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

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Date
2022-02-28
Authors
Molines, Arthur T.
Lemière, Joë
Gazzola, Morgan
Steinmark, Ida Emilie
Edrington, Claire H.
Hsu, Chieh-Ting
Real-Calderon, Paula
Suhling, Klaus
Goshima, Gohta
Holt, Liam J.
Thery, Manuel
Brouhard, Gary J.
Chang, Fred
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10.1016/j.devcel.2022.02.001
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Keywords
Cytoskeleton dynamics
Microtubules
Cytoplasm
Crowding
Viscosity
Diffusion
Density
Rheology
Mitosis
Fission yeast Schizosaccharomyces pombe
Abstract
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.
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© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in 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. Physical properties of the cytoplasm modulate the rates of microtubule polymerization and depolymerization. Developmental Cell, 57(4), (2022): 466-479.e6, https://doi.org/10.1016/j.devcel.2022.02.001.
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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, 57(4), 466-479.e6.
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