Solid-state NMR-restrained ensemble dynamics of a membrane protein in explicit membranes

Biophysical Journal

Volumn 108, Issue 8, 2015, Pages 1954-1962

  Cheng, Xi ^a   Jo, Sunhwan ^a   Qi, Yifei ^a   Marassi, Francesca M ^b   Im, Wonpil ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; LIPID BILAYER; MEMBRANE PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; CHEMISTRY; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

AMINO ACID SEQUENCE; CAPSID PROTEINS; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING;

EID: 84928230032     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.03.012     Document Type: Article

References (55)

1. T.A. Cross, and V. Ekanayake A. Wright Solid state NMR: the essential technology for helical membrane protein structural characterization J. Magn. Reson. 239 2014 100 109
2. S. Wang, and V. Ladizhansky Recent advances in magic angle spinning solid state NMR of membrane proteins Prog. Nucl. Magn. Reson. Spectrosc. 82 2014 1 26
3. A.M. Bonvin, and A.T. Brünger Conformational variability of solution nuclear magnetic resonance structures J. Mol. Biol. 250 1995 80 93
4. O.F. Lange, and N.A. Lakomek B.L. de Groot Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution Science 320 2008 1471 1475
5. B. Richter, and J. Gsponer M. Vendruscolo The MUMO (minimal under-restraining minimal over-restraining) method for the determination of native state ensembles of proteins J. Biomol. NMR 37 2007 117 135
6. S. Jo, and W. Im Transmembrane helix orientation and dynamics: insights from ensemble dynamics with solid-state NMR observables Biophys. J. 100 2011 2913 2921
7. W. Im, S. Jo, and T. Kim An ensemble dynamics approach to decipher solid-state NMR observables of membrane proteins Biochim. Biophys. Acta 1818 2012 252 262
8. W. Im, M. Feig, and C.L. Brooks III An implicit membrane generalized born theory for the study of structure, stability, and interactions of membrane proteins Biophys. J. 85 2003 2900 2918
9. T. Lazaridis Effective energy function for proteins in lipid membranes Proteins 52 2003 176 192
10. X. Cheng, and S. Jo W. Im NMR-based simulation studies of Pf1 coat protein in explicit membranes Biophys. J. 105 2013 691 698
11. T. Kim, and K.I. Lee W. Im Influence of hydrophobic mismatch on structures and dynamics of gramicidin a and lipid bilayers Biophys. J. 102 2012 1551 1560
12. F.M. Marassi, and S.J. Opella Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints Protein Sci. 12 2003 403 411
13. A.C. Zeri, and M.F. Mesleh S.J. Opella Structure of the coat protein in fd filamentous bacteriophage particles determined by solid-state NMR spectroscopy Proc. Natl. Acad. Sci. USA 100 2003 6458 6463
14. B.R. Brooks, and C.L. Brooks III M. Karplus CHARMM: the biomolecular simulation program J. Comput. Chem. 30 2009 1545 1614
15. J. Lee, and J. Chen W. Im Application of solid-state NMR restraint potentials in membrane protein modeling J. Magn. Reson. 193 2008 68 76
16. L. Shi, and N.J. Traaseth G. Veglia A refinement protocol to determine structure, topology, and depth of insertion of membrane proteins using hybrid solution and solid-state NMR restraints J. Biomol. NMR 44 2009 195 205
17. Y. Tian, and C.D. Schwieters F.M. Marassi AssignFit: a program for simultaneous assignment and structure refinement from solid-state NMR spectra J. Magn. Reson. 214 2012 42 50
18. S. Jo, T. Kim, and W. Im Automated builder and database of protein/membrane complexes for molecular dynamics simulations PLoS ONE 2 2007 e880
19. S. Jo, and J.B. Lim W. Im CHARMM-GUI Membrane Builder for mixed bilayers and its application to yeast membranes Biophys. J. 97 2009 50 58
20. S. Jo, and T. Kim W. Im CHARMM-GUI: a web-based graphical user interface for CHARMM J. Comput. Chem. 29 2008 1859 1865
21. S.E. Feller, Y.H. Zhang, and R.W. Pastor Computer simulation of liquid/liquid interfaces. 2. Surface tension-area dependence of a bilayer and monolayer J. Chem. Phys. 103 1995 10267 10276
22. A.D. MacKerell, and D. Bashford M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616
23. A.D. Mackerell Jr., M. Feig, and C.L. Brooks III Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415
24. J.B. Klauda, and R.M. Venable R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
25. W.L. Jorgensen, and J. Chandrasekhar M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 935
26. E.A. Dolan, and R.M. Venable B.R. Brooks Simulations of membranes and other interfacial systems using P2(1) and Pc periodic boundary conditions Biophys. J. 82 2002 2317 2325
27. J.P. Ryckaert, G. Ciccotti, and H.J.C. Berendsen Numerical integration of Cartesian equations of motion of a system with constraints - molecular-dynamics of N-alkanes J. Comput. Phys. 23 1977 327 341
