Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles

Regulation of size and growth is a fundamental problem in biology. A prominent example is the formation of the mitotic spindle, where protein concentration gradients around chromosomes are thought to regulate spindle growth by controlling microtubule nucleation. Previous evidence suggests that micro...

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Main Authors: Franziska Decker, David Oriola, Benjamin Dalton, Jan Brugués
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/31149
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author Franziska Decker
David Oriola
Benjamin Dalton
Jan Brugués
author_facet Franziska Decker
David Oriola
Benjamin Dalton
Jan Brugués
author_sort Franziska Decker
collection DOAJ
description Regulation of size and growth is a fundamental problem in biology. A prominent example is the formation of the mitotic spindle, where protein concentration gradients around chromosomes are thought to regulate spindle growth by controlling microtubule nucleation. Previous evidence suggests that microtubules nucleate throughout the spindle structure. However, the mechanisms underlying microtubule nucleation and its spatial regulation are still unclear. Here, we developed an assay based on laser ablation to directly probe microtubule nucleation events in Xenopus laevis egg extracts. Combining this method with theory and quantitative microscopy, we show that the size of a spindle is controlled by autocatalytic growth of microtubules, driven by microtubule-stimulated microtubule nucleation. The autocatalytic activity of this nucleation system is spatially regulated by the limiting amounts of active microtubule nucleators, which decrease with distance from the chromosomes. This mechanism provides an upper limit to spindle size even when resources are not limiting.
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spelling doaj.art-1fba0337e1ed4fe095730923d7a90b482022-12-22T04:32:26ZengeLife Sciences Publications LtdeLife2050-084X2018-01-01710.7554/eLife.31149Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindlesFranziska Decker0https://orcid.org/0000-0002-3241-6575David Oriola1https://orcid.org/0000-0002-8356-7832Benjamin Dalton2Jan Brugués3https://orcid.org/0000-0002-6731-4130Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Center for Systems Biology Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Center for Systems Biology Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Center for Systems Biology Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Center for Systems Biology Dresden, Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, Dresden, GermanyRegulation of size and growth is a fundamental problem in biology. A prominent example is the formation of the mitotic spindle, where protein concentration gradients around chromosomes are thought to regulate spindle growth by controlling microtubule nucleation. Previous evidence suggests that microtubules nucleate throughout the spindle structure. However, the mechanisms underlying microtubule nucleation and its spatial regulation are still unclear. Here, we developed an assay based on laser ablation to directly probe microtubule nucleation events in Xenopus laevis egg extracts. Combining this method with theory and quantitative microscopy, we show that the size of a spindle is controlled by autocatalytic growth of microtubules, driven by microtubule-stimulated microtubule nucleation. The autocatalytic activity of this nucleation system is spatially regulated by the limiting amounts of active microtubule nucleators, which decrease with distance from the chromosomes. This mechanism provides an upper limit to spindle size even when resources are not limiting.https://elifesciences.org/articles/31149cytoskeletonmicrotubule nucleationspindlelaser ablationorganelle sizeautocatalytic process
spellingShingle Franziska Decker
David Oriola
Benjamin Dalton
Jan Brugués
Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles
eLife
cytoskeleton
microtubule nucleation
spindle
laser ablation
organelle size
autocatalytic process
title Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles
title_full Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles
title_fullStr Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles
title_full_unstemmed Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles
title_short Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles
title_sort autocatalytic microtubule nucleation determines the size and mass of xenopus laevis egg extract spindles
topic cytoskeleton
microtubule nucleation
spindle
laser ablation
organelle size
autocatalytic process
url https://elifesciences.org/articles/31149
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AT benjamindalton autocatalyticmicrotubulenucleationdeterminesthesizeandmassofxenopuslaeviseggextractspindles
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