Interkinetic Nuclear Migration Is Centrosome Independent and Ensures Apical Cell Division to Maintain Tissue Integrity
Pseudostratified epithelia are widespread during animal development and feature elongated cells whose nuclei adopt various positions along the apicobasal cell axis. Before mitosis, nuclei migrate toward the apical surface, and subsequent divisions occur apically. So far, the exact purpose of this nu...
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Veröffentlicht in: | Developmental cell 2015-01, Vol.32 (2), p.203-219 |
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creator | Strzyz, Paulina J. Lee, Hyun O. Sidhaye, Jaydeep Weber, Isabell P. Leung, Louis C. Norden, Caren |
description | Pseudostratified epithelia are widespread during animal development and feature elongated cells whose nuclei adopt various positions along the apicobasal cell axis. Before mitosis, nuclei migrate toward the apical surface, and subsequent divisions occur apically. So far, the exact purpose of this nuclear migration remained elusive. One hypothesis was that apical migration ensures that nuclei and centrosomes meet for mitosis. We here demonstrate that in zebrafish neuroepithelia apical nuclear migration occurs independently of centrosome position or integrity. It is a highly reproducible phenomenon linked to the cell cycle via CDK1 activity. We propose that the robustness of bringing nuclei apically for mitosis ensures that cells are capable of reintegrating into the epithelium after division. Nonapical divisions lead to cell delamination and formation of cell clusters that subsequently interfere with neuronal layering. Therefore, positioning divisions apically in pseudostratified neuroepithelia could serve to safeguard epithelial integrity and enable proper proliferation and maturation.
[Display omitted]
•Apical IKNM is highly robust and occurs independently of the centrosome•CDK1 activity is necessary and sufficient to drive apical IKNM•Nonapical divisions perturb integrity of the pseudostratified neuroepithelium•Apical localization of divisions safeguards tissue architecture and maturation
Strzyz et al. show that, in zebrafish, pseudostratified retinal neuroepithelia apical nuclear migration prior to mitosis is a highly reproducible phenomenon. It does not depend on centrosome number, location, integrity, or position of mitotic entry. This ensures that proliferative cells robustly divide apically and safeguards tissue architecture and maturation. |
doi_str_mv | 10.1016/j.devcel.2014.12.001 |
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[Display omitted]
•Apical IKNM is highly robust and occurs independently of the centrosome•CDK1 activity is necessary and sufficient to drive apical IKNM•Nonapical divisions perturb integrity of the pseudostratified neuroepithelium•Apical localization of divisions safeguards tissue architecture and maturation
Strzyz et al. show that, in zebrafish, pseudostratified retinal neuroepithelia apical nuclear migration prior to mitosis is a highly reproducible phenomenon. It does not depend on centrosome number, location, integrity, or position of mitotic entry. This ensures that proliferative cells robustly divide apically and safeguards tissue architecture and maturation.</description><identifier>ISSN: 1534-5807</identifier><identifier>EISSN: 1878-1551</identifier><identifier>DOI: 10.1016/j.devcel.2014.12.001</identifier><identifier>PMID: 25600237</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cell Division - physiology ; Cell Nucleus - metabolism ; Cell Nucleus - pathology ; Centrosome - metabolism ; Dietary Sucrose - metabolism ; Epithelial Cells - cytology ; Epithelium - metabolism ; Epithelium - pathology ; Zebrafish - metabolism</subject><ispartof>Developmental cell, 2015-01, Vol.32 (2), p.203-219</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c478t-89fb0a08b61c93123b62073c22955592bb765a516bc7dcb23978de7c2685dece3</citedby><cites>FETCH-LOGICAL-c478t-89fb0a08b61c93123b62073c22955592bb765a516bc7dcb23978de7c2685dece3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1534580714007989$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25600237$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Strzyz, Paulina J.