The protonation-deprotonation kinetics of the protonated Schiff base in bicelle bacteriorhodopsin crystals

Biophysical Journal

Volumn 89, Issue 1, 2005, Pages 444-451

  Sanii, Laurie S ^a   Schill, Alex W ^a   Moran, Cristin E ^b   El Sayed, Mostafa A ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b AIR FORCE RESEARCH LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BACTERIORHODOPSIN; SCHIFF BASE; WATER;

ABSORPTION SPECTROSCOPY; ARTICLE; CRYSTAL; CRYSTAL STRUCTURE; DEPROTONATION; HYDROPHOBICITY; KINETICS; NONHUMAN; PHOTOSYNTHESIS; PKA; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTON TRANSPORT; RAMAN SPECTROMETRY; TIME RESOLVED TRANSIENT ABSORPTION SPECTROSCOPY;

EID: 23244434448     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.059675     Document Type: Article

References (60)

1. Goldschmidt, C. R., M. Ottolenghi, and R. Korenstein. 1976. On the primary quantum yields in the bacteriorhodopsin photocycle. Biophys. J. 16:839-843.M
2. Fodor, S. P., J. B. Ames, R. Gebhard, E. M. van den Berg, W. Stoeckenius, J. Lugtenburg, and R. A. Mathies. 1988. Chromophore structure in bacteriorhodopsin's N intermediate: implications for the proton-pumping mechanism. Biochemistry. 27:7097-7101.
3. Oesterhelt, D., and B. Hess. 1973. Reversible photolysis of the purple complex in the purple membrane of Halobacterium halobium. Eur. J. Biochem. 37:316-326.
4. Stoeckenius, W., and R. H. Lozier. 1974. Light energy conversion in Halobacterium-halobium. J. Supramol. Struct. 2:769-774.
5. Lozier, R. H., R. A. Bogomolni, and W. Stoeckenius. 1975. Bacteriorhodopsin, a light-driven proton pump in Halobacterium halobium. Biophys. J. 15:955-962.
6. Jan, L. Y. 1975. Isomeric configuration of the bacteriorhodopsin chromophore. Vision Res. 15:1081-1086.
7. Henderson, R. 1977. The purple membrane from Halobacterium halobium. Annu. Rev. Biophys. Bioeng. 6:87-109.
8. Stoeckenius, W., R. H. Lozier, and R. A. Bogomolni. 1979. Bacteriorhodopsin and the purple membrane of halobacteria. Biochim. Biophys. Acta. 505:215-278.
9. Michel, H., and D. Oesterhelt. 1976. Light-induced changes of the pH gradient and the membrane potential in H. halobium. FEBS Lett. 65:175-178.
10. Bakker, E. P., H. Rottenberg, and S. R. Caplan. 1976. An estimation of the light-induced electrochemical potential difference of protons across the membrane of Halobacterium halobium. Biochim. Biophys. Acta. 440:557-572.
11. Belyakova, T. N., J. Kadziauskas, V. P. Skulachev, I. A. Smirnova, L. N. Chekulaeva, and A. Jasaitis. 1975. Generation of hydrogen(1+) ion electrochemical potential and photophosphorylation in Halobacterium halobium cells. Dokl. Akad. Nauk SSSR. 223:483-486.
12. 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.
13. Braiman, M., and R. Mathies. 1982. Resonance Raman spectra of bacteriorhodopsin's primary photoproduct: evidence for a distorted 13-cis retinal chromophore. Proc. Natl. Acad. Sci. USA. 79:403-407.
14. Mathies, R. A., C. H. Brito Cruz, W. T. Pollard, and C. V. Shank. 1988. Direct observation of the femtosecond excited-state cis-trans isomerization in bacteriorhodopsin. Science. 240:777-779.
15. Pollard, W. T., C. H. Cruz, C. V. Shank, and R. A. Mathies. 1989. Direct observation of the excited-state cis-trans photoisomerization of bacteriorhodopsin: multilevel line shape theory for femtosecond dynamic hole burning and its application. J. Chem. Phys. 90:199-208.
16. Ames, J. B., and R. A. Mathies. 1990. The role of back-reactions and proton uptake during the N-O transition in bacteriorhodopsin's photocycle: a kinetic resonance Raman study. Biochemistry. 29:7181-7190.
