A stable microtubule bundle formed through an orchestrated multistep process controls quiescence exit

Damien Laporte; Aurelie Massoni-Laporte; Charles Lefranc; Jim Dompierre; David Mauboules; Emmanuel T. Nsamba; Anne Royou; Lihi Gal; Maya Schuldiner; Mohan L. Gupta; Isabelle Sagot

doi:10.7554/eLife.89958

A stable microtubule bundle formed through an orchestrated multistep process controls quiescence exit

Damien Laporte, Aurelie Massoni-Laporte, Charles Lefranc, Jim Dompierre, David Mauboules, Emmanuel T. Nsamba, Anne Royou, Lihi Gal, Maya Schuldiner, Mohan L. Gupta, Isabelle Sagot

Department of Molecular Genetics

Research output: Contribution to journal › Article › peer-review

Abstract

Cells fine-tune microtubule assembly in both space and time to give rise to distinct edifices with specific cellular functions. In proliferating cells, microtubules are highly dynamics, and proliferation cessation often leads to their stabilization. One of the most stable microtubule structures identified to date is the nuclear bundle assembled in quiescent yeast. In this article, we characterize the original multistep process driving the assembly of this structure. This Aurora B-dependent mechanism follows a precise temporality that relies on the sequential actions of kinesin-14, kinesin-5, and involves both microtubule-kinetochore and kinetochore-kinetochore interactions. Upon quiescence exit, the microtubule bundle is disassembled via a cooperative process involving kinesin-8 and its full disassembly is required prior to cells re-entry into proliferation. Overall, our study provides the first description, at the molecular scale, of the entire life cycle of a stable microtubule structure in vivo and sheds light on its physiological function.

Original language	English
Article number	RP89958
Number of pages	25
Journal	eLife
Volume	12
DOIs	https://doi.org/10.7554/eLife.89958
Publication status	Published - 25 Mar 2024

Bibliographical note

We thank the Bordeaux Imaging Center for the help in super-resolution imaging. We express our gratitude to E O’Shea, A Marston, S Jaspersen, J-P Javerzat, Wei-Lih Lee, C Boone, and B Goode for sharing reagents and M Rojo for providing us with the mCherry-specific antibodies. We thank Michaël Gué (Zeiss) for helping us a with the lattice SIM Elyra 7 microscope. We would like to thank J-P Javerzat for helpful and constructive discussions about our work. DL, AML, JD, and IS were supported by a grant from the ANR-21-CE13-0023-01, la Ligue Contre le Cancer Régionale – Dordogne grant #193366 and the CNRS. MG and EN were supported by a National Science Foundation grant number MCB-1846262. AR was supported by the Conseil Régional de Nouvelle Aquitaine (#20111301010) and the CNRS.

Publisher Copyright:
© 2023, Laporte et al.

All Science Journal Classification (ASJC) codes

General Neuroscience
General Biochemistry,Genetics and Molecular Biology
General Immunology and Microbiology

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10.7554/eLife.89958Licence: CC BY

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title = "A stable microtubule bundle formed through an orchestrated multistep process controls quiescence exit",

abstract = "Cells fine-tune microtubule assembly in both space and time to give rise to distinct edifices with specific cellular functions. In proliferating cells, microtubules are highly dynamics, and proliferation cessation often leads to their stabilization. One of the most stable microtubule structures identified to date is the nuclear bundle assembled in quiescent yeast. In this article, we characterize the original multistep process driving the assembly of this structure. This Aurora B-dependent mechanism follows a precise temporality that relies on the sequential actions of kinesin-14, kinesin-5, and involves both microtubule-kinetochore and kinetochore-kinetochore interactions. Upon quiescence exit, the microtubule bundle is disassembled via a cooperative process involving kinesin-8 and its full disassembly is required prior to cells re-entry into proliferation. Overall, our study provides the first description, at the molecular scale, of the entire life cycle of a stable microtubule structure in vivo and sheds light on its physiological function.",

author = "Damien Laporte and Aurelie Massoni-Laporte and Charles Lefranc and Jim Dompierre and David Mauboules and Nsamba, {Emmanuel T.} and Anne Royou and Lihi Gal and Maya Schuldiner and Gupta, {Mohan L.} and Isabelle Sagot",

note = "We thank the Bordeaux Imaging Center for the help in super-resolution imaging. We express our gratitude to E O{\textquoteright}Shea, A Marston, S Jaspersen, J-P Javerzat, Wei-Lih Lee, C Boone, and B Goode for sharing reagents and M Rojo for providing us with the mCherry-specific antibodies. We thank Micha{\"e}l Gu{\'e} (Zeiss) for helping us a with the lattice SIM Elyra 7 microscope. We would like to thank J-P Javerzat for helpful and constructive discussions about our work. DL, AML, JD, and IS were supported by a grant from the ANR-21-CE13-0023-01, la Ligue Contre le Cancer R{\'e}gionale – Dordogne grant #193366 and the CNRS. MG and EN were supported by a National Science Foundation grant number MCB-1846262. AR was supported by the Conseil R{\'e}gional de Nouvelle Aquitaine (#20111301010) and the CNRS. Publisher Copyright: {\textcopyright} 2023, Laporte et al.",

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AU - Mauboules, David

AU - Nsamba, Emmanuel T.

AU - Royou, Anne

AU - Gal, Lihi

AU - Schuldiner, Maya

AU - Gupta, Mohan L.

AU - Sagot, Isabelle

N1 - We thank the Bordeaux Imaging Center for the help in super-resolution imaging. We express our gratitude to E O’Shea, A Marston, S Jaspersen, J-P Javerzat, Wei-Lih Lee, C Boone, and B Goode for sharing reagents and M Rojo for providing us with the mCherry-specific antibodies. We thank Michaël Gué (Zeiss) for helping us a with the lattice SIM Elyra 7 microscope. We would like to thank J-P Javerzat for helpful and constructive discussions about our work. DL, AML, JD, and IS were supported by a grant from the ANR-21-CE13-0023-01, la Ligue Contre le Cancer Régionale – Dordogne grant #193366 and the CNRS. MG and EN were supported by a National Science Foundation grant number MCB-1846262. AR was supported by the Conseil Régional de Nouvelle Aquitaine (#20111301010) and the CNRS. Publisher Copyright: © 2023, Laporte et al.

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A stable microtubule bundle formed through an orchestrated multistep process controls quiescence exit

Abstract

Bibliographical note

All Science Journal Classification (ASJC) codes

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