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Physical properties of the cytoplasm modulate the rates of microtubule polymerization and depolymerization

Authors :
Arthur T. Molines
Joël Lemière
Morgan Gazzola
Ida Emilie Steinmark
Claire H. Edrington
Chieh-Ting Hsu
Paula Real-Calderon
Klaus Suhling
Gohta Goshima
Liam J. Holt
Manuel Thery
Gary J. Brouhard
Fred Chang
Departments of Cell & Tissue Biology and Medicine
University of California [San Francisco] (UC San Francisco)
University of California (UC)-University of California (UC)
Marine Biological Laboratory, Woods Hole, Massachusetts, USA
CytoMorphoLab
Physiologie cellulaire et végétale (LPCV)
Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG)
Direction de Recherche Fondamentale (CEA) (DRF (CEA))
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA))
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG)
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)
Department of Physics, King's College London
Department of Biology [McGill University]
McGill University = Université McGill [Montréal, Canada]
Department of Physics [McGill University]
Sugashima Marine Biological Laboratory
Nagoya University
New York University Langone Health, Institute for Systems Genetics
Université de Paris, INSERM, CEA, Institut de Recherche Saint Louis, U 976
Grants NIH GM115185, NIH GM056836, NIH GM146438, NIH GM132447, NIH CA240765
American Cancer Society RSG-19-073-01-TBE
Pershing Square Sohn Cancer Award
Chan Zuckerberg Initiative
JSPS KAKENHI 17H06471 and 18KK0202
UK’s Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/R004803/1
European Project: 771599,ICEBERG
Martin-Laffon, Jacqueline
Exploration below the tip of the microtubule - ICEBERG - 771599 - INCOMING
Source :
Developmental Cell, Developmental Cell, 2022, 57 (4), pp.466-479.e6. ⟨10.1016/j.devcel.2022.02.001⟩, Dev Cell, Molines, A T, Lemière, J, Gazzola, M, Steinmark, I E, Edrington, C H, Hsu, C T, Real-Calderon, P, Suhling, K, Goshima, G, Holt, L J, Thery, M, Brouhard, G J & Chang, F 2022, ' Physical properties of the cytoplasm modulate the rates of microtubule polymerization and depolymerization ', Developmental Cell, vol. 57, no. 4, pp. 466-479.e6 . https://doi.org/10.1016/j.devcel.2022.02.001
Publication Year :
2021

Abstract

International audience; The cytoplasm is a crowded, visco-elastic environment whose physical properties change according to physiological or developmental states. How the physical properties of the cytoplasm impact cellular functions in vivo remains poorly understood. Here, we probe the effects of cytoplasmic concentration on microtubules by applying osmotic shifts to fission yeast, moss, and mammalian cells. We show that the rates of both microtubule polymerization and depolymerization scale linearly and inversely with cytoplasmic concentration; an increase in cytoplasmic concentration decreases the rates of microtubule polymerization and depolymerization proportionally, whereas a decrease in cytoplasmic concentration leads to the opposite. Numerous lines of evidence indicate that these effects are due to changes in cytoplasmic viscosity rather than cellular stress responses or macromolecular crowding per se. We reconstituted these effects on microtubules in vitro by tuning viscosity. Our findings indicate that, even in normal conditions, the viscosity of the cytoplasm modulates the reactions that underlie microtubule dynamic behaviors.

Details

ISSN :
18781551 and 15345807
Volume :
57
Issue :
4
Database :
OpenAIRE
Journal :
Developmental cell
Accession number :
edsair.doi.dedup.....5da6feb7240a994a01061e2d98ab8fa2