Structural changes due to the deprotonation of the proton release group in the M-photointermediate of bacteriorhodopsin as revealed by time-resolved FTIR spectroscopy

Biochemistry

Volumn 47, Issue 44, 2008, Pages 11598-11605

  Morgan, Joel E ^a   Vakkasoglu, Ahmet S ^b   Lugtenburg, Johan ^c   Gennis, Robert B ^b   Maeda, Akio ^b  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

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

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONYLATION; DEPROTONATION; DEUTERIUM; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN; HYDROGEN BONDS; PROTONS; RAIN GAGES;

BACKBONE CARBONYLS; BACTERIORHODOPSIN (BR); BROAD BANDS; DEUTERATION; EXTRACELLULAR; FTIR SPECTROSCOPIES; HYDROGEN BONDINGS; LOWER FREQUENCIES; PHOTOACTIVATION; PHOTOCYCLE; PROTON RELEASES; PROTONATED; PUMPING CYCLES; SCHIFF BASE; SIDE CHAINS; SPECTRAL CHANGES; STRUCTURAL CHANGES; TIME-RESOLVED; TRANSITION DIPOLES; VIBRATIONAL BANDS; WATER MOLECULES;

PROTON TRANSFER;

ARGININE; ASPARTIC ACID; BACTERIORHODOPSIN; CARBONYL DERIVATIVE; RETINAL; SCHIFF BASE; TYROSINE;

ARTICLE; HYDROGEN BOND; INFRARED SPECTROSCOPY; PH; PHOTOACTIVATION; PKA; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON TRANSPORT;

ASPARTIC ACID; BACTERIORHODOPSINS; CARBON RADIOISOTOPES; DEUTERIUM; HALOBACTERIUM SALINARUM; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; PHOTOCHEMISTRY; PROTEIN STRUCTURE, SECONDARY; PROTONS; SCHIFF BASES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TYROSINE;

EID: 55249119081     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801405v     Document Type: Article

References (59)

