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Oxytocin signaling is necessary for synaptic maturation of adult-born neurons

Neural circuit plasticity and sensory response dynamics depend on forming new synaptic connections. Despite recent advances toward understanding the consequences of circuit plasticity, the mechanisms driving circuit plasticity are unknown. Adult-born neurons within the olfactory bulb have proven to...

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Autores principales: Pekarek, Brandon T., Kochukov, Mikhail, Lozzi, Brittney, Wu, Timothy, Hunt, Patrick J., Tepe, Burak, Hanson Moss, Elizabeth, Tantry, Evelyne K., Swanson, Jessica L., Dooling, Sean W., Patel, Mayuri, Belfort, Benjamin D.W., Romero, Juan M., Bao, Suyang, Hill, Matthew C., Arenkiel, Benjamin R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851403/
https://www.ncbi.nlm.nih.gov/pubmed/36617877
http://dx.doi.org/10.1101/gad.349930.122
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author Pekarek, Brandon T.
Kochukov, Mikhail
Lozzi, Brittney
Wu, Timothy
Hunt, Patrick J.
Tepe, Burak
Hanson Moss, Elizabeth
Tantry, Evelyne K.
Swanson, Jessica L.
Dooling, Sean W.
Patel, Mayuri
Belfort, Benjamin D.W.
Romero, Juan M.
Bao, Suyang
Hill, Matthew C.
Arenkiel, Benjamin R.
author_facet Pekarek, Brandon T.
Kochukov, Mikhail
Lozzi, Brittney
Wu, Timothy
Hunt, Patrick J.
Tepe, Burak
Hanson Moss, Elizabeth
Tantry, Evelyne K.
Swanson, Jessica L.
Dooling, Sean W.
Patel, Mayuri
Belfort, Benjamin D.W.
Romero, Juan M.
Bao, Suyang
Hill, Matthew C.
Arenkiel, Benjamin R.
author_sort Pekarek, Brandon T.
collection PubMed
description Neural circuit plasticity and sensory response dynamics depend on forming new synaptic connections. Despite recent advances toward understanding the consequences of circuit plasticity, the mechanisms driving circuit plasticity are unknown. Adult-born neurons within the olfactory bulb have proven to be a powerful model for studying circuit plasticity, providing a broad and accessible avenue into neuron development, migration, and circuit integration. We and others have shown that efficient adult-born neuron circuit integration hinges on presynaptic activity in the form of diverse signaling peptides. Here, we demonstrate a novel oxytocin-dependent mechanism of adult-born neuron synaptic maturation and circuit integration. We reveal spatial and temporal enrichment of oxytocin receptor expression within adult-born neurons in the murine olfactory bulb, with oxytocin receptor expression peaking during activity-dependent integration. Using viral labeling, confocal microscopy, and cell type-specific RNA-seq, we demonstrate that oxytocin receptor signaling promotes synaptic maturation of newly integrating adult-born neurons by regulating their morphological development and expression of mature synaptic AMPARs and other structural proteins.
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spelling pubmed-98514032023-01-20 Oxytocin signaling is necessary for synaptic maturation of adult-born neurons Pekarek, Brandon T. Kochukov, Mikhail Lozzi, Brittney Wu, Timothy Hunt, Patrick J. Tepe, Burak Hanson Moss, Elizabeth Tantry, Evelyne K. Swanson, Jessica L. Dooling, Sean W. Patel, Mayuri Belfort, Benjamin D.W. Romero, Juan M. Bao, Suyang Hill, Matthew C. Arenkiel, Benjamin R. Genes Dev Research Paper Neural circuit plasticity and sensory response dynamics depend on forming new synaptic connections. Despite recent advances toward understanding the consequences of circuit plasticity, the mechanisms driving circuit plasticity are unknown. Adult-born neurons within the olfactory bulb have proven to be a powerful model for studying circuit plasticity, providing a broad and accessible avenue into neuron development, migration, and circuit integration. We and others have shown that efficient adult-born neuron circuit integration hinges on presynaptic activity in the form of diverse signaling peptides. Here, we demonstrate a novel oxytocin-dependent mechanism of adult-born neuron synaptic maturation and circuit integration. We reveal spatial and temporal enrichment of oxytocin receptor expression within adult-born neurons in the murine olfactory bulb, with oxytocin receptor expression peaking during activity-dependent integration. Using viral labeling, confocal microscopy, and cell type-specific RNA-seq, we demonstrate that oxytocin receptor signaling promotes synaptic maturation of newly integrating adult-born neurons by regulating their morphological development and expression of mature synaptic AMPARs and other structural proteins. Cold Spring Harbor Laboratory Press 2022 /pmc/articles/PMC9851403/ /pubmed/36617877 http://dx.doi.org/10.1101/gad.349930.122 Text en © 2022 Pekarek et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article, published in Genes & Development, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Research Paper
Pekarek, Brandon T.
Kochukov, Mikhail
Lozzi, Brittney
Wu, Timothy
Hunt, Patrick J.
Tepe, Burak
Hanson Moss, Elizabeth
Tantry, Evelyne K.
Swanson, Jessica L.
Dooling, Sean W.
Patel, Mayuri
Belfort, Benjamin D.W.
Romero, Juan M.
Bao, Suyang
Hill, Matthew C.
Arenkiel, Benjamin R.
Oxytocin signaling is necessary for synaptic maturation of adult-born neurons
title Oxytocin signaling is necessary for synaptic maturation of adult-born neurons
title_full Oxytocin signaling is necessary for synaptic maturation of adult-born neurons
title_fullStr Oxytocin signaling is necessary for synaptic maturation of adult-born neurons
title_full_unstemmed Oxytocin signaling is necessary for synaptic maturation of adult-born neurons
title_short Oxytocin signaling is necessary for synaptic maturation of adult-born neurons
title_sort oxytocin signaling is necessary for synaptic maturation of adult-born neurons
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851403/
https://www.ncbi.nlm.nih.gov/pubmed/36617877
http://dx.doi.org/10.1101/gad.349930.122
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