Nanosecond retinal structure changes in K-590 during the room temperature bacteriorhodopsin photocycle: Picosecond time-resolved coherent anti-stokes Raman spectroscopy

Biophysical Journal

Volumn 72, Issue 5, 1997, Pages 2329-2341

  Weidlich, Olaf ^a   Ujj, Laszlo ^a   Jäger, Frank ^a   Atkinson, G H ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN;

ARTICLE; CHROMATOPHORE; HALOBACTERIUM; NONHUMAN; PHOTOACTIVATION; RAMAN SPECTROMETRY; RETINA; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; VIBRATION;

HALOBACTERIUM;

EID: 0030998542     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78877-5     Document Type: Article

References (79)

1. Althaus, T., W. Eisfeld, R. Lohrmann, and M. Stockburger. 1995. Application of raman spectroscopy to retinal proteins [review]. Isr. J. Chem. 35:227-251.
2. 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.
3. Atkinson, G. H. 1990. Picosecond reaction dynamics in photosynthetic and proton pumping systems: picosecond time-resolved Raman spectroscopy of electronic and vibrationally excited states. SPIE. 1403:50-58.
4. Atkinson, G. H., T. L. Brack, D. Blanchard, and G. Rumbles. 1989. Picosecond time-resolved resonance Raman spectroscopy of the initial trans to cis isomerization in the bacteriorhodopsin photocycle. Chem. Phys. 131:1-15.
5. Atkinson, G. H., A. Popp, and L. Ujj. 1994. Picosecond-Resonance Coherent Anti-Stokes Raman Scattering in Biophysics: Power Dependence in the Bacteriorhodopsin Photocycle, Vol. 74. A. Lau, F. Siebert, and W. Werncke, editors. Springer-Verlag, Berlin. 153-157.
6. Atkinson, G. H., and L. Ujj. 1992. Picosecond Time-Resolved Resonance CARS of Bacteriorhdopsin. In Institute of Physics Conference Series, no. 126, section VIII. IOP Publishing. 599-604.
7. Birge, R. R. 1990. Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin. Biochim. Biophys. Acta. 1016:293-327.
8. Bitting, H. C., D.-J. Jang, and M. A. El-Sayed. 1990. On the multiple cycles of bacteriorhodopsin at high pH. Photochem. Photobiol. 51: 593-598.
9. Blanchard, D., D. A. Gilmore, T. L. Brack, H. Lemaire, D. Hughes, and G. H. Atkinson. 1991. Picosecond time-resolved absorption and fluorescence in the bacteriorhodopsin photocycle: vibrationally-excited species. Chem. Phys. 156:155-170.
10. Brack, T. L., and G. H. Atkinson. 1989. Picosecond time-resolved resonance raman spectrum of the K-590 intermediate in the room temperature bacteriorhodopsin photocycle. J. Mol. Struct. 289-303.
11. Brack, T. L., and G. H. Atkinson. 1991. Vibrationally excited retinal in the bacteriorhodopsin photocycle: picosecond time-resolved anti-Stokes resonance Raman scattering. J. Phys. Chem. 95:2352-2356.
12. Braiman, M. 1986. Resonance Raman methods for proton translocation in bacteriorhodopsin. Methods Enzymol. 127:587-597.
13. 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.
14. Braiman, M., and R. A. 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.
15. Braiman, M., and R. A. Mathies. 1983. Structural relaxation of the Schiff base bond in bacteriorhodopsin's primary photoproduct. Biophys. J. 41:14a.
16. Curry, B., I. Palings, A. D. Brock, J. A. Pardoen, J. Lugtenburg, and R. Mathies. 1985. Vibrational analysis of the retinal isomers. In Advances in Infrared and Raman Spectroscopy, Vol. 12. John Wiley and Sons, New York. 115-178.
17. Dáncshazy, Z., R. Govindjee, and T. G. Ebrey. 1988. Independent photocycles of the spectrally distinct forms of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 85:6358-6361.
18. Delaney, J. K., T. L. Brack, and G. H. Atkinson. 1993. Time-resolved absorption and fluorescence from the bacteriorhodopsin photocycle in the nanosecond time regime. Biophys. J. 64:1512-1519.
19. Diller, R., M. Iannone, R. A. Bogomolni, and R. M. Hochstrasser. 1991. Ultrafast infrared spectroscopy of bacteriorhodopsin. Biophys. J. 60: 286-289.
