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PMID: 8034743 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mapping actin surfaces required for functional interactions in vivo.

The Journal of cell biology ·Vol. 126 ·No. 2 ·1994-07-00 ·Pages 423-32

Holtzman DA, Wertman KF, Drubin DG

Abstract

An in vivo strategy to identify amino acids of actin required for functional interactions with actin-binding proteins was developed. This approach is based on the assumption that an actin mutation that specifically impairs the interaction with an actin-binding protein will cause a phenotype similar to a null mutation in the gene that encodes the actin-binding protein. 21 actin mutations were analyzed in budding yeast, and specific regions of actin subdomain 1 were implicated in the interaction with fimbrin, an actin filament-bundling protein. Mutations in this actin subdomain were shown to be, like a null allele of the yeast fimbrin gene (SAC6), lethal in combination with null mutations in the ABP1 and SLA2 genes, and viable in combination with a null mutation in the SLA1 gene. Biochemical experiments with act1-120 actin (E99A, E100A) verified a defect in the fimbrin-actin interaction. Genetic interactions between mutant alleles of the yeast actin gene and null alleles of the SAC6, ABP1, SLA1, and SLA2 genes also demonstrated that the effects of the 21 actin mutations are diverse and allowed four out of seven pseudo-wild-type actin alleles to be distinguished from the wild-type gene for the first time, providing evidence for functional redundancy between different surfaces of actin.

