Mitochondrial RNA in Alzheimer’s Disease Circulating Extracellular Vesicles
Alzheimer's disease (AD) is the most common type of dementia. Amyloid β (Aβ) plaques, tau-containing neurofibrillary tangles, and neuronal loss leading to brain atrophy are pathologic hallmarks of AD. Given the importance of early diagnosis, extensive efforts have been undertaken to identify di...
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| Veröffentlicht in: | Frontiers in cell and developmental biology Jg. 8; S. 581882 |
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16.11.2020
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| Abstract | Alzheimer's disease (AD) is the most common type of dementia. Amyloid β (Aβ) plaques, tau-containing neurofibrillary tangles, and neuronal loss leading to brain atrophy are pathologic hallmarks of AD. Given the importance of early diagnosis, extensive efforts have been undertaken to identify diagnostic and prognostic biomarkers for AD. Circulating extracellular vesicles (EVs) provide a platform for "liquid biopsy" biomarkers for AD. Here, we characterized the RNA contents of plasma EVs of age-matched individuals who were cognitively normal (healthy controls (HC)) or had mild cognitive impairment (MCI) due to AD or had mild AD dementia (AD). Using RNA sequencing analysis, we found that mitochondrial (mt)-RNAs, including MT-ND1-6 mRNAs and other protein-coding and non-coding mt-RNAs, were strikingly elevated in plasma EVs of MCI and AD individuals compared with HC. EVs secreted from cultured astrocytes, microglia, and neurons after exposure to toxic conditions relevant to AD pathogenesis (Aβ aggregates and H2O2), contained mitochondrial structures (detected by electron microscopy) and mitochondrial RNA and protein. We propose that in the AD brain, toxicity-causing mitochondrial damage results in the packaging of mitochondrial components for export in EVs and further propose that mt-RNAs in plasma EVs can be diagnostic and prognostic biomarkers for MCI and AD.Alzheimer's disease (AD) is the most common type of dementia. Amyloid β (Aβ) plaques, tau-containing neurofibrillary tangles, and neuronal loss leading to brain atrophy are pathologic hallmarks of AD. Given the importance of early diagnosis, extensive efforts have been undertaken to identify diagnostic and prognostic biomarkers for AD. Circulating extracellular vesicles (EVs) provide a platform for "liquid biopsy" biomarkers for AD. Here, we characterized the RNA contents of plasma EVs of age-matched individuals who were cognitively normal (healthy controls (HC)) or had mild cognitive impairment (MCI) due to AD or had mild AD dementia (AD). Using RNA sequencing analysis, we found that mitochondrial (mt)-RNAs, including MT-ND1-6 mRNAs and other protein-coding and non-coding mt-RNAs, were strikingly elevated in plasma EVs of MCI and AD individuals compared with HC. EVs secreted from cultured astrocytes, microglia, and neurons after exposure to toxic conditions relevant to AD pathogenesis (Aβ aggregates and H2O2), contained mitochondrial structures (detected by electron microscopy) and mitochondrial RNA and protein. We propose that in the AD brain, toxicity-causing mitochondrial damage results in the packaging of mitochondrial components for export in EVs and further propose that mt-RNAs in plasma EVs can be diagnostic and prognostic biomarkers for MCI and AD. |