17. 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.
18. 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.
19. Varo, G., and J. K. Lanyi. 1991. Thermodynamics and energy coupling in the bacteriorhodopsin photocycle. Biochemistry. 30:5016-5022.
20. Oesterhelt, D., and W. Stoeckenius. 1973. Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci. USA. 70:2853-2857.
21. Lanyi, J. 1993. Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim. Biophys. Acta. 1183:241-261.
22. Glaeser, R. M., J. S. Jubb, and R. Henderson. 1985. Structural comparison of native and deoxycholate-treated purple membrane. Biophys. J. 48:775-780.
23. Nuss, M. C., W. Zinth, W. Kaiser, E. Koelling, and D. Oesterhelt. 1985. Femtosecond spectroscopy of the first events of the photochemical cycle in bacteriorhodopsin. Chem. Phys. Lett. 117:1-7.
24. Lanyi, J. K. 2000. Molecular mechanism of ion transport in bacteriorhodopsin: insights from crystallographic, spectroscopic, kinetic, and mutational studies. J. Phys. Chem. B. 104:11441-11448.
25. 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.
26. 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.
27. Heberle, J., G. Buldt, 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.
28. Heyes, C. D., and M. A. El-Sayed. 2003. Proton transfer reactions in native and deionized bacteriorhodopsin upon delipidation and monomerization. Biophys. J. 85:426-434.
29. Bowie, J., and S. Farham. 2002. Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J. Mol. Biol. 316:1-6.
30. Szundi, I., and W. Stoeckenius. 1987. Effect of lipid surface charges on the purple-to-blue transition of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 84:3681-3684.
31. Pebay-Peyroula, E., R. Neutze, and E. M. Landau. 2000. Lipidic cubic phase crystallization of bacteriorhodopsin and cryotrapping of intermediates: towards resolving a photocycle. Biochim. Biophys. Acta. 1460:119-132.
32. Faham, S., D. Yang, E. Bare, S. Yohannan, J. P. Whitelegge, and J. U. Bowie. 2003. Side-chain contributions to membrane protein structure and stability. J. Mol. Biol. 335:297-305.
33. Hanamoto, J. H., P. Dupuis, and M. A. El-Sayed. 1984. On the protein (tyrosine)-chromophore (protonated Schiff base) coupling in bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 81:7083-7087.
34. Jang, D. J., and M. A. El-Sayed. 1988. Deprotonation of lipid-depleted bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 85:5918-5922.
35. Varo, G., and J. K. Lanyi. 1990. Pathways of the rise and decay of the M photointermediate(s) of bacteriorhodopsin. Biochemistry. 29:2241-2250.
36. Slifkin, M. A., and S. R. Caplan. 1975. Modulation excitation spectrophotometry of purple membrane of Halobacterium halobium. Nature. 253:56-58.
37. Hendler, R. W., Z. Dancshazy, S. Bose, R. I. Shrager, and Z. Tokaji. 1994. Influence of excitation energy on the bacteriorhodopsin photocycle. Biochemistry. 33:4604-4610.
38. Dencher, N. A., K. D. Kohl, and M. P. Heyn. 1983. Photochemical cycle and light-dark adaptation of monomeric and aggregated bacteriorhodopsin in various lipid environments. Biochemistry. 22:1323-1334.
39. Balashov, S. P., R. Govindjee, and T. G. Ebrey. 1991. Red shift of the purple membrane absorption band and the deprotonation of tyrosine residues at high pH. Origin of the parallel photocycles of transbacteriorhodopsin. Biophys. J. 60:475-490.
40. Eisfeld, W., T. Althaus, and M. Stockburger. 1995. Evidence for parallel photocycles and implications for the proton pump in bacteriorhodopsin. Biophys. Chem. 56:105-112.
