Crystal structure of the M intermediate of bacteriorhodopsin: Allosteric structural changes mediated by sliding movement of a transmembrane helix

Journal of Molecular Biology

Volumn 341, Issue 4, 2004, Pages 1023-1037

  Takeda, Kazuki ^a   Matsui, Yasuhiro ^a   Kamiya, Nobuo ^b   Adachi, Shin Ichi ^b   Okumura, Hideo ^a   Kouyama, Tsutomu ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b RIKEN HARIMA INSTITUTE   (Japan)

Author keywords

allosteric effect; proton pump; retinal; water; X ray crystallography

Indexed keywords

BACTERIAL PROTEIN; BACTERIORHODOPSIN; LYSINE; MEMBRANE PROTEIN;

ALLOSTERISM; ARTICLE; BIOACCUMULATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HALOBACTERIUM SALINARUM; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; NONHUMAN; PHOTON; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; ROOM TEMPERATURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

EID: 3843096037     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.06.080     Document Type: Article

References (67)

1. U. Haupts, J. Tittor, and D. Oesterhelt Closing in on bacteriorhodopsin: progress in understanding the molecule Annu. Rev. Biophys. Biomol. Struct. 8 1999 367 399
2. F.M.H. Betancourt, and R.M. Glaeser Chemical and physical evidence for multiple functional steps comprising the M state of the bacteriorhodopsin photocycle Biochim. Biophys. Acta 1460 2000 106 108
3. N.A. Dencher, H.J. Sass, and G. Bueldt Water and bacteriorhodopsin: structure, dynamics, and function Biochim. Biophys. Acta 1460 2000 192 203
4. S. Subramaniam, and R. Henderson Crystallographic analysis of protein conformational changes in the bacteriorhodpsin photocycle Biochim. Biophys. Acta 1460 2000 157 165
5. J.K. Lanyi, and H. Luecke Bacteriorhodopsin Curr. Opin. Struct. Biol. 11 2001 415 419
6. S.P. Balashov, and T.G. Ebrey Trapping and spectroscopic identification of the photointermediates of bacteriorhodopsin at low temperatures Photochem. Photobiol. 73 2001 453 462
7. Y. Matsui, K. Sakai, M. Murakami, Y. Shiro, S. Adachi, H. Okumura, and T. Kouyama Specific damages induced by X-ray radiation and structural changes in the primary photoreaction of bacteriorhodopsin J. Mol. Biol. 324 2002 469 481
8. S. Hayashi, E. Tajkhorshid, and K. Schulten Structural changes during the formation of early intermediates in the bacteriorhodopsin photocycle Biophys. J. 83 2002 1281 1297
9. B. Schobert, J. Cupp-Vickery, V. Hornak, S. Smith, and J. Lanyi Crystallographic structure of the K intermediate of bacteriorhodopsin: conservation of free energy after photoisomerization of the retinal J. Mol. Biol. 321 2002 715 726
10. H. Kandori, M. Belenky, and J. Herzfeld Vibrational frequency and dipolar orientation of the protonated Schiff base in bacteriorhodopsin before and after photoisomerization Biochemistry 41 2003 6026 6031
11. T. Kouyama, T. Nishikawa, T. Tokuhisa, and H. Okumura Crystal structure of the L intermediate of bacteriorhodopsin: evidence for vertical translocation of a water molecule during the proton pumping cycle J. Mol. Biol. 335 2004 531 546
12. S.P. Fodor, W.T. Pollard, R. Gebhard, E.M. van den Berg, and R.A. Mathies Bacteriorhodopsin's L550 intermediate contains a C14-C15 s-trans-retinal chromophore Proc. Natl Acad. Sci. USA 85 1988 2156 2160
13. H. Belrhali, P. Nollert, A. Royant, C. Menzel, J.P. Rosenbusch, E.M. Landau, and E. Pebay-Peyroula Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the pruple membrane at 1.9 resolution Proteins: Struct. Funct. Genet. 7 1999 909 917
14. H. Luecke, B. Schobert, H.-T. Richter, J.-P. Cartailler, and J.K. Lanyi Structure of bacteriorhodopsin at 1.55 resolution J. Mol. Biol. 291 1999 899 911
15. A. Maeda Internal water molecules as mobile polar groups for light-induced proton translocation in bacteriorhodopsin and rhodopsin as studied by difference FTIR spectroscopy Biochemistry (Moscow) 66 2001 1256 1268
16. A. Maeda, S.P. Balashov, J. Lugtenburg, M.A. Verhoeven, J. Herzfeld, and M. Belenky Interaction of internal water molecules with the Schiff base in the L intermediate of the bacteriorhodopsin photocycle Biochemistry 41 2002 3803 3809
17. N.A. Dencher, D. Dresselhaus, G. Zaccai, and G. Bueldt Structural changes in bacteriorhodopsin during proton translocation revealed by neutron diffraction Proc. Natl Acad. Sci. USA 86 1989 7876 7879
