The RalB-RLIP76 complex reveals a novel mode of ral-effector interaction

Structure

Volumn 18, Issue 8, 2010, Pages 985-995

  Fenwick, R Brynmor ^a,c   Campbell, Louise J ^a   Rajasekar, Karthik ^a   Prasannan, Sunil ^a,d   Nietlispach, Daniel ^a   Camonis, Jacques ^b   Owen, Darerca ^a   Mott, Helen R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUT CURIE   (France)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Cellbio; Signaling

Indexed keywords

EXOCYST; MUTANT PROTEIN; PROTEIN RALB; PROTEIN RLIP76; RAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; CRYSTALLOGRAPHY, X-RAY; GTPASE-ACTIVATING PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIPROTEIN COMPLEXES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RAL GTP-BINDING PROTEINS; SCINTILLATION COUNTING; SEQUENCE ALIGNMENT; VESICULAR TRANSPORT PROTEINS;

EID: 77955480325     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2010.05.013     Document Type: Article

References (47)

1. Awasthi S., Cheng J.Z., Singhal S.S., Pandya U., Sharma R., Singh S.V., Zimniak P., Awasthi Y.C. Functional reassembly of ATP-dependent xenobiotic transport by the N- and C-terminal domains of RLIP76 and identification of ATP binding sequences. Biochemistry 2001, 40:4159-4168.
2. Awasthi S., Sharma R., Yang Y.S., Singhal S.S., Pikula S., Bandorowicz-Pikula J., Singh S.V., Zimniak P., Awasthi Y.C. Transport functions and physiological significance of 76 kDa Ral-binding GTPase activating protein (RLIP76). Acta Biochim. Pol. 2002, 49:855-867.
3. Bauer B., Mirey G., Vetter I.R., Garcia-Ranea J.A., Valencia A., Wittinghofer A., Camonis J.H., Cool R.H. Effector recognition by the small GTP-binding proteins Ras and Ral. J. Biol. Chem. 1999, 274:17763-17770.
4. Brunger 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. 1998, 54:905-921.
5. Cantor S.B., Urano T., Feig L.A. Identification and characterization of Ral-binding protein-1, a potential downstream target of Ral Gtpases. Mol. Cell. Biol. 1995, 15:4578-4584.
6. Cavanagh J., Fairbrother W.J., Palmer A.G., Rance M., Skelton N.J. Protein NMR Spectroscopy: Principles and Practice 2007, Academic Press, San Diego. Second Edition.
7. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 1999, 13:289-302.
8. Eathiraj S., Pan X.J., Ritacco C., Lambright D.G. Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 2005, 436:415-419.
9. Elliot-Smith A.E., Owen D., Mott H.R., Lowe P.N. Double mutant cycle thermodynamic analysis of the hydrophobic Cdc42-ACK protein-protein interaction. Biochemistry 2007, 46:14087-14099.
10. Fenwick R.B., Prasannan S., Campbell L.J., Evetts K.A., Nietlispach D., Owen D., Mott H.R. H-1, C-13 and N-15 resonance assignments for the active conformation of the small G protein RalB in complex with its effector RLIP76. Biomol. NMR Assign. 2008, 2:179-182.
11. Fenwick R.B., Prasannan S., Campbell L.J., Evetts K.A., Nietlispach D., Owen D., Mott H.R. Resonance assignments for the RLIP76 Ral binding domain in its free form and in complex with the small G protein RalB. Biomol. NMR Assign. 2008, 2:191-194.
12. Fenwick R.B., Prasannan S., Campbell L.J., Nietlispach D., Evetts K.A., Camonis J., Mott H.R., Owen D. Solution structure and dynamics of the small GTPase RalB in its active conformation: significance for effector protein binding. Biochemistry 2009, 48:2192-2206.
13. Frankel P., Aronheim A., Kavanagh E., Balda M.S., Matter K., Bunney T.D., Marshall C.J. RalA interacts with ZONAB in a cell density-dependent manner and regulates its transcriptional activity. EMBO J. 2005, 24:54-62.
14. Fukai S., Matern H.T., Jagath J.R., Scheller R.H., Brunger A.T. Structural basis of the interaction between RalA and Sec5, a subunit of the sec6/8 complex. EMBO J. 2003, 22:3267-3278.
15. Geyer M., Schweins T., Herrmann C., Prisner T., Wittinghofer A., Kalbitzer H.R. Conformational transitions in p21(ras) and in its complexes with the effector protein Raf-RBD and the GTPase activating protein GAP. Biochemistry 1996, 35:10308-10320.
16. Gildea J.J., Harding M.A., Seraj M.J., Gulding K.M., Theodorescu D. The role of Ral A in epidermal growth factor receptor-regulated cell motility. Cancer Res. 2002, 62:982-985.
17. Graham D.L., Eccleston J.F., Lowe P.N. The conserved arginine in Rho-GTPase-activating protein is essential for efficient catalysis but not for complex formation with rho CDP and aluminum fluoride. Biochemistry 1999, 38:985-991.
18. Hwang T.L., van Zijl P.C.M., Mori S. Accurate quantitation of water-amide proton exchange rates using the Phase-Modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a Fast-HSQC (FHSQC) detection scheme. J. Biomol. NMR 1998, 11:221-226.
19. Jiang H., Luo J.Q., Urano T., Frankel P., Lu Z.M., Foster D.A., Feig L.A. Involvement of Ral Gtpase in V-Src-induced phospholipase-D activation. Nature 1995, 378:409-412.
