Associative mechanism for phosphoryl transfer: A molecular dynamics simulation of Escherichia coli adenylate kinase complexed with its substrates

Proteins: Structure, Function and Genetics

Volumn 58, Issue 1, 2005, Pages 88-100

  Krishnamurthy, Harini ^a,b   Lou, Hongfeng ^b   Kimple, Adam ^b   Vieille, Claire ^a   Cukier, Robert I ^b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Adenylate kinase; Molecular dynamics; Phosphoryl transfer; TP and AMP

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; PHOSPHORYLASE;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME SUBSTRATE; GEOBACILLUS STEAROTHERMOPHILUS; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; REACTION ANALYSIS; SIMULATION; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS;

EID: 10844273276     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20301     Document Type: Article

References (57)

1. Walsh C. Enzymatic reaction mechanisms. San Francisco: W. H. Freeman; 1979. 978 p.
2. Schulz GE, Muller CW, Diederichs K. Induced-fit movements in adenylate kinases. J Mol Biol 1990;213:627-630.
3. Schulz GE. Induced-fit movements in adenylate kinases. Faraday Discuss 1992;93:85-93.
4. Vieille C, Krishnamurthy H, Hyun HH, Savchenko A, Yan H, Zeikus JG. Thermotoga neapolitana adenylate kinase is highly active at 30°C. Biochem J 2003;372:577-585.
5. Dreusicke D, Karplus PA, Schulz GE. Refined structure of porcine cytosolic adenylate kinase at 2.1 Å resolution. J Mol Biol 1988;199:359-371.
6. Müller CW, Schulz GE. Structure of the complex of adenylate kinase from Escherichia coli with the inhibitor P1,P5-di(adenosine-5′-) pentaphosphate. J Mol Biol 1988;202:909-912.
7. Müller CW, Schulz GE. Structure of the complex between adenylate kinase from Escherichia coli and the inhibitor Ap5A refined at 1.9 Å resolution: a model for a catalytic transition state. J Mol Biol 1992;224:159-177.
8. Müller CW, Schulz GE. Crystal structures of two mutants of adenylate kinase from Escherichia coli that modify the Gly-loop. Proteins 1993;15:42-49.
9. Berry MB, Meador B, Bilderback T, Liang P, Glaser M, Phillips GN Jr. The closed conformation of a highly flexible protein: the structure of E. coli adenylate kinase with bound AMP and AMPPNP. Proteins 1994;19:183-198.
10. Müller CW, Schlauderer GJ, Reinstein J, Schulz GE. Adenylate kinase motions during catalysis: an energetic counterweight balancing substrate binding. Structure 1996;4:147-156.
11. 2+. Proteins 1998;32:276-288.
12. 5A, showing the pathway of phosphoryl transfer. Protein Sci 1995;4:1262-1271.
13. Egner U, Tomasselli AG, Schulz GE. Structure of the complex of yeast adenylate kinase with the inhibitor P1,P5-di(adenosine-5′-)pentaphosphate at 2.6 Å resolution. J Mol Biol 1987;195:649-658.
14. Diederichs K, Schulz GE. Three-dimensional structure of the complex between the mitochondrial matrix adenylate kinase and its substrate AMP. Biochemistry 1990;29:8138-8144.
15. Schlauderer GJ, Proba K, Schulz GE. Structure of a mutant adenylate kinase ligated with an ATP-analogue showing domain closure over ATP. J Mol Biol 1996;256:223-227.
16. Schlauderer GJ, Schulz GE. The structure of bovine mitochondrial adenylate kinase: Comparison with isoenzymes in other compartments. Protein Sci 1996;5:434-441.
17. Sheng XR, Li X, Pan XM. An iso-random Bi Bi mechanism for adenylate kinase. J Biol Chem 1999;274:22238-22242.
18. Sinev MA, Sineva EV, Ittah V, Haas E. Domain closure in adenylate kinase. Biochemistry 1996;35:6425-6437.
