Home LiteratureArticle Details
PMID: 19176533 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Structural determinants of integrin binding to the talin rod.

The Journal of biological chemistry ·Vol. 284 ·No. 13 ·2009-03-27 ·Pages 8866-76

Gingras AR, Ziegler WH, Bobkov AA, Joyce MG, Fasci D, Himmel M, Rothemund S, Ritter A, Grossmann JG, Patel B, Bate N, Goult BT, Emsley J, Barsukov IL, Roberts GC, Liddington RC, Ginsberg MH, Critchley DR

Abstract

The adaptor protein talin serves both to activate the integrin family of cell adhesion molecules and to couple integrins to the actin cytoskeleton. Integrin activation has been shown to involve binding of the talin FERM domain to membrane proximal sequences in the cytoplasmic domain of the integrin beta-subunit. However, a second integrin-binding site (IBS2) has been identified near the C-terminal end of the talin rod. Here we report the crystal structure of IBS2 (residues 1974-2293), which comprises two five-helix bundles, "IBS2-A" (1974-2139) and "IBS2-B" (2140-2293), connected by a continuous helix with a distinct kink at its center that is stabilized by side-chain H-bonding. Solution studies using small angle x-ray scattering and NMR point to a fairly flexible quaternary organization. Using pull-down and enzyme-linked immunosorbent assays, we demonstrate that integrin binding requires both IBS2 domains, as does binding to acidic phospholipids and robust targeting to focal adhesions. We have defined the membrane proximal region of the integrin cytoplasmic domain as the major binding region, although more membrane distal regions are also required for strong binding. Alanine-scanning mutagenesis points to an important electrostatic component to binding. Thermal unfolding experiments show that integrin binding induces conformational changes in the IBS2 module, which we speculate are linked to vinculin and membrane binding.

