Self-generated chemoattractant gradients: attractant depletion extends the range and robustness of chemotaxis

Tweedy, L., Knecht, D. A., Mackay, G. N. and Insall, R. H. (2016) Self-generated chemoattractant gradients: attractant depletion extends the range and robustness of chemotaxis. PLoS Biology, 14(3), e1002404. (doi:10.1371/journal.pbio.1002404) (PMID:26981861) (PMCID:PMC4794234)

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Abstract

Chemotaxis is fundamentally important, but the sources of gradients in vivo are rarely well understood. Here, we analyse self-generated chemotaxis, in which cells respond to gradients they have made themselves by breaking down globally available attractants, using both computational simulations and experiments. We show that chemoattractant degradation creates steep local gradients. This leads to surprising results, in particular the existence of a leading population of cells that moves highly directionally, while cells behind this group are undirected. This leading cell population is denser than those following, especially at high attractant concentrations. The local gradient moves with the leading cells as they interact with their surroundings, giving directed movement that is unusually robust and can operate over long distances. Even when gradients are applied from external sources, attractant breakdown greatly changes cells' responses and increases robustness. We also consider alternative mechanisms for directional decision-making and show that they do not predict the features of population migration we observe experimentally. Our findings provide useful diagnostics to allow identification of self-generated gradients and suggest that self-generated chemotaxis is unexpectedly universal in biology and medicine.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Insall, Professor Robert and Mackay, Dr Gillian and Knecht, Prof David
Authors: Tweedy, L., Knecht, D. A., Mackay, G. N., and Insall, R. H.
College/School:College of Medical Veterinary and Life Sciences > Institute of Cancer Sciences
Journal Name:PLoS Biology
Publisher:Public Library of Science
ISSN:1544-9173
ISSN (Online):1545-7885
Copyright Holders:Copyright © 2016 Tweedy et al.
First Published:First published in PLoS Biology 14(3):e1002404
Publisher Policy:Reproduced under a creative commons license
Related URLs:
Data DOI:10.5525/gla.researchdata.252

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
303051Molecular recognition, subunit interaction & structure function analysis of Recombinant human and plant PDCsJohn Gordon LindsayBiotechnology and Biological Sciences Research Council (BBSRC)17/B15672RI MOLECULAR CELL & SYSTEMS BIOLOGY