Sensory lesioning induces microglial synapse elimination via ADAM10 and fractalkine signaling
Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to da...
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| Published in | Nature neuroscience Vol. 22; no. 7; pp. 1075 - 1088 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.07.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that
Cx3cl1
is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies
Cx3cr1
−/−
and
Cx3cl1
−/−
synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain.
Microglia are resident immune cells of the CNS. Here the authors show that neurons communicate to microglia via activity-dependent fractalkine and ADAM10 signaling to induce removal of synapses in the brain after sensory loss. |
|---|---|
| AbstractList | Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remains a key open question. Here, whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. We show that this synapse elimination is dependent on the microglial fractalkine receptor, CX3CR1, but not complement receptor 3, signaling. Further, mice deficient in the CX3CR1 ligand (CX3CL1) also have profound defects in synapse elimination. Single-cell RNAseq then revealed that
Cx3cl1
is cortical neuron-derived and
Adam10
, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and microglia following whisker lesioning. Finally, inhibition of
Adam10
phenocopies
Cx3cr1
−/−
and
Cx3cl1
−/−
synapse elimination defects. Together, these results identify novel neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1 −/− and Cx3cl1 −/− synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. Microglia are resident immune cells of the CNS. Here the authors show that neurons communicate to microglia via activity-dependent fractalkine and ADAM10 signaling to induce removal of synapses in the brain after sensory loss. Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1.sup.-/- and Cx3cl1.sup.-/- synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1 and Cx3cl1 synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1−/− and Cx3cl1−/− synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1.sup.-/- and Cx3cl1.sup.-/- synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. Microglia are resident immune cells of the CNS. Here the authors show that neurons communicate to microglia via activity-dependent fractalkine and ADAM10 signaling to induce removal of synapses in the brain after sensory loss. Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1-/- and Cx3cl1-/- synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain.Microglia rapidly respond to changes in neural activity and inflammation to regulate synaptic connectivity. The extracellular signals, particularly neuron-derived molecules, that drive these microglial functions at synapses remain a key open question. Here we show that whisker lesioning, known to dampen cortical activity, induces microglia-mediated synapse elimination. This synapse elimination is dependent on signaling by CX3CR1, the receptor for microglial fractalkine (also known as CXCL1), but not complement receptor 3. Furthermore, mice deficient in CX3CL1 have profound defects in synapse elimination. Single-cell RNA sequencing revealed that Cx3cl1 is derived from cortical neurons, and ADAM10, a metalloprotease that cleaves CX3CL1 into a secreted form, is upregulated specifically in layer IV neurons and in microglia following whisker lesioning. Finally, inhibition of ADAM10 phenocopies Cx3cr1-/- and Cx3cl1-/- synapse elimination defects. Together, these results identify neuron-to-microglia signaling necessary for cortical synaptic remodeling and reveal that context-dependent immune mechanisms are utilized to remodel synapses in the mammalian brain. |
| Audience | Academic |
| Author | Schafer, Dorothy P. Cheadle, Lucas Badimon, Ana Bemiller, Shane M. Lamb, Bruce T. Nagy, M. Aurel Kim, Ki-Wook Lira, Sergio A. Tapper, Andrew R. Schaefer, Anne Gunner, Georgia Liu, Liwang Mondo, Erica Ransohoff, Richard M. Johnson, Kasey M. Ayata, Pinar Greenberg, Michael E. |
| AuthorAffiliation | 1 Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School, Worcester, MA 01605, USA 3 Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA 4 Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai, New York, NY, USA 5 Stark Neurosciences Research Institute, Indiana University, Indianapolis, IN, 46202, USA 2 Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA 6 Department of Pharmacology and Center for Stem Cell and Regenerative Medicine, University of Illinois College of Medicine, Chicago, IL 60612, USA 7 Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA 8 Third Rock Ventures, Boston, MA 02116, USA |
| AuthorAffiliation_xml | – name: 6 Department of Pharmacology and Center for Stem Cell and Regenerative Medicine, University of Illinois College of Medicine, Chicago, IL 60612, USA – name: 7 Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA – name: 5 Stark Neurosciences Research Institute, Indiana University, Indianapolis, IN, 46202, USA – name: 2 Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA – name: 1 Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School, Worcester, MA 01605, USA – name: 8 Third Rock Ventures, Boston, MA 02116, USA – name: 3 Fishberg Department of Neuroscience, Department of Psychiatry, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA – name: 4 Ronald M. Loeb Center for Alzheimer’s Disease, Icahn School of Medicine at Mount Sinai, New York, NY, USA |
