Water dynamics simulation as a tool for probing proton transfer pathways in a heptahelical membrane protein

Proteins: Structure, Function and Genetics

Volumn 58, Issue 3, 2005, Pages 528-537

  Kandt, Christian ^a   Gerwert, Klaus ^a   Schlitter, Jürgen ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Bacteriorhodopsin; H bonded network; Internal water; Molecular dynamics simulation; N intermediate; Proton pump; Retinal protein; Water density

Indexed keywords

BACTERIORHODOPSIN; MEMBRANE PROTEIN; PROTON; SCHIFF BASE; WATER;

ARTICLE; BINDING SITE; DIFFUSION; FOURIER TRANSFORMATION; HYDROGEN BOND; LIGHT; MEMBRANE BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON TRANSPORT; SIMULATION; STRUCTURE ANALYSIS; WATER TRANSPORT; X RAY ANALYSIS;

ASPARTIC ACID; BACTERIORHODOPSINS; BINDING SITES; CELL MEMBRANE; COMPUTER SIMULATION; CYTOPLASM; HALOBACTERIUM SALINARUM; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; LIGHT; MEMBRANE PROTEINS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEINS; PROTONS; RETINALDEHYDE; SCHIFF BASES; THERMODYNAMICS; WATER;

EID: 12944262223     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20343     Document Type: Article

References (48)

