The initiation of GTP hydrolysis by the g-domain of FeoB: Insights from a transition-state complex structure

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Ash, Miriam Rose ^a   Maher, Megan J ^b   Guss, J Mitchell ^a   Jormakka, Mika ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b CENTENARY INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLUTAMINE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; POTASSIUM ION; PROTEIN NFEOB; SERINE; TYROSINE; UNCLASSIFIED DRUG; ALUMINUM DERIVATIVE; CATION TRANSPORT PROTEIN; FLUORIDE; GUANOSINE DIPHOSPHATE; POTASSIUM; TETRAFLUOROALUMINATE; THREONINE; WATER;

ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GENETIC CONSERVATION; HYDROLYSIS; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; RESIDUE ANALYSIS; STREPTOCOCCUS THERMOPHILUS; STRUCTURE ANALYSIS; WILD TYPE; AMINO ACID SEQUENCE; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

PROKARYOTA; STREPTOCOCCUS THERMOPHILUS;

ALUMINUM COMPOUNDS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BIOCATALYSIS; CATION TRANSPORT PROTEINS; CRYSTALLOGRAPHY, X-RAY; FLUORIDES; GTP PHOSPHOHYDROLASES; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HYDROLYSIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; POTASSIUM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOCOCCUS THERMOPHILUS; SUBSTRATE SPECIFICITY; THREONINE; WATER;

EID: 79961214373     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023355     Document Type: Article

References (50)

