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BioMed Research International
Volume 2013 (2013), Article ID 628536, 7 pages
http://dx.doi.org/10.1155/2013/628536
Research Article

Molecular Dynamics Studies on the Conformational Transitions of Adenylate Kinase: A Computational Evidence for the Conformational Selection Mechanism

1Pathogen Diagnostic Center, Institut Pasteur of Shanghai Chinese Academy of Sciences, Shanghai 200025, China
2Shanghai Center for Bioinformation Technology, 100 Qinzhou Road, Shanghai 200235, China
3Bioinformatics Center, Key Laboratory of Systems Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
4Key Laboratory of Systems Biomedicine (Ministry of Education), Shanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, Shanghai 200240, China

Received 5 April 2013; Accepted 13 June 2013

Academic Editor: Yudong Cai

Copyright © 2013 Jie Ping et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Vonrhein, G. J. Schlauderer, and G. E. Schulz, “Movie of the structural changes during a catalytic cycle of nucleoside monophosphate kinases,” Structure, vol. 3, no. 5, pp. 483–490, 1995. View at Scopus
  2. C. W. Müller, G. J. Schlauderer, J. Reinstein, and G. E. Schulz, “Adenylate kinase motions during catalysis: an energetic counterweight balancing substrate binding,” Structure, vol. 4, no. 2, pp. 147–156, 1996. View at Scopus
  3. G. J. Schlauderer, K. Proba, and G. E. Schulz, “Structure of a mutant adenylate kinase ligated with an ATP-analogue showing domain closure over ATP,” Journal of Molecular Biology, vol. 256, no. 2, pp. 223–227, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. G. J. Schlauderer and G. E. Schulz, “The structure of bovine mitochondrial adenylate kinase: comparison with isoenzymes in other compartments,” Protein Science, vol. 5, no. 3, pp. 434–441, 1996. View at Scopus
  5. K. A. Henzler-Wildman, V. Thai, M. Lei et al., “Intrinsic motions along an enzymatic reaction trajectory,” Nature, vol. 450, no. 7171, pp. 838–844, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. J. A. Hanson, K. Duderstadt, L. P. Watkins et al., “Illuminating the mechanistic roles of enzyme conformational dynamics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 46, pp. 18055–18060, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Arora and C. L. Brooks, “Large-scale allosteric conformational transitions of adenylate kinase appear to involve a population-shift mechanism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 47, pp. 18496–18501, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Snow, G. Y. Qi, and S. Hayward, “Essential dynamics sampling study of adenylate kinase: comparison to citrate synthase and implication for the hinge and shear mechanisms of domain motions,” Proteins, vol. 67, no. 2, pp. 325–337, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. B. Kubitzki and B. L. de Groot, “The atomistic mechanism of conformational transition in adenylate kinase: a TEE-REX molecular dynamics study,” Structure, vol. 16, no. 8, pp. 1175–1182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. K. A. Henzler-Wildman, M. Lei, V. Thai, S. J. Kerns, M. Karplus, and D. Kern, “A hierarchy of timescales in protein dynamics is linked to enzyme catalysis,” Nature, vol. 450, no. 7171, pp. 913–916, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Wolf-Watz, V. Thai, K. Henzler-Wildman, G. Hadjipavlou, E. Z. Eisenmesser, and D. Kern, “Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair,” Nature Structural and Molecular Biology, vol. 11, no. 10, pp. 945–949, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Jana, B. V. Adkar, R. Biswas, and B. Bagchi, “Dynamic coupling between the LID and NMP domain motions in the catalytic conversion of ATP and AMP to ADP by adenylate kinase,” Journal of Chemical Physics, vol. 134, no. 3, Article ID 035101, 10 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. J. B. Brokaw and J. W. Chu, “On the roles of substrate binding and hinge unfolding in conformational changes of adenylate kinase,” Biophysical Journal, vol. 99, no. 10, pp. 3420–3429, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Pontiggia, A. Zen, and C. Micheletti, “Small- and large-scale conformational changes of adenylate kinase: a molecular dynamics study of the subdomain motion and mechanics,” Biophysical Journal, vol. 95, no. 12, pp. 5901–5912, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Dong, S. Qin, and H. X. Zhou, “Effects of macromolecular crowding on protein conformational changes,” PLoS Computational Biology, vol. 6, Article ID e1000833, 2010. View at Scopus