</creatorcontrib><creatorcontrib>Lee, Hyun O.</creatorcontrib><creatorcontrib>Sidhaye, Jaydeep</creatorcontrib><creatorcontrib>Weber, Isabell P.</creatorcontrib><creatorcontrib>Leung, Louis C.</creatorcontrib><creatorcontrib>Norden, Caren</creatorcontrib><title>Interkinetic Nuclear Migration Is Centrosome Independent and Ensures Apical Cell Division to Maintain Tissue Integrity</title><title>Developmental cell</title><addtitle>Dev Cell</addtitle><description>Pseudostratified epithelia are widespread during animal development and feature elongated cells whose nuclei adopt various positions along the apicobasal cell axis. Before mitosis, nuclei migrate toward the apical surface, and subsequent divisions occur apically. So far, the exact purpose of this nuclear migration remained elusive. One hypothesis was that apical migration ensures that nuclei and centrosomes meet for mitosis. We here demonstrate that in zebrafish neuroepithelia apical nuclear migration occurs independently of centrosome position or integrity. It is a highly reproducible phenomenon linked to the cell cycle via CDK1 activity. We propose that the robustness of bringing nuclei apically for mitosis ensures that cells are capable of reintegrating into the epithelium after division. Nonapical divisions lead to cell delamination and formation of cell clusters that subsequently interfere with neuronal layering. Therefore, positioning divisions apically in pseudostratified neuroepithelia could serve to safeguard epithelial integrity and enable proper proliferation and maturation.
[Display omitted]
•Apical IKNM is highly robust and occurs independently of the centrosome•CDK1 activity is necessary and sufficient to drive apical IKNM•Nonapical divisions perturb integrity of the pseudostratified neuroepithelium•Apical localization of divisions safeguards tissue architecture and maturation
Strzyz et al. show that, in zebrafish, pseudostratified retinal neuroepithelia apical nuclear migration prior to mitosis is a highly reproducible phenomenon. It does not depend on centrosome number, location, integrity, or position of mitotic entry. This ensures that proliferative cells robustly divide apically and safeguards tissue architecture and maturation.</description><subject>Animals</subject><subject>Cell Division - physiology</subject><subject>Cell Nucleus - metabolism</subject><subject>Cell Nucleus - pathology</subject><subject>Centrosome - metabolism</subject><subject>Dietary Sucrose - metabolism</subject><subject>Epithelial Cells - cytology</subject><subject>Epithelium - metabolism</subject><subject>Epithelium - pathology</subject><subject>Zebrafish - metabolism</subject><issn>1534-5807</issn><issn>1878-1551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1v1DAQhq0K1JbSf1AhH7kkeJz4IxekaltgpRYu5Ww59mzlJesstrNS_z1ebeHIweM5PO-M5iHkBlgLDOSnbevx4HBqOYO-Bd4yBmfkErTSDQgBb2ovur4RmqkL8i7nbQUkaHZOLriQjPFOXZLDOhZMv0LEEhz9vrgJbaKP4TnZEuZI15muMJY053mHdB097rGWWKiNnt7HvCTM9HYfnJ0qOU30LhxCPkbLTB9tiKU--hRyXo75gs8plJf35O3GThmvX_8r8vPL_dPqW_Pw4-t6dfvQuF7p0uhhMzLL9CjBDR3wbpScqc5xPgghBj6OSgorQI5OeTfyblDao3JcauHRYXdFPp7m7tP8e8FczC7kKm2yEeclG5CC96D5ABXtT6irx-aEG7NPYWfTiwFmjsbN1pyMm6NxA9xUoTX24XXDMu7Q_wv9VVyBzycA652HgMlkFzA69CGhK8bP4f8b_gDp7ZSa</recordid><startdate>20150126</startdate><enddate>20150126</enddate><creator>Strzyz, Paulina J.</creator><creator>Lee, Hyun O.</creator><creator>Sidhaye, Jaydeep</creator><creator>Weber, Isabell P.</creator><creator>Leung, Louis C.