Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53

EMBO Journal

Volumn 24, Issue 2, 2005, Pages 240-250

  Millard, Thomas H ^a   Bompard, Guillaume ^a   Heung, Man Yeung ^a   Dafforn, Timothy R ^a   Scott, David J ^b   Machesky, Laura M ^a   Fütterer, Klaus ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Actin bundling; Cell motility; Filopodia; IRSp53; X ray crystallography

Indexed keywords

DIMER; F ACTIN; G ACTIN; INSULIN RECEPTOR KINASE; PROTEIN IRSP53; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS7; CONTROLLED STUDY; CRYSTAL STRUCTURE; FILOPODIUM; FLUORESCENCE MICROSCOPY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SEDIMENTATION RATE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; DIMERIZATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROTEIN CONFORMATION; PSEUDOPODIA; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA;

EID: 13444291116     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600535     Document Type: Article

References (57)

1. Amann KJ, Renley BA, Ervasti JM (1998) A cluster of basic repeats in the dystrophin rod domain binds F-actin through an electrostatic interaction. J Biol Chem 273: 28419-28423
2. Bakolitsa C, Cohen DM, Bankston LA, Bobkov AA, Cadwell GW, Jennings L, Critchley DR, Craig SW, Liddington RC (2004) Structural basis for vinculin activation at sites of cell adhesion. Nature 430: 583-586
3. Bakolitsa C, de Pereda JM, Bagshaw CR, Critchley DR, Liddington RC (1999) Crystal structure of the vinculin tail suggests a pathway for activation. Cell 99: 603-613
4. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB (2002) Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109: 509-521
5. Bockmann J, Kreutz MR, Gundelfinger ED, Bockers TM (2002) ProSAP/Shank postsynaptic density proteins interact with insulin receptor tyrosine kinase substrate IRSp53. J Neurochem 83: 1013-1017
6. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921
7. Burkhard P, Kammerer RA, Steinmetz MO, Bourenkov GP, Aebi U (2000) The coiled-coil trigger site of the rod domain of cortexillin I unveils a distinct network of interhelical and intrahelical salt bridges. Struct Fold Des 8: 223-230
8. Carson M (1997) Ribbons. Methods Enzymol 277: 493-505
9. Carugo KD, Banuelos S, Saraste M (1997) Crystal structure of a calponin homology domain. Nat Struct Biol 4: 175-179
10. CCP4 (1994) Collaborative computational project number 4. The CCP4 suite of programs for protein crystallography. Acta Crystallogr D 50: 760-763
11. Engh RA, Huber R (1991) Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr A47: 392-400
12. Faix J, Steinmetz M, Boves H, Kammerer RA, Lottspeich F, Mintert U, Murphy J, Stock A, Aebi U, Gerisch G (1996) Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail. Cell 86: 631-642
13. Fujiwara T, Mammoto A, Kim Y, Takai Y (2000) Rho small G-protein-dependent binding of mDia to an Src homology 3 domain-containing IRSp53/BAIAP2. Biochem Biophys Res Commun 271: 626-629
14. Funato Y, Terabayashi T, Suenaga N, Seiki M, Takenawa T, Miki H (2004) IRSp53/Eps8 complex is important for positive regulation of Rac and cancer cell motility/invasiveness. Cancer Res 64: 5237-5244
15. Govind S, Kozma R, Monfries C, Lim L, Ahmed S (2001) Cdc42Hs facilitates cytoskeletal reorganization and neurite outgrowth by localizing the 58-kD insulin receptor substrate to filamentous actin. J Cell Biol 152: 579-594
16. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723
17. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514
18. Holm L, Sander C (1998) Touring protein fold space with Dali/FSSP. Nucleic Acids Res 26: 316-319
19. Hori K, Konno D, Maruoka H, Sobue K (2003) MALS is a binding partner of IRSp53 at cell-cell contacts. FEBS Lett 554: 30-34
20. Izard T, Evans G, Borgon RA, Rush CL, Bricogne G, Bois PR (2004) Vinculin activation by talin through helical bundle conversion. Nature 427: 171-175
21. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A47: 110-119
22. Klein MG, Shi W, Ramagopal U, Tseng Y, Wirtz D, Kovar DR, Staiger CJ, Almo SC (2004) Structure of the actin crosslinking core of fimbrin. Structure (Camb) 12: 999-1013
23. Krugmann S, Jordens I, Gevaert K, Driessens M, Vandekerckhove J, Hall A (2001) Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr Biol 11: 1645-1655
24. Laue T, Shah B, Ridgeway T, Pelletier S (1992) Cambridge, U.K. In Analytical Ultracentrifugation in Biochemistry and Polymer Science, Harding S, Rowe A and Horyon J (eds), pp 90-125. Royal Society of Chemistry: Cambridge, UK