41. Hendler, R. W., R. I. Shrager, and S. Bose. 2001. Theory and procedures for finding a correct kinetic model for the bacteriorhodopsin photocycle. J. Phys. Chem. B. 105:3319-3328.
42. Oka, T., N. Yagi, F. Tokunaga, and M. Kataoka. 2002. Time-resolved X-ray diffraction reveals movement of F helix of D96N bacteriorhodopsin during M-MN transition at neutral pH. Biophys. J. 82:2610-2616.
43. 2 substates of bacteriorhodopsin by the combined use of visible and infrared spectroscopy. J. Struct. Biol. 109:142-151.
44. Lanyi, J. K. 1992. Reaction cycle and thermodynamics in bacteriorhodopsin. Acta Physiol. Scand. 607:245-248.
45. Schatzler, B., N. A. Dencher, J. Tittor, D. Oesterhelt, S. Yaniv-Checover, E. Nachliel, and M. Gutman. 2003. Subsecond proton-hole propagation in bacteriorhodopsin. Biophys. J. 84:671-686.
46. Kates, M. 1973. Techniques of Lipidology: Isolation, Analysis, and Identification of Lipids. American Elsevier Publishing, New York, NY.
47. Danshina, S. V., L. A. Drachev, A. D. Kaulen, and V. P. Skulachev. 1992. The inward hydrogen ion pathway in bacteriorhodopsin: the role of M412 and P(N)560 intermediates. Photochem. Photobiol. 55:735-740.
48. Dioumaev, A. K., L. S. Brown, R. Needleman, and J. K. Lanyi. 1998. Partitioning of free energy gain between the photoisomerized retinal and the protein in bacteriorhodopsin. Biochemistry. 37:9889-9893.
49. Chon, Y.-S., J. Sasaki, H. Kandori, L. S. Brown, J. K. Lanyi, R. Needleman, and A. Maeda. 1996. Hydration of the counterion of the Schiff base in the chloride-transporting mutant of bacteriorhodopsin: FTIR and FT-Raman studies of the effects of anion binding when Asp85 is replaced with a neutral residue. Biochemistry. 35:14244-14250.
50. Brown, L. S., A. K. Dioumaev, R. Needleman, and J. K. Lanyi. 1998. Local-Access model for proton transfer in bacteriorhodopsin. Biochemistry. 37:3982-3993.
51. Druckmann, S., M. Ottolenghi, A. Pande, J. Pande, and R. H. Callender. 1982. Acid-base equilibrium of the Schiff base in bacteriorhodopsin. Biochemistry. 21:4953-4959.
52. a of the bacteriorhodopsin Schiff base by use of artificial retinal analogs. Proc. Natl. Acad. Sci. USA. 83:3262-3266.
53. a's of aspartate-85 and control of thermal isomerization and proton release in the arginine-82 to lysine mutant of bacteriorhodopsin. Biochemistry. 34:8820-8834.
54. Balashov, S. P., R. Govindjee, M. Kono, E. Imasheva, E. Lukashev, T. G. Ebrey, R. K. Crouch, D. R. Menick, and Y. Feng. 1993. Effect of the arginine-82 to alanine mutation in bacteriorhodopsin on dark adaptation, proton release, and the photochemical cycle. Biochemistry. 32:10331-10343.
55. Brown, L. S., L. Bonet, R. Needleman, and J. K. Lanyi. 1993. Estimated acid dissociation constants of the Schiff base, Asp-85, and Arg-82 during the bacteriorhodopsin photocycle. Biophys. J. 65:124-130.
56. Chronister, E. L., T. C. Corcoran, L. Song, and M. A. El-Sayed. 1986. On the molecular mechanisms of the Schiff base deprotonation during the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA. 83:8580-8584.
57. Otto, H., T. Marti, M. Holz, T. Mogi, M. Lindau, H. G. Khorana, and M. P. Heyn. 1989. Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 86:9228-9232.
58. Maeda, A., F. L. Tomson, R. B. Gennis, H. Kandori, T. G. Ebrey, and S. P. Balashov. 2000. Relocation of internal bound water in bacteriorhodopsin during the photoreaction of m at low temperatures: an FTIR study. Biochemistry. 39:10154-10162.
59. Cao, Y., G. Varo, M. Chang, B. F. Ni, R. Needleman, and J. K. Lanyi. 1991. Water is required for proton transfer from aspartate-96 to the bacteriorhodopsin Schiff base. Biochemistry. 30:10972-10979.
60. 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.