Epigenetic regulation of brain region-specific microglia clearance activity
The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, bu...
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| Published in | Nature neuroscience Vol. 21; no. 8; pp. 1049 - 1060 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.08.2018
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, but not striatal or cortical, microglia exhibited high levels of basal clearance activity, which correlated with an elevated degree of cerebellar neuronal attrition. Exposing forebrain microglia to apoptotic cells activated gene-expression programs supporting clearance activity. We provide evidence that the polycomb repressive complex 2 (PRC2) epigenetically restricts the expression of genes that support clearance activity in striatal and cortical microglia. Loss of PRC2 leads to aberrant activation of a microglia clearance phenotype, which triggers changes in neuronal morphology and behavior. Our data highlight a key role of epigenetic mechanisms in preventing microglia-induced neuronal alterations that are frequently associated with neurodegenerative and psychiatric diseases.
Microglia clearance activity in adult brain is regulated epigenetically and region-specifically to match neuronal attrition rates. Uncoupling this activity from neural apoptosis leads to aberrant microglia activation & neurodegenerative-like changes. |
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| AbstractList | The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, but not striatal or cortical, microglia exhibited high levels of basal clearance activity, which correlated with an elevated degree of cerebellar neuronal attrition. Exposing forebrain microglia to apoptotic cells activated gene-expression programs supporting clearance activity. We provide evidence that the polycomb repressive complex 2 (PRC2) epigenetically restricts the expression of genes that support clearance activity in striatal and cortical microglia. Loss of PRC2 leads to aberrant activation of a microglia clearance phenotype, which triggers changes in neuronal morphology and behavior. Our data highlight a key role of epigenetic mechanisms in preventing microglia-induced neuronal alterations that are frequently associated with neurodegenerative and psychiatric diseases.The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, but not striatal or cortical, microglia exhibited high levels of basal clearance activity, which correlated with an elevated degree of cerebellar neuronal attrition. Exposing forebrain microglia to apoptotic cells activated gene-expression programs supporting clearance activity. We provide evidence that the polycomb repressive complex 2 (PRC2) epigenetically restricts the expression of genes that support clearance activity in striatal and cortical microglia. Loss of PRC2 leads to aberrant activation of a microglia clearance phenotype, which triggers changes in neuronal morphology and behavior. Our data highlight a key role of epigenetic mechanisms in preventing microglia-induced neuronal alterations that are frequently associated with neurodegenerative and psychiatric diseases. The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, but not striatal or cortical, microglia exhibited high levels of basal clearance activity, which correlated with an elevated degree of cerebellar neuronal attrition. Exposing forebrain microglia to apoptotic cells activated gene-expression programs supporting clearance activity. We provide evidence that the polycomb repressive complex 2 (PRC2) epigenetically restricts the expression of genes that support clearance activity in striatal and cortical microglia. Loss of PRC2 leads to aberrant activation of a microglia clearance phenotype, which triggers changes in neuronal morphology and behavior. Our data highlight a key role of epigenetic mechanisms in preventing microglia-induced neuronal alterations that are frequently associated with neurodegenerative and psychiatric diseases. The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, but not striatal or cortical, microglia exhibited high levels of basal clearance activity, which correlated with an elevated degree of cerebellar neuronal attrition. Exposing forebrain microglia to apoptotic cells activated gene-expression programs supporting clearance activity. We provide evidence that the polycomb repressive complex 2 (PRC2) epigenetically restricts the expression of genes that support clearance activity in striatal and cortical microglia. Loss of PRC2 leads to aberrant activation of a microglia clearance phenotype, which triggers changes in neuronal morphology and behavior. Our data highlight a key role of epigenetic mechanisms in preventing microglia-induced neuronal alterations that are frequently associated with neurodegenerative and psychiatric diseases. Microglia clearance activity in adult brain is regulated epigenetically and region-specifically to match neuronal attrition rates. Uncoupling this activity from neural apoptosis leads to aberrant microglia activation & neurodegenerative-like changes. The rapid elimination of dying neurons and non-functional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we