Time-resolved microspectroscopy on a single crystal of bacteriorhodopsin reveals lattice-induced differences in the photocycle kinetics

Biophysical Journal

Volumn 91, Issue 4, 2006, Pages 1441-1451

  Efremov, R ^a,b   Gordeliy, V I ^a,b   Heberle, J ^a,c   Buldt G ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

^c BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; INFRARED SPECTROSCOPY; INFRARED SPECTROSCOPY MICROSPECTROSCOPY; KINETICS; PHOTOREACTIVITY; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PURPLE MEMBRANE; SPECTROSCOPY; STRUCTURE ANALYSIS; ULTRAVIOLET SPECTROSCOPY;

EID: 33746795960     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.083345     Document Type: Article

References (67)

1. Oesterhelt, D., and W. Stoeckenius. 1973. Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci. USA. 70:2853-2857.
2. Lanyi, J. K. 2004. Bacteriorhodopsin. Annu. Rev. Physiol. 66:665-688.
3. Oesterhelt, D. 1998. The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr. Opin. Struct. Biol. 8:489-500.
4. Landau, E. M., and J. P. Rosenbusch. 1996. Lipidic cubic phases: a novel concept for the crystallization of membrane proteins. Proc. Natl. Acad. Sci. USA. 93:14532-14535.
5. Faham, S., and J. U. Bowie. 2002. Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J. Mol. Biol. 316:1-6.
6. Essen, L. O., R. Siegert, W. D. Lehmannn, and D. Oesterhelt. 1998. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex. Proc. Natl. Acad. Sci. USA. 95:11673-11678.
7. Takeda, K., H. Sato, T. Hino, M. Kono, K. Fukuda, I. Sakurai, T. Okada, and T. Kouyama. 1998. A novel three-dimensional crystal of bacteriorhodopsin obtained by successive fusion of the vesicular assemblies. J. Mol. Biol. 283:463-474.
8. Lanyi, J. K., and B. Schobert. 2004. Local-global conformational coupling in a heptahelical membrane protein: transport mechanism from crystal structures of the nine states in the bacteriorhodopsin photocycle. Biochemistry. 43:3-8.
9. Pebay-Peyroula, E., G. Rummel, J. P. Rosenbusch, and E. M. Landau. 1997. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science. 277:1676-1681.
10. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:899-911.
11. Heberle, J., G. Büldt, E. Koglin, J. P. Rosenbusch, and E. M. Landau. 1998. Assessing the functionality of a membrane protein in a three-dimensional crystal. J. Mol. Biol. 281:587-592.
12. Balashov, S. P., and T. G. Ebrey. 2001. Trapping and spectroscopic identification of the photointermediates of bacteriorhodopsin at low temperatures. Photochem. Photobiol. 73:453-462.
13. Lanyi, J. K., and B. Schobert. 2003. Mechanism of proton transport in bacteriorhodopsin from crystallographic structures of the K, L, M-1, M-2, and M-2′ intermediates of the photocycle. J. Mol. Biol. 328:439-450.
14. Royant, A., K. Edman, T. Ursby, E. Pebay-Peyroula, E. M. Landau, and R. Neutze. 2001. Spectroscopic characterization of bacteriorhodopsin's L-intermediate in 3D crystals cooled to 170 K. Photochem. Photobiol. 74:794-804.
15. Schenkl, S., E. Portuondo, G. Zgrablic, M. Chergui, W. Suske, M. Dolder, E. M. Landau, and S. Haacke. 2003. Compositional heterogeneity reflects partial dehydration in three-dimensional crystals of bacteriorhodopsin. J. Mol. Biol. 329:711-719.
16. Edman, K., P. Nollert, A. Royant, H. Belrhali, E. Pebay-Peyroula, J. Hajdu, R. Neutze, and E. M. Landau. 1999. High-resolution x-ray structure of an early intermediate in the bacteriorhodopsin photocycle. Nature. 401:822-826.
