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...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Nature materials 2022-05, Vol.21 (5), p.588-597
Hauptverfasser: Guillamat, Pau, Blanch-Mercader, Carles, Pernollet, Guillaume, Kruse, Karsten, Roux, Aurélien
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 597
container_issue 5
container_start_page 588
container_title Nature materials
container_volume 21
creator Guillamat, Pau
Blanch-Mercader, Carles
Pernollet, Guillaume
Kruse, Karsten
Roux, Aurélien
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
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7612693</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2658985034</sourcerecordid><originalsourceid>FETCH-LOGICAL-c508t-2d044b20076f6e8f40ad5c56b7b33e19a97a9c53182b79d08b8bf3bea0e8cd03</originalsourceid><addsrcrecordid>eNp9kU9v1DAQxSMEoqXwBTigSFzgEBj_jXNBqqqWFq3EpXfLSSZZV1l78SQrwafHJUuBHjjZ8vzemxm_onjN4AMDYT6SZEqLCjivgLFGVupJccpkrSupNTw93hnj_KR4QXQHwJlS-nlxIhSTiitzWny5CTOOmMo57uMUR9-5qexxwG6mMqbRBf8DS5oTEiGVffIHH8Zy9kQLlruY9ts4YkDy9LJ4NriJ8NXxPCtury5vL66rzdfPNxfnm6pTYOaK9yBlywFqPWg0gwTXq07ptm6FQNa4pnZNpwQzvK2bHkxr2kG06ABN14M4Kz6ttvul3WHfYZiTm-w--Z1L32103v5bCX5rx3iwtWZcNyIbvF8Nto9k1-cbe_8GQtTScHVgmX13bJbitwVptjtPHU6TCxgXslxzI4DlbTL69hF6F5cU8k9kSpnGKBAyU3yluhSJEg4PEzCw96naNVWbU7W_UrUqi978vfKD5HeMGRArQLkUcpx_ev_H9ie9Zq4Z</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2658985034</pqid></control><display><type>article</type><title>Integer topological defects organize stresses driving tissue morphogenesis</title><source>MEDLINE</source><source>SpringerLink Journals</source><source>Nature</source><creator>Guillamat, Pau ; Blanch-Mercader, Carles ; Pernollet, Guillaume ; Kruse, Karsten ; Roux, Aurélien</creator><creatorcontrib>Guillamat, Pau ; Blanch-Mercader, Carles ; Pernollet, Guillaume ; Kruse, Karsten ; Roux, Aurélien</creatorcontrib><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><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 ; Blanch-Mercader, Carles ; Pernollet, Guillaume ; Kruse, Karsten ; Roux, Aurélien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c508t-2d044b20076f6e8f40ad5c56b7b33e19a97a9c53182b79d08b8bf3bea0e8cd03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>639/766/119/2792/4129</topic><topic>639/766/747</topic><topic>Biomaterials</topic><topic>Cell Differentiation</topic><topic>Chemistry and Materials Science</topic><topic>Compressive properties</topic><topic>Concentration gradient</topic><topic>Condensed Matter</topic><topic>Condensed Matter Physics</topic><topic>Cytoskeleton</topic><topic>Defects</topic><topic>Differentiation (biology)</topic><topic>Elastic deformation</topic><topic>Integers</topic><topic>Materials Science</topic><topic>Modulators</topic><topic>Morphogenesis</topic><topic>Nanotechnology</topic><topic>Optical and Electronic Materials</topic><topic>Physics</topic><topic>Spirals</topic><topic>Stresses</topic><topic>Swirling</topic><topic>Topology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guillamat, Pau</creatorcontrib><creatorcontrib>Blanch-Mercader, Carles</creatorcontrib><creatorcontrib>Pernollet, Guillaume</creatorcontrib><creatorcontrib>Kruse, Karsten</creatorcontrib><creatorcontrib>Roux, Aurélien</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Engineered Materials Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>Materials Research Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>ProQuest Engineering Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Engineering Database</collection><collection>Materials Science Collection</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature materials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guillamat, Pau</au><au>Blanch-Mercader, Carles</au><au>Pernollet, Guillaume</au><au>Kruse, Karsten</au><au>Roux, Aurélien</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Integer topological defects organize stresses driving tissue morphogenesis</atitle><jtitle>Nature materials</jtitle><stitle>Nat. 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>
fulltext fulltext
identifier ISSN: 1476-1122
ispartof Nature materials, 2022-05, Vol.21 (5), p.588-597
issn 1476-1122
1476-4660
1476-4660
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7612693
source MEDLINE; SpringerLink Journals; Nature
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
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-04T23%3A41%3A57IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Integer%20topological%20defects%20organize%20stresses%20driving%20tissue%20morphogenesis&rft.jtitle=Nature%20materials&rft.au=Guillamat,%20Pau&rft.date=2022-05-01&rft.volume=21&rft.issue=5&rft.spage=588&rft.epage=597&rft.pages=588-597&rft.issn=1476-1122&rft.eissn=1476-4660&rft_id=info:doi/10.1038/s41563-022-01194-5&rft_dat=%3Cproquest_pubme%3E2658985034%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2658985034&rft_id=info:pmid/35145258&rfr_iscdi=true