Local and tissue-scale forces drive oriented junction growth during tissue extension
Convergence–extension is a widespread morphogenetic process driven by polarized cell intercalation. In the Drosophila germ band, epithelial intercalation comprises loss of junctions between anterior–posterior neighbours followed by growth of new junctions between dorsal–ventral neighbours. Much is k...
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creator | Collinet, Claudio Rauzi, Matteo Lenne, Pierre-François Lecuit, Thomas |
description | Convergence–extension is a widespread morphogenetic process driven by polarized cell intercalation. In the
Drosophila
germ band, epithelial intercalation comprises loss of junctions between anterior–posterior neighbours followed by growth of new junctions between dorsal–ventral neighbours. Much is known about how active stresses drive polarized junction shrinkage. However, it is unclear how tissue convergence–extension emerges from local junction remodelling and what the specific role, if any, of junction growth is. Here we report that tissue convergence and extension correlate mostly with new junction growth. Simulations and
in vivo
mechanical perturbations reveal that junction growth is due to local polarized stresses driven by medial actomyosin contractions. Moreover, we find that tissue-scale pulling forces at the boundary with the invaginating posterior midgut actively participate in tissue extension by orienting junction growth. Thus, tissue extension is akin to a polarized fluid flow that requires parallel and concerted local and tissue-scale forces to drive junction growth and cell–cell displacement.
Lecuit and colleagues use live imaging and laser ablation approaches to show that germ-band extension of the
Drosophila
embryo is associated with new junction growth, which is dependent on both tissue-level and local forces. |
doi_str_mv | 10.1038/ncb3226 |
format | Article |
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Drosophila
germ band, epithelial intercalation comprises loss of junctions between anterior–posterior neighbours followed by growth of new junctions between dorsal–ventral neighbours. Much is known about how active stresses drive polarized junction shrinkage. However, it is unclear how tissue convergence–extension emerges from local junction remodelling and what the specific role, if any, of junction growth is. Here we report that tissue convergence and extension correlate mostly with new junction growth. Simulations and
in vivo
mechanical perturbations reveal that junction growth is due to local polarized stresses driven by medial actomyosin contractions. Moreover, we find that tissue-scale pulling forces at the boundary with the invaginating posterior midgut actively participate in tissue extension by orienting junction growth. Thus, tissue extension is akin to a polarized fluid flow that requires parallel and concerted local and tissue-scale forces to drive junction growth and cell–cell displacement.
Lecuit and colleagues use live imaging and laser ablation approaches to show that germ-band extension of the
Drosophila
embryo is associated with new junction growth, which is dependent on both tissue-level and local forces.</description><identifier>ISSN: 1465-7392</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/ncb3226</identifier><identifier>PMID: 26389664</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14 ; 14/19 ; 631/136/1660 ; 631/136/334/1582/715 ; 631/80/79/2028 ; 64/24 ; Animals ; Animals, Genetically Modified ; Body Patterning - genetics ; Cadherins - genetics ; Cadherins - metabolism ; Cancer Research ; Cell Adhesion - genetics ; Cell Biology ; Cell development (Biology) ; Cell Tracking - methods ; Cellular Biology ; Developmental Biology ; Drosophila melanogaster - embryology ; Drosophila melanogaster - genetics ; Drosophila melanogaster - metabolism ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Embryo, Nonmammalian - embryology ; Embryo, Nonmammalian - metabolism ; Fluid flow ; Fluorescence Recovery After Photobleaching ; Gene Expression Regulation, Developmental ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Intercellular Junctions - metabolism ; Life Sciences ; Luminescent Proteins - genetics ; Luminescent Proteins - metabolism ; Methods ; Microscopy, Confocal ; Observations ; Red Fluorescent Protein ; RNA Interference ; Stem Cells ; Time-Lapse Imaging ; Tissue engineering ; Tissues</subject><ispartof>Nature cell biology, 2015-10, Vol.17 (10), p.1247-1258</ispartof><rights>Springer Nature Limited 2015</rights><rights>COPYRIGHT 2015 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Oct 2015</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c547t-c9d3e2f401447146aedeee120e3fbe03ce279c7a7b32b847733ec32df2e633193</citedby><cites>FETCH-LOGICAL-c547t-c9d3e2f401447146aedeee120e3fbe03ce279c7a7b32b847733ec32df2e633193</cites><orcidid>0000-0002-6313-0668</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/ncb3226$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/ncb3226$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,777,781,882,27905,27906,41469,42538,51300</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26389664$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01428973$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Collinet, Claudio</creatorcontrib><creatorcontrib>Rauzi, Matteo</creatorcontrib><creatorcontrib>Lenne, Pierre-François</creatorcontrib><creatorcontrib>Lecuit, Thomas</creatorcontrib><title>Local and tissue-scale forces drive oriented junction growth during tissue extension</title><title>Nature cell biology</title><addtitle>Nat Cell Biol</addtitle><addtitle>Nat Cell Biol</addtitle><description>Convergence–extension is a widespread morphogenetic process driven by polarized cell intercalation. In the
Drosophila
germ band, epithelial intercalation comprises loss of junctions between anterior–posterior neighbours followed by growth of new junctions between dorsal–ventral neighbours. Much is known about how active stresses drive polarized junction shrinkage. However, it is unclear how tissue convergence–extension emerges from local junction remodelling and what the specific role, if any, of junction growth is. Here we report that tissue convergence and extension correlate mostly with new junction growth. Simulations and
in vivo
mechanical perturbations reveal that junction growth is due to local polarized stresses driven by medial actomyosin contractions. Moreover, we find that tissue-scale pulling forces at the boundary with the invaginating posterior midgut actively participate in tissue extension by orienting junction growth. Thus, tissue extension is akin to a polarized fluid flow that requires parallel and concerted local and tissue-scale forces to drive junction growth and cell–cell displacement.
