How calcium inhibits the magnesium-dependent kinase gsk3β: A molecular simulation study

Proteins: Structure, Function and Bioinformatics

Volumn 81, Issue 5, 2013, Pages 740-753

  Lu, Shao Yong ^a   Huang, Zhi Min ^a   Huang, Wen Kang ^a   Liu, Xin Yi ^a   Chen, Ying Yi ^a   Shi, Ting ^a   Zhang, Jian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

ATP; Calcium; GSK3 ; Magnesium; MD simulations

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; GLYCOGEN SYNTHASE KINASE 3BETA; LYSINE; MAGNESIUM ION;

ARTICLE; ATOM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GEOMETRY; HYDROGEN BOND; INHIBITION KINETICS; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; SUBSTITUTION REACTION;

ADENOSINE TRIPHOSPHATE; CALCIUM; CATALYTIC DOMAIN; GLYCOGEN SYNTHASE KINASE 3; HUMANS; HYDROGEN BONDING; MAGNESIUM; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION;

EID: 84875859742     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24221     Document Type: Article

References (65)

1. Zurita A, Zhang Y, Pedersen L, Darden T, Birnbaumer L. Obligatory role in GTP hydrolysis for the amide carbonyl oxygen of the Mg(2+)-coordinating Thr of regulatory GTPases. Proc Natl Acad Sci USA 2010; 107: 9596-9601.
2. Babu CS, Dudev T, Casareno R, Cowan JA, Lim C. A combined experimental and theoretical study of divalent metal ion selectivity and function in proteins: application to E-coli ribonuclease H1. J Am Chem Soc 2003; 125: 318-9328.
3. Peeraer Y, abijns A, Collet JF, Schaftingen EV, Ranter CD. How calcium inhibits the magnesium-dependent enzyme human phosphoserine phosphatase. Eur J Biochem 2004; 271: 3421-3427.
4. Lu S, Huang W, Li X, Huang Z, Liu X, Chen Y, Shi T, Zhang J. Insights into the role of magnesium triad in myo-inositol monophosphatase: metal mechanism, substrate binding, and lithium therapy. J Chem Inf Model 2012; 52:2398-2409.
5. Dudev T, Lim C. Metal binding affinity and selectivity in metalloproteins: insights from computational studies. Annu Rev Biophys 2008; 37: 97-116.
6. 2+-binding sites using refined carbon clusters. Proteins 2012; 80: 2666-2679.
7. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM. Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 2008; 13: 1205-1218.
8. 2+ binding sites. J Biol Inorg Chem 2008; 13: 1169-1181.
9. Ali A, Hoeflich KP, Woodgett JR. Glycogen synthase kinase-3: properties, functions, and regulation. Chem Rev 2001; 101: 2527-2540.
10. Pearl LH, Barford D. Regulation of protein kinases in insulin, growth factor, and Wnt signaling. Curr Opin Struc Biol 2000; 12: 761-767.
11. Cohen P, Frame S. The renaissance of GSK3. Nat Mol Cell Bio 2001; 2: 769-776.
12. Eldar-Finkelman H, Licht-Murava A, Pietrokovaski S, Eisenstein M. Substrate-competitive GSK-3 inhibitors-strategy and implications. Biochim Biophys Acta 2010; 1804: 598-603.
13. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. Binding of GSK3-beta to the APC-beta-catenin complex and regulation of complex assembly. Science 1996; 272: 1023-1026.
14. 2+ in metalloproteins: implications for lithium therapy. J Am Chem Soc 2011; 133: 9506-9515.
15. Lu S-Y, Jiang Y-J, Zou J-W, Wu T-X. Molecular modeling and molecular dynamics simulation studies of the GSK3β/ATP/Substrate complex: understanding the unique P+4 primed phosphorylation specificity for GSK3β substrates. J Chem Inf Model 2011; 51: 1025-1036.
16. Lu S-Y, Jiang Y-J, Zou J-W, Wu T-X. Dissection of the difference between the group I metal ions in inhibiting GSK3β: a computational study. Phys Chem Chem Phys 2011; 13: 7014-7023.
17. Lu S-Y, Jiang Y-J, Lv J, Zou J-W, Wu T-X. Role of bridging water molecules in GSK3β-inhibitor complexes: insights from QM/MM, MD, and molecular docking studies. J Comput Chem 2011; 32: 1907-1918.
18. Lu S-Y, Jiang Y-J, Zou J-W, Wu T-X. Effect of double mutations K214/A-E215/Q of FRATide on GSK3β: insights from molecular dynamics simulation and normal mode analysis. Amino Acids 2012; 43: 267-277.
19. Lu S, Jiang Y, Lv J, Zou J, Wu T. Mechanism of kinase inactivation and nonbinding of FRATide to GSK3β due to K85M mutation: molecular dynamics simulation and normal mode analysis. Biopolymers 2011; 95: 669-681.
