Native-state proteomics of Parvalbumin interneurons identifies unique molecular signatures and vulnerabilities to early Alzheimer’s pathology
Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotin...
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| Vydáno v: | Nature communications Ročník 15; číslo 1; s. 2823 - 26 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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Nature Publishing Group UK
01.04.2024
Nature Publishing Group Nature Portfolio |
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| ISSN: | 2041-1723, 2041-1723 |
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| Abstract | Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis.
Native state proteomics of PV interneurons revealed unique molecular features of high translational and metabolic activity, and enrichment of Alzheimer’s risk genes. Early amyloid pathology exerted unique effects on mitochondria, mTOR signaling and neurotransmission in PV neurons. |
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| AbstractList | Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer's Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis.Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer's Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis. Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer's Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis. Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis. Native state proteomics of PV interneurons revealed unique molecular features of high translational and metabolic activity, and enrichment of Alzheimer’s risk genes. Early amyloid pathology exerted unique effects on mitochondria, mTOR signaling and neurotransmission in PV neurons. Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis. Native state proteomics of PV interneurons revealed unique molecular features of high translational and metabolic activity, and enrichment of Alzheimer’s risk genes. Early amyloid pathology exerted unique effects on mitochondria, mTOR signaling and neurotransmission in PV neurons. Abstract Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD). Defining early proteomic alterations in PV-INs can provide key biological and translationally-relevant insights. We used cell-type-specific in-vivo biotinylation of proteins (CIBOP) coupled with mass spectrometry to obtain native-state PV-IN proteomes. PV-IN proteomic signatures include high metabolic and translational activity, with over-representation of AD-risk and cognitive resilience-related proteins. In bulk proteomes, PV-IN proteins were associated with cognitive decline in humans, and with progressive neuropathology in humans and the 5xFAD mouse model of Aβ pathology. PV-IN CIBOP in early stages of Aβ pathology revealed signatures of increased mitochondria and metabolism, synaptic and cytoskeletal disruption and decreased mTOR signaling, not apparent in whole-brain proteomes. Furthermore, we demonstrated pre-synaptic defects in PV-to-excitatory neurotransmission, validating our proteomic findings. Overall, in this study we present native-state proteomes of PV-INs, revealing molecular insights into their unique roles in cognitive resiliency and AD pathogenesis. |
| ArticleNumber | 2823 |
| Author | Cheng, Lihong Kumar, Prateek Duong, Duc D. Dammer, Eric B. Rowan, Matthew J. M. Espinosa-Garcia, Claudia Goettemoeller, Annie M. Malepati, Sneha Seyfried, Nicholas T. Tfaily, Ali Wood, Levi B. Rangaraju, Srikant Natu, Aditya Xiao, Hailian Santiago, Juliet V. Nelson, Ruth S. Tobin, Brendan R. |
| Author_xml | – sequence: 1 givenname: Prateek orcidid: 0000-0001-5875-4065 surname: Kumar fullname: Kumar, Prateek organization: Department of Neurology, Emory University School of Medicine, Center for Neurodegenerative Disease, Emory University School of Medicine, 3 Department of Neurology, Yale University School of Medicine – sequence: 2 givenname: Annie M. surname: Goettemoeller fullname: Goettemoeller, Annie M. organization: Center for Neurodegenerative Disease, Emory University School of Medicine, Neuroscience Graduate Program, Laney Graduate School, Emory University – sequence: 3 givenname: Claudia surname: Espinosa-Garcia fullname: Espinosa-Garcia, Claudia organization: Department of Neurology, Emory University School of Medicine, 3 Department of Neurology, Yale University School of Medicine – sequence: 4 givenname: Brendan R. orcidid: 0000-0003-1250-4356 surname: Tobin fullname: Tobin, Brendan R. organization: Georgia W. Woodruff School of Mechanical Engineering, Parker H. Petit Institute for Bioengineering and Bioscience, and Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology – sequence: 5 givenname: Ali orcidid: 0000-0002-1534-5752 surname: Tfaily fullname: Tfaily, Ali organization: 3 Department of Neurology, Yale University School of Medicine – sequence: 6 givenname: Ruth S. surname: Nelson fullname: Nelson, Ruth S. organization: 3 Department of Neurology, Yale University School of Medicine – sequence: 7 givenname: Aditya surname: Natu fullname: Natu, Aditya organization: Department of Neurology, Emory University School of Medicine – sequence: 8 givenname: Eric B. orcidid: 0000-0003-2947-7606 surname: Dammer fullname: Dammer, Eric B. organization: Center for Neurodegenerative Disease, Emory University School of Medicine, Department of Biochemistry, Emory University – sequence: 9 givenname: Juliet V. surname: Santiago fullname: Santiago, Juliet V. organization: Department of Neurology, Emory University School of Medicine, Center for Neurodegenerative Disease, Emory University School of Medicine, Neuroscience Graduate Program, Laney Graduate School, Emory University – sequence: 10 givenname: Sneha surname: Malepati fullname: Malepati, Sneha organization: Center for Neurodegenerative Disease, Emory University School of Medicine, Department of Cell Biology, Emory University School of Medicine – sequence: 11 givenname: Lihong surname: Cheng fullname: Cheng, Lihong organization: Department of Neurology, Emory University School of Medicine, Center for Neurodegenerative Disease, Emory University School of Medicine – sequence: 12 givenname: Hailian surname: Xiao fullname: Xiao, Hailian organization: Department of Neurology, Emory University School of Medicine, Center for Neurodegenerative Disease, Emory University School of Medicine – sequence: 13 givenname: Duc D. surname: Duong fullname: Duong, Duc D. organization: Center for Neurodegenerative Disease, Emory University School of Medicine, Department of Biochemistry, Emory University – sequence: 14 givenname: Nicholas T. orcidid: 0000-0002-4507-624X surname: Seyfried fullname: Seyfried, Nicholas T. organization: Department of Neurology, Emory University School of Medicine, Center for Neurodegenerative Disease, Emory University School of Medicine, Department of Biochemistry, Emory University – sequence: 15 givenname: Levi B. surname: Wood fullname: Wood, Levi B. organization: Georgia W. Woodruff School of Mechanical Engineering, Parker H. Petit Institute for Bioengineering and Bioscience, and Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, School of Chemical and Biological Engineering, GeoInsrgia titute of Technology – sequence: 16 givenname: Matthew J. M. orcidid: 0000-0003-0955-0706 surname: Rowan fullname: Rowan, Matthew J. M. email: mjrowan@emory.edu organization: Center for Neurodegenerative Disease, Emory University School of Medicine, Department of Cell Biology, Emory University School of Medicine – sequence: 17 givenname: Srikant orcidid: 0000-0003-2765-1500 surname: Rangaraju fullname: Rangaraju, Srikant email: srikant.rangaraju@yale.edu organization: Department of Neurology, Emory University School of Medicine, Center for Neurodegenerative Disease, Emory University School of Medicine, 3 Department of Neurology, Yale University School of Medicine |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38561349$$D View this record in MEDLINE/PubMed |
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| Snippet | Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD). Defining... Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer's Disease (AD). Defining... Abstract Dysfunction in fast-spiking parvalbumin interneurons (PV-INs) may represent an early pathophysiological perturbation in Alzheimer’s Disease (AD).... |
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| Title | Native-state proteomics of Parvalbumin interneurons identifies unique molecular signatures and vulnerabilities to early Alzheimer’s pathology |
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