Physical origin of the opsin shift of bacteriorhodopsin. Comprehensive analysis based on medium effect theory of absorption spectra

Journal of the American Chemical Society

Volumn 120, Issue 18, 1998, Pages 4459-4470

  Houjou, Hirohiko ^a   Inoue, Yoshio ^a   Sakurai, Minoru ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; RETINAL;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MATHEMATICAL ANALYSIS; PROTEIN CONFORMATION; STRUCTURE ANALYSIS;

EID: 0032513712     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja973941t     Document Type: Article

References (72)

1. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
2. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
3. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
4. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
5. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
6. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
7. See for reviews: (a) Birge, R. R. Annu. Rev. Phys. Chem. 1990, 41, 683. (b) Lanyi, J. K. Biochim. Biophys. Acta 1993, 1183, 241. Nathans, J. Biochemistry 1992, 31, 4923. Khorana, H. G. Ann. N. Y. Acad. Sci. 1986,471, 272. (e) Mathies, R. A.; Lin, S. W.; Ames, J. B.; Pollard, W. T. Annu. Rev. Biophys. Biophys. Chem. 1991, 20, 491. (f) Nakanishi, K. Pure Appl. Chem. 1991, 63, 161. (g) Ottolenghi, M.; Sheves, M. J. Menbr. Biol. 1989, 112, 193.
8. Lozier, R.; Bogomolni, R. A.; Stoeckenius, W. Biophys. J. 1975, 15, 955.
9. van der Steen, R.; Biesheuvel, P. L.; Mathies, M. A.; Lugtenburg, J. J. Am. Chem. Soc. 1986, 108, 6410.
10. Harbison, G. S.; Smith, S. O.; Pardoen, J. A.; Courtin, J. M. L.; Lugtenburg, J.; Herzfeld, J.; Mathies, R. A.; Griffin, R. G. Biochemistry 1985, 24, 6955.
11. Harbison, G. S.; Mulder, P. P. J.; Pardoen, H.; Lugtenburg, J.; Herzfeld, J.; Griffin, R. G. J. Am. Chem. Soc. 1985, 107, 4809.
12. Wada, M.; Sakurai, M.; Inoue, Y.; Tamura, Y.; Watanabe, Y. J. Am. Chem. Soc. 1994, 116, 1537.
13. Bassov, T.; Sheves, M. J. Am. Chem. Soc. 1985, 107, 7524.
14. (a) Blatz, P. E.; Johnson, R. H.; Mohler, J. H.; AI-Dilaimi, S. K.; Dewhurst, S.; Erickson, J. O. Photochem. Photobiol 1971, 13, 237.
15. (b) Blatz, P. E.; Mohler, J. H.; Navanglu, H. V. Biochemistry 1972, 11, 848.
16. Blatz, P. E.; Mohler, J. H. Biochemistry 1972, 11, 3240.
17. Blatz, P. E.; Mohler, J. H. Biochemistry 1975, 14, 2340.
18. (a) Arnaboldi, M.; Motto, M. G.; Tsujimoto, K.; Balogh-Nair, V.; Nakanishi, K. J. Am. Chem. Soc. 1979, 101, 7082.
19. (b) Honig, B.; Dinur, U.; Nakanishi, K.; Balogh-Nair, V.; Gawinowics, M. A.; Arnaboldi, M.; Motto, M. G. J. Am. Chem. Soc. 1979, 101, 7084.
20. Sheves, M.; Nakanishi, K.; Honig, B. J. Am. Chem. Soc. 1979, 101, 7086.
21. (a) Irving. C. S.; Byers, G. W.; Leermakers, P. A. J. Am. Chem. Soc. 1969, 91, 2141.
22. (b) Irving, C. S.; Byers, G. W.; Leermakers, P. A. Biochemistry 1970, 9, 858.
23. Honig, B.; Greenberg, A. D.; Dinur, U.; Ebrey, T. G. Biochemistry 1976, 15, 4593.
24. (a) Nakanishi, K.; Balogh-Nair, V.; Arnaboldi, M.; Tsujimoto, K.; Honig, B. J. Am. Chem. Soc. 1980, 102, 7945.
25. (b) Motto, M. G.; Sheves, M.; Tsujimoto, K.; Balogh-Nair, V.; Nakanishi, K. J. Am. Chem. Soc. 1980, 102, 7947.
26. Mao, B.; Govindjee, R.; Ebrey, T.; Arnaboldi, M.; Balogh-Nair, V.; Nakanishi, K Biochemistry 1981, 20, 428.
