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The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines

The 30-amino acid peptide Y-P30 corresponds to the N-terminus of the primate-specific, sweat gland-derived dermcidin prepropeptide. Previous work has revealed that Y-P30 enhances the interaction of pleiotrophin and syndecans-2/3, and thus represents a natural ligand to study this signaling pathway....

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Autores principales: Neumann, Janine R., Dash-Wagh, Suvarna, Jack, Alexander, Räk, Andrea, Jüngling, Kay, Hamad, Mohammad I. K., Pape, Hans-Christian, Kreutz, Michael R., Puskarjov, Martin, Wahle, Petra
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6373909/
https://www.ncbi.nlm.nih.gov/pubmed/30759095
http://dx.doi.org/10.1371/journal.pone.0211151
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author Neumann, Janine R.
Dash-Wagh, Suvarna
Jack, Alexander
Räk, Andrea
Jüngling, Kay
Hamad, Mohammad I. K.
Pape, Hans-Christian
Kreutz, Michael R.
Puskarjov, Martin
Wahle, Petra
author_facet Neumann, Janine R.
Dash-Wagh, Suvarna
Jack, Alexander
Räk, Andrea
Jüngling, Kay
Hamad, Mohammad I. K.
Pape, Hans-Christian
Kreutz, Michael R.
Puskarjov, Martin
Wahle, Petra
author_sort Neumann, Janine R.
collection PubMed
description The 30-amino acid peptide Y-P30 corresponds to the N-terminus of the primate-specific, sweat gland-derived dermcidin prepropeptide. Previous work has revealed that Y-P30 enhances the interaction of pleiotrophin and syndecans-2/3, and thus represents a natural ligand to study this signaling pathway. In immature neurons, Y-P30 activates the c-Src and p42/44 ERK kinase pathway, increases the amount of F-actin in axonal growth cones, and promotes neuronal survival, cell migration and axonal elongation. The action of Y-P30 on axonal growth requires syndecan-3 and heparan sulfate side chains. Whether Y-P30 has the potential to influence dendrites and dendritic protrusions has not been explored. The latter is suggested by the observations that syndecan-2 expression increases during postnatal development, that syndecan-2 becomes enriched in dendritic spines, and that overexpression of syndecan-2 in immature neurons results in a premature morphological maturation of dendritic spines. Here, analysing rat cortical pyramidal and non-pyramidal neurons in organotypic cultures, we show that Y-P30 does not alter the development of the dendritic arborization patterns. However, Y-P30 treatment decreases the density of apical, but not basal dendritic protrusions at the expense of the filopodia. Analysis of spine morphology revealed an unchanged mushroom/stubby-to-thin spine ratio and a shortening of the longest decile of dendritic protrusions. Whole-cell recordings from cortical principal neurons in dissociated cultures grown in the presence of Y-P30 demonstrated a decrease in the frequency of glutamatergic mEPSCs. Despite these differences in protrusion morphology and synaptic transmission, the latter likely attributable to presynaptic effects, calcium event rate and amplitude recorded in pyramidal neurons in organotypic cultures were not altered by Y-P30 treatment. Together, our data suggest that Y-P30 has the capacity to decelerate spinogenesis and to promote morphological, but not synaptic, maturation of dendritic protrusions.
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spelling pubmed-63739092019-03-01 The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines Neumann, Janine R. Dash-Wagh, Suvarna Jack, Alexander Räk, Andrea Jüngling, Kay Hamad, Mohammad I. K. Pape, Hans-Christian Kreutz, Michael R. Puskarjov, Martin Wahle, Petra PLoS One Research Article The 30-amino acid peptide Y-P30 corresponds to the N-terminus of the primate-specific, sweat gland-derived dermcidin prepropeptide. Previous work has revealed that Y-P30 enhances the interaction of pleiotrophin and syndecans-2/3, and thus represents a natural ligand to study this signaling pathway. In immature neurons, Y-P30 activates the c-Src and p42/44 ERK kinase pathway, increases the amount of F-actin in axonal growth cones, and promotes neuronal survival, cell migration and axonal elongation. The action of Y-P30 on axonal growth requires syndecan-3 and heparan sulfate side chains. Whether Y-P30 has the potential to influence dendrites and dendritic protrusions has not been explored. The latter is suggested by the observations that syndecan-2 expression increases during postnatal development, that syndecan-2 becomes enriched in dendritic spines, and that overexpression of syndecan-2 in immature neurons results in a premature morphological maturation of dendritic spines. Here, analysing rat cortical pyramidal and non-pyramidal neurons in organotypic cultures, we show that Y-P30 does not alter the development of the dendritic arborization patterns. However, Y-P30 treatment decreases the density of apical, but not basal dendritic protrusions at the expense of the filopodia. Analysis of spine morphology revealed an unchanged mushroom/stubby-to-thin spine ratio and a shortening of the longest decile of dendritic protrusions. Whole-cell recordings from cortical principal neurons in dissociated cultures grown in the presence of Y-P30 demonstrated a decrease in the frequency of glutamatergic mEPSCs. Despite these differences in protrusion morphology and synaptic transmission, the latter likely attributable to presynaptic effects, calcium event rate and amplitude recorded in pyramidal neurons in organotypic cultures were not altered by Y-P30 treatment. Together, our data suggest that Y-P30 has the capacity to decelerate spinogenesis and to promote morphological, but not synaptic, maturation of dendritic protrusions. Public Library of Science 2019-02-13 /pmc/articles/PMC6373909/ /pubmed/30759095 http://dx.doi.org/10.1371/journal.pone.0211151 Text en © 2019 Neumann et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Neumann, Janine R.
Dash-Wagh, Suvarna
Jack, Alexander
Räk, Andrea
Jüngling, Kay
Hamad, Mohammad I. K.
Pape, Hans-Christian
Kreutz, Michael R.
Puskarjov, Martin
Wahle, Petra
The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines
title The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines
title_full The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines
title_fullStr The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines
title_full_unstemmed The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines
title_short The primate-specific peptide Y-P30 regulates morphological maturation of neocortical dendritic spines
title_sort primate-specific peptide y-p30 regulates morphological maturation of neocortical dendritic spines
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6373909/
https://www.ncbi.nlm.nih.gov/pubmed/30759095
http://dx.doi.org/10.1371/journal.pone.0211151
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