  16. H. Lou and R. I. Cukier, “Molecular dynamics of apo-adenylate kinase: a principal component analysis,” Journal of Physical Chemistry B, vol. 110, no. 25, pp. 12796–12808, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Bae and G. N. Phillips Jr., “Identifying and engineering ion pairs in adenylate kinases: Insights from molecular dynamics simulations of thermophilic and mesophilic homologues,” The Journal of Biological Chemistry, vol. 280, no. 35, pp. 30943–30948, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Krishnamurthy, H. Lou, A. Kimple, C. Vieille, and R. I. Cukier, “Associative mechanism for phosphoryl transfer: a molecular dynamics simulation of Escherichia coli adenylate kinase complexed with its substrates,” Proteins, vol. 58, no. 1, pp. 88–100, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. Lu and J. Wang, “Single molecule conformational dynamics of adenylate kinase: energy landscape, structural correlations, and transition state ensembles,” Journal of the American Chemical Society, vol. 130, no. 14, pp. 4772–4783, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. O. Beckstein, E. J. Denning, J. R. Perilla, and T. B. Woolf, “Zipping and unzipping of adenylate kinase: atomistic insights into the ensemble of open closed transitions,” Journal of Molecular Biology, vol. 394, no. 1, pp. 160–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. M. D. Daily, G. N. Phillips Jr., and Q. Cui, “Many local motions cooperate to produce the adenylate kinase conformational transition,” Journal of Molecular Biology, vol. 400, no. 3, pp. 618–631, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Potestio, F. Pontiggia, and C. Micheletti, “Coarse-grained description of protein internal dynamics: an optimal strategy for decomposing proteins in rigid subunits,” Biophysical Journal, vol. 96, no. 12, pp. 4993–5002, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. R. D. Hills Jr., L. Lu, and G. A. Voth, “Multiscale coarse-graining of the protein energy landscape,” PLoS Computational Biology, vol. 6, no. 6, Article ID e1000827, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. O. Miyashita, P. G. Wolynes, and J. N. Onuchic, “Simple energy landscape model for the kinetics of functional transitions in proteins,” Journal of Physical Chemistry B, vol. 109, no. 5, pp. 1959–1969, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. Q. Lu and J. Wang, “Kinetics and statistical distributions of single-molecule conformational dynamics,” Journal of Physical Chemistry B, vol. 113, no. 5, pp. 1517–1521, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. P. C. Whitford, O. Miyashita, Y. Levy, and J. N. Onuchic, “Conformational transitions of adenylate kinase: switching by cracking,” Journal of Molecular Biology, vol. 366, no. 5, pp. 1661–1671, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Peng, L. Zhang, and T. Head-Gordon, “Instantaneous normal modes as an unforced reaction coordinate for protein conformational transitions,” Biophysical Journal, vol. 98, no. 10, pp. 2356–2364, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Ahmed, F. Rippmann, G. Barnickel, and H. Gohlke, “A normal mode-based geometric simulation approach for exploring biologically relevant conformational transitions in proteins,” Journal of Chemical Information and Modeling, vol. 51, no. 7, pp. 1604–1622, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Kirillova, J. Cortés, A. Stefaniu, and T. Siméon, “An NMA-guided path planning approach for computing large-amplitude conformational changes in proteins,” Proteins, vol. 70, no. 1, pp. 131–143, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. N. A. Temiz, E. Meirovitch, and I. Bahar, “Escherichia coli adenylate kinase dynamics: comparison of elastic network model modes with mode-coupling 15N-NMR relaxation data,” Proteins, vol. 57, no. 3, pp. 468–480, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. J. N. Stember and W. Wriggers, “Bend-twist-stretch model for coarse elastic network simulation of biomolecular motion,” Journal of Chemical Physics, vol. 131, no. 7, Article ID 074112, 9 pages, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. W. J. Zheng, B. R. Brooks, and G. Hummer, “Protein conformational transitions explored by mixed elastic network models,” Proteins, vol. 69, no. 1, pp. 43–57, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Maragakis and M. Karplus, “Large amplitude conformational change in proteins explored with a plastic network model: adenylate kinase,” Journal of Molecular Biology, vol. 352, no. 4, pp. 807–822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. M. B. Berry and G. N. J. Philips, “Crystal structures of Bacillus stearothermophilus adenylate kinase with bound Ap5A, Mg2+ Ap5A, and Mn2+ Ap5A reveal an intermediate lid position and six coordinate octahedral geometry for bound Mg2+ and Mn2+,” Proteins, vol. 32, no. 3, pp. 276–288, 1998. View at Publisher · View at Google Scholar
