Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.

Embryonic development is guided by a complex and integrated set of stimuli that results in collective system-wide organization that is both time and space regulated. These regulatory interactions result in the emergence of highly functional units, which are correlated to frequency-modulated stimulat...

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Main Authors: Yongtae Kim, Sagar D Joshi, William C Messner, Philip R LeDuc, Lance A Davidson
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3031512?pdf=render
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spelling doaj-6f4b224deb27439e9d7332c41b4b1b782020-11-25T01:18:25ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0161e1462410.1371/journal.pone.0014624Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.Yongtae KimSagar D JoshiWilliam C MessnerPhilip R LeDucLance A DavidsonEmbryonic development is guided by a complex and integrated set of stimuli that results in collective system-wide organization that is both time and space regulated. These regulatory interactions result in the emergence of highly functional units, which are correlated to frequency-modulated stimulation profiles. We have determined the dynamic response of vertebrate embryonic tissues to highly controlled, time-varying localized chemical stimulation using a microfluidic system with feedback control. Our approach has enabled localized spatiotemporal manipulation of the steroid hormone dexamethasone (DEX) in Animal Cap (AC) tissues isolated from gastrulating Xenopus embryos. Using this approach we investigated cell-scale responses to precisely controlled stimulation by tracking the redistribution of a GFP-tagged DEX-reporter constructed from the human glucocorticoid receptor (GR). We exposed defined regions of a single AC explant to different stimulation conditions--continuous stimulation, periodic stimulation, and no stimulation. We observed collective behavior of the GR transport into the nucleus was first-order. Furthermore, the dynamic response was well-modeled by a first-order differential equation with a single time derivative. The model predicted that responses to periodic stimulations closely matched the results of the frequency-based experiments. We find that stimulation with localized bursts versus continuous stimulation can result in highly distinct responses. This finding is critical as controlled space and time exposure to growth factors is a hallmark of complex processes in embryonic development. These complex responses to cellular signaling and transport machinery were similar to emergent behaviors in other complex systems, suggesting that even within a complex embryonic tissue, the overall system can converge toward a predictive first-order response.http://europepmc.org/articles/PMC3031512?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yongtae Kim
Sagar D Joshi
William C Messner
Philip R LeDuc
Lance A Davidson
spellingShingle Yongtae Kim
Sagar D Joshi
William C Messner
Philip R LeDuc
Lance A Davidson
Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.
PLoS ONE
author_facet Yongtae Kim
Sagar D Joshi
William C Messner
Philip R LeDuc
Lance A Davidson
author_sort Yongtae Kim
title Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.
title_short Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.
title_full Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.
title_fullStr Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.
title_full_unstemmed Detection of dynamic spatiotemporal response to periodic chemical stimulation in a Xenopus embryonic tissue.
title_sort detection of dynamic spatiotemporal response to periodic chemical stimulation in a xenopus embryonic tissue.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2011-01-01
description Embryonic development is guided by a complex and integrated set of stimuli that results in collective system-wide organization that is both time and space regulated. These regulatory interactions result in the emergence of highly functional units, which are correlated to frequency-modulated stimulation profiles. We have determined the dynamic response of vertebrate embryonic tissues to highly controlled, time-varying localized chemical stimulation using a microfluidic system with feedback control. Our approach has enabled localized spatiotemporal manipulation of the steroid hormone dexamethasone (DEX) in Animal Cap (AC) tissues isolated from gastrulating Xenopus embryos. Using this approach we investigated cell-scale responses to precisely controlled stimulation by tracking the redistribution of a GFP-tagged DEX-reporter constructed from the human glucocorticoid receptor (GR). We exposed defined regions of a single AC explant to different stimulation conditions--continuous stimulation, periodic stimulation, and no stimulation. We observed collective behavior of the GR transport into the nucleus was first-order. Furthermore, the dynamic response was well-modeled by a first-order differential equation with a single time derivative. The model predicted that responses to periodic stimulations closely matched the results of the frequency-based experiments. We find that stimulation with localized bursts versus continuous stimulation can result in highly distinct responses. This finding is critical as controlled space and time exposure to growth factors is a hallmark of complex processes in embryonic development. These complex responses to cellular signaling and transport machinery were similar to emergent behaviors in other complex systems, suggesting that even within a complex embryonic tissue, the overall system can converge toward a predictive first-order response.
url http://europepmc.org/articles/PMC3031512?pdf=render
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