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  1. Article ; Online: Proteomic profiling of interferon-responsive reactive astrocytes in rodent and human.

    Prakash, Priya / Erdjument-Bromage, Hediye / O'Dea, Michael R / Munson, Christy N / Labib, David / Fossati, Valentina / Neubert, Thomas A / Liddelow, Shane A

    Glia

    2023  Volume 72, Issue 3, Page(s) 625–642

    Abstract: Astrocytes are a heterogeneous population of central nervous system glial cells that respond to pathological insults and injury by undergoing a transformation called "reactivity." Reactive astrocytes exhibit distinct and context-dependent cellular, ... ...

    Abstract Astrocytes are a heterogeneous population of central nervous system glial cells that respond to pathological insults and injury by undergoing a transformation called "reactivity." Reactive astrocytes exhibit distinct and context-dependent cellular, molecular, and functional state changes that can either support or disturb tissue homeostasis. We recently identified a reactive astrocyte sub-state defined by interferon-responsive genes like Igtp, Ifit3, Mx1, and others, called interferon-responsive reactive astrocytes (IRRAs). To further this transcriptomic definition of IRRAs, we wanted to define the proteomic changes that occur in this reactive sub-state. We induced IRRAs in immunopanned rodent astrocytes and human iPSC-differentiated astrocytes using TNF, IL1α, C1Q, and IFNβ and characterized their proteomic profile (both cellular and secreted) using unbiased quantitative proteomics. We identified 2335 unique cellular proteins, including IFIT2/3, IFITM3, OASL1/2, MX1/2/3, and STAT1. We also report that rodent and human IRRAs secrete PAI1, a serine protease inhibitor which may influence reactive states and functions of nearby cells. Finally, we evaluated how IRRAs are distinct from neurotoxic reactive astrocytes (NRAs). While NRAs are described by expression of the complement protein C3, it was not upregulated in IRRAs. Instead, we found ~90 proteins unique to IRRAs not identified in NRAs, including OAS1A, IFIT3, and MX1. Interferon signaling in astrocytes is critical for the antiviral immune response and for regulating synaptic plasticity and glutamate transport mechanisms. How IRRAs contribute to these functions is unknown. This study provides the basis for future experiments to define the functional roles of IRRAs in the context of neurodegenerative disorders.
    MeSH term(s) Animals ; Humans ; Astrocytes/metabolism ; Interferons/metabolism ; Rodentia/metabolism ; Proteomics ; Central Nervous System/metabolism ; Membrane Proteins/metabolism ; RNA-Binding Proteins/metabolism
    Chemical Substances Interferons (9008-11-1) ; IFITM3 protein, human ; Membrane Proteins ; RNA-Binding Proteins
    Language English
    Publishing date 2023-11-30
    Publishing country United States
    Document type Journal Article
    ZDB-ID 639414-0
    ISSN 1098-1136 ; 0894-1491
    ISSN (online) 1098-1136
    ISSN 0894-1491
    DOI 10.1002/glia.24494
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  2. Article ; Online: The embryonic zebrafish brain is seeded by a lymphatic-dependent population of mrc1

    Green, Lauren A / O'Dea, Michael R / Hoover, Camden A / DeSantis, Dana F / Smith, Cody J

    Nature neuroscience

    2022  Volume 25, Issue 7, Page(s) 849–864

    Abstract: Microglia are the resident macrophages of the CNS that serve critical roles in brain construction. Although human brains contain microglia by 4 weeks gestation, an understanding of the earliest microglia that seed the brain during its development remains ...

