Crystal structures of the human G3BP1 NTF2-like domain visualize FxFG Nup repeat specificity

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Vognsen, Tina ^a   Møller, Ingvar Runár ^a   Kristensen, Ole ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; GLYCINE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; LEUCINE; NUCLEOPORIN; PHENYLALANINE; PROTEIN FXFG; PROTEIN G3BP1; PROTEIN NTF2; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CRYSTALLOGRAPHY; HUMAN; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR MECHANICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID MOTIFS; BINDING SITES; CARRIER PROTEINS; CELL CYCLE PROTEINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PREGNANCY PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84891898406     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080947     Document Type: Article

References (50)

1. Barnes CJ, Li F, Mandal M, Yang Z, Sahin A, et al. (2002) Heregulin induces expression, ATPase activity, and nuclear localization of G3BP, a Ras signaling component, in human breast tumors. Cancer Res 62: 1251-1255.
2. French J, Stirling R, Walsh M, Kennedy HD (2002) The expression of Ras-GTPase activating protein SH3 domain-binding proteins, G3BPs, in human breast cancers. Histochem J 34: 223-231.
3. Guitard E, Parker F, Millon R, Abecassis J, Tocqué B (2001) G3BP is overexpressed in human tumors and promotes S phase entry. Cancer Lett 162: 213-221.
4. Zhang H-Z, Liu J-G, Wei Y-P, Wu C, Cao Y-K, et al. (2007) Expression of G3BP and RhoC in esophageal squamous carcinoma and their effect on prognosis. World J Gastroenterol 13: 4126-4130.
5. Shim J-H, Su Z-Y, Chae J-I, Kim DJ, Zhu F, et al. (2010) Epigallocatechin gallate suppresses lung cancer cell growth through Ras-GTPase-activating protein SH3 domain-binding protein 1. Cancer Prev Res (Phila) 3: 670-679.
6. Cui W, Wei Z, Chen Q, Cheng Y, Geng L, et al. (2010) Structure-based design of peptides against G3BP with cytotoxicity on tumor cells. J Chem Inf Model 50: 380-387.
7. Zhang H, Zhang S, He H, Zhao W, Chen J, et al. (2012) GAP161 targets and downregulates G3BP to suppress cell growth and potentiate cisplaitin-mediated cytotoxicity to colon carcinoma HCT116 cells. Cancer Sci: 1-9.
8. Tourrière H, Chebli K, Zekri L, Courselaud B, Blanchard JM, et al. (2003) The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol 160: 823-831.
9. Gallouzi IE, Parker F, Chebli K, Maurier F, Labourier E, et al. (1998) A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol Cell Biol 18: 3956-3965.
10. Atlas R, Behar L, Elliott E, Ginzburg I (2004) The insulin-like growth factor mRNA binding-protein IMP-1 and the Ras-regulatory protein G3BP associate with tau mRNA and HuD protein in differentiated P19 neuronal cells. J Neurochem 89: 613-626. Available: http://www.ncbi.nlm.nih.gov/pubmed/15086518. Accessed 11 August 2011.
11. Taniuchi K, Nishimori I, Hollingsworth M a (2011) The N-terminal domain of G3BP enhances cell motility and invasion by posttranscriptional regulation of BART. Mol Cancer Res 9: 856-866.
12. Prigent M, Barlat I, Langen H, Dargemont C (2000) IkappaBalpha and IkappaBalpha/NF-kappa B complexes are retained in the cytoplasm through interaction with a novel partner, RasGAP SH3-binding protein 2. J Biol Chem 275: 36441-36449.
13. Kennedy D, French J, Guitard E, Ru K, Tocque B, et al. (2002) Characterization of G3BPs: Tissue Specific Expression, Chromosomal Localisation and rasGAP 120 Binding Studies. J Cell Biochem 187.
14. Parker F, Maurier F, Delumeau I, Duchesne M, Faucher D, et al. (1996) A Ras-GTPase-activating protein SH3-domain-binding protein. Mol Cell Biol 16: 2561-2569.
15. Bikkavilli RK, Malbon CC (2011) Arginine methylation of G3BP1 in response to Wnt3a regulates β-catenin mRNA. J Cell Sci 124: 2310-2320.
16. Bikkavilli, Rama Kamesh and Malbon CC (2012) Wnt3a-stimulated LRP6 phosphorylation is dependent upon arginine methylation of G3BP2. J Cell Sci 125: 2446-2456.
17. Annibaldi A, Dousse A, Martin S, Tazi J, Widmann C (2011) Revisiting G3BP1 as a RasGAP Binding Protein: Sensitization of Tumor Cells to Chemotherapy by the RasGAP 317-326 Sequence Does Not Involve G3BP1. PLoS One 6: e29024.
18. Xu C, Wang P, Liu Y, Zhang Y, Fan W, et al. (2013) Integrative genomics in combination with RNA interference identifies prognostic and functionally relevant gene targets for oral squamous cell carcinoma. PLoS Genet 9: e1003169.
