Flexible search for single-axon morphology during neuronal spontaneous polarization.

Polarization, a disruption of symmetry in cellular morphology, occurs spontaneously, even in symmetrical extracellular conditions. This process is regulated by intracellular chemical reactions and the active transport of proteins and it is accompanied by cellular morphological changes. To elucidate...

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Main Authors: Honda Naoki, Shinichi Nakamuta, Kozo Kaibuchi, Shin Ishii
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-04-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21559492/pdf/?tool=EBI
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author Honda Naoki
Shinichi Nakamuta
Kozo Kaibuchi
Shin Ishii
author_facet Honda Naoki
Shinichi Nakamuta
Kozo Kaibuchi
Shin Ishii
author_sort Honda Naoki
collection DOAJ
description Polarization, a disruption of symmetry in cellular morphology, occurs spontaneously, even in symmetrical extracellular conditions. This process is regulated by intracellular chemical reactions and the active transport of proteins and it is accompanied by cellular morphological changes. To elucidate the general principles underlying polarization, we focused on developing neurons. Neuronal polarity is stably established; a neuron initially has several neurites of similar length, but only one elongates and is selected to develop into an axon. Polarization is flexibly controlled; when multiple neurites are selected, the selection is eventually reduced to yield a single axon. What is the system by which morphological information is decoded differently based on the presence of a single or multiple axons? How are stability and flexibility achieved? To answer these questions, we constructed a biophysical model with the active transport of proteins that regulate neurite growth. Our mathematical analysis and computer simulation revealed that, as neurites elongate, transported factors accumulate in the growth cone but are degraded during retrograde diffusion to the soma. Such a system effectively works as local activation-global inhibition mechanism, resulting in both stability and flexibility. Our model shows good accordance with a number of experimental observations.
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spelling doaj.art-aa9fd00e82384b4ab1d82776825095482022-12-21T19:09:49ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-04-0164e1903410.1371/journal.pone.0019034Flexible search for single-axon morphology during neuronal spontaneous polarization.Honda NaokiShinichi NakamutaKozo KaibuchiShin IshiiPolarization, a disruption of symmetry in cellular morphology, occurs spontaneously, even in symmetrical extracellular conditions. This process is regulated by intracellular chemical reactions and the active transport of proteins and it is accompanied by cellular morphological changes. To elucidate the general principles underlying polarization, we focused on developing neurons. Neuronal polarity is stably established; a neuron initially has several neurites of similar length, but only one elongates and is selected to develop into an axon. Polarization is flexibly controlled; when multiple neurites are selected, the selection is eventually reduced to yield a single axon. What is the system by which morphological information is decoded differently based on the presence of a single or multiple axons? How are stability and flexibility achieved? To answer these questions, we constructed a biophysical model with the active transport of proteins that regulate neurite growth. Our mathematical analysis and computer simulation revealed that, as neurites elongate, transported factors accumulate in the growth cone but are degraded during retrograde diffusion to the soma. Such a system effectively works as local activation-global inhibition mechanism, resulting in both stability and flexibility. Our model shows good accordance with a number of experimental observations.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21559492/pdf/?tool=EBI
spellingShingle Honda Naoki
Shinichi Nakamuta
Kozo Kaibuchi
Shin Ishii
Flexible search for single-axon morphology during neuronal spontaneous polarization.
PLoS ONE
title Flexible search for single-axon morphology during neuronal spontaneous polarization.
title_full Flexible search for single-axon morphology during neuronal spontaneous polarization.
title_fullStr Flexible search for single-axon morphology during neuronal spontaneous polarization.
title_full_unstemmed Flexible search for single-axon morphology during neuronal spontaneous polarization.
title_short Flexible search for single-axon morphology during neuronal spontaneous polarization.
title_sort flexible search for single axon morphology during neuronal spontaneous polarization
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21559492/pdf/?tool=EBI
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AT shinichinakamuta flexiblesearchforsingleaxonmorphologyduringneuronalspontaneouspolarization
AT kozokaibuchi flexiblesearchforsingleaxonmorphologyduringneuronalspontaneouspolarization
AT shinishii flexiblesearchforsingleaxonmorphologyduringneuronalspontaneouspolarization