Crystal structure of the ATP-dependent maturation factor of Ni,Fe-containing carbon monoxide dehydrogenases

Journal of Molecular Biology

Volumn 396, Issue 4, 2010, Pages 1165-1179

  Jeoung, Jae Hun ^a   Giese, Till ^a   Grünwald, Marlene ^a   Dobbek, Holger ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Carboxydothermus hydrogenoformans; CODH; CooC1; Nickel; Zinc

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CARBON MONOXIDE DEHYDROGENASE; IRON; NICKEL; NUCLEOTIDE; PROTEIN COOC1; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; BACTERIUM; BINDING SITE; CARBOXYDOTHERMUS HYDROGENOFORMANS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME BINDING; ENZYME STRUCTURE; METAL BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN MOTIF;

BACTERIA (MICROORGANISMS); CARBOXYDOTHERMUS HYDROGENOFORMANS;

EID: 77649270822     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.12.062     Document Type: Article

References (58)

1. Kuchar J., Hausinger R.P. Biosynthesis of metal sites. Chem. Rev. 2004, 104:509-525.
2. Zambelli B., Stola M., Musiani F., De Vriendt K., Samyn B., Devreese B., et al. UreG, a chaperone in the urease assembly process, is an intrinsically unstructured GTPase that specifically binds Zn. J. Biol. Chem. 2005, 280:4684-4695.
3. Leach M.R., Zamble D.B. Metallocenter assembly of the hydrogenase enzymes. Curr. Opin. Chem. Biol. 2007, 11:159-165.
4. Loke H.K., Lindahl P.A. Identification and preliminary characterization of AcsF, a putative Ni-insertase used in the biosynthesis of acetyl-CoA synthase from Clostridium thermoaceticum. J. Inorg. Biochem. 2003, 93:33-40.
5. Jeon W.B., Cheng J.J., Ludden P.W. Purification and characterization of membrane-associated CooC protein and its functional role in the insertion of nickel into carbon monoxide dehydrogenase from Rhodospirillum rubrum. J. Biol. Chem. 2001, 276:38602-38609.
6. Jeoung J.-H., Giese T., Grünwald M., Dobbek H. CooC1 from Carboxydothermus hydrogenoformans is a nickel-binding ATPase. Biochemistry 2009, 48:11505-11513.
7. Leipe D.D., Wolf Y.I., Koonin E.V., Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 2002, 317:41-72.
8. Maier T., Lottspeich F., Bock A. GTP hydrolysis by HypB is essential for nickel insertion into hydrogenase of Escherichia coli. Eur. J. Biochem. 1995, 230:133-138.
9. Soriano A., Hausinger R.P. GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins. Proc. Natl Acad. Sci. USA 1999, 96:11140-11144.
10. Gasper R., Scrima A., Wittinghofer A. Structural insights into HypB, a GTP-binding protein that regulates metal binding. J. Biol. Chem. 2006, 281:27492-27502.
11. Leach M.R., Sandal S., Sun H.W., Zamble D.B. Metal binding activity of the Escherichia coli hydrogenase maturation factor HypB. Biochemistry 2005, 44:12229-12238.
12. Dias A.V., Mulvihill C.M., Leach M.R., Pickering I.J., George G.N., Zamble D.B. Structural and biological analysis of the metal sites of Escherichia coli hydrogenase accessory protein HypB. Biochemistry 2008, 47:11981-11991.
13. Atanassova A., Zamble D.B. Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel. J. Bacteriol. 2005, 187:4689-4697.
14. Zhang J.W., Butland G., Greenblatt J.F., Emili A., Zamble D.B. A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J. Biol. Chem. 2005, 280:4360-4366.
15. Scholz C., Eckert B., Hagn F., Schaarschmidt P., Balbach J., Schmid F.X. SlyD proteins from different species exhibit high prolyl isomerase and chaperone activities. Biochemistry 2006, 45:20-33.
16. Weininger U., Haupt C., Schweimer K., Graubner W., Kovermann M., Bruser T., et al. NMR solution structure of SlyD from Escherichia coli: spatial separation of prolyl isomerase and chaperone function. J. Mol. Biol. 2009, 387:295-305.
17. Forzi L., Sawers R.G. Maturation of [NiFe]-hydrogenases in Escherichia coli. BioMetals 2007, 20:565-578.
18. Wu M., Ren Q.H., Durkin A.S., Daugherty S.C., Brinkac L.M., Dodson R.J., et al. Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z-2901. PLoS Genet. 2005, 1:563-574.
19. Dobbek H., Svetlitchnyi V., Gremer L., Huber R., Meyer O. Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 2001, 293:1281-1285.
20. Drennan C.L., Heo J.Y., Sintchak M.D., Schreiter E., Ludden P.W. Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase. Proc. Natl Acad. Sci. USA 2001, 98:11973-11978.
21. Darnault C., Volbeda A., Kim E.J., Legrand P., Vernede X., Lindahl P.A., Fontecilla-Camps J.C. Ni-Zn-[Fe4-S4] and Ni-Ni-[Fe4-S4] clusters in closed and open subunits of acetyl-CoA synthase/carbon monoxide dehydrogenase. Nat. Struct. Biol. 2003, 10:271-279.
22. Jeoung J.H., Dobbek H. Carbon dioxide activation at the Ni,Fe-cluster of anaerobic carbon monoxide dehydrogenase. Science 2007, 318:1461-1464.
