Molecular dynamics study of the nature and origin of retinal’s twisted structure in bacteriorhodopsin

Biophysical Journal

Volumn 78, Issue 2, 2000, Pages 683-693

  Tajkhorshid, Emadeddin ^a,b   Baudry, Jérôme ^a   Schulten, Klaus ^a   Suhai, Saándor ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; RETINAL;

AMINO ACID COMPOSITION; ARTICLE; CONTROLLED STUDY; HALOBACTERIUM SALINARUM; HYDROGEN BOND; ISOMERISM; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN CONFORMATION;

HALOBACTERIUM SALINARUM;

EID: 0034128699     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76626-4     Document Type: Article

References (74)

1. 13C-NMR studies of model compounds for bacteriorhodopsin: facts affecting the retinal chromophore chemical shifts and absorption maximum. J. Am. Chem. Soc. 114:2400-2411.
2. a of the bacteriorhodopsin protonated Schiff base. A study with model compounds. Biochemistry. 25:5249-5258.
3. a of aspartate-85 and control of thermal isomerization and proton release in the arginine-82 to lysine mutant of bacteriorhodopsin. Biochemistry. 34: 8820-8834.
4. Balashov, S. P., E. S. Imasheva, R. Govindjee, and T. G. Ebray. 1996. Titration of aspartate-82 in bacteriorhodopsin: what it says about chromophore isomerization and proton release. Biophys. J. 70:473-481.
5. Baudry, J., S. Crouzy, B. Roux, and J. C. Smith. 1997. Quantum chemical and free energy simulation analysis of retinal conformational energetics. J. Chem. Inf. Comput. Sci.37:1018-1024.
6. Baudry, J., S. Crouzy, B. Roux, and J. C. Smith. 1999. Simulation analysis of the retinal conformational equilibrium in dark-adapted bacteriorhodopsin. Biophys. J. 76:1909-1917.
7. Ben-Nun, M., F. Molnar, H. Lu, J. C. Phillips, T. J. Martiánez, and K. Schulten. 1998. Quantum dynamics of retinal's femtosecond photoisomerization in bacteriorhodopsin. Chemical Reaction Theory. Special issue of the Faraday Discuss. 110:447-462.
8. Bifone, A., H. J. M. de Groot, and F. Buda. 1996. Ab initio molecular dynamics of retinals. Chem. Phys. Lett. 248:165-172.
9. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comp. Chem. 4:187-217.
10. 15N shift anisotropy. Biochemistry. 28:3346-3353.
11. Delaney, J. K., P. Schmidt, G. H. Atkinson, and S. Subramaniam. 1997. Evidence for a long-lived 13-cis-containing intermediate in the photocycle of the Leu93 → Ala bacteriorhodopsin mutant. J. Phys. Chem. B. 101:5619-5621.
12. de Lera, A. R., B. Iglesias, J. Rodriguez, R. Alvarez, S. Lopez, X. Villanueva, and E. J. Padros. 1995. Experimental and theoretical analysis of the steric tolerance of the binding site of bacterioopsin with the use of side chain methyl shifted retinal analogs. J. Am. Chem. Soc. 117:8220-8231.
13. Druckman, 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.
14. DuPuis, P., I. Harosi, C. Sandorfy, J. Leclerq, and D. Vocelle. 1980. First step in vision: proton transfer or isomerization? Rev. Can. Biol. 39: 247-258.
15. Essen, L. O., R. Siegert, W. D. Lehmann, 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.
16. Ferrand, M., G. Zaccai, M. Nina, J. C. Smith, C. Etchebest, and B. Roux. 1993. Structure and dynamics of bacteriorhodopsin: comparison of simulation and experiment. FEBS. Lett. 327:256-260.