17. Lanyi, J., and B. Schobert. 2002. Crystallographic structure of the retinal and the protein after deprotonation of the Schiff base: the switch in the bacteriorhodopsin photocycle. J. Mol. Biol. 321:727-737.
18. Fedorov, R., I. Schlichting, E. Hartmann, T. Domratcheva, M. Fuhrmann, and P. Hegemann. 2003. Crystal structures and molecular mechanism of a light-induced signaling switch: the Phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys. J. 84:2474-2482.
19. Kort, R., R. B. Ravelli, F. Schotte, D. Bourgeois, W. Crielaard, K. J. Hellingwerf, and M. Wulff. 2003. Characterization of photocycle intermediates in crystalline photoactive yellow protein. Photochem. Photobiol. 78:131-137.
20. Schobert, B., L. S. Brown, and J. K. Lanyi. 2003. 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 Schiff base. J. Mol. Biol. 330:553-570.
21. Ng, K., E. D. Getzoff, and K. Moffat. 1995. Optical studies of a bacterial photoreceptor protein, photoactive yellow protein, in single crystals. Biochemistry. 34:879-890.
22. Gerwert, K., B. Hess, H. Michel, and S. Buchanan. 1988. FTIR studies on crystals of photosynthetic reaction centers. FEBS Lett. 232:303-307.
23. Facciotti, M. T., S. Rouhani, F. T. Burkard, F. M. Betancourt, K. H. Downing, R. B. Rose, G. McDermott, and R. M. Glaeser. 2001. Structure of an early intermediate in the M-state phase of the bacteriorhodopsin photocycle. Biophys. J. 81:3442-3455.
24. Oesterhelt, D., and W. Stoeckenius. 1974. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31:667-686.
25. Gordeliy, V. I., R. Schlesinger, R. Efremov, G. Büldt, and J. Heberle. 2003. Crystallization in lipidic cubic phases: a case study with bacteriorhodopsin. In Membrane Protein Protocols: Expression, Purification, and Crystallization. B. Selinsky, editor. Humana Press, Totowa, NJ. 305-316.
26. Muller, K. H., and T. Plesser. 1991. Variance reduction by simultaneous multiexponential analysis of data sets from different experiments. Eur. Biophys. J. 19:231-240.
27. Chizhov, I., D. S. Chernavskii, M. Engelhard, K. H. Mueller, B. V. Zubov, and B. Hess. 1996. Spectrally silent transitions in the bacteriorhodopsin photocycle. Biophys. J. 71:2329-2345.
28. Fischer, U., and D. Oesterhelt. 1979. Chromophore equilibria in bacteriorhodopsin. Biophys. J. 28:211-230.
29. Dencher, N. A., and M. P. Heyn. 1978. Formation and properties of bacteriorhodopsin monomers in the non-ionic detergents octyl-beta-D-glucoside and Triton X-100. FEBS Lett. 96:322-326.
30. Metz, G., F. Siebert, and M. Engelhard. 1992. Asp85 is the only internal aspartic acid that gets protonated in the M intermediate and the purple-to-blue transition of bacteriorhodopsin. A solid-state 13C CP-MAS NMR investigation. FEBS Lett. 303:237-241.
31. Hildebrandt, P., and M. Stockburger. 1984. Role of water in bacteriorhodopsin's chromophore: resonance Raman study. Biochemistry. 23:5539-5548.
32. le Coutre, J., and K. Gerwert. 1996. Kinetic isotope effects reveal an ice-like and a liquid-phase-type intramolecular proton transfer in bacteriorhodopsin. FEBS Lett. 398:333-336.
33. Balashov, S. P., M. Lu, E. S. Imasheva, R. Govindjee, T. G. Ebrey, B. Othersen, Y. M. Chen, R. K. Crouch, and D. R. Menick. 1999. The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH. Biochemistry. 38:2026-2039.