MeSH Terms
Animals Binding Sites/physiology Cell Membrane/chemistry,genetics,metabolism Crystallography, X-Ray/methods Cytoplasm/chemistry,genetics,metabolism Integrins/chemistry,genetics,metabolism Mice Peptide Mapping/methods Protein Binding/physiology Protein Structure, Tertiary/physiology Talin/chemistry,genetics,metabolism Vinculin/chemistry,genetics,metabolism
Chemicals
Integrins Talin talin protein, mouse Vinculin
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Gingras Alexandre R
Department of Biochemistry, University of Leicester, Lancaster Road, Leicester LE1 9HN, United Kingdom.
Ziegler Wolfgang H
Bobkov Andrey A
Joyce M Gordon
Fasci Domenico
Himmel Mirko
Rothemund Sven
Ritter Anett
Grossmann J Günter
Patel Bipin
Bate Neil
Goult Benjamin T
Emsley Jonas
Barsukov Igor L
Roberts Gordon C K
Liddington Robert C
Ginsberg Mark H
Critchley David R
References (42)
42 references, click to expand
  1. Analysis of repeated motifs in the talin rod.
    J Mol Biol. 1994 Jan 28;235(4):1278-90 PMID: 8308890
  2. Mapping and consensus sequence identification for multiple vinculin binding sites within the talin rod.
    J Biol Chem. 2005 Nov 4;280(44):37217-24 PMID: 16135522
  3. Identification of a repeated domain within mammalian alpha-synemin that interacts directly with talin.
    Exp Cell Res. 2008 May 1;314(8):1839-49 PMID: 18342854
  4. Structural determinants of integrin recognition by talin.
    Mol Cell. 2003 Jan;11(1):49-58 PMID: 12535520
  5. Role of vinculin in regulating focal adhesion turnover.
    Eur J Cell Biol. 2006 Jun;85(6):487-500 PMID: 16584805
  6. A fluorescence cell biology approach to map the second integrin-binding site of talin to a 130-amino acid sequence within the rod domain.
    J Biol Chem. 2004 May 21;279(21):22258-66 PMID: 15031296
  7. Cell adhesion: a FERM grasp of membrane dynamics.
    Curr Biol. 2003 Feb 4;13(3):R94-5 PMID: 12573235
  8. Calpain cleavage promotes talin binding to the beta 3 integrin cytoplasmic domain.
    J Biol Chem. 2001 Jul 27;276(30):28164-70 PMID: 11382782
  9. Structural basis of integrin activation by talin.
    Cell. 2007 Jan 12;128(1):171-82 PMID: 17218263
  10. The talin rod IBS2 alpha-helix interacts with the beta3 integrin cytoplasmic tail membrane-proximal helix by establishing charge complementary salt bridges.
    J Biol Chem. 2008 Aug 29;283(35):24212-23 PMID: 18577523
  11. Localization of an integrin binding site to the C terminus of talin.
    J Biol Chem. 2001 Nov 30;276(48):44373-8 PMID: 11555663
  12. The structure of the C-terminal actin-binding domain of talin.
    EMBO J. 2008 Jan 23;27(2):458-69 PMID: 18157087
  13. The cytoskeletal protein talin contains at least two distinct vinculin binding domains.
    J Cell Biol. 1993 Jul;122(2):337-47 PMID: 8320257
  14. Activation of a vinculin-binding site in the talin rod involves rearrangement of a five-helix bundle.
    EMBO J. 2004 Aug 4;23(15):2942-51 PMID: 15272303
  15. Alpha4 integrins are type I cAMP-dependent protein kinase-anchoring proteins.
    Nat Cell Biol. 2007 Apr;9(4):415-21 PMID: 17369818
  16. The NHL-domain protein Wech is crucial for the integrin-cytoskeleton link.
    Nat Cell Biol. 2008 Apr;10(4):422-8 PMID: 18327251
  17. Talin at a glance.
    J Cell Sci. 2008 May 1;121(Pt 9):1345-7 PMID: 18434644
  18. An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton.
    Nat Cell Biol. 2006 Jun;8(6):601-6 PMID: 16648844
  19. ILK, PINCH and parvin: the tIPP of integrin signalling.
    Nat Rev Mol Cell Biol. 2006 Jan;7(1):20-31 PMID: 16493410
  20. Structural basis for phosphatidylinositol phosphate kinase type Igamma binding to talin at focal adhesions.
    J Biol Chem. 2005 Mar 4;280(9):8381-6 PMID: 15623515
  21. Refinement of macromolecular structures by the maximum-likelihood method.
    Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55 PMID: 15299926
  22. Structural and dynamic characterization of a vinculin binding site in the talin rod.
    Biochemistry. 2006 Feb 14;45(6):1805-17 PMID: 16460027
  23. The CCP4 molecular-graphics project.
    Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1955-7 PMID: 12393928
  24. The I/LWEQ module: a conserved sequence that signifies F-actin binding in functionally diverse proteins from yeast to mammals.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5679-84 PMID: 9159132
  25. Structural basis for the interaction between the cytoplasmic domain of the hyaluronate receptor layilin and the talin F3 subdomain.
    J Mol Biol. 2008 Sep 26;382(1):112-26 PMID: 18638481
  26. The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation.
    J Biol Chem. 1999 Oct 1;274(40):28071-4 PMID: 10497155
  27. Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage.
    Nature. 1986 Apr 10-16;320(6062):531-3 PMID: 2938015
  28. The activity of the vinculin binding sites in talin is influenced by the stability of the helical bundles that make up the talin rod.
    J Biol Chem. 2006 Mar 17;281(11):7458-67 PMID: 16407302
  29. Talin contains three similar vinculin-binding sites predicted to form an amphipathic helix.
    Biochem J. 1999 Jul 15;341 ( Pt 2):257-63 PMID: 10393080
  30. Stereochemical quality of protein structure coordinates.
    Proteins. 1992 Apr;12(4):345-64 PMID: 1579569
  31. Indications for a novel muscular dystrophy pathway. gamma-filamin, the muscle-specific filamin isoform, interacts with myotilin.
    J Cell Biol. 2000 Oct 16;151(2):235-48 PMID: 11038172
  32. Structural basis for the autoinhibition of talin in regulating integrin activation.
    Mol Cell. 2008 Jul 11;31(1):124-33 PMID: 18614051
  33. Phosphatidylinositol phosphate kinase type 1gamma and beta1-integrin cytoplasmic domain bind to the same region in the talin FERM domain.
    J Biol Chem. 2003 Aug 15;278(33):31202-9 PMID: 12782621
  34. Vinculin acts as a sensor in lipid regulation of adhesion-site turnover.
    J Cell Sci. 2005 Apr 1;118(Pt 7):1461-72 PMID: 15769850
  35. Vinculin knockout results in heart and brain defects during embryonic development.
    Development. 1998 Jan;125(2):327-37 PMID: 9486805
  36. Dali: a network tool for protein structure comparison.
    Trends Biochem Sci. 1995 Nov;20(11):478-80 PMID: 8578593
  37. Coot: model-building tools for molecular graphics.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32 PMID: 15572765
  38. Determination of domain structure of proteins from X-ray solution scattering.
    Biophys J. 2001 Jun;80(6):2946-53 PMID: 11371467
  39. Talin contains three actin-binding sites each of which is adjacent to a vinculin-binding site.
    J Cell Sci. 1996 Nov;109 ( Pt 11):2715-26 PMID: 8937989
  40. The integrin binding site 2 (IBS2) in the talin rod domain is essential for linking integrin beta subunits to the cytoskeleton.
    J Biol Chem. 2007 Jun 8;282(23):17280-8 PMID: 17430904
  41. Automated MAD and MIR structure solution.
    Acta Crystallogr D Biol Crystallogr. 1999 Apr;55(Pt 4):849-61 PMID: 10089316
  42. The phosphotyrosine binding-like domain of talin activates integrins.
    J Biol Chem. 2002 Jun 14;277(24):21749-58 PMID: 11932255
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2009-03-27
Epub
2009-00-27
Pages
8866-76
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2659244
Subset
IM
Grants
NIGMS NIH HHS · U54 GM64346 · United States
Wellcome Trust · United Kingdom
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: [email protected]