Role of arginine-82 in fast proton release during the bacteriorhodopsin photocycle: A time-resolved FT-IR study of purple membranes containing 15N-labeled arginine

Biochemistry

Volumn 43, Issue 40, 2004, Pages 12809-12818

  Xiao, Yaowu ^a   Hutson, M Shane ^a,c   Belenky, Marina ^b   Herzfeld, Judith ^b   Braiman, Mark S ^a  

^a SYRACUSE UNIVERSITY   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ENZYMES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; ISOTOPES; PH; PROTONS; STOICHIOMETRY;

BACTERIORHODOPSIN PHOTOCYCLE; CHEMICAL LABELING; LIGHT INDUCED DEPROTONATION;

MUTAGENESIS;

ARGININE; BACTERIORHODOPSIN; ISOTOPE; NITROGEN 15; PROTON;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL LABELING; INFRARED SPECTROSCOPY; PH; PHOTOCATALYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS; STOICHIOMETRY; STRUCTURE ANALYSIS; VIBRATION; WILD TYPE;

ARGININE; BACTERIORHODOPSINS; HYDROGEN-ION CONCENTRATION; KINETICS; NITROGEN ISOTOPES; PHOTOCHEMISTRY; PROTONS; PURPLE MEMBRANE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TEMPERATURE; TIME FACTORS;

EID: 4944249406     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049238g     Document Type: Article

References (58)