    Abstract Microglia are the resident macrophages of the CNS that serve critical roles in brain construction. Although human brains contain microglia by 4 weeks gestation, an understanding of the earliest microglia that seed the brain during its development remains unresolved. Using time-lapse imaging in zebrafish, we discovered a mrc1a
    MeSH term(s) Animals ; Brain/physiology ; Humans ; Microglia/metabolism ; Yolk Sac/metabolism ; Zebrafish ; Zebrafish Proteins/genetics ; Zebrafish Proteins/metabolism
    Chemical Substances Zebrafish Proteins
    Language English
    Publishing date 2022-06-16
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 1420596-8
    ISSN 1546-1726 ; 1097-6256
    ISSN (online) 1546-1726
    ISSN 1097-6256
    DOI 10.1038/s41593-022-01091-9
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  3. Article ; Online: Astrocytes and oligodendrocytes undergo subtype-specific transcriptional changes in Alzheimer's disease.

    Sadick, Jessica S / O'Dea, Michael R / Hasel, Philip / Dykstra, Taitea / Faustin, Arline / Liddelow, Shane A

    Neuron

    2022  Volume 110, Issue 11, Page(s) 1788–1805.e10

    Abstract: Resolving glial contributions to Alzheimer's disease (AD) is necessary because changes in neuronal function, such as reduced synaptic density, altered electrophysiological properties, and degeneration, are not entirely cell autonomous. To improve ... ...

    Abstract Resolving glial contributions to Alzheimer's disease (AD) is necessary because changes in neuronal function, such as reduced synaptic density, altered electrophysiological properties, and degeneration, are not entirely cell autonomous. To improve understanding of transcriptomic heterogeneity in glia during AD, we used single-nuclei RNA sequencing (snRNA-seq) to characterize astrocytes and oligodendrocytes from apolipoprotein (APOE) Ɛ2/3 human AD and age- and genotype-matched non-symptomatic (NS) brains. We enriched astrocytes before sequencing and characterized pathology from the same location as the sequenced material. We characterized baseline heterogeneity in both astrocytes and oligodendrocytes and identified global and subtype-specific transcriptomic changes between AD and NS astrocytes and oligodendrocytes. We also took advantage of recent human and mouse spatial transcriptomics resources to localize heterogeneous astrocyte subtypes to specific regions in the healthy and inflamed brain. Finally, we integrated our data with published AD snRNA-seq datasets, highlighting the power of combining datasets to resolve previously unidentifiable astrocyte subpopulations.
    MeSH term(s) Alzheimer Disease/pathology ; Animals ; Astrocytes/pathology ; Humans ; Mice ; Neuroglia/pathology ; Oligodendroglia/pathology ; RNA, Small Nuclear ; Transcriptome
    Chemical Substances RNA, Small Nuclear
    Language English
    Publishing date 2022-04-04
    Publishing country United States
    Document type Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
    ZDB-ID 808167-0
    ISSN 1097-4199 ; 0896-6273
    ISSN (online) 1097-4199
    ISSN 0896-6273
    DOI 10.1016/j.neuron.2022.03.008
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  4. Article ; Online: Identification of astroglia-like cardiac nexus glia that are critical regulators of cardiac development and function.

    Kikel-Coury, Nina L / Brandt, Jacob P / Correia, Isabel A / O'Dea, Michael R / DeSantis, Dana F / Sterling, Felicity / Vaughan, Kevin / Ozcebe, Gulberk / Zorlutuna, Pinar / Smith, Cody J

    PLoS biology

    2021  Volume 19, Issue 11, Page(s) e3001444

    Abstract: Glial cells are essential for functionality of the nervous system. Growing evidence underscores the importance of astrocytes; however, analogous astroglia in peripheral organs are poorly understood. Using confocal time-lapse imaging, fate mapping, and ... ...