17. Frisch, M. J., G. W. Trucks, H. B. Schlegel, P. M. W. Gill, B. G. Johnson. M. A. Robb, J. R. Cheeseman, T. Keith, G. A. Peterson, J. V. Oritz, J. B. Foresman, J. Cioslowski, B. B. Stefanov, A. Nanayakkara, M. Challacombe, C. Y. Peng, P. Y. Ayala, W. Chen, M. W. Wong, J. L. Andres, E. S. Replogle, R. Gomperts, R. L. Martin, D. J. Fox, J. S. Binkley, D. J. Defrees, J. Baker, J. P. Stewart, M. Head-Gordon, C. Gonzales, and J. A. Pople. 1985. Gaussian 94, Revision C.3. Gaussian Inc., Pittsburgh. PA.
18. a of the retinal protonated Schiff base in retinal proteins. J. Am. Chem. Soc. 115:3772-3773.
19. Grigorieff, N. T., T. A. Cesta, K. H. Downing, J. M. Baldwinn, and R. Henderson. 1996. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:393-421.
20. Hamanaka, T., T. Mitsui, T. Ashida, and M. Kakudo. 1972. The crystal structure of all-trans retinal. Acta Crystallogr. B. 28:214.
21. 13C-NMR detection of a perturbed 6-s-trans chromophore in bacteriorhodopsin. Biochemistry. 24:6955-6962.
22. Henderson, R. 1977. The purple membrane from Halobacterium halobium. Annu. Rev. Biophys. Bioeng. 6:87-109.
23. Hermone, A., and K. Kuczera. 1998. Free-energy simulations of the retinal cis→trans isomerization in bacteriorhodopsin. Biochemistry. 37: 2843-2853.
24. Hildebrandt, P., and M. Stockburger. 1984. Role of water in bacteriorhodopsin's chromophore: resonance Raman study. Biochemistry. 23: 5539-5548.
25. Humphrey, W., D. Xu, M. Sheves, and K. Schulten. 1995. Molecular dynamics study of the early intermediates in the bacteriorhodopsin photocycle. J. Phys. Chem. 99:14549-14560.
26. Krebs, M. P., and H. J. Khorana. 1993. Mechanism of light-dependent proton translocation by bacteriorhodopsin. J. Bacteriol. 175:1555-1560.
27. Lanyi, J. K. 1993. Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim. Biophys. Acta Bioenerg. 1183:241-261.
28. Logunov, S. L., M. A. El-Sayed, and J. K. Lanyi. 1996a. Replacement effects of neutral amino acid residues of different molecular volumes in the retinal binding cavity of bacteriorhodopsin on the dynamics of its primary process. Biophys. J. 70:2875-2881.
29. Logunov, S. L., M. A. El-Sayed, L. Song, and J. K. Lanyi. 1996b. Photoisomerization quantum yield and apparent energy content of the K intermediate in the photocycles of bacteriorhodopsin, its mutants D85N, R82Q, and D212N, and deionized blue bacteriorhodopsin. J. Phys. Chem. 100:2391-2398.
30. 548) of bacteriorhodopsin and its photocycle. Biophys. J. 68:1270-1282.
31. Logunov, I., and K. Schulten. 1996. Quantum chemistry: molecular dynamics study of the dark-adaptation process in bacteriorhodopsin. J. Am. Chem. Soc. 118:9727-9735.
32. Lueke, H., H. T. Richter, and J. K. Lanyi. 1998. Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. Science. 280: 1934-1937.
33. Lueke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 Angstroms resolution. J. Mol. Biol. 291:899-911.
34. MacKerell et al., 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
35. Mathies, R. A., S. W. Lin, J. B. Ames, and W. T. Pollard. 1991. From femtosecond to biology: mechanism of bacteriorhodopsin light-driven proton pump. Annu. Rev. Biophys. Biophys. Chem. 20:491-518.
36. Nakayama, T. A., W. Zhang, A. Cowan, and M. Kung. 1998. Mutagenesis studies of human red opsin: Trp-281 is essential for proper folding and protein retinal interactions. Biochemistry. 37:17487-17494.