18. M. Weik, G. Zaccai, N.A. Dencher, D. Oesterhelt, and T. Hauss Structure and hydration of the M-state of the bacteriorhodopsin mutant D96N studied by neutron diffraction J. Mol. Biol. 275 1998 625 634
19. M. Nakasako, M. Kataoka, Y. Amemiya, and F. Tokunaga Crystallographic characterization by X-ray diffraction of the M-intermediate from the photo-cycle of bacteriorhodopsin at room temperature FEBS Letters 292 1991 73 75
20. M.H.J. Koch, N.A. Dencher, D. Oesterhelt, H.-J. Ploehn, G. Rapp, and G. Bueldt Time-resolved X-ray diffraction study of structural changes associated with the photocycle of bacteriorhodopsin EMBO J. 10 1991 521 526
21. H. Kamikubo, T. Oka, Y. Imamoto, F. Tokunaga, J.K. Lanyi, and M. Kataoka The last phase of the reprotonation switch in bacteriorhodopsin: The transition between the M-type and the N-type protein conformation depends on hydration Biochemistry 36 1997 12282 12287
22. T. Oka, N. Yagi, T. Fujisawa, H. Kamikubo, F. Tokunaga, and M. Kataoka Time-resolved X-ray diffraction reveals multiple conformations in the M-N transition of the bacteriorhodopsin photocycle Proc. Natl Acad. Sci. USA 97 2000 14278 14282
23. S. Subramaniam, M. Gerstein, D. Oesterhelt, and R. Henderson Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin EMBO J. 12 1993 1 8
24. B.-G. Han, J. Vonck, and R.M. Glaeser The bacteriorhodopsin photocycle: direct structural study of two substrates of the M-intermediate Biophys. J. 67 1994 1179 1186
25. J. Vonck A three-dimensional difference map of the N intermediate in the bacteriorhodopsin photocycle: part of the F helix tilts in the M to N transition Biochemistry 35 1996 5870 5878
26. F.M. Hendrickson, F. Burkard, and R.M. Glaeser Structural characterization of the L-to-M transition of the bacteriorhodopsin photocycle Biophys. J. 75 1998 1446 1454
27. S. Subramaniam, M. Lindahl, P. Bullough, A.R. Fauqi, J. Tittor, and D. Oesterhelt Protein conformational changes in the bacteriorhodopsin photocycle J. Mol. Biol. 287 1999 145 161
28. J. Tittor, S. Paula, S. Subramaniam, J. Heberle, R. Henderson, and D. Oesterhelt Proton translocation by bacteriorhodopsin in the absence of substantial conformational changes J. Mol. Biol. 319 2002 555 565
29. J. Vonck Structure of the bacteriorhodopsin mutant F219L N intermediate revealed by electron crystallography EMBO J. 19 2000 2152 2160
30. G.F. Schertler, R. Lozier, H. Michel, and D. Oesterhelt Chromophore motion during the bacteriorhodopsin photocycle: polarized absorption spectroscopy of bacteriorhodopsin and its M-state in bacteriorhodopsin crystals EMBO J. 10 1991 2353 2361
31. T. Kouyama, M. Yamamoto, N. Kamiya, H. Iwasaki, T. Ueki, and I. Sakurai Polyhedral assembly of a membrane protein in its three-dimensional crystal J. Mol. Biol. 236 1994 990 994
32. E.M. Landau, and J.P. Rosenbusch Lipidic cubic phases: a novel concept for the crystallization of membrane proteins Proc. Natl Acad. Sci. USA 93 1996 14532 14535
33. L.-O. Essen, R. Siegert, W.D. Lehmann, and D. Oesterhelt Lipid patches in membrane protein oligomers: crystal struture of the bacteriorhodopsin-lipid complex Proc. Natl Acad. Sci. USA 95 1998 11673 11678
34. K. Takeda, H. Sato, T. Hino, M. Kono, K. Fukuda, and I. Sakurai A novel three-dimensional crystal of bacteriorhodopsin obtained by successive fusion of the vesicular assemblies J. Mol. Biol. 283 1998 463 474
35. S. Faham, and J.U. Bowie Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure J. Mol. Biol. 316 2002 1 6
36. H. Luecke, B. Schobert, H.-T. Richter, J.-P. Cartailler, and J.K. Lanyi Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution Science 286 1999 255 260
37. H. Luecke, B. Schobert, H.-T. Richter, J.-P. Cartailler, and J.K. Lanyi Coupling photoisomerization of retinal to directional transport in bacteriorhodopsin J. Mol. Biol. 300 2000 1237 1255
38. K. Edman, P. Nollert, A. Royant, H. Belrhali, E. Pebay-Peyroula, and J. Hajdu High-resolution X-ray structure of an early intermediate in the bacteriorhodopsin photocycle Nature 401 1999 822 826
39. H.J. Sass, G. Bueldt, R. Gessenich, D. Hehn, D. Neff, and R. Schlesinger Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin Nature 406 2000 649 653
40. A. Royant, K. Edman, T. Ursby, E. Pebay-Peyroula, E.M. Landau, and R. Neutze Helix deformation is coupled to vectorial proton transport in the photocycle of bacteriorhodopsin Nature 406 2000 645 648
41. M.T. Facciotti, S. Rouhani, F.T. Burkard, F.M. Betancourt, K.H. Downing, and R.B. Rose Structure of an early intermediate in the M-state phase of the bacteriorhodopsin photocycle Biophys. J. 81 2001 3442 3455
