• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of biochemjBJ Latest papers and much more!
Biochem J. Oct 15, 2003; 375(Pt 2): 287–295.
PMCID: PMC1223692

SCP1 encodes an actin-bundling protein in yeast.

Abstract

The association of F-actin (filamentous actin) with a large number of binding proteins is essential for cellular function. Actin-binding proteins control the dynamics of actin filaments, nucleate new filaments and facilitate formation of higher-order structures such as actin bundles. The yeast gene SCP1 encodes a small protein with significant homology to mammalian SM22/transgelin. We have investigated the role of Scp1p in budding yeast to probe the fundamental role of this family of proteins. Here, we demonstrate that Scp1p binds to F-actin and induces the formation of tight F-actin bundles in vitro. Deletion of SCP1 in yeast lacking the actin-bundling protein, fimbrin (Sac6p), exacerbates the disrupted actin phenotype and enhances latrunculin-A sensitivity. Furthermore, Scp1p co-localizes with actin in cortical patches and its localization is lost in the presence of latrunculin-A. Our data support a role for Scp1p in bundling actin filaments and, in concert with Sac6p, acting as a second actin-bundling activity crucial to the stability of the yeast actin cytoskeleton.

Full Text

The Full Text of this article is available as a PDF (428K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ayscough KR. In vivo functions of actin-binding proteins. Curr Opin Cell Biol. 1998 Feb;10(1):102–111. [PubMed]
  • Lees-Miller JP, Heeley DH, Smillie LB, Kay CM. Isolation and characterization of an abundant and novel 22-kDa protein (SM22) from chicken gizzard smooth muscle. J Biol Chem. 1987 Mar 5;262(7):2988–2993. [PubMed]
  • Shapland C, Hsuan JJ, Totty NF, Lawson D. Purification and properties of transgelin: a transformation and shape change sensitive actin-gelling protein. J Cell Biol. 1993 Jun;121(5):1065–1073. [PMC free article] [PubMed]
  • Gimona Mario, Djinovic-Carugo Kristina, Kranewitter Wolfgang J, Winder Steven J. Functional plasticity of CH domains. FEBS Lett. 2002 Feb 20;513(1):98–106. [PubMed]
  • Fu Y, Liu HW, Forsythe SM, Kogut P, McConville JF, Halayko AJ, Camoretti-Mercado B, Solway J. Mutagenesis analysis of human SM22: characterization of actin binding. J Appl Physiol (1985) 2000 Nov;89(5):1985–1990. [PubMed]
  • Zhang JC, Kim S, Helmke BP, Yu WW, Du KL, Lu MM, Strobeck M, Yu Q, Parmacek MS. Analysis of SM22alpha-deficient mice reveals unanticipated insights into smooth muscle cell differentiation and function. Mol Cell Biol. 2001 Feb;21(4):1336–1344. [PMC free article] [PubMed]
  • Gonos ES, Derventzi A, Kveiborg M, Agiostratidou G, Kassem M, Clark BF, Jat PS, Rattan SI. Cloning and identification of genes that associate with mammalian replicative senescence. Exp Cell Res. 1998 Apr 10;240(1):66–74. [PubMed]
  • Lawson D, Harrison M, Shapland C. Fibroblast transgelin and smooth muscle SM22alpha are the same protein, the expression of which is down-regulated in many cell lines. Cell Motil Cytoskeleton. 1997;38(3):250–257. [PubMed]
  • Winder SJ, Kendrick-Jones J. Protein production in three different expression vectors from a single polymerase chain reaction product. Anal Biochem. 1995 Oct 10;231(1):271–273. [PubMed]
  • Winder SJ, Hemmings L, Maciver SK, Bolton SJ, Tinsley JM, Davies KE, Critchley DR, Kendrick-Jones J. Utrophin actin binding domain: analysis of actin binding and cellular targeting. J Cell Sci. 1995 Jan;108(Pt 1):63–71. [PubMed]
  • Spudich JA, Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem. 1971 Aug 10;246(15):4866–4871. [PubMed]
  • Winder SJ, Walsh MP. Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J Biol Chem. 1990 Jun 15;265(17):10148–10155. [PubMed]
  • Dewar H, Warren DT, Gardiner FC, Gourlay CG, Satish N, Richardson MR, Andrews PD, Ayscough KR. Novel proteins linking the actin cytoskeleton to the endocytic machinery in Saccharomyces cerevisiae. Mol Biol Cell. 2002 Oct;13(10):3646–3661. [PMC free article] [PubMed]
  • Ayscough KR, Stryker J, Pokala N, Sanders M, Crews P, Drubin DG. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol. 1997 Apr 21;137(2):399–416. [PMC free article] [PubMed]
