Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo
Pulsed actomyosin contractility underlies diverse modes of tissue morphogenesis, but the underlying mechanisms remain poorly understood. Here, we combined quantitative imaging with genetic perturbations to identify a core mechanism for pulsed contractility in early embryos. We show that pulsed accum...
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| Veröffentlicht in: | The Journal of cell biology 2018-12, Vol.217 (12), p.4230-4252 |
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| creator | Michaux, Jonathan B Robin, François B McFadden, William M Munro, Edwin M |
| description | Pulsed actomyosin contractility underlies diverse modes of tissue morphogenesis, but the underlying mechanisms remain poorly understood. Here, we combined quantitative imaging with genetic perturbations to identify a core mechanism for pulsed contractility in early
embryos. We show that pulsed accumulation of actomyosin is governed by local control of assembly and disassembly downstream of RhoA. Pulsed activation and inactivation of RhoA precede, respectively, the accumulation and disappearance of actomyosin and persist in the absence of Myosin II. We find that fast (likely indirect) autoactivation of RhoA drives pulse initiation, while delayed, F-actin-dependent accumulation of the RhoA GTPase-activating proteins RGA-3/4 provides negative feedback to terminate each pulse. A mathematical model, constrained by our data, suggests that this combination of feedbacks is tuned to generate locally excitable RhoA dynamics. We propose that excitable RhoA dynamics are a common driver for pulsed contractility that can be tuned or coupled differently to actomyosin dynamics to produce a diversity of morphogenetic outcomes. |
| doi_str_mv | 10.1083/jcb.201806161 |
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embryos. We show that pulsed accumulation of actomyosin is governed by local control of assembly and disassembly downstream of RhoA. Pulsed activation and inactivation of RhoA precede, respectively, the accumulation and disappearance of actomyosin and persist in the absence of Myosin II. We find that fast (likely indirect) autoactivation of RhoA drives pulse initiation, while delayed, F-actin-dependent accumulation of the RhoA GTPase-activating proteins RGA-3/4 provides negative feedback to terminate each pulse. A mathematical model, constrained by our data, suggests that this combination of feedbacks is tuned to generate locally excitable RhoA dynamics. We propose that excitable RhoA dynamics are a common driver for pulsed contractility that can be tuned or coupled differently to actomyosin dynamics to produce a diversity of morphogenetic outcomes.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201806161</identifier><identifier>PMID: 30275107</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Accumulation ; Actin ; Actomyosin ; Contractility ; Deactivation ; Dismantling ; Dynamics ; Embryology ; Embryos ; Guanosine triphosphatases ; Inactivation ; Life Sciences ; Mathematical models ; Medical imaging ; Morphogenesis ; Myosin ; Negative feedback ; Proteins ; Quantitative analysis ; RhoA protein</subject><ispartof>The Journal of cell biology, 2018-12, Vol.217 (12), p.4230-4252</ispartof><rights>2018 Michaux et al.</rights><rights>Copyright Rockefeller University Press Dec 2018</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2018 Michaux et al. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c515t-2dd531f11f046734598bbe6f38a5645d60826cd0406bae063ca327b262011f573</citedby><cites>FETCH-LOGICAL-c515t-2dd531f11f046734598bbe6f38a5645d60826cd0406bae063ca327b262011f573</cites><orcidid>0000-0001-5535-5675 ; 0000-0002-2420-2593</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://www.ncbi.nlm.nih.gov/pubmed/30275107$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03989022$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Michaux, Jonathan B</creatorcontrib><creatorcontrib>Robin, François B</creatorcontrib><creatorcontrib>McFadden, William M</creatorcontrib><creatorcontrib>Munro, Edwin M</creatorcontrib><title>Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Pulsed actomyosin contractility underlies diverse modes of tissue morphogenesis, but the underlying mechanisms remain poorly understood. Here, we combined quantitative imaging with genetic perturbations to identify a core mechanism for pulsed contractility in early