1. Lanyi JK, Schobert B. Local-global conformational coupling in a heptahelical membrane protein: transport mechanism from crystal structures of the nine states in the bacteriorhodopsin photocycle. Biochemistry 2004;43:3-8.
2. Lozier RH, Bogomolni RA, Stoeckenius W. Bacteriorhodopsin: a light-driven proton pump in Halobacterium halobium. Biophys J 1975;15:955-962.
3. Gerwert K, Hess B, Soppa J, Oesterhelt D. Role of aspartate-96 in proton translocation by bacteriorhodopsin. Proc Nat Acad Sci USA 1989;86:4943-4947.
4. Gerwert K, Souvignier G, Hess B. Simultaneous monitoring of light-induced changes in protein side-group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier-transform infrared spectroscopy. Proc Nat Acad Sci USA 1990;87:9774-9778.
5. Richter HT, Brown LS, Needleman R, Lanyi JK. A linkage of the pKa's of asp-85 and glu-204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry 1996;35:4054-4062.
6. Rammelsberg R, Huhn G, Lubben M, Gerwert K. Bacteriorhodopsins intramolecular proton-release pathway consists of a hydrogen-bonded network. Biochemistry 1998;37:5001-5009.
7. Heßling B, Souvignier G, Gerwert K. A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates. Biophys J 1993;65:1929-1941.
8. Wicke E, Eigen M, Ackermann T. Über den Zustand des Protons (Hydroniumions) in wässriger Lösung. Zeitschrift für Physikalische Chemie (NF) 1954;1:340-364.
9. Zundel G. Proton polarizability and proton transfer processes in hydrogen bonds and cation polarizabilities of other cation bonds: their importance to understand molecular processes in electrochemistry and biology. Trends Phys Chem 1992;3:129-156.
10. Le Coutre J, Tittor J, Oesterhelt D, Gerwert K. Experimental evidence for hydrogen-bonded network proton transfer in bacteriorhodopsin shown by Fourier-transform infrared spectroscopy using azide as catalyst. Proc Nat Acad Sci USA 1995;92:4962-4966.
11. Spassov VZ, Luecke H, Gerwert K, Bashford D. pK(a) calculations suggest storage of an excess proton in a hydrogen-bonded water network in bacteriorhodopsin. J Mol Biol 2001;312:203-219.
12. Garczarek F, Wang J, El-Sayed MA, Gerwert K. The assignment of the different infrared continuum absorbance changes observed in the 3000-1800-cm-1 region during the bacteriorhodopsin photocycle. Biophys J 2004;87:2676-2682.
13. Belrhali H, Nollert P, Royant A, Menzel C, Rosenbusch JP, Landau EM, Pebay-Peyroula E. Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrana at 1.9 angstrom resolution. Structure 1999;7:909-917.
14. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. Structure of bacteriorhodopsin at 1.55 angstrom resolution. J Mol Biol 1999;291:899-911.
15. Sass HJ, Buldt G, Gessenich R, Hehn D, Neff D, Schlesinger R, Berendzen J, Ormos P. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature 2000;406: 649-653.
16. Henderson R, Baldwin JM, Ceska TA, Zemlin F, Beckmann E, Downing KH. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 1990;213: 539-560.
17. Grigorieff N, Ceska TA, Downing KH, Baldwin JM, Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol 1996;259:393-421.
18. Papadopoulos G, Dencher NA, Zaccai G, Büldt G. Water molecules and exchangeable hydrogen ions at the active centre of bacteriorhodopsin localized by neutron diffraction: elements of the proton pathway? J Mol Biol 1990;214:15-19.
19. Papadopoulos G, Hauss T. Determination of water molecules in the proton pathway of bacteriorhodopsin using neutron diffraction data. Eur Biophys J 2003;32:392-401.
20. Nagel J, Edholm O, Berger O, Jänig F. Investigation of the proton release channel of Bacteriorhodopsin in different intermediates of the photo cycle: a molecular dynamics study. Biochemistry 1997; 36:2875-2883.
21. Roux B, Nina M, Regis P, Smith JC. Thermodynamic stability of water molecules in the Bacteriorhodopsin proton channel: a molecular dynamics free energy perturbation study. Biophys J 1996;71:670-681.
22. Pebay-Peyroula E, Rummel G, Rosenbusch JP, Landau EM. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science 1997;277:1676-1681.
23. Essen L, Siegert R, Lehmann WD, Oesterhelt D. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex. Proc Natl Acad Sci USA 1998;95:11673-11678.
24. Baudry J, Taijkorshid E, Molnar F, Phillips J, K. S. Molecular dynamics study of Bacteriorhodopsin and the purple membrane. J Phys Chem 2001;105:905-918.
25. Hayashi S, Tajkhorshid E, Schulten K. Structural changes during the formation of early intermediates in the bacteriorhodopsin photocycle. Biophys J 2002;83:1281-1297.
26. Edholm O, Jänig F. Molecular dynamics simulation of bacteriorhodopsin. In: Pullman A, Jortner J, and Pullman B, editors. Membrane proteins: structures, interactions and models. Dordrecht: Kluwer Academic; 1992.
27. Kandt C, Schlitter J, Gerwert K. Dynamics of water molecules in the bacteriorhodopsin trimer in explicit lipid/water environment. Biophys J 2004;86:705-717.
28. Bashford D, Gerwert K. Electrostatic calculations of the pKa values of ionizable groups in bacteriorhodopsin. J Mol Biol 1992; 224:473-486.
29. Scharnagl C, Fischer SF. Conformational flexibility of arginine-82 as source for the heterogeneous and pH-dependent kinetics of the primary proton transfer step in the bacteriorhodopsin photocycle: an electrostatic model. Chem Phys 1996;212:231-246.
30. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science 1999;286:255-261.
31. Hutson MS, Alexiev U, Shilov SV, Wise KJ, Braiman MS. Evidence for a perturbation of arginine-82 in the bacteriorhodopsin photocycle from time-resolved infrared spectra. Biochemistry 2000;39:13189-13200.
32. Heberle J, Dencher NA. Surface-bound optical probes monitor protein translocation and surface potential changes during the bacteriorhodopsin photocycle. Proc Nat Acad Sci USA 1992;89: 5996-6000.
33. Zimanyi L, Cao Y, Chang M, Ni B, Needleman R, Lanyi JK. The two consecutive M substates in the photocycle of bacteriorhodopsin are affected specifically by the D85N and D96N residue replacements. Photochem Photobiol 1992;56:1049-1055.
34. Heberle J, Riesle J, Thiedemann G, Oesterhelt D, Dencher NA. Proton migration along the membrane surface and retarded surface to bulk transfer. Nature 1994;370:379-382.
35. Alexiev U, Mollaghababa R, Scherrer P, Khorana HG, Heyn M. Rapid long-range proton diffusion along the surface of the purple membrane and delayed proton transfer into the bulk. Proc Natl Acad Sci USA 1995;92:372-376.
36. Dencher NA, Heberle J, Büldt G, Höltje H-D, Höltje M. What do neutrons, X-ray synchrotron radiation, optical pH-indicators, and mutagenesis tell us about the light-driven proton pump bacteriorhodopsin? In: Pullman A, Jortner J, and Pullman B, editors. Membrane proteins: structures, interactions and models. Dordrecht: Kluwer Academic; 1992. p 69-84.
37. Dencher NA, Heberle J, Büldt G, Höltje H-D, Höltje M. Active and passive proton transfer steps through bacteriorhodopsin are controlled by a light-triggered hydrophobic gate. In: Rigaud JL, editor. Structures and functions of retinal proteins. Vol. 221. John Libbey Eurotext Ltd., Montrouge; 1992. p 213-216.
38. Lanyi JK. Progress toward an explicit mechanistic model for the light-driven pump, bacteriorhodopsin. FEBS Lett 1999;464:103-107.
39. Riesle J, Oesterhelt D, Dencher NA, Heberle J. D38 is an essential part of the proton translocation pathway in bacteriorhodopsin. Biochemistry 1996;35:6635-6643.
40. Schobert B, Brown LS, Lanyi JK. Crystallographic structures of the M and N intermediates of bacteriorhodopsin: assembly of a hydrogen-bonded chain of water molecules between Asp-96 and the retinal Schiffbase. J Mol Biol 2003;330:553-570.
41. Laskowski RA. Surfnet - a program for visualizing molecular surfaces, cavities, and intermolecular interactions. J Mol Graphics 1995;13:323-330.
42. Tieleman DP, Sansom MSP, Berendsen HJC. Alamethicin helices in a bilayer and in solution: molecular dynamics simulations. Biophys J 1999;76:40-49.
43. Berendsen HJC, Vanderspoel D, Vandrunen R. Gromacs - a message-passing parallel molecular dynamics implementation. Comput Phys Commun 1995;91:43-56.
44. Lindahl E, Hess B, van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J Mol Model 2001;7: 306-317.
45. Makarov V, Andrews B, Smith P, Pettitt B. Residence times of water molecules in the hydration sites of myoglobin. Biophys J 2000;79:2966-2974.
46. Henchman R, McCammon JA. Extracting hydration sites around proteins from explicit water simulations. J Comput Chem 2002;23: 861-869.
47. Koradi R, Billeter M, Wüthrich K. MolMol: a program for display and analysis of macromolecular structures. J Mol Graphics 1996; 14:51-55.
48. Schaetzler B, Dencher NA, Tittor J, Oesterhelt D, Yaniv-Checover S, Nachliel E, Gutman M. Subsecond proton-hole propagation in bacteriorhodopsin. Biophys J 2003;84:671-686.