Native cyclase-associated protein and actin from Xenopus laevis oocytes form a unique 4:4 complex with a tripartite structure

Abstract

Cyclase-associated protein (CAP) is a conserved actin-binding protein that regulates multiple aspects of actin dynamics, including polymerization, depolymerization, filament severing, and nucleotide exchange. CAP has been isolated from different cells and tissues in an equimolar complex with actin, and previous studies have shown that a CAP–actin complex contains six molecules each of CAP and actin. Intriguingly, here, we successfully isolated a complex of Xenopus cyclase-associated protein 1 (XCAP1) with actin from oocyte extracts, which contained only four molecules each of XCAP1 and actin. This XCAP1–actin complex remained stable as a single population of 340 kDa species during hydrodynamic analyses using gel filtration or analytical ultracentrifugation. Examination of the XCAP1–actin complex by high-speed atomic force microscopy revealed a tripartite structure: one middle globular domain and two globular arms. The two arms were observed in high and low states. The arms at the high state were spontaneously converted to the low state by dissociation of actin from the complex. However, when extra G-actin was added, the arms at the low state were converted to the high state. Based on the known structures of the N-terminal helical-folded domain and C-terminal CARP domain, we hypothesize that the middle globular domain corresponds to a tetramer of the N-terminal helical-folded domain of XCAP1 and that each arm in the high state corresponds to a heterotetramer containing a dimer of the C-terminal CARP domain of XCAP1 and two G-actin molecules. This novel configuration of a CAP–actin complex should help to understand how CAP promotes actin filament disassembly. Cyclase-associated protein (CAP) is a conserved actin-binding protein that regulates multiple aspects of actin dynamics, including polymerization, depolymerization, filament severing, and nucleotide exchange. CAP has been isolated from different cells and tissues in an equimolar complex with actin, and previous studies have shown that a CAP–actin complex contains six molecules each of CAP and actin. Intriguingly, here, we successfully isolated a complex of Xenopus cyclase-associated protein 1 (XCAP1) with actin from oocyte extracts, which contained only four molecules each of XCAP1 and actin. This XCAP1–actin complex remained stable as a single population of 340 kDa species during hydrodynamic analyses using gel filtration or analytical ultracentrifugation. Examination of the XCAP1–actin complex by high-speed atomic force microscopy revealed a tripartite structure: one middle globular domain and two globular arms. The two arms were observed in high and low states. The arms at the high state were spontaneously converted to the low state by dissociation of actin from the complex. However, when extra G-actin was added, the arms at the low state were converted to the high state. Based on the known structures of the N-terminal helical-folded domain and C-terminal CARP domain, we hypothesize that the middle globular domain corresponds to a tetramer of the N-terminal helical-folded domain of XCAP1 and that each arm in the high state corresponds to a heterotetramer containing a dimer of the C-terminal CARP domain of XCAP1 and two G-actin molecules. This novel configuration of a CAP–actin complex should help to understand how CAP promotes actin filament disassembly. Regulated assembly and disassembly of actin filaments are vital to the diverse function of the actin cytoskeleton (1Pollard T.D. Cooper J.A. Actin, a central player in cell shape and movement.Science. 