1. Herzfeld, J., and Lansing, J. C. (2002) Magnetic resonance studies of the bacteriorhodopsin pump cycle, Annu. Rev. Biophys. Biomol. Struct. 31, 73-95.
2. Neutze, R., Pebay-Peyroula, E., Edman, K., Royant, A., Navarro, J., and Landau E. M. (2002) Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport, Biochim. Biophys. Acta 1565, 144-167.
3. Lanyi, J. K. (2004) Bacteriorhodopsin, Annu. Rev. Physiol. 66, 665-688.
4. Mathies, R. A., Lin, S. W., Ames, J. B., and Pollard, W. T. (1991) From femtoseconds to biology: Mechanism of bacteriorhodopsin's light-driven proton pump, Annu. Rev. Biophys. Biophys. Chem. 20, 491-518.
5. Mathies, R. A., Brito, C. C. H., Pollard, W. T., and Shank, C. V. (1988) Direct observation of the femtosecond excited-state cis-trans isomerization in bacteriorhodopsin, Science 240, 777-779.
6. Dobler, J., Zinth, W., Kaiser, W., and Oesterhelt, D. (1988) Excited-state reaction dynamics of bacteriorhodopsin studied by femtosecond spectroscopy, Chem. Phys. Lett. 144, 215-220.
7. Sass, H. J., Buldt, G., Gessenich, R., Hehn, D., Neff, D., Schlesinger, R., Berendzen, J., and Ormos, P. (2000) Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin, Nature 406, 649-653.
8. Braiman, M. S., Mogi, T., Marti, T., Stern, L. J., Khorana, H. G., and Rothschild, K. J. (1988) Vibrational spectroscopy of bacteriorhodopsin mutants: Light-driven proton transport involves protonation changes of aspartic acid residues 85, 96, and 212, Biochemistry 27, 8516-8520.
9. Xie A. H., Nagle J. F., and Lozier R. H. (1987) Flash spectroscopy of purple membrane, Biophys. J. 51, 627-635.
10. Heberle, J., and Dencher, N. A. (1992) Surface-bound optical probes monitor proton translocation and surface potential changes during the bacteriorhodopsin photocycle, Proc. Natl. Acad. Sci. U.S.A. 89, 5996-6000.
11. Alexiev, U., Mollaaghababa, R., Scherrer, P., Khorana, H. G., and Heyn, M. P. (1995) Rapid long-range proton diffusion along the surface of the purple membrane and delayed proton transfer into the bulk, Proc. Natl. Acad. Sci. U.S.A. 92, 372-376.
12. Cao, Y., Brown, L. S., Sasaki, J., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Relationship of proton release at the extracellular surface to deprotonation of the schiff base in the bacteriorhodopsin photocycle, Biophys. J. 68, 1518-1530.
13. Siebert, F., Mäntele, W., and Kreutz, W. (1982) Evidence for the protonation of two internal carboxylic groups during the photocycle of bacteriorhodopsin: Investigation of kinetic infrared spectroscopy, FEBS Lett. 141, 82-87.
14. Zimányi, L., Váró, G., Chang, M., Ni, B., Needleman, R., and Lanyi, J. K. (1992) Pathways of proton release in the bacteriorhodopsin photocycle, Biochemistry 31, 8535-8543.
15. Brown, L. S., Needleman, R., and Lanyi, J. K. (1996) Interaction of proton and chloride transfer pathways in recombinant bacteriorhodopsin with chloride transport activity: Implications for the chloride translocation mechanism, Biochemistry 35, 16048-16054.
16. Brown, L. S., Sasaki, J., Kandori, H., Maeda, A., Needleman, A., and Lanyi, J. K. (1995) Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin, J. Biol. Chem. 270, 27122-27126.
17. a's of asp-85 and glu-204 forms part of the reprotonation switch of bacteriorhodopsin, Biochemistry, 35, 4054-4062.
18. Richter, H. T., Needleman, R., Kandori, H., Maeda, A., and Lanyi, J. K. (1996) Relationship of retinal configuration and internal proton transfer at the end of the bacteriorhodopsin photocycle, Biochemistry 35, 15461-15466.
19. Dioumaev, A. K., Richter, H. T., Brown, L. S., Tanio, M., Satoru, T., Saito, H., Kimura, Y., Needleman, R., and Lanyi, J. K. (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.
20. 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.
21. Hutson, M. S., Alexiev, U., Shilov, S. V., Wise, K. J., and Braiman, M. S. (2000) Evidence for a perturbation of arginine-82 in the bacteriorhodopsin photocycle from time-resolved infrared spectra, Biochemistry 39, 13189-13200.
22. Kono, M., Misra, S., and Ebrey, T. G. (1993) pH dependence of light-induced proton release by bacteriorhodopsin, FEBS Lett. 331, 31-34.
23. Rammelsberg, R., Huhn, G., Lübben, M., and Gerwert, K. (1998) Bacteriorhodopsin's intramolecular proton-release pathway consists of a hydrogen-bonded network, Biochemistry 37, 5001-5009.
24. a calculations suggest storage of an excess proton in a hydrogen-bonded water network in bacteriorhodopsin, J. Mol. Biol. 312, 203-219.
25. Braiman, M. S., Bousché, O., and Rothschild, K. J. (1991) Protein dynamics in the bacteriorhodopsin photocycle: Submillisecond Fourier transform infrared spectra of the L, M, and N photointermediates, Proc. Natl. Acad. Sci. U.S.A. 88, 2388-2392.
26. Bousché, O., Sonar, S., Krebs, M. P., Khorana, H. G., and Rothschild, K. J. (1992) Time-resolved Fourier transform infrared spectroscopy of the bacteriorhodopsin mutant tyr-185→phe: asp-96 reprotonates during O formation; asp-85 and asp-212 deprotonate during O decay, Photochem. Photobiol. 56, 1085-1095.
27. Gerwert, K., Souvignier, G., and Hess, B. (1990) Simultaneous monitoring of light-induced changes in protein side-group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier-transform infrared spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 87, 9774-9778.
28. Dencher, N. A., and Wilms, M. (1975) Flash photometric experiments on the photochemical cycle of bacteriorhodopsin, Biophys. Struct. Mech. 1, 259-271.
29. Cao Y., Brown, L. S., Needleman, R., and Layni, J. K. (1993) Relationship of proton uptake on the cytoplasmic surface and reisomerization of the retinal in the bacteriorhodopsin photocycle: An attempt to understand the complex kinetics of the pH changes and the N and O intermediates, Biochemistry 32, 10239-10248.
