Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis
Abstract Direct interactions between receptors at the neuronal surface have long been proposed to tune signaling cascades and neuronal communication in health and disease. Yet, the lack of direct investigation methods to measure, in live neurons, the interaction between different membrane receptors...
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| Format: | Article |
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Nature Portfolio
2024-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-44301-z |
| _version_ | 1797363041249001472 |
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| author | Nathan Bénac G. Ezequiel Saraceno Corey Butler Nahoko Kuga Yuya Nishimura Taiki Yokoi Ping Su Takuya Sasaki Mar Petit-Pedrol Rémi Galland Vincent Studer Fang Liu Yuji Ikegaya Jean-Baptiste Sibarita Laurent Groc |
| author_facet | Nathan Bénac G. Ezequiel Saraceno Corey Butler Nahoko Kuga Yuya Nishimura Taiki Yokoi Ping Su Takuya Sasaki Mar Petit-Pedrol Rémi Galland Vincent Studer Fang Liu Yuji Ikegaya Jean-Baptiste Sibarita Laurent Groc |
| author_sort | Nathan Bénac |
| collection | DOAJ |
| description | Abstract Direct interactions between receptors at the neuronal surface have long been proposed to tune signaling cascades and neuronal communication in health and disease. Yet, the lack of direct investigation methods to measure, in live neurons, the interaction between different membrane receptors at the single molecule level has raised unanswered questions on the biophysical properties and biological roles of such receptor interactome. Using a multidimensional spectral single molecule-localization microscopy (MS-SMLM) approach, we monitored the interaction between two membrane receptors, i.e. glutamatergic NMDA (NMDAR) and G protein-coupled dopamine D1 (D1R) receptors. The transient interaction was randomly observed along the dendritic tree of hippocampal neurons. It was higher early in development, promoting the formation of NMDAR-D1R complexes in an mGluR5- and CK1-dependent manner, favoring NMDAR clusters and synaptogenesis in a dopamine receptor signaling-independent manner. Preventing the interaction in the neonate, and not adult, brain alters in vivo spontaneous neuronal network activity pattern in male mice. Thus, a weak and transient interaction between NMDAR and D1R plays a structural and functional role in the developing brain. |
| first_indexed | 2024-03-08T16:16:05Z |
| format | Article |
| id | doaj.art-2d86b146b2a6411f89c908ab69a9fb73 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T16:16:05Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-2d86b146b2a6411f89c908ab69a9fb732024-01-07T12:34:22ZengNature PortfolioNature Communications2041-17232024-01-0115111910.1038/s41467-023-44301-zNon-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesisNathan Bénac0G. Ezequiel Saraceno1Corey Butler2Nahoko Kuga3Yuya Nishimura4Taiki Yokoi5Ping Su6Takuya Sasaki7Mar Petit-Pedrol8Rémi Galland9Vincent Studer10Fang Liu11Yuji Ikegaya12Jean-Baptiste Sibarita13Laurent Groc14Univ. Bordeaux, CNRS, IINS, UMR 5297Univ. Bordeaux, CNRS, IINS, UMR 5297Univ. Bordeaux, CNRS, IINS, UMR 5297Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of TokyoLaboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of TokyoDepartment of Pharmacology, Graduate School of Pharmaceutical Sciences, Tohoku UniversityCampbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, University of TorontoLaboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of TokyoUniv. Bordeaux, CNRS, IINS, UMR 5297Univ. Bordeaux, CNRS, IINS, UMR 5297Univ. Bordeaux, CNRS, IINS, UMR 5297Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, University of TorontoLaboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of TokyoUniv. Bordeaux, CNRS, IINS, UMR 5297Univ. Bordeaux, CNRS, IINS, UMR 5297Abstract Direct interactions between receptors at the neuronal surface have long been proposed to tune signaling cascades and neuronal communication in health and disease. Yet, the lack of direct investigation methods to measure, in live neurons, the interaction between different membrane receptors at the single molecule level has raised unanswered questions on the biophysical properties and biological roles of such receptor interactome. Using a multidimensional spectral single molecule-localization microscopy (MS-SMLM) approach, we monitored the interaction between two membrane receptors, i.e. glutamatergic NMDA (NMDAR) and G protein-coupled dopamine D1 (D1R) receptors. The transient interaction was randomly observed along the dendritic tree of hippocampal neurons. It was higher early in development, promoting the formation of NMDAR-D1R complexes in an mGluR5- and CK1-dependent manner, favoring NMDAR clusters and synaptogenesis in a dopamine receptor signaling-independent manner. Preventing the interaction in the neonate, and not adult, brain alters in vivo spontaneous neuronal network activity pattern in male mice. Thus, a weak and transient interaction between NMDAR and D1R plays a structural and functional role in the developing brain.https://doi.org/10.1038/s41467-023-44301-z |
| spellingShingle | Nathan Bénac G. Ezequiel Saraceno Corey Butler Nahoko Kuga Yuya Nishimura Taiki Yokoi Ping Su Takuya Sasaki Mar Petit-Pedrol Rémi Galland Vincent Studer Fang Liu Yuji Ikegaya Jean-Baptiste Sibarita Laurent Groc Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis Nature Communications |
| title | Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis |
| title_full | Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis |
| title_fullStr | Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis |
| title_full_unstemmed | Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis |
| title_short | Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis |
| title_sort | non canonical interplay between glutamatergic nmda and dopamine receptors shapes synaptogenesis |
| url | https://doi.org/10.1038/s41467-023-44301-z |
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