Identification of a novel actin-binding domain within the Rho guanine nucleotide exchange factor TEM4

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Mitin, Natalia ^a   Rossman, Kent L ^a   Der, Channing J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; F ACTIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PLECKSTRIN; PROTEIN TEM4; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTIN BINDING DOMAIN; ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE DELETION; GENE LOCATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; POINT MUTATION; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS;

ACTINS; AMINO ACID SEQUENCE; ARGININE; CYTOSKELETON; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RHOA GTP-BINDING PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP; SUBCELLULAR FRACTIONS;

EID: 84864243965     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041876     Document Type: Article

References (66)

1. Vetter IR, Wittinghofer A, (2001) The guanine nucleotide-binding switch in three dimensions. Science 294: 1299-1304.
2. Rossman KL, Der CJ, Sondek J, (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167-180.
3. Schmidt A, Hall A, (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 16: 1587-1609.
4. Vega FM, Ridley AJ, (2007) SnapShot: Rho family GTPases. Cell 129: 1430.
5. Krendel M, Zenke FT, Bokoch GM, (2002) Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4: 294-301.
6. Nalbant P, Chang YC, Birkenfeld J, Chang ZF, Bokoch GM, (2009) Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol Biol Cell 20: 4070-4082.
7. Chang YC, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM, (2008) GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell 19: 2147-2153.
8. Tatsumoto T, Xie X, Blumenthal R, Okamoto I, Miki T, (1999) Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J Cell Biol 147: 921-928.
9. Wolfe BA, Takaki T, Petronczki M, Glotzer M, (2009) Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol 7: e1000110.
10. Fields AP, Justilien V, (2010) The guanine nucleotide exchange factor (GEF) Ect2 is an oncogene in human cancer. Adv Enzyme Regul 50: 190-200.
11. St Croix B, Rago C, Velculescu V, Traverso G, Romans KE, et al. (2000) Genes expressed in human tumor endothelium. Science 289: 1197-1202.
12. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5: 605-607.
13. Cai L, Marshall TW, Uetrecht AC, Schafer DA, Bear JE, (2007) Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 128: 915-929.
14. Roberts PJ, Mitin N, Keller PJ, Chenette EJ, Madigan JP, et al. (2008) Rho Family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J Biol Chem 283: 25150-25163.
15. Mitin N, Betts L, Yohe ME, Der CJ, Sondek J, et al. (2007) Release of autoinhibition of ASEF by APC leads to CDC42 activation and tumor suppression. Nat Struct Mol Biol 14: 814-823.
16. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD, (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124: 423-435.
17. Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, et al. (2005) Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 15: 1276-1285.
18. Cai L, Makhov AM, Bear JE, (2007) F-actin binding is essential for coronin 1B function in vivo. J Cell Sci 120: 1779-1790.
19. Pollard TD, (1986) Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol 103: 2747-2754.
20. Rumenapp U, Freichel-Blomquist A, Wittinghofer B, Jakobs KH, Wieland T, (2002) A mammalian Rho-specific guanine-nucleotide exchange factor (p164-RhoGEF) without a pleckstrin homology domain. Biochem J 366: 721-728.
21. De Toledo M, Colombo K, Nagase T, Ohara O, Fort P, et al. (2000) The yeast exchange assay, a new complementary method to screen for Dbl-like protein specificity: identification of a novel RhoA exchange factor. FEBS Lett 480: 287-292.
22. Welch HC, Coadwell WJ, Ellson CD, Ferguson GJ, Andrews SR, et al. (2002) P-Rex1, a PtdIns(3,4,5)P3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 108: 809-821.
23. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P, (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28: 231-234.
24. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
25. Lemmon MA, (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9: 99-111.
26. Baumeister MA, Rossman KL, Sondek J, Lemmon MA, (2006) The Dbs PH domain contributes independently to membrane targeting and regulation of guanine nucleotide-exchange activity. Biochem J 400: 563-572.
27. Fuentes EJ, Karnoub AE, Booden MA, Der CJ, Campbell SL, (2003) Critical role of the pleckstrin homology domain in Dbs signaling and growth regulation. J Biol Chem 278: 21188-21196.
28. Coue M, Brenner SL, Spector I, Korn ED, (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett 213: 316-318.
29. Djinovic Carugo K, Banuelos S, Saraste M, (1997) Crystal structure of a calponin homology domain. Nat Struct Biol 4: 175-179.
30. Banuelos S, Saraste M, Djinovic Carugo K, (1998) Structural comparisons of calponin homology domains: implications for actin binding. Structure 6: 1419-1431.
31. Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ, (2002) Functional plasticity of CH domains. FEBS Lett 513: 98-106.
