Kinetic and thermodynamic study of the bacteriorhodopsin photocycle over a wide pH range

Biophysical Journal

Volumn 75, Issue 6, 1998, Pages 3110-3119

  Ludmann, Krisztina ^a   Gergely, Csilla ^a   Váró, György ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN;

ARTICLE; BACTERIAL MEMBRANE; ENTHALPY; ENTROPY; HALOBACTERIUM SALINARUM; KINETICS; NONHUMAN; PH; PROTON TRANSPORT; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); HALOBACTERIUM SALINARUM;

EID: 0031738407     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)77752-5     Document Type: Article

References (74)

1. Alexiev, U., T. Marti, M. P. Heyn, H. G. Khorana, and P. Scherrer. 1994. Surface charge of bacteriorhodopsin detected with covalently bound pH indicators at selected extracellular and cytoplasmic sites. Biochemistry. 33:298-306.
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. Balashov, S. P., E. S. Imasheva, R. Govindjee, and T. G. Ebrey. 1996. Titration of aspartate-85 in bacteriorhodopsin: what it says about chromophore isomerization and proton release. Biophys. J. 70:473-481.
4. Baldwin, R. L. 1986. Temperature dependence of the hydrophobic interaction in protein folding. Proc. Natl. Acad. Sci. USA. 83:8069-8072.
5. a values of ionizable groups in bacteriorhodopsin. J. Mol. Biol. 224: 473-486.
6. Brown, L. S., M. 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.
7. Brown, L. S., J. Sasaki, H. Kandori, A. Maeda, R. Needleman, and J. K. Lanyi. 1995. Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol. Chem. 270: 27122-27126.
8. Cao, Y., L. S. Brown, R. Needleman, and J. K. Lanyi. 1993. Relationship of proton uptake on the cytoplasmic surface and the reisomerization of the retinal in the bacteriorhodopsin photocycle: an attempt to understand the complex kinetics of the protons and the N and O intermediates. Biochemistry. 32:10239-10248.
9. Chizhov, I. V., D. S. Chernavskii, M. Engelhard, K. H. Mueller, B. V. Zubov, and B. Hess. 1996. Spectrally silent transitions in the bacteriorhodopsin photocycle. Biophys. J. 71:2329-2345.
10. 640 intermediate of the bacteriorhodopsin photocycle. Biophys. J. 61:1001-1006.
11. Dancsházy, 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.
12. Dér, A., P. Hargittai, and J. Simon. 1985. Time-resolved photoelectric and absorption signals from oriented purple membranes immobilized in gel. J. Biochem. Biophys. Methods. 10(5-6):295-300.
13. Dér, A., S. Száraz, R. Tóth-Boconádi, Z. Tokaji, L. Keszthelyi, and W. Stoeckenius. 1991. Alternative translocation of protons and halide ions by bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 88:4751-4755.
14. Dioumaev, A. K. 1997. Evaluation of intrinsic chemical kinetics and transient product spectra from time-resolved spectroscopic data. Biophys. Chem. 67:1-25.
15. Drachev, L. A., A. D. Kaulen, and A. Y. Komrakov. 1993. On the two pathways of the M-intermediate formation in the photocycle of bacteriorhodopsin. Biochem. Int. 30:461-469.
16. Draheim, J. E., and J. Y. Cassim. 1985. Large-scale global structural changes of the purple membrane during the photocycle. Biophys. J. 47:497-507.
17. Druckmann, S., M. P. Heyn, J. K. Lanyi, M. Ottolenghi, and L. Zimányi. 1993. Thermal equilibration between the M and N intermediates in the photocycle of bacteriorhodopsin. Biophys. J.
18. Ebrey, T. G. 1993. Light energy transduction in bacteriorhodopsin. In Thermodynamics of Membranes, Receptors and Channels. M. Jackson, editor. CRC Press, Boca Raton, FL. 353-387.
19. Eisfeld, W., C. Pusch, R. Diller, R. Lohrmann, and M. Stockburger. 1993. Resonance Raman and optical transient studies on the light-induced proton pump of bacteriorhodopsin reveal parallel photocycles. Biochemistry. 32:7196-7215.
20. Friedman, N., Y. Gat, M. Sheves, and M. Ottolenghi. 1994. On the heterogeneity of the M population in the photocycle of bacteriorhodopsin. Biochemistry. 33:14758-14767.
21. Garty, H., S. R. Caplan, and D. Cahen. 1982. Photoacoustic photocalorimetry and spectroscopy of Halobacterium halobium purple membranes. Biophys. J. 37:405-415.
22. Gergely, C., C. Ganea, G. I. Groma, and G. Váró. 1993. Study of the photocycle and charge motions of the bacteriorhodopsin mutant D96N. Biophys. J. 65:2478-2483.
23. Gergely, C., C. Ganea, and G. Váró. 1994. Combined optical and photoelectric study of the photocycle of 13-cis bacteriorhodopsin. Biophys. J. 67:855-861.
