SAXS and X-ray Crystallography Suggest an Unfolding Model for the GDP/GTP Conformational Switch of the Small GTPase Arf6

Journal of Molecular Biology

Volumn 402, Issue 4, 2010, Pages 696-707

  Biou, Valérie ^a   Aizel, Kaheina ^a   Roblin, Pierre ^b   Thureau, Aurélien ^c   Jacquet, Eric ^c   Hansson, Sebastian ^a   Guibert, Bernard ^a   Guittet, Eric ^c   van Heijenoort, Carine ^c   Zeghouf, Mahel ^a   Perez, Javier ^b   Cherfils, Jacqueline ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b SYNCHROTRON SOLEIL   (France)

^c CNRS   (France)

Author keywords

Arf; Crystal structure; NMR; SAXS; Small GTPases

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BREFELDIN A; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; ISOPROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6;

AB INITIO CALCULATION; ANALYTIC METHOD; ARTICLE; BETA SHEET; CONFORMATIONAL TRANSITION; HYDRODYNAMICS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY; CHEMISTRY; HUMAN; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

ADP-RIBOSYLATION FACTORS; CRYSTALLOGRAPHY, X-RAY; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HUMANS; PROTEIN CONFORMATION; PROTEIN FOLDING; SCATTERING, SMALL ANGLE; THERMODYNAMICS; X-RAY DIFFRACTION;

EID: 77956899406     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.08.002     Document Type: Article

References (46)

1. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 2006, 7:347-358.
2. Gillingham A.K., Munro S. The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 2007, 23:579-611.
3. Donaldson J.G., Honda A. Localization and function of Arf family GTPases. Biochem. Soc. Trans. 2005, 33:639-642.
4. DiNitto J.P., Delprato A., Gabe Lee M.T., Cronin T.C., Huang S., Guilherme A., et al. Structural basis and mechanism of autoregulation in 3-phosphoinositide-dependent Grp1 family Arf GTPase exchange factors. Mol. Cell 2007, 28:569-583.
5. Cohen L.A., Honda A., Varnai P., Brown F.D., Balla T., Donaldson J.G. Active Arf6 recruits ARNO/cytohesin GEFs to the PM by binding their PH domains. Mol. Biol. Cell 2007, 18:2244-2253.
6. Macia E., Chabre M., Franco M. Specificities for the small G proteins ARF1 and ARF6 of the guanine nucleotide exchange factors ARNO and EFA6. J. Biol. Chem. 2001, 276:24925-24930.
7. Zeeh J.C., Zeghouf M., Grauffel C., Guibert B., Martin E., Dejaegere A., Cherfils J. Dual specificity of the interfacial inhibitor brefeldin A for Arf proteins and Sec7 domains. J. Biol. Chem. 2006, 281:11805-11814.
8. Amor J.C., Harrison D.H., Kahn R.A., Ringe D. Structure of the human ADP-ribosylation factor 1 complexed with GDP. Nature 1994, 372:704-708.
9. Menetrey J., Macia E., Pasqualato S., Franco M., Cherfils J. Structure of Arf6-GDP suggests a basis for guanine nucleotide exchange factors specificity. Nat. Struct. Biol. 2000, 7:466-469.
10. Goldberg J. Structural basis for activation of ARF GTPase: mechanisms of guanine nucleotide exchange and GTP-myristoyl switching. Cell 1998, 95:237-248.
11. Pasqualato S., Menetrey J., Franco M., Cherfils J. The structural GDP/GTP cycle of human Arf6. EMBO Rep. 2001, 2:234-238.
12. Mossessova E., Corpina R.A., Goldberg J. Crystal structure of ARF1*Sec7 complexed with brefeldin A and its implications for the guanine nucleotide exchange mechanism. Mol. Cell 2003, 12:1403-1411.
13. Renault L., Guibert B., Cherfils J. Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature 2003, 426:525-530.
14. Henzler-Wildman K., Kern D. Dynamic personalities of proteins. Nature 2007, 450:964-972.
15. Pasqualato S., Renault L., Cherfils J. Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication. EMBO Rep. 2002, 3:1035-1041.
16. Peyroche A., Antonny B., Robineau S., Acker J., Cherfils J., Jackson C.L. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol. Cell 1999, 3:275-285.
17. Antonny B., Beraud-Dufour S., Chardin P., Chabre M. N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange. Biochemistry 1997, 36:4675-4684.
18. Pasqualato S., Renault L., Cherfils J. The GDP/GTP cycle of Arf proteins. Structural and biochemical aspects. The ARF Book 2004, Kluwer Academic Publishers, Boston, MA. R.A. Kahn (Ed.).
19. 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.
20. Koch M.H., Vachette P., Svergun D.I. Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q. Rev. Biophys. 2003, 36:147-227.
21. Rambo R.P., Tainer J.A. Bridging the solution divide: comprehensive structural analyses of dynamic RNA, DNA, and protein assemblies by small-angle X-ray scattering. Curr. Opin. Struct. Biol. 2010, 20:128-137.
22. Putnam C.D., Hammel M., Hura G.L., Tainer J.A. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys. 2007, 40:191-285.
23. Franke D., Svergun D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 2009, 42:342-346.
24. Kozin M.B., Svergun D.I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 2000, 34:33-41.
25. Ericsson U.B., Hallberg B.M., Detitta G.T., Dekker N., Nordlund P. Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal. Biochem. 2006, 357:289-298.
26. Pantoliano M.W., Petrella E.C., Kwasnoski J.D., Lobanov V.S., Myslik J., Graf E., et al. High-density miniaturized thermal shift assays as a general strategy for drug discovery. J. Biomol. Screen. 2001, 6:429-440.
27. Chavas L.M.G., Torii S., Kamikubo H., Kawasaki M., Ihara K., Kato R., et al. Structure of the small GTPase Rab27b shows an unexpected swapped dimer. Acta Crystallogr. Sect. D 2007, 63:769-779.
28. Ostrowski M., Carmo N.B., Krumeich S., Fanget I., Raposo G., Savina A., et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2010, 12:19-30.
29. Chavrier P., Franco M. Expression, purification, and biochemical properties of EFA6, a Sec7 domain-containing guanine exchange factor for ADP-ribosylation factor 6 (ARF6). Methods Enzymol. 2001, 329:272-279.
30. Kabsch W. XDS. Acta Crystallogr. Sect. D 2010, 66:125-132.
31. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J. Appl. Crystallogr. 2007, 40:658-674.
32. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 2004, 60:2126-2132.
33. Blanc E., Roversi P., Vonrhein C., Flensburg C., Lea S.M., Bricogne G. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. Sect. D 2004, 60:2210-2221.
34. Garcia De La Torre J., Huertas M.L., Carrasco B. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 2000, 78:719-730.
35. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
36. David G., Perez J. Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline. J. Appl. Crystallogr. 2009, 42:892-900.
37. Konarev P.V., Volkov V.V., Petoukhov M.V., Svergun D.I. ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 2006, 39:277-286.
38. Guinier A. La diffraction des rayons X aux très petits angles: application à l'étude de phénomènes ultramicroscopiques. Ann.de Phys. (Paris) 1939, 12:161-237.
39. Svergun D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 1992, 25:495-503.
40. Svergun D.I., Barberato C., Koch M.H.J. CRYSOL, a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 1995, 28:768-773.
41. Kozin M.B., Svergun D.I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 2001, 34:33-41.
42. Lescop E., Schanda P., Brutscher B. A set of BEST triple-resonance experiments for time-optimized protein resonance assignment. J. Magn. Reson. 2007, 187:163-169.
43. Zur Y. An algorithm to calculate the NMR signal of a multi spin-echo sequence with relaxation and spin-diffusion. J. Magn. Reson. 2004, 171:97-106.
44. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 1995, 6:277-293.
45. Lee W., Westler W.M., Bahrami A., Eghbalnia H.R., Markley J.L. PINE-SPARKY: graphical interface for evaluating automated probabilistic peak assignments in protein NMR spectroscopy. Bioinformatics 2009, 25:2085-2087.
46. Charveriat M., Reboul M., Wang Q., Picoli C., Lenuzza N., Montagnac A., et al. New inhibitors of prion replication that target the amyloid precursor. J. Gen. Virol. 2009, 90:1294-1301.