32. Blanchoin L, Pollard TD, (2002) Hydrolysis of ATP by polymerized actin depends on the bound divalent cation but not profilin. Biochemistry 41: 597-602.
33. Pollard TD, Blanchoin L, Mullins RD, (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29: 545-576.
34. Pollard TD, Borisy GG, (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453-465.
35. Blanchoin L, Pollard TD, Mullins RD, (2000) Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr Biol 10: 1273-1282.
36. Friederich E, Vancompernolle K, Huet C, Goethals M, Finidori J, et al. (1992) An actin-binding site containing a conserved motif of charged amino acid residues is essential for the morphogenic effect of villin. Cell 70: 81-92.
37. Banerjee J, Wedegaertner PB, (2004) Identification of a novel sequence in PDZ-RhoGEF that mediates interaction with the actin cytoskeleton. Mol Biol Cell 15: 1760-1775.
38. Obaishi H, Nakanishi H, Mandai K, Satoh K, Satoh A, et al. (1998) Frabin, a novel FGD1-related actin filament-binding protein capable of changing cell shape and activating c-Jun N-terminal kinase. J Biol Chem 273: 18697-18700.
39. Banerjee J, Fischer CC, Wedegaertner PB, (2009) The amino acid motif L/IIxxFE defines a novel actin-binding sequence in PDZ-RhoGEF. Biochemistry 48: 8032-8043.
40. Ruskamo S, Ylanne J, (2009) Structure of the human filamin A actin-binding domain. Acta Crystallogr D Biol Crystallogr 65: 1217-1221.
41. Mohl M, Winkler S, Wieland T, Lutz S, (2006) Gef10 - the third member of a Rho-specific guanine nucleotide exchange factor subfamily with unusual protein architecture. Naunyn Schmiedebergs Arch Pharmacol 373: 333-341.
42. Winkler S, Mohl M, Wieland T, Lutz S, (2005) GrinchGEF - a novel Rho-specific guanine nucleotide exchange factor. Biochem Biophys Res Commun 335: 1280-1286.
43. Svitkina TM, Borisy GG, (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145: 1009-1026.
44. Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, et al. (2000) Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151: 29-40.
45. Cai L, Makhov AM, Schafer DA, Bear JE, (2008) Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134: 828-842.
46. Bravo-Cordero JJ, Oser M, Chen X, Eddy R, Hodgson L, et al. (2011) A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr Biol 21: 635-644.
47. Hall A, Nobes CD, (2000) Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond B Biol Sci 355: 965-970.
48. Aktories K, Just I, (2005) Clostridial Rho-inhibiting protein toxins. Curr Top Microbiol Immunol 291: 113-145.
49. Ridley AJ, (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16: 522-529.
50. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709.
51. Raftopoulou M, Hall A, (2004) Cell migration: Rho GTPases lead the way. Dev Biol 265: 23-32.
52. Simpson KJ, Dugan AS, Mercurio AM, (2004) Functional analysis of the contribution of RhoA and RhoC GTPases to invasive breast carcinoma. Cancer Res 64: 8694-8701.
53. Hakem A, Sanchez-Sweatman O, You-Ten A, Duncan G, Wakeham A, et al. (2005) RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev 19: 1974-1979.
54. Narumiya S, Tanji M, Ishizaki T, (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev 28: 65-76.
55. Ridley AJ, (2001) Rho family proteins: coordinating cell responses. Trends Cell Biol 11: 471-477.
56. Buchsbaum RJ, Connolly BA, Feig LA, (2002) Interaction of Rac exchange factors Tiam1 and Ras-GRF1 with a scaffold for the p38 mitogen-activated protein kinase cascade. Mol Cell Biol 22: 4073-4085.
57. Connolly BA, Rice J, Feig LA, Buchsbaum RJ, (2005) Tiam1-IRSp53 Complex Formation Directs Specificity of Rac-Mediated Actin Cytoskeleton Regulation. Mol Cell Biol 25: 4602-4614.
58. Ito M, Yoshioka K, Akechi M, Yamashita S, Takamatsu N, et al. (1999) JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway. Mol Cell Biol 19: 7539-7548.
59. Kelkar N, Gupta S, Dickens M, Davis RJ, (2000) Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3. Mol Cell Biol 20: 1030-1043.
60. Chen CK, Chan NL, Wang AH, (2011) The many blades of the beta-propeller proteins: conserved but versatile. Trends Biochem Sci 36: 553-561.
61. Sondek J, Bohm A, Lambright DG, Hamm HE, Sigler PB, (1996) Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 379: 369-374.
62. Zheng J, Chen RH, Corblan-Garcia S, Cahill SM, Bar-Sagi D, et al. (1997) The solution structure of the pleckstrin homology domain of human SOS1. A possible structural role for the sequential association of diffuse B cell lymphoma and pleckstrin homology domains. J Biol Chem 272: 30340-30344.
63. Worthylake DK, Rossman KL, Sondek J, (2000) Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1. Nature 408: 682-688.
64. Skowronek KR, Guo F, Zheng Y, Nassar N, (2004) The C-terminal basic tail of RhoG assists the guanine nucleotide exchange factor trio in binding to phospholipids. J Biol Chem 279: 37895-37907.
65. Gibrat JF, Madej T, Bryant SH, (1996) Surprising similarities in structure comparison. Curr Opin Struct Biol 6: 377-385.
66. Rost B, Yachdav G, Liu J, (2004) The PredictProtein server. Nucleic Acids Res 32: W321-326.