20. Diller, R., M. Iannone, B. R. Cowen, S. Maiti, R. A. Bogomolni, and R. M. Hochstrasser. 1992. Picosecond dynamics of bacteriorhodopsin, probed by time-resolved infrared spectroscopy. Biochemistry. 31:5567-5572.
21. Diller, R., S. Maiti, G. C. Walker, B. R. Cowen, R. Pippenger, R. A. Bogomolni, and R. M. Hochstrasser. 1995. Femtosecond time-resolved infrared laser study of the J-K transition of bacteriorhodopsin. Chem. Phys. Lett. 241:109-115.
22. Dobler, J., W. Zinth, W. Kaiser, and D. Oesterhelt. 1988. Excited-state reaction dynamics of bacteriorhodopsin studied by femtosecond spectroscopy. Chem. Phys. Lett. 144:215-220.
23. Doig, S. J., P. J. Reid, and R. A. Mathies. 1991. Picosecond time-resolved resonance Raman spectroscopy of bacteriorhodopsin's J, K, and KL intermediates. J. Chem. Phys. 95:6372-6379.
24. Ebrey, T. G. 1993. Light Energy Transduction in Bacteriorhodopsin. M. B. Jackson, editor. CRC Press, Boca Raton, FL. 353-387.
25. Eisfeld, W., R. Diller, C. Pusch, R. Lohrmann, and M. Stockburger. 1993. Resonance Raman and optical transient studies on the proton pump of bacteriorhodopsin reveal parallel photocycles. Biochemistry. 32: 7196-7215.
26. Fahmy, K., F. Siebert, M. F. Grossjean, and P. Tavan. 1989. Photoisomerization in bacteriorhodopsin studied by FTIR, linear dichroism and photoselection expierments combined with quantum chemical theoretical analysis. J. Mol. Struct. 214:257-288.
27. Fahmy, K., F. Siebert, and P. Tavan. 1991. Structural investigation of bacteriorhodopsin and some of its photoproducts by polarized Fourier transform infrared spectroscopic methods - difference spectroscopy and photoselection. Biophys. J. 60:989-1001.
28. Gerwert, K., and F. Siebert. 1986. Evidence for light-induced 13-cis, 14-cis isomerization in bacteriorhodopsin obtained by FTIR difference spectroscopy using isotopically labelled retinals. EMBO J. 5:805-811.
29. Grossjean, M. F., P. Tavan, and K. Schulten. 1990. Quantum chemical vibrational analysis of the chromophore of bacteriorhodopsin. J. Phys. Chem. 94:8059-8069.
30. Hage, W., M. Kim, H. Frei, and R. A. Mathies. 1996. Protein dynamics in the bacteriorhodopsin photocycle: a nanosecond step-scan FTIR investigation of the KL to L transition. J. Phys. Chem. 100:16026-16033.
31. 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.
32. 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.
33. Hsieh, C.-L., M. A. El-Sayed, M. Nicol, M. Nagumo, and J.-H. Lee. 1983. Time-resolved resonance Raman spectroscopy of the bacteriorhodopsin photocycle on the picosecond and nanosecond time scales. Photochem. Photobiol. 38:83-94.
34. Hsieh, C.-L., M. Nagumo, M. Nicol, and M. A. El-Sayed. 1981. Picosecond and nanosecond resonance Raman studies of bacteriorhodopsin. Do configurational changes of retinal occur in picoseconds? J. Phys. Chem. 85:2714-2717.
35. 14,15 retinal: picosecond time-resolved Coherent anti-Stokes Raman spectroscopy of the room temperature bacteriorhodopsin photocycle. J. Phys. Chem. 100: 12066-12075.
36. Kandori, H., K. Yoshihara, H. Tomioka, H. Sasabe, and Y. Shichida. 1993. Comparative study of primary photochemical events of two retinal proteins, bacteriorhodopsin and halorhodopsin, by use of subpicosecond time-resolved spectroscopy. Chem. Phys. Lett. 211:385-391.
37. Kochendörfer, G. G., and R. A. Mathies. 1995. Ultrafast spectroscopy of rhodopsins - photochemistry at its best! Isr. J. Chem. 35:211-226.
38. Krebs, M. P., and H. G. Khorana. 1993. Mechanism of light-dependent proton translocation by bacteriorhodopsin. J. Bacteriol. 175:1555-1560.
39. Lanyi, J. K., and G. Váró. 1995. The photocycles of bacteriorhodopsin. Isr. J. Chem. 35:365-386.
