Amyloid-β Increases Tau by Mediating Sirtuin 3 in Alzheimer’s Disease

Increasing evidence indicates that sirtuin 3 (Sirt3) has neuroprotective effects in regulating oxidative stress and energy metabolism, both of which are involved in the pathogenesis of Alzheimer’s disease (AD). However, it is unclear whether Sirt3 is associated with cognitive performance and patholo...

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Published inMolecular neurobiology Vol. 55; no. 11; pp. 8592 - 8601
Main Authors Yin, Junxiang, Han, Pengcheng, Song, Melissa, Nielsen, Megan, Beach, Thomas G., Serrano, Geidy E., Liang, Winnie S., Caselli, Richard J., Shi, Jiong
Format Journal Article
LanguageEnglish
Published New York Springer US 01.11.2018
Springer Nature B.V
Subjects
Online AccessGet full text
ISSN0893-7648
1559-1182
1559-1182
DOI10.1007/s12035-018-0977-0

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Abstract Increasing evidence indicates that sirtuin 3 (Sirt3) has neuroprotective effects in regulating oxidative stress and energy metabolism, both of which are involved in the pathogenesis of Alzheimer’s disease (AD). However, it is unclear whether Sirt3 is associated with cognitive performance and pathological changes in AD. We conducted a case-control study of the postmortem brains of AD ( n  = 16), mild cognitive impairment ( n  = 13), and age- and education-matched cognitively normal (CN, n  = 11) subjects. We measured the mRNA and protein levels of Sirt3 and assessed their association with cognitive performance and AD pathology. In an ex vivo model of cortical neurons from transgenic mice that carry human tau protein, we modified Sirt3 expression by genetic knockdown and knock-in to investigate the cause-effect relationship between Sirt3 and tau. Sirt3 levels were reduced in the entorhinal cortex, the middle temporal gyrus, and the superior frontal gyrus of AD subjects compared to those of CN. This reduction was associated with poorer test scores of neuropsychological evaluation and the severity of tau pathology. Further study with genetic manipulation of Sirt3 revealed that amyloid-β increased levels of total tau acetylated tau through its modulation of Sirt3. These data suggest that reduction of Sirt3 is critically involved in pathogenesis of AD.
AbstractList Increasing evidence indicates that sirtuin 3 (Sirt3) has neuroprotective effects in regulating oxidative stress and energy metabolism, both of which are involved in the pathogenesis of Alzheimer’s disease (AD). However, it is unclear whether Sirt3 is associated with cognitive performance and pathological changes in AD. We conducted a case-control study of the postmortem brains of AD (n = 16), mild cognitive impairment (n = 13), and age- and education-matched cognitively normal (CN, n = 11) subjects. We measured the mRNA and protein levels of Sirt3 and assessed their association with cognitive performance and AD pathology. In an ex vivo model of cortical neurons from transgenic mice that carry human tau protein, we modified Sirt3 expression by genetic knockdown and knock-in to investigate the cause-effect relationship between Sirt3 and tau. Sirt3 levels were reduced in the entorhinal cortex, the middle temporal gyrus, and the superior frontal gyrus of AD subjects compared to those of CN. This reduction was associated with poorer test scores of neuropsychological evaluation and the severity of tau pathology. Further study with genetic manipulation of Sirt3 revealed that amyloid-β increased levels of total tau acetylated tau through its modulation of Sirt3. These data suggest that reduction of Sirt3 is critically involved in pathogenesis of AD.
