Dissection of two parallel pathways for formin-mediated actin filament elongation
Formins direct the elongation of unbranched actin filaments that are incorporated into a diverse set of cytoskeletal structures. Elongation of formin-bound filaments occurs along two parallel pathways. The formin homology 2 (FH2) pathway allows actin monomers to bind directly to barbed ends bound by...
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| Veröffentlicht in: | The Journal of biological chemistry 2018-11, Vol.293 (46), p.17917-17928 |
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| container_issue | 46 |
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| container_title | The Journal of biological chemistry |
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| creator | Sherer, Laura A. Zweifel, Mark E. Courtemanche, Naomi |
| description | Formins direct the elongation of unbranched actin filaments that are incorporated into a diverse set of cytoskeletal structures. Elongation of formin-bound filaments occurs along two parallel pathways. The formin homology 2 (FH2) pathway allows actin monomers to bind directly to barbed ends bound by dimeric FH2 domains. The formin homology 1 (FH1) pathway involves transfer of profilin-bound actin to the barbed end from polyproline tracts located in the disordered FH1 domains. Here, we used a total internal reflection fluorescence (TIRF) microscopy-based fluorescence approach to determine the fraction of actin subunits incorporated via the FH1 and FH2 pathways during filament elongation mediated by two formins. We found that the fraction of filament elongation that occurs via each pathway directly depends on the efficiency of the other pathway, indicating that these two pathways compete with each other for subunit addition by formins. We conclude that this competition allows formins to compensate for changes in the efficiency of one pathway by adjusting the frequency of subunit addition via the other, thus increasing the overall robustness of formin-mediated actin polymerization. |
| doi_str_mv | 10.1074/jbc.RA118.004845 |
| format | Article |
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Elongation of formin-bound filaments occurs along two parallel pathways. The formin homology 2 (FH2) pathway allows actin monomers to bind directly to barbed ends bound by dimeric FH2 domains. The formin homology 1 (FH1) pathway involves transfer of profilin-bound actin to the barbed end from polyproline tracts located in the disordered FH1 domains. Here, we used a total internal reflection fluorescence (TIRF) microscopy-based fluorescence approach to determine the fraction of actin subunits incorporated via the FH1 and FH2 pathways during filament elongation mediated by two formins. We found that the fraction of filament elongation that occurs via each pathway directly depends on the efficiency of the other pathway, indicating that these two pathways compete with each other for subunit addition by formins. 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Elongation of formin-bound filaments occurs along two parallel pathways. The formin homology 2 (FH2) pathway allows actin monomers to bind directly to barbed ends bound by dimeric FH2 domains. The formin homology 1 (FH1) pathway involves transfer of profilin-bound actin to the barbed end from polyproline tracts located in the disordered FH1 domains. Here, we used a total internal reflection fluorescence (TIRF) microscopy-based fluorescence approach to determine the fraction of actin subunits incorporated via the FH1 and FH2 pathways during filament elongation mediated by two formins. We found that the fraction of filament elongation that occurs via each pathway directly depends on the efficiency of the other pathway, indicating that these two pathways compete with each other for subunit addition by formins. We conclude that this competition allows formins to compensate for changes in the efficiency of one pathway by adjusting the frequency of subunit addition via the other, thus increasing the overall robustness of formin-mediated actin polymerization.