40. Lohrmann, R., T. Althaus, W. Eisfeld, and M. Stockburger. 1995. Light-induced reaction sequence of the chromophore in bacteriorhodopsin studied by time-resolved RR spectroscopy. In Time-Resolved Vibrational Spectroscopy VI, Vol. 74. A. Lau, F. Siebert, and W. Werncke, editors. Springer-Verlag, Berlin. 208-214.
41. Lohrmann, R., I. Grieger, and M. Stockburger. 1991. Resonance Raman studies on the intermediate K-590 in the photocycle of bacteriorhodopsin. J. Phys. Chem. 95:1993-2001.
42. 550: biological implications. J. Raman Spectrosc. 23:575-583.
43. Lozier, R. H., A. Xie, J. Hofrichter, and G. M. Clore. 1992. Reversible steps in the bacteriorhodopsin photocycle. Proc. Natl. Acad. Sci. USA. 89:3610-3614.
44. Maeda, A. 1995. Application of FTIR spectroscopy to the structural study on the function of bacteriorhodopsin. Isr. J. Chem. 35:387-400.
45. Maeda, A., J. Sasaki, J. Pfefferle, Y. Shichida, and T. Yoshizawa. 1991. Fourier transform infared spectral studies on the Schiff base mode of all-trans bacteriorhodopsin and its photointermediates, K and L. Photochem. Photobiol. 54:911-921.
46. Mathies, R. A., C. H. Cruz, W. T. Pollard, and C. V. Shank. 1988. Direct observation of the femtosecond excited-state cis-trans isomerization in bacteriorhodopsin. Science. 243:777-779.
47. 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.
48. Milder, S., and D. S. Kliger. 1988. A time-resolved spectral study of the K and KL intermediates of bacteriorhodopsin. Biophys. J. 53:465-468.
49. Nölker, K., O. Weidlich, and F. Siebert. 1992. Chromophore and protein reactions of bacteriorhodopsin studied by sub-microsecond time-resolved step-scan FTIR spectroscopy. In Time-Resolved Vibrational Spectroscopy V, Vol. 68. H. Takahashi, editor. Springer-Verlag, Berlin. 57-60.
50. Nuss, M. C., W. Zinth, W. Kaiser, E. Kolling, and D. Oesterhelt. 1985. Femtosecond spectroscopy of the first events of the photochemical cycle in bacteriorhodopsin. Chem. Phys. Lett. 117:1-7.
51. Oesterhelt, D., and W. Stoeckenius. 1974. Isolation of the cell membrane of Halobacterium halobium and its fraction into red and purple membrane. Methods Enzymol. 31:667-668.
52. Oesterhelt, D., J. Tittor, and E. Bamberg. 1992. A unifying concept for ion translocation in retinal proteins. J. Bioenerg. Biomembr. 24:181-191.
53. Petrich, J. W., J. Breton, J. L. Martin, and A. Antonetti. 1987. Femtosecond absorption spectroscopy of light-adapted and dark-adapted bacteriorhodopsin. Chem. Phys. Lett. 137:369-375.
54. Polland, H.-J., M. A. Franz, W. Zinth, W. Kaiser, E. Kolling, and D. Oesterhelt. 1986. Early picosecond events in the photocycle of bacteriorhodopsin. Biophys. J. 49:651-662.
55. Popp, A., L. Ujj, and G. H. Atkinson. 1996. Bathorhodopsin structure in the room-temperature rhodopsin photosequence: picosecond time-resolved Coherent anti-Stokes Raman scattering. Proc. Natl. Acad. Sci. USA. 93:372-376.
56. Rothschild, K. J. 1992. FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model. J. Bioenerg. Biomembr. 24:147-167.
57. Rothschild, K. J., J. Gillespie, and P. Roepe. 1985. Fourier transform infrared spectroscopic evidence for the existence of two conformations ot the bacteriorhodopsin primary photoproduct at low temperature. Biochim. Biophys. Acta. 808:140-148.
58. Rothschild, K. J., and H. Marrero. 1982. Infrared evidence that the Schiff base of bacteriorhodopsin is protonated. Proc. Natl. Acad. Sci. USA. 79:4045-4049.
59. Sasaki, J., A. Maeda, C. Kato, and H. Hamaguchi. 1993. Time-resolved infared spectral analysis of the KL-to-L conversion in the photocycle of bacteriorhodopsin. Biochemistry. 32:867-871.
60. Sasaki, J., T. Yuzawa, H. Kandori, A. Maeda, and H. Hamaguchi. 1995. Nanosecond time-resolved infared spectroscopy distinguishes two K species in the bacteriorhosopsin photocycle. Biophys. J. 68:2073-2080.