Increasing evidence indicates that sirtuin 3 (Sirt3) has neuroprotective effects in regulating oxidative stress and energy metabolism, both of which are involved in the pathogenesis of Alzheimer’s disease (AD). However, it is unclear whether Sirt3 is associated with cognitive performance and pathological changes in AD. We conducted a case-control study of the postmortem brains of AD ( n  = 16), mild cognitive impairment ( n  = 13), and age- and education-matched cognitively normal (CN, n  = 11) subjects. We measured the mRNA and protein levels of Sirt3 and assessed their association with cognitive performance and AD pathology. In an ex vivo model of cortical neurons from transgenic mice that carry human tau protein, we modified Sirt3 expression by genetic knockdown and knock-in to investigate the cause-effect relationship between Sirt3 and tau. Sirt3 levels were reduced in the entorhinal cortex, the middle temporal gyrus, and the superior frontal gyrus of AD subjects compared to those of CN. This reduction was associated with poorer test scores of neuropsychological evaluation and the severity of tau pathology. Further study with genetic manipulation of Sirt3 revealed that amyloid-β increased levels of total tau acetylated tau through its modulation of Sirt3. These data suggest that reduction of Sirt3 is critically involved in pathogenesis of AD.
Increasing evidence indicates that sirtuin 3 (Sirt3) has neuroprotective effects in regulating oxidative stress and energy metabolism, both of which are involved in the pathogenesis of Alzheimer's disease (AD). However, it is unclear whether Sirt3 is associated with cognitive performance and pathological changes in AD. We conducted a case-control study of the postmortem brains of AD (n = 16), mild cognitive impairment (n = 13), and age- and education-matched cognitively normal (CN, n = 11) subjects. We measured the mRNA and protein levels of Sirt3 and assessed their association with cognitive performance and AD pathology. In an ex vivo model of cortical neurons from transgenic mice that carry human tau protein, we modified Sirt3 expression by genetic knockdown and knock-in to investigate the cause-effect relationship between Sirt3 and tau. Sirt3 levels were reduced in the entorhinal cortex, the middle temporal gyrus, and the superior frontal gyrus of AD subjects compared to those of CN. This reduction was associated with poorer test scores of neuropsychological evaluation and the severity of tau pathology. Further study with genetic manipulation of Sirt3 revealed that amyloid-β increased levels of total tau acetylated tau through its modulation of Sirt3. These data suggest that reduction of Sirt3 is critically involved in pathogenesis of AD.Increasing evidence indicates that sirtuin 3 (Sirt3) has neuroprotective effects in regulating oxidative stress and energy metabolism, both of which are involved in the pathogenesis of Alzheimer's disease (AD). However, it is unclear whether Sirt3 is associated with cognitive performance and pathological changes in AD. We conducted a case-control study of the postmortem brains of AD (n = 16), mild cognitive impairment (n = 13), and age- and education-matched cognitively normal (CN, n = 11) subjects. We measured the mRNA and protein levels of Sirt3 and assessed their association with cognitive performance and AD pathology. In an ex vivo model of cortical neurons from transgenic mice that carry human tau protein, we modified Sirt3 expression by genetic knockdown and knock-in to investigate the cause-effect relationship between Sirt3 and tau. Sirt3 levels were reduced in the entorhinal cortex, the middle temporal gyrus, and the superior frontal gyrus of AD subjects compared to those of CN. This reduction was associated with poorer test scores of neuropsychological evaluation and the severity of tau pathology. Further study with genetic manipulation of Sirt3 revealed that amyloid-β increased levels of total tau acetylated tau through its modulation of Sirt3. These data suggest that reduction of Sirt3 is critically involved in pathogenesis of AD.
Author Liang, Winnie S.
Han, Pengcheng
Yin, Junxiang
Nielsen, Megan
Serrano, Geidy E.
Shi, Jiong
Song, Melissa
Beach, Thomas G.
Caselli, Richard J.
