Home LiteratureArticle Details
PMID: 12429848 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The diaphanous-related formin mDia1 controls serum response factor activity through its effects on actin polymerization.

Molecular biology of the cell ·Vol. 13 ·No. 11 ·2002-11-00 ·Pages 4088-99

Copeland JW, Treisman R

Abstract

SRF-dependent transcription is regulated by the small GTPase RhoA via its effects on actin dynamics. The diaphanous-related formin (DRF) proteins have been identified as candidate RhoA effectors mediating signaling to SRF. Here we investigate the relationship between SRF activation and actin polymerization by the DRF mDia1. We show that the ability of mDia1 to potentiate SRF activity is strictly correlated with its ability to promote F-actin assembly. Both processes can occur independently of the mDia1 FH1 domain but require sequences in an extended C-terminal region encompassing the conserved FH2 domain. mDia-mediated SRF activation, but not F-actin assembly, can be blocked by a nonpolymerizable actin mutant, placing actin downstream of mDia in the signal pathway. The SRF activation assay was used to identify inactive mDia1 derivatives that inhibit serum- and LPA-induced signaling to SRF. We show that these interfering mutants also block F-actin assembly, whether induced by mDia proteins or extracellular signals. These results identify novel functional elements of mDia1 and show that it regulates SRF activity by inducing depletion of the cellular pool of G-actin.

