The Importance of Charge Transfer between the Retinal Chromophore and the Protein Environment in Bacteriorhodopsin: A Theoretical Analysis on Reduced and Oxidized Chromophores

Photochemistry and Photobiology

Volumn 66, Issue 4, 1997, Pages 532-540

  Sakai, K ^a,d   Vacek, G ^b   Luthi H P ^b   Nagashima, U ^c  

^a JAPAN ADVANCED INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b Centro Svizzero Di Calcolo Scientifico   (Switzerland)

^c OCHANOMIZU UNIVERSITY   (Japan)

^d Japan Institute of Science and Technology   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0001330994     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1751-1097.1997.tb03185.x     Document Type: Article

References (47)

1. Oesterhelt, D. and W. Stoeckenius (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature New Biol. 233, 149-152.
2. Racker, E. and W. Stoeckenius (1974) Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. J. Biol. Chem. 249, 662-663.
3. Rothschild, K. J., P. V. Argade, T. N. Earnest, K.-S. Huang, E. London, M.-J. Liao, H. Bayley, H. G. Khorana and J. Herzfeld (1982) The site of attachment of retinal in bacteriorhodopsin. J. Biol. Chem. 257, 8592-8595.
4. 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.
5. Smith, O. S., A. B. Myers, J. A. Pardoen, C. Winkel, P. P. J. Mulder, J. Lugtenburg and R. Mathies (1984) Determination of retinal Schiff base configuration in bacteriorhodopsin. Proc. Natl. Acad. Sci. USA 81, 2055-2059.
6. Braiman, M. and R. Mathies (1982) Resonance Raman spectra of bacteriorhodopsin's photoproduct: evidence for a distorted 13-cis retinal. Proc. Natl. Acad. Sci. USA 79, 403-407.
7. Lozier, R. H., R. A. Bogomolni and W. Stoeckenius (1975) Bacteriorhodopsin: a light driven proton pump in Halobacterium halobium. Biophys. J. 15, 955-962.
8. Nakanishi, K., V. Balogh-Nair, M. Arnaboldi, K. Tsujimoto and B. Honig (1980) An external point-charge model for bacteriorhodopsin. J. Am. Chem. Soc. 102, 7945-7947.
9. Lugtenburg, J., M. Muradin-Szweykowska, C. Heeremans, J. A. Pardoen, G. S. Harbison, J. Herzfeld, R. G. Griffin, S. O. Smith and R. A. Mathies (1986) Mechanism for the opsin shift of retinal's absorption in bacteriorhodopsin. J. Am. Chem. Soc. 108, 3104-3105.
10. Yan, B., J. L. Spudich, P. Mazur, S. Vunnam, F. Derguini and K. Nakanishi (1995) Spectral tuning in bacteriorhodopsin in the absence of counterion and coplanarization effects. J. Biol. Chem. 270, 29668-29670.
11. Irving, C. S., G. W. Byers and P. A. Leermakers (1970) Spectroscopic model for the visual pigments. Influence of microenvironmental polarizability. Biochemistry 9, 858-864.
12. Beppu, Y. and T. Kakitani (1994) Theoretical study of color control mechanism in retinal proteins. I. Role of the tryptophan residue, tyrosine residue and water molecule. Photochem. Photobiol. 59, 660-669.
13. Kakitani, H., T. Kakitani, H. Rodman and B. Honig (1985) On the mechanism of wavelength regulation in visual pigment. Photochem. Photobiol. 41, 471-479.
14. Hu, J., R. G. Griffin and J. Herzfeld (1994) Synergy in the spectral tuning of retinal pigments: complete accounting of the opsin shift in bacteriorhodopsin. Proc. Natl. Acad. Sci. USA 91, 8880-8884.
15. 15N NMR study of the low pH forms of bacteriorhodopsin. Biochemistry 29, 6873-6882.
16. Deng, H., L. Huang. R. Callender and T. Ebrey (1994) Evidence for a bound water molecule next to the retinal Schiff base in bacteriorhodopsin and rhodopsin: a resonance Raman study of the Schiff base hydrogen/deuterium exchange. Biophys. J. 66 1129-1136.
17. a of the retinal protonated Schiff base in retinal proteins. A study with model compounds. J. Am. Chem. Soc. 115, 3772-3773.
18. Nina, N., B. Roux and J. C. Smith (1995) Functional interaction in bacteriorhodopsin: a theoretical analysis of retinal hydrogen bonding with water. Biophys. J. 68, 25-39.
19. Papadopoulos, G., N. Dencher, G. Zaccai and G. Buldt (1990) Water molecules and exchangeable hydrogen ions at the active centre of bacteriorhodopsin localized by neutron diffraction. Elements of the proton pathway. J. Mol. Biol. 214, 15-19.
20. Humphrey, W., I. Logunov, K. Schulten and M. Sheves (1994) Molecular dynamics study of bacteriorhodopsin and artificial pigment. Biochemstry 33, 3668-3678.
21. Pimentel, C. G. and A. L. McClellan (1971) The Hydrogen Bond. Freeman, San Francisco.
