Abstract
Here we describe the identification of a novel 37-kD actin monomer binding protein in budding yeast. This protein, which we named twinfilin, is composed of two cofilin-like regions. In our sequence database searches we also identified human, mouse, and Caenorhabditis elegans homologues of yeast twinfilin, suggesting that twinfilins form an evolutionarily conserved family of actin-binding proteins. Purified recombinant twinfilin prevents actin filament assembly by forming a 1:1 complex with actin monomers, and inhibits the nucleotide exchange reaction of actin monomers. Despite the sequence homology with the actin filament depolymerizing cofilin/actin-depolymerizing factor (ADF) proteins, our data suggests that twinfilin does not induce actin filament depolymerization. In yeast cells, a green fluorescent protein (GFP)-twinfilin fusion protein localizes primarily to cytoplasm, but also to cortical actin patches. Overexpression of the twinfilin gene (TWF1) results in depolarization of the cortical actin patches. A twf1 null mutation appears to result in increased assembly of cortical actin structures and is synthetically lethal with the yeast cofilin mutant cof1-22, shown previously to cause pronounced reduction in turnover of cortical actin filaments. Taken together, these results demonstrate that twinfilin is a novel, highly conserved actin monomer-sequestering protein involved in regulation of the cortical actin cytoskeleton.
MeSH Terms
Actin Depolymerizing Factors
Actins/metabolism,physiology
Amino Acid Sequence
Binding, Competitive
Cytoplasm/metabolism
Cytoskeleton/chemistry,physiology
Fungal Proteins/genetics,isolation & purification,physiology
Gene Deletion
Green Fluorescent Proteins
Humans
Luminescent Proteins
Microfilament Proteins/genetics,isolation & purification,metabolism,physiology
Molecular Sequence Data
Protein-Tyrosine Kinases
Recombinant Fusion Proteins/metabolism
Saccharomyces cerevisiae/chemistry,genetics,physiology
Saccharomyces cerevisiae Proteins
Sequence Homology, Amino Acid
Chemicals
Actin Depolymerizing Factors
Actins
Fungal Proteins
Luminescent Proteins
Microfilament Proteins
Ptk9 protein, mouse
Recombinant Fusion Proteins
Saccharomyces cerevisiae Proteins
TWF1 protein, S cerevisiae
TWF1 protein, human
Green Fluorescent Proteins
Protein-Tyrosine Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Goode B L
Department of Molecular and Cell Biology, University of California, Berkeley, California 94720-3202, USA.
Drubin D G
Lappalainen P
References (30)
30 references, click to expand
-
Movement of cortical actin patches in yeast.
J Cell Biol. 1996 Mar;132(5):861-70
PMID: 8603918
-
The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics.
Mol Biol Cell. 1995 Nov;6(11):1423-31
PMID: 8589446
-
Role of nucleotide exchange and hydrolysis in the function of profilin in action assembly.
J Biol Chem. 1996 May 24;271(21):12302-9
PMID: 8647830
-
T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli.
Anal Biochem. 1996 May 1;236(2):371-3
PMID: 8660525
-
Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes.
Nature. 1997 Jan 16;385(6613):265-9
PMID: 9000076
-
A role for the actin cytoskeleton of Saccharomyces cerevisiae in bipolar bud-site selection.
J Cell Biol. 1997 Jan 13;136(1):111-23
PMID: 9008707
-
Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility.
J Cell Biol. 1997 Mar 24;136(6):1307-22
PMID: 9087445
-
Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails.
J Cell Biol. 1997 Mar 24;136(6):1323-32
PMID: 9087446
-
Structure determination of yeast cofilin.
Nat Struct Biol. 1997 May;4(5):366-9
PMID: 9145106
-
Cofilin promotes rapid actin filament turnover in vivo.
Nature. 1997 Jul 3;388(6637):78-82
PMID: 9214506
-
Control of actin dynamics in cell motility.
J Mol Biol. 1997 Jun 20;269(4):459-67
PMID: 9217250
-
Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis.
EMBO J. 1997 Sep 15;16(18):5520-30
PMID: 9312011
-
Structure of the profilin-poly-L-proline complex involved in morphogenesis and cytoskeletal regulation.
Nat Struct Biol. 1997 Nov;4(11):953-60
PMID: 9360613
-
The ADF homology (ADF-H) domain: a highly exploited actin-binding module.
Mol Biol Cell. 1998 Aug;9(8):1951-9
PMID: 9693358
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Opposite effects of cofilin and profilin from porcine brain on rate of exchange of actin-bound adenosine 5'-triphosphate.
Biochemistry. 1985 Feb 26;24(5):1160-4
PMID: 4096896
-
An electrophoretic procedure for detecting proteins that bind actin monomers.
Anal Biochem. 1989 Apr;178(1):32-7
PMID: 2543235
-
A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
Genetics. 1989 May;122(1):19-27
PMID: 2659436
-
Yeast endocytosis assays.
Methods Enzymol. 1991;194:697-710
PMID: 2005817
-
Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae.
J Cell Biol. 1993 Aug;122(3):635-44
PMID: 8335689
-
A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae.
Nucleic Acids Res. 1993 Jul 11;21(14):3329-30
PMID: 8341614
-
How profilin promotes actin filament assembly in the presence of thymosin beta 4.
Cell. 1993 Dec 3;75(5):1007-14
PMID: 8252614
-
Prokaryotic expression cloning of a novel human tyrosine kinase.
Mol Cell Biol. 1994 Feb;14(2):982-8
PMID: 7507208
-
Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site.
Mol Biol Cell. 1993 Dec;4(12):1277-94
PMID: 8167410
-
Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose.
J Cell Biol. 1994 Oct;127(1):107-15
PMID: 7929556
-
An actin monomer binding activity localizes to the carboxyl-terminal half of the Saccharomyces cerevisiae cyclase-associated protein.
J Biol Chem. 1995 Mar 10;270(10):5680-5
PMID: 7890691
-
Patterns of bud-site selection in the yeast Saccharomyces cerevisiae.
J Cell Biol. 1995 May;129(3):751-65
PMID: 7730409
-
Actin monomer binding proteins.
Curr Opin Cell Biol. 1995 Feb;7(1):102-10
PMID: 7755981
-
Capping protein levels influence actin assembly and cell motility in dictyostelium.
Cell. 1995 May 19;81(4):591-600
PMID: 7758113
-
Movement of yeast cortical actin cytoskeleton visualized in vivo.
Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3886-91
PMID: 8632984