MeSH Terms
3T3 Cells Actins/metabolism Amino Acid Sequence Animals Carrier Proteins/genetics,metabolism Cytoskeleton/metabolism Formins Genes, Reporter Mice Molecular Sequence Data Phalloidine/chemistry,metabolism Protein Structure, Tertiary Sequence Alignment Serum Response Factor/metabolism Signal Transduction/physiology rhoA GTP-Binding Protein/metabolism
Chemicals
Actins Carrier Proteins Diap1 protein, mouse Formins Serum Response Factor Phalloidine rhoA GTP-Binding Protein
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Copeland John W
Cancer Research UK, London Research Institute, Lincoln's Inn Fields laboratories.
Treisman Richard
References (53)
53 references, click to expand
  1. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1.
    Cell. 2001 Dec 28;107(7):843-54 PMID: 11779461
  2. Distinct actions and cooperative roles of ROCK and mDia in Rho small G protein-induced reorganization of the actin cytoskeleton in Madin-Darby canine kidney cells.
    Mol Biol Cell. 1999 Aug;10(8):2481-91 PMID: 10436006
  3. Yeast formins regulate cell polarity by controlling the assembly of actin cables.
    Nat Cell Biol. 2002 Jan;4(1):42-50 PMID: 11740491
  4. Functional characterization and localization of the Aspergillus nidulans formin SEPA.
    Mol Biol Cell. 2002 Feb;13(2):469-79 PMID: 11854405
  5. LIM kinase and Diaphanous cooperate to regulate serum response factor and actin dynamics.
    J Cell Biol. 2002 May 27;157(5):831-8 PMID: 12034774
  6. Role of formins in actin assembly: nucleation and barbed-end association.
    Science. 2002 Jul 26;297(5581):612-5 PMID: 12052901
  7. Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor.
    Mol Biol Cell. 2002 Dec;13(12):4167-78 PMID: 12475943
  8. Chemotactic peptide modulation of actin assembly and locomotion in neutrophils.
    J Cell Biol. 1984 Apr;98(4):1265-71 PMID: 6232281
  9. Xenopus cytoskeletal actin and human c-fos gene promoters share a conserved protein-binding site.
    EMBO J. 1987 Mar;6(3):667-73 PMID: 3582369
  10. Isolation of an abundant 50,000-dalton actin filament bundling protein from Dictyostelium amoebae.
    J Biol Chem. 1990 Feb 5;265(4):2286-91 PMID: 2404981
  11. Identification of an actin-binding protein from Dictyostelium as elongation factor 1a.
    Nature. 1990 Oct 4;347(6292):494-6 PMID: 2215665
  12. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors.
    Cell. 1992 Aug 7;70(3):389-99 PMID: 1643657
  13. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain.
    Cell. 1993 Apr 23;73(2):381-93 PMID: 8386592
  14. Stress fibres take shape.
    Nat Cell Biol. 1999 Jul;1(3):E64-6 PMID: 10559912
  15. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization.
    Nat Cell Biol. 1999 Jul;1(3):136-43 PMID: 10559899
  16. Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells.
    Blood. 1999 Dec 1;94(11):3658-67 PMID: 10572077
  17. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling.
    Mol Cell. 2000 Jan;5(1):13-25 PMID: 10678165
  18. Epidermal growth factor receptor tyrosine kinase mediates Ras activation by gonadotropin-releasing hormone.
    J Biol Chem. 2000 Apr 21;275(16):12251-60 PMID: 10766863
  19. Rho small G-protein-dependent binding of mDia to an Src homology 3 domain-containing IRSp53/BAIAP2.
    Biochem Biophys Res Commun. 2000 May 19;271(3):626-9 PMID: 10814512
  20. Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex.
    J Cell Biol. 2000 Oct 2;151(1):29-40 PMID: 11018051
  21. Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization.
    J Biol Chem. 2001 Jan 5;276(1):341-7 PMID: 11035001
  22. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Feb;21(3):827-39 PMID: 11154270
  23. Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1.
    Nat Cell Biol. 2001 Jan;3(1):8-14 PMID: 11146620
  24. Activation of Arp2/3 complex-mediated actin polymerization by cortactin.
    Nat Cell Biol. 2001 Mar;3(3):259-66 PMID: 11231575
  25. Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain.
    J Biol Chem. 2001 Jan 26;276(4):2824-30 PMID: 11035012
  26. mDia mediates Rho-regulated formation and orientation of stable microtubules.
    Nat Cell Biol. 2001 Aug;3(8):723-9 PMID: 11483957
  27. mDia-interacting protein acts downstream of Rho-mDia and modifies Src activation and stress fiber formation.
    J Biol Chem. 2001 Oct 19;276(42):39290-4 PMID: 11509578
  28. Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division.
    Curr Biol. 2001 Oct 30;11(21):1656-65 PMID: 11696322
  29. Characterization of functional domains of mDia1, a link between the small GTPase Rho and the actin cytoskeleton.
    J Cell Sci. 2001 Oct;114(Pt 20):3663-72 PMID: 11707518
  30. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene.
    Development. 1994 Dec;120(12):3367-77 PMID: 7821209
  31. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF.
    Cell. 1995 Jun 30;81(7):1159-70 PMID: 7600583
  32. Autoregulation of actin synthesis in hepatocytes by transcriptional and posttranscriptional mechanisms.
    Eur J Biochem. 1995 May 15;230(1):32-7 PMID: 7601117
  33. c-Src regulates the simultaneous rearrangement of actin cytoskeleton, p190RhoGAP, and p120RasGAP following epidermal growth factor stimulation.
    J Cell Biol. 1995 Jul;130(2):355-68 PMID: 7542246
  34. Formin binding proteins bear WWP/WW domains that bind proline-rich peptides and functionally resemble SH3 domains.
    EMBO J. 1996 Mar 1;15(5):1045-54 PMID: 8605874
  35. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae.
    EMBO J. 1996 Nov 15;15(22):6060-8 PMID: 8947028
  36. Bundling of actin filaments by elongation factor 1 alpha inhibits polymerization at filament ends.
    J Cell Biol. 1996 Dec;135(5):1309-21 PMID: 8947553
  37. Molecular interaction between limb deformity proteins (formins) and Src family kinases.
    J Biol Chem. 1996 Dec 27;271(52):33525-30 PMID: 8969217
  38. Translocation of Src kinase to the cell periphery is mediated by the actin cytoskeleton under the control of the Rho family of small G proteins.
    J Cell Biol. 1996 Dec;135(6 Pt 1):1551-64 PMID: 8978822
  39. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1)
    J Exp Med. 1996 Sep 1;184(3):1101-9 PMID: 9064327
  40. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis.
    Science. 1997 Apr 4;276(5309):118-22 PMID: 9082982
  41. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin.
    J Cell Biol. 1997 Apr 7;137(1):169-82 PMID: 9105045
  42. Autoregulation of actin synthesis responds to monomeric actin levels.
    J Cell Biochem. 1997 Jun 15;65(4):469-78 PMID: 9178097
  43. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae.
    EMBO J. 1997 May 15;16(10):2745-55 PMID: 9184220
  44. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin.
    EMBO J. 1997 Jun 2;16(11):3044-56 PMID: 9214622
  45. Interaction of Rho1p target Bni1p with F-actin-binding elongation factor 1alpha: implication in Rho1p-regulated reorganization of the actin cytoskeleton in Saccharomyces cerevisiae.
    Oncogene. 1998 Apr 16;16(15):2011-6 PMID: 9591785
  46. FH3, a domain found in formins, targets the fission yeast formin Fus1 to the projection tip during conjugation.
    J Cell Biol. 1998 Jun 1;141(5):1217-28 PMID: 9606213
  47. FH proteins as cytoskeletal organizers.
    Trends Cell Biol. 1998 Mar;8(3):111-5 PMID: 9695820
  48. Serum response factor is essential for mesoderm formation during mouse embryogenesis.
    EMBO J. 1998 Nov 2;17(21):6289-99 PMID: 9799237
  49. Regulation of p190 Rho-GAP by v-Src is linked to cytoskeletal disruption during transformation.
    J Cell Sci. 1999 Mar;112 ( Pt 6):947-56 PMID: 10036244
  50. Formin defines a large family of morphoregulatory genes and functions in establishment of the polarising region.
    Cell Tissue Res. 1999 Apr;296(1):85-93 PMID: 10199968
  51. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics.
    Cell. 1999 Jul 23;98(2):159-69 PMID: 10428028
  52. Signaling to actin dynamics.
    J Cell Biol. 1999 Jul 26;146(2):267-72 PMID: 10427083
  53. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast.
    Nat Cell Biol. 2002 Jan;4(1):32-41 PMID: 11740490
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2002-11-00
Pages
4088-99
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC133616
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com