An intersubunit disulfide bridge stabilizes the tetrameric nucleoside diphosphate kinase of Aquifex aeolicus

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 6, 2012, Pages 1658-1668

  Boissier, Fanny ^a,b   Georgescauld, Florian ^a,b   Moynié, Lucile ^a,b   Dupuy, Jean William ^a   Sarger, Claude ^a,b   Podar, Mircea ^c   Lascu, Ioan ^a,b   Giraud, Marie France ^a,b   Dautant, Alain ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b Institut de Biochimie et Genetique Cellulaires   (France)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

Crystal structure; Hyperthermophile; Oligomerization; Radiation damage

Indexed keywords

CYSTEINE; DIMER; DISULFIDE; NUCLEOSIDE DIPHOSPHATE KINASE; TETRAMER;

ALKYLATION; ALPHA HELIX; AQUIFEX AEOLICUS; ARTICLE; CROSS LINKING; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ESCHERICHIA COLI; HYPERTHERMOPHILIC BACTERIUM; MYXOCOCCUS XANTHUS; PRIORITY JOURNAL; PROTEIN CONFORMATION; RADIATION INJURY;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; ENZYME STABILITY; HOT TEMPERATURE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOSIDE-DIPHOSPHATE KINASE; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; SULFATES; X-RAYS;

AQUIFEX AEOLICUS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MYXOCOCCUS XANTHUS;

EID: 84860611156     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24062     Document Type: Article

References (41)