| Author_xml | – sequence: 1 givenname: Georgia orcidid: 0000-0002-6734-9632 surname: Gunner fullname: Gunner, Georgia organization: Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School – sequence: 2 givenname: Lucas surname: Cheadle fullname: Cheadle, Lucas organization: Department of Neurobiology, Harvard Medical School – sequence: 3 givenname: Kasey M. surname: Johnson fullname: Johnson, Kasey M. organization: Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School – sequence: 4 givenname: Pinar orcidid: 0000-0001-7621-832X 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: 5 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: 6 givenname: Erica surname: Mondo fullname: Mondo, Erica organization: Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School – sequence: 7 givenname: M. Aurel surname: Nagy fullname: Nagy, M. Aurel organization: Department of Neurobiology, Harvard Medical School – sequence: 8 givenname: Liwang orcidid: 0000-0003-4689-1964 surname: Liu fullname: Liu, Liwang organization: Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School – sequence: 9 givenname: Shane M. surname: Bemiller fullname: Bemiller, Shane M. organization: Stark Neurosciences Research Institute, Indiana University – sequence: 10 givenname: Ki-Wook surname: Kim fullname: Kim, Ki-Wook organization: Department of Pharmacology and Center for Stem Cell and Regenerative Medicine, University of Illinois College of Medicine – sequence: 11 givenname: Sergio A. surname: Lira fullname: Lira, Sergio A. organization: Precision Immunology Institute, Icahn School of Medicine at Mount Sinai – sequence: 12 givenname: Bruce T. orcidid: 0000-0001-8507-2561 surname: Lamb fullname: Lamb, Bruce T. organization: Stark Neurosciences Research Institute, Indiana University – sequence: 13 givenname: Andrew R. orcidid: 0000-0002-8358-6937 surname: Tapper fullname: Tapper, Andrew R. organization: Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School – sequence: 14 givenname: Richard M. orcidid: 0000-0003-0175-6910 surname: Ransohoff fullname: Ransohoff, Richard M. organization: Third Rock Ventures – sequence: 15 givenname: Michael E. orcidid: 0000-0003-1380-2160 surname: Greenberg fullname: Greenberg, Michael E. organization: Department of Neurobiology, Harvard Medical School – sequence: 16 givenname: Anne orcidid: 0000-0002-1051-3710 surname: Schaefer fullname: Schaefer, Anne 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: 17 givenname: Dorothy P. orcidid: 0000-0003-2201-6276 surname: Schafer fullname: Schafer, Dorothy P. email: Dorothy.schafer@umassmed.edu organization: Department of Neurobiology, Brudnick Neuropsychiatric Research Institute, University of Massachusetts Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31209379$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Authors contributed equally G.G. and D.P.S. designed the study, performed most experiments, analyzed most data, and wrote the manuscript, K.M.J. assisted in the design of initial experiments and performed experiments to identify initial synapse remodeling and engulfment phenotypes, L.C., M.A.N., and M.E.G. performed single-cell sequencing experiments. E.M. performed in situ hybridization experiments, P.A., A.B., and A.S. performed bulk RNAseq experiments of whole barrel cortex, L.L. and A.R.T. performed electrophysiology experiments. K.-W.K., S.M.B. and B.T.L. performed experiments related to Cx3cl1−/− mice, S.A.L. provided Cx3cl1−/− mice, R.M.R. provided critical input into study design and feedback on writing of the manuscript. Author Contributions |
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| SubjectTerms | 14 14/19 38 38/91 631/378 631/378/2596 631/378/340 631/378/3920 631/378/87 64 64/110 64/60 96 ADAM10 Protein - antagonists & inhibitors ADAM10 Protein - genetics ADAM10 Protein - physiology Alzheimer's disease Amyloid Precursor Protein Secretases - antagonists & inhibitors Amyloid Precursor Protein Secretases - genetics Amyloid Precursor Protein Secretases - physiology Analysis Animal Genetics and Genomics Animals Apoptosis Behavioral Sciences Biological Techniques Biomedical and Life Sciences Biomedicine Brain Brain research Cell Count Chemokine CX3CL1 - physiology Complement receptor 3 Control CX3C Chemokine Receptor 1 - deficiency CX3C Chemokine Receptor 1 - genetics CX3C Chemokine Receptor 1 - physiology CX3CR1 protein Defects Female Fractalkine Gene Expression Regulation Gene sequencing Ligands Male Medicine Membrane Proteins - antagonists & inhibitors Membrane Proteins - genetics Membrane Proteins - physiology Metalloproteinase Mice Mice, Inbred C57BL Mice, Knockout Microfluidic Analytical Techniques Microglia Microglia - physiology Neural networks Neural transmission Neurobiology Neurons Neurosciences Physiological aspects Ribonucleic acid RNA RNA, Messenger - biosynthesis RNA, Messenger - genetics Sensorimotor Cortex - metabolism Sensorimotor Cortex - pathology Sensorimotor Cortex - physiopathology Signal Transduction - physiology Signaling Single-Cell Analysis Synapse elimination Synapses Touch - physiology Transcriptome Vibrissae Vibrissae - injuries Vibrissae - physiology |
| Title | Sensory lesioning induces microglial synapse elimination via ADAM10 and fractalkine signaling |
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