Senolytic therapy alleviates Aβ-associated oligodendrocyte progenitor cell senescence and cognitive deficits in an Alzheimer's disease model
Neuritic plaques, a pathological hallmark in Alzheimer's disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating neurites that accumulate autolysosomes. We found that, in the brains of patients with AD and in AD mouse models, Aβ plaque-associated Oli...
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| Vydané v: | Nature neuroscience Ročník 22; číslo 5; s. 719 - 728 |
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| Hlavní autori: | , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
United States
Nature Publishing Group
01.05.2019
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| Predmet: | |
| ISSN: | 1097-6256, 1546-1726, 1546-1726 |
| On-line prístup: | Získať plný text |
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| Abstract | Neuritic plaques, a pathological hallmark in Alzheimer's disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating neurites that accumulate autolysosomes. We found that, in the brains of patients with AD and in AD mouse models, Aβ plaque-associated Olig2- and NG2-expressing oligodendrocyte progenitor cells (OPCs), but not astrocytes, microglia, or oligodendrocytes, exhibit a senescence-like phenotype characterized by the upregulation of p21/CDKN1A, p16/INK4/CDKN2A proteins, and senescence-associated β-galactosidase activity. Molecular interrogation of the Aβ plaque environment revealed elevated levels of transcripts encoding proteins involved in OPC function, replicative senescence, and inflammation. Direct exposure of cultured OPCs to aggregating Aβ triggered cell senescence. Senolytic treatment of AD mice selectively removed senescent cells from the plaque environment, reduced neuroinflammation, lessened Aβ load, and ameliorated cognitive deficits. Our findings suggest a role for Aβ-induced OPC cell senescence in neuroinflammation and cognitive deficits in AD, and a potential therapeutic benefit of senolytic treatments. |
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| AbstractList | Neuritic plaques, a pathological hallmark in Alzheimer's disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating neurites that accumulate autolysosomes. We found that, in the brains of patients with AD and in AD mouse models, Aβ plaque-associated Olig2- and NG2-expressing oligodendrocyte progenitor cells (OPCs), but not astrocytes, microglia, or oligodendrocytes, exhibit a senescence-like phenotype characterized by the upregulation of p21/CDKN1A, p16/INK4/CDKN2A proteins, and senescence-associated β-galactosidase activity. Molecular interrogation of the Aβ plaque environment revealed elevated levels of transcripts encoding proteins involved in OPC function, replicative senescence, and inflammation. Direct exposure of cultured OPCs to aggregating Aβ triggered cell senescence. Senolytic treatment of AD mice selectively removed senescent cells from the plaque environment, reduced neuroinflammation, lessened Aβ load, and ameliorated cognitive deficits. Our findings suggest a role for Aβ-induced OPC cell senescence in neuroinflammation and cognitive deficits in AD, and a potential therapeutic benefit of senolytic treatments.Neuritic plaques, a pathological hallmark in Alzheimer's disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating neurites that accumulate autolysosomes. We found that, in the brains of patients with AD and in AD mouse models, Aβ plaque-associated Olig2- and NG2-expressing oligodendrocyte progenitor cells (OPCs), but not astrocytes, microglia, or oligodendrocytes, exhibit a senescence-like phenotype characterized by the upregulation of p21/CDKN1A, p16/INK4/CDKN2A proteins, and senescence-associated β-galactosidase activity. Molecular interrogation of the Aβ plaque environment revealed elevated levels of transcripts encoding proteins involved in OPC function, replicative senescence, and inflammation. Direct exposure of cultured OPCs to aggregating Aβ triggered cell senescence. Senolytic treatment of AD mice selectively removed senescent cells from the plaque environment, reduced neuroinflammation, lessened Aβ load, and ameliorated cognitive deficits. Our findings suggest a role for Aβ-induced OPC cell senescence in neuroinflammation and cognitive deficits in AD, and a potential therapeutic benefit of senolytic treatments. Neuritic plaques, a pathological hallmark in Alzheimer's disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating neurites that accumulate autolysosomes. We found that, in the brains of patients with AD and in AD mouse models, Aβ plaque-associated Olig2- and NG2-expressing oligodendrocyte progenitor cells (OPCs), but not astrocytes, microglia, or oligodendrocytes, exhibit a senescence-like phenotype characterized by the upregulation of p21/CDKN1A, p16/INK4/CDKN2A proteins, and senescence-associated β-galactosidase activity. Molecular interrogation of the Aβ plaque environment revealed elevated levels of transcripts encoding proteins involved in OPC function, replicative senescence, and inflammation. Direct exposure of cultured OPCs to aggregating Aβ triggered cell senescence. Senolytic treatment of AD mice selectively removed senescent cells from the plaque environment, reduced neuroinflammation, lessened Aβ load, and ameliorated cognitive deficits. Our findings suggest a role for Aβ-induced OPC cell senescence in