    Abstract Glial cells are essential for functionality of the nervous system. Growing evidence underscores the importance of astrocytes; however, analogous astroglia in peripheral organs are poorly understood. Using confocal time-lapse imaging, fate mapping, and mutant genesis in a zebrafish model, we identify a neural crest-derived glial cell, termed nexus glia, which utilizes Meteorin signaling via Jak/Stat3 to drive differentiation and regulate heart rate and rhythm. Nexus glia are labeled with gfap, glast, and glutamine synthetase, markers that typically denote astroglia cells. Further, analysis of single-cell sequencing datasets of human and murine hearts across ages reveals astrocyte-like cells, which we confirm through a multispecies approach. We show that cardiac nexus glia at the outflow tract are critical regulators of both the sympathetic and parasympathetic system. These data establish the crucial role of glia on cardiac homeostasis and provide a description of nexus glia in the PNS.
    MeSH term(s) Animals ; Astrocytes/cytology ; Astrocytes/metabolism ; Glial Fibrillary Acidic Protein/metabolism ; Heart/embryology ; Heart/physiology ; Heart Rate/physiology ; Heart Ventricles/metabolism ; Humans ; Mice ; Myocytes, Cardiac/metabolism ; Nerve Tissue Proteins/metabolism ; Neural Crest/metabolism ; Neuroglia/cytology ; Neuroglia/metabolism ; Neurons/metabolism ; Parasympathetic Nervous System/physiology ; Signal Transduction ; Species Specificity ; Sympathetic Nervous System/physiology ; Zebrafish
    Chemical Substances Glial Fibrillary Acidic Protein ; Nerve Tissue Proteins
    Language English
    Publishing date 2021-11-18
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2126776-5
    ISSN 1545-7885 ; 1544-9173
    ISSN (online) 1545-7885
    ISSN 1544-9173
    DOI 10.1371/journal.pbio.3001444
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    Zs.A 6193: Show issues Location:
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  5. Article: Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation

    Fernández-Castañeda, Anthony / Lu, Peiwen / Geraghty, Anna C. / Song, Eric / Lee, Myoung-Hwa / Wood, Jamie / O’Dea, Michael R. / Dutton, Selena / Shamardani, Kiarash / Nwangwu, Kamsi / Mancusi, Rebecca / Yalçın, Belgin / Taylor, Kathryn R. / Acosta-Alvarez, Lehi / Malacon, Karen / Keough, Michael B. / Ni, Lijun / Woo, Pamelyn J. / Contreras-Esquivel, Daniel /
    Shaw Toland, Angus Martin / Gehlhausen, Jeff R. / Klein, Jon / Takahashi, Takehiro / Silva, Julio / Israelow, Benjamin / Lucas, Carolina / Mao, Tianyang / Peña-Hernández, Mario A. / Tabachnikova, Alexandra / Homer, Robert J. / Tabacof, Laura / Tosto-Mancuso, Jenna / Breyman, Erica / Kontorovich, Amy / McCarthy, Dayna / Quezado, Martha / Vogel, Hannes / Hefti, Marco M. / Perl, Daniel P. / Liddelow, Shane / Folkerth, Rebecca / Putrino, David / Nath, Avindra / Iwasaki, Akiko / Monje, Michelle

    Cell. 2022 June 07,

    2022  

    Abstract: COVID survivors frequently experience lingering neurological symptoms that resemble cancer therapy-related cognitive impairment, a syndrome for which white-matter microglial reactivity and consequent neural dysregulation is central. Here, we explored the ...

    Abstract COVID survivors frequently experience lingering neurological symptoms that resemble cancer therapy-related cognitive impairment, a syndrome for which white-matter microglial reactivity and consequent neural dysregulation is central. Here, we explored the neurobiological effects of respiratory SARS-CoV-2 infection and found white-matter-selective microglial reactivity in mice and humans. Following mild respiratory COVID in mice, persistently impaired hippocampal neurogenesis, decreased oligodendrocytes and myelin loss were evident together with elevated CSF cytokines/chemokines including CCL11. Systemic CCL11 administration specifically caused hippocampal microglial reactivity and impaired neurogenesis. Concordantly, humans with lasting cognitive symptoms post-COVID exhibit elevated CCL11 levels. Compared to SARS-CoV-2, mild respiratory influenza in mice caused similar patterns of white matter-selective microglial reactivity, oligodendrocyte loss, impaired neurogenesis and elevated CCL11 at early timepoints, but after influenza only elevated CCL11 and hippocampal pathology persisted. These findings illustrate similar neuropathophysiology after cancer therapy and respiratory SARS-CoV-2 infection which may contribute to cognitive impairment following even mild COVID.
    Keywords Severe acute respiratory syndrome coronavirus 2 ; cancer therapy ; cognition ; cognitive disorders ; influenza ; myelin sheath ; neurogenesis ; oligodendroglia
    Language English
    Dates of publication 2022-0607
    Publishing place Elsevier Inc.
    Document type Article
    Note Pre-press version
    ZDB-ID 187009-9
    ISSN 1097-4172 ; 0092-8674
    ISSN (online) 1097-4172
    ISSN 0092-8674
    DOI 10.1016/j.cell.2022.06.008
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  6. Article ; Online: Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation.