20. Sun H, Jiang Y-J, Yu Q-S, Luo C-C, Zou J-W. Effect of mutation K85R on GSK-3β: molecular dynamics simulation. Biochem Biophys Res Commun 2008; 377: 962-965.
21. + on GSK-3 inhibition: molecular dynamics simulation. J Mol Model 2011; 17: 377-381.
22. Zhang N, Jiang Y, Zou J, Zhuang S, Jin H, Yu, Q. Insights into unbinding mechanisms upon two mutations investigated by molecular dynamics study of GSK3β-Axin complexes: role of packing hydrophobic residues. Proteins 2007; 67: 941-949.
23. Zhang N, Jiang Y, Zou J, Yu Q, Zhao W. Structural basis for the complete loss of GSK3β catalytic activity due to R96 mutation investigated by molecular dynamics study. Proteins 2009; 75: 671-681.
24. Buch I, Fishelovitch D, London N, Raveh B, Wolfson HJ, Nussinov R. Allosteric regulation of glycogen synthase kinase 3β: a theoretical study. Biochemistry 2010; 49: 10890-10901.
25. Tang XN, Lo CW, Chuang YC, Chen CT, Sun YC, Hong YR, Yang CN. Prediction of the binding mode between GSK3β and a peptide derived from GSKIP using molecular dynamics simulation. Biopolymers 2011; 95: 461-471.
26. Huang Z, Zhu L, Cao Y, Wu G, Liu X, Chen Y, Wang Q, Shi T, Zhao Y, Wang Y, Li W, Li Y, Chen H, Chen G, Zhang J. ASD: a comprehensive database of allosteric proteins and modulators. Nucleic Acids Res 2011; 39: D663-D669.
27. Bertrand JA, Thieffine S, Vulpetti A, Cristiani C, Valsasina B, Knapp S, Kalisz H M, Flocco M. Structural characterization of the GSK-3 beta active site using selective and non-selective ATP-mimetic inhibitors. J Mol Biol 2003; 333: 393-407.
28. ter Haar E, Coll JT., Austen DA, Hsiao HM, Swenson L, Jain J. Structure of GSK3β reveals a primed phosphorylation mechanism. Nat Struct Biol 2001; 8: 593-596.
29. Ryves WJ, Harwood AJ. Lithium inhibits glycogen synthase kinase-3 by competition for magnesium. Biochem Biophys Res Commun 2001; 280: 720-725.
30. Ryves WJ, Dajani R, Pearl L, Harwood AJ. Glycogen synthase kinase-3 inhibition by lithium and beryllium suggests the presence of two magnesium binding sites. Biochem Biophys Res Commun 2002; 290: 967-972.
31. Sybyl version 6.8; Tripos Associates Inc.: St. Louis, MO, 2001.
32. Bas DC, Rogers DM, Jensen JH. Very fast prediction and rationalization of PKa values for protein-ligand complexes. Proteins 2008; 73: 765-783.
33. Oelschlaeger P, Klahn M, Beard WA, Wilson SH, Warshel A. Magnesium-cationic dummy atom molecules enhance representation of DNA polymerase β in molecular dynamics simulations: improved accuracy in studies of structural features and mutational effects. J Mol Biol 2007; 366: 687-701.
34. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T. A point-charge force field for molecular mechanics simulations of proteins. J Comput Chem 2003; 24: 1999-2012.
35. Homeyer N, Horn AH, Lanig H, Sticht H. AMBER force field parameters for phosphorylated amino acids in different protonation states: Phosphoserine, phosphothreonine, phosphotyrosine and phosphohistidine. J Mol Model 2006; 12: 281-289.
36. Bradbrook GM, Gleichmann T, Harrop SJ, Habash J, Raftery J, Kalb J, Yariv J, Hillier IH, Helliwell JR. X-ray and molecular dynamics studies of concanavalin-A glucoside and mannoside complexes: relating structure to thermodynamics of binding. J Chem Soc Faraday Trans 1998; 94: 1603-1611.
37. Bryce RA, Hillier IH, Naismith JH. Carbohydrate-protein recognition: molecular dynamics simulations and free energy analysis of oligosaccharide binding to concanavalin A. Biophys J 2001; 81: 1373-1388.
38. Kaushik S, Mohanty D, Surolia A. The role of metal ions in substrate recognition and stability of concanavalin A; a molecular dynamics study. Biophys J 2009; 96: 21-34.
39. Laine E, Yoneda JD, Blondel A, Malliavin TE. The conformational plasticity of calmodulin upon calcium complexation gives a model of its interaction with the oedema factor of Bacillus anthracis. Proteins 2008; 71: 1813-1829.
40. 2+ binding to calmodulin loop. Biophys J 2006; 90: 3043-3051.
41. Li JL, Ceng CY, Bu Y, Huang XR, Sun CC. Conformational transition pathway in the allosteric process of calcium-induced recoverin: molecular dynamics simulations. J Comput Chem 2009; 30: 1135-1145.