</description><subject>Actins - metabolism</subject><subject>Animals</subject><subject>Carboxylic Acids - chemistry</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Chickens</subject><subject>Cytoskeletal Proteins - metabolism</subject><subject>Fluorescence</subject><subject>Fluorescent Dyes - chemistry</subject><subject>Microfilament Proteins - metabolism</subject><subject>Microscopy, Fluorescence</subject><subject>Molecular Biophysics</subject><subject>Profilins - metabolism</subject><subject>Protein Binding</subject><subject>Protein Domains</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Schizosaccharomyces</subject><subject>Schizosaccharomyces pombe Proteins - metabolism</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1UUFLHDEYDdJSV9u7J5mjl9l-mUkyiQdBttUKgigK3kIm-0UjM5M1mVX892a6KvbQwEcC33svj_cI2aMwp9Cwnw-tnV8dUyrnAEwyvkVmFGRd1pzefiEzgIqWquJym-yk9AD5MEW_ke0aKiEkyBm5_OVTQjv6MBTBFeNzKFYmmq7DLj_G-2fzkgoX4jS9H8oel96MuCxM5gyF853pcRgL7MJwZyaZ7-SrM13CH2_3Lrk5-X29-FOeX5yeLY7PS8tYM5ZtTVmtOKPMQqugspYDFdgqp5CKRjolaiERFDbAuWubZcbzyjpVMcpNU--So43uat1mVza7yL71KvrexBcdjNf_bgZ_r-_CkxYVA9lMAgdvAjE8rjGNuvfJYteZAcM66YpSJpRgfILCBmpjSCmi-_iGgp6a0LkJ_bcJvWkiU_Y_2_sgvEefAYcbAOaQnjxGnazHweaAYy5EL4P_v_orB3iZVA</recordid><startdate>20181116</startdate><enddate>20181116</enddate><creator>Sherer, Laura A.</creator><creator>Zweifel, Mark E.</creator><creator>Courtemanche, Naomi</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20181116</creationdate><title>Dissection of two parallel pathways for formin-mediated actin filament elongation</title><author>Sherer, Laura A. ; Zweifel, Mark E. ; Courtemanche, Naomi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c447t-b314395414c0b902cc5016eb9f9e1678f96368e09e7055fb7d14352cf92415a73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Actins - metabolism</topic><topic>Animals</topic><topic>Carboxylic Acids - chemistry</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Chickens</topic><topic>Cytoskeletal Proteins - metabolism</topic><topic>Fluorescence</topic><topic>Fluorescent Dyes - chemistry</topic><topic>Microfilament Proteins - metabolism</topic><topic>Microscopy, Fluorescence</topic><topic>Molecular Biophysics</topic><topic>Profilins - metabolism</topic><topic>Protein Binding</topic><topic>Protein Domains</topic><topic>Saccharomyces cerevisiae</topic><topic>Saccharomyces cerevisiae Proteins - metabolism</topic><topic>Schizosaccharomyces</topic><topic>Schizosaccharomyces pombe Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sherer, Laura A.</creatorcontrib><creatorcontrib>Zweifel, Mark E.</creatorcontrib><creatorcontrib>Courtemanche, Naomi</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sherer, Laura A.</au><au>Zweifel, Mark E.</au><au>Courtemanche, Naomi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dissection of two parallel pathways for formin-mediated actin filament elongation</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2018-11-16</date><risdate>2018</risdate><volume>293</volume><issue>46</issue><spage>17917</spage><epage>17928</epage><pages>17917-17928</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Formins direct the elongation of unbranched actin filaments that are incorporated into a diverse set of cytoskeletal structures. Elongation of formin-bound filaments occurs along two parallel pathways. The formin homology 2 (FH2) pathway allows actin monomers to bind directly to barbed ends bound by dimeric FH2 domains. The formin homology 1 (FH1) pathway involves transfer of profilin-bound actin to the barbed end from polyproline tracts located in the disordered FH1 domains. Here, we used a total internal reflection fluorescence (TIRF) microscopy-based fluorescence approach to determine the fraction of actin subunits incorporated via the FH1 and FH2 pathways during filament elongation mediated by two formins. We found that the fraction of filament elongation that occurs via each pathway directly depends on the efficiency of the other pathway, indicating that these two pathways compete with each other for subunit addition by formins. 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| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central; Alma/SFX Local Collection |
| subjects | Actins - metabolism Animals Carboxylic Acids - chemistry Cell Cycle Proteins - metabolism Chickens Cytoskeletal Proteins - metabolism Fluorescence Fluorescent Dyes - chemistry Microfilament Proteins - metabolism Microscopy, Fluorescence Molecular Biophysics Profilins - metabolism Protein Binding Protein Domains Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins - metabolism Schizosaccharomyces Schizosaccharomyces pombe Proteins - metabolism |
| title | Dissection of two parallel pathways for formin-mediated actin filament elongation |
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