Related Genes
MeSH Terms
Actin Depolymerizing Factors Actins/genetics,isolation & purification,metabolism,ultrastructure Binding Sites Carrier Proteins/genetics Cytoskeletal Proteins Fungal Proteins/genetics,metabolism Genes, Fungal/genetics Genes, Lethal Membrane Glycoproteins/genetics,metabolism Microfilament Proteins/genetics,metabolism Models, Molecular Mutation Nerve Tissue Proteins/metabolism Phenotype Saccharomyces cerevisiae Proteins Suppression, Genetic/genetics Yeasts/genetics
Chemicals
ABP1 protein, S cerevisiae Actin Depolymerizing Factors Actins Carrier Proteins Cytoskeletal Proteins Fungal Proteins Membrane Glycoproteins Microfilament Proteins Nerve Tissue Proteins SLA1 protein, S cerevisiae SLA2 protein, S cerevisiae Saccharomyces cerevisiae Proteins plastin
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Holtzman D A
Department of Molecular and Cell Biology, University of California, Berkeley 94720.
Wertman K F
Drubin D G
References (47)
47 references, click to expand
  1. Cofilin is an essential component of the yeast cortical cytoskeleton.
    J Cell Biol. 1993 Jan;120(2):421-35 PMID: 8421056
  2. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo.
    Nature. 1991 Dec 5;354(6352):404-8 PMID: 1956405
  3. Further characterization of the alpha-actinin-actin interface and comparison with filamin-binding sites on actin.
    J Biol Chem. 1993 Mar 15;268(8):5642-8 PMID: 8449927
  4. Charge-reversion mutagenesis of Dictyostelium actin to map the surface recognized by myosin during ATP-driven sliding motion.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2127-31 PMID: 8460118
  5. Molecular genetics of actin function.
    Biochem J. 1993 May 1;291 ( Pt 3):657-71 PMID: 8489492
  6. Structure of the actin-myosin complex and its implications for muscle contraction.
    Science. 1993 Jul 2;261(5117):58-65 PMID: 8316858
  7. Three-dimensional atomic model of F-actin decorated with Dictyostelium myosin S1.
    Nature. 1993 Jul 8;364(6433):171-4 PMID: 8321290
  8. Unexpected combinations of null mutations in genes encoding the actin cytoskeleton are lethal in yeast.
    Mol Biol Cell. 1993 May;4(5):459-68 PMID: 8334302
  9. 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
  10. Structure of gelsolin segment 1-actin complex and the mechanism of filament severing.
    Nature. 1993 Aug 19;364(6439):685-92 PMID: 8395021
  11. A 13-A map of the actin-scruin filament from the limulus acrosomal process.
    J Cell Biol. 1993 Oct;123(2):337-44 PMID: 8408217
  12. Yeast actin with a mutation in the "hydrophobic plug" between subdomains 3 and 4 (L266D) displays a cold-sensitive polymerization defect.
    J Cell Biol. 1993 Dec;123(5):1185-95 PMID: 8245125
  13. Mutations that enhance the cap2 null mutant phenotype in Saccharomyces cerevisiae affect the actin cytoskeleton, morphogenesis and pattern of growth.
    Genetics. 1993 Nov;135(3):693-709 PMID: 8293974
  14. The yeast actin cytoskeleton.
    Curr Opin Cell Biol. 1994 Feb;6(1):110-9 PMID: 8167016
  15. 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
  16. Actin mutations that show suppression with fimbrin mutations identify a likely fimbrin-binding site on actin.
    J Cell Biol. 1994 Jul;126(2):413-22 PMID: 8034742
  17. Determination of the alpha-actinin-binding site on actin filaments by cryoelectron microscopy and image analysis.
    J Cell Biol. 1994 Jul;126(2):433-43 PMID: 8034744
  18. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  19. Filamin inhibits actin activation of heavy meromyosin ATPase.
    FEBS Lett. 1977 May 15;77(2):228-32 PMID: 140819
  20. Identification of myosin-binding sites on the actin sequence.
    Biochemistry. 1982 Jul 20;21(15):3654-61 PMID: 7115691
  21. Transformation of intact yeast cells treated with alkali cations.
    J Bacteriol. 1983 Jan;153(1):163-8 PMID: 6336730
  22. Construction and genetic characterization of temperature-sensitive mutant alleles of the yeast actin gene.
    Proc Natl Acad Sci U S A. 1984 Aug;81(15):4889-93 PMID: 6379652
  23. Phenotypic analysis of temperature-sensitive yeast actin mutants.
    Cell. 1985 Feb;40(2):405-16 PMID: 3967297
  24. Dual effect of filamin on actomyosin ATPase activity.
    J Muscle Res Cell Motil. 1985 Feb;6(1):29-42 PMID: 3159750
  25. Actin-fragmin interactions as revealed by chemical cross-linking.
    Biochemistry. 1986 Jan 28;25(2):435-40 PMID: 3955005
  26. Actin and actin-binding proteins. A critical evaluation of mechanisms and functions.
    Annu Rev Biochem. 1986;55:987-1035 PMID: 3527055
  27. Improved method for mapping the binding site of an actin-binding protein in the actin sequence. Use of a site-directed antibody against the N-terminal region of actin as a probe of its N-terminus.
    Biochemistry. 1986 Oct 7;25(20):6186-92 PMID: 3790514
  28. Physico-chemical properties of rat and dog cardiac alpha-actinin.
    Biochim Biophys Acta. 1986 Dec 12;874(3):347-54 PMID: 2947632
  29. Genetically essential and nonessential alpha-tubulin genes specify functionally interchangeable proteins.
    Mol Cell Biol. 1986 Nov;6(11):3722-33 PMID: 3540600
  30. Nonmuscle actin-binding proteins.
    Annu Rev Cell Biol. 1985;1:353-402 PMID: 3030380
  31. Further characterization of a conserved actin-binding 27-kDa fragment of actinogelin and alpha-actinins and mapping of their binding sites on the actin molecule by chemical cross-linking.
    J Biol Chem. 1987 Apr 5;262(10):4717-23 PMID: 3558365
  32. Plasmid construction by homologous recombination in yeast.
    Gene. 1987;58(2-3):201-16 PMID: 2828185
  33. Probing actin polymerization by intermolecular cross-linking.
    J Cell Biol. 1988 Mar;106(3):785-96 PMID: 3346326
  34. Yeast actin-binding proteins: evidence for a role in morphogenesis.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2551-61 PMID: 3060468
  35. Dominant suppressors of yeast actin mutations that are reciprocally suppressed.
    Genetics. 1989 Apr;121(4):675-83 PMID: 2656402
  36. Acanthamoeba actin and profilin can be cross-linked between glutamic acid 364 of actin and lysine 115 of profilin.
    J Cell Biol. 1989 Aug;109(2):619-26 PMID: 2569469
  37. Homology of a yeast actin-binding protein to signal transduction proteins and myosin-I.
    Nature. 1990 Jan 18;343(6255):288-90 PMID: 2405279
  38. Removal of the amino-terminal acidic residues of yeast actin. Studies in vitro and in vivo.
    J Biol Chem. 1992 May 5;267(13):9430-6 PMID: 1349604
  39. Yeast actin filaments display ATP-dependent sliding movement over surfaces coated with rabbit muscle myosin.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4466-70 PMID: 1533933
  40. The identification and characterisation of an actin-binding site in alpha-actinin by mutagenesis.
    FEBS Lett. 1992 Jun 15;304(2-3):201-6 PMID: 1618324
  41. Systematic mutational analysis of the yeast ACT1 gene.
    Genetics. 1992 Oct;132(2):337-50 PMID: 1427032
  42. Actin constitution: guaranteeing the right to assemble.
    Science. 1992 Oct 30;258(5083):759-60 PMID: 1439782
  43. Atomic structure of the actin:DNase I complex.
    Nature. 1990 Sep 6;347(6288):37-44 PMID: 2395459
  44. Atomic model of the actin filament.
    Nature. 1990 Sep 6;347(6288):44-9 PMID: 2395461
  45. Molecular structure of F-actin and location of surface binding sites.
    Nature. 1990 Nov 15;348(6298):217-21 PMID: 2234090
  46. Site-directed mutagenesis of the yeast actin gene: a test for actin function in vivo.
    EMBO J. 1991 Dec;10(12):3951-8 PMID: 1935913
  47. Enhanced stimulation of myosin subfragment 1 ATPase activity by addition of negatively charged residues to the yeast actin NH2 terminus.
    J Biol Chem. 1993 Feb 5;268(4):2410-5 PMID: 8428914
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-07-00
Pages
423-32
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2200022
Subset
IM
Grants
NIGMS NIH HHS · GM-42759 · United States
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