embryos. We show that pulsed accumulation of actomyosin is governed by local control of assembly and disassembly downstream of RhoA. Pulsed activation and inactivation of RhoA precede, respectively, the accumulation and disappearance of actomyosin and persist in the absence of Myosin II. We find that fast (likely indirect) autoactivation of RhoA drives pulse initiation, while delayed, F-actin-dependent accumulation of the RhoA GTPase-activating proteins RGA-3/4 provides negative feedback to terminate each pulse. A mathematical model, constrained by our data, suggests that this combination of feedbacks is tuned to generate locally excitable RhoA dynamics. We propose that excitable RhoA dynamics are a common driver for pulsed contractility that can be tuned or coupled differently to actomyosin dynamics to produce a diversity of morphogenetic outcomes.</description><subject>Accumulation</subject><subject>Actin</subject><subject>Actomyosin</subject><subject>Contractility</subject><subject>Deactivation</subject><subject>Dismantling</subject><subject>Dynamics</subject><subject>Embryology</subject><subject>Embryos</subject><subject>Guanosine triphosphatases</subject><subject>Inactivation</subject><subject>Life Sciences</subject><subject>Mathematical models</subject><subject>Medical imaging</subject><subject>Morphogenesis</subject><subject>Myosin</subject><subject>Negative feedback</subject><subject>Proteins</subject><subject>Quantitative analysis</subject><subject>RhoA protein</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNpdkU2P0zAQhi0EYrsLR67IEhf2kDLjz-SCVFULi1QJhOBsOY6zTZXExU4q-u9x1aWCPY0088w7Hy8hbxCWCCX_sHP1kgGWoFDhM7JAKaAoUcBzsgBgWFSSyStyndIOAIQW_CW54sC0RNAL8u3ut-smW_eeft-GFW2Oox06l2gTu4On-7lPvqEujFO0burCmGg30mnrqbexP9L1kvreP9ic90Mdj-EVedHa3PT6Md6Qn5_ufqzvi83Xz1_Wq03hJMqpYE0jObaILQiluZBVWddetby0UgnZKCiZcg0IULX1oLiznOmaqXwrtlLzG_LxrLuf68E3zp827M0-doONRxNsZ_6vjN3WPISDUUxXXJdZ4PYssH3Sdr_amFMOeFVWwNgBM_v-cVgMv2afJjN0yfm-t6MPczIMUWopVAkZffcE3YU5jvkVmVIIUmt5Gl6cKRdDStG3lw0QzMlXk301F18z__bfay_0XyP5H7pWm_Q</recordid><startdate>20181203</startdate><enddate>20181203</enddate><creator>Michaux, Jonathan B</creator><creator>Robin, François B</creator><creator>McFadden, William M</creator><creator>Munro, Edwin M</creator><general>Rockefeller University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5535-5675</orcidid><orcidid>https://orcid.org/0000-0002-2420-2593</orcidid></search><sort><creationdate>20181203</creationdate><title>Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo</title><author>Michaux, Jonathan B ; Robin, François B ; McFadden, William M ; Munro, Edwin M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c515t-2dd531f11f046734598bbe6f38a5645d60826cd0406bae063ca327b262011f573</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Accumulation</topic><topic>Actin</topic><topic>Actomyosin</topic><topic>Contractility</topic><topic>Deactivation</topic><topic>Dismantling</topic><topic>Dynamics</topic><topic>Embryology</topic><topic>Embryos</topic><topic>Guanosine triphosphatases</topic><topic>Inactivation</topic><topic>Life Sciences</topic><topic>Mathematical models</topic><topic>Medical imaging</topic><topic>Morphogenesis</topic><topic>Myosin</topic><topic>Negative feedback</topic><topic>Proteins</topic><topic>Quantitative analysis</topic><topic>RhoA protein</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Michaux, Jonathan B</creatorcontrib><creatorcontrib>Robin, François B</creatorcontrib><creatorcontrib>McFadden, William M</creatorcontrib><creatorcontrib>Munro, Edwin M</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Michaux, Jonathan B</au><au>Robin, François B</au><au>McFadden, William M</au><au>Munro, Edwin M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2018-12-03</date><risdate>2018</risdate><volume>217</volume><issue>12</issue><spage>4230</spage><epage>4252</epage><pages>4230-4252</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><abstract>Pulsed actomyosin contractility underlies diverse modes of tissue morphogenesis, but the underlying mechanisms remain poorly understood. 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embryos. We show that pulsed accumulation of actomyosin is governed by local control of assembly and disassembly downstream of RhoA. Pulsed activation and inactivation of RhoA precede, respectively, the accumulation and disappearance of actomyosin and persist in the absence of Myosin II. We find that fast (likely indirect) autoactivation of RhoA drives pulse initiation, while delayed, F-actin-dependent accumulation of the RhoA GTPase-activating proteins RGA-3/4 provides negative feedback to terminate each pulse. A mathematical model, constrained by our data, suggests that this combination of feedbacks is tuned to generate locally excitable RhoA dynamics. We propose that excitable RhoA dynamics are a common driver for pulsed contractility that can be tuned or coupled differently to actomyosin dynamics to produce a diversity of morphogenetic outcomes.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>30275107</pmid><doi>10.1083/jcb.201806161</doi><tpages>23</tpages><orcidid>https://orcid.org/0000-0001-5535-5675</orcidid><orcidid>https://orcid.org/0000-0002-2420-2593</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Accumulation Actin Actomyosin Contractility Deactivation Dismantling Dynamics Embryology Embryos Guanosine triphosphatases Inactivation Life Sciences Mathematical models Medical imaging Morphogenesis Myosin Negative feedback Proteins Quantitative analysis RhoA protein |
| title | Excitable RhoA dynamics drive pulsed contractions in the early C. elegans embryo |
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