25. Lebrand C, Dent EW Strasser GA, Lanier LM, Krause M, Svitkina TM, Borisy GG, Gertler FB (2004) Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42: 37-49
26. Leslie AGW (1992) Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography, 26
27. Machesky LM, Hall A (1997) Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J Cell Biol 138: 913-926
28. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG (2004) Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118: 363-373
29. Miki H, Takenawa T (2002) WAVE2 serves a functional partner of IRSp53 by regulating its interaction with Rac. Biochem Biophys Res Commun 293: 93-99
30. Miki H, Yamaguchi H, Suetsugu S, Takenawa T (2000) IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408: 732-735
31. Millard TH, Sharp SJ, Machesky LM (2004) Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem J 380: 1-17
32. Morris RJ, Perrakis A, Lamzin A (2002) ARP/wARP's model-building algorithms. I. The main chain. Acta Crystallogr D 58: 968-975
33. Murshudov A, Vagin A, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255
34. Nakagawa H, Miki H, Nozumi M, Takenawa T, Miyamoto S, Wehland J, Small JV (2003) IRSp53 is colocalised with WAVE2 at the tips of protruding lamellipodia and filopodia independently of Mena. J Cell Sci 116: 2577-2583
35. Nicholls A, Sharp KA, Honig B (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296
36. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303: 495-499
37. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465
38. Ponting CP, Russell RB (2000) Identification of distant homologues of fibroblast growth factors suggests a common ancestor for all beta-trefoil proteins. J Mol Biol 302: 1041-1047
39. Rybakova IN, Patel JR, Davies KE, Yurchenco PD, Ervasti JM (2002) Utrophin binds laterally along actin filaments and can couple costameric actin with sarcolemma when overexpressed in dystrophin-deficient muscle. Mol Cell Biol 13: 1512-1521
40. Sambrook J, Fritsch FE, Maniatis T (1998) Molecular Cloning: A Laboratory Manual. Cold Spring Harbour Laboratory Press: Cold Spring Harbour, NY
41. Schuck P (1998) Sedimentation analysis of noninteracting and self-associating solutes using numerical solutions to the Lamm equation. Biophys J 75: 1503-1512
42. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys J 78: 1606-1619
43. Sekerkova G, Loomis PA, Changyaleket B, Zheng L, Eytan R, Chen B, Mugnaini E, Bartles JR (2003) Novel espin actin-bundling proteins are localized to Purkinje cell dendritic spines and bind the Src homology 3 adapter protein insulin receptor substrate p53. J Neurosci 23: 1310-1319
44. Small JV, Stradal T, Vignal E, Rottner K (2002) The lamellipodium: where motility begins. Trends Cell Biol 12: 112-120
45. Soltau M, Berhorster K, Kindler S, Buck F, Richter D, Kreienkamp HJ (2004) Insulin receptor substrate of 53 kDa links postsynaptic shank to PSD-95. J Neurochem 90: 659-665
46. Soltau M, Richter D, Kreienkamp HJ (2002) The insulin receptor substrate IRSp53 links postsynaptic shank1 to the small G-protein cdc42. Mol Cell Neurosci 21: 575-583
47. Spudich JA, Watt S (1971) 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 246: 4866-4871
48. Tarricone C, Xiao B, Justin N, Walker PA, Rittinger K, Gamblin SJ, Smerdon SJ (2001) The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature 411: 215-219
49. Terwilliger TC (2002) Automated structure solution, density modification and model building. Acta Crystallogr D 58: 1937-1940
50. Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D 55: 849-861
51. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882
52. Weeks CM, Miller R (1999) The design and implementation of SnB v2.0. J Appl Crystallogr 32: 120-124
53. Winn MD, Isupov MN, Murshudov GN (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D 57: 122-133
54. Woodings JA, Sharp SJ, Machesky LM (2003) MIM-B, a putative metastasis suppressor protein, binds to actin and to protein tyrosine phosphatase delta. Biochem J 371: 463-471
55. Yamagishi A, Masuda M, Ohki T, Onishi H, Mochizuki N (2004) A novel actin bundling/filopodium-forming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein. J Biol Chem 279: 14929-14936
56. Yeh TC, Ogawa W, Danielsen AG, Roth RA (1996) Characterization and cloning of a 58/53-kDa substrate of the insulin receptor tyrosine kinase. J Biol Chem 271: 2921-2928
57. Ylanne J, Scheffzek K, Young P, Saraste M (2001) Crystal structure of the alpha-actinin rod reveals an extensive torsional twist. Structure (Camb) 9: 597-604