22. Otto, H., T. Marti, M. Holz, T. Mogi, L. J. Stern, F. Engel, H. G. Khorana and M. P. Heyn (1990) Substitution of amino acids Asp-85, Asp-212 and Arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base. Proc. Natl. Acad. Sci. USA 87, 1018-1022.
23. Stewart, J. J. P. and J. Frank (1989) MOPAC ver. 6.0. Seiler Research Laboratory, U.S. Air Force Academy, Colorado Springs, CO 80840-6528, USA.
24. Vacek, G. and H. P. Lüthi (1997) Disco-Sciddle SCSC/CSCS, Zurich.
25. Andzelm, J. and E. Wimmer (1992) Density functional Gaussian-type-orbital approach to molecular geometries, vibrations, and reaction energies. J. Chem. Phys. 96, 1280-1303.
26. ZINDO 95.0/3.0.0 (1995) BIOSYM/MSI. San Diego, CA.
27. Blatz, P. E., J. H. Mohler and H. V. Navangul (1972) Anion-induced wavelength regulation of absorption maxima of Schiff base of retinal. Biochemistry 11, 848-855.
28. Fodor, S. P. A., J. B. Ames, R. Gebhard, E. M. 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.
29. Zhou, F., A. Windemuth and K. Schulten (1993) Molecular dynamics study of the proton pump cycle of bacteriorhodopsin. Biochemistry 32, 2291-2306.
30. Maeda, A., J. Sasaki, Y. Yamazaki, R. Needleman and J. K. Lanyi (1994) Interaction of aspartate-85 with a water molecule and the protonated Schiff base in the L intermediate of bacteriorhodopsin: a Fourier-transform infrared spectroscopic study. Biochemistry 33, 1713-1717.
31. Song, L., M. A. El-Sayed and J. K. Lanyi (1993) Protein catalysis of the retinal subpicosecound photoisomerization in primary process of bacteriorhodopsin photosynthesis. Science 261, 891-894.
32. Nagaoka, S. and U. Nagashima (1990) Effects of nodal plane of wave function upon photochemical reactions of organic molecules. J. Phys. Chem. 94, 1425-1431.
33. Nagaoka, S. and U. Nagashima (1991) Effects of nodal plane of wave function upon photochemical reactions of organic molecules. 2. J. Phys. Chem. 95, 4006-4008.
34. Stern, L. J. and H. G. Khorana (1989) Structure-function studies on bacteriorhodopsin. J. Biol. Chem. 264, 14192-14196.
35. Mogi, T., L. J. Stern, T. Marti, B. H. Chao and H. G. Khorana (1988) Aspartic acid substitutions affect proton translocation by bacteriorhodopsin. Proc. Natl. Acad. Sci. USA 85, 4148-4152.
36. Mathies, R. A., S. W. Lin, J. B. Ames and W. T. Pollard (1991) From femtoseconds to biology: mechanism of bacteriorhodopsin's light-driven proton pump. Annu. Rev. Biophys. Biophys. Chem. 20, 491-518.
37. Grigorieff, N., T. A. Ceska, K. H. Downing, J. M. Balwin and R. Henderson (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259, 393-421.
38. Aton, B., A. G. Doukas, R. H. Callender, B. Becher and T. G. Ebrey (1977) Resonance Raman studies of purple membrane. Biochemistry 16, 2995-2999.
39. van den Berg, R., D.-J. Jang, H. C. Bitting and M. A. El-Sayed (1990) Subpicosecond resonance Raman spectra of the early intermediates in the photocycle of bacteriorhodopsin. Biophys J. 58, 135-141.
40. Callender, R. H., A. Doukas, R. Crouch and K. Nakanishi (1976) Molecular flow resonance Raman effect from retinal and rhodopsin. Biochemistry 15, 1621-1629.
41. Maeda, A. T. Ogurusu, T. Yoshizawa and T. Kitagawa (1985) Resonance Raman study on binding of chloride to the chromophore of halorhodopsin. Biochemistry 24, 2517-2521.
42. Rath, P., T. Marti, S. Sonar, H. G. Khorana and K. J. Rothschild (1993) Hydrogen bonding interaction with the Schiff base of bacteriorhodopsin. J. Biol. Chem. 268, 17742-17749.
43. Rousso, I., I. Brodsky, A. Lewis and M. Sheves (1995) The role of water in retinal complexation to bacterio-opsin. J. Biol. Chem. 270, 13860-13868.
44. Marti, T., H. Otto, S. J. Rosselet, M. P. Heyn and G. Khorana (1992) Anion binding to the Schiff base of the bacteriorhodopsin mutants Asp-85 Asn/Asp-212 Asn and Arg-82 Gln/Asp-85 Asn/Asp-212 Asn. J. Biol. Chem. 267, 16922-16927.
45. Stuart, J. A., B. W. Vought, C. F. Zhang and R. R. Birge (1995) The active site of bacteriorhodopsin. Two-photon spectroscopic evidence for a positively charged chromophore binding site mediated by calcium. Biospectroscopy 1, 9-28.
46. Birge, R. R., D. S. K. Govender, K. C. Izgi and E. H. L. Tan (1996) Role of calcium in the proton pump of bacteriorhodopsin. Microwave evidence for a cation-gated mechanism. J. Phys. Chem. 100, 9990-10004.
47. Mitani, T. and T. Inabe (1993) Spectroscopy of new materials. In Advances in Spectroscopy, Vol. 22 (Edited by R.J.H. Clark and R.E. Hester), pp. 291-331. John Wiley & Sons, Chichester.