Actomyosin controls planarity and folding of epithelia in response to compression
Throughout embryonic development and adult life, epithelia are subjected to compressive deformations. While these have been shown to trigger mechanosensitive responses such as cell extrusion and differentiation, which span tens of minutes, little is known about how epithelia adapt to compression ove...
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Veröffentlicht in: | Nature materials 2020-01, Vol.19 (1), p.109-117 |
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description | Throughout embryonic development and adult life, epithelia are subjected to compressive deformations. While these have been shown to trigger mechanosensitive responses such as cell extrusion and differentiation, which span tens of minutes, little is known about how epithelia adapt to compression over shorter timescales. Here, using suspended epithelia, we uncover the immediate response of epithelial tissues to the application of in-plane compressive strains (5–80%). We show that fast compression induces tissue buckling followed by actomyosin-dependent tissue flattening that erases the buckle within tens of seconds, in both mono- and multi-layered epithelia. Strikingly, we identify a well-defined limit to this response, so that stable folds form in the tissue when compressive strains exceed a ‘buckling threshold’ of ~35%. A combination of experiment and modelling shows that this behaviour is orchestrated by adaptation of the actomyosin cytoskeleton as it re-establishes tissue tension following compression. Thus, tissue pre-tension allows epithelia to both buffer against deformation and sets their ability to form and retain folds during morphogenesis.
Epithelial tissues behave as pre-tensed viscoelastic sheets that can buffer against compression and rapidly recover from buckling. Epithelial mechanical properties define a tissue-intrinsic buckling threshold that dictates the compressive strain above which tissue folds become permanent. |
doi_str_mv | 10.1038/s41563-019-0461-x |
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Epithelial tissues behave as pre-tensed viscoelastic sheets that can buffer against compression and rapidly recover from buckling. Epithelial mechanical properties define a tissue-intrinsic buckling threshold that dictates the compressive strain above which tissue folds become permanent.</description><identifier>ISSN: 1476-1122</identifier><identifier>EISSN: 1476-4660</identifier><identifier>DOI: 10.1038/s41563-019-0461-x</identifier><identifier>PMID: 31451778</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/136 ; 631/57 ; 639/301/54/994 ; Actomyosin ; Actomyosin - chemistry ; Adaptation ; Animals ; Biological Physics ; Biology ; Biomaterials ; Buckling ; Cadherins - physiology ; Chemistry and Materials Science ; Compressive properties ; Compressive Strength ; Condensed Matter Physics ; Cytoskeleton ; Deformation ; Dogs ; Elasticity ; Epithelial Cells - cytology ; Epithelium - embryology ; Epithelium - physiology ; Green Fluorescent Proteins ; Madin Darby Canine Kidney Cells ; Materials Science ; Mechanical properties ; Microscopy, Confocal ; Models, Biological ; Morphogenesis ; Nanotechnology ; Optical and Electronic Materials ; Physics ; Stress, Mechanical ; University colleges ; Viscosity</subject><ispartof>Nature materials, 2020-01, Vol.19 (1), p.109-117</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2019</rights><rights>Copyright Nature Publishing Group Jan 2020</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c486t-f97c8c8dc956606fffd05338be82cada2b3642fe10eacfb6029afc3d46817ab23</citedby><cites>FETCH-LOGICAL-c486t-f97c8c8dc956606fffd05338be82cada2b3642fe10eacfb6029afc3d46817ab23</cites><orcidid>0000-0002-7902-0279 ; 0000-0002-9201-6186 ; 0000-0001-8259-0582 ; 0000-0002-0280-3531 ; 0000-0002-9976-462X</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/s41563-019-0461-x$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41563-019-0461-x$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31451778$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02359375$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Wyatt, Tom P. J.</creatorcontrib><creatorcontrib>Fouchard, Jonathan</creatorcontrib><creatorcontrib>Lisica, Ana</creatorcontrib><creatorcontrib>Khalilgharibi, Nargess</creatorcontrib><creatorcontrib>Baum, Buzz</creatorcontrib><creatorcontrib>Recho, Pierre</creatorcontrib><creatorcontrib>Kabla, Alexandre J.</creatorcontrib><creatorcontrib>Charras, Guillaume T.</creatorcontrib><title>Actomyosin controls planarity and folding of epithelia in response to compression</title><title>Nature materials</title><addtitle>Nat. Mater</addtitle><addtitle>Nat Mater</addtitle><description>Throughout embryonic development and adult life, epithelia are subjected to compressive deformations. While these have been shown to trigger mechanosensitive responses such as cell extrusion and differentiation, which span tens of minutes, little is known about how epithelia adapt to compression over shorter timescales. Here, using suspended epithelia, we uncover the immediate response of epithelial tissues to the application of in-plane compressive strains (5–80%). We show that fast compression induces tissue buckling followed by actomyosin-dependent tissue flattening that erases the buckle within tens of seconds, in both mono- and multi-layered epithelia. Strikingly, we identify a well-defined limit to this response, so that stable folds form in the tissue when compressive strains exceed a ‘buckling threshold’ of ~35%. A combination of experiment and modelling shows that this behaviour is orchestrated by adaptation of the actomyosin cytoskeleton as it re-establishes tissue tension following compression. Thus, tissue pre-tension allows epithelia to both buffer against deformation and sets their ability to form and retain folds during morphogenesis.
