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The nature of cell division forces in epithelial monolayers
Epithelial cells undergo striking morphological changes during division to ensure proper segregation of genetic and cytoplasmic materials. These morphological changes occur despite dividing cells being mechanically restricted by neighboring cells, indicating the need for extracellular force generati...
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| Published in: | The Journal of cell biology 2021-08, Vol.220 (8), p.1 |
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| Main Authors: | , , , , , , , , , |
| Format: | Article |
| Language: | English |
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| cites | cdi_FETCH-LOGICAL-c415t-bfb45eae7c98d7e32bde73722e14b69a468b5897576d744ed94dbb9242d38d4e0 |
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| container_issue | 8 |
| container_start_page | 1 |
| container_title | The Journal of cell biology |
| container_volume | 220 |
| creator | Gupta, Vivek K Nam, Sungmin Yim, Donghyun Camuglia, Jaclyn Martin, Judy Lisette Sanders, Erin Nicole O'Brien, Lucy Erin Martin, Adam C Kim, Taeyoon Chaudhuri, Ovijit |
| description | Epithelial cells undergo striking morphological changes during division to ensure proper segregation of genetic and cytoplasmic materials. These morphological changes occur despite dividing cells being mechanically restricted by neighboring cells, indicating the need for extracellular force generation. Beyond driving cell division itself, forces associated with division have been implicated in tissue-scale processes, including development, tissue growth, migration, and epidermal stratification. While forces generated by mitotic rounding are well understood, forces generated after rounding remain unknown. Here, we identify two distinct stages of division force generation that follow rounding: (1) Protrusive forces along the division axis that drive division elongation, and (2) outward forces that facilitate postdivision spreading. Cytokinetic ring contraction of the dividing cell, but not activity of neighboring cells, generates extracellular forces that propel division elongation and contribute to chromosome segregation. Forces from division elongation are observed in epithelia across many model organisms. Thus, division elongation forces represent a universal mechanism that powers cell division in confining epithelia. |
| doi_str_mv | 10.1083/jcb.202011106 |
| format | article |
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These morphological changes occur despite dividing cells being mechanically restricted by neighboring cells, indicating the need for extracellular force generation. Beyond driving cell division itself, forces associated with division have been implicated in tissue-scale processes, including development, tissue growth, migration, and epidermal stratification. While forces generated by mitotic rounding are well understood, forces generated after rounding remain unknown. Here, we identify two distinct stages of division force generation that follow rounding: (1) Protrusive forces along the division axis that drive division elongation, and (2) outward forces that facilitate postdivision spreading. Cytokinetic ring contraction of the dividing cell, but not activity of neighboring cells, generates extracellular forces that propel division elongation and contribute to chromosome segregation. Forces from division elongation are observed in epithelia across many model organisms. Thus, division elongation forces represent a universal mechanism that powers cell division in confining epithelia.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.202011106</identifier><identifier>PMID: 34132746</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Animals, Genetically Modified ; Biophysics ; Cell Communication ; Cell Cycle and Division ; Cell Division ; Cell Shape ; Chromosome Segregation ; Chromosomes ; Computer Simulation ; Contraction ; Dogs ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Elongation ; Epithelial cells ; Epithelial Cells - metabolism ; Epithelial Cells - physiology ; Epithelium ; Madin Darby Canine Kidney Cells ; Mechanotransduction, Cellular ; Microscopy, Confocal ; Microscopy, Fluorescence ; Models, Biological ; Morphology ; Rounding ; Stress, Mechanical ; Time Factors ; Time-Lapse Imaging</subject><ispartof>The Journal of cell biology, 2021-08, Vol.220 (8), p.1</ispartof><rights>2021 Gupta et al.</rights><rights>Copyright Rockefeller University Press Aug 2021</rights><rights>2021 Gupta et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-bfb45eae7c98d7e32bde73722e14b69a468b5897576d744ed94dbb9242d38d4e0</citedby><cites>FETCH-LOGICAL-c415t-bfb45eae7c98d7e32bde73722e14b69a468b5897576d744ed94dbb9242d38d4e0</cites><orcidid>0000-0001-7660-2524 ; 0000-0002-9287-3401 ; 0000-0002-3299-7832 ; 0000-0003-2724-7145 ; 0000-0003-2312-6346 ; 0000-0001-8060-2607</orcidid></display><links><openurl>$$Topenurl_article</openurl><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>780,885</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34132746$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gupta, Vivek K</creatorcontrib><creatorcontrib>Nam, Sungmin</creatorcontrib><creatorcontrib>Yim, Donghyun</creatorcontrib><creatorcontrib>Camuglia, Jaclyn</creatorcontrib><creatorcontrib>Martin, Judy Lisette</creatorcontrib><creatorcontrib>Sanders, Erin Nicole</creatorcontrib><creatorcontrib>O'Brien, Lucy Erin</creatorcontrib><creatorcontrib>Martin, Adam C</creatorcontrib><creatorcontrib>Kim, Taeyoon</creatorcontrib><creatorcontrib>Chaudhuri, Ovijit</creatorcontrib><title>The nature of cell division