42. Case DA, Darden TA, Cheatham TEIII, Simmerling CL, Wang J, Duke RE, Luo R, Walker RC, Zhang W, Merz KM, Roberts BP, Wang B, Hayik S, Roitberg A, Seabra G, Kolossvary I, Wong KF, Paesani F, Vanicek J, Liu J, Wu X, Brozell SR, Steinbrecher T, Gohlke H, Cai Q, Ye X, Wang J, Hsieh M-J, Cui G, Roe DR, Mathews DH, Seetin MG, Sagui C, Babin V, Luchko T, Gusarov S, Kovalenko A, Kollman PA. AMBER 11, University of California: San Francisco, 2010.
43. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of single potential function for simulating liquid water. J Chem Phys 1983; 79: 926-935.
44. Darden T, York D, Pedersen L. Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J Chem Phys 1993; 98: 10089-10094.
45. Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977; 23: 327-341.
46. Wu X, Brooks BR. Self-guided Langevin dynamics simulation method. Chem Phys Lett 2003; 381: 512-518.
47. 2+ ions in a class I RNA polymerase ribozyme: a molecular simulation study. J Phys Chem B 2012; 116: 2259-2268.
48. Wang PF, Flynn AJ, Naor M, Jensen JH, Cui GL, Merz KMJr, Kenyon GL, McLeish MJ. Exploring the role of the active site cysteine in human muscle creatine kinase. Biochemistry 2006; 45: 11464-11672.
49. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmuller L, Lautwein A, Schmitz A, Wittinghofer A. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 1997; 277: 333-338.
50. Zhang B, Tan VBC, Lim KM, Tay TE. The activation and inhibition of cyclin-dependent kinase-5 by phosphorylation. Biochemistry 2007; 46: 10841-10851.
51. Bártová I, Otyepka M, Kríž Z, Koca J. Activation and inhibition of cyclin-dependent kinase-2 by phosphorylation; A molecular dynamics study reveals the functional importance of the glycine-rich loop. Protein Sci 2004; 13: 1449-1457.
52. Bártová I, Otyepka M, Kríž Z, Koca J. The mechanism of inhibition of the cylinc-dependent kinase-2 as revealed by the molecular dynamics study on the complex CDK2 with the peptide substrate HHASPPK. Protein Sci 2005; 14: 445-451.
53. Humphrey W, Dake A, Schulten K. VMD: visual molecular dynamics. J Mol Graphics 1996; 14: 33-38.
54. Cheng Y, Zhang Y, McCammon JA. How does the cAMP-dependent protein kinase catalyze the phosphorylation reaction: an ab initio QM/MM study. J Am Chem Soc 2005; 127: 1553-1562.
55. Valiev M, Kawai R, Adams JA, Weare JH. The role of the putative catalytic base in the phosphoryl transfer reaction in a protein kinase: First-principles calculations. J Am Chem Soc 2003; 125: 9926-9927.
56. Gibbs CS, Zoller MJ. Rational scanning mutagenesis of a protein kinase identifies functional regions involved in catalysis and substrate interactions. J Biol Chem 1991; 266: 8923-8931.
57. Skamnaki VT, Owen DJ, Noble MEM, Lowe ED, Lowe G, Oikonomakos NG, Johnson LN. Catalytic mechanism of phosphorylase kinase probed by mutational studies. Biochemistry 1999; 38: 14718-14730.
58. Szarek P, Dyguda-Kazimierowicz E, Tachibana A, Sokalski WA. Physical nature of intermolecular interactions within cAMP-dependent protein kinase active site: differential transition state stabilization in phosphoryl transfer reaction. J Phys Chem B 2008; 112: 11819-11826.
59. Bossemeyer D. Protein kinases: structure and function. FEBS Lett 1995; 369: 57-61.
60. He X, Saint-Jeannet JP, Woodgett JR, Varmus HE, Dawid IB. Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 1995; 374: 617-622.
61. Fraser E, Young N, Dajani R, Franca-Koh J, Ryves J, Williams RSB, Yeo M, Webster MT, Richardson C, Smalley MJ, Pearl LH, Harwood A, Dale TC. Identification of the Axin and Frat binding region of glycogen synthase kinase-3. J Biol Chem 2002; 277: 2176-2185.
62. Romani A, Scarpa A. Arch Biochem Biophys 1992; 298: 1-12.
63. Dudev T, Lim C. Principles governing Mg, Ca, and Zn binding and selectivity in proteins. Chem Rev 2003; 103: 773-787.
64. Dudev T, Lim C. Monodentate versus bidentate carboxylate binding in magnesium and calcium proteins: what are the basic principles? J Phys Chem B 2004; 108: 4546-4557.
65. 2+. J Phys Chem B 2001; 105: 4446-4452.