Danio rerio αE-catenin Is a Monomeric F-actin Binding Protein with Distinct Properties from Mus musculus αE-catenin

It is unknown whether homologs of the cadherin·catenin complex have conserved structures and functions across the Metazoa. Mammalian αE-catenin is an allosterically regulated actin-binding protein that binds the cadherin·β-catenin complex as a monomer and whose dimerization potentiates F-actin assoc...

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Veröffentlicht in:The Journal of biological chemistry 2013-08, Vol.288 (31), p.22324-22332
Hauptverfasser: Miller, Phillip W., Pokutta, Sabine, Ghosh, Agnidipta, Almo, Steven C., Weis, William I., Nelson, W. James, Kwiatkowski, Adam V.
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container_end_page 22332
container_issue 31
container_start_page 22324
container_title The Journal of biological chemistry
container_volume 288
creator Miller, Phillip W.
Pokutta, Sabine
Ghosh, Agnidipta
Almo, Steven C.
Weis, William I.
Nelson, W. James
Kwiatkowski, Adam V.
description It is unknown whether homologs of the cadherin·catenin complex have conserved structures and functions across the Metazoa. Mammalian αE-catenin is an allosterically regulated actin-binding protein that binds the cadherin·β-catenin complex as a monomer and whose dimerization potentiates F-actin association. We tested whether these functional properties are conserved in another vertebrate, the zebrafish Danio rerio. Here we show, despite 90% sequence identity, that Danio rerio and Mus musculus αE-catenin have striking functional differences. We demonstrate that D. rerio αE-catenin is monomeric by size exclusion chromatography, native PAGE, and small angle x-ray scattering. D. rerio αE-catenin binds F-actin in cosedimentation assays as a monomer and as an α/β-catenin heterodimer complex. D. rerio αE-catenin also bundles F-actin, as shown by negative stained transmission electron microscopy, and does not inhibit Arp2/3 complex-mediated actin nucleation in bulk polymerization assays. Thus, core properties of α-catenin function, F-actin and β-catenin binding, are conserved between mouse and zebrafish. We speculate that unique regulatory properties have evolved to match specific developmental requirements. Background: Mammalian αE-catenin is an allosterically regulated F-actin binding protein that inhibits the Arp2/3 complex. Results:D. rerio αE-catenin is a monomer that binds β-catenin and F-actin simultaneously but does not inhibit the Arp2/3 complex. Conclusion:D. rerio αE-catenin directly links the cadherin-catenin complex to F-actin. Significance: Core functions but not regulatory properties are conserved between α-catenin orthologs.
doi_str_mv 10.1074/jbc.M113.458406
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James ; Kwiatkowski, Adam V.</creator><creatorcontrib>Miller, Phillip W. ; Pokutta, Sabine ; Ghosh, Agnidipta ; Almo, Steven C. ; Weis, William I. ; Nelson, W. James ; Kwiatkowski, Adam V.</creatorcontrib><description>It is unknown whether homologs of the cadherin·catenin complex have conserved structures and functions across the Metazoa. Mammalian αE-catenin is an allosterically regulated actin-binding protein that binds the cadherin·β-catenin complex as a monomer and whose dimerization potentiates F-actin association. We tested whether these functional properties are conserved in another vertebrate, the zebrafish Danio rerio. Here we show, despite 90% sequence identity, that Danio rerio and Mus musculus αE-catenin have striking functional differences. We demonstrate that D. rerio αE-catenin is monomeric by size exclusion chromatography, native PAGE, and small angle x-ray scattering. D. rerio αE-catenin binds F-actin in cosedimentation assays as a monomer and as an α/β-catenin heterodimer complex. D. rerio αE-catenin also bundles F-actin, as shown by negative stained transmission electron microscopy, and does not inhibit Arp2/3 complex-mediated actin nucleation in bulk polymerization assays. Thus, core properties of α-catenin function, F-actin and β-catenin binding, are conserved between mouse and zebrafish. We speculate that unique regulatory properties have evolved to match specific developmental requirements. Background: Mammalian αE-catenin is an allosterically regulated F-actin binding protein that inhibits the Arp2/3 complex. Results:D. rerio αE-catenin is a monomer that binds β-catenin and F-actin simultaneously but does not inhibit the Arp2/3 complex. Conclusion:D. rerio αE-catenin directly links the cadherin-catenin complex to F-actin. 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D. rerio αE-catenin binds F-actin in cosedimentation assays as a monomer and as an α/β-catenin heterodimer complex. D. rerio αE-catenin also bundles F-actin, as shown by negative stained transmission electron microscopy, and does not inhibit Arp2/3 complex-mediated actin nucleation in bulk polymerization assays. Thus, core properties of α-catenin function, F-actin and β-catenin binding, are conserved between mouse and zebrafish. We speculate that unique regulatory properties have evolved to match specific developmental requirements. Background: Mammalian αE-catenin is an allosterically regulated F-actin binding protein that inhibits the Arp2/3 complex. Results:D. rerio αE-catenin is a monomer that binds β-catenin and F-actin simultaneously but does not inhibit the Arp2/3 complex. Conclusion:D. rerio αE-catenin directly links the cadherin-catenin complex to F-actin. 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Results:D. rerio αE-catenin is a monomer that binds β-catenin and F-actin simultaneously but does not inhibit the Arp2/3 complex. Conclusion:D. rerio αE-catenin directly links the cadherin-catenin complex to F-actin. Significance: Core functions but not regulatory properties are conserved between α-catenin orthologs.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23788645</pmid><doi>10.1074/jbc.M113.458406</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record>
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subjects Actin
Adherens Junction
alpha Catenin - metabolism
Animals
Carrier Proteins - metabolism
Catenin
Cell Adhesion
Cell Biology
Chromatography, Gel
Mice
Microfilament Proteins - metabolism
Native Polyacrylamide Gel Electrophoresis
Protein Binding
Protein Evolution
Scattering, Radiation
Zebrafish
title Danio rerio αE-catenin Is a Monomeric F-actin Binding Protein with Distinct Properties from Mus musculus αE-catenin
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