42. S. Rouhani, J.-P. Cartailler, M.T. Facciotti, P. Walian, R. Needleman, and J.K. Lanyi Crystal structure of the D85S mutant of bacteriorhodopsin: model of an O-like photocycle intermediate J. Mol. Biol. 313 2001 615 628
43. B. Schobert, L.S. Brown, and J.K. Lanyi Crystallographic structures of the M and N intermediates of bacteriorhodopsin: assembly of a hydrogen-bonded chain of water molecules between Asp96 and the retinal Schiff base J. Mol. Biol. 330 2003 553 570
44. 22, intermediates of the photocycle J. Mol. Biol. 328 2003 439 450
45. H. Kandori, Y. Yamazaki, Y. Shichida, J. Raap, J. Lugtenburg, M. Belenky, and J. Herzfeld Tight Asp-85-Thr-89 association during the pump switch of bacteriorhodopsin Proc. Natl Acad. Sci. USA 98 2001 1571 1576
46. H. Sato, K. Takeda, K. Tani, T. Hino, T. Okada, and M. Nakasako Specific lipid-protein interactions in a novel honeycomb lattice structure of bacteriorhodopsin Acta Crystallog. sect. D 55 1999 1251 1256
47. N. Radzwill, K. Gerwert, and H.-J. Steinhoff Time-resolved detection of transient movement of helices F and G in doubly spin-labeled bacteriorhodopsin Biophys. J. 80 2001 2856 2866
48. N.A. Dencher, G. Papadopoulos, D. Dresselhaus, and G. Bueldt Light and dark-adapted bacteriorhodopsin: a time-resolved neutron diffraction study Biochim. Biophys. Acta 1026 1990 51 56
49. H. Takei, G. Yahaloma, Z. Rothman, A. Lewis, and M. Sheves Active site lysine backbone undergoes conformational changes in the bacteriorhodopsin photocycle J. Biol. Chem. 269 1994 7387 7389
50. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
51. S.P. Balashov, M. Lu, E.S. Imasheva, R. Govindjee, T.G. Ebrey, and B. Othersen III The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH Biochemistry 38 1999 2026 2039
52. A.V. Dioumaev, H.-T. Richter, L.S. Brown, M. Tanio, S. Tuzi, and H. Saito Existence of a proton transfer chain in bacteriorhodopsin: participation of Glu-194 in the release of protons to the extracellular surface Biochemistry 37 1998 2496 2506
53. a changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy Proc. Natl Acad. Sci. USA 96 1999 5498 5503
54. a of the group responsible for the light-driven proton release in bacteriorhodopsin Biophys. J. 71 1996 1011 1023
55. T. Althaus, and M. Stockburger Time and pH dependence of the L-to-M transition in the photocycle of bacteriorhodopsin and its correlation with proton release Biochemistry 37 1998 2807 2817
56. A. Maeda, F.L. Tomson, R.B. Gennis, H. Kandori, T.G. Ebrey, and S.P. Balashov Relocation of internal bound water in bacteriorhodopsin during the photoreaction of M at low temperatures: an FTIR study Biochemistry 39 2000 10154 10162
57. M.T. Facciotti, S. Rouhani, and R.M. Glaeser Crystal structures of bR(D85S) favor a model of bacteriorhodopsin as a hydroxyl-ion pump FEBS Letters 564 2004 301 306
58. J. Hu, R.G. Griffin, and J. Herzfeld Synergy in the spectral tuning of retinal pigments: complete accounting of the opsin shift in bacteriorhodopsin Proc. Natl Acad. Sci. USA 91 1994 8880 8884
59. D. Oesterhelt, and W. Stoeckenius Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane Methods Enzymol. 31 1974 667 678
60. K. Sakai, Y. Matsui, T. Kouyama, Y. Shiro, and S. Adachi Optical monitoring of freeze-trapped reaction intermediates in protein crystals: a microspectrophotometer for cryogenic protein crystallography J. Appl. Crystallog. sect. D 35 2002 270 273
61. I. Steller, B. Bolotovsky, and M.G. Rossmann An algorithm for automatic indexing of oscillation images using Fourier analysis J. Appl. Crystallog. sect. D 30 1997 1036 1040
62. Collaborative Computating Project Number 4 (1994) Programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
63. A.T. Brünger, P.D. Adams, G.M. Glore, W.L. Delano, P. Gros, and R.W. Grosse-Kunstleve Crystallography and NMR system (CNS): a new software system for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
64. D.E. McRee Practical Protein Crystallography 1993 Academic Press San Diego
65. A.C. Wallace, R.A. Laskowski, and J.M. Thornton LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8 1995 127 134
66. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallog. 24 1991 946 950
67. E.A. Merritt, and M.E.P. Murphy Raster3D version 2.0. A program for photorealistic molecular graphics Acta Crystallog. sect. D 50 1994 869 873