Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis

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 and Laurent Groc ()
Additional contact information
Nathan Bénac: Univ. Bordeaux, CNRS, IINS, UMR 5297
G. Ezequiel Saraceno: Univ. Bordeaux, CNRS, IINS, UMR 5297
Corey Butler: Univ. Bordeaux, CNRS, IINS, UMR 5297
Nahoko Kuga: The University of Tokyo
Yuya Nishimura: The University of Tokyo
Taiki Yokoi: Tohoku University
Ping Su: University of Toronto
Takuya Sasaki: The University of Tokyo
Mar Petit-Pedrol: Univ. Bordeaux, CNRS, IINS, UMR 5297
Rémi Galland: Univ. Bordeaux, CNRS, IINS, UMR 5297
Vincent Studer: Univ. Bordeaux, CNRS, IINS, UMR 5297
Fang Liu: University of Toronto
Yuji Ikegaya: The University of Tokyo
Jean-Baptiste Sibarita: Univ. Bordeaux, CNRS, IINS, UMR 5297
Laurent Groc: Univ. Bordeaux, CNRS, IINS, UMR 5297

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-023-44301-z

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