Control of nuclear size by osmotic forces in Schizosaccharomyces pombe
The size of the nucleus scales robustly with cell size so that the nuclear-to-cell volume ratio (N/C ratio) is maintained during cell growth in many cell types. The mechanism responsible for this scaling remains mysterious. Previous studies have established that the N/C ratio is not determined by DN...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-07-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/76075 |
| _version_ | 1811205090907783168 |
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| author | Joël Lemière Paula Real-Calderon Liam J Holt Thomas G Fai Fred Chang |
| author_facet | Joël Lemière Paula Real-Calderon Liam J Holt Thomas G Fai Fred Chang |
| author_sort | Joël Lemière |
| collection | DOAJ |
| description | The size of the nucleus scales robustly with cell size so that the nuclear-to-cell volume ratio (N/C ratio) is maintained during cell growth in many cell types. The mechanism responsible for this scaling remains mysterious. Previous studies have established that the N/C ratio is not determined by DNA amount but is instead influenced by factors such as nuclear envelope mechanics and nuclear transport. Here, we developed a quantitative model for nuclear size control based upon colloid osmotic pressure and tested key predictions in the fission yeast Schizosaccharomyces pombe. This model posits that the N/C ratio is determined by the numbers of macromolecules in the nucleoplasm and cytoplasm. Osmotic shift experiments showed that the fission yeast nucleus behaves as an ideal osmometer whose volume is primarily dictated by osmotic forces. Inhibition of nuclear export caused accumulation of macromolecules in the nucleoplasm, leading to nuclear swelling. We further demonstrated that the N/C ratio is maintained by a homeostasis mechanism based upon synthesis of macromolecules during growth. These studies demonstrate the functions of colloid osmotic pressure in intracellular organization and size control. |
| first_indexed | 2024-04-12T03:25:48Z |
| format | Article |
| id | doaj.art-217be082c8ed49b0b6a15583892db6fd |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T03:25:48Z |
| publishDate | 2022-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-217be082c8ed49b0b6a15583892db6fd2022-12-22T03:49:43ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.76075Control of nuclear size by osmotic forces in Schizosaccharomyces pombeJoël Lemière0https://orcid.org/0000-0002-9017-1959Paula Real-Calderon1https://orcid.org/0000-0002-4158-9582Liam J Holt2Thomas G Fai3https://orcid.org/0000-0003-0383-5217Fred Chang4https://orcid.org/0000-0002-8907-3286Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United StatesDepartment of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United States; Centro Andaluz de Biología del Desarrollo, Sevilla, SpainInstitute for Systems Genetics, New York University Langone Health, New York, United StatesDepartment of Mathematics and Volen Center for Complex Systems, Brandeis University, Waltham, United StatesDepartment of Cell and Tissue Biology, University of California, San Francisco, San Francisco, United StatesThe size of the nucleus scales robustly with cell size so that the nuclear-to-cell volume ratio (N/C ratio) is maintained during cell growth in many cell types. The mechanism responsible for this scaling remains mysterious. Previous studies have established that the N/C ratio is not determined by DNA amount but is instead influenced by factors such as nuclear envelope mechanics and nuclear transport. Here, we developed a quantitative model for nuclear size control based upon colloid osmotic pressure and tested key predictions in the fission yeast Schizosaccharomyces pombe. This model posits that the N/C ratio is determined by the numbers of macromolecules in the nucleoplasm and cytoplasm. Osmotic shift experiments showed that the fission yeast nucleus behaves as an ideal osmometer whose volume is primarily dictated by osmotic forces. Inhibition of nuclear export caused accumulation of macromolecules in the nucleoplasm, leading to nuclear swelling. We further demonstrated that the N/C ratio is maintained by a homeostasis mechanism based upon synthesis of macromolecules during growth. These studies demonstrate the functions of colloid osmotic pressure in intracellular organization and size control.https://elifesciences.org/articles/76075nuclear mechanobiologyosmotic pressuremacromolecular crowdingsize homeostasisorganelle size scalingcell size |
| spellingShingle | Joël Lemière Paula Real-Calderon Liam J Holt Thomas G Fai Fred Chang Control of nuclear size by osmotic forces in Schizosaccharomyces pombe eLife nuclear mechanobiology osmotic pressure macromolecular crowding size homeostasis organelle size scaling cell size |
| title | Control of nuclear size by osmotic forces in Schizosaccharomyces pombe |
| title_full | Control of nuclear size by osmotic forces in Schizosaccharomyces pombe |
| title_fullStr | Control of nuclear size by osmotic forces in Schizosaccharomyces pombe |
| title_full_unstemmed | Control of nuclear size by osmotic forces in Schizosaccharomyces pombe |
| title_short | Control of nuclear size by osmotic forces in Schizosaccharomyces pombe |
| title_sort | control of nuclear size by osmotic forces in schizosaccharomyces pombe |
| topic | nuclear mechanobiology osmotic pressure macromolecular crowding size homeostasis organelle size scaling cell size |
| url | https://elifesciences.org/articles/76075 |
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