    Fernández-Castañeda, Anthony / Lu, Peiwen / Geraghty, Anna C / Song, Eric / Lee, Myoung-Hwa / Wood, Jamie / O'Dea, Michael R / Dutton, Selena / Shamardani, Kiarash / Nwangwu, Kamsi / Mancusi, Rebecca / Yalçın, Belgin / Taylor, Kathryn R / Acosta-Alvarez, Lehi / Malacon, Karen / Keough, Michael B / Ni, Lijun / Woo, Pamelyn J / Contreras-Esquivel, Daniel /
    Toland, Angus Martin Shaw / Gehlhausen, Jeff R / Klein, Jon / Takahashi, Takehiro / Silva, Julio / Israelow, Benjamin / Lucas, Carolina / Mao, Tianyang / Peña-Hernández, Mario A / Tabachnikova, Alexandra / Homer, Robert J / Tabacof, Laura / Tosto-Mancuso, Jenna / Breyman, Erica / Kontorovich, Amy / McCarthy, Dayna / Quezado, Martha / Vogel, Hannes / Hefti, Marco M / Perl, Daniel P / Liddelow, Shane / Folkerth, Rebecca / Putrino, David / Nath, Avindra / Iwasaki, Akiko / Monje, Michelle

    Cell

    2022  Volume 185, Issue 14, Page(s) 2452–2468.e16

    Abstract: COVID survivors frequently experience lingering neurological symptoms that resemble cancer-therapy-related cognitive impairment, a syndrome for which white matter microglial reactivity and consequent neural dysregulation is central. Here, we explored the ...

    Abstract COVID survivors frequently experience lingering neurological symptoms that resemble cancer-therapy-related cognitive impairment, a syndrome for which white matter microglial reactivity and consequent neural dysregulation is central. Here, we explored the neurobiological effects of respiratory SARS-CoV-2 infection and found white-matter-selective microglial reactivity in mice and humans. Following mild respiratory COVID in mice, persistently impaired hippocampal neurogenesis, decreased oligodendrocytes, and myelin loss were evident together with elevated CSF cytokines/chemokines including CCL11. Systemic CCL11 administration specifically caused hippocampal microglial reactivity and impaired neurogenesis. Concordantly, humans with lasting cognitive symptoms post-COVID exhibit elevated CCL11 levels. Compared with SARS-CoV-2, mild respiratory influenza in mice caused similar patterns of white-matter-selective microglial reactivity, oligodendrocyte loss, impaired neurogenesis, and elevated CCL11 at early time points, but after influenza, only elevated CCL11 and hippocampal pathology persisted. These findings illustrate similar neuropathophysiology after cancer therapy and respiratory SARS-CoV-2 infection which may contribute to cognitive impairment following even mild COVID.
    MeSH term(s) Animals ; COVID-19 ; Humans ; Influenza, Human/pathology ; Mice ; Microglia/pathology ; Myelin Sheath ; Neoplasms/pathology ; SARS-CoV-2
    Language English
    Publishing date 2022-06-13
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 187009-9
    ISSN 1097-4172 ; 0092-8674
    ISSN (online) 1097-4172
    ISSN 0092-8674
    DOI 10.1016/j.cell.2022.06.008
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