AuthorAffiliation 5 Department of Neurology, Mayo Clinic Arizona, Scottsdale, AZ, USA
3 Civin Laboratory for Neuropathology, Banner Sun Health Research, Institute, Sun City, AZ, USA
6 Tianjin Neurological Institute, Tianjin Medical University General Hospital, Tianjin, China
1 Barrow Neurological Institute, St. Joseph Hospital and Medical Center, Phoenix, AZ, USA
2 School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, USA
4 Translational Genomics Research Institute (TGen), Phoenix, AZ, USA
7 Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
AuthorAffiliation_xml – name: 6 Tianjin Neurological Institute, Tianjin Medical University General Hospital, Tianjin, China
– name: 2 School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, USA
– name: 4 Translational Genomics Research Institute (TGen), Phoenix, AZ, USA
– name: 1 Barrow Neurological Institute, St. Joseph Hospital and Medical Center, Phoenix, AZ, USA
– name: 5 Department of Neurology, Mayo Clinic Arizona, Scottsdale, AZ, USA
– name: 3 Civin Laboratory for Neuropathology, Banner Sun Health Research, Institute, Sun City, AZ, USA
– name: 7 Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
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  givenname: Junxiang
  surname: Yin
  fullname: Yin, Junxiang
  organization: Barrow Neurological Institute, St. Joseph Hospital and Medical Center
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  givenname: Pengcheng
  surname: Han
  fullname: Han, Pengcheng
  organization: Barrow Neurological Institute, St. Joseph Hospital and Medical Center
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  givenname: Melissa
  surname: Song
  fullname: Song, Melissa
  organization: Barrow Neurological Institute, St. Joseph Hospital and Medical Center, School of Arts and Sciences, University of Pennsylvania
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  givenname: Megan
  surname: Nielsen
  fullname: Nielsen, Megan
  organization: Barrow Neurological Institute, St. Joseph Hospital and Medical Center
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  fullname: Beach, Thomas G.
  organization: Civin Laboratory for Neuropathology, Banner Sun Health Research Institute
– sequence: 6
  givenname: Geidy E.
  surname: Serrano
  fullname: Serrano, Geidy E.
  organization: Civin Laboratory for Neuropathology, Banner Sun Health Research Institute
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  fullname: Liang, Winnie S.
  organization: Translational Genomics Research Institute (TGen)
– sequence: 8
  givenname: Richard J.
  surname: Caselli
  fullname: Caselli, Richard J.
  organization: Department of Neurology, Mayo Clinic Arizona
– sequence: 9
  givenname: Jiong
  orcidid: 0000-0001-7694-1366
  surname: Shi
  fullname: Shi, Jiong
  email: Jiong.Shi@DignityHealth.org
  organization: Barrow Neurological Institute, St. Joseph Hospital and Medical Center, Tianjin Neurological Institute, Tianjin Medical University General Hospital, Department of Neurology, Beijing Tiantan Hospital, Capital Medical University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29574628$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Springer Science+Business Media, LLC, part of Springer Nature 2018
Molecular Neurobiology is a copyright of Springer, (2018). All Rights Reserved.
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Issue 11
Keywords Tau
Amyloid
Acetylation
Alzheimer’s disease
Mild cognitive impairment
Sirtuin
Language English
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SubjectTerms Aged, 80 and over
Alzheimer Disease - metabolism
Alzheimer Disease - pathology
Alzheimer Disease - physiopathology
Alzheimer's disease
Amyloid beta-Peptides - toxicity
Animals
Autopsy
Biomedical and Life Sciences
Biomedicine
Brain - metabolism
Brain - pathology
Cell Biology
Cells, Cultured
Cognition
Cognitive ability
Cortex (entorhinal)
Energy metabolism
Female
Frontal gyrus
Humans
Male
Mice, Transgenic
mRNA
Neurobiology
Neurofibrillary Tangles - metabolism
Neurology
Neuroprotection
Neuropsychological Tests
Neurosciences
Oxidative metabolism
Oxidative stress
Pathogenesis
Pathology
Rodents
Sirtuin 3 - metabolism
Tau protein
tau Proteins - metabolism
Temporal gyrus
Temporal lobe
Temporal Lobe - metabolism
Temporal Lobe - pathology
Transgenic mice
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Title Amyloid-β Increases Tau by Mediating Sirtuin 3 in Alzheimer’s Disease
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