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| AbstractList | Alzheimer’s disease (AD) is the most common type of dementia. Amyloid β (Aβ) plaques, tau-containing neurofibrillary tangles, and neuronal loss leading to brain atrophy are pathologic hallmarks of AD. Given the importance of early diagnosis, extensive efforts have been undertaken to identify diagnostic and prognostic biomarkers for AD. Circulating extracellular vesicles (EVs) provide a platform for “liquid biopsy” biomarkers for AD. Here, we characterized the RNA contents of plasma EVs of age-matched individuals who were cognitively normal (healthy controls (HC)) or had mild cognitive impairment (MCI) due to AD or had mild AD dementia (AD). Using RNA sequencing analysis, we found that mitochondrial (mt)-RNAs, including MT-ND1-6 mRNAs and other protein-coding and non-coding mt-RNAs, were strikingly elevated in plasma EVs of MCI and AD individuals compared with HC. EVs secreted from cultured astrocytes, microglia, and neurons after exposure to toxic conditions relevant to AD pathogenesis (Aβ aggregates and H2O2), contained mitochondrial structures (detected by electron microscopy) and mitochondrial RNA and protein. We propose that in the AD brain, toxicity-causing mitochondrial damage results in the packaging of mitochondrial components for export in EVs and further propose that mt-RNAs in plasma EVs can be diagnostic and prognostic biomarkers for MCI and AD. Alzheimer's disease (AD) is the most common type of dementia. Amyloid β (Aβ) plaques, tau-containing neurofibrillary tangles, and neuronal loss leading to brain atrophy are pathologic hallmarks of AD. Given the importance of early diagnosis, extensive efforts have been undertaken to identify diagnostic and prognostic biomarkers for AD. Circulating extracellular vesicles (EVs) provide a platform for "liquid biopsy" biomarkers for AD. Here, we characterized the RNA contents of plasma EVs of age-matched individuals who were cognitively normal (healthy controls (HC)) or had mild cognitive impairment (MCI) due to AD or had mild AD dementia (AD). Using RNA sequencing analysis, we found that mitochondrial (mt)-RNAs, including MT-ND1-6 mRNAs and other protein-coding and non-coding mt-RNAs, were strikingly elevated in plasma EVs of MCI and AD individuals compared with HC. EVs secreted from cultured astrocytes, microglia, and neurons after exposure to toxic conditions relevant to AD pathogenesis (Aβ aggregates and H2O2), contained mitochondrial structures (detected by electron microscopy) and mitochondrial RNA and protein. We propose that in the AD brain, toxicity-causing mitochondrial damage results in the packaging of mitochondrial components for export in EVs and further propose that mt-RNAs in plasma EVs can be diagnostic and prognostic biomarkers for MCI and AD.Alzheimer's disease (AD) is the most common type of dementia. Amyloid β (Aβ) plaques, tau-containing neurofibrillary tangles, and neuronal loss leading to brain atrophy are pathologic hallmarks of AD. Given the importance of early diagnosis, extensive efforts have been undertaken to identify diagnostic and prognostic biomarkers for AD. Circulating extracellular vesicles (EVs) provide a platform for "liquid biopsy" biomarkers for AD. Here, we characterized the RNA contents of plasma EVs of age-matched individuals who were cognitively normal (healthy controls (HC)) or had mild cognitive impairment (MCI) due to AD or had mild AD dementia (AD). Using RNA sequencing analysis, we found that mitochondrial (mt)-RNAs, including MT-ND1-6 mRNAs and other protein-coding and non-coding mt-RNAs, were strikingly elevated in plasma EVs of MCI and AD individuals compared with HC. EVs secreted from cultured astrocytes, microglia, and neurons after exposure to toxic conditions relevant to AD pathogenesis (Aβ aggregates and H2O2), contained mitochondrial structures (detected by electron microscopy) and mitochondrial RNA and protein. We propose that in the AD brain, toxicity-causing mitochondrial damage results in the packaging of mitochondrial components for export in EVs and further propose that mt-RNAs in plasma EVs can be diagnostic and prognostic biomarkers for MCI and AD. |
| Author | Kapogiannis, Dimitrios Noh, Ji Heon Kim, Kyoung Mi Gorospe, Myriam De, Supriyo Cheng, Lesley Wood, William H. Kundu, Gautam Piao, Yulan Meng, Qiong Delannoy, Michael Abdelmohsen, Kotb Perez de Acha, Olivia Cheng, Aiwu Mustapic, Maja Eren, Erden Munk, Rachel |