30. Petkova, A. T., Hu, J. G., Bizounok, M., Simpson, M., Griffin, R. G., and Herzfeld, J. (1999) Arginine activity in the proton-motive photocycle of bacteriorhodopsin: Solid-state NMR studies of the wild-type and D85N proteins, Biochemistry 38, 1562-1572.
31. Braiman, M. S., Ahl, P. L., and Rothschild, K. J. (1987) Millisecond Fourier-transform infrared difference spectra of bacteriorhodopsin's M412 photoproduct, Proc. Natl. Acad. Sci. U.S.A. 84, 5221-5225.
32. Doherty, D. G., Shapira, R. H., and Burnett, W. T. (1957) Synthesis of aminoalkylisothiuronium salts and their conversion to mercaptoalkylguanidines and thiazolines, J. Am. Chem. Soc. 79, 5667-5671.
33. Chizhov, I., Chernavskii, D. S., Engelhard, M., Mueller, K. H., Zubov, B. V., and Hess, H. (1996) Spectrally silent transitions in the bacteriorhodopsin photocycle, Biophys. J. 71, 2329-2345.
34. Rödig, C., Chizhov, I., Weidlich, O., and Siebert, F. (1999) Time-resolved step-scan Fourier transform infrared spectroscopy reveals differences between early and late M intermediates of bacteriorhodopsin, Biophys. J. 76, 2687-2701.
35. Sharonov, A. Yu., Tkachenko, N. V., Savransky, V. V., and Dioumaev, A. K. (1991) Time-resolved ultraviolet absorption changes in the photocycle of bacteriorhodopsin, Photochem. Photobiol. 54, 889-893.
36. Dioumaev, A. K. (1997) Evaluation of intrinsic chemical kinetics and transient product spectra from time-resolved spectroscopic data, Biophys. Chem. 67, 1-25.
37. Sasaki, J., Lanyi, J. K., Needleman, R., Yoshizawa, T., and Maeda, A. (1994) Complete identification of CO stretching vibrational bands of protonated aspartic acid residues in the difference infrared spectra of M and N intermediates versus bacteriorhodopsin, Biochemistry 33, 3178-3184.
38. a changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 96, 5498-5503.
39. Dickopf, S., and Heyn, M. P. (1997) Evidence for the first phase of the reprotonation switch of bacteriorhodopsin from time-resolved photovoltage and flash photolysis experiments on the photoreversal of the M-intermediate, Biophys J. 73, 3171-3181.
40. Misra, S., Govindjee, R., Ebrey, T. G., Chen, N., Ma, J. X., and Crouch, R. K. (1997) Proton uptake and release are rate-limiting steps in the photocycle of the bacteriorhodopsin mutant E204Q, Biochemistry 36, 4875-4883.
41. Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E., and Downing, K. H. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy, J. Mol. Biol. 213, 899-929.
42. Subramaniam, S., Marti, T., and Khorana, H. G. (1990) Protonation state of asp (glu)-85 regulates the purple-to-blue transition in bacteriorhodopsin mutants arg-82-ala and asp-85-glu: the blue form is inactive in proton translocation, Proc. Natl. Acad. Sci. U.S.A. 87, 1013-1017.
43. Thorgeirsson, T. E., Milder, S. J., Miercke, L. J., Betlach, M. C., Shand, R. F., Stroud, R. M., and Kliger, D. S. (1991) Effects of asp-96→asn, asp-85→asn, and arg-82→gln single-site substitutions on the photocycle of bacteriorhodopsin, Biochemistry 30, 9133-9142.
44. Brown, L. S., Bonet, L., Needleman, R., and Lanyi, J. K. (1993) Estimated acid dissociation constants of the Schiff base, asp-85, and arg-82 during the bacteriorhodopsin photocycle, Biophys. J. 65, 124-130.
45. Otto, H., Marti, T., Holz, M., Mogi, T., Stern, L. J., Engel, F., Khorana, H. G., and Heyn, M. P. (1990) Substitution of amino acids asp-85, asp-212, and arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base, Proc. Natl. Acad. Sci. U.S.A. 87, 1018-1022.
46. Braiman, M. S., Briercheck, D. M., and Kriger, K. M. (1999) Modeling vibrational spectra of amino acid side chains in proteins: effects of protonation state, counterion, and solvent on arginine C-N stretch frequencies, J. Phys. Chem. B 103, 4744-4750
47. Hatanaka, M., Sasaki, J., Kandori, H., Ebrey, T. G., Needleman, R., Lanyi, J. K., and Maeda, A. (1996) Effects of arginine-82 on the interactions of internal water molecules in bacteriorhodopsin, Biochemistry 35, 6308-6312.
48. Bagley, K., Dollinger, G., Eisenstein, L., Singh, A. K., and Zimányi, L. (1982) Fourier transform infrared difference spectroscopy of bacteriorhodopsin and its photoproducts, Proc. Natl. Acad. Sci. U.S.A. 79, 4972-4976.
49. Grieger, I., and Atkinson, G. H. (1985) Photolytic interruptions of the bacteriorhodopsin photocycle examined by time-resolved resonance Raman spectroscopy, Biochemistry 24, 5660-5665.
50. Kluge, T., Olejnik, J., Smilowitz, L., and Rothschild, K. J. (1998) Conformational changes in the core structure of bacteriorhodopsin, Biochemistry 37, 10279-10285.
51. Rothschild, K. J., Marti, T., Sonar, S., He, Y., Rath, P., Fischer, W., and Khorana, H. G. (1993) Asp96 deprotonation and transmembrane alpha-helical structural changes in bacteriorhodopsin, J. Biol. Chem. 268, 27046-27052.
52. 2O) solution. I. Spectral parameters of amino acid residue absorption bands, Biopolymers 30, 1243-1257.
53. Kanamori, K., and Roberts, J. D. (1983) A nitrogen-15 NMR study of the barriers to isomerization about guanidinium and guanidino carbon-nitrogen bonds in L-arginine, J. Am. Chem. Soc. 105, 4698-4701.
54. Levy, G. C., and Lichter, R. L. (1979) Nitrogen-15 Nuclear Magnetic Resonance Spectroscopy, Wiley-Interscience, New York.
55. a increase of the chromophore counterion in bacteriorhodopsin: implications for ion transport mechanisms of retinal proteins, Biophys. J. 70, 939-947.
56. Luecke, H., Schobert, B., Richter, H., Cartailler, J., and Lanyi, J. K. (1999) Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution, Science 286, 255-260.
57. a of the group responsible for the light-driven proton release in bacteriorhodopsin, Biophys. J. 71, 1011-1023.
58. Brown, L. S., Váró, G., Hatanaka, M., Sasaki, J., Kandori, H., Maeda, A., Friedman, N., Sheves, M., Needleman, R., and Lanyi, J. K. (1995) The complex extracellular domain regulates the deprotonation and reprotonation of the retinal Schiff base during the bacteriorhodopsin photocycle, Biochemistry 34, 12903-12911.