27. Spudich, J. L.; McCain, D. A.; Nakanishi, K.; Okabe, M.; Shimizu, N.; Rodman, H.; Honig, B.; Bogomolni, A. Biophys. J. 1986, 49, 479.
28. Koutalos, Y.; Ebrey, T. G.; Tsuda, M.; Odashima, K.; Lien, T.; Park, M. H.; Shimizu, N.; Derguini, F.; Nakanishi, K.; Gilson, H. R.; Honig, B. Biochemistry 1989, 28, 2732.
29. Lugtenburg, J.; Muradin-Szweykowska, M.; Heeremans, C.; Pardoen, J. A.; Griffin, R. G.; Smith, S. O.; Mathies, R. A. J. Am. Chem. Soc. 1986, 108, 3104.
30. Sheves, M.; Nakanishi, K. J. Am. Chem. Soc. 1983, 105, 4033.
31. Derguini, F.; Caldwell, C. G.; Motto, M. G.; Balogh-Nair, v.; Nakanishi, K. J. Am. Chem. Soc. 1983, 105, 646.
32. Gat, Y.; Sheves, M. Photochem. Photobiol. 1994, 59, 371.
33. Grigorieff, T.; Ceska, K.; Downing, K. H.; Baldwin, J. M.; Henderson, R. J. Mol. Biol. 1996, 259, 393.
34. Mogi, T.; Stern, L. J.; Marti, T.; Chao, B. H.; Khorana, H. G. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 4148.
35. Birge, R. R.; Murray. L. P.; Pierce, B. M.; Akita, H.; Balogh-Nair, V.; Findsen, L. A.; Nakanishi, K. Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 4117.
36. Mathies, R.; Stryer, L. Proc. Natl. Acad. Sci. U.S.A. 1976, 73, 2169.
37. Suzuki, T.; Kito, Y. Photochem. Photobiol. 1972, 15, 275.
38. (a) Kliger, D. S.; Milder, S. J.; Dratz, E. A. Photochem. Photobiol. 1977, 25, 277.
39. (b) Milder, S. J.; Kliger, D. S. Photochem. Photobiol. 1977, 25, 287.
40. Yan, B.; Spudich, J. L.; Mazur, P.; Vunnam, S.; Dergini, F.; Nakanishi, K. J. Biol. Chem. 1995, 270, 29668.
41. Hu, J.; Griffin, R. G.; Herzfeld, J. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 8880.
42. For example, (a) Muthukumar, M.; WeimAnn, L. J. Chem. Phys. Lett. 1978, 53, 436. (b) Kakitani, H.; Kakitani, T.; Rodman, H.; Honig, B. Photochem. Photobiol. 1985, 41, 471. Beppu, Y.; Kakitani, T. Photochem. Photobiol. 1994, 59, 660. Tallent, J. R.; Hyde, E. W.; Findsen, L. A.; Fox, G. C.; Birge, R. R. J. Am. Chem. Soc. 1992, 114, 1581. (d) Gilson, H. S. R.; Honig, B. H.; J. Am. Chem. Soc. 1988, 110, 1943.
43. For example, (a) Muthukumar, M.; WeimAnn, L. J. Chem. Phys. Lett. 1978, 53, 436. (b) Kakitani, H.; Kakitani, T.; Rodman, H.; Honig, B. Photochem. Photobiol. 1985, 41, 471. Beppu, Y.; Kakitani, T. Photochem. Photobiol. 1994, 59, 660. Tallent, J. R.; Hyde, E. W.; Findsen, L. A.; Fox, G. C.; Birge, R. R. J. Am. Chem. Soc. 1992, 114, 1581. (d) Gilson, H. S. R.; Honig, B. H.; J. Am. Chem. Soc. 1988, 110, 1943.
44. For example, (a) Muthukumar, M.; WeimAnn, L. J. Chem. Phys. Lett. 1978, 53, 436. (b) Kakitani, H.; Kakitani, T.; Rodman, H.; Honig, B. Photochem. Photobiol. 1985, 41, 471. Beppu, Y.; Kakitani, T. Photochem. Photobiol. 1994, 59, 660. Tallent, J. R.; Hyde, E. W.; Findsen, L. A.; Fox, G. C.; Birge, R. R. J. Am. Chem. Soc. 1992, 114, 1581. (d) Gilson, H. S. R.; Honig, B. H.; J. Am. Chem. Soc. 1988, 110, 1943.
45. For example, (a) Muthukumar, M.; WeimAnn, L. J. Chem. Phys. Lett. 1978, 53, 436. (b) Kakitani, H.; Kakitani, T.; Rodman, H.; Honig, B. Photochem. Photobiol. 1985, 41, 471. Beppu, Y.; Kakitani, T. Photochem. Photobiol. 1994, 59, 660. Tallent, J. R.; Hyde, E. W.; Findsen, L. A.; Fox, G. C.; Birge, R. R. J. Am. Chem. Soc. 1992, 114, 1581. (d) Gilson, H. S. R.; Honig, B. H.; J. Am. Chem. Soc. 1988, 110, 1943.
