Loading…

How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale

Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlle...

Full description

Saved in:
Bibliographic Details
Published in:Interface focus 2022-10, Vol.12 (6)
Main Authors: Erlich, Alexander, Pearce, Philip, Mayo, Romina Plitman, Jensen, Oliver, Chernyavsky, Igor
Format: Article
Language:English
Subjects:
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by
cites
container_end_page
container_issue 6
container_start_page
container_title Interface focus
container_volume 12
creator Erlich, Alexander
Pearce, Philip
Mayo, Romina Plitman
Jensen, Oliver
Chernyavsky, Igor
description Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress—topological prestress—can result from active processes altering the microstructure of tissue.
doi_str_mv 10.1098/rsfs.2022.0038
format article
fullrecord <record><control><sourceid>hal</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_04799755v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>oai_HAL_hal_04799755v1</sourcerecordid><originalsourceid>FETCH-hal_primary_oai_HAL_hal_04799755v13</originalsourceid><addsrcrecordid>eNqVikFrgzAYhkNhMOm87vxdC639Eu3UYxkbHnrsPaQ21oxoJF90-O_rWP9AX3h44eFh7J1jwrEs9p4aSgQKkSCmxYpFAjOxK0rkrywm-sFl2QcvUERMVu4XrnOvOlPD4DWFBYKbm7TvCUKrgVo1aHANWDOZ_gY0U9AdbaHxrvsvxkutrR2t8hAcBEM0LrZWVr-xl0ZZ0vHj12zz_XX-rHatsnLwplN-lk4ZWR1P8s9hlpdlfjhMPH2mvQNITU5E</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale</title><source>Open Access: PubMed Central</source><source>Royal Society Publishing Jisc Collections Royal Society Journals Read &amp; Publish Transitional Agreement 2025 (reading list)</source><creator>Erlich, Alexander ; Pearce, Philip ; Mayo, Romina Plitman ; Jensen, Oliver ; Chernyavsky, Igor</creator><creatorcontrib>Erlich, Alexander ; Pearce, Philip ; Mayo, Romina Plitman ; Jensen, Oliver ; Chernyavsky, Igor</creatorcontrib><description>Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress—topological prestress—can result from active processes altering the microstructure of tissue.</description><identifier>EISSN: 2042-8901</identifier><identifier>DOI: 10.1098/rsfs.2022.0038</identifier><language>eng</language><publisher>Royal Society publishing</publisher><subject>Biochemistry, Molecular Biology ; Biophysics ; Life Sciences</subject><ispartof>Interface focus, 2022-10, Vol.12 (6)</ispartof><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0002-2294-1894 ; 0000-0001-5788-3826 ; 0000-0003-0172-6578 ; 0000-0001-5788-3826 ; 0000-0003-0172-6578 ; 0000-0002-2294-1894</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://hal.science/hal-04799755$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Erlich, Alexander</creatorcontrib><creatorcontrib>Pearce, Philip</creatorcontrib><creatorcontrib>Mayo, Romina Plitman</creatorcontrib><creatorcontrib>Jensen, Oliver</creatorcontrib><creatorcontrib>Chernyavsky, Igor</creatorcontrib><title>How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale</title><title>Interface focus</title><description>Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress—topological prestress—can result from active processes altering the microstructure of tissue.</description><subject>Biochemistry, Molecular Biology</subject><subject>Biophysics</subject><subject>Life Sciences</subject><issn>2042-8901</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqVikFrgzAYhkNhMOm87vxdC639Eu3UYxkbHnrsPaQ21oxoJF90-O_rWP9AX3h44eFh7J1jwrEs9p4aSgQKkSCmxYpFAjOxK0rkrywm-sFl2QcvUERMVu4XrnOvOlPD4DWFBYKbm7TvCUKrgVo1aHANWDOZ_gY0U9AdbaHxrvsvxkutrR2t8hAcBEM0LrZWVr-xl0ZZ0vHj12zz_XX-rHatsnLwplN-lk4ZWR1P8s9hlpdlfjhMPH2mvQNITU5E</recordid><startdate>20221014</startdate><enddate>20221014</enddate><creator>Erlich, Alexander</creator><creator>Pearce, Philip</creator><creator>Mayo, Romina Plitman</creator><creator>Jensen, Oliver</creator><creator>Chernyavsky, Igor</creator><general>Royal Society publishing</general><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-2294-1894</orcidid><orcidid>https://orcid.org/0000-0001-5788-3826</orcidid><orcidid>https://orcid.org/0000-0003-0172-6578</orcidid><orcidid>https://orcid.org/0000-0001-5788-3826</orcidid><orcidid>https://orcid.org/0000-0003-0172-6578</orcidid><orcidid>https://orcid.org/0000-0002-2294-1894</orcidid></search><sort><creationdate>20221014</creationdate><title>How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale</title><author>Erlich, Alexander ; Pearce, Philip ; Mayo, Romina Plitman ; Jensen, Oliver ; Chernyavsky, Igor</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-hal_primary_oai_HAL_hal_04799755v13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biochemistry, Molecular Biology</topic><topic>Biophysics</topic><topic>Life Sciences</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Erlich, Alexander</creatorcontrib><creatorcontrib>Pearce, Philip</creatorcontrib><creatorcontrib>Mayo, Romina Plitman</creatorcontrib><creatorcontrib>Jensen, Oliver</creatorcontrib><creatorcontrib>Chernyavsky, Igor</creatorcontrib><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Interface focus</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Erlich, Alexander</au><au>Pearce, Philip</au><au>Mayo, Romina Plitman</au><au>Jensen, Oliver</au><au>Chernyavsky, Igor</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale</atitle><jtitle>Interface focus</jtitle><date>2022-10-14</date><risdate>2022</risdate><volume>12</volume><issue>6</issue><eissn>2042-8901</eissn><abstract>Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress—topological prestress—can result from active processes altering the microstructure of tissue.</abstract><pub>Royal Society publishing</pub><doi>10.1098/rsfs.2022.0038</doi><orcidid>https://orcid.org/0000-0002-2294-1894</orcidid><orcidid>https://orcid.org/0000-0001-5788-3826</orcidid><orcidid>https://orcid.org/0000-0003-0172-6578</orcidid><orcidid>https://orcid.org/0000-0001-5788-3826</orcidid><orcidid>https://orcid.org/0000-0003-0172-6578</orcidid><orcidid>https://orcid.org/0000-0002-2294-1894</orcidid></addata></record>
fulltext fulltext
identifier EISSN: 2042-8901
ispartof Interface focus, 2022-10, Vol.12 (6)
issn 2042-8901
language eng
recordid cdi_hal_primary_oai_HAL_hal_04799755v1
source Open Access: PubMed Central; Royal Society Publishing Jisc Collections Royal Society Journals Read & Publish Transitional Agreement 2025 (reading list)
subjects Biochemistry, Molecular Biology
Biophysics
Life Sciences
title How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T15%3A37%3A01IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-hal&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=How%20dynamic%20prestress%20governs%20the%20shape%20of%20living%20systems,%20from%20the%20subcellular%20to%20tissue%20scale&rft.jtitle=Interface%20focus&rft.au=Erlich,%20Alexander&rft.date=2022-10-14&rft.volume=12&rft.issue=6&rft.eissn=2042-8901&rft_id=info:doi/10.1098/rsfs.2022.0038&rft_dat=%3Chal%3Eoai_HAL_hal_04799755v1%3C/hal%3E%3Cgrp_id%3Ecdi_FETCH-hal_primary_oai_HAL_hal_04799755v13%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_id=info:pmid/&rfr_iscdi=true