19. Lin Y, Nageswara Rao BD. Structural characterization of adenine nucleotides bound to Escherichia coli adenylate kinase: 1. Adenosine conformations by proton two-dimensional transferred nuclear Overhauser effect spectroscopy. Biochemistry 2000;39:3636-3646.
20. 13C relaxation measurements in the presence of cobalt(II) and manganese(II). Biochemistry 2000;39:3647-3655.
21. Shapiro YE, Sinev MA, Sineva EV, Tugarinov V, Meirovitch E. Backbone dynamics of Escherichia coli adenylate kinase at the extreme stages of the catalytic cycle studied by (15)N NMR relaxation. Biochemistry 2000;39:6634-6644.
22. Shapiro YE, Kahana E, Tugarinov V, Liang ZC, Freed JH, Meirovitch E. Domain flexibility in ligand-free and inhibitor-bound Escherichia coli adenylate kinase based on a mode-coupling analysis of N-15 spin relaxation. Biochemistry 2002;41:6271-6281.
23. Reinstein J, Brune M, Wittinghofer A. Mutations in the nucleotide binding loop of adenylate kinase of Escherichia coli. Biochemistry 1988;27:4712-4720.
24. Reinstein J, Gilles AM, Rose T, Wittinghofer A, Saint Girons I, Barzu O, Surewicz WK, Mantsch HH. Structural and catalytic role of arginine 88 in Escherichia coli adenylate kinase as evidenced by chemical modification and site-directed mutagenesis. J Biol Chem 1989;264:8107-8112.
25. Reinstein J, Schlichting I, Wittinghofer A. Structurally and catalytically important residues in the phosphate binding loop of adenylate kinase of Escherichia coli. Biochemistry 1990;29:7451-7459.
26. Rose T, Glaser P, Surewicz WK, Mantsch HH, Reinstein J, Le Blay K, Gilles AM, Barzu O. Structural and functional consequences of amino acid substitutions in the second conserved loop of Escherichia coli adenylate kinase. J Biol Chem 1991;266:23654-23659.
27. Rose T, Brune M, Wittinghofer A, Le Blay K, Surewicz WK, Mantsch HH, Barzu O, Gilles AM. Structural and catalytic properties of a deletion derivative (Δ133-157) of Escherichia coli adenylate kinase. J Biol Chem 1991;266:10781-10786.
28. Tsai MD, Yan HG. Mechanism of adenylate kinase: site-directed mutagenesis versus X-ray and NMR. Biochemistry 1991;30:6806-6818.
29. Kern P, Brunne RM, Folkers G. Nucleotide-binding properties of adenylate kinase from Escherichia coli: a molecular dynamics study in aqueous and vacuum environments. J Comput Aided Mol Des 1994;8:367-838.
30. Elamrani S, Berry MB, Phillips GN, McCammon JA. Study of global motions in proteins by weighted masses molecular dynamics: adenylate kinase as a test case. Proteins 1996;25:79-88.
31. Knowles JR. Enzyme-catalyzed phosphoryl transfer reactions. Ann Rev Biochem 1980;49:877-919.
32. Hollfelder F, Herschlag D. The nature of the transition-state for enzyme-catalyzed phosphoryl transfer-hydrolysis of O-aryl phosphorothioates by alkaline-phosphatase. Biochemistry 1995;34:12255-12264.
33. Matte A, Tari LW, Delbaere LTJ. How do kinases transfer phosphoryl groups? Structure 1998;6:413-419.
34. Lahiri SD, Zhang GF, Dunaway-Mariano D, Allen KN. The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science 2003;299:2067-2071.
35. van Gunsteren WF, Billeter SR, Eising AA, Hünnenberger PH, Krüger P, Mark AE, Scott WRP, Tironi IG. Biomolecular simulation: the GROMOS96 manual and user guide. Zürich: Vdf Hochschulverlag AG an der ETH Zürich; 1996.
36. Tsodikov OV, Record MTJ, Sergeev YV. A novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J Comput Chem 2002;23:600-609.