34. Pettei, M. J., A. P. Yudd, K. Nakanishi, R. Henselman, and W. Stoeckenius. 1977. Identification of retinal isomers isolated from bacteriorhodopsin. Biochemistry. 16:1955-1959.
35. Scherrer, P., M. K. Mathew, W. Sperling, and W. Stoeckenius. 1989. Retinal isomer ratio in dark-adapted purple membrane and bacteriorhodopsin monomers. Biochemistry. 28:829-834.
36. Maeda, A. 1995. Application of FTIR spectroscopy to the structural study on the function of bacteriorhodopsin. Isr. J. Chem. 35:387-400.
37. Bagley, K., G. Dollinger, L. Eisenstein, A. K. Singh, and L. Zimanyi. 1982. Fourier transform infrared difference spectroscopy of bacteriorhodopsin and its photoproducts. Proc. Natl. Acad. Sci. USA. 79:4972-4976.
38. Zscherp, C., and J. Heberle. 1997. Infrared difference spectra of the intermediates L, M, N, and O of the bacteriorhodopsin photoreaction obtained by time-resolved attenuated total reflection spectroscopy. J. Phys. Chem. B. 101:10542-10547.
39. Hessling, B., G. Souvignier, and K. Gerwert. 1993. A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates. Biophys. J. 65:1929-1941.
40. Braiman, M. S., O. Bousche, and K. J. Rothschild. 1991. Protein dynamics in the bacteriorhodopsin photocycle: submillisecond Fourier transform infrared spectra of the L, M, and N photointermediates. Proc. Natl. Acad. Sci. USA. 88:2388-2392.
41. Maeda, A., J. Sasaki, Y. Shichida, T. Yoshizawa, M. Chang, B. Ni, R. Needleman, and J. K. Lanyi. 1992. Structures of aspartic acid-96 in the L and N intermediates of bacteriorhodopsin: analysis by Fourier transform infrared spectroscopy. Biochemistry. 31:4684-4690.
42. Gerwert, K., B. Hess, J. Soppa, and D. Oesterhelt. 1989. Role of aspartate-96 in proton translocation by bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 86:4943-4947.
43. Braiman, M. S., T. Mogi, T. Marti, L. J. Stern, H. G. Khorana, and K. J. Rothschild. 1988. Vibrational spectroscopy of bacteriorhodopsin mutants: light-driven proton transport involves protonation changes of aspartic acid residues 85, 96, and 212. Biochemistry. 27:8516-8520.
44. Hutson, M. S., U. Alexiev, S. V. Shilov, K. J. Wise, and M. S. Braiman. 2000. Evidence for a perturbation of arginine-82 in the bacteriorhodopsin photocycle from time-resolved infrared spectra. Biochemistry. 39:13189-13200.
45. Lewis, A., J. Spoonhower, R. A. Bogomolni, R. H. Lozier, and W. Stoeckenius. 1974. Tunable laser resonance Raman spectroscopy of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 71:4462-4466.
46. Takei, H., Y. Gat, Z. Rothman, A. Lewis, and M. Sheves. 1994. Active site lysine backbone undergoes conformational changes in the bacteriorhodopsin photocycle. J. Biol. Chem. 269:7387-7389.
47. Pfefferle, J. M., A. Maeda, J. Sasaki, and T. Yoshizawa. 1991. Fourier transform infrared study of the N intermediate of bacteriorhodopsin. Biochemistry. 30:6548-6556.
48. Zscherp, C., R. Schlesinger, J. Tittor, D. Oesterhelt, and J. Heberle. 1999. In situ determination of transient pKa changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy. Proc. Natl. Acad. Sci. USA. 96:5498-5503.
49. Engelhard, M., K. Gerwert, B. Hess, W. Kreutz, and F. Siebert. 1985. Light-driven protonation changes of internal aspartic acids of bacteriorhodopsin: an investigation by static and time-resolved infrared difference spectroscopy using [4-13C]aspartic acid labeled purple membrane. Biochemistry. 24:400-407.