2009; 326: 1208-1212Crossref PubMed Scopus (1265) Google Scholar). Cyclase-associated protein (CAP) is one of the actin-regulatory proteins that control multiple key aspects of actin filament dynamics (2Ono S. The role of cyclase-associated protein in regulating actin filament dynamics - more than a monomer-sequestration factor.J. Cell Sci. 2013; 126: 3249-3258Crossref PubMed Scopus (73) Google Scholar, 3Rust M.B. Khudayberdiev S. Pelucchi S. Marcello E. CAPt’n of actin dynamics: Recent advances in the molecular, developmental and physiological functions of cyclase-associated protein (CAP).Front. Cell Dev. Biol. 2020; 8: 586631Crossref PubMed Scopus (7) Google Scholar). CAP was originally identified in yeast as a protein that binds to adenylyl cyclase and is involved in the Ras signaling pathway (4Field J. Vojtek A. Ballester R. Bolger G. Colicelli J. Ferguson K. Gerst J. Kataoka T. Michaeli T. Powers S. Riggs M. Rodgers L. Wieland I. Wheland B. Wigler M. Cloning and characterization of CAP, the S. cerevisiae gene encoding the 70 kd adenylyl cyclase-associated protein.Cell. 1990; 61: 319-327Abstract Full Text PDF PubMed Scopus (179) Google Scholar, 5Fedor-Chaiken M. Deschenes R.J. Broach J.R. SRV2, a gene required for RAS activation of adenylate cyclase in yeast.Cell. 1990; 61: 329-340Abstract Full Text PDF PubMed Scopus (189) Google Scholar). However, CAP was later recognized as an actin-binding protein in a variety of eukaryotes. CAP binds to actin monomers and inhibits polymerization (6Freeman N.L. Chen Z. Horenstein J. Weber A. Field J. An actin monomer binding activity localizes to the carboxyl-terminal half of the Saccharomyces cerevisiae cyclase-associated protein.J. Biol. Chem. 1995; 270: 5680-5685Abstract Full Text Full Text PDF PubMed Scopus (113) Google Scholar). CAP also promotes exchange of actin-bound nucleotides in competition with cofilin and increases ATP-bound actin monomers that are readily available for polymerization (7Moriyama K. Yahara I. Human CAP1 is a key factor in the recycling of cofilin and actin for rapid actin turnover.J. Cell Sci. 2002; 115: 1591-1601Crossref PubMed Google Scholar, 8Balcer H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar, 9Nomura K. Ono S. ATP-dependent regulation of actin monomer-filament equilibrium by cyclase-associated protein and ADF/cofilin.Biochem. J. 2013; 453: 249-259Crossref PubMed Scopus (16) Google Scholar). In addition, CAP and cofilin interact with actin filaments to enhance severing (10Chaudhry F. Breitsprecher D. Little K. Sharov G. Sokolova O. Goode B.L. Srv2/cyclase-associated protein forms hexameric shurikens that directly catalyze actin filament severing by cofilin.Mol. Biol. Cell. 2013; 24: 31-41Crossref PubMed Scopus (68) Google Scholar, 11Normoyle K.P. Brieher W.M. Cyclase-associated protein (CAP) acts directly on F-actin to accelerate cofilin-mediated actin severing across the range of physiological pH.J. Biol. Chem. 2012; 287: 35722-35732Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar) and monomer dissociation from the pointed ends (12Kotila T. Wioland H. Enkavi G. Kogan K. Vattulainen I. Jegou A. Romet-Lemonne G. Lappalainen P. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin.Nat. Comm. 2019; 10: 5320Crossref PubMed Scopus (35) Google Scholar, 13Shekhar S. Chung J. Kondev J. Gelles J. Goode B.L. Synergy between cyclase-associated protein and cofilin accelerates actin filament depolymerization by two orders of magnitude.Nat. Comm. 2019; 10: 5319Crossref PubMed Scopus (25) Google Scholar). A combination of CAP and twinfilin also enhances actin monomer dissociation from filament ends (14Johnston A.B. Collins A. Goode B.L. High-speed depolymerization at actin filament ends jointly catalysed by twinfilin and Srv2/CAP.Nat. Cell Biol. 2015; 17: 1504-1511Crossref PubMed Scopus (69) Google Scholar, 15Hilton D.M. Aguilar R.M. Johnston A.B. Goode B.L. Species-specific functions of twinfilin in actin filament depolymerization.J. Mol. Biol. 2018; 430: 3323-3336Crossref PubMed Scopus (21) Google Scholar). CAP is involved in a number of cellular events that require actin remodeling in various cell types and tissues. For example, CAP is essential for muscle sarcomere organization in Caenorhabditis elegans (16Nomura K. Ono K. Ono S. CAS-1, a C. elegans cyclase-associated protein, is required for sarcomeric actin assembly in striated muscle.J. Cell Sci. 2012; 125: 4077-4089Crossref PubMed Scopus (20) Google Scholar) and mice F. T. C. A. M.B. actin cytoskeleton and muscle and Sci. S. A. 2019; PubMed Scopus Google and of a CAP in mice S. M. H. R. M. G. I. A.A. cyclase-associated protein is a Mol. Sci. PubMed Scopus Google Scholar, J. M. F. M. T. M. Chung in and 2015; PubMed Scopus (21) Google Scholar) and L. A. S. H. L. R. R. to actin dynamics and with and 2019; PubMed Scopus (16) Google