Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina

An important question in early neural development is the origin of stochastic nuclear movement between apical and basal surfaces of neuroepithelia during interkinetic nuclear migration. Tracking of nuclear subpopulations has shown evidence of diffusion - mean squared displacements growing linearly i...

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Main Authors: Afnan Azizi, Anne Herrmann, Yinan Wan, Salvador JRP Buse, Philipp J Keller, Raymond E Goldstein, William A Harris
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/58635
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spelling doaj-cb6f95198caa4b61838500dac621e7ec2021-05-05T21:34:58ZengeLife Sciences Publications LtdeLife2050-084X2020-10-01910.7554/eLife.58635Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retinaAfnan Azizi0https://orcid.org/0000-0002-3288-9612Anne Herrmann1https://orcid.org/0000-0003-1745-7499Yinan Wan2Salvador JRP Buse3Philipp J Keller4https://orcid.org/0000-0003-2896-4920Raymond E Goldstein5https://orcid.org/0000-0003-2645-0598William A Harris6https://orcid.org/0000-0002-9995-8096Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomDepartment of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United KingdomHoward Hughes Medical Institute, Janelia Research Campus, Ashburn, United StatesDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomHoward Hughes Medical Institute, Janelia Research Campus, Ashburn, United StatesDepartment of Applied Mathematics and Theoretical Physics, Centre for Mathematical Sciences, University of Cambridge, Cambridge, United KingdomDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United KingdomAn important question in early neural development is the origin of stochastic nuclear movement between apical and basal surfaces of neuroepithelia during interkinetic nuclear migration. Tracking of nuclear subpopulations has shown evidence of diffusion - mean squared displacements growing linearly in time - and suggested crowding from cell division at the apical surface drives basalward motion. Yet, this hypothesis has not yet been tested, and the forces involved not quantified. We employ long-term, rapid light-sheet and two-photon imaging of early zebrafish retinogenesis to track entire populations of nuclei within the tissue. The time-varying concentration profiles show clear evidence of crowding as nuclei reach close-packing and are quantitatively described by a nonlinear diffusion model. Considerations of nuclear motion constrained inside the enveloping cell membrane show that concentration-dependent stochastic forces inside cells, compatible in magnitude to those found in cytoskeletal transport, can explain the observed magnitude of the diffusion constant.https://elifesciences.org/articles/58635nuclear crowdingdiffusioninterkinetic nuclear migration
collection DOAJ
language English
format Article
sources DOAJ
author Afnan Azizi
Anne Herrmann
Yinan Wan
Salvador JRP Buse
Philipp J Keller
Raymond E Goldstein
William A Harris
spellingShingle Afnan Azizi
Anne Herrmann
Yinan Wan
Salvador JRP Buse
Philipp J Keller
Raymond E Goldstein
William A Harris
Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
eLife
nuclear crowding
diffusion
interkinetic nuclear migration
author_facet Afnan Azizi
Anne Herrmann
Yinan Wan
Salvador JRP Buse
Philipp J Keller
Raymond E Goldstein
William A Harris
author_sort Afnan Azizi
title Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
title_short Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
title_full Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
title_fullStr Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
title_full_unstemmed Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
title_sort nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-10-01
description An important question in early neural development is the origin of stochastic nuclear movement between apical and basal surfaces of neuroepithelia during interkinetic nuclear migration. Tracking of nuclear subpopulations has shown evidence of diffusion - mean squared displacements growing linearly in time - and suggested crowding from cell division at the apical surface drives basalward motion. Yet, this hypothesis has not yet been tested, and the forces involved not quantified. We employ long-term, rapid light-sheet and two-photon imaging of early zebrafish retinogenesis to track entire populations of nuclei within the tissue. The time-varying concentration profiles show clear evidence of crowding as nuclei reach close-packing and are quantitatively described by a nonlinear diffusion model. Considerations of nuclear motion constrained inside the enveloping cell membrane show that concentration-dependent stochastic forces inside cells, compatible in magnitude to those found in cytoskeletal transport, can explain the observed magnitude of the diffusion constant.
topic nuclear crowding
diffusion
interkinetic nuclear migration
url https://elifesciences.org/articles/58635
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