Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain

Tissue mechanics is important for development; however, the spatio-temporal dynamics of in vivo tissue stiffness is still poorly understood. We here developed tiv-AFM, combining time-lapse in vivo atomic force microscopy with upright fluorescence imaging of embryonic tissue, to show that during deve...

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Main Authors: Amelia J Thompson, Eva K Pillai, Ivan B Dimov, Sarah K Foster, Christine E Holt, Kristian Franze
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/39356
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spelling doaj-eaf90d88b5664d0ca2bb49d877b9cc5d2021-05-05T17:18:50ZengeLife Sciences Publications LtdeLife2050-084X2019-01-01810.7554/eLife.39356Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brainAmelia J Thompson0https://orcid.org/0000-0002-3912-3652Eva K Pillai1Ivan B Dimov2Sarah K Foster3Christine E Holt4Kristian Franze5https://orcid.org/0000-0002-8425-7297Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomTissue mechanics is important for development; however, the spatio-temporal dynamics of in vivo tissue stiffness is still poorly understood. We here developed tiv-AFM, combining time-lapse in vivo atomic force microscopy with upright fluorescence imaging of embryonic tissue, to show that during development local tissue stiffness changes significantly within tens of minutes. Within this time frame, a stiffness gradient arose in the developing Xenopus brain, and retinal ganglion cell axons turned to follow this gradient. Changes in local tissue stiffness were largely governed by cell proliferation, as perturbation of mitosis diminished both the stiffness gradient and the caudal turn of axons found in control brains. Hence, we identified a close relationship between the dynamics of tissue mechanics and developmental processes, underpinning the importance of time-resolved stiffness measurements.https://elifesciences.org/articles/39356atomic force microscopymechanicsstiffnessmechanotransductiondurotaxisaxon guidance
collection DOAJ
language English
format Article
sources DOAJ
author Amelia J Thompson
Eva K Pillai
Ivan B Dimov
Sarah K Foster
Christine E Holt
Kristian Franze
spellingShingle Amelia J Thompson
Eva K Pillai
Ivan B Dimov
Sarah K Foster
Christine E Holt
Kristian Franze
Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
eLife
atomic force microscopy
mechanics
stiffness
mechanotransduction
durotaxis
axon guidance
author_facet Amelia J Thompson
Eva K Pillai
Ivan B Dimov
Sarah K Foster
Christine E Holt
Kristian Franze
author_sort Amelia J Thompson
title Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
title_short Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
title_full Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
title_fullStr Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
title_full_unstemmed Rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
title_sort rapid changes in tissue mechanics regulate cell behaviour in the developing embryonic brain
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-01-01
description Tissue mechanics is important for development; however, the spatio-temporal dynamics of in vivo tissue stiffness is still poorly understood. We here developed tiv-AFM, combining time-lapse in vivo atomic force microscopy with upright fluorescence imaging of embryonic tissue, to show that during development local tissue stiffness changes significantly within tens of minutes. Within this time frame, a stiffness gradient arose in the developing Xenopus brain, and retinal ganglion cell axons turned to follow this gradient. Changes in local tissue stiffness were largely governed by cell proliferation, as perturbation of mitosis diminished both the stiffness gradient and the caudal turn of axons found in control brains. Hence, we identified a close relationship between the dynamics of tissue mechanics and developmental processes, underpinning the importance of time-resolved stiffness measurements.
topic atomic force microscopy
mechanics
stiffness
mechanotransduction
durotaxis
axon guidance
url https://elifesciences.org/articles/39356
work_keys_str_mv AT ameliajthompson rapidchangesintissuemechanicsregulatecellbehaviourinthedevelopingembryonicbrain
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AT sarahkfoster rapidchangesintissuemechanicsregulatecellbehaviourinthedevelopingembryonicbrain
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