Scholar). Intriguingly, when CAP is isolated from tissues or actin is with CAP in a complex at an equimolar and CAP as was isolated from as a complex with actin, and actin was from CAP by R. K. a actin protein from with to CAP, an adenylate cyclase-associated protein from PubMed Scopus Google Scholar). CAP–actin complex has been isolated from yeast H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google K.P. Brieher W.M. Cyclase-associated protein (CAP) acts directly on F-actin to accelerate cofilin-mediated actin severing across the range of physiological pH.J. Biol. Chem. 2012; 287: 35722-35732Abstract Full Text Full Text PDF PubMed Scopus (51) Google and A. R. A complex containing actin inhibits the Cell Biol. 2019; PubMed Scopus Google Scholar). The CAP–actin complex promotes actin filament disassembly in the of cofilin H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar, 11Normoyle K.P. Brieher W.M. Cyclase-associated protein (CAP) acts directly on F-actin to accelerate cofilin-mediated actin severing across the range of physiological pH.J. Biol. Chem. 2012; 287: 35722-35732Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar). In addition, studies have shown that the CAP–actin complex containing actin is an of A. R. A complex containing actin inhibits the Cell Biol. 2019; PubMed Scopus Google Scholar, A. T. T. Z. of actin polymerization of actin Sci. S. A. 2020; PubMed Scopus Google Scholar). the CAP and actin have functions as a complex, how the complex is and the complex is for functions The complex of yeast CAP known as and actin is a complex of kDa H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google which from O. E. L. F. M. Lappalainen P. Goode B.L. and of the Srv2/CAP for and binding in actin turnover.J. Biol. Chem. 2009; Full Text Full Text PDF PubMed Scopus (51) Google Scholar). The CAP–actin complex from is also in a A. R. A complex containing actin inhibits the Cell Biol. 2019; PubMed Scopus Google Scholar). The N-terminal half of yeast and a hexameric which is by of a at the (10Chaudhry F. Breitsprecher D. Little K. Sharov G. Sokolova O. Goode B.L. Srv2/cyclase-associated protein forms hexameric shurikens that directly catalyze actin filament severing by cofilin.Mol. Biol. Cell. 2013; 24: 31-41Crossref PubMed Scopus (68) Google Scholar, S. Collins A. L. Sokolova O. Goode B.L. and of cyclase-associated protein in regulating actin Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar) and of the helical-folded domain (12Kotila T. Wioland H. Enkavi G. Kogan K. Vattulainen I. Jegou A. Romet-Lemonne G. Lappalainen P. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin.Nat. Comm. 2019; 10: 5320Crossref PubMed Scopus (35) Google Scholar, A. A. for of the N-terminal domain of cyclase-associated protein PubMed Scopus Google Scholar, E. A.A. M. A. Mechanism of of cyclase-associated protein from in Mol. Biol. PubMed Scopus (7) Google Scholar). The C-terminal half of CAP contains a CAP and protein domain that the C-terminal T. A.A. M. L. E. E. T. A. of the actin binding domain of the cyclase-associated PubMed Scopus Google Scholar, S. Ono S. The C-terminal of cyclase-associated protein is essential for actin monomer J. PubMed Scopus (7) Google Scholar). The CARP domain of CAP binds to actin monomer (6Freeman N.L. Chen Z. Horenstein J. Weber A. Field J. An actin monomer binding activity localizes to the carboxyl-terminal half of the Saccharomyces cerevisiae cyclase-associated protein.J. Biol. Chem. 1995; 270: 5680-5685Abstract Full Text Full Text PDF PubMed Scopus (113) Google Scholar, O. Kugler J. Lappalainen P. Goode B.L. A with monomers the and in function of Srv2/cyclase-associated Biol. Cell. PubMed Scopus Google Scholar, S. Ono S. in the domain of cyclase-associated protein are involved in actin monomer Scopus Google Scholar, M. E. J. Lappalainen P. and cyclase-associated proteins catalyze nucleotide exchange on G-actin a conserved Biol. Chem. 2013; Full Text Full Text PDF PubMed Scopus Google and a CARP dimer and two actin molecules a globular T. Kogan K. Enkavi G. S. Vattulainen I. Goode B.L. Lappalainen P. of actin monomer by cyclase-associated Comm. 2018; PubMed Scopus Google Scholar). we structures of of the CAP–actin complex, we have on the of the complex. a has that the N-terminal