24. Gergely, C., L. Zimányi, and G. Váró. 1997. Bacteriorhodopsin intermediate spectra determined over a wide pH range. J. Phys. Chem. B. 101:9390-9395.
25. Grigorieff, N., T. A. Ceska, K. H. Downing, J. M. Baldwin, and R. Henderson. 1996. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:393-421.
26. Han, B.-G., J. Vonck, and R. M. Glaeser. 1994. The bacteriorhodopsin photocycle: direct structural study of two substates of the M-intermediate. Biophys. J. 67:1179-1186.
27. Haupts, U., J. Tittor, E. Bamberg, and D. Oesterhelt. 1997. General concenpt for ion translocation by halobacterial retinal proteins: the isomerization/switch/transfer (IST) model. Biochemistry. 36:2-7.
28. Henderson, R., J. M. Baldwin, T. A. Ceska, F. Zemlin, E. Beckmann, and K. H. Downing. 1990. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213: 899-929.
29. Hendler, R. W., Z. Dancsházy, S. Bose, R. I. Shrager, and Z. Tokaji. 1994. Influence of excitation energy on the bacteriorhodopsin photocycle. Biochemistry. 33:4604-4610.
30. 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.
31. Kandori, H., Y. Yamazaki, M. Hatanaka, R. Needleman, L. S. Brown, H. T. Richter, J. K. Lanyi, and A. Maeda. 1997. Time-resolved Fourier transform infrared study of structural changes in the last steps of the photocycle of Glu-204 and Leu-93 mutants of bacteriorhodopsin. Biochemistry. 36:5134-5141.
32. Kimura, Y., D. G. Vassylyev, A. Miyazawa, A. Kidera, M. Matsushima, K. Mitsuoka, K. Murata, T. Hirai, and Y. Fujiyoshi. 1997. Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature. 389:206-211.
33. Komrakov, A. Y., and A. D. Kaulen. 1995. M-decay in the bacteriorhodopsin photocycle: effect of cooperativity and pH. Biophys. Chem. 56:113-119.
34. Krebs, M. P., and H. Gobind Khorana. 1993. Mechanism of light-dependent proton translocation by bacteriorhodopsin. J. Bacteriol. 175: 1555-1560.
35. Lanyi, J. K., and G. Váró. 1995. The photocycle of bacteriorhodopsin. Isr. J. Chem. 35:365-385.
36. 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.
37. Luchian, T., Z. Tokaji, and Z. Dancsházy. 1996. Actinic light density dependence of the O intermediate of the photocycle of bacteriorhodopsin. FEBS Lett. 386:55-59.
38. Ludmann, K., C. Gergely, A. Dér, and G. Váró. 1998. II. Electric signals during the bacteriorhodopsin photocycle, determined over a wide pH range. Biophys. J. 75:3120-3126.
39. Marque, J., L. Eisenstein, E. Gratton, J. M. Sturtevant, and C. J. Hardy. 1984. Thermodynamic properties of purple membrane. Biophys. J. 46: 567-572.
40. Miller, A., and D. Oesterhelt. 1990. Kinetic optimization of bacteriorhodopsin by aspartic acid 96 as an internal proton donor. Biochim. Biophys. Acta Bio-Energetics. 1020:57-64.
41. Mowery, P. C., R. H. Lozier, Q. Chae, Y. W. Tseng, M. Taylor, and W. Stoeckenius. 1979. Effect of acid pH on the absorption spectra and photoreactions of bacteriorhodopsin. Biochemistry. 18:4100-4107.
42. Murphy, K. P., P. L. Privalov, and S. J. Gill. 1990. Common features of protein unfolding and dissolution of hydrophobic compounds. Science. 247:559-561.
43. Nagle, J. F. 1991. Solving complex photocycle kinetics. Theory and direct method. Biophys. J. 59:476-487.
44. Oesterhelt, D., and W. Stoeckenius. 1974. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31:667-678.
45. Ort, D. R., and W. W. Parson. 1979. Enthalpy changes during the photochemical cycle of bacteriorhodopsin. Biophys. J. 25:355-364.
46. Otto, H., C. Zscherp, B. Borucki, and M. P. Heyn. 1995. Time-resolved polarized absorption spectroscopy with isotropically excited oriented purple membranes: the orientation of the electronic transition dipole moment of the chromophore in the O-intermediate of bacteriorhodopsin. J. Phys. Chem. 99:3847-3853.
47. 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 phase. Science. 277:1676-1681.
48. Popp, A., M. Wolperdinger, N. Hampp, C. Bräuchle, and D. Oesterhelt. 1993. Photochemical conversion of the O-intermediate to 9-cis-retinal-containing products in bacteriorhodopsin films. Biophys. J. 65: 1449-1459.
49. a's of Asp-85 and Glu-204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry. 35:4054-4062.
50. Richter, H. T., R. Needleman, H. Kandori, A. Maeda, and J. K. Lanyi. 1996b. Relationship of retinal configuration and internal proton transfer at the end of the bacteriorhodopsin photocycle. Biochemistry. 35: 15461-15466.
