Testing the limits of gradient sensing.

The ability to detect a chemical gradient is fundamental to many cellular processes. In multicellular organisms gradient sensing plays an important role in many physiological processes such as wound healing and development. Unicellular organisms use gradient sensing to move (chemotaxis) or grow (che...

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Main Authors: Vinal Lakhani, Timothy C Elston
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-02-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC5347372?pdf=render
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author Vinal Lakhani
Timothy C Elston
author_facet Vinal Lakhani
Timothy C Elston
author_sort Vinal Lakhani
collection DOAJ
description The ability to detect a chemical gradient is fundamental to many cellular processes. In multicellular organisms gradient sensing plays an important role in many physiological processes such as wound healing and development. Unicellular organisms use gradient sensing to move (chemotaxis) or grow (chemotropism) towards a favorable environment. Some cells are capable of detecting extremely shallow gradients, even in the presence of significant molecular-level noise. For example, yeast have been reported to detect pheromone gradients as shallow as 0.1 nM/μm. Noise reduction mechanisms, such as time-averaging and the internalization of pheromone molecules, have been proposed to explain how yeast cells filter fluctuations and detect shallow gradients. Here, we use a Particle-Based Reaction-Diffusion model of ligand-receptor dynamics to test the effectiveness of these mechanisms and to determine the limits of gradient sensing. In particular, we develop novel simulation methods for establishing chemical gradients that not only allow us to study gradient sensing under steady-state conditions, but also take into account transient effects as the gradient forms. Based on reported measurements of reaction rates, our results indicate neither time-averaging nor receptor endocytosis significantly improves the cell's accuracy in detecting gradients over time scales associated with the initiation of polarized growth. Additionally, our results demonstrate the physical barrier of the cell membrane sharpens chemical gradients across the cell. While our studies are motivated by the mating response of yeast, we believe our results and simulation methods will find applications in many different contexts.
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spelling doaj.art-10af1d7f9056467280727675ff82ec192022-12-22T01:31:54ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582017-02-01132e100538610.1371/journal.pcbi.1005386Testing the limits of gradient sensing.Vinal LakhaniTimothy C ElstonThe ability to detect a chemical gradient is fundamental to many cellular processes. In multicellular organisms gradient sensing plays an important role in many physiological processes such as wound healing and development. Unicellular organisms use gradient sensing to move (chemotaxis) or grow (chemotropism) towards a favorable environment. Some cells are capable of detecting extremely shallow gradients, even in the presence of significant molecular-level noise. For example, yeast have been reported to detect pheromone gradients as shallow as 0.1 nM/μm. Noise reduction mechanisms, such as time-averaging and the internalization of pheromone molecules, have been proposed to explain how yeast cells filter fluctuations and detect shallow gradients. Here, we use a Particle-Based Reaction-Diffusion model of ligand-receptor dynamics to test the effectiveness of these mechanisms and to determine the limits of gradient sensing. In particular, we develop novel simulation methods for establishing chemical gradients that not only allow us to study gradient sensing under steady-state conditions, but also take into account transient effects as the gradient forms. Based on reported measurements of reaction rates, our results indicate neither time-averaging nor receptor endocytosis significantly improves the cell's accuracy in detecting gradients over time scales associated with the initiation of polarized growth. Additionally, our results demonstrate the physical barrier of the cell membrane sharpens chemical gradients across the cell. While our studies are motivated by the mating response of yeast, we believe our results and simulation methods will find applications in many different contexts.http://europepmc.org/articles/PMC5347372?pdf=render
spellingShingle Vinal Lakhani
Timothy C Elston
Testing the limits of gradient sensing.
PLoS Computational Biology
title Testing the limits of gradient sensing.
title_full Testing the limits of gradient sensing.
title_fullStr Testing the limits of gradient sensing.
title_full_unstemmed Testing the limits of gradient sensing.
title_short Testing the limits of gradient sensing.
title_sort testing the limits of gradient sensing
url http://europepmc.org/articles/PMC5347372?pdf=render
work_keys_str_mv AT vinallakhani testingthelimitsofgradientsensing
AT timothycelston testingthelimitsofgradientsensing