| AuthorAffiliation | 1 Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, National Institutes of Health , Baltimore, MD , United States 2 Department of Biological Sciences, Chungnam National University , Daejeon , South Korea 3 Laboratory of Clinical Investigation, National Institute on Aging Intramural Research Program, National Institutes of Health , Baltimore, MD , United States 4 Department of Biochemistry, Chungnam National University , Daejeon , South Korea 5 Department of Cell Biology and Imaging Facility, Johns Hopkins University School of Medicine , Baltimore, MD , United States 6 Department of Biochemistry and Genetics, School of Molecular Science, La Trobe University , Melbourne, VI , Australia |
| AuthorAffiliation_xml | – name: 2 Department of Biological Sciences, Chungnam National University , Daejeon , South Korea – name: 6 Department of Biochemistry and Genetics, School of Molecular Science, La Trobe University , Melbourne, VI , Australia – name: 1 Laboratory of Genetics and Genomics, National Institute on Aging Intramural Research Program, National Institutes of Health , Baltimore, MD , United States – name: 5 Department of Cell Biology and Imaging Facility, Johns Hopkins University School of Medicine , Baltimore, MD , United States – name: 3 Laboratory of Clinical Investigation, National Institute on Aging Intramural Research Program, National Institutes of Health , Baltimore, MD , United States – name: 4 Department of Biochemistry, Chungnam National University , Daejeon , South Korea |
| Author_xml | – sequence: 1 givenname: Kyoung Mi surname: Kim fullname: Kim, Kyoung Mi – sequence: 2 givenname: Qiong surname: Meng fullname: Meng, Qiong – sequence: 3 givenname: Olivia surname: Perez de Acha fullname: Perez de Acha, Olivia – sequence: 4 givenname: Maja surname: Mustapic fullname: Mustapic, Maja – sequence: 5 givenname: Aiwu surname: Cheng fullname: Cheng, Aiwu – sequence: 6 givenname: Erden surname: Eren fullname: Eren, Erden – sequence: 7 givenname: Gautam surname: Kundu fullname: Kundu, Gautam – sequence: 8 givenname: Yulan surname: Piao fullname: Piao, Yulan – sequence: 9 givenname: Rachel surname: Munk fullname: Munk, Rachel – sequence: 10 givenname: William H. surname: Wood fullname: Wood, William H. – sequence: 11 givenname: Supriyo surname: De fullname: De, Supriyo – sequence: 12 givenname: Ji Heon surname: Noh fullname: Noh, Ji Heon – sequence: 13 givenname: Michael surname: Delannoy fullname: Delannoy, Michael – sequence: 14 givenname: Lesley surname: Cheng fullname: Cheng, Lesley – sequence: 15 givenname: Kotb surname: Abdelmohsen fullname: Abdelmohsen, Kotb – sequence: 16 givenname: Dimitrios surname: Kapogiannis fullname: Kapogiannis, Dimitrios – sequence: 17 givenname: Myriam surname: Gorospe fullname: Gorospe, Myriam |
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| Copyright | Copyright © 2020 Kim, Meng, Perez de Acha, Mustapic, Cheng, Eren, Kundu, Piao, Munk, Wood, De, Noh, Delannoy, Cheng, Abdelmohsen, Kapogiannis and Gorospe. Copyright © 2020 Kim, Meng, Perez de Acha, Mustapic, Cheng, Eren, Kundu, Piao, Munk, Wood, De, Noh, Delannoy, Cheng, Abdelmohsen, Kapogiannis and Gorospe. 2020 Kim, Meng, Perez de Acha, Mustapic, Cheng, Eren, Kundu, Piao, Munk, Wood, De, Noh, Delannoy, Cheng, Abdelmohsen, Kapogiannis and Gorospe |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Raman Chandrasekar, Kansas State University, United States; Suvendra Bhattacharyya, Indian Institute of Chemical Biology (CSIR), India Edited by: Oleg Shupliakov, Karolinska Institutet (KI), Sweden This article was submitted to Molecular Medicine, a section of the journal Frontiers in Cell and Developmental Biology These authors share first authorship |
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