46. For example, (a) Muthukumar, M.; WeimAnn, L. J. Chem. Phys. Lett. 1978, 53, 436. (b) Kakitani, H.; Kakitani, T.; Rodman, H.; Honig, B. Photochem. Photobiol. 1985, 41, 471. Beppu, Y.; Kakitani, T. Photochem. Photobiol. 1994, 59, 660. Tallent, J. R.; Hyde, E. W.; Findsen, L. A.; Fox, G. C.; Birge, R. R. J. Am. Chem. Soc. 1992, 114, 1581. Gilson, H. S. R.; Honig, B. H.; J. Am. Chem. Soc. 1988, 110, 1943.
47. Han, M.; DeDecker, B. S.; Smith, S. O. Biophys. J. 1993, 65, 899.
48. (a) Han, M.; Smith, S. O. Biochemistry 1995, 34, 1425.
49. (b) Han, M.; Smith, S. O. Biophys. Chem. 1995, 56, 23.
50. See for review: Tomasi, J.; Perisico, M. Chem. Rev. 1994, 94, 2027.
51. (a) Raudino, A.; Zuccarello, F.; Buemi, G. J. Chem. Soc., Faraday Trans. 2 1983, 79, 1759.
52. (b) Zuccarello, F.; Raudino, A.; Buemi, G. J. Mol. Struct. (THEOCHEM) 1984, 107, 215.
53. Houjou, H.; Sakurai, M.; Inoue, Y. J. Chem. Phys. 1997,107, 5652.
54. (a) Hoshi, H.; Sakurai, M.; Inoue, Y.; Chûjô, R. J. Chem. Phys. 1987, 87, 1107.
55. (b) Hoshi, H.; Sakurai, M.; Inoue, Y.; Chûjô, R. J. Mol. Struct. (THEOCHEM) 1988, 180, 267.
56. Stewart, J. J. P. J. Comput. Chem. 1989, 10, 209.
57. Stewart, J. J. P.; Frank, J. MOPAC Ver6.0l; Seilar Research Laboratory, U. S. Air Force Academy: Colorado Springs, CO 80840-6528, 1989.
58. Pearlman, D. A.; Case, D. A.; Caldwel, J. W.; Ross, W. S.; Cheatham III, T. E.; Ferguson, D. M.; Seibel, G. L.; ChandraSingh, U.; Weiner, P. K.; Kollman, P. A. AMBER ver. 4.1; University of Calfornia, San Francisco, 1995.
59. (a) Krough-Jespersen, K.; Ratner, M. J. Chem. Phys. 1976. 65, 1305. We adopted the β° value of -30 eV for oxygen according to
60. (b) Faure, P. J. J.; Chalvet, O.; Jaffe, H. H. J. Phys. Chem. 1981,85, 473.
61. RajzmAnn, M.; Francois, P. QCPE 11 1979, 382.
62. Furuki, T.; Umeda, A.; Sakurai, M.; Inoue, Y.; Chûjô, R.; Harata, K. J. Comput. Chem. 1994, 15, 90.
63. Inoue, Y.; Tokitô, Y.; Chûjô, R.; Miyoshi, Y. J. Am. Chem. Soc. 1977, 99, 5592.
64. Lange's Handbook of Chemistry, 11th ed.; Dean, J. A. Ed.; McGraw-Hill: New York, 1973.
65. The volume of the binding pocket defined in the text was calculated as follows: (i) calculate the surface area (S) of the interlocking spheres whose radii are R = 5 Å; (ii) calculate the surface area (s) of the interlocking spheres whose radii are van der Waals radii (r) of each atom; (iii) the volume of the region enclosed by these two interlocking spheres is estimated by (1/3)(RS - rs).
66. Bashold, B.; Gerwert, K. J. Mol. Biol. 1992, 224, 473.
67. a values of the ionizable residues in bR were consistently reproduced on the assumption that the dielectric constant of the protein interior was 4.0.
68. Mogi, T.; Marti, T.; Khorana, H. G. J. Biol. Chem. 1989, 264, 14197.
69. Hisatomi, O.; Kayada, S.; Aoki, Y,; Iwasa, T.; Tokunaga, F. Vision Res. 1994, 34, 3097.
70. Nakayama, T.; Khorana, H. G. J. Biol. Chem. 1991, 266, 4269.
71. (a) Abola, E. E.; Bernstein, F. C.; Koetzle, T. F.; Weng, J. Protein Data Bank. In Cristallographic Databases-Information Content, Software Systems, Scientific Applications; Allen, F. H., Bergerhoff, G., Siebers, R., Eds.; Data Commission of the International Union of Crystallography: Bonn/Cambridge/Chester, 1987; pp 107-132.
72. (b) Bernstein, F. C; Koetzle, T. F.; Williams, G. J. B.; Meyer, E. F., Jr.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimonouchi, T.; Tasumi, M. The Protein Data Bank: a Computer-based Archival File for Macromolecular Structures J. Mol. Biol. 1977, 112, 535.