51. Schulenberg, P. J., W. Gärtner, and S. E. Braslavsky. 1994. A possible protein motion during the bacteriorhodopsin photocycle detected by combined photothermal beam deflection and optical detection. Biochim. Biophys. Acta Bio-Energetics. 1185:92-96.
52. Sherman, W. V., and S. R. Caplan. 1975. Arrhenius parameters of phototransients in Halobacterium halobium in physiological conditions. Nature. 258:766-768.
53. Song, L., S. L. Logunov, D. Yang, and M. A. El-Sayed. 1994. The pH dependence of the subpicosecond retinal photoisomerization process in bacteriorhodopsin: evidence for parallel photocycles. Biophys. J. 67: 2008-2012.
54. Subramaniam, S., A. R. Faruqi, D. Oesterhelt, and R. Henderson. 1997. Electron diffraction studies of light-induced conformational changes in the Leu-93→Ala bacteriorhodopsin mutant. Proc. Natl. Acad. Sci. USA. 94:1767-1772.
55. Subramaniam, S., M. Gerstein, D. Oesterhelt, and R. Henderson. 1993. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12:1-8.
56. Száraz, S., D. Oesterhelt, and P. Ormos. 1994. pH-induced structural changes in bacteriorhodopsin studied by Fourier transform infrared spectroscopy. Biophys. J. 67:1706-1712.
57. Szundi, I., J. W. Lewis, and D. S. Kliger. 1997. Deriving reaction mechanisms from kinetic spectroscopy. Application to late rhodopsin intermediates. Biophys. J. 73:688-702.
58. Tokaji, Z. 1995. Cooperativity-regulated parallel pathways of the bacteriorhodopsin photocycle. FEBS Lett. 357:156-160.
59. Tokaji, Z., and Z. Dancsházy. 1992. Kinetics of the N intermediate and the two pathways of recovery of the ground-state of bacteriorhodopsin. FEBS Lett. 311:267-270.
60. Tsuda, M., R. Govindjee, and T. G. Ebrey. 1983. Effects of pressure and temperature on the M412 intermediate of the bacteriorhodopsin photocycle. Implications for the phase transition of the purple membrane. Biophys. J. 44:249-254.
61. Váró, G., A. Duschl, and J. K. Lanyi. 1990. Interconversions of the M, N, and O intermediates of the bacteriorhodopsin photocycle. Biochemistry. 29:3798-3804.
62. Váró, G., and L. Keszthelyi. 1985. Arrhenius parameters of the bacteriorhodopsin photocycle in dried oriented samples. Biophys. J. 47:243-246.
63. Váró, G., and J. K. Lanyi. 1989. Photoreactions of bacteriorhodopsin at acid pH. Biophys. J. 56:1143-1151.
64. Váró, G., and J. K. Lanyi. 1990a. Pathways of the rise and decay of the M photointermediate of bacteriorhodopsin. Biochemistry. 29:2241-2250.
65. Váró, G., and J. K. Lanyi. 1990b. Protonation and deprotonation of the M, N, and O intermediates during the bacteriorhodopsin photocycle. Biochemistry. 29:6858-6865.
66. Váró, G., and J. K. Lanyi. 1991a. Effects of the crystalline structure of purple membrane on the kinetics and energetics of the bacteriorhodopsin photocycle. Biochemistry. 30:7165-7171.
67. Váró, G., and J. K. Lanyi. 1991b. Thermodynamics and energy coupling in the bacteriorhodopsin photocycle. Biochemistry. 30:5016-5022.
68. Váró, G., and J. K. Lanyi. 1995. Effects of hydrostatic pressure on the kinetics reveal a volume increase during the bacteriorhodopsin photocycle. Biochemistry. 34:12161-12169.
69. Váró, G., R. Needleman, and J. K. Lanyi. 1995. Light-driven chloride ion transport by halorhodopsin from Natronobacterium pharaonis. 2. Chloride release and uptake, protein conformation change, and thermodynamics. Biochemistry. 34:14500-14507.
70. Váró, G., R. Needleman, and J. K. Lanyi. 1996. Protein structural change at the cytoplasmic surface as the cause of cooperativity in the bacteriorhodopsin photocycle. Biophys. J. 70:461-467.
71. Zhang, D., and D. Mauzerall. 1996. Volume and enthalpy changes in the early steps of bacteriorhodopsin photocycle studied by time-resolved photoacoustics. Biophys. J. 71:381-388.
72. Zimányi, L., Y. Cao, R. Needleman, M. Ottolenghi, and J. K. Lanyi. 1993. Pathway of proton uptake in the bacteriorhodopsin photocycle. Biochemistry. 32:7669-7678.
73. Zimányi, L., Z. Tokaji, and G. Dollinger. 1987. Circular dichroic spectrum of the L form and the blue light product of the M form of purple membrane. Biophys. J. 51:145-148.
74. Zimányi, L., G. Váró, M. Chang, B. Ni, R. Needleman, and J. K. Lanyi. 1992. Pathways of proton release in the bacteriorhodopsin photocycle. Biochemistry. 31:8535-8543.