Molecular dynamics simulations provide atomistic insight into hydrogen exchange mass spectrometry experiments

Journal of Chemical Theory and Computation

Volumn 9, Issue 1, 2013, Pages 658-669

  Petruk, Ariel A ^a   Defelipe, Lucas A ^a,b   Rodríguez Limardo, Ramiro G ^a,b   Bucci, Hernán ^b   Marti, Marcelo A ^a,b   Turjanski, Adrian G ^a,b  

^a Instituto de Quimica Fisica de los Materiales Medio Ambiente y Energia   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84872145488     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct300519v     Document Type: Article

References (36)

1. Monod, J.; Wyman, J.; Changeux, J. P. On the nature of allosteric transitions: a plausible model J. Mol. Biol. 1965, 12, 88-118
2. Grzesiek, S.; Sass, H. J. From biomolecular structure to functional understanding: new NMR developments narrow the gap Curr. Opin. Struct. Biol. 2009, 19, 585-95
3. Konermann, L.; Pan, J.; Liu, Y. H. Hydrogen exchange mass spectrometry for studying protein structure and dynamics Chem. Soc. Rev. 2011, 40, 1224-34
4. Hoofnagle, A. N.; Resing, K. A.; Ahn, N. G. Protein analysis by hydrogen exchange mass spectrometry Annu. Rev. Biophys. Biomol. Struct. 2003, 32, 1-25
5. Chalmers, M. J.; Busby, S. A.; Pascal, B. D.; West, G. M.; Griffin, P. R. Differential hydrogen/deuterium exchange mass spectrometry analysis of protein-ligand interactions Expert Rev. Proteomics 2011, 8, 43-59
6. Liu, T.; Pantazatos, D.; Li, S.; Hamuro, Y.; Hilser, V. J.; Woods, V. L., Jr. Quantitative assessment of protein structural models by comparison of H/D exchange MS data with exchange behavior accurately predicted by DXCOREX J. Am. Soc. Mass Spectrom. 2012, 23, 43-56
7. Hilser, V. J.; Garcia-Moreno, E. B.; Oas, T. G.; Kapp, G.; Whitten, S. T. A statistical thermodynamic model of the protein ensemble Chem. Rev. 2006, 106, 1545-58
8. Klepeis, J. L.; Lindorff-Larsen, K.; Dror, R. O.; Shaw, D. E. Long-timescale molecular dynamics simulations of protein structure and function Curr. Opin. Struct. Biol. 2009, 19, 120-7
9. Case, D. A.; Cheatham Iii, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M., Jr.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26, 1668-1688
10. Brooks, B. R.; Brooks, C. L., 3rd; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-614
11. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. GROMACS: fast, flexible, and free J. Comput. Chem. 2005, 26, 1701-18
12. Craig, P. O.; Latzer, J.; Weinkam, P.; Hoffman, R. M.; Ferreiro, D. U.; Komives, E. A.; Wolynes, P. G. Prediction of native-state hydrogen exchange from perfectly funneled energy landscapes J. Am. Chem. Soc. 2011, 133, 17463-72
13. Turjanski, A. G.; Vaque, J. P.; Gutkind, J. S. MAP kinases and the control of nuclear events Oncogene 2007, 26, 3240-53
14. Bellon, S.; Fitzgibbon, M. J.; Fox, T.; Hsiao, H. M.; Wilson, K. P. The structure of phosphorylated p38gamma is monomeric and reveals a conserved activation-loop conformation Structure 1999, 7, 1057-1065
15. Goldsmith, E. J.; Cobb, M. H.; Chang, C. I. Structure of MAPKs Methods Mol. Biol. (N. Y., NY, U. S.) 2004, 250, 127-144
16. White, A.; Pargellis, C. A.; Studts, J. M.; Werneburg, B. G.; Farmer, B. T., 2nd. Molecular basis of MAPK-activated protein kinase 2:p38 assembly Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 6353-8