1. Lozier, R. H., Bogomolni, R. A., and Stoeckenius, W. (1975) Bacteriorhodopsin: A light-driven proton pump in Halobacterium halobium. Biophys. J. 15, 955-963.
2. Xie, A., Nagle, J. F., and Lozier, R. H. (1987) Flash spectroscopy of purple membrane. Biophys. J. 51, 627-635.
3. Maeda, A., Morgan, J. E., Gennis, R. B., and Ebrey, T. G. (2006) Water as a cofactor in the unidirectional light-driven proton transfer steps in bacteriorhodopsin. Photochem. Photobiol. 82, 1396-1405.
4. Morgan, J. E., Gennis, R. B., and Maeda, A. (2008) A role for internal water molecules in proton affinity changes of the Schiff base and Asp85 for one-way proton transfer in bacteriorhodopsin. Photochem. Photobiol. 84, 1038-1045.
5. Morgan, J. E., Vakkasoglu, A. S., Gennis, R. B., and Maeda, A. (2007) Water structural changes in the L and M intermediates of bacteriorhodopsin as revealed by time-resolved step-scan FTIR spectroscopy. Biochemistry 46, 2787-2796.
6. Lórenz-Fonfría, V. A., Furutani, Y., and Kandori, H. (2008) Active internal waters in the bacteriorhodopsin photocycle. A comparative study of the L and M intermediates at room and cryogenic temperatures by infrared spectroscopy. Biochemistry 47, 4071-4081.
7. Váró, G., and Keszthelyi, L. (1983) Photoelectric signals from dried oriented purple membranes of Halobacterium halobium. Biophys. J. 43, 47-51.
8. Váró, G., and Lanyi, J. K. (1991) Distortion in the photocycle of bacteriorhodopsin at moderate dehydration. Biophys. J. 59, 313-322.
9. Heberle, J., and Dencher, N. A. (1992) Surface-bound optical probes monitor proton translocation and surface potential changes during the bacteriorhodpsin photocycle. Proc. Natl. Acad. Sci. U.S.A. 89, 5996-6000.
10. Zimanyi, 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.
11. Brown, L. S., Sasaki, J., Kandori, H., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Glutamic acid 204 in the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol. Chem. 270, 27122-27126.
12. Balashov, S. P., Imasheva, E. S., Ebrey, T. G., Chen, N., Menick, D. R., and Crouch, R. K. (1997) Glutamate-194 to cysteine mutation inhibits fast light-induced proton release in bacteriorhodopsin. Biochemistry 36, 8671-8676.
13. Dioumaev, A. K., Richter, H.-T., Brown, L. S., Tanio, M., Tuzi, S., Saitô, 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.
14. Garczarek, F., Brown, L. S., Lanyi, J. K., and Gerwert, K. (2005) Proton binding within a membrane protein by a protonated water cluster. Proc. Natl. Acad. Sci. U.S.A. 102, 3633-3638.
15. Balashov, S. P., Govindjee, R., Kono, M., Imasheva, E. S., Lukashev, E., Ebrey, T. G., Crouch, R. K., Menick, D. R., and Feng, Y. (1993) Effect of the arginine-82 to alanine mutation in bacteriorhodopsinon dark adaptation, proton release, and the photochemical cycle. Biochemistry 32, 10331-10343.
16. a of the group responsible for the light-driven proton release in bacteriorhodopsin. Biophys. J. 71, 1011-1023.
17. Govindjee, R., Kono, M., Balashov, S. P., Imasheva, E., Sheves, M., and Ebrey, T. G. (1995) Effect of substitution of tyrosine 57 with asparagine and phenylalanine on the properties of bacteriorhodopsin. Biochemistry 34, 4828-4838.
18. Luecke, H., Schobert, B., Richter, H.-T., Cartailler, J.-P., and Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291, 899-911.
19. Belrhali, H., Nollert, P., Royant, A., Menzel, C., Rosenbusch, J. P., Landau, E. M., and Pebay-Peyroula, E. (1999) Protein, lipid and water organization in bacteriorhodopsin crystals: a moleculear view of the purple membrane at 1.9 Å resolution. Structure 7, 909-917.
20. a calculations suggest storage of an excess proton in a hydrogen-bonded water network in bacteriorhodopsin. J. Mol. Biol. 312, 203-219.
21. Mathias, G., and Marx, D. (2007) Structures and spectral signatures of protonated water networks in bacteriorhodopsin. Proc. Natl. Acad. Sci. U.S.A. 104, 6980-6985.
22. a's of asp-85 and glu204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry 35, 4054-4062.
23. Balashov, S. P., Imasheva, E. S., Givindjee, R., and Ebrey, T. G. (1996) Titration of aspartate-85 in bacteriorhodopsin: What it says about chromophore isomerization and proton release. Biophys. J. 70, 473-481.
24. Váró, G., and Lanyi, J. K. (1991) Kinetics and spectroscopic evidence for an irreversible step between deprotonation and reprotonation of the Schiff base in the bateriorhodopsi photocycle. Biochemistry 30, 5008-5015.
25. 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.
26. -1 region during the bacteriorhodopsin photocycle. Biophys. J. 87, 2676-2682.
27. Garczarek, F., and Gerwert, K. (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439, 109-112.
28. Balashov, S. P., Govindjee, R., and Ebrey, T. (1991) Red shift of the purple membrane absorption band and the deprotonation of tyrosine residues at high pH. Biophys. J. 60, 475-490.
29. Maeda, A., Balashov, S. P., Lugtenburg, J., Verhoeven, M., Herzfeld, J., Belenky, M., Gennis, R. B., Tomson, F. L., and Ebrey, T. G. (2002) Interaction of internal water molecules with the Schiff base in the L intermediate of the bacteriorhodopsin photocycle. Biochemistry 41, 3803-3809.
30. Provencher, S. W., and Vogel, R. H. (1983) Regularization Techniques for Inverse Problems in Molecular Biology, in Numerical Treatment of Inverse Problems in Differential and Integral Equations (Deuflhard, P., and Hairer, E., Eds.) pp304-319, Birkhäuser, Boston, MA.
31. Chizhov, I., Chernavskii, D. S., Engelhard, M., Mueller, K.-H., Zubov, B. V., and Hess, B. (1996) Spectrally silent transitions in the bacteriorhodopsin photocycle. Biophys. J. 71, 2329-2345.
32. Szundi, I., Lewis, J. W., and Kliger, D. S. (1997) Deriving reaction mechanism from kinetic spectroscopy. Application to late rhodopsin intermediates. Biophys. J. 73, 688-702.
33. a increase of the chromophore counterion in bacteriorhodopsin: Implications for ion transport mechanisms of retinal proteins. Biophys. J. 70