19. Solomon S, Xu Y, Wang B, David MD, Schubert P, et al. (2007) Distinct structural features of caprin-1 mediate its interaction with G3BP-1 and its induction of phosphorylation of eukaryotic translation initiation factor 2alpha, entry to cytoplasmic stress granules, and selective interaction with a subset of mRNAs. Mol Cell Biol 27: 2324-2342.
20. Vognsen T, Kristensen O (2012) Crystal structure of the Rasputin NTF2-like domain from Drosophila melanogaster. Biochem Biophys Res Commun 420: 188-192.
21. Clarkson WD, Kent HM, Stewart M (1996) Separate binding sites on nuclear transport factor 2 (NTF2) for GDP-Ran and the phenylalanine-rich repeat regions of nucleoporins p62 and Nsp1p. J Mol Biol 263: 517-524.
22. Fribourg S, Braun IC, Izaurralde E, Conti E (2001) Structural basis for the recognition of a nucleoporin FG repeat by the NTF2-like domain of the TAP/p15 mRNA nuclear export factor. Mol Cell 8: 645-656.
23. Bayliss R, Leung SW, Baker RP, Quimby BB, Corbett AH, et al. (2002) Structural basis for the interaction between NTF2 and nucleoporin FxFG repeats. EMBO J 21: 2843-2853.
24. Vognsen T, Möller IR, Kristensen O (2011) Purification, crystallization and preliminary X-ray diffraction of the G3BP1 NTF2-like domain. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 48-50.
25. Katsafanas GC, Moss B (2004) Vaccinia virus intermediate stage transcription is complemented by Ras-GTPase-activating protein SH3 domain-binding protein (G3BP) and cytoplasmic activation/proliferation- associated protein (p137) individually or as a heterodimer. J Biol Chem 279: 52210-52217.
26. Studier FW (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expr Purif 41: 207-234.
27. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
28. Winter G (2009) Xia2: an Expert System for Macromolecular Crystallography Data Reduction. J Appl Crystallogr 43: 186-190.
29. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
30. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
31. Vedadi M, Lew J, Artz J, Amani M, Zhao Y, et al. (2007) Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Mol Biochem Parasitol 151: 100-110.
32. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W (2003) Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr Sect D Biol Crystallogr 59: 2023-2030.
33. Adams PD, Afonine P V, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
34. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
35. Adams PD, Afonine P V, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
36. Chen VB, Arendall WB, Headd JJ, Keedy D a, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
37. Holm L, Rosenström P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-9.
38. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
39. Huang B, Schroeder M (2006) LIGSITEcsc: predicting ligand binding sites using the Connolly surface and degree of conservation. BMC Struct Biol 6: 19.
40. Soncini C, Berdo I, Draetta G (2001) Ras-GAP SH3 domain binding protein (G3BP) is a modulator of USP10, a novel human ubiquitin specific protease. Oncogene 20: 3869-3879.
41. Gao X, Ge L, Shao J, Su C, Zhao H, et al. (2010) Tudor-SN interacts with and co-localizes with G3BP in stress granules under stress conditions. FEBS Lett 584: 3525-3532.
42. Bayliss R, Littlewood T, Strawn L a, Wente SR, Stewart M (2002) GLFG and FxFG nucleoporins bind to overlapping sites on importin-beta. J Biol Chem 277: 50597-50606.
43. Bayliss R, Ribbeck K, Akin D, Kent HM, Feldherr CM, et al. (1999) Interaction between NTF2 and xFxFG-containing nucleoporins is required to mediate nuclear import of RanGDP. J Mol Biol 293: 579-593.
44. Chaillan-huntington C, Villa C, Stewart M (2000) Dissecting the Interactions between NTF2, RanGDP, and the Nucleoporin XFXFG Repeats*. Biochemistry 275: 5874-5879.
45. Tourriere H, Gallouzi I, Chebli K, Capony JP, Mouaikel J, et al. (2001) RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol Cell Biol 21: 7747.
46. Macara IG (2001) Transport into and out of the Nucleus. Microbiol Mol Biol Rev 65: 570-594.
47. Stewart M, Kent HM, McCoy a J (1998) Structural basis for molecular recognition between nuclear transport factor 2 (NTF2) and the GDP-bound form of the Ras-family GTPase Ran. J Mol Biol 277: 635-646.
48. Irvine K, Stirling R, Hume D, Kennedy D (2004) Rasputin, more promiscuous than ever: a review of G3BP. Int J Dev Biol 48: 1065-1077.
49. Kim MM, Wiederschain D, Kennedy D, Hansen E, Yuan Z-M (2007) Modulation of p53 and MDM2 activity by novel interaction with Ras-GAP binding proteins (G3BP). Oncogene 26: 4209-4215.
50. Eisenberg D, Schwarz E, Komaromy M, Wall R (1984) Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol 179: 125-142.