  35. C. W. Muller and G. E. Schulz, “Crystal structures of two mutants of adenylate kinase from Escherichia coli that modify the Gly-loop,” Proteins, vol. 15, no. 1, pp. 42–49, 1993. View at Publisher · View at Google Scholar · View at Scopus
  36. M. B. Berry, E. Bae, T. R. Bilderback, M. Glaser, and G. N. Phillips Jr., “Crystal structure of ADP/AMP complex of Escherichia coli adenylate kinase,” Proteins, vol. 62, no. 2, pp. 555–556, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. M. B. Berry, B. Meador, T. Bilderback, P. Liang, M. Glaser, and G. N. Phillips Jr., “The closed conformation of a highly flexible protein: the structure of E. coli adenylate kinase with bound AMP and AMPPNP,” Proteins, vol. 19, no. 3, pp. 183–198, 1994. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Bae and G. N. Phillips Jr., “Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases,” The Journal of Biological Chemistry, vol. 279, no. 27, pp. 28202–28208, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Couñago, S. Chen, and Y. Shamoo, “In vivo molecular evolution reveals biophysical origins of organismal fitness,” Molecular Cell, vol. 22, no. 4, pp. 441–449, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. U. Abele and G. E. Schulz, “High-resolution structures of adenylate kinase from yeast ligated with inhibitor Ap5A, showing the pathway of phosphoryl transfer,” Protein Science, vol. 4, no. 7, pp. 1262–1271, 1995. View at Scopus
  41. P. Spuergin, U. Abele, and G. E. Schulz, “Stability, activity and structure of adenylate kinase mutants,” European Journal of Biochemistry, vol. 231, no. 2, pp. 405–413, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Gu, H. F. Chen, D. Q. Wei, and J. F. Wang, “Molecular dynamics simulations exploring drug resistance in HIV-1 proteases,” Chinese Science Bulletin, vol. 55, no. 24, pp. 2677–2683, 2010. View at Publisher · View at Google Scholar
  43. K. Wild, R. Grafmüller, E. Wagner, and G. E. Schulz, “Structure, catalytsis and supramolecular assembly of adenylate kinase from maize,” European Journal of Biochemistry, vol. 250, no. 2, pp. 326–331, 1997.
  44. G. J. Schlauderer and G. E. Schulz, “The structure of bovine mitochondrial adenylate kinase: comparison with isoenzymes in other compartments,” Protein Science, vol. 5, no. 3, pp. 434–441, 1996. View at Scopus
  45. K. Diederichs and G. E. Schulz, “The refined structure of the complex between adenylate kinase from beef heart mitochondrial matrix and its substrate AMP at 1.85 Å resolution,” Journal of Molecular Biology, vol. 217, no. 3, pp. 541–549, 1991. View at Scopus
  46. C. W. Müller and G. E. Schulz, “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,” Journal of Molecular Biology, vol. 224, no. 1, pp. 159–177, 1992. View at Publisher · View at Google Scholar · View at Scopus
  47. R. E. Georgescu, E. G. Alexov, and M. R. Gunner, “Combining conformational flexibility and continuum electrostatics for calculating pKas in proteins,” Biophysical Journal, vol. 83, no. 4, pp. 1731–1748, 2002. View at Scopus
  48. W. Rocchia, E. Alexov, and B. Honig, “Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions,” Journal of Physical Chemistry B, vol. 105, no. 28, pp. 6507–6514, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. D. A. Case, T. E. Cheatham III, T. Darden et al., “The Amber biomolecular simulation programs,” Journal of Computational Chemistry, vol. 26, no. 16, pp. 1668–1688, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. J. W. Ponder and D. A. Case, “Force fields for protein simulations,” Advances in Protein Chemistry, vol. 66, pp. 27–85, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Wang, W. Wang, P. A. Kollman, and D. A. Case, “Antechamber, an accessory software package for molecular mechanical calculations,” Journal of Computational Chemistry, vol. 25, pp. 1157–1174, 2005.