1. Janin J, Dumas C, Moréra S, Xu Y, Meyer P, Chiadmi M, Cherfils J. Three-dimensional structure of nucleoside diphosphate kinase. J Bioenerg Biomembr 2000; 32: 215-225.
2. Williams RL, Oren DA, Muñoz-Dorado J, Inouye S, Inouye M, Arnold E. Crystal structure of Myxococcus xanthus nucleoside diphosphate kinase and its interaction with a nucleotide substrate at 2.0 A resolution. J Mol Biol 1993; 234: 1230-1247.
3. Moynié L, Giraud M-F, Georgescauld F, Lascu I, Dautant A. The structure of the Escherichia coli nucleoside diphosphate kinase reveals a new quaternary architecture for this enzyme family. Proteins 2007; 67: 755-765.
4. Tepper AD, Dammann H, Bominaar AA, Veron M. Investigation of the active site and the conformational stability of nucleoside diphosphate kinase by site-directed mutagenesis. J Biol Chem 1994; 269: 32175-32180.
5. Moréra S, LeBras G, Lascu I, Lacombe ML, Véron M, Janin J. Refined X-ray structure of Dictyostelium discoideum nucleoside diphosphate kinase at 1.8 Å resolution. J Mol Biol 1994; 243: 873-890.
6. Tokunaga H, Ishibashi M, Arisaka F, Arai S, Kuroki, R, Arakawa T, Tokunaga M. Residue 134 determines the dimer-tetramer assembly of nucleoside diphosphate kinase from moderately halophilic bacteria. FEBS Lett 2008; 582: 1049-1054.
7. Arai S, Yonezawa Y, Okazaki N, Matsumoto F, Tamada T, Tokunaga H, Ishibashi M, Blaber M, Tokunaga M, Kuroki R. A structural mechanism for dimeric to tetrameric oligomer conversion in halomonas sp. nucleoside diphosphate kinase. Protein Sci 2012; doi: 10.1002/pro.2032.
8. Shen R, Wheeler LJ, Mathews CK. Molecular interactions involving Escherichia coli nucleoside diphosphate kinase. J Bioenerg Biomembr 2006; 38: 255-259.
9. Misra G, Aggarwal A, Dube D, Zaman MS, Singh Y, Ramachandran R. Crystal structure of the Bacillus anthracis nucleoside diphosphate kinase and its characterization reveals an enzyme adapted to perform under stress conditions. Proteins 2009; 76: 496-506.
10. Takeishi S, Nakagawa N, Maoka N, Kihara M, Moriguchi M, Masui R, Kuramitsi S. Crystallization and preliminary X-ray diffraction studies of nucleoside diphosphate kinase from Thermus thermophilus HB8. Acta Crystallogr D 2003; 59: 1843-1845.
11. Kato-Murayama M, Murayama K, Shirouzu M, Yokoyama S. Crystal structure of nucleotide diphosphate kinase from Pyrococcus horikoshii, doi:10.2210/pdb2cwk/pdb.
12. Pédelacq J, Waldo GS, Cabantous S, Liong EC, Terwilliger TC. Structural and functional features of an NDP kinase from the hyperthermophile crenarchaeon Pyrobaculum aerophilum. Protein Sci 2005; 14: 2562-2573.
13. Lascu I, Kezdi M, Goia I, Jebeleanu G, Bârzu O, Pansini A, Papa S, Mantsch HH. Enzymatic properties of 8-bromoadenine nucleotides. Biochemistry 1979; 18: 4818-4826.
14. Leslie AGW. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 1992; 26.
15. CCP4. Collaborative Computational Project, Number 4. Acta Crystallogr D 1994; 50: 760-763.
16. DeLano WL. The PyMOL molecular graphics system. CA: DeLano Scientific; 2002.
17. Krissinel E. Crystal contacts as nature's docking solutions. J Comput Chem 2009; 31: 133-143.
18. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007; 40: 658-674.
19. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Cryst D 2004; 60: 2126-2132.
20. Adams PD, Gopal K, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Pai RK, Read RJ, Romo TD, Sacchettini JC, Sauter NK, Storoni LC, Terwilliger TC. Recent developments in the PHENIX software for automated crystallographic structure determination. J Synchrotron Radiat 2004; 11: 53-55.
21. Painter J, Merritt EA. TLSMD web server for the generation of multi-group TLS models. J Appl Crystallogr 2006; 39: 109-111.
22. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Cryst D 2010; 66: 12-21.
23. Gouet P, Courcelle E, Stuart DI, Metoz F. ESPript: multiple sequence alignments in PostScript. Bioinformatics 1999; 15: 305-308.
24. Chen Y, Gallois-Montbrun S, Schneider B, Véron M, Moréra S, Deville-Bonne D, Janin J. Nucleotide binding to nucleoside diphosphate kinases: X-ray structure of human NDPK-A in complex with ADP and comparison to protein kinases. J Mol Biol 2003; 332: 915-926.
25. Xu YW, Moréra S, Janin J, Cherfils J. AlF3 mimics the transition state of protein phosphorylation in the crystal structure of nucleoside diphosphate kinase and MgADP. Proc Natl Acad Sci USA 1997; 94: 3579-3583.
26. Richardson JS. The anatomy and taxonomy of protein structure. Adv Protein Chem 1981; 34: 167-339.
27. Haworth NL, Gready JE, George RA, Wouters MA. Evaluating the stability of disulfide bridges in proteins: a torsional potential energy surface for diethyl disulfide. Mol Simul 2007; 33: 475-485.
28. Weik M, Ravelli RB, Kryger G, McSweeney S, Raves ML, Harel M, Gros P, Silman I, Kroon J, Sussman JL. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc Natl Acad Sci USA 1999; 97: 623-628.
29. Karshikoff A, Ladenstein R. Ion pairs and the thermotolerance of proteins from hyperthermophiles: a 'traffic rule' for hot roads. Trends Biol Sci 2001; 26: 550-556.
30. Yano JK, Poulos TL. New understandings of thermostable and peizostable enzymes. Curr Opin Biotechnol 2003; 14: 360-365.
31. Ladenstein R, Ren B. Reconsideration of an early dogma, saying "there is no evidence for disulfide bonds in proteins from archaea". Extremophiles 2008; 12: 29-38.
32. Mallick P, Boutz DR, Eisenberg D, Yeates TO. Genomic evidence that the intracellular proteins of archaeal microbes contain disulfide bonds. Proc Natl Acad Sci USA 2002; 99: 9679-9684.
33. Boutz DR, Cascio D, Whitelegge J, Perry LJ, Yeates TO. Discovery of a thermophilic protein complex stabilized by topologically interlinked chains. J Mol Biol 2007; 368: 1332-1344.
34. Vieille C, Zeikus GJ. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 2001; 65: 1-43.
35. Walden H, Bell GS, Russell RJM, Siebersm B, Hensel R, Taylor GL. Tiny TIM: a small tetrameric, hyperthermostable triosephosphate isomerase. J Mol Biol 2001; 306: 745-757.
36. Nakka M, Iyer RB, Bachas LG. Intersubunit disulfide interactions play a critical role in maintaining the thermostability of glucose-6-phosphate dehydrogenase from the hyperthermophilic bacterium Aquifex aeolicus. Protein J 2006; 25: 17-21.
37. Bjørk A, Dalhus B, Mantzilas D, Eijsink VGH, Sirevåg R. Stabilization of a tetrameric malate dehydrogenase by introduction of a disulfide bridge at the dimer-dimer interface. J Mol Biol 2003; 334: 811-821.
38. Beeby M, O'Connor BD, Ryttersgaard C, Boutz DR, Perry LJ, Yeates TO. The genomics of disulfide bonding and protein stabilization in thermophiles. PLoS Biol 2005; 3: e309.
39. Dar HH, Chakraborti PK. Intermolecular phosphotransfer is crucial for efficient catalytic activity of nucleoside diphosphate kinase. Biochem J 2010; 430: 539-549.
40. Tokunaga H, Izutsu K-I, Arai S, Yonezawa Y, Kuroki R, Arakawa T, Tokunaga M. Dimer-tetramer assembly of nucleoside diphosphate kinase from moderately halophilic bacterium Chromohalobacter salexigens DSM3043: Both residues 134 and 136 are critical for the tetramer assembly. Enzyme Microb Technol 2010; 46: 129-135.
41. Gonin P, Xu Y, Milon L, Dabernat S, Morr M, Kumar R, Lacombe M-L, Janin J, Lascu I. Catalytic mechanism of nucleoside diphosphate kinase investigated using nucleotide analogues, viscosity effects, and X-ray crystallography. Biochemistry 1999; 38: 7265-7272.