Raver1 Interactions with Vinculin and RNA Suggest a Feed-Forward Pathway in Directing mRNA to Focal Adhesions

Structure

Volumn 17, Issue 6, 2009, Pages 833-842

  Lee, Jun Hyuck ^a   Rangarajan, Erumbi S ^a   Yogesha, S D ^a   Izard, Tina ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

PROTEINS; RNA

Indexed keywords

F ACTIN; MESSENGER RNA; RAVER1; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VINCULIN;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; FOCAL ADHESION; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING;

ACTINS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL ADHESION; CONSERVED SEQUENCE; CRYSTALLIZATION; CYTOSKELETON; FOCAL ADHESIONS; GENETIC VECTORS; HELA CELLS; HUMANS; HYDROGEN BONDING; HYDROPHOBICITY; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RNA; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; TRANSFECTION; VINCULIN;

EID: 66349131836     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2009.04.010     Document Type: Article

References (50)

1. Bakolitsa C., Cohen D.M., Bankston L.A., Bobkov A.A., Cadwell G.W., Jennings L., Critchley D.R., Craig S.W., and Liddington R.C. Structural basis for vinculin activation at sites of cell adhesion. Nature 430 (2004) 583-586
2. Bois P.R.J., Borgon R.A., Vonrhein C., and Izard T. Structural dynamics of α-actinin-vinculin interactions. Mol. Cell. Biol. 25 (2005) 6112-6122
3. Bois P.R.J., O'Hara B.P., Nietlispach D., Kirkpatrick J., and Izard T. The vinculin binding sites of talin and α-actinin are sufficient to activate vinculin. J. Biol. Chem. 281 (2006) 7228-7236
4. Borgon R.A., Vonrhein C., Bricogne G., Bois P.R.J., and Izard T. Crystal structure of human vinculin. Structure 12 (2004) 1189-1197
5. Bricogne G. The Bayesian viewpoint in crystallography: Basic concepts and applications. Methods Enzymol. 276 (1997) 361-423
6. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
7. Chandrasekar I., Stradal T.E., Holt M.R., Entschladen F., Jockusch B.M., and Ziegler W.H. Vinculin acts as a sensor in lipid regulation of adhesion-site turnover. J. Cell Sci. 118 (2005) 1461-1472
8. Chicurel M.E., Singer R.H., Meyer C.J., and Ingber D.E. Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions. Nature 392 (1998) 730-733
9. Cléry A., Blatter M., and Allain F.H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18 (2008) 290-298
10. Corsini L., Bonnal S., Basquin J., Hothorn M., Scheffzek K., Valcárcel J., and Sattler M. U2AF-homology motif interactions are required for alternative splicing regulation by SPF45. Nat. Struct. Mol. Biol. 14 (2007) 620-629
11. Czaplinski K., and Singer R.H. Pathways for mRNA localization in the cytoplasm. Trends Biochem. Sci. 31 (2006) 687-693
12. DeMali K.A., and Burridge K. Coupling membrane protrusion and cell adhesion. J. Cell Sci. 116 (2003) 2389-2397
13. del Rio A., Perez-Jimenez R., Liu R., Roca-Cusachs P., Fernandez J.M., and Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 323 (2009) 638-641
14. Fillingham I., Gingras A.R., Papagrigoriou E., Patel B., Emsley J., Critchley D.R., Roberts G.C., and Barsukov I.L. A vinculin binding domain from the talin rod unfolds to form a complex with the vinculin head. Structure 13 (2005) 65-74
15. Fribourg S., Gatfield D., Izaurralde E., and Conti E. A novel mode of RBD-protein recognition in the Y14-Mago complex. Nat. Struct. Biol. 10 (2003) 433-439
16. Gilmore A.P., and Burridge K. Regulation of vinculin binding to talin and actin by phosphatidylinositol-4-5-bisphosphate. Nature 381 (1996) 531-535
17. Gromak N., Rideau A., Southby J., Scadden A.D., Gooding C., Hüttelmaier S., Singer R.H., and Smith C.W. The PTB interacting protein raver1 regulates-tropomyosin alternative splicing. EMBO J. 22 (2003) 6356-6364
18. Hüttelmaier S., Illenberger S., Grosheva I., Rüdiger M., Singer R.H., and Jockusch B.M. Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins. J. Cell Biol. 155 (2001) 775-786
19. Hüttelmaier S., Zenklusen D., Lederer M., Dictenberg J., Lorenz M., Meng X., Bassell G.J., Condeelis J., and Singer R.H. Spatial regulation of β-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438 (2005) 512-515
20. Izard T., and Vonrhein C. Structural basis for amplifying vinculin activation by talin. J. Biol. Chem. 279 (2004) 27667-27678
21. Izard T., Evans G., Borgon R.A., Rush C.L., Bricogne G., and Bois P.R. Vinculin activation by talin through helical bundle conversion. Nature 427 (2004) 171-175