show that microglia clearance activity in the adult brain is regionally regulated and depends on the rate of neuronal attrition. Cerebellar, but not striatal or cortical, microglia exhibited high levels of basal clearance activity, which correlated with an elevated degree of cerebellar neuronal attrition. Exposing forebrain microglia to apoptotic cells activated gene expression programs supporting clearance activity. We provide evidence that the Polycomb repressive complex 2 (PRC2) epigenetically restricts the expression of genes that support clearance activity in striatal and cortical microglia. Loss of PRC2 led to the aberrant activation of a microglia clearance phenotype, which triggers changes in neuronal morphology and behavior. Our data highlight a key role of epigenetic mechanisms in preventing microglia-induced neuronal alterations that are frequently associated with neurodegenerative and psychiatric diseases. |
| Author | Losic, Bojan Badimon, Ana Loh, Yong-Hwee E. Goate, Alison M. Ramirez, Brianna R. Busslinger, Meinrad Pimenova, Anna A. Shen, Li Scarpa, Joseph R. Strasburger, Hayley J. Duff, Mary Kaye Ebert, Anja Montgomery, Sarah E. Schaefer, Anne Sullivan, Josefa M. Purushothaman, Immanuel Chan, Andrew T. Ayata, Pinar |
| AuthorAffiliation | 4 Department of Genetics & Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 2 Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai, New York, NY, USA 1 Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 3 Research Institute of Molecular Pathology, Vienna Biocenter, 1030 Vienna, Austria |
| AuthorAffiliation_xml | – name: 3 Research Institute of Molecular Pathology, Vienna Biocenter, 1030 Vienna, Austria – name: 2 Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai, New York, NY, USA – name: 4 Department of Genetics & Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 1 Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA |
| Author_xml | – sequence: 1 givenname: Pinar surname: Ayata fullname: Ayata, Pinar organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai – sequence: 2 givenname: Ana surname: Badimon fullname: Badimon, Ana organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 3 givenname: Hayley J. surname: Strasburger fullname: Strasburger, Hayley J. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 4 givenname: Mary Kaye surname: Duff fullname: Duff, Mary Kaye organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 5 givenname: Sarah E. surname: Montgomery fullname: Montgomery, Sarah E. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 6 givenname: Yong-Hwee E. surname: Loh fullname: Loh, Yong-Hwee E. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 7 givenname: Anja surname: Ebert fullname: Ebert, Anja organization: Research Institute of Molecular Pathology – sequence: 8 givenname: Anna A. orcidid: 0000-0003-3342-8778 surname: Pimenova fullname: Pimenova, Anna A. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai – sequence: 9 givenname: Brianna R. surname: Ramirez fullname: Ramirez, Brianna R. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 10 givenname: Andrew T. surname: Chan fullname: Chan, Andrew T. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 11 givenname: Josefa M. surname: Sullivan fullname: Sullivan, Josefa M. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 12 givenname: Immanuel surname: Purushothaman fullname: Purushothaman, Immanuel organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 13 givenname: Joseph R. surname: Scarpa fullname: Scarpa, Joseph R. organization: Department of Genetics & Genomic Sciences, Icahn School of Medicine at Mount Sinai – sequence: 14 givenname: Alison M. orcidid: 0000-0002-0576-2472 surname: Goate fullname: Goate, Alison M. organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai, Department of Genetics & Genomic Sciences, Icahn School of Medicine at Mount Sinai – sequence: 15 givenname: Meinrad surname: Busslinger fullname: Busslinger, Meinrad organization: Research Institute of Molecular Pathology – sequence: 16 givenname: Li orcidid: 0000-0002-5190-2851 surname: Shen fullname: Shen, Li organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai – sequence: 17 givenname: Bojan surname: Losic fullname: Losic, Bojan organization: Department of Genetics & Genomic Sciences, Icahn School of Medicine at Mount Sinai, Tisch Cancer Institute, Cancer Immunology Program, Icahn School of Medicine at Mount Sinai – sequence: 18 givenname: Anne orcidid: 0000-0002-1051-3710 surname: Schaefer fullname: Schaefer, Anne email: anne.schaefer@mssm.edu organization: Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30038282$$D View this record in MEDLINE/PubMed |
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| Snippet | The rapid elimination of dying neurons and nonfunctional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we... The rapid elimination of dying neurons and non-functional synapses in the brain is carried out by microglia, the resident myeloid cells of the brain. Here we... |
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| Title | Epigenetic regulation of brain region-specific microglia clearance activity |
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