50. Braiman, M. S., P. L. Ahl, and K. J. Rothschild. 1987. Millisecond Fourier-transform infrared difference spectra of bacteriorhodopsin's M412 photoproduct. Proc. Natl. Acad. Sci. USA. 84:5221-5225.
51. Smith, S. O., J. Lugtenburg, and R. A. Mathies. 1985. Determination of retinal chromophore structure in bacteriorhodopsin with resonance Raman spectroscopy. J. Membr. Biol. 85:95-109.
52. Althaus, T., W. Eisfeld, R. Lohrmann, and M. Stockburger. 1995. Application of Raman spectroscopy to retinal proteins. Isr. J. Chem. 35:227-251.
53. Facciotti, M. T., V. S. Cheung, D. Nguyen, S. Rouhani, and R. M. Glaeser. 2003. Crystal structure of the bromide-bound D85S mutant of bacteriorhodopsin: principles of ion pumping. Biophys. J. 85:451-458.
54. Mitsuoka, K., T. Hirai, K. Murata, A. Miyazawa, A. Kidera, Y. Kimura, and Y. Fujiyoshi. 1999. The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: implication of the charge distribution. J. Mol. Biol. 286:861-882.
55. Subramaniam, S., and R. Henderson. 2000. Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature. 406:653-657.
56. Sasaki, J., Y. Shichida, J. K. Lanyi, and A. Maeda. 1992. Protein changes associated with reprotonation of the Schiff base in the photocycle of Asp96→Asn bacteriorhodopsin. The MN intermediate with unprotonated Schiff base but N-like protein structure. J. Biol. Chem. 267:20782-20786.
57. Dencher, N. A., H. J. Sass, and G. Büldt. 2000. Water and bacteriorhodopsin: structure, dynamics, and function. Biochim. Biophys. Acta. 1460:192-203.
58. Sass, H. J., I. W. Schachowa, G. Rapp, M. H. Koch, D. Oesterhelt, N. A. Dencher, and G. Büldt. 1997. The tertiary structural changes in bacteriorhodopsin occur between M states: x-ray diffraction and Fourier transform infrared spectroscopy. EMBO J. 16:1484-1491.
59. Fitter, J., S. A. Verclas, R. E. Lechner, H. Seelert, and N. A. Dencher. 1998. Function and picosecond dynamics of bacteriorhodopsin in purple membrane at different lipidation and hydration. FEBS Lett. 433:321-325.
60. Hildebrandt, V., K. Fendler, J. Heberle, A. Hoffmann, E. Bamberg, and G. Büldt. 1993. Bacteriorhodopsin expressed in Schizosaccharomyces pombe pumps protons through the plasma membrane. Proc. Natl. Acad. Sci. USA. 90:3578-3582.
61. Dracheva, S., S. Bose, and R. W. Hendler. 1996. Chemical and functional studies on the importance of purple membrane lipids in bacteriorhodopsin photocycle behavior. FEBS Lett. 382:209-212.
62. Belrhali, H., P. Nollert, A. Royant, C. Menzel, J. P. Rosenbusch, E. M. Landau, and E. Pebay-Peyroula. 1999. Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution. Struct. Fold. Des. 7:909-917.
63. Efremov, R., R. Moukhametzianov, G. Buldt, and V. Gordeliy. 2004. Physical detwinning of hemihedrally twinned hexagonal crystals of bacteriorhodopsin. Biophys. J. 87:3608-3613.
64. Zaccai, G. 1987. Structure and hydration of purple membranes in different conditions. J. Mol. Biol. 194:569-572.
65. Lanyi, J. K. 2004. What is the real crystallographic structure of the L photointermediate of bacteriorhodopsin? Biochim. Biophys. Acta. 1658:14-22.
66. Sass, H. J., G. Büldt, R. Gessenich, D. Hehn, D. Neff, R. Schlesinger, J. Berendzen, and P. Ormos. 2000. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin. Nature. 406:649-653.
67. Kamikubo, H., and M. Kataoka. 2005. Can the low-resolution structures of photointermediates of bacteriorhodopsin explain their crystal structures? Biophys. J. 88:1925-1931.