20. Jin R., Junutula J.R., Matern H.T., Ervin K.E., Scheller R.H., Brunger A.T. Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase. EMBO J. 2005, 24:2064-2074.
21. Jullien-Flores V., Dorseuil O., Romero F., Letourneur F., Saragosti S., Berger R., Tavitian A., Gacon G., Camonis J.H. Bridging Ral Gtpase to Rho-pathways-Rlip76, a Ral effector with Cdc42/Rac Gtpase-activating protein activity. J. Biol. Chem. 1995, 270:22473-22477.
22. Jullien-Flores V., Mahe Y., Mirey G., Leprince C., Meunier-Bisceuil B., Sorkin A., Camonis J.H. RLIP76, an effector of the GTPase Ral, interacts with the AP2 complex: involvement of the Ral pathway in receptor endocytosis. J. Cell Sci. 2000, 113:2837-2844.
23. Kraulis P.J. Molscript-a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 1991, 24:946-950.
24. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
25. Lim K.H., Brady D.C., Kashatus D.F., Ancrile B.B., Der C.J., Cox A.D., Counter C.M. Aurora-A phosphorylates, activates, and relocalizes the small GTPase RalA. Mol. Cell Biol. 2010, 30:508-523.
26. Linge J.P., O'Donoghue S.I., Nilges M. Automated assignment of ambiguous NOEs with ARIA. Methods Enzymol. 2001, 339:71-90.
27. Maesaki R., Ihara K., Shimizu T., Kuroda S., Kaibuchi K., Hakoshima T. The structural basis of Rho effector recognition revealed by the crystal structure of human RhoA complexed with the effector domain of PKN/PRK1. Mol. Cell 1999, 4:793-803.
28. Merritt E.A., Bacon D.J. Raster3D: Photorealistic molecular graphics. Methods Enzymol. 1997, 277:505-524.
29. Modha R., Campbell L.J., Nietlispach D., Buhecha H.R., Owen D., Mott H.R. The Rac1 polybasic region is required for interaction with its effector PRK1. J. Biol. Chem. 2008, 283:1492-1500.
30. Moskalenko S., Henry D.O., Rosse C., Mirey G., Camonis J.H., White M.A. The exocyst is a Ral effector complex. Nat. Cell Biol. 2002, 4:66-72.
31. Moskalenko S., Tong C., Rosse C., Mirey G., Formstecher E., Daviet L., Camonis J., White M.A. Ral GTPases regulate exocyst assembly through dual subunit interactions. J. Biol. Chem. 2003, 278:51743-51748.
32. Nicely N.I., Kosak J., de Serrano V., Mattos C. Crystal structures of Ral-GppNHp and Ral-GDP reveal two binding sites that are also present in Ras and Rap. Structure 2004, 12:2025-2036.
33. Ohta Y., Suzuki N., Nakamura S., Hartwig J.H., Stossel T.P. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. USA 1999, 96:2122-2128.
34. Panic B., Perisic O., Veprintsev D.B., Williams R.L., Munro S. Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus. Mol. Cell 2003, 12:863-874.
35. Park S.H., Weinberg R.A. A putative effector of Ral has homology to Rho/Rac GTPase activating proteins. Oncogene 1995, 11:2349-2355.
36. Prasannan S., Fenwick R.B., Campbell L.J., Evetts K.A., Nietlispach D., Owen D., Mott H.R. H-1, C-13, and N-15 resonance assignments for the small G protein RalB in its active conformation. Biomol. NMR Assign. 2007, 1:147-149.
37. Sidhu R.S., Clough R.R., Bhullar R.P. Regulation of phospholipase C-delta 1 through direct interactions with the small GTPase Ral and calmodulin. J. Biol. Chem. 2005, 280:21933-21941.
38. Sporn M.B. The war on cancer. Lancet 1996, 347:1377-1381.
39. Strugnell S.A., Wiefling B.A., DeLuca H.F. A modified pGEX vector with a C-terminal histidine tag: recombinant double-tagged protein obtained in greater yield and purity. Anal. Biochem. 1997, 254:147-149.
40. Sugihara K., Asano S., Tanaka K., Iwamatsu A., Okawa K., Ohta Y. The exocyst complex binds the small GTPase RaIA to mediate filopodia formation. Nat. Cell Biol. 2002, 4:73-78.
41. Thompson G., Owen D., Chalk P.A., Lowe P.N. Delineation of the Cdc42/Rac-binding domain of p21-activated kinase. Biochemistry 1998, 37:7885-7891.
42. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas P., Ulrich E.L., Markley J.L., Ionides J., Laue E.D. The CCPN data model for NMR spectroscopy: Development of a software pipeline. Proteins 2005, 59:687-696.
43. Wang Z.X. An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule. FEBS Lett. 1995, 360:111-114.
44. Ward Y., Wang W., Woodhouse E., Linnoila I., Liotta L., Kelly K. Signal pathways which promote invasion and metastasis: critical and distinct contributions of extracellular signal-regulated kinase and Ral-specific guanine exchange factor pathways. Mol. Cell. Biol. 2001, 21:5958-5969.
45. Wu M., Lu L., Hong W.J., Song H.W. Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Arl1. Nat. Struct. Mol. Biol. 2004, 11:86-94.
46. Yamaguchi A., Urano T., Goi T., Feig L.A. An eps homology (EH) domain protein that binds to the Ral-GTPase target, RalBP1. J. Biol. Chem. 1997, 272:31230-31234.
47. Ye M., Shima F., Muraoka S., Liao J.L., Okamoto H., Yamamoto M., Tamura A., Yagi N., Ueki T., Kataoka T. Crystal structure of M-Ras reveals a GTP-bound "off" state conformation of Ras family small GTPases. J. Biol. Chem. 2005, 280:31267-31275.