Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.

Eukaryotic cells respond to a chemoattractant gradient by forming intracellular gradients of signaling molecules that reflect the extracellular chemical gradient-an ability called directional sensing. Quantitative experiments have revealed two characteristic input-output relations of the system: Fir...

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Main Authors: Keita Kamino, Yohei Kondo
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC5085096?pdf=render
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author Keita Kamino
Yohei Kondo
author_facet Keita Kamino
Yohei Kondo
author_sort Keita Kamino
collection DOAJ
description Eukaryotic cells respond to a chemoattractant gradient by forming intracellular gradients of signaling molecules that reflect the extracellular chemical gradient-an ability called directional sensing. Quantitative experiments have revealed two characteristic input-output relations of the system: First, in a static chemoattractant gradient, the shapes of the intracellular gradients of the signaling molecules are determined by the relative steepness, rather than the absolute concentration, of the chemoattractant gradient along the cell body. Second, upon a spatially homogeneous temporal increase in the input stimulus, the intracellular signaling molecules are transiently activated such that the response magnitudes are dependent on fold changes of the stimulus, not on absolute levels. However, the underlying mechanism that endows the system with these response properties remains elusive. Here, by adopting a widely used modeling framework of directional sensing, local excitation and global inhibition (LEGI), we propose a hypothesis that the two rescaling behaviors stem from a single design principle, namely, invariance of the governing equations to a scale transformation of the input level. Analyses of the LEGI-based model reveal that the invariance can be divided into two parts, each of which is responsible for the respective response properties. Our hypothesis leads to an experimentally testable prediction that a system with the invariance detects relative steepness even in dynamic gradient stimuli as well as in static gradients. Furthermore, we show that the relation between the response properties and the scale invariance is general in that it can be implemented by models with different network topologies.
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spelling doaj.art-8f9e8505383c42cdbc5b593ff68cb3ce2022-12-22T00:43:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032016-01-011110e016467410.1371/journal.pone.0164674Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.Keita KaminoYohei KondoEukaryotic cells respond to a chemoattractant gradient by forming intracellular gradients of signaling molecules that reflect the extracellular chemical gradient-an ability called directional sensing. Quantitative experiments have revealed two characteristic input-output relations of the system: First, in a static chemoattractant gradient, the shapes of the intracellular gradients of the signaling molecules are determined by the relative steepness, rather than the absolute concentration, of the chemoattractant gradient along the cell body. Second, upon a spatially homogeneous temporal increase in the input stimulus, the intracellular signaling molecules are transiently activated such that the response magnitudes are dependent on fold changes of the stimulus, not on absolute levels. However, the underlying mechanism that endows the system with these response properties remains elusive. Here, by adopting a widely used modeling framework of directional sensing, local excitation and global inhibition (LEGI), we propose a hypothesis that the two rescaling behaviors stem from a single design principle, namely, invariance of the governing equations to a scale transformation of the input level. Analyses of the LEGI-based model reveal that the invariance can be divided into two parts, each of which is responsible for the respective response properties. Our hypothesis leads to an experimentally testable prediction that a system with the invariance detects relative steepness even in dynamic gradient stimuli as well as in static gradients. Furthermore, we show that the relation between the response properties and the scale invariance is general in that it can be implemented by models with different network topologies.http://europepmc.org/articles/PMC5085096?pdf=render
spellingShingle Keita Kamino
Yohei Kondo
Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.
PLoS ONE
title Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.
title_full Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.
title_fullStr Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.
title_full_unstemmed Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.
title_short Rescaling of Spatio-Temporal Sensing in Eukaryotic Chemotaxis.
title_sort rescaling of spatio temporal sensing in eukaryotic chemotaxis
url http://europepmc.org/articles/PMC5085096?pdf=render
work_keys_str_mv AT keitakamino rescalingofspatiotemporalsensingineukaryoticchemotaxis
AT yoheikondo rescalingofspatiotemporalsensingineukaryoticchemotaxis