17. Liu, S.; Sun, J. P.; Zhou, B.; Zhang, Z. Y. Structural basis of docking interactions between ERK2 and MAP kinase phosphatase 3 Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 5326-5331
18. Shaw, D.; Wang, S. M.; Villasenor, A. G.; Tsing, S.; Walter, D.; Browner, M. F.; Barnett, J.; Kuglstatter, A. The crystal structure of JNK2 reveals conformational flexibility in the MAP kinase insert and indicates its involvement in the regulation of catalytic activity J. Mol. Biol. 2008, 383, 885-93
19. Zhou, T.; Sun, L.; Humphreys, J.; Goldsmith, E. J. Docking interactions induce exposure of activation loop in the MAP kinase ERK2 Structure 2006, 14, 1011-1019
20. Hoofnagle, A. N.; Stoner, J. W.; Lee, T.; Eaton, S. S.; Ahn, N. G. Phosphorylation-dependent changes in structure and dynamics in ERK2 detected by SDSL and EPR Biophys. J. 2004, 86, 395-403
21. Rodriguez Limardo, R. G.; Ferreiro, D. N.; Roitberg, A. E.; Marti, M. A.; Turjanski, A. G. p38gamma activation triggers dynamical changes in allosteric docking sites Biochemistry 2011, 50, 1384-95
22. Tanoue, T.; Nishida, E. Molecular recognitions in the MAP kinase cascades Cell Signal 2003, 15, 455-62
23. Hoofnagle, A. N.; Resing, K. A.; Goldsmith, E. J.; Ahn, N. G. Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 956-961
24. Lee, T.; Hoofnagle, A. N.; Kabuyama, Y.; Stroud, J.; Min, X.; Goldsmith, E. J.; Chen, L.; Resing, K. A.; Ahn, N. G. Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry Mol. Cell 2004, 14, 43-55
25. Lee, T.; Hoofnagle, A. N.; Resing, K. A.; Ahn, N. G. Hydrogen exchange solvent protection by an ATP analogue reveals conformational changes in ERK2 upon activation J. Mol. Biol. 2005, 353, 600-612
26. Emrick, M. A.; Lee, T.; Starkey, P. J.; Mumby, M. C.; Resing, K. A.; Ahn, N. G. The gatekeeper residue controls autoactivation of ERK2 via a pathway of intramolecular connectivity Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 18101-6
27. Kornev, A. P.; Taylor, S. S. Defining the conserved internal architecture of a protein kinase Biochim. Biophys. Acta 2010, 1804, 440-4
28. Zhang, F.; Strand, A.; Robbins, D.; Cobb, M. H.; Goldsmith, E. J. Atomic structure of the MAP kinase ERK2 at 2.3 A resolution Nature 1994, 367, 704-711
29. Canagarajah, B. J.; Khokhlatchev, A.; Cobb, M. H.; Goldsmith, E. J. Activation mechanism of the MAP kinase ERK2 by dual phosphorylation Cell 1997, 90, 859-869
30. Robinson, M. J.; Harkins, P. C.; Zhang, J.; Baer, R.; Haycock, J. W.; Cobb, M. H.; Goldsmith, E. J. Mutation of position 52 in ERK2 creates a nonproductive binding mode for adenosine 5′-triphosphate Biochemistry 1996, 35, 5641-5646
31. Turjanski, A. G.; Hummer, G.; Gutkind, J. S. How mitogen-activated protein kinases recognize and phosphorylate their targets: A QM/MM study J. Am. Chem. Soc. 2009, 131, 6141-8
32. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684-3690
33. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple amber force fields and development of improved protein backbone parameters Proteins: Struct., Funct., Bioinf. 2006, 65, 712-725
34. Meagher, K. L.; Redman, L. T.; Carlson, H. A. Development of polyphosphate parameters for use with the AMBER force field J. Comput. Chem. 2003, 24, 1016-1025
35. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics J. Mol. Graphics 1996, 14, 33-38
36. The PyMOL Molecular Graphics System, version 1.3r1; Schrodinger, LLC: Cambridge, MA, 2010.