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Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis

Cell mass and composition change with cell cycle progression. Our previous work characterized buoyant mass dynamics in mitosis (Miettinen et al., 2019), but how dry mass and cell composition change in mitosis has remained unclear. To better understand mitotic cell growth and compositional changes, w...

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Detalles Bibliográficos
Autores principales: Miettinen, Teemu P, Ly, Kevin S, Lam, Alice, Manalis, Scott R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9090323/
https://www.ncbi.nlm.nih.gov/pubmed/35535854
http://dx.doi.org/10.7554/eLife.76664
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author Miettinen, Teemu P
Ly, Kevin S
Lam, Alice
Manalis, Scott R
author_facet Miettinen, Teemu P
Ly, Kevin S
Lam, Alice
Manalis, Scott R
author_sort Miettinen, Teemu P
collection PubMed
description Cell mass and composition change with cell cycle progression. Our previous work characterized buoyant mass dynamics in mitosis (Miettinen et al., 2019), but how dry mass and cell composition change in mitosis has remained unclear. To better understand mitotic cell growth and compositional changes, we develop a single-cell approach for monitoring dry mass and the density of that dry mass every ~75 s with 1.3% and 0.3% measurement precision, respectively. We find that suspension grown mammalian cells lose dry mass and increase dry mass density following mitotic entry. These changes display large, non-genetic cell-to-cell variability, and the changes are reversed at metaphase-anaphase transition, after which dry mass continues accumulating. The change in dry mass density causes buoyant and dry mass to differ specifically in early mitosis, thus reconciling existing literature on mitotic cell growth. Mechanistically, cells in early mitosis increase lysosomal exocytosis, and inhibition of lysosomal exocytosis decreases the dry mass loss and dry mass density increase in mitosis. Overall, our work provides a new approach for monitoring single-cell dry mass and dry mass density, and reveals that mitosis is coupled to extensive exocytosis-mediated secretion of cellular contents.
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spelling pubmed-90903232022-05-11 Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis Miettinen, Teemu P Ly, Kevin S Lam, Alice Manalis, Scott R eLife Cell Biology Cell mass and composition change with cell cycle progression. Our previous work characterized buoyant mass dynamics in mitosis (Miettinen et al., 2019), but how dry mass and cell composition change in mitosis has remained unclear. To better understand mitotic cell growth and compositional changes, we develop a single-cell approach for monitoring dry mass and the density of that dry mass every ~75 s with 1.3% and 0.3% measurement precision, respectively. We find that suspension grown mammalian cells lose dry mass and increase dry mass density following mitotic entry. These changes display large, non-genetic cell-to-cell variability, and the changes are reversed at metaphase-anaphase transition, after which dry mass continues accumulating. The change in dry mass density causes buoyant and dry mass to differ specifically in early mitosis, thus reconciling existing literature on mitotic cell growth. Mechanistically, cells in early mitosis increase lysosomal exocytosis, and inhibition of lysosomal exocytosis decreases the dry mass loss and dry mass density increase in mitosis. Overall, our work provides a new approach for monitoring single-cell dry mass and dry mass density, and reveals that mitosis is coupled to extensive exocytosis-mediated secretion of cellular contents. eLife Sciences Publications, Ltd 2022-05-10 /pmc/articles/PMC9090323/ /pubmed/35535854 http://dx.doi.org/10.7554/eLife.76664 Text en © 2022, Miettinen et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Miettinen, Teemu P
Ly, Kevin S
Lam, Alice
Manalis, Scott R
Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
title Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
title_full Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
title_fullStr Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
title_full_unstemmed Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
title_short Single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
title_sort single-cell monitoring of dry mass and dry mass density reveals exocytosis of cellular dry contents in mitosis
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9090323/
https://www.ncbi.nlm.nih.gov/pubmed/35535854
http://dx.doi.org/10.7554/eLife.76664
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