1. Physical properties of the cytoplasm modulate the rates of microtubule polymerization and depolymerization
- Author
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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, and Exploration below the tip of the microtubule - ICEBERG - 771599 - INCOMING
- Subjects
MESH: Cell Nucleus ,Cytoplasm ,fission yeast Schizosaccharomyces pombe ,[SDV.BC]Life Sciences [q-bio]/Cellular Biology ,Spindle Apparatus ,Microtubules ,General Biochemistry, Genetics and Molecular Biology ,Article ,Polymerization ,microtubules ,MESH: Interphase ,Cytosol ,Schizosaccharomyces ,MESH: Spindle Apparatus ,Molecular Biology ,[SDV.BC] Life Sciences [q-bio]/Cellular Biology ,Interphase ,mitosis ,Cell Nucleus ,density ,MESH: Microtubules ,MESH: Cytoplasm ,diffusion ,MESH: Schizosaccharomyces pombe Proteins ,Cell Biology ,cytoskeleton dynamics ,crowding ,MESH: Polymerization ,MESH: Schizosaccharomyces ,viscosity ,cytoplasm ,rheology ,Schizosaccharomyces pombe Proteins ,Developmental Biology - 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.
- Published
- 2021