  52. J. F. Wang and K. C. Chou, “Insights from modeling the 3D structure of New Delhi metallo-β-lactamse and its binding interactions with antibiotic drugs,” PLoS ONE, vol. 6, no. 4, Article ID e18414, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Lian, D. Q. Wei, J. F. Wang, and K. C. Chou, “An allosteric mechanism inferred from molecular dynamics simulations on phospholamban pentamer in lipid membranes,” PLoS ONE, vol. 6, no. 4, Article ID e18587, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Wang, D. Q. Wei, and J. F. Wang, “Molecular dynamics studies on T1 lipase: insight into a double-flap mechanism,” Journal of Chemical Information and Modeling, vol. 50, no. 5, pp. 875–878, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. J. F. Wang, P. Hao, Y. X. Li, J. L. Dai, and X. Li, “Exploration of conformational transition in the aryl-binding site of human FXa using molecular dynamics simulations,” Journal of Molecular Modeling, vol. 18, no. 6, pp. 2717–2725, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Li, D. Q. Wei, J. F. Wang, and Y. X. Li, “A negative cooperativity mechanism of human CYP2E1 inferred from molecular dynamics simulations and free energy calculations,” Journal of Chemical Information and Modeling, vol. 51, no. 12, pp. 3217–3225, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. J. F. Wang and K. C. Chou, “Insights into the mutation-induced HHH syndrome from modeling human mitochondrial ornithine transporter-1,” PLoS ONE, vol. 7, no. 1, Article ID e31048, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Li, D. Q. Wei, J. F. Wang, Z. T. Yu, and K. C. Chou, “Molecular dynamics simulations of CYP2E1,” Medicinal Chemistry, vol. 8, no. 2, pp. 208–221, 2012. View at Publisher · View at Google Scholar
  59. J. He, D. Q. Wei, J. F. Wang, and K. C. Chou, “Predicting protein-ligand binding sites based on an improved geometric algorithm,” Protein and Peptide Letters, vol. 18, no. 10, pp. 997–1001, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Dahnke, Z. Shi, H. Yan, R. T. Jiang, and M. D. Tsai, “Mechanism of adenylate kinase. Structural and functional roles of the conserved arginine-97 and arginine-132,” Biochemistry, vol. 31, no. 27, pp. 6318–6328, 1992. View at Scopus
  61. M. A. Sinev, E. V. Sineva, V. Ittah, and E. Haas, “Domain closure in adenylate kinase,” Biochemistry, vol. 35, no. 20, pp. 6425–6437, 1996. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. E. Shapiro, M. A. Sinev, E. V. Sineva, V. Tugarinov, and E. Meirovitch, “Backbone dynamics of Escherichia coli adenylate kinase at the extreme stages of the catalytic cycle studied by 15N NMR relaxation,” Biochemistry, vol. 39, no. 22, pp. 6634–6644, 2000. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Wolf-Watz, V. Thai, K. Henzler-Wildman, G. Hadjipavlou, E. Z. Eisenmesser, and D. Kern, “Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair,” Nature Structural and Molecular Biology, vol. 11, no. 10, pp. 945–949, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. E. Shapiro and E. Meirovitch, “Activation energy of catalysis-related domain motion in E. coli adenylate kinase,” Journal of Physical Chemistry B, vol. 110, no. 23, pp. 11519–11524, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. O. Miyashita, J. N. Onuchic, and P. G. Wolynes, “Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 12570–12575, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. P. C. Whitford, S. Gosavi, and J. N. Onuchic, “Conformational transitions in adenylate kinase: allosteric communication reduces misligation,” The Journal of Biological Chemistry, vol. 283, no. 4, pp. 2042–2048, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. D. E. Koshland Jr., “Application of a theory of enzyme specificity to protein synthesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 44, no. 2, pp. 98–104, 1958.
  68. B. Ma, S. Kumar, C. Tsai, and R. Nussinov, “Folding funnels and binding mechanisms,” Protein Engineering, vol. 12, no. 9, pp. 713–720, 1999. View at Scopus
  69. C. Tsai, S. Kumar, B. Ma, and R. Nussinov, “Folding funnels, binding funnels, and protein function,” Protein Science, vol. 8, no. 6, pp. 1181–1190, 1999. View at Scopus
  70. H. J. Zhang, X. R. Sheng, W. D. Niu, X. M. Pan, and J. M. Zhou, “Evidence for at least two native forms of rabbit muscle adenylate kinase in equilibrium in aqueous solution,” The Journal of Biological Chemistry, vol. 273, no. 13, pp. 7448–7456, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Han, X. Li, and X. M. Pan, “Native states of adenylate kinase are two active sub-ensembles,” FEBS Letters, vol. 528, no. 1–3, pp. 161–165, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Z. Eisenmesser, O. Millet, W. Labeikovsky et al., “Intrinsic dynamics of an enzyme underlies catalysis,” Nature, vol. 438, no. 7064, pp. 117–121, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Tobi and I. Bahar, “Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 52, pp. 18908–18913, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. P. C. Whitford, O. Miyashita, Y. Levy, and J. N. Onuchic, “Conformational transitions of adenylate kinase: switching by cracking,” Journal of Molecular Biology, vol. 366, no. 5, pp. 1661–1671, 2007. View at Publisher · View at Google Scholar · View at Scopus