Fourier transform infrared evidence for early deprotonation of Asp85 at alkaline pH in the photocycle of bacteriorhodopsin mutants containing E194Q

Biophysical Journal

Volumn 78, Issue 4, 2000, Pages 2022-2030

  Lazarova, Tzvetana ^a,b   Sanz, Carolina ^a   Querol, Enric ^a   Padrós, Esteve ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUTE OF BIOPHYSICS AND BIOMEDICAL ENGINEERING   (Bulgaria)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BACTERIORHODOPSIN; PROTON;

ALKALINITY; ARTICLE; CONTROLLED STUDY; FOURIER TRANSFORMATION; HUMIDITY; INFRARED SPECTROSCOPY; PROTON TRANSPORT; STEADY STATE;

EID: 0034029916     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76749-X     Document Type: Article

References (38)

1. Althaus, T., and M. Stockburger. 1998. Time and pH dependence of the L-to-M transition in the photocycle of bacteriorhodopsin and its correlation with proton release. Biochemistry. 37:2807-2817.
2. a's of aspartate-85 and control of thermal isomerization and proton release in the arginine-82 to lysine mutant of bacteriorhodopsin. Biochemistry. 34:8820-8834.
3. Balashov, S. P., R. Govindjee, M. Kono, E. Imasheva, E. Lukashev, T. G. Ebrey, R. K. Crouch, D. R. Menick, and Y. Feng. 1993. Effect of the arginine-82 to alanine mutation in bacteriorhodopsin on dark adaptation, proton release, and the photochemical cycle. Biochemistry. 32: 10331-10343.
4. Balashov, S. P., E. S. Imasheva, T. G. Ebrey, N. Chen, D. R. Menick, and R. K. Crouch. 1997. Glutamate-194 to cysteine mutation inhibits fast light-induced proton release in bacteriorhodopsin. Biochemistry. 36: 8671-8676.
5. 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.
6. Balashov, S. P., M. Lu, E. S. Imasheva, R. Govindjee, T. G. Ebrey, B. Othersen III, Y. Chen, R. K. Crouch, and D. R. Menick. 1999. The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH. Biochemistry. 38:2026-2039.
7. a increase of the chromophore counterion in bacteriorhodopsin: implications for ion transport mechanisms of retinal proteins. Biophys. J. 70:939-947.
8. Braiman, M. S., T. Mogi, T. Marti, L. J. Stern, H. G. Khorana, and K. J. Rothschild. 1988. Vibrational spectroscopy of bacteriorhodopsin mutants: light-driven proton transport involves protonation changes of aspartate residues 85, 96, and 212. Biochemistry. 27:8516-8520.
9. a of the retinal Schiff base during the photocycle of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 93:1731-1734.
10. 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.
11. Dioumaev, A. K., H. T. Richter, L. S. Brown, M. Tanio, S. Tuzi, H. Saitô, Y. Kimura, R. Needleman, and J. K. Lanyi. 1998. Existence of a proton transfer chain in bacteriorhodopsin: participation of Glu-194 in the release of protons to the extracellular surface. Biochemistry. 37: 2496-2506.
12. Ebrey, T. G. 1993. Thermodynamics of Membranes, Receptors and Channels. M. Jackson, editor. CRC Press, Boca Raton, FL. 353-387.
13. 13C]aspartic acid labeled purple membrane. Biochemistry. 24:400-407.
14. Essen, L., 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.
15. Genvert, K., B. Hess, J. Soppa, and D. Oesterhelt. 1989. Role of aspartate-96 in proton translocation by bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 86:4943-4947.
16. a of the group responsible tor the light-driven proton release in bacteriorhodopsin. Biophys. J. 71:1011-1023.
17. 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.
18. 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.
19. Kalaidzidis, I. V., I. N. Belevich, and A. D. Kaulen. 1998. Photovoltage evidence that Glu-204 is the intermediate proton donor rather than the terminal proton release group in bacteriorhodopsin. FEBS Lett. 434: 197-200.
20. Koyama, K., T. Miyasaka, R. Needleman, and J. K. Lanyi. 1998. Photoelectrical verification of proton-releasing groups in bacteriorhodopsin. Photochem. Photobiol. 68:400-406.
21. Lanyi, J. K. 1997. Mechanism of ion transport across membranes. Bacteriorhodopsin as a prototype for proton pumps. J. Biol. Chem. 272: 31209-31212.
22. Lazarova, Tz., and E. Padrós. 1996. Helical and reverse turn changes in the BR→N transition of bacteriorhodopsin. Biochemistry. 35:8354-8358.
23. Luecke, H., B. Schobert, H.-T. Richter, J.-P. Cartailler, and J. K. Lanyi. 1999a. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:899-911.
24. Luecke, H., B. Schobert, H.-T. Richter, J.-P. Cartailler, and J. K. Lanyi. 1999b. Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science. 286:255-260.
25. Maeda, A., J. Sasaki, Y. Shichida, T. Yoshizawa, M. Chang, B. Ni, R. Needleman, and J. K. Lanyi. 1992. Structures of aspartic acid-96 in the L and N intermediates of bacteriorhodopsin: analysis by Fourier transform infrared spectroscopy. Biochemistry. 31:4684-1690.
26. Mitsuoka, K., T. Hirai, K. Murata, A. Miyazawa, A. Kidera, Y. Kimura, and Y. Fujiyoshi. 1999. The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: implication of the charge distribution. J. Mol. Biol. 286:861-882.
27. Oesterhelt, D. 1998. The structure and mechanism of the family of retinal proteins from halophilic archea. Curr. Opin. Struct. Biol. 8:489-500.
28. 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.
29. Pebay-Peyroula, E., G. Rummel, J. Rosenbusch, and E. M. Landau. 1997. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science. 277:1676-1681.
30. Pfefferlé. J.-M., A. Maeda, J. Sasaki, and T. Yoshizawa. 1991. Fourier transform infrared study of the N intermediate of bacteriorhodopsin. Biochemistry. 30:6548-65.56.
31. Rammelsberg, R., G. Huhn, M. Lübben, and K. Gerwert. 1998. Bacteriorhodopsin's intramolecular proton-release pathway consists of a hydrogen-bonded network. Biochemistry. 37:5001-5009.
32. a's of Asp-85 and Glu-204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry. 35:4054-4062.
33. Rüdiger, M., J. Tittor, K. Gerwert, and D. Oesterhelt. 1997. Reconstitution of bacteriorhodopsin from the apoprotein and retinal studied by Fourier-transform infrared spectroscopy. Biochemistry. 36:4867-4874.
34. Sanz, C., Tz. Lazarova, F. Sepulcre, R. González Moreno, J.-L. Bourdelande, E. Querol, and E. Padrós. 1999. Opening the Schiff base moiety of bacteriorhodopsin by mutation of the four extracellular Glu side chains. FEBS Lett. 456:191-195.
35. Sasaki, J., Y. Shichida, J. K. Lanyi, and A. Maeda. 1992. Protein changes associated with reprotonation of the Schiff base in the photocycle of Asp96-Asn bacteriorhodopsin. The MN intermediate with unprotonated Schiff base but N-Iike protein structure. J. Biol. Chem. 267: 20782-20786.
36. 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.
37. Zscherp, C., and J. Heberle. 1997. Infrared difference spectra of the intermediates L, M, N, and O of the bacteriorhodopsin photoreaction obtained by time-resolved attenuated total reflection spectroscopy. J. Phys. Chem. B. 101:10542-10547.
38. a changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy. Proc. Natl. Acad. Sci. USA. 96:5498-5503.