Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels
Abstract Cell elongation along the division axis, or mitotic elongation, mediates proper segregation of chromosomes and other intracellular materials, and is required for completion of cell division. In three‐dimensionally confining extracellular matrices, such as dense collagen gels, dividing cells...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Wiley
2021-02-01
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| Series: | Advanced Science |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/advs.202000403 |
| _version_ | 1819296087495671808 |
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| author | Sungmin Nam Yung‐Hao Lin Taeyoon Kim Ovijit Chaudhuri |
| author_facet | Sungmin Nam Yung‐Hao Lin Taeyoon Kim Ovijit Chaudhuri |
| author_sort | Sungmin Nam |
| collection | DOAJ |
| description | Abstract Cell elongation along the division axis, or mitotic elongation, mediates proper segregation of chromosomes and other intracellular materials, and is required for completion of cell division. In three‐dimensionally confining extracellular matrices, such as dense collagen gels, dividing cells must generate space to allow mitotic elongation to occur. In principle, cells can generate space for mitotic elongation during cell spreading, prior to mitosis, or via extracellular force generation or matrix degradation during mitosis. However, the processes by which cells drive mitotic elongation in collagen‐rich extracellular matrices remains unclear. Here, it is shown that single cancer cells generate substantial pushing forces on the surrounding collagen extracellular matrix to drive cell division in confining collagen gels and allow mitotic elongation to proceed. Neither cell spreading, prior to mitosis, nor matrix degradation, during spreading or mitotic elongation, are found to be required for mitotic elongation. Mechanistically, laser ablation studies, pharmacological inhibition studies, and computational modeling establish that pushing forces generated during mitosis in collagen gels arise from a combination of interpolar spindle elongation and cytokinetic ring contraction. These results reveal a fundamental mechanism mediating cell division in confining extracellular matrices, providing insight into how tumor cells are able to proliferate in dense collagen‐rich tissues. |
| first_indexed | 2024-12-24T04:52:32Z |
| format | Article |
| id | doaj.art-680fd3c88b39481e90ce50e2fa2ac8bd |
| institution | Directory Open Access Journal |
| issn | 2198-3844 |
| language | English |
| last_indexed | 2024-12-24T04:52:32Z |
| publishDate | 2021-02-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj.art-680fd3c88b39481e90ce50e2fa2ac8bd2022-12-21T17:14:29ZengWileyAdvanced Science2198-38442021-02-0184n/an/a10.1002/advs.202000403Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen GelsSungmin Nam0Yung‐Hao Lin1Taeyoon Kim2Ovijit Chaudhuri3Department of Mechanical Engineering Stanford University 418 Panama Mall Stanford CA 94305 USADepartment of Chemical Engineering Stanford University 418 Panama Mall Stanford CA 94305 USAWeldon School of Biomedical Engineering Purdue University 206 S Martin Jischke Drive West Lafayette IN 47907 USADepartment of Mechanical Engineering Stanford University 418 Panama Mall Stanford CA 94305 USAAbstract Cell elongation along the division axis, or mitotic elongation, mediates proper segregation of chromosomes and other intracellular materials, and is required for completion of cell division. In three‐dimensionally confining extracellular matrices, such as dense collagen gels, dividing cells must generate space to allow mitotic elongation to occur. In principle, cells can generate space for mitotic elongation during cell spreading, prior to mitosis, or via extracellular force generation or matrix degradation during mitosis. However, the processes by which cells drive mitotic elongation in collagen‐rich extracellular matrices remains unclear. Here, it is shown that single cancer cells generate substantial pushing forces on the surrounding collagen extracellular matrix to drive cell division in confining collagen gels and allow mitotic elongation to proceed. Neither cell spreading, prior to mitosis, nor matrix degradation, during spreading or mitotic elongation, are found to be required for mitotic elongation. Mechanistically, laser ablation studies, pharmacological inhibition studies, and computational modeling establish that pushing forces generated during mitosis in collagen gels arise from a combination of interpolar spindle elongation and cytokinetic ring contraction. These results reveal a fundamental mechanism mediating cell division in confining extracellular matrices, providing insight into how tumor cells are able to proliferate in dense collagen‐rich tissues.https://doi.org/10.1002/advs.202000403biophysicscell divisioncollagen gelscytokinesisextracellular matrixmechanotransduction |
| spellingShingle | Sungmin Nam Yung‐Hao Lin Taeyoon Kim Ovijit Chaudhuri Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels Advanced Science biophysics cell division collagen gels cytokinesis extracellular matrix mechanotransduction |
| title | Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels |
| title_full | Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels |
| title_fullStr | Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels |
| title_full_unstemmed | Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels |
| title_short | Cellular Pushing Forces during Mitosis Drive Mitotic Elongation in Collagen Gels |
| title_sort | cellular pushing forces during mitosis drive mitotic elongation in collagen gels |
| topic | biophysics cell division collagen gels cytokinesis extracellular matrix mechanotransduction |
| url | https://doi.org/10.1002/advs.202000403 |
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