28. P.J. Steinbach, and B.R. Brooks New spherical-cutoff methods for long-range forces in macromolecular simulation J. Comput. Chem. 15 1994 667 683
29. U. Essmann, and L. Perera L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
30. D.E. Shaw, and M.M. Deneroff S.C. Wang Anton, a special-purpose machine for molecular dynamics simulation Commun. ACM 51 2008 91 97
31. G.J. Martyna, D.J. Tobias, and M.L. Klein Constant-pressure molecular-dynamics algorithms J. Chem. Phys. 101 1994 4177 4189
32. G.J. Martyna, and M.E. Tuckerman M.L. Klein Explicit reversible integrators for extended systems dynamics Mol. Phys. 87 1996 1117 1157
33. Y. Shan, and J.L. Klepeis D.E. Shaw Gaussian split Ewald: A fast Ewald mesh method for molecular simulation J. Chem. Phys. 122 2005 54101
34. J.W. Pitera, and J.D. Chodera On the use of experimental observations to bias simulated ensembles J. Chem. Theory Comput. 8 2012 3445 3451
35. S.M. Islam, and R.A. Stein B. Roux Structural refinement from restrained-ensemble simulations based on EPR/DEER data: application to T4 lysozyme J. Phys. Chem. B 117 2013 4740 4754
36. J. Chen, and H.S. Won C.L. Brooks III Generation of native-like protein structures from limited NMR data, modern force fields and advanced conformational sampling J. Biomol. NMR 31 2005 59 64
37. B. Xia, and V. Tsui P.E. Wright Comparison of protein solution structures refined by molecular dynamics simulation in vacuum, with a generalized Born model, and with explicit water J. Biomol. NMR 22 2002 317 331
38. X. Cheng, and W. Im NMR observable-based structure refinement of DAP12-NKG2C activating immunoreceptor complex in explicit membranes Biophys. J. 102 2012 L27 L29
39. J. Chen, W. Im, and C.L. Brooks III Refinement of NMR structures using implicit solvent and advanced sampling techniques J. Am. Chem. Soc. 126 2004 16038 16047
40. F.C. Almeida, and S.J. Opella fd coat protein structure in membrane environments: structural dynamics of the loop between the hydrophobic trans-membrane helix and the amphipathic in-plane helix J. Mol. Biol. 270 1997 481 495
41. T. Kim, S. Jo, and W. Im Solid-state NMR ensemble dynamics as a mediator between experiment and simulation Biophys. J. 100 2011 2922 2928
42. W. Im, and C.L. Brooks III Interfacial folding and membrane insertion of designed peptides studied by molecular dynamics simulations Proc. Natl. Acad. Sci. USA 102 2005 6771 6776
43. J.A. Killian, and T.K. Nyholm Peptides in lipid bilayers: the power of simple models Curr. Opin. Struct. Biol. 16 2006 473 479
44. E. Strandberg, and S. Esteban-Martín J. Salgado Hydrophobic mismatch of mobile transmembrane helices: merging theory and experiments Biochim. Biophys. Acta 1818 2012 1242 1249
45. M.B. Ulmschneider, M.S. Sansom, and A. Di Nola Properties of integral membrane protein structures: derivation of an implicit membrane potential Proteins 59 2005 252 265
46. O.S. Andersen, and R.E. Koeppe 2nd Bilayer thickness and membrane protein function: an energetic perspective Annu. Rev. Biophys. Biomol. Struct. 36 2007 107 130
47. S. Dorairaj, and T.W. Allen On the thermodynamic stability of a charged arginine side chain in a transmembrane helix Proc. Natl. Acad. Sci. USA 104 2007 4943 4948
48. T. Kim, and W. Im Revisiting hydrophobic mismatch with free energy simulation studies of transmembrane helix tilt and rotation Biophys. J. 99 2010 175 183
49. T. Mori, F. Ogushi, and Y. Sugita Analysis of lipid surface area in protein-membrane systems combining Voronoi tessellation and Monte Carlo integration methods J. Comput. Chem. 33 2012 286 293
50. H. Rui, R. Kumar, and W. Im Membrane tension, lipid adaptation, conformational changes, and energetics in MscL gating Biophys. J. 101 2011 671 679
51. H. Rui, J. Lee, and W. Im Comparative molecular dynamics simulation studies of protegrin-1 monomer and dimer in two different lipid bilayers Biophys. J. 97 2009 787 795
52. H. Rui, and K.T. Root W. Im Probing the U-shaped conformation of caveolin-1 in a bilayer Biophys. J. 106 2014 1371 1380
53. S. Choe, K.A. Hecht, and M. Grabe A continuum method for determining membrane protein insertion energies and the problem of charged residues J. Gen. Physiol. 131 2008 563 573
54. A. Panahi, and M. Feig Dynamic heterogeneous dielectric generalized Born (DHDGB): an implicit membrane model with a dynamically varying bilayer thickness J. Chem. Theory Comput. 9 2013 1709 1719
55. Y.C. Zhou, B. Lu, and A.A. Gorfe Continuum electromechanical modeling of protein-membrane interactions Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 82 2010 041923