Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe

The size and position of mitotic spindles is determined by the lengths of their constituent microtubules. Regulation of microtubule length requires feedback to set the balance between growth and shrinkage. Whereas negative feedback mechanisms for microtubule length control, based on depolymerizing k...

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Main Authors: Anneke Hibbel, Aliona Bogdanova, Mohammed Mahamdeh, Anita Jannasch, Marko Storch, Erik Schäffer, Dimitris Liakopoulos, Jonathon Howard
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/10542
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author Anneke Hibbel
Aliona Bogdanova
Mohammed Mahamdeh
Anita Jannasch
Marko Storch
Erik Schäffer
Dimitris Liakopoulos
Jonathon Howard
author_facet Anneke Hibbel
Aliona Bogdanova
Mohammed Mahamdeh
Anita Jannasch
Marko Storch
Erik Schäffer
Dimitris Liakopoulos
Jonathon Howard
author_sort Anneke Hibbel
collection DOAJ
description The size and position of mitotic spindles is determined by the lengths of their constituent microtubules. Regulation of microtubule length requires feedback to set the balance between growth and shrinkage. Whereas negative feedback mechanisms for microtubule length control, based on depolymerizing kinesins and severing proteins, have been studied extensively, positive feedback mechanisms are not known. Here, we report that the budding yeast kinesin Kip2 is a microtubule polymerase and catastrophe inhibitor in vitro that uses its processive motor activity as part of a feedback loop to further promote microtubule growth. Positive feedback arises because longer microtubules bind more motors, which walk to the ends where they reinforce growth and inhibit catastrophe. We propose that positive feedback, common in biochemical pathways to switch between signaling states, can also be used in a mechanical signaling pathway to switch between structural states, in this case between short and long polymers.
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spelling doaj.art-ba4c6ae3190241f79a1e98a283b088f42022-12-22T03:52:38ZengeLife Sciences Publications LtdeLife2050-084X2015-11-01410.7554/eLife.10542Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastropheAnneke Hibbel0Aliona Bogdanova1Mohammed Mahamdeh2Anita Jannasch3Marko Storch4Erik Schäffer5Dimitris Liakopoulos6Jonathon Howard7Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Institute of Biochemistry, ETH Zurich, Zurich, SwitzerlandMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyDepartment of Molecular Biophysics & Biochemistry, Yale University, New Haven, United StatesMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Zentrum für Molekularbiologie der Pflanzen, Eberhard-Karls-Universität, Tübingen, GermanyDepartment of Life Sciences, Imperial College London, London, United KingdomZentrum für Molekularbiologie der Pflanzen, Eberhard-Karls-Universität, Tübingen, GermanyCRBM-CRNS, Montpellier, FranceDepartment of Molecular Biophysics & Biochemistry, Yale University, New Haven, United StatesThe size and position of mitotic spindles is determined by the lengths of their constituent microtubules. Regulation of microtubule length requires feedback to set the balance between growth and shrinkage. Whereas negative feedback mechanisms for microtubule length control, based on depolymerizing kinesins and severing proteins, have been studied extensively, positive feedback mechanisms are not known. Here, we report that the budding yeast kinesin Kip2 is a microtubule polymerase and catastrophe inhibitor in vitro that uses its processive motor activity as part of a feedback loop to further promote microtubule growth. Positive feedback arises because longer microtubules bind more motors, which walk to the ends where they reinforce growth and inhibit catastrophe. We propose that positive feedback, common in biochemical pathways to switch between signaling states, can also be used in a mechanical signaling pathway to switch between structural states, in this case between short and long polymers.https://elifesciences.org/articles/10542microtubule dynamicsmotor proteinlength regulationpositive feedback
spellingShingle Anneke Hibbel
Aliona Bogdanova
Mohammed Mahamdeh
Anita Jannasch
Marko Storch
Erik Schäffer
Dimitris Liakopoulos
Jonathon Howard
Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe
eLife
microtubule dynamics
motor protein
length regulation
positive feedback
title Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe
title_full Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe
title_fullStr Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe
title_full_unstemmed Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe
title_short Kinesin Kip2 enhances microtubule growth in vitro through length-dependent feedback on polymerization and catastrophe
title_sort kinesin kip2 enhances microtubule growth in vitro through length dependent feedback on polymerization and catastrophe
topic microtubule dynamics
motor protein
length regulation
positive feedback
url https://elifesciences.org/articles/10542
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