forces in epithelial monolayers</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Epithelial cells undergo striking morphological changes during division to ensure proper segregation of genetic and cytoplasmic materials. These morphological changes occur despite dividing cells being mechanically restricted by neighboring cells, indicating the need for extracellular force generation. Beyond driving cell division itself, forces associated with division have been implicated in tissue-scale processes, including development, tissue growth, migration, and epidermal stratification. While forces generated by mitotic rounding are well understood, forces generated after rounding remain unknown. Here, we identify two distinct stages of division force generation that follow rounding: (1) Protrusive forces along the division axis that drive division elongation, and (2) outward forces that facilitate postdivision spreading. Cytokinetic ring contraction of the dividing cell, but not activity of neighboring cells, generates extracellular forces that propel division elongation and contribute to chromosome segregation. Forces from division elongation are observed in epithelia across many model organisms. Thus, division elongation forces represent a universal mechanism that powers cell division in confining epithelia.</description><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Biophysics</subject><subject>Cell Communication</subject><subject>Cell Cycle and Division</subject><subject>Cell Division</subject><subject>Cell Shape</subject><subject>Chromosome Segregation</subject><subject>Chromosomes</subject><subject>Computer Simulation</subject><subject>Contraction</subject><subject>Dogs</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Elongation</subject><subject>Epithelial cells</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelial Cells - physiology</subject><subject>Epithelium</subject><subject>Madin Darby Canine Kidney Cells</subject><subject>Mechanotransduction, Cellular</subject><subject>Microscopy, Confocal</subject><subject>Microscopy, Fluorescence</subject><subject>Models, Biological</subject><subject>Morphology</subject><subject>Rounding</subject><subject>Stress, Mechanical</subject><subject>Time Factors</subject><subject>Time-Lapse Imaging</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>false</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNpdkUFr3DAQRkVISDbbHnsNhlx6cTKSR5ZMIRCWpi0EeknPQrLGXS1eayPZC_n39ZJ0aXqawzw-5pvH2CcONxx0dbtp3Y0AAZxzqE_YgkuEUnOEU7YAELxspJAX7DLnDQCgwuqcXVTIK6GwXrAvT2sqBjtOiYrYFS31feHDPuQQh6KLqaVchKGgXRjX1AfbF9s4xN6-UMof2Fln-0wf3-aS_Xr4-rT6Xj7-_PZjdf9YtsjlWLrOoSRLqm20V1QJ50lVSgji6OrGYq2d1I2SqvYKkXyD3rlGoPCV9kiwZHevubvJbcm3NIzJ9maXwtamFxNtMO83Q1ib33FvtEDQ8z-W7PNbQIrPE-XRbEM-VLUDxSkbIZErrSXwGb3-D93EKQ1zvZmSSshG1dVMla9Um2LOibrjMRzMQYuZtZijlpm_-rfBkf7rAf4AnRWIRQ</recordid><startdate>20210802</startdate><enddate>20210802</enddate><creator>Gupta, Vivek K</creator><creator>Nam, Sungmin</creator><creator>Yim, Donghyun</creator><creator>Camuglia, Jaclyn</creator><creator>Martin, Judy Lisette</creator><creator>Sanders, Erin Nicole</creator><creator>O'Brien, Lucy Erin</creator><creator>Martin, Adam C</creator><creator>Kim, Taeyoon</creator><creator>Chaudhuri, Ovijit</creator><general>Rockefeller University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7660-2524</orcidid><orcidid>https://orcid.org/0000-0002-9287-3401</orcidid><orcidid>https://orcid.org/0000-0002-3299-7832</orcidid><orcidid>https://orcid.org/0000-0003-2724-7145</orcidid><orcidid>https://orcid.org/0000-0003-2312-6346</orcidid><orcidid>https://orcid.org/0000-0001-8060-2607</orcidid></search><sort><creationdate>20210802</creationdate><title>The nature of cell division forces in epithelial monolayers</title><author>Gupta, Vivek K ; 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These morphological changes occur despite dividing cells being mechanically restricted by neighboring cells, indicating the need for extracellular force generation. Beyond driving cell division itself, forces associated with division have been implicated in tissue-scale processes, including development, tissue growth, migration, and epidermal stratification. While forces generated by mitotic rounding are well understood, forces generated after rounding remain unknown. Here, we identify two distinct stages of division force generation that follow rounding: (1) Protrusive forces along the division axis that drive division elongation, and (2) outward forces that facilitate postdivision spreading. Cytokinetic ring contraction of the dividing cell, but not activity of neighboring cells, generates extracellular forces that propel division elongation and contribute to chromosome segregation. Forces from division elongation are observed in epithelia across many model organisms. 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| identifier | ISSN: 0021-9525 |
| ispartof | The Journal of cell biology, 2021-08, Vol.220 (8), p.1 |
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| subjects | Animals Animals, Genetically Modified Biophysics Cell Communication Cell Cycle and Division Cell Division Cell Shape Chromosome Segregation Chromosomes Computer Simulation Contraction Dogs Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Elongation Epithelial cells Epithelial Cells - metabolism Epithelial Cells - physiology Epithelium Madin Darby Canine Kidney Cells Mechanotransduction, Cellular Microscopy, Confocal Microscopy, Fluorescence Models, Biological Morphology Rounding Stress, Mechanical Time Factors Time-Lapse Imaging |
| title | The nature of cell division forces in epithelial monolayers |
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