</creator><creator>Norden, Caren</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope></search><sort><creationdate>20150126</creationdate><title>Interkinetic Nuclear Migration Is Centrosome Independent and Ensures Apical Cell Division to Maintain Tissue Integrity</title><author>Strzyz, Paulina J. ; Lee, Hyun O. ; Sidhaye, Jaydeep ; Weber, Isabell P. ; Leung, Louis C. ; Norden, Caren</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c478t-89fb0a08b61c93123b62073c22955592bb765a516bc7dcb23978de7c2685dece3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Cell Division - physiology</topic><topic>Cell Nucleus - metabolism</topic><topic>Cell Nucleus - pathology</topic><topic>Centrosome - metabolism</topic><topic>Dietary Sucrose - metabolism</topic><topic>Epithelial Cells - cytology</topic><topic>Epithelium - metabolism</topic><topic>Epithelium - pathology</topic><topic>Zebrafish - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Strzyz, Paulina J.</creatorcontrib><creatorcontrib>Lee, Hyun O.</creatorcontrib><creatorcontrib>Sidhaye, Jaydeep</creatorcontrib><creatorcontrib>Weber, Isabell P.</creatorcontrib><creatorcontrib>Leung, Louis C.</creatorcontrib><creatorcontrib>Norden, Caren</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Developmental cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Strzyz, Paulina J.</au><au>Lee, Hyun O.</au><au>Sidhaye, Jaydeep</au><au>Weber, Isabell P.</au><au>Leung, Louis C.</au><au>Norden, Caren</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interkinetic Nuclear Migration Is Centrosome Independent and Ensures Apical Cell Division to Maintain Tissue Integrity</atitle><jtitle>Developmental cell</jtitle><addtitle>Dev Cell</addtitle><date>2015-01-26</date><risdate>2015</risdate><volume>32</volume><issue>2</issue><spage>203</spage><epage>219</epage><pages>203-219</pages><issn>1534-5807</issn><eissn>1878-1551</eissn><abstract>Pseudostratified epithelia are widespread during animal development and feature elongated cells whose nuclei adopt various positions along the apicobasal cell axis. Before mitosis, nuclei migrate toward the apical surface, and subsequent divisions occur apically. So far, the exact purpose of this nuclear migration remained elusive. One hypothesis was that apical migration ensures that nuclei and centrosomes meet for mitosis. We here demonstrate that in zebrafish neuroepithelia apical nuclear migration occurs independently of centrosome position or integrity. It is a highly reproducible phenomenon linked to the cell cycle via CDK1 activity. We propose that the robustness of bringing nuclei apically for mitosis ensures that cells are capable of reintegrating into the epithelium after division. Nonapical divisions lead to cell delamination and formation of cell clusters that subsequently interfere with neuronal layering. Therefore, positioning divisions apically in pseudostratified neuroepithelia could serve to safeguard epithelial integrity and enable proper proliferation and maturation.
[Display omitted]
•Apical IKNM is highly robust and occurs independently of the centrosome•CDK1 activity is necessary and sufficient to drive apical IKNM•Nonapical divisions perturb integrity of the pseudostratified neuroepithelium•Apical localization of divisions safeguards tissue architecture and maturation
Strzyz et al. show that, in zebrafish, pseudostratified retinal neuroepithelia apical nuclear migration prior to mitosis is a highly reproducible phenomenon. It does not depend on centrosome number, location, integrity, or position of mitotic entry. This ensures that proliferative cells robustly divide apically and safeguards tissue architecture and maturation.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25600237</pmid><doi>10.1016/j.devcel.2014.12.001</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cell Division - physiology Cell Nucleus - metabolism Cell Nucleus - pathology Centrosome - metabolism Dietary Sucrose - metabolism Epithelial Cells - cytology Epithelium - metabolism Epithelium - pathology Zebrafish - metabolism |
title | Interkinetic Nuclear Migration Is Centrosome Independent and Ensures Apical Cell Division to Maintain Tissue Integrity |
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