37. Cukier RI, Seibold SA. Molecular dynamics simulations of prostaglandin endoperoxide II synthase-1: role of water and the mechanism of compound I formation from hydrogen peroxide. J Phys Chem B 2002;106:12031-12044.
38. Hockney RW, Eastwood JW. Computer simulation using particles. New York: McGraw-Hill; 1981. 540 p.
39. Allen MP, Tildesley DJ. Computer simulation of liquids. Oxford, UK: Clarendon Press; 1987. 385 p.
40. Tomasselli AG, Noda LH. Mitochondrial ATP:AMP phosphotransferase from beef heart: purification and properties. Eur J Biochem 1980;103:481-491.
41. Ito Y, Tomasselli AG, Noda LH. ATP:AMP phosphotransferase from baker's yeast: purification and properties. Eur J Biochem 1980;105:85-92.
42. Saint Girons I, Gilles AM, Margarita D, Michelson S, Monnot M, Fermandjian S, Danchin A, Barzu O. Structural and catalytic characteristics of Escherichia coli adenylate kinase. J Biol Chem 1987;262:622-629.
43. Yan H, Tsai MD. Nucleoside monophosphate kinases: structure, mechanism, and substrate specificity. Adv Enzymol Relat Areas Mol Biol 1999;73:103-134.
44. Beichner S, Byeon I-JL, Tsai M-D. Structure-function relationship of adenylate kinase: Glu-101 in AMP specificity. In: Kaumaya PTP, Hodges RS, editors. Peptides: chemistry, structure and biology. Kingswinford, UK: Mayflower Scientific; 1996. p 721-723.
45. Okajima T, Tanizawa K, Yoneya T, Fukui T. Role of leucine 66 in the asymmetric recognition of substrates in chicken muscle adenylate kinase. J Biol Chem 1991;266:11442-11447.
46. Okajima T, Tanizawa K, Fukui T. Site-directed random mutagenesis of AMP-binding residues in adenylate kinase. J Biochem 1993;114:627-633.
47. Kim HJ, Nishikawa S, Tokutomi Y, Takenaka H, Hamada M, Kuby SA, Uesugi S. In vitro mutagenesis studies at the arginine residues of adenylate kinase: a revised binding site for AMP in the X-ray-deduced model. Biochemistry 1990;29:1107-1111.
48. Yan HG, Dahnke T, Zhou BB, Nakazawa A, Tsai MD. Mechanism of adenylate kinase: critical evaluation of the X-ray model and assignment of the AMP site. Biochemistry 1990;29:10956-10964.
49. Yan HG, Shi ZT, Tsai MD. Mechanism of adenylate kinase: structural and functional demonstration of arginine-138 as a key catalytic residue that cannot be replaced by lysine. Biochemistry 1990;29:6385-6392.
50. Dahnke T, Shi Z, Yan H, Jiang RT, Tsai MD. Mechanism of adenylate kinase: structural and functional roles of the conserved arginine-97 and arginine-132. Biochemistry 1992;31:6318-6328.
51. Dreusicke D, Schulz GE. The glycine-rich loop of adenylate kinase forms a giant anion hole. FEBS Lett 1986;208:301-304.
52. Byeon IJ, Yan H, Edison AS, Mooberry ES, Abildgaard F, Markley JL, Tsai MD. Mechanism of adenylate kinase: 1H, 13C, and 15N NMR assignments, secondary structures, and substrate binding sites. Biochemistry 1993;32:12508-12521.
53. Shi Z, Byeon IJ, Jiang RT, Tsai MD. Mechanism of adenylate kinase: What can be learned from a mutant enzyme with minor perturbation in kinetic parameters? Biochemistry 1993;32:6450-6458.
54. 31P NMR studies of the structure of cation-nucleotide complexes bound to porcine muscle adenylate kinase. Biochemistry 1988;27:8669-8676.
55. Banci L. Molecular dynamics simulations of metalloproteins. Curr Opin Chem Biol 2003;7:143-149.
56. 2+ by site-directed mutagenesis and proton, phosphorus-31, and magnesium-25 NMR. Biochemistry 1991;30:5539-5546.
57. Mildvan AS. Mechanisms of signaling and related enzymes. Proteins 1997;29:401-416.