23. Ragsdale S.W. Life with carbon monoxide. Crit. Rev. Biochem. Mol. 2004, 39:165-195.
24. Jeoung J.H., Dobbek H. Ni-containing carbon monoxide dehydrogenase. Handbook of Metalloproteins 2007, John Wiley and Sons, New York, NY. A. Messerschmidt, R. Huber, T.L. Poulos, K. Wieghardt (Eds.).
25. Lindahl P.A. Implications of a carboxylate-bound C-cluster structure of carbon monoxide dehydrogenase. Angew. Chem. Int. Ed. 2008, 47:4054-4056.
26. Kerby R.L., Ludden P.W., Roberts G.P. In vivo nickel insertion into the carbon monoxide dehydrogenase of Rhodospirillum rubrum: molecular and physiological characterization of cooCTJ. J. Bacteriol. 1997, 179:2259-2266.
27. Lutkenhaus J., Sundaramoorthy M. MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol. Microbiol. 2003, 48:295-303.
28. Leonard T.A., Butler P.J., Lowe J. Bacterial chromosome segregation: structure and DNA binding of the Soj dimer-a conserved biological switch. EMBO J. 2005, 24:270-282.
29. Zhou T.Q., Radaev S., Rosen B.P., Gatti D.L. Structure of the ArsA ATPase: the catalytic subunit of a heavy metal resistance pump. EMBO J. 2000, 19:4838-4845.
30. - stabilized nitrogenase complex and its implications for signal transduction. Nature 1997, 387:370-376.
31. Chan J.M., Ryle M.J., Seefeldt L.C. Evidence that MgATP accelerates primary electron transfer in a Clostridium pasteurianum Fe protein-Azotobacter vinelandii MoFe protein nitrogenase tight complex. J. Biol. Chem. 1999, 274:17593-17598.
32. Hu Y.L., Corbett M.C., Fay A.W., Webber J.A., Hodgson K.O., Hedman B., Ribbe M.W. FeMo cofactor maturation on NifEN. Proc. Natl Acad. Sci. USA 2006, 103:17119-17124.
33. Hu Z., Lutkenhaus J. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 2003, 47:345-355.
34. Lutkenhaus J. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 2007, 76:539-562.
35. Cordell S.C., Lowe J. Crystal structure of the bacterial cell division regulator MinD. FEBS Lett. 2001, 492:160-165.
36. Sakai N., Yao M., Itou H., Watanabe N., Yumoto F., Tanokura M., Tanaka I. The three-dimensional structure of septum site-determining protein MinD from Pyrococcus horikoshii OT3 in complex with Mg-ADP. Structure 2001, 9:817-826.
37. Hayashi I., Oyama T., Morikawa K. Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. EMBO J. 2001, 20:1819-1828.
38. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
39. Holm L., Sander C. Protein-structure comparison by alignment of distance matrices. J. Mol. Biol. 1993, 233:123-138.
40. Vogeley L., Palm G.J., Mesters J.R., Hilgenfeld R. Conformational change of elongation factor Tu (EF-Tu) induced by antibiotic binding-crystal structure of the complex between EF-Tu center dot GDP and aurodox. J. Biol. Chem. 2001, 276:17149-17155.
41. Georgiadis M.M., Komiya H., Chakrabarti P., Woo D., Kornuc J.J., Rees D.C. Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science 1992, 257:1653-1659.
42. Mateja A., Szlachcic A., Downing M.E., Dobosz M., Mariappan M., Hegde R.S., Keenan R.J. The structural basis of tail-anchored membrane protein recognition by Get3. Nature 2009, 461:361-366.
43. Walker J.E., Saraste M., Runswick M.J., Gay N.J. Distantly related sequences in the alpha-subunits and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1:945-951.
44. Sprang S.R. G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 1997, 66:639-678.
45. Moodie S.L., Thornton J.M. A study into the effects of protein-binding on nucleotide conformation. Nucleic Acids Res. 1993, 21:1369-1380.
46. Lo Conte L., Chothia C., Janin J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 1999, 285:2177-2198.
47. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 2004, 60:2126-2132.
48. Coyle C.L., Stiefel E.I. The coordination chemistry of nickel. The Bioinorganic Chemistry 1988, VCH Publishers, New York, NY. J.R.J. Lancaster (Ed.).
49. 2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation. Proteins Struct. Funct. Bioinf. 2009, 74:222-239.
50. Outten C.E., O'Halloran T.V. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 2001, 292:2488-2492.
51. Rees D.C. Great metalloclusters in enzymology. Annu. Rev. Biochem. 2002, 71:221-246.
52. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 1993, 26:795-800.
53. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. Sect. D 1999, 55:849-861.
54. Terwilliger T.C., Klei H., Adams P.D., Moriarty N.W., Cohn J.D. Automated ligand fitting by core-fragment fitting and extension into density. Acta Crystallogr. Sect. D 2006, 62:915-922.
55. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D 1998, 54:905-921.
56. 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.
57. 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. Crystallogr. 1993, 26:283-291.
58. Lee B., Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 1971, 55:379-400.