neuroinflammation and cognitive deficits in AD, and a potential therapeutic benefit of senolytic treatments. Neuritic plaques, a pathological hallmark in Alzheimer’s disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating neurites that accumulate autolysosomes. We found that, in the brains of patients with AD and in AD mouse models, Aβ plaque-associated Olig2- and NG2-expressing oligodendrocyte progenitor cells (OPCs), but not astrocytes, microglia, or oligodendrocytes, exhibit a senescence-like phenotype characterized by the upregulation of p21/CDKN1A, p16/INK4/CDKN2A proteins, and senescence-associated β-galactosidase activity. Molecular interrogation of the Aβ plaque environment revealed elevated levels of transcripts encoding proteins involved in OPC function, replicative senescence, and inflammation. Direct exposure of cultured OPCs to aggregating Aβ triggered cell senescence. Senolytic treatment of AD mice selectively removed senescent cells from the plaque environment, reduced neuroinflammation, lessened Aβ load, and ameliorated cognitive deficits. Our findings suggest a role for Aβ-induced OPC cell senescence in neuroinflammation and cognitive deficits in AD, and a potential therapeutic benefit of senolytic treatments.The Alzheimer’s disease (AD) amyloid-beta peptide causes oligodendrocyte progenitor cells to undergo senescence, contributing to neuroinflammation and cognitive impairment. Treatment of AD mice with senolytic drugs ameliorates AD neuropathologies and cognitive deficits. |
| Author | Mattson, Mark P Kishimoto, Yuki Zhang, Peisu Abdelmohsen, Kotb Gorospe, Myriam Misra Sen, Jyoti Grammatikakis, Ioannis Cutler, Roy G Zhang, Shiliang Gottimukkala, Kamalvishnu Bohr, Vilhelm A |
| Author_xml | – sequence: 1 givenname: Peisu orcidid: 0000-0003-2719-4143 surname: Zhang fullname: Zhang, Peisu email: zhangpei@mail.nih.gov organization: Laboratory of Neurosciences, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA. zhangpei@mail.nih.gov – sequence: 2 givenname: Yuki surname: Kishimoto fullname: Kishimoto, Yuki organization: Laboratory of Neurosciences, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 3 givenname: Ioannis surname: Grammatikakis fullname: Grammatikakis, Ioannis organization: Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 4 givenname: Kamalvishnu surname: Gottimukkala fullname: Gottimukkala, Kamalvishnu organization: Laboratory of Clinical Investigation, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 5 givenname: Roy G surname: Cutler fullname: Cutler, Roy G organization: Laboratory of Neurosciences, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 6 givenname: Shiliang surname: Zhang fullname: Zhang, Shiliang organization: Electron Microscopy Core, National Institute on Drug Abuse Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 7 givenname: Kotb surname: Abdelmohsen fullname: Abdelmohsen, Kotb organization: Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 8 givenname: Vilhelm A orcidid: 0000-0003-4823-6429 surname: Bohr fullname: Bohr, Vilhelm A organization: Laboratory of Molecular Gerontology, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 9 givenname: Jyoti surname: Misra Sen fullname: Misra Sen, Jyoti organization: Immunology Program, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA – sequence: 10 givenname: Myriam surname: Gorospe fullname: Gorospe, Myriam organization: Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, NIH, Baltimore, MD, USA – sequence: 11 givenname: Mark P orcidid: 0000-0002-9816-4155 surname: Mattson fullname: Mattson, Mark P email: mark.mattson@nih.gov, mark.mattson@nih.gov organization: Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD, USA. mark.mattson@nih.gov |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30936558$$D View this record in MEDLINE/PubMed |
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| References | 31024116 - Nat Neurosci. 2019 May;22(5):683-684. doi: 10.1038/s41593-019-0395-2. |
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| Snippet | Neuritic plaques, a pathological hallmark in Alzheimer's disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating... Neuritic plaques, a pathological hallmark in Alzheimer’s disease (AD) brains, comprise extracellular aggregates of amyloid-beta (Aβ) peptide and degenerating... |
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| SubjectTerms | Alzheimer Disease - drug therapy Alzheimer Disease - metabolism Alzheimer Disease - psychology Alzheimer's disease Amyloid beta-Peptides - administration & dosage Amyloid beta-Peptides - metabolism Animal models Animals Astrocytes Axons Cells (biology) Cellular Senescence - drug effects Cognitive ability Cyclin-dependent kinase inhibitors Dasatinib - administration & dosage Disease Models, Animal Female Galactosidase Glial stem cells Inflammation INK4 protein Interrogation Male Maze Learning - drug effects Mice, Transgenic Microglia Olig2 protein Oligodendrocyte Precursor Cells - metabolism Oligodendrocytes Phenotypes Plaque, Amyloid - ultrastructure Progenitor cells Prosencephalon - metabolism Prosencephalon - ultrastructure Proteins Quercetin - administration & dosage Senescence Senile plaques β-Amyloid β-Galactosidase |
| Title | Senolytic therapy alleviates Aβ-associated oligodendrocyte progenitor cell senescence and cognitive deficits in an Alzheimer's disease model |
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