Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast
Intracellular density impacts the physical nature of the cytoplasm and can globally affect cellular processes, yet density regulation remains poorly understood. Here, using a new quantitative phase imaging method, we determined that dry-mass density in fission yeast is maintained in a narrow distrib...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/64901 |
| _version_ | 1811200767411879936 |
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| author | Pascal D Odermatt Teemu P Miettinen Joël Lemière Joon Ho Kang Emrah Bostan Scott R Manalis Kerwyn Casey Huang Fred Chang |
| author_facet | Pascal D Odermatt Teemu P Miettinen Joël Lemière Joon Ho Kang Emrah Bostan Scott R Manalis Kerwyn Casey Huang Fred Chang |
| author_sort | Pascal D Odermatt |
| collection | DOAJ |
| description | Intracellular density impacts the physical nature of the cytoplasm and can globally affect cellular processes, yet density regulation remains poorly understood. Here, using a new quantitative phase imaging method, we determined that dry-mass density in fission yeast is maintained in a narrow distribution and exhibits homeostatic behavior. However, density varied during the cell cycle, decreasing during G2, increasing in mitosis and cytokinesis, and dropping rapidly at cell birth. These density variations were explained by a constant rate of biomass synthesis, coupled to slowdown of volume growth during cell division and rapid expansion post-cytokinesis. Arrest at specific cell-cycle stages exacerbated density changes. Spatially heterogeneous patterns of density suggested links between density regulation, tip growth, and intracellular osmotic pressure. Our results demonstrate that systematic density variations during the cell cycle are predominantly due to modulation of volume expansion, and reveal functional consequences of density gradients and cell-cycle arrests. |
| first_indexed | 2024-04-12T02:09:12Z |
| format | Article |
| id | doaj.art-805e3887740b465cacc02c0671d8b0d7 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:09:12Z |
| publishDate | 2021-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-805e3887740b465cacc02c0671d8b0d72022-12-22T03:52:26ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.64901Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeastPascal D Odermatt0https://orcid.org/0000-0002-1307-1364Teemu P Miettinen1https://orcid.org/0000-0002-5975-200XJoël Lemière2https://orcid.org/0000-0002-9017-1959Joon Ho Kang3https://orcid.org/0000-0003-4165-7538Emrah Bostan4Scott R Manalis5Kerwyn Casey Huang6https://orcid.org/0000-0002-8043-8138Fred Chang7https://orcid.org/0000-0002-8907-3286Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United States; Department of Bioengineering, Stanford University, Stanford, United StatesKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United States; MRC Laboratory for Molecular Cell Biology, University College, London, United KingdomDepartment of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United StatesKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United States; Department of Physics, Massachusetts Institute of Technology, Cambridge, United States; Brain Science Institute, Korea Institute of Science and Technology, Seoul, Republic of KoreaInformatics Institute, University of Amsterdam, Amsterdamn, NetherlandsKoch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, United States; Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, United States; Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, United StatesDepartment of Bioengineering, Stanford University, Stanford, United States; Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, United States; Chan Zuckerberg Biohub, San Francisco, United StatesDepartment of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United StatesIntracellular density impacts the physical nature of the cytoplasm and can globally affect cellular processes, yet density regulation remains poorly understood. Here, using a new quantitative phase imaging method, we determined that dry-mass density in fission yeast is maintained in a narrow distribution and exhibits homeostatic behavior. However, density varied during the cell cycle, decreasing during G2, increasing in mitosis and cytokinesis, and dropping rapidly at cell birth. These density variations were explained by a constant rate of biomass synthesis, coupled to slowdown of volume growth during cell division and rapid expansion post-cytokinesis. Arrest at specific cell-cycle stages exacerbated density changes. Spatially heterogeneous patterns of density suggested links between density regulation, tip growth, and intracellular osmotic pressure. Our results demonstrate that systematic density variations during the cell cycle are predominantly due to modulation of volume expansion, and reveal functional consequences of density gradients and cell-cycle arrests.https://elifesciences.org/articles/64901quantitative phase imagingSchizosaccharomyces pombedry-mass densitycell-cycle arrestcell polaritypolarized tip growth |
| spellingShingle | Pascal D Odermatt Teemu P Miettinen Joël Lemière Joon Ho Kang Emrah Bostan Scott R Manalis Kerwyn Casey Huang Fred Chang Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast eLife quantitative phase imaging Schizosaccharomyces pombe dry-mass density cell-cycle arrest cell polarity polarized tip growth |
| title | Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast |
| title_full | Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast |
| title_fullStr | Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast |
| title_full_unstemmed | Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast |
| title_short | Variations of intracellular density during the cell cycle arise from tip-growth regulation in fission yeast |
| title_sort | variations of intracellular density during the cell cycle arise from tip growth regulation in fission yeast |
| topic | quantitative phase imaging Schizosaccharomyces pombe dry-mass density cell-cycle arrest cell polarity polarized tip growth |
| url | https://elifesciences.org/articles/64901 |
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