  • Ayscough K. Use of latrunculin-A, an actin monomer-binding drug. Methods Enzymol. 1998;298:18–25. [PubMed]
  • Mumberg D, Müller R, Funk M. Regulatable promoters of Saccharomyces cerevisiae: comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 1994 Dec 25;22(25):5767–5768. [PMC free article] [PubMed]
  • Bramham Janice, Hodgkinson Julie L, Smith Brian O, Uhrín Dusan, Barlow Paul N, Winder Steven J. Solution structure of the calponin CH domain and fitting to the 3D-helical reconstruction of F-actin:calponin. Structure. 2002 Feb;10(2):249–258. [PubMed]
  • Stafford WF, 3rd, Mabuchi K, Takahashi K, Tao T. Physical characterization of calponin. A circular dichroism, analytical ultracentrifuge, and electron microscopy study. J Biol Chem. 1995 May 5;270(18):10576–10579. [PubMed]
  • Pruyne D, Bretscher A. Polarization of cell growth in yeast. J Cell Sci. 2000 Feb;113(Pt 4):571–585. [PubMed]
  • Adams AE, Botstein D, Drubin DG. A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science. 1989 Jan 13;243(4888):231–233. [PubMed]
  • Adams AE, Botstein D, Drubin DG. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature. 1991 Dec 5;354(6352):404–408. [PubMed]
  • Drubin DG, Miller KG, Botstein D. Yeast actin-binding proteins: evidence for a role in morphogenesis. J Cell Biol. 1988 Dec;107(6 Pt 2):2551–2561. [PMC free article] [PubMed]
  • Gimona M, Winder SJ. Single calponin homology domains are not actin-binding domains. Curr Biol. 1998 Sep 24;8(19):R674–R675. [PubMed]
  • Winder Steven J. Structural insights into actin-binding, branching and bundling proteins. Curr Opin Cell Biol. 2003 Feb;15(1):14–22. [PubMed]
  • Gimona M, Mital R. The single CH domain of calponin is neither sufficient nor necessary for F-actin binding. J Cell Sci. 1998 Jul;111(Pt 13):1813–1821. [PubMed]
  • Burgstaller Gerald, Kranewitter Wolfgang J, Gimona Mario. The molecular basis for the autoregulation of calponin by isoform-specific C-terminal tail sequences. J Cell Sci. 2002 May 15;115(Pt 10):2021–2029. [PubMed]
  • Tang JX, Janmey PA. The polyelectrolyte nature of F-actin and the mechanism of actin bundle formation. J Biol Chem. 1996 Apr 12;271(15):8556–8563. [PubMed]
  • Kranewitter WJ, Ylanne J, Gimona M. UNC-87 is an actin-bundling protein. J Biol Chem. 2001 Mar 2;276(9):6306–6312. [PubMed]
  • Owen C, DeRosier D. A 13-A map of the actin-scruin filament from the limulus acrosomal process. J Cell Biol. 1993 Oct;123(2):337–344. [PMC free article] [PubMed]
  • Sanders MC, Way M, Sakai J, Matsudaira P. Characterization of the actin cross-linking properties of the scruin-calmodulin complex from the acrosomal process of Limulus sperm. J Biol Chem. 1996 Feb 2;271(5):2651–2657. [PubMed]
  • Schmid MF, Agris JM, Jakana J, Matsudaira P, Chiu W. Three-dimensional structure of a single filament in the Limulus acrosomal bundle: scruin binds to homologous helix-loop-beta motifs in actin. J Cell Biol. 1994 Feb;124(3):341–350. [PMC free article] [PubMed]
  • Ayscough KR, Drubin DG. A role for the yeast actin cytoskeleton in pheromone receptor clustering and signalling. Curr Biol. 8(16):927–930. [PubMed]
  • Morton WM, Ayscough KR, McLaughlin PJ. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol. 2000 Jun;2(6):376–378. [PubMed]
  • Goode BL, Wong JJ, Butty AC, Peter M, McCormack AL, Yates JR, Drubin DG, Barnes G. Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J Cell Biol. 1999 Jan 11;144(1):83–98. [PMC free article] [PubMed]
  • Ho Yuen, Gruhler Albrecht, Heilbut Adrian, Bader Gary D, Moore Lynda, Adams Sally-Lin, Millar Anna, Taylor Paul, Bennett Keiryn, Boutilier Kelly, et al. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature. 2002 Jan 10;415(6868):180–183. [PubMed]
  • Goodman Anya, Goode Bruce L, Matsudaira Paul, Fink Gerald R. The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol Biol Cell. 2003 Jul;14(7):2617–2629. [PMC free article] [PubMed]
  • Higgins DG, Bleasby AJ, Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. [PubMed]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...