22. Jockusch B.M., Hüttelmaier S., and Illenberger S. From the nucleus toward the cell periphery: a guided tour for mRNAs. News Physiol. Sci. 18 (2003) 7-11
23. Johnson R.P., and Craig S.W. F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature 373 (1995) 261-264
24. Jones T.A., Zou J.-Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models into electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
25. Kadlec J., Izaurralde E., and Cusack S. The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nat. Struct. Mol. Biol. 11 (2004) 330-337
26. Kielkopf C.L., Rodionova N.A., Green M.R., and Burley S.K. A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer. Cell 106 (2001) 595-605
27. Kielkopf C.L., Lücke S., and Green M.R. U2AF homology motifs: protein recognition in the RRM world. Genes Dev. 18 (2004) 1513-1526
28. Lau C.K., Diem M.D., Dreyfuss G., and Van Duyne G.D. Structure of the Y14-Magoh core of the exon junction complex. Curr. Biol. 13 (2003) 933-941
29. Lunde B.M., Moore C., and Varani G. RNA-binding proteins: modular design for efficient function. Nat. Rev. Mol. Cell Biol. 8 (2007) 479-490
30. Maris C., Dominguez C., and Allain F.H. The RNA recognition motif, a plastic RNA- binding platform to regulate post-transcriptional gene expression. FEBS J. 272 (2005) 2118-2131
31. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33 (1968) 491-497
32. Mili S., Moissoglu K., and Macara I.G. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453 (2008) 115-119
33. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
34. Ngo J.C., Giang K., Chakrabarti S., Ma C.T., Huynh N., Hagopian J.C., Dorrestein P.C., Fu X.D., Adams J.A., and Ghosh G. A sliding docking interaction is essential for sequential and processive phosphorylation of an SR protein by SRPK1. Mol. Cell 29 (2008) 563-576
35. Nhieu G.T., and Izard T. Vinculin binding in its closed conformation by a helix addition mechanism. EMBO J. 26 (2007) 4588-4596
36. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
37. Pan F., Hüttelmaier S., Singer R.H., and Gu W. ZBP2 facilitates binding of ZBP1 to beta-actin mRNA during transcription. Mol. Cell. Biol. 27 (2007) 8340-8351
38. Price S.R., Evans P.R., and Nagai K. Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature 394 (1998) 645-650
39. Rideau A.P., Gooding C., Simpson P.J., Monie T.P., Lorenz M., Hüttelmaier S., Singer R.H., Matthews S., Curry S., and Smith C.W. A peptide motif in Raver1 mediates splicing repression by interaction with the PTB RRM2 domain. Nat. Struct. Mol. Biol. 13 (2006) 839-848
40. Rodriguez A.J., Shenoy S.M., Singer R.H., and Condeelis J. Visualization of mRNA translation in living cells. J. Cell Biol. 175 (2006) 67-76
41. Schellenberg M.J., Edwards R.A., Ritchie D.B., Kent O.A., Golas M.M., Stark H., Lührmann R., Glover J.N., and MacMillan A.M. Crystal structure of a core spliceosomal protein interface. Proc. Natl. Acad. Sci. USA 103 (2006) 1266-1271
42. Shi H., and Xu R.M. Crystal structure of the Drosophila Mago nashi-Y14 complex. Genes Dev. 17 (2003) 971-976
43. Selenko P., Gregorovic G., Sprangers R., Stier G., Rhani Z., Krämer A., and Sattler M. Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol. Cell 11 (2003) 965-976
44. Spadaccini R., Reidt U., Dybkov O., Will C., Frank R., Stier G., Corsini L., Wahl M.C., Lührmann R., and Sattler M. Biochemical and NMR analyses of an SF3b 155-p 1 4-U2AF-RNA interaction network involved in branch point definition during pre-mRNA splicing. RNA 12 (2006) 410-425
45. Spellman R., Rideau A., Matlin A., Gooding C., Robinson F., McGlincy N., Grellscheid S.N., Southby J., Wollerton M., and Smith C.W. Regulation of alternative splicing by PTB and associated factors. Biochem. Soc. Trans. 33 (2005) 457-460
46. Tronrud D.E., Eyck L.F.T., and Matthews B.W. An efficient general-purpose least- squares refinement program for macromolecular structures. Acta Crystallogr. A 43 (1987) 489-501
47. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
48. Weis W.I. Cell biology: how to build a cell junction. Nature 430 (2004) 513-515
49. Ziegler W.H., Liddington R.C., and Critchley D.R. The structure and regulation of vinculin. Trends Cell Biol. 16 (2006) 453-460
50. Zieseniss A., Schroeder U., Buchmeier S., Schoenenberger C.A., van den Heuvel J., Jockusch B.M., and Illenberger S. Raver1 is an integral component of muscle contractile elements. Cell Tissue Res. 327 (2007) 583-594