Epithelial tissues behave as pre-tensed viscoelastic sheets that can buffer against compression and rapidly recover from buckling. Epithelial mechanical properties define a tissue-intrinsic buckling threshold that dictates the compressive strain above which tissue folds become permanent.</description><subject>631/136</subject><subject>631/57</subject><subject>639/301/54/994</subject><subject>Actomyosin</subject><subject>Actomyosin - chemistry</subject><subject>Adaptation</subject><subject>Animals</subject><subject>Biological Physics</subject><subject>Biology</subject><subject>Biomaterials</subject><subject>Buckling</subject><subject>Cadherins - physiology</subject><subject>Chemistry and Materials Science</subject><subject>Compressive properties</subject><subject>Compressive Strength</subject><subject>Condensed Matter Physics</subject><subject>Cytoskeleton</subject><subject>Deformation</subject><subject>Dogs</subject><subject>Elasticity</subject><subject>Epithelial Cells - cytology</subject><subject>Epithelium - embryology</subject><subject>Epithelium - physiology</subject><subject>Green Fluorescent Proteins</subject><subject>Madin Darby Canine Kidney Cells</subject><subject>Materials Science</subject><subject>Mechanical properties</subject><subject>Microscopy, Confocal</subject><subject>Models, Biological</subject><subject>Morphogenesis</subject><subject>Nanotechnology</subject><subject>Optical and Electronic Materials</subject><subject>Physics</subject><subject>Stress, Mechanical</subject><subject>University colleges</subject><subject>Viscosity</subject><issn>1476-1122</issn><issn>1476-4660</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kUtr3DAUhUVJaNJpf0A3wZBNu3Cqq5fl5RDaJjBQAulayLKUKNiSI3lC5t9HgycpBLrS6zvn3quD0FfAF4Cp_JEZcEFrDG2NmYD6-QM6BdaImgmBjw57AEJO0KecHzAmwLn4iE4oMA5NI0_RzdrMcdzF7ENlYphTHHI1DTro5OddpUNfuTj0PtxV0VV28vO9HbyuCp5snmLItppjkY5TOWcfw2d07PSQ7ZfDukJ_f_28vbyqN39-X1-uN7VhUsy1axsjjexNy0uzwjnXY06p7KwkRveadFQw4ixgq43rBCatdob2TEhodEfoCn1ffO_1oKbkR512KmqvrtYbtb_DhPKWNvwJCvttYacUH7c2z2r02dihzGnjNitCJJQf5c0ePX-HPsRtCmUSRSiRFDNZyBWChTIp5pyse-sAsNpno5ZsVMlG7bNRz0VzdnDedqPt3xSvYRSALEAuT-HOpn-l_-_6Am6Tmhk</recordid><startdate>20200101</startdate><enddate>20200101</enddate><creator>Wyatt, Tom P. 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J.</au><au>Fouchard, Jonathan</au><au>Lisica, Ana</au><au>Khalilgharibi, Nargess</au><au>Baum, Buzz</au><au>Recho, Pierre</au><au>Kabla, Alexandre J.</au><au>Charras, Guillaume T.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Actomyosin controls planarity and folding of epithelia in response to compression</atitle><jtitle>Nature materials</jtitle><stitle>Nat. Mater</stitle><addtitle>Nat Mater</addtitle><date>2020-01-01</date><risdate>2020</risdate><volume>19</volume><issue>1</issue><spage>109</spage><epage>117</epage><pages>109-117</pages><issn>1476-1122</issn><eissn>1476-4660</eissn><abstract>Throughout embryonic development and adult life, epithelia are subjected to compressive deformations. While these have been shown to trigger mechanosensitive responses such as cell extrusion and differentiation, which span tens of minutes, little is known about how epithelia adapt to compression over shorter timescales. Here, using suspended epithelia, we uncover the immediate response of epithelial tissues to the application of in-plane compressive strains (5–80%). We show that fast compression induces tissue buckling followed by actomyosin-dependent tissue flattening that erases the buckle within tens of seconds, in both mono- and multi-layered epithelia. Strikingly, we identify a well-defined limit to this response, so that stable folds form in the tissue when compressive strains exceed a ‘buckling threshold’ of ~35%. A combination of experiment and modelling shows that this behaviour is orchestrated by adaptation of the actomyosin cytoskeleton as it re-establishes tissue tension following compression. Thus, tissue pre-tension allows epithelia to both buffer against deformation and sets their ability to form and retain folds during morphogenesis.
Epithelial tissues behave as pre-tensed viscoelastic sheets that can buffer against compression and rapidly recover from buckling. Epithelial mechanical properties define a tissue-intrinsic buckling threshold that dictates the compressive strain above which tissue folds become permanent.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31451778</pmid><doi>10.1038/s41563-019-0461-x</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-7902-0279</orcidid><orcidid>https://orcid.org/0000-0002-9201-6186</orcidid><orcidid>https://orcid.org/0000-0001-8259-0582</orcidid><orcidid>https://orcid.org/0000-0002-0280-3531</orcidid><orcidid>https://orcid.org/0000-0002-9976-462X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 631/136 631/57 639/301/54/994 Actomyosin Actomyosin - chemistry Adaptation Animals Biological Physics Biology Biomaterials Buckling Cadherins - physiology Chemistry and Materials Science Compressive properties Compressive Strength Condensed Matter Physics Cytoskeleton Deformation Dogs Elasticity Epithelial Cells - cytology Epithelium - embryology Epithelium - physiology Green Fluorescent Proteins Madin Darby Canine Kidney Cells Materials Science Mechanical properties Microscopy, Confocal Models, Biological Morphogenesis Nanotechnology Optical and Electronic Materials Physics Stress, Mechanical University colleges Viscosity |
title | Actomyosin controls planarity and folding of epithelia in response to compression |
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