1. Kammler M, Schon C, Hantke K, (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175: 6212-6219.
2. Marlovits TC, Haase W, Herrmann C, Aller SG, Unger VM, (2002) The membrane protein FeoB contains an intramolecular G protein essential for Fe(II) uptake in bacteria. Proc Natl Acad Sci U S A 99: 16243-16248.
3. Velayudhan J, Hughes NJ, McColm AA, Bagshaw J, Clayton CL, et al. (2000) Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol Microbiol 37: 274-286.
4. Naikare H, Palyada K, Panciera R, Marlow D, Stintzi A, (2006) Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74: 5433-5444.
5. Robey M, Cianciotto NP, (2002) Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect Immun 70: 5659-5669.
6. Eng ET, Jalilian AR, Spasov KA, Unger VM, (2008) Characterization of a novel prokaryotic GDP dissociation inhibitor domain from the G protein coupled membrane protein FeoB. J Mol Biol 375: 1086-1097.
7. Hattori M, Jin Y, Nishimasu H, Tanaka Y, Mochizuki M, et al. (2009) Structural basis of novel interactions between the small-GTPase and GDI-like domains in prokaryotic FeoB iron transporter. Structure 17: 1345-1355.
8. Ash MR, Guilfoyle A, Clarke RJ, Guss JM, Maher MJ, et al. (2010) Potassium-activated GTPase reaction in the G Protein-coupled ferrous iron transporter B. J Biol Chem 285: 14594-14602.
9. Scrima A, Wittinghofer A, (2006) Dimerisation-dependent GTPase reaction of MnmE: how potassium acts as GTPase-activating element. EMBO J 25: 2940-2951.
10. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmuller L, Lautwein A, et al. (1997) The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277: 333-338.
11. Rittinger K, Walker PA, Eccleston JF, Smerdon SJ, Gamblin SJ, (1997) Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389: 758-762.
12. Seewald MJ, Korner C, Wittinghofer A, Vetter IR, (2002) RanGAP mediates GTP hydrolysis without an arginine finger. Nature 415: 662-666.
13. Bi X, Corpina RA, Goldberg J, (2002) Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419: 271-277.
14. Mishra R, Gara SK, Mishra S, Prakash B, (2005) Analysis of GTPases carrying hydrophobic amino acid substitutions in lieu of the catalytic glutamine: implications for GTP hydrolysis. Proteins 59: 332-338.
15. Hung KW, Chang YW, Eng ET, Chen JH, Chen YC, et al. (2010) Structural fold, conservation and Fe(II) binding of the intracellular domain of prokaryote FeoB. J Struct Biol 170: 501-512.
16. Koster S, Wehner M, Herrmann C, Kuhlbrandt W, Yildiz O, (2009) Structure and function of the FeoB G-domain from Methanococcus jannaschii. J Mol Biol 392: 405-419.
17. Guilfoyle A, Maher MJ, Rapp M, Clarke R, Harrop S, et al. (2009) Structural basis of GDP release and gating in G protein coupled Fe2+ transport. EMBO J 28: 2677-2685.
18. Leipe DD, Wolf YI, Koonin EV, Aravind L, (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317: 41-72.
19. Britton RA, (2009) Role of GTPases in bacterial ribosome assembly. Annu Rev Microbiol 63: 155-176.
20. Caldon CE, Yoong P, March PE, (2001) Evolution of a molecular switch: universal bacterial GTPases regulate ribosome function. Mol Microbiol 41: 289-297.
21. Anand B, Surana P, Prakash B, (2010) Deciphering the catalytic machinery in 30S ribosome assembly GTPase YqeH. PLoS One 5: e9944.
22. Harding MM, (2002) Metal-ligand geometry relevant to proteins and in proteins: sodium and potassium. Acta Crystallogr D Biol Crystallogr 58: 872-874.
23. Vetter IR, Wittinghofer A, (2001) The guanine nucleotide-binding switch in three dimensions. Science 294: 1299-1304.
24. Martin RB, (1988) Ternary hydroxide complexes in neutral solutions of Al3+ and F. Biochem Biophys Res Commun 155: 1194-1200.
25. Martin RB, (1996) Ternary complexes of Al3+ and F- with a third ligand. Coord Chem Rev 149: 23-32.
26. Birnbaumer L, Zurita AR, (2010) On the roles of Mg in the activation of G proteins. J Recept Signal Transduct Res 30: 372-375.
27. John J, Rensland H, Schlichting I, Vetter I, Borasio GD, et al. (1993) Kinetic and structural analysis of the Mg(2+)-binding site of the guanine nucleotide-binding protein p21H-ras. J Biol Chem 268: 923-929.
28. Zurita A, Zhang Y, Pedersen L, Darden T, Birnbaumer L, (2010) Obligatory role in GTP hydrolysis for the amide carbonyl oxygen of the Mg(2+)-coordinating Thr of regulatory GTPases. Proc Natl Acad Sci U S A 107: 9596-9601.
29. Bos JL, Rehmann H, Wittinghofer A, (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129: 865-877.
30. Bollag G, McCormick F, (1991) Differential regulation of rasGAP and neurofibromatosis gene product activities. Nature 351: 576-579.
31. Yamanaka K, Hwang J, Inouye M, (2000) Characterization of GTPase activity of TrmE, a member of a novel GTPase superfamily, from Thermotoga maritima. J Bacteriol 182: 7078-7082.
32. Hwang J, Inouye M, (2001) An essential GTPase, der, containing double GTP-binding domains from Escherichia coli and Thermotoga maritima. J Biol Chem 276: 31415-31421.
33. Tomar SK, Kumar P, Prakash B, (2011) Deciphering the catalytic machinery in a universally conserved ribosome binding ATPase YchF. Biochem Biophys Res Commun.
34. Bharat A, Jiang M, Sullivan SM, Maddock JR, Brown ED, (2006) Cooperative and critical roles for both G domains in the GTPase activity and cellular function of ribosome-associated Escherichia coli EngA. J Bacteriol 188: 7992-7996.
35. Robinson VL, Hwang J, Fox E, Inouye M, Stock AM, (2002) Domain arrangement of Der, a switch protein containing two GTPase domains. Structure 10: 1649-1658.
36. Tu C, Zhou X, Tropea JE, Austin BP, Waugh DS, et al. (2009) Structure of ERA in complex with the 3′ end of 16S rRNA: implications for ribosome biogenesis. Proc Natl Acad Sci U S A 106: 14843-14848.
37. Chakrabarti PP, Daumke O, Suveyzdis Y, Kotting C, Gerwert K, et al. (2007) Insight into catalysis of a unique GTPase reaction by a combined biochemical and FTIR approach. J Mol Biol 367: 983-995.
38. Frech M, John J, Pizon V, Chardin P, Tavitian A, et al. (1990) Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science 249: 169-171.
39. Scrima A, Thomas C, Deaconescu D, Wittinghofer A, (2008) The Rap-RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues. EMBO J 27: 1145-1153.
40. Huang B, Wu H, Hao N, Blombach F, van der Oost J, et al. (2010) Functional study on GTP hydrolysis by the GTP-binding protein from Sulfolobus solfataricus, a member of the HflX family. J Biochem 148: 103-113.
41. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC, (2006) Feo--transport of ferrous iron into bacteria. Biometals 19: 143-157.
42. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM, et al. (2002) Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 9: 401-406.
43. Otwinowski Z, Minor W, Charles W, Carter J, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 276: 307-326.
44. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
45. Collaborative Computational Project N (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
46. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
47. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
48. Kabsch W, (1976) A solution for the best rotation to relate two sets of vectors. Acta Crystallogr A 32: 922-923.
49. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
50. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.