37. Nina, M., B. Roux, and J. C. Smith. 1993. Ab initio quantum chemical analysis of retinal Schiff base hydration in bacteriorhodopsin. J. Mol. Struct. (THEOCHEM). 286:231-245.
38. Nina, M., B. Roux, and J. C. Smith. 1995. Functional interactions in bacteriorhodopsin: a theoretical analysis of retinal hydrogen bonding with water. Biophys. J. 68:25-39.
39. Oesterhelt, D. 1976. Bacteriorhodopsin as an example of a light-driven proton pump. Angew. Chem., Int. Ed. Engl. 15:17-24.
40. Oesterhelt, D., and W. Stoeckenius. 1973. Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci. USA. 70:2853-2857.
41. Oesterhelt, D., J. Tittor, and E. Bamberg. 1992. A unifying concept for ion translocation in retinal proteins. J. Bioenerg. Biomembr. 24:181-191.
42. Orlandi, G., and K. Schulten. 1979. Coupling of stereochemistry and proton donor-acceptor properties of a Schiff base: a model of a light-driven proton pump. Chem. Phys. Lett. 64:370-374.
43. Paizs, B., E. Tajkhorshid, and S. Suhai. 1999. Electronic effects on the ground state rotational barrier of the chromophore in bacteriorhodopsin: a molecular orbital study. Phys. Chem. B. 103:5388-5395.
44. 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 phase. Science. 277:1676-1691.
45. Rotschild, K. J. 1992. FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model. J. Bioenerg. Biomembr. 24:147-167.
46. a of the protonated Schiff base and aspartic-85 in the bacteriorhodopsin binding site is controlled by a specific geometry between the two residues. Biochemistry. 34:12059-12065.
47. Roux, B., M. Nina, R. Pomes, and J. C. Smith. 1996. Thermodynamic stability of water molecules in the bacteriorhodopsin proton channel: a molecular dynamics free-energy perturbation study. Biophys. J. 71: 670-681.
48. Santarsiero, B. D., M. N. G. James, M. Mahendran, and R. F. Childs. 1990. Crystal structure of N-methyl-N-phenylretinal iminium perchlorate: a structural model for the bacteriorhodopsin chromophore. J. Am. Chem. Soc. 112:9416-9418.
49. Scheiner, S., and X. Duan. 1991. Effect of intermolecular orientation upon proton transfer within a polarizable medium. Biophys. J. 60:874-883.
50. Scheiner, S., and E. A. Hillenbrand. 1985. Modification of pK values caused by change in H-bond geometry. Proc. Natl. Acad. Sci. USA. 82:2741-2745.
51. Schreckenbach, T., B. Walckhoff, and D. Oesterhelt. 1978. Specificity of the retinal binding site of bacteriorhodopsin: chemical and stereochemical requirements for the binding of retinol and retinal. Biochemistry. 17:5353-5359.
52. Schulten, K., W. Humphrey, I. Logunov, M. Sheves, and D. Xu. 1995. Molecular dynamics studies of bacteriorhodopsin's photocycles. Isr. J. Chem. 35:447-464.
53. a of the bacteriorhodopsin Schiff base by use of artificial retinal analogues. Proc. Natl. Acad. Sci. USA. 83:3262-3266.
54. Sheves, M., and T. Baasov. 1984. Factors affecting the rate of thermal isomerization of 13-cis-bacteriorhodopsin to all-trans. J. Am. Chem. Soc. 106:6840-6841.
55. Simmons, C. J., R. S. H. Liu, M. Denny, and K. Seff. 1981. The crystal structure of 13-cis-retinal. The molecular structures of its 6-s-cis and 6-s-trans conformers. Acta Crystallogr. B. 37:2197.
56. Song, L., M. A. El-Sayed, and J. K. Lanyi. 1993. Protein catalysis of the retinal subpicosecond photoisomerization in the primary process of bacteriorhodopsin photosynthesis. Science. 261:891-894.
