Excitation-Transcription Coupling in Parvalbumin-Positive Interneurons Employs a Novel CaM Kinase-Dependent Pathway Distinct from Excitatory Neurons
Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is po...
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| Published in | Neuron (Cambridge, Mass.) Vol. 90; no. 2; pp. 292 - 307 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
20.04.2016
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0896-6273 1097-4199 1097-4199 |
| DOI | 10.1016/j.neuron.2016.03.001 |
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| Abstract | Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca2+ influx through CaV1 channels triggers CaM nuclear translocation via local Ca2+ signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca2+ transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease.
•Voltage-gated Ca2+ influx triggers nuclear translocation of CaM in PV+ interneurons•CaMK signaling promotes CREB phosphorylation and activates key genes in PV+ cells•γCaMKI, not γCaMKII, operates to shuttle CaM to the nucleus in PV+ cells•Low CaMKIV levels rate-limit CREB phosphorylation in PV+ cells
Activity-dependent gene regulation is critical for long-term plasticity. Cohen et al. demonstrate that PV+ cortical interneurons rely on a CaM kinase-dependent signaling pathway, hinging on γCaMKI and rate-limited by CaMKIV, to trigger CREB phosphorylation and gene expression. |
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| AbstractList | Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca(2+) influx through CaV1 channels triggers CaM nuclear translocation via local Ca(2+) signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca(2+) transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease. Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca2+ influx through CaV1 channels triggers CaM nuclear translocation via local Ca2+ signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by gamma CaMKI, not gamma CaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca2+ transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease. Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca(2+) influx through CaV1 channels triggers CaM nuclear translocation via local Ca(2+) signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca(2+) transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease.Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca(2+) influx through CaV1 channels triggers CaM nuclear translocation via local Ca(2+) signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca(2+) transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease. Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca2+ influx through CaV1 channels triggers CaM nuclear translocation via local Ca2+ signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca2+ transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease. •Voltage-gated Ca2+ influx triggers nuclear translocation of CaM in PV+ interneurons•CaMK signaling promotes CREB phosphorylation and activates key genes in PV+ cells•γCaMKI, not γCaMKII, operates to shuttle CaM to the nucleus in PV+ cells•Low CaMKIV levels rate-limit CREB phosphorylation in PV+ cells Activity-dependent gene regulation is critical for long-term plasticity. Cohen et al. demonstrate that PV+ cortical interneurons rely on a CaM kinase-dependent signaling pathway, hinging on γCaMKI and rate-limited by CaMKIV, to trigger CREB phosphorylation and gene expression. Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity, and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. We report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca2+influx through CaV1 channels triggers CaM nuclear translocation via local Ca2+signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca2+transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and they are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease. Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development, connectivity and excitatory-inhibitory coordination. Despite its importance, excitation-transcription coupling in inhibitory interneurons is poorly understood. Here, we report that PV+ interneurons employ a novel CaMK-dependent pathway to trigger CREB phosphorylation and gene expression. As in excitatory neurons, voltage-gated Ca 2+ influx through Ca V 1 channels triggers CaM nuclear translocation via local Ca 2+ signaling. However, PV+ interneurons are distinct in that nuclear signaling is mediated by γCaMKI, not γCaMKII. CREB phosphorylation also proceeds with slow, sigmoid kinetics, rate-limited by paucity of CaMKIV, protecting against saturation of phospho-CREB in the face of higher firing rates and bigger Ca 2+ transients. Our findings support the generality of CaM shuttling to drive nuclear CaMK activity, and are relevant to disease pathophysiology, insofar as dysfunction of PV+ interneurons and molecules underpinning their excitation-transcription coupling both relate to neuropsychiatric disease. |
| Author | Ma, Huan Watson, Brendon O. Froemke, Robert C. Kuchibhotla, Kishore V. Buzsáki, György Tsien, Richard W. Cohen, Samuel M. |
| AuthorAffiliation | 3 The Helen and Martin Kimmel Center for Biology and Medicine at the Skirball Institute for Biomolecular Medicine, Molecular Neurobiology Program, Neuroscience Institute, Departments of Otolaryngology, Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA 4 Department of Psychiatry and Mind Brain Research Institute, Weill-Cornell Medical College, New York, NY, 10021, USA 2 Department of Physiology, Institute of Neuroscience, Program in Molecular Cell Biology, Zhejiang University School of Medicine, Hangzhou, China 1 NYU Neuroscience Institute and Department of Neuroscience and Physiology, NYU Langone Medical Center, New York, NY 10016, USA |
| AuthorAffiliation_xml | – name: 3 The Helen and Martin Kimmel Center for Biology and Medicine at the Skirball Institute for Biomolecular Medicine, Molecular Neurobiology Program, Neuroscience Institute, Departments of Otolaryngology, Neuroscience and Physiology, New York University School of Medicine, New York, NY 10016, USA – name: 4 Department of Psychiatry and Mind Brain Research Institute, Weill-Cornell Medical College, New York, NY, 10021, USA – name: 1 NYU Neuroscience Institute and Department of Neuroscience and Physiology, NYU Langone Medical Center, New York, NY 10016, USA – name: 2 Department of Physiology, Institute of Neuroscience, Program in Molecular Cell Biology, Zhejiang University School of Medicine, Hangzhou, China |
| Author_xml | – sequence: 1 givenname: Samuel M. surname: Cohen fullname: Cohen, Samuel M. organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA – sequence: 2 givenname: Huan surname: Ma fullname: Ma, Huan organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA – sequence: 3 givenname: Kishore V. surname: Kuchibhotla fullname: Kuchibhotla, Kishore V. organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA – sequence: 4 givenname: Brendon O. surname: Watson fullname: Watson, Brendon O. organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA – sequence: 5 givenname: György surname: Buzsáki fullname: Buzsáki, György organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA – sequence: 6 givenname: Robert C. surname: Froemke fullname: Froemke, Robert C. organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA – sequence: 7 givenname: Richard W. surname: Tsien fullname: Tsien, Richard W. email: richard.tsien@nyumc.org organization: Department of Neuroscience and Physiology and NYU Neuroscience Institute, NYU Langone Medical Center, New York, NY 10016, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27041500$$D View this record in MEDLINE/PubMed |
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| Snippet | Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development,... Properly functional CNS circuits depend on inhibitory interneurons that in turn rely upon activity-dependent gene expression for morphological development,... |
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| SubjectTerms | Acoustic Stimulation Animals Auditory Cortex - metabolism Calcium - metabolism Calcium-Calmodulin-Dependent Protein Kinases - metabolism Caveolin 1 - physiology Cyclic AMP Response Element-Binding Protein - metabolism Experiments Gene expression Immunoglobulins Interneurons - metabolism Interneurons - physiology Isoenzymes - metabolism Kinases Mice Neurons Neurons - metabolism Neurons - physiology Parvalbumins - metabolism Phosphorylation Rats Signal Transduction Statistical analysis Transcription, Genetic - physiology |
| Title | Excitation-Transcription Coupling in Parvalbumin-Positive Interneurons Employs a Novel CaM Kinase-Dependent Pathway Distinct from Excitatory Neurons |
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