61. Schulten, K., and P. Tavan. 1978. A mechanism for the light driven proton pump of Halobacterium halobium. Nature. 272:85-86.
62. Sharkov, A. V., A. V. Pakulev, S. V. Chekalin, and Y. A. Matveetz. 1996. Primary events in bacteriorhodopsin probed by subpicosecond spectroscopy. Biochim. Biophys. Acta. 808:94-102.
63. Shichida, Y., S. Matuoka, Y. Hidaka, and T. Yoshizawa. 1983. Absorption spectra of intermediates of bacteriorhodopsin measured by laser photolysis at room temperatures. Biochim. Biophys. Acta. 723:240-246.
64. Siebert, F., and W. Mäntele. 1983. Investigation of the primary photochemistry of bacteriorhodopsin by low-temperature Fourier-transform infrared spectroscopy. Eur. J. Biochem. 130:565-573.
65. Smith, S. O. 1985. Resonance Raman studies on the mechanism of proton translocation by bacteriorhodopsin's retinal chromophore. Thesis, California State University.
66. Smith, S. O., M. Braiman, and R. A. Mathies. 1983. Time-resolved resonance Raman spectroscopy of the K-610 and O-640 photointermediates of bacteriorhodopsin. In Time-Resolved Vibrational Spectroscopy. G. H. Atkinson, editor. Academic Press, New York. 219-230.
67. 15 single bond isomerizations of the retinal chromophore involved in the proton-pumping mechanism of bacteriorhodopsin? Proc. Natl. Acad. Sci. USA. 83: 967-971.
68. Stern, D., and R. A. Mathies. 1985. Picosecond and nanosecond resonance Raman evidence for structural relaxation in bacteriorhodopsin's primary photoproduct. In Springer Proceedings in Physics 4. A. Laubereau and M. Stockburger, editors. Springer-Verlag, Berlin. 250-254.
69. Stockburger, M., T. Alshuth, D. Oesterhelt, and W. Gärtner. 1986. Resonance Raman Spectroscopy of Bacteriorhodopsin: Structure and Function. R. J. Clark and R. E. Hester, editors. John Wiley and Sons, New York. 483-535.
70. 590 intermediate. Proc. Natl. Acad. Sci. USA. 76:3046-3050.
71. Uhmann, W., A. Becker, C. Taran, and F. Siebert. 1991. Time-resolved FT-IR absorption spectroscopy using a step-scan interferometer. Appl. Spectrosc. 45:390-397.
72. Ujj, L., F. Jäger, A. Popp, and G. H. Atkinson. 1996. Vibrational spectrum of the K-590 intermediate in the bacteriorhodopsin photocycle at room temperature: picosecond time-resolved resonance Coherent anti-Stokes Raman spectroscopy. Chem. Phys. 212:421-436.
73. Ujj, L., A. Popp, and G. H. Atkinson. 1994a. Picosecond resonance Coherent anti-Stokes Raman spectroscopy of bacteriorhodopsin: quantitative third-order susceptibility analysis of the dark-adapted mixture. Chem. Phys. 188:221-234.
74. Ujj, L., B. L. Volodin, A. Popp, J. K. Delaney, and G. H. Atkinson. 1994b. Picosecond resonance Coherent anti-Stokes Raman spectroscopy of bacteriorhodopsin: spectra and quantitative third-order susceptibility analysis of the light-adapted BR-570. Chem. Phys. 182:291-311.
75. van den Berg, R., 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.
76. Váró, G., and J. K. Lanyi. 1991. Kinetic and spectroscopic evidence for an irreversible step between deprotonation and reprotonation of the Schiff base in the bacteriorhodopsin photocycle. Biochemistry. 30:5008-5015.
77. Weidlich, O., and F. Siebert. 1993. Time-resolved step-scan FT-IR investigations of the transition from KL to L in bacteriorhodopsin photocycle: identification of chromophore twists by assigning hydrogen-out-of-plane (HOOP) bending vibrations. Appl. Spectrosc. 47:1394-1400.
78. Xu, D., C. Martin, and K. Schulten. 1996. Molecular dynamics study of early picosecond events in the bacteriorhodopsin photocycle: dielectic response, vibrational cooling and the J, K, intermediates. Biophys. J. 70:453-460.
79. Yamamoto, N., T. W. Ebbesen, and H. Ohtani. 1994. Does the KL intermediate exist in the photocycle of bacteriorhodopsin? Chem. Phys. Lett. 228:61-65.