, it is not sufficient for causing cognitive impairment. Up to one third of community dwelling older adults harbor intermediate to high levels of AD neuropathology at death yet demonstrate no significant cognitive impairment. Conversely, there are individuals who exhibit dementia with no gross explanatory neuropathology. In prior studies, synapse loss correlated with cognitive impairment. To understand how synaptic composition changes in relation to neuropathology and cognition, multiplexed liquid chromatography mass-spectrometry was used to quantify enriched synaptic proteins from the parietal association cortex of 100 subjects with contrasting levels of AD pathology and cognitive performance. 123 unique proteins were significantly associated with diagnostic category. Functional analysis showed enrichment of serotonin release and oxidative phosphorylation categories in normal (cognitively unimpaired, low neuropathology) and "resilient" (unimpaired despite AD pathology) individuals. In contrast, frail individuals, (low pathology, impaired cognition) showed a metabolic shift towards glycolysis and increased presence of proteasome subunits.
Author Schneider, Julie A.
Bennett, David A.
Nairn, Angus C.
Morris, Robert
Arnold, Steven E.
Kandigian, Savannah E.
Kreuzer, Johannes
Petyuk, Vladislav A.
Trombetta, Bianca A.
Kuo, Yikai
Haas, Wilhelm
Carlyle, Becky C.
Kitchen, Robert R.
Das, Sudeshna
Hyman, Bradley T.
AuthorAffiliation c Massachusetts General Hospital Cancer Center, Charlestown, MA, USA
d Massachusetts General Hospital, Cardiology Division, Charlestown, MA, USA
a Massachusetts General Hospital Department of Neurology, Charlestown, MA, USA
e Rush Alzheimer’s Disease Center, Chicago, IL, USA
b Harvard Medical School, Boston, MA, USA
g Yale Department of Psychiatry, New Haven, CT, USA
f Pacific Northwest National Laboratory, Richland, WA, USA
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  surname: Petyuk
  fullname: Petyuk, Vladislav A.
  organization: Pacific Northwest National Laboratory, Richland, WA, USA
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  surname: Nairn
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  givenname: Steven E.
  surname: Arnold
  fullname: Arnold, Steven E.
  organization: Massachusetts General Hospital Department of Neurology, Charlestown, MA, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34052751$$D View this record in MEDLINE/PubMed
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Issue C
Keywords FDG-PET
LC-MS3
Neuroproteomics
AD
Angular gyrus
SPS-MS3
GSEA
SPE
Cognition
ROSMAP
MS1, MS2, MS3
Aβ
MMSE
Cognitive resilience
Aging
TMT11
m/z
BA39
bRPLC
Alzheimer's disease
AGC
HPLC
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2021. Published by Elsevier Inc.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
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content type line 23
USDOE
AC05-76RL01830
Becky C. Carlyle: Conceptualization, Methodology, Formal analysis, Investigation, Data curation, Writing – original draft, Visualization. Savannah E. Kandigian: Investigation, Writing – review & editing. Johannes Kreuzer: Investigation. Sudeshna Das: Supervision. Bianca A. Trombetta: Validation, Writing – review & editing. Yikai Kuo: Formal analysis, Visualization, Data curation. David A. Bennett: Resources, Writing – review & editing, Conceptualization. Julie A. Schneider: Resources, Conceptualization. Vladislav A. Petyuk: Writing – review & editing, Supervision. Robert R. Kitchen: Formal analysis, Data curation, Supervision, Resources. Robert Morris: Data curation. Angus C. Nairn: Writing – review & editing, Supervision. Bradley T. Hyman: Writing – review & editing, Supervision, Resources. Wilhelm Haas: Resources, Data curation, Writing – review & editing, Funding acquisition. Steven E. Arnold: Conceptualization, Resources, Data curation, Writing – review & editing, Funding acquisition.
CRediT authorship contribution statement
ORCID 0000-0003-1443-8559
0000-0002-7075-0195
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OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC8338777
PMID 34052751
PQID 2535106041
PQPubID 23479
PageCount 16
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_8338777
osti_scitechconnect_2471545
proquest_miscellaneous_2535106041
pubmed_primary_34052751
crossref_citationtrail_10_1016_j_neurobiolaging_2021_04_012
crossref_primary_10_1016_j_neurobiolaging_2021_04_012
elsevier_sciencedirect_doi_10_1016_j_neurobiolaging_2021_04_012
elsevier_clinicalkey_doi_10_1016_j_neurobiolaging_2021_04_012
PublicationCentury 2000
PublicationDate 2021-09-01
PublicationDateYYYYMMDD 2021-09-01
PublicationDate_xml – month: 09
  year: 2021
  text: 2021-09-01
  day: 01
PublicationDecade 2020
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PublicationTitle Neurobiology of aging
PublicationTitleAlternate Neurobiol Aging
PublicationYear 2021
Publisher Elsevier Inc
Elsevier
Publisher_xml – name: Elsevier Inc
– name: Elsevier
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Snippet •Proteomics linked 123 proteins to AD pathology and cognitive performance•Proteins involved in glucose metabolism are altered in cognitive impairment•Frail...
Alzheimer's disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis,...
Alzheimer’s disease (AD) is defined by the presence of abundant amyloid-β (Aβ) and tau neuropathology. While this neuropathology is necessary for AD diagnosis,...
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SubjectTerms 60 APPLIED LIFE SCIENCES
Aged
Aged, 80 and over
Aging
Aging - pathology
Aging - psychology
Alzheimer Disease - diagnosis
Alzheimer Disease - genetics
Alzheimer Disease - pathology
Alzheimer Disease - psychology
Alzheimer's disease
Angular gyrus
Chromatography, Liquid
Cognition
Cognition - physiology
Cognitive resilience
Female
Geriatrics & Gerontology
Glycolysis
Humans
Independent Living
Male
Mass Spectrometry
Neuroproteomics
Neurosciences & Neurology
Parietal Lobe - metabolism
Phosphorylation
Proteasome Endopeptidase Complex - metabolism
Proteomics - methods
Serotonin - metabolism
Synapses - metabolism
Synapses - pathology
Title Synaptic proteins associated with cognitive performance and neuropathology in older humans revealed by multiplexed fractionated proteomics
URI https://www.clinicalkey.com/#!/content/1-s2.0-S0197458021001275
https://dx.doi.org/10.1016/j.neurobiolaging.2021.04.012
https://www.ncbi.nlm.nih.gov/pubmed/34052751
https://www.proquest.com/docview/2535106041
https://www.osti.gov/servlets/purl/2471545
https://pubmed.ncbi.nlm.nih.gov/PMC8338777
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