Lecuit and colleagues use live imaging and laser ablation approaches to show that germ-band extension of the
Drosophila
embryo is associated with new junction growth, which is dependent on both tissue-level and local forces.</description><subject>14</subject><subject>14/19</subject><subject>631/136/1660</subject><subject>631/136/334/1582/715</subject><subject>631/80/79/2028</subject><subject>64/24</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Body Patterning - genetics</subject><subject>Cadherins - genetics</subject><subject>Cadherins - metabolism</subject><subject>Cancer Research</subject><subject>Cell Adhesion - genetics</subject><subject>Cell Biology</subject><subject>Cell development (Biology)</subject><subject>Cell Tracking - methods</subject><subject>Cellular Biology</subject><subject>Developmental Biology</subject><subject>Drosophila melanogaster - embryology</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Nature cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Collinet, Claudio</au><au>Rauzi, Matteo</au><au>Lenne, Pierre-François</au><au>Lecuit, Thomas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Local and tissue-scale forces drive oriented junction growth during tissue extension</atitle><jtitle>Nature cell biology</jtitle><stitle>Nat Cell Biol</stitle><addtitle>Nat Cell Biol</addtitle><date>2015-10-01</date><risdate>2015</risdate><volume>17</volume><issue>10</issue><spage>1247</spage><epage>1258</epage><pages>1247-1258</pages><issn>1465-7392</issn><eissn>1476-4679</eissn><abstract>Convergence–extension is a widespread morphogenetic process driven by polarized cell intercalation. In the
Drosophila
germ band, epithelial intercalation comprises loss of junctions between anterior–posterior neighbours followed by growth of new junctions between dorsal–ventral neighbours. Much is known about how active stresses drive polarized junction shrinkage. However, it is unclear how tissue convergence–extension emerges from local junction remodelling and what the specific role, if any, of junction growth is. Here we report that tissue convergence and extension correlate mostly with new junction growth. Simulations and
in vivo
mechanical perturbations reveal that junction growth is due to local polarized stresses driven by medial actomyosin contractions. Moreover, we find that tissue-scale pulling forces at the boundary with the invaginating posterior midgut actively participate in tissue extension by orienting junction growth. Thus, tissue extension is akin to a polarized fluid flow that requires parallel and concerted local and tissue-scale forces to drive junction growth and cell–cell displacement.
Lecuit and colleagues use live imaging and laser ablation approaches to show that germ-band extension of the
Drosophila
embryo is associated with new junction growth, which is dependent on both tissue-level and local forces.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>26389664</pmid><doi>10.1038/ncb3226</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-6313-0668</orcidid></addata></record> |
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subjects | 14 14/19 631/136/1660 631/136/334/1582/715 631/80/79/2028 64/24 Animals Animals, Genetically Modified Body Patterning - genetics Cadherins - genetics Cadherins - metabolism Cancer Research Cell Adhesion - genetics Cell Biology Cell development (Biology) Cell Tracking - methods Cellular Biology Developmental Biology Drosophila melanogaster - embryology Drosophila melanogaster - genetics Drosophila melanogaster - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Embryo, Nonmammalian - embryology Embryo, Nonmammalian - metabolism Fluid flow Fluorescence Recovery After Photobleaching Gene Expression Regulation, Developmental Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Intercellular Junctions - metabolism Life Sciences Luminescent Proteins - genetics Luminescent Proteins - metabolism Methods Microscopy, Confocal Observations Red Fluorescent Protein RNA Interference Stem Cells Time-Lapse Imaging Tissue engineering Tissues |
title | Local and tissue-scale forces drive oriented junction growth during tissue extension |
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