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Remodeling of the postsynaptic plasma membrane during neural development

Neuronal synapses are the fundamental units of neural signal transduction and must maintain exquisite signal fidelity while also accommodating the plasticity that underlies learning and development. To achieve these goals, the molecular composition and spatial organization of synaptic terminals must...

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Autores principales: Tulodziecka, Karolina, Diaz-Rohrer, Barbara B., Farley, Madeline M., Chan, Robin B., Di Paolo, Gilbert, Levental, Kandice R., Waxham, M. Neal, Levental, Ilya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5221582/
https://www.ncbi.nlm.nih.gov/pubmed/27535429
http://dx.doi.org/10.1091/mbc.E16-06-0420
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author Tulodziecka, Karolina
Diaz-Rohrer, Barbara B.
Farley, Madeline M.
Chan, Robin B.
Di Paolo, Gilbert
Levental, Kandice R.
Waxham, M. Neal
Levental, Ilya
author_facet Tulodziecka, Karolina
Diaz-Rohrer, Barbara B.
Farley, Madeline M.
Chan, Robin B.
Di Paolo, Gilbert
Levental, Kandice R.
Waxham, M. Neal
Levental, Ilya
author_sort Tulodziecka, Karolina
collection PubMed
description Neuronal synapses are the fundamental units of neural signal transduction and must maintain exquisite signal fidelity while also accommodating the plasticity that underlies learning and development. To achieve these goals, the molecular composition and spatial organization of synaptic terminals must be tightly regulated; however, little is known about the regulation of lipid composition and organization in synaptic membranes. Here we quantify the comprehensive lipidome of rat synaptic membranes during postnatal development and observe dramatic developmental lipidomic remodeling during the first 60 postnatal days, including progressive accumulation of cholesterol, plasmalogens, and sphingolipids. Further analysis of membranes associated with isolated postsynaptic densities (PSDs) suggests the PSD-associated postsynaptic plasma membrane (PSD-PM) as one specific location of synaptic remodeling. We analyze the biophysical consequences of developmental remodeling in reconstituted synaptic membranes and observe remarkably stable microdomains, with the stability of domains increasing with developmental age. We rationalize the developmental accumulation of microdomain-forming lipids in synapses by proposing a mechanism by which palmitoylation of the immobilized scaffold protein PSD-95 nucleates domains at the postsynaptic plasma membrane. These results reveal developmental changes in lipid composition and palmitoylation that facilitate the formation of postsynaptic membrane microdomains, which may serve key roles in the function of the neuronal synapse.
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spelling pubmed-52215822017-01-22 Remodeling of the postsynaptic plasma membrane during neural development Tulodziecka, Karolina Diaz-Rohrer, Barbara B. Farley, Madeline M. Chan, Robin B. Di Paolo, Gilbert Levental, Kandice R. Waxham, M. Neal Levental, Ilya Mol Biol Cell Articles Neuronal synapses are the fundamental units of neural signal transduction and must maintain exquisite signal fidelity while also accommodating the plasticity that underlies learning and development. To achieve these goals, the molecular composition and spatial organization of synaptic terminals must be tightly regulated; however, little is known about the regulation of lipid composition and organization in synaptic membranes. Here we quantify the comprehensive lipidome of rat synaptic membranes during postnatal development and observe dramatic developmental lipidomic remodeling during the first 60 postnatal days, including progressive accumulation of cholesterol, plasmalogens, and sphingolipids. Further analysis of membranes associated with isolated postsynaptic densities (PSDs) suggests the PSD-associated postsynaptic plasma membrane (PSD-PM) as one specific location of synaptic remodeling. We analyze the biophysical consequences of developmental remodeling in reconstituted synaptic membranes and observe remarkably stable microdomains, with the stability of domains increasing with developmental age. We rationalize the developmental accumulation of microdomain-forming lipids in synapses by proposing a mechanism by which palmitoylation of the immobilized scaffold protein PSD-95 nucleates domains at the postsynaptic plasma membrane. These results reveal developmental changes in lipid composition and palmitoylation that facilitate the formation of postsynaptic membrane microdomains, which may serve key roles in the function of the neuronal synapse. The American Society for Cell Biology 2016-11-07 /pmc/articles/PMC5221582/ /pubmed/27535429 http://dx.doi.org/10.1091/mbc.E16-06-0420 Text en © 2016 Tulodziecka et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Tulodziecka, Karolina
Diaz-Rohrer, Barbara B.
Farley, Madeline M.
Chan, Robin B.
Di Paolo, Gilbert
Levental, Kandice R.
Waxham, M. Neal
Levental, Ilya
Remodeling of the postsynaptic plasma membrane during neural development
title Remodeling of the postsynaptic plasma membrane during neural development
title_full Remodeling of the postsynaptic plasma membrane during neural development
title_fullStr Remodeling of the postsynaptic plasma membrane during neural development
title_full_unstemmed Remodeling of the postsynaptic plasma membrane during neural development
title_short Remodeling of the postsynaptic plasma membrane during neural development
title_sort remodeling of the postsynaptic plasma membrane during neural development
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5221582/
https://www.ncbi.nlm.nih.gov/pubmed/27535429
http://dx.doi.org/10.1091/mbc.E16-06-0420
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