Integer topological defects organize stresses driving tissue morphogenesis
Tissues acquire function and shape via differentiation and morphogenesis. Both processes are driven by coordinating cellular forces and shapes at the tissue scale, but general principles governing this interplay remain to be discovered. Here we report that self-organization of myoblasts around integ...
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Veröffentlicht in: | Nature materials 2022-05, Vol.21 (5), p.588-597 |
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description | Tissues acquire function and shape via differentiation and morphogenesis. Both processes are driven by coordinating cellular forces and shapes at the tissue scale, but general principles governing this interplay remain to be discovered. Here we report that self-organization of myoblasts around integer topological defects, namely spirals and asters, suffices to establish complex multicellular architectures. In particular, these arrangements can trigger localized cell differentiation or, alternatively, when differentiation is inhibited, they can drive the growth of swirling protrusions. Both localized differentiation and growth of cellular vortices require specific stress patterns. By analysing the experimental velocity and orientational fields through active gel theory, we show that integer topological defects can generate force gradients that concentrate compressive stresses. We reveal these gradients by assessing spatial changes in nuclear volume and deformations of elastic pillars. We propose integer topological defects as mechanical organizing centres controlling differentiation and morphogenesis.
Integer topological defects promote cellular self-organization, leading to the formation of complex cellular assemblies that trigger cell differentiation and the formation of swirling cellular pillars once differentiation is inhibited. These findings suggest that integer topological defects are important modulators of cellular differentiation and tissue morphogenesis. |
doi_str_mv | 10.1038/s41563-022-01194-5 |
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Integer topological defects promote cellular self-organization, leading to the formation of complex cellular assemblies that trigger cell differentiation and the formation of swirling cellular pillars once differentiation is inhibited. These findings suggest that integer topological defects are important modulators of cellular differentiation and tissue morphogenesis.</description><identifier>ISSN: 1476-1122</identifier><identifier>ISSN: 1476-4660</identifier><identifier>EISSN: 1476-4660</identifier><identifier>DOI: 10.1038/s41563-022-01194-5</identifier><identifier>PMID: 35145258</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>639/766/119/2792/4129 ; 639/766/747 ; Biomaterials ; Cell Differentiation ; Chemistry and Materials Science ; Compressive properties ; Concentration gradient ; Condensed Matter ; Condensed Matter Physics ; Cytoskeleton ; Defects ; Differentiation (biology) ; Elastic deformation ; Integers ; Materials Science ; Modulators ; Morphogenesis ; Nanotechnology ; Optical and Electronic Materials ; Physics ; Spirals ; Stresses ; Swirling ; Topology</subject><ispartof>Nature materials, 2022-05, Vol.21 (5), p.588-597</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2022</rights><rights>2022. The Author(s), under exclusive licence to Springer Nature Limited.</rights><rights>The Author(s), under exclusive licence to Springer Nature Limited 2022.</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-c508t-2d044b20076f6e8f40ad5c56b7b33e19a97a9c53182b79d08b8bf3bea0e8cd03</citedby><cites>FETCH-LOGICAL-c508t-2d044b20076f6e8f40ad5c56b7b33e19a97a9c53182b79d08b8bf3bea0e8cd03</cites><orcidid>0000-0001-8665-2349 ; 0000-0002-6088-0711 ; 0000-0002-7050-4672 ; 0000-0003-1536-8548</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/s41563-022-01194-5$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41563-022-01194-5$$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/35145258$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.sorbonne-universite.fr/hal-03374825$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Guillamat, Pau</creatorcontrib><creatorcontrib>Blanch-Mercader, Carles</creatorcontrib><creatorcontrib>Pernollet, Guillaume</creatorcontrib><creatorcontrib>Kruse, Karsten</creatorcontrib><creatorcontrib>Roux, Aurélien</creatorcontrib><title>Integer topological defects organize stresses driving tissue morphogenesis</title><title>Nature materials</title><addtitle>Nat. Mater</addtitle><addtitle>Nat Mater</addtitle><description>Tissues acquire function and shape via differentiation and morphogenesis. Both processes are driven by coordinating cellular forces and shapes at the tissue scale, but general principles governing this interplay remain to be discovered. Here we report that self-organization of myoblasts around integer topological defects, namely spirals and asters, suffices to establish complex multicellular architectures. In particular, these arrangements can trigger localized cell differentiation or, alternatively, when differentiation is inhibited, they can drive the growth of swirling protrusions. Both localized differentiation and growth of cellular vortices require specific stress patterns. By analysing the experimental velocity and orientational fields through active gel theory, we show that integer topological defects can generate force gradients that concentrate compressive stresses. We reveal these gradients by assessing spatial changes in nuclear volume and deformations of elastic pillars. We propose integer topological defects as mechanical organizing centres controlling differentiation and morphogenesis.