57. Song, L., M. A. El-Sayed, and J. K. Lanyi. 1996. Effect of changing the position and orientation of Asp85 relative to the protonated Schiff base within the retinal cavity on the rate of photoisomerization in bacteriorhodopsin. J. Phys. Chem. 100:10479-10481.
58. Tajkhorshid, E., B. Paizs, and S. Suhai. 1997. Conformational effects on the proton affinity of the Schiff base in bacteriorhodopsin: a density functional study. J. Phys. Chem. B. 101:8021-8028.
59. a control of the retinal Schiff base: a density functional study. J. Phys. Chem. B. 103:4518-4527.
60. Tajkhorshid, E., and S. Suhai. 1999a. Dielectric effects due to the environment on the structure and proton affinity of retinal Schiff base models. Chem. Phys. Lett. 299:457-464.
61. a of the retinal Schiff base and on the stabilization of the ion pair in bacteriorhodopsin. J. Mol. Struct. (THEOCHEM) in press.
62. Tajkhorshid, E., and S. Suhai. 1999c. The effect of the protein environment on the structure and charge distribution of the retinal Schiff base in bacteriorhodopsin. Theoret. Chem. Acc. 101:180-185.
63. Tajkhorshid, E., and S. Suhai. 1999d. Influence of the methyl groups on the structure, charge distribution and proton affinity of the retinal Schiff base. J. Phys. Chem. B. 103:5581-5590.
64. Tavan, P., K. Schulten, and D. Oesterhelt. 1985. The effect of protonation and electrical interactions on the stereochemistry of retinal Schiff bases. Biophys. J. 47:415-430.
65. Volkov, V., Y. P. Svirko, V. F. Kamalov, L. Song, and M. A. El-Sayed. 1997. Optical rotation of the second harmonic radiation from retinal in bacteriorhodopsin monomers in Langmuir-Blodgett film: evidence for nonplanar retinal structure. Biophys. J. 73:3164-3170.
66. Warshel, A. 1979. Conversion of light energy to electrostatic energy in the proton pump of Halobacterium halobium. Photochem. Photobiol. 30: 285-290.
67. Warshel, A. 1986. Correlation between the structure and efficiency of light-induced proton pumps. Methods Enzymol. 127:578-587.
68. Warshel, A., Z. T. Chu, and J. K. Hwang. 1991. The dynamics of the primary event in rhodopsins revisited. Chem. Phys. 158:303-314.
69. Warshel, A., and M. J. Levin. 1976. Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J. Mol. Biol. 103:227-249.
70. Weidlich, O., B. Schalt, N. Friedman, M. Sheves, J. K. Lanyi, L. S. Brown, and F. Siebert. 1996. Steric interaction between the 9-methyl group of the retinal and tryptophan-182 controls 13-cis to all-trans reisomerization and proton uptake in the bacteriorhodopsin photocycle. Biochemistry. 35:10807-10814.
71. Weidlich, O., and F. Siebert. 1993. Time-resolved step-scan FTIR investigations of the transition from K to L in the bacteriorhodopsin photocycle; identification of chromophore twists by assigning hydrogen-out-of-plane (hoop) bending vibrations. Appl. Spectrosc. 47:1394-1400.
72. Wu, S., and M. A. El-Sayed. 1991. CD spectrum of bacteriorhodopsin: best evidence against exciton model. Biophys. J. 60:190-197.
73. Xu, D., C. Martin, and K. Schulten. 1996. Molecular dynamics study of early picosecond events in the bacteriorhodopsin photocycle: dielectric response, vibrational cooling, and the J, K intermediates. Biophys. J. 70:453-460.
74. Xu, D., M. Sheves, and K. Schulten. 1995. Molecular dynamics study of the M412 intermediate of bacteriorhodopsin. Biophys. J. 69:2745-2760.