Miro1-dependent mitochondrial dynamics in parvalbumin interneurons
The spatiotemporal distribution of mitochondria is crucial for precise ATP provision and calcium buffering required to support neuronal signaling. Fast-spiking GABAergic interneurons expressing parvalbumin (PV+) have a high mitochondrial content reflecting their large energy utilization. The importa...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/65215 |
| _version_ | 1811227780951572480 |
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| author | Georgina Kontou Pantelis Antonoudiou Marina Podpolny Blanka R Szulc I Lorena Arancibia-Carcamo Nathalie F Higgs Guillermo Lopez-Domenech Patricia C Salinas Edward O Mann Josef T Kittler |
| author_facet | Georgina Kontou Pantelis Antonoudiou Marina Podpolny Blanka R Szulc I Lorena Arancibia-Carcamo Nathalie F Higgs Guillermo Lopez-Domenech Patricia C Salinas Edward O Mann Josef T Kittler |
| author_sort | Georgina Kontou |
| collection | DOAJ |
| description | The spatiotemporal distribution of mitochondria is crucial for precise ATP provision and calcium buffering required to support neuronal signaling. Fast-spiking GABAergic interneurons expressing parvalbumin (PV+) have a high mitochondrial content reflecting their large energy utilization. The importance for correct trafficking and precise mitochondrial positioning remains poorly elucidated in inhibitory neurons. Miro1 is a Ca²+-sensing adaptor protein that links mitochondria to the trafficking apparatus, for their microtubule-dependent transport along axons and dendrites, in order to meet the metabolic and Ca2+-buffering requirements of the cell. Here, we explore the role of Miro1 in PV+ interneurons and how changes in mitochondrial trafficking could alter network activity in the mouse brain. By employing live and fixed imaging, we found that the impairments in Miro1-directed trafficking in PV+ interneurons altered their mitochondrial distribution and axonal arborization, while PV+ interneuron-mediated inhibition remained intact. These changes were accompanied by an increase in the ex vivo hippocampal γ-oscillation (30–80 Hz) frequency and promoted anxiolysis. Our findings show that precise regulation of mitochondrial dynamics in PV+ interneurons is crucial for proper neuronal signaling and network synchronization. |
| first_indexed | 2024-04-12T09:47:30Z |
| format | Article |
| id | doaj.art-4d3e5b3159ce4d0cb90916065d78e0f0 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:47:30Z |
| publishDate | 2021-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-4d3e5b3159ce4d0cb90916065d78e0f02022-12-22T03:37:54ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.65215Miro1-dependent mitochondrial dynamics in parvalbumin interneuronsGeorgina Kontou0https://orcid.org/0000-0002-0551-1577Pantelis Antonoudiou1Marina Podpolny2Blanka R Szulc3I Lorena Arancibia-Carcamo4https://orcid.org/0000-0002-0624-3850Nathalie F Higgs5Guillermo Lopez-Domenech6https://orcid.org/0000-0002-3114-2082Patricia C Salinas7https://orcid.org/0000-0002-5748-083XEdward O Mann8https://orcid.org/0000-0002-2468-7148Josef T Kittler9https://orcid.org/0000-0002-3437-9456Department of Neuroscience, Physiology and Pharmacology, University College London, London, United KingdomDepartment of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United KingdomDepartment of Cell and Developmental Biology, University College London, London, United KingdomDepartment of Neuroscience, Physiology and Pharmacology, University College London, London, United KingdomDepartment of Neuroscience, Physiology and Pharmacology, University College London, London, United KingdomDepartment of Neuroscience, Physiology and Pharmacology, University College London, London, United KingdomDepartment of Neuroscience, Physiology and Pharmacology, University College London, London, United KingdomDepartment of Cell and Developmental Biology, University College London, London, United KingdomDepartment of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom; Oxford Ion Channel Initiative, University of Oxford, Oxford, United KingdomDepartment of Neuroscience, Physiology and Pharmacology, University College London, London, United KingdomThe spatiotemporal distribution of mitochondria is crucial for precise ATP provision and calcium buffering required to support neuronal signaling. Fast-spiking GABAergic interneurons expressing parvalbumin (PV+) have a high mitochondrial content reflecting their large energy utilization. The importance for correct trafficking and precise mitochondrial positioning remains poorly elucidated in inhibitory neurons. Miro1 is a Ca²+-sensing adaptor protein that links mitochondria to the trafficking apparatus, for their microtubule-dependent transport along axons and dendrites, in order to meet the metabolic and Ca2+-buffering requirements of the cell. Here, we explore the role of Miro1 in PV+ interneurons and how changes in mitochondrial trafficking could alter network activity in the mouse brain. By employing live and fixed imaging, we found that the impairments in Miro1-directed trafficking in PV+ interneurons altered their mitochondrial distribution and axonal arborization, while PV+ interneuron-mediated inhibition remained intact. These changes were accompanied by an increase in the ex vivo hippocampal γ-oscillation (30–80 Hz) frequency and promoted anxiolysis. Our findings show that precise regulation of mitochondrial dynamics in PV+ interneurons is crucial for proper neuronal signaling and network synchronization.https://elifesciences.org/articles/65215mitochondrial traffickingparvalbumin interneuronsgamma oscillations |
| spellingShingle | Georgina Kontou Pantelis Antonoudiou Marina Podpolny Blanka R Szulc I Lorena Arancibia-Carcamo Nathalie F Higgs Guillermo Lopez-Domenech Patricia C Salinas Edward O Mann Josef T Kittler Miro1-dependent mitochondrial dynamics in parvalbumin interneurons eLife mitochondrial trafficking parvalbumin interneurons gamma oscillations |
| title | Miro1-dependent mitochondrial dynamics in parvalbumin interneurons |
| title_full | Miro1-dependent mitochondrial dynamics in parvalbumin interneurons |
| title_fullStr | Miro1-dependent mitochondrial dynamics in parvalbumin interneurons |
| title_full_unstemmed | Miro1-dependent mitochondrial dynamics in parvalbumin interneurons |
| title_short | Miro1-dependent mitochondrial dynamics in parvalbumin interneurons |
| title_sort | miro1 dependent mitochondrial dynamics in parvalbumin interneurons |
| topic | mitochondrial trafficking parvalbumin interneurons gamma oscillations |
| url | https://elifesciences.org/articles/65215 |
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