Integer topological defects promote cellular self-organization, leading to the formation of complex cellular assemblies that trigger cell differentiation and the formation of swirling cellular pillars once differentiation is inhibited. These findings suggest that integer topological defects are important modulators of cellular differentiation and tissue morphogenesis.</description><subject>639/766/119/2792/4129</subject><subject>639/766/747</subject><subject>Biomaterials</subject><subject>Cell Differentiation</subject><subject>Chemistry and Materials Science</subject><subject>Compressive properties</subject><subject>Concentration gradient</subject><subject>Condensed Matter</subject><subject>Condensed Matter Physics</subject><subject>Cytoskeleton</subject><subject>Defects</subject><subject>Differentiation (biology)</subject><subject>Elastic deformation</subject><subject>Integers</subject><subject>Materials Science</subject><subject>Modulators</subject><subject>Morphogenesis</subject><subject>Nanotechnology</subject><subject>Optical and Electronic Materials</subject><subject>Physics</subject><subject>Spirals</subject><subject>Stresses</subject><subject>Swirling</subject><subject>Topology</subject><issn>1476-1122</issn><issn>1476-4660</issn><issn>1476-4660</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp9kU9v1DAQxSMEoqXwBTigSFzgEBj_jXNBqqqWFq3EpXfLSSZZV1l78SQrwafHJUuBHjjZ8vzemxm_onjN4AMDYT6SZEqLCjivgLFGVupJccpkrSupNTw93hnj_KR4QXQHwJlS-nlxIhSTiitzWny5CTOOmMo57uMUR9-5qexxwG6mMqbRBf8DS5oTEiGVffIHH8Zy9kQLlruY9ts4YkDy9LJ4NriJ8NXxPCtury5vL66rzdfPNxfnm6pTYOaK9yBlywFqPWg0gwTXq07ptm6FQNa4pnZNpwQzvK2bHkxr2kG06ABN14M4Kz6ttvul3WHfYZiTm-w--Z1L32103v5bCX5rx3iwtWZcNyIbvF8Nto9k1-cbe_8GQtTScHVgmX13bJbitwVptjtPHU6TCxgXslxzI4DlbTL69hF6F5cU8k9kSpnGKBAyU3yluhSJEg4PEzCw96naNVWbU7W_UrUqi978vfKD5HeMGRArQLkUcpx_ev_H9ie9Zq4Z</recordid><startdate>20220501</startdate><enddate>20220501</enddate><creator>Guillamat, Pau</creator><creator>Blanch-Mercader, Carles</creator><creator>Pernollet, Guillaume</creator><creator>Kruse, Karsten</creator><creator>Roux, Aurélien</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>3V.</scope><scope>7SR</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8BQ</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>JG9</scope><scope>K9.</scope><scope>KB.</scope><scope>L6V</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7S</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>Q9U</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8665-2349</orcidid><orcidid>https://orcid.org/0000-0002-6088-0711</orcidid><orcidid>https://orcid.org/0000-0002-7050-4672</orcidid><orcidid>https://orcid.org/0000-0003-1536-8548</orcidid></search><sort><creationdate>20220501</creationdate><title>Integer topological defects organize stresses driving tissue morphogenesis</title><author>Guillamat, Pau ; 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Mater</stitle><addtitle>Nat Mater</addtitle><date>2022-05-01</date><risdate>2022</risdate><volume>21</volume><issue>5</issue><spage>588</spage><epage>597</epage><pages>588-597</pages><issn>1476-1122</issn><issn>1476-4660</issn><eissn>1476-4660</eissn><abstract>Tissues acquire function and shape via differentiation and morphogenesis. Both processes are driven by coordinating cellular forces and shapes at the tissue scale, but general principles governing this interplay remain to be discovered. Here we report that self-organization of myoblasts around integer topological defects, namely spirals and asters, suffices to establish complex multicellular architectures. In particular, these arrangements can trigger localized cell differentiation or, alternatively, when differentiation is inhibited, they can drive the growth of swirling protrusions. Both localized differentiation and growth of cellular vortices require specific stress patterns. By analysing the experimental velocity and orientational fields through active gel theory, we show that integer topological defects can generate force gradients that concentrate compressive stresses. We reveal these gradients by assessing spatial changes in nuclear volume and deformations of elastic pillars. We propose integer topological defects as mechanical organizing centres controlling differentiation and morphogenesis.
Integer topological defects promote cellular self-organization, leading to the formation of complex cellular assemblies that trigger cell differentiation and the formation of swirling cellular pillars once differentiation is inhibited. These findings suggest that integer topological defects are important modulators of cellular differentiation and tissue morphogenesis.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>35145258</pmid><doi>10.1038/s41563-022-01194-5</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-8665-2349</orcidid><orcidid>https://orcid.org/0000-0002-6088-0711</orcidid><orcidid>https://orcid.org/0000-0002-7050-4672</orcidid><orcidid>https://orcid.org/0000-0003-1536-8548</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 639/766/119/2792/4129 639/766/747 Biomaterials Cell Differentiation Chemistry and Materials Science Compressive properties Concentration gradient Condensed Matter Condensed Matter Physics Cytoskeleton Defects Differentiation (biology) Elastic deformation Integers Materials Science Modulators Morphogenesis Nanotechnology Optical and Electronic Materials Physics Spirals Stresses Swirling Topology |
title | Integer topological defects organize stresses driving tissue morphogenesis |
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