of CAP1 and of F. E. the of cyclase-associated proteins 1 and to actin severing by J. Mol. Sci. 2019; Scopus Google Scholar). the configuration is conserved CAP–actin from different In we a complex of Xenopus CAP1 and actin and that the complex contained the two proteins in a which is a novel configuration of the CAP–actin complex. a complex of CAP and actin from Xenopus oocyte Xenopus oocyte were to a in which Xenopus was proteins to the as K. T. H. A Xenopus of yeast actin protein 1 which disassembly of actin filaments with Cell Sci. PubMed Google Scholar) that the and proteins were Xenopus protein 1 actin, and K. T. H. A Xenopus of yeast actin protein 1 which disassembly of actin filaments with Cell Sci. PubMed Google Scholar). identified that the and proteins were T. J.A. J. regulating actin assembly in and of Xenopus is the actin-binding protein.J. Cell Biol. PubMed Scopus Google Scholar) and cyclase-associated protein 1 (XCAP1) F. CAP1 is in Dev. 2002; PubMed Scopus Google to XCAP1 using by XCAP1 and actin were during and were in an equimolar gel filtration using also in of XCAP1 and actin in a single at kDa which is than XCAP1 or actin or a complex, that a stable complex. of the XCAP1–actin complex was more by two different with and analytical ultracentrifugation. In the XCAP1–actin complex was as a single with a of 340 kDa were that to XCAP1 or actin, that the XCAP1–actin complex was stable during the in analytical the XCAP1–actin complex was as a single of kDa which with the of the of XCAP1 and actin the of the XCAP1–actin complex with that of a complex of The was than the This to dissociation of the complex during the which is a known in of E. of of proteins in of an and in a 10: Google Scholar). are known to to actin the XCAP1–actin complex contains that the XCAP1 and G-actin a stable complex at a of the XCAP1–actin complex in state was by high-speed atomic force microscopy and on that the complex of globular which we as the middle globular domain shown in in and two arms 1 and shown in or in The of was and and remained stable during A and the two arms were observed in two different a high state shown in in and a low state shown in in also The of was and that of was and and In the arms from to A and at or from to A and at that or dissociation of a during the of that was converted to by dissociation of actin to by the and of the complex on the of the the by and the of was XCAP1–actin complex with arms in a low state is of the XCAP1–actin complex containing arms in on a was with was of the of globular analyses of and at the on the in A. of and and single of and as in the of the between the at of the between two arms and between and one of the arms and single as in the The two arms were when were in of and as the arms were to by The between the of the two arms in in a range with an of and the of between and each However, arms were converted from to were in remained and The between two arms that between each arm and that was by to the how the of the XCAP1–actin complex, we a that was with which to the and of the two arms were in the low state with the of The and shape of were between and and The between the two arms remained at and which is than that of two arms in on that the two arms were on the and the between and an arm remained on the and in a to and on the that of the XCAP1–actin complex a to by dissociation of an which we hypothesize to the of the arms is to G-actin dissociation and we of on the XCAP1–actin complex of the XCAP1–actin complex contained However, of were converted to of the arms were converted to was added, and of the complex were observed and In the of and of the arms between and were observed In the shown in arms were at one arm was converted to at and arm was converted to at from to were also observed at and at A of events that the between and was and at each arm between the two arms a single complex. The of events from to in the of was in the of of to was observed at a of to of G-actin to the complex, which is with the from to as in In the of or in the of the XCAP1–actin complex and that the of or were observed that G-actin is a of the two arm of the XCAP1–actin complex. Based on known and of CAP from we a for the of the XCAP1–actin complex, which is in the of two and a hypothesize that corresponds to a tetramer of the of XCAP1 and that each arm domain in the high state corresponds to a heterotetramer containing a dimer of the CARP domain of XCAP1 and two G-actin molecules The of CAP by forms a dimer (12Kotila T. Wioland H. Enkavi G. Kogan K. Vattulainen I. Jegou A. Romet-Lemonne G. Lappalainen P. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin.Nat. Comm. 2019; 10: 5320Crossref PubMed Scopus (35) Google Scholar, A. A. for of the N-terminal domain of cyclase-associated protein PubMed Scopus Google Scholar, E. A.A. M. A. Mechanism of of cyclase-associated protein from in Mol. Biol. PubMed Scopus (7) Google and the N-terminal forms a and of a tetramer F. E. the of cyclase-associated proteins 1 and to actin severing by J. Mol. Sci. 2019; Scopus Google Scholar) or (10Chaudhry F. Breitsprecher D. Little K. Sharov G. Sokolova O. Goode B.L. Srv2/cyclase-associated protein forms hexameric shurikens that directly catalyze actin filament severing by cofilin.Mol. Biol. Cell. 2013; 24: 31-41Crossref PubMed Scopus (68) Google Scholar, O. E. L. F. M. Lappalainen P. Goode B.L. and of the Srv2/CAP for and binding in actin turnover.J. Biol. Chem. 2009; Full Text Full Text PDF PubMed Scopus (51) Google Scholar, S. Collins A. L. Sokolova O. Goode B.L. and of cyclase-associated protein in regulating actin Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar) of the The of and with that of the of one (12Kotila T. Wioland H. Enkavi G. Kogan K. Vattulainen I. Jegou A. Romet-Lemonne G. Lappalainen P. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin.Nat. Comm. 2019; 10: 5320Crossref PubMed Scopus (35) Google Scholar, A. A. for of the N-terminal domain of cyclase-associated protein PubMed Scopus Google that each is to the the C-terminal of the CARP domain T. A.A. M. L. E. E. T. A. of the actin binding domain of the cyclase-associated PubMed Scopus Google which binds to two G-actin molecules T. Kogan K. Enkavi G. S. Vattulainen I. Goode B.L. Lappalainen P. of actin monomer by cyclase-associated Comm. 2018; PubMed Scopus Google Scholar). the of with the of the heterotetramer of CARP and G-actin T. Kogan K. Enkavi G. S. Vattulainen I. Goode B.L. Lappalainen P. of actin monomer by cyclase-associated Comm. 2018; PubMed Scopus Google Scholar). the between and is by and dissociation of G-actin that G-actin is a of and as a between and CARP of CAP binds to G-actin M. E. J. Lappalainen P. and cyclase-associated proteins catalyze nucleotide exchange on G-actin a conserved Biol. Chem. 2013; Full Text Full Text PDF PubMed Scopus Google Scholar, F. Little K. L. O. Goode B.L. A central role for the domain of Srv2/CAP in actin monomers to actin turnover in and in Google dissociation of from G-actin of the with of CAP also binds to the N-terminal domain of A. T. T. Z. of actin polymerization of actin Sci. S. A. 2020; PubMed Scopus Google Scholar). of in the CAP–actin complex should with This of the XCAP1–actin complex to by at or of using The configuration of the XCAP1–actin complex in a is different from of CAP–actin from different in a H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar, O. E. L. F. M. Lappalainen P. Goode B.L. and of the Srv2/CAP for and binding in actin turnover.J. Biol. Chem. 2009; Full Text Full Text PDF PubMed Scopus (51) Google Scholar). is that the tripartite of the XCAP1–actin complex is to one of the microscopy of yeast complex 1 of H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google However, the yeast complex is a complex containing Srv2/CAP and actin in a of H.I. Goodman A.L. Rodal A.A. Smith E. Kugler J. Heuser J.E. Goode B.L. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1.Curr. Biol. 2003; 13: 2159-2169Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar). a an variety of the complex assembly or in the analyses or studies are to the XCAP1–actin complex with a configuration from XCAP1 and which should of and that are required for assembly of the XCAP1–actin complex. of the CAP–actin complex the actin-binding of that two of the four interact with two actin at the pointed end of a filament to accelerate depolymerization (12Kotila T. Wioland H. Enkavi G. Kogan K. Vattulainen I. Jegou A. Romet-Lemonne G. Lappalainen P. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin.Nat. Comm. 2019; 10: 5320Crossref PubMed Scopus (35) Google Scholar, 13Shekhar S. Chung J. Kondev J. Gelles J. Goode B.L. Synergy between cyclase-associated protein and cofilin accelerates actin filament depolymerization by two orders of magnitude.Nat. Comm. 2019; 10: 5319Crossref PubMed Scopus (25) Google Scholar). two to interact with actin at the pointed that CAP to a filament and actin filaments from the pointed CAP binds to the pointed end of actin filaments with a of to (12Kotila T. Wioland H. Enkavi G. Kogan K. Vattulainen I. Jegou A. Romet-Lemonne G. Lappalainen P. Mechanism of synergistic actin filament pointed end depolymerization by cyclase-associated protein and cofilin.Nat. Comm. 2019; 10: 5320Crossref PubMed Scopus (35) Google Scholar, 13Shekhar S. Chung J. Kondev J. Gelles J. Goode B.L. Synergy between cyclase-associated protein and cofilin accelerates actin filament depolymerization by two orders of magnitude.Nat. Comm. 2019; 10: 5319Crossref PubMed Scopus (25) Google the of actin depolymerization to In addition, the CARP domain, which has nucleotide exchange is in and available to and rapid to to binding of proteins to or in the A. T. T. Z. of actin polymerization of actin Sci. S. A. 2020; PubMed Scopus Google Scholar, E. O. Goode B.L. Lappalainen P. Mechanism and role of Cell Sci. PubMed Scopus Google Scholar, N.L. T. Chen Z. R. Field J. A conserved of the Saccharomyces cerevisiae cyclase-associated protein binds and Cell. Biol. PubMed Scopus Google Scholar, T. for and two Saccharomyces cerevisiae domain an adenylyl cyclase-associated protein and the actin Biol. Cell. 8: PubMed Scopus Google Scholar) or of CAP H. H. P. Field J. of the protein CAP1 with cofilin and Cell Sci. PubMed Scopus Google Scholar, H. A. J. T. Ono S. and of cyclase-associated protein 1 by signaling and are for the protein functions in actin filament disassembly and cell Cell. Biol. 2020; PubMed Scopus Google Scholar) the and function of the CAP–actin complex. the function of CAP in the regulation of actin from were and to an in which Xenopus been as K. T. H. A Xenopus of yeast actin protein 1 which disassembly of actin filaments with Cell Sci. PubMed Google Scholar). to the were with 1 1 and The was with at The by were and and to a with the and with a of to The containing XCAP1–actin complex were directly to a with and with the XCAP1–actin complex was with a of to at XCAP1–actin complex was by with and 1 and were by a with an analytical were from an that was at containing was in a was using a from a and a were The were using and and the from was to of the as as hydrodynamic were with were using a analytical using a of at were by the of the at using a of a of a of and of were using P. of by and J. Full Text Full Text PDF PubMed Scopus Google Scholar) and B. for the and of and equilibrium with Sci. PubMed Scopus Google Scholar). analyses were by at The and were was as from muscle as by and J.A. of muscle PubMed Scopus Google Scholar) and converted to as by T.D. I. and of filaments from and Biol. Chem. Full Text PDF PubMed Google Scholar) by containing was in at using a T. E. D. K. A. A high-speed atomic force for Sci. S. A. PubMed Scopus Google Scholar, T. T. T. High-speed atomic force microscopy for of Sci. Scopus Google as T. T. to of dynamics and of proteins by high-speed atomic force 2012; PubMed Scopus Google Scholar). In a with a in and in to the by was the of a by a of or M. H. S. T. T. O. and dynamics of by high-speed atomic force 8: PubMed Scopus Google Scholar) was as a a of protein 1 with A was for the was with of A and in A. was in a using in in The was on the end of a using and was using a an and for The and were at and The and for each are in the were and using the E. T. in actin filaments revealed by high-speed atomic force 2015; Scopus Google Scholar). In a to and a to the were to The and of the each domain were using the the was the was by a the A of the CAP–actin complex was using and using are contained in the are available from S. O. This contains The of for in to the at the H. for and at the of for the of and for and analyses at the H. and S. O. and the P. D. and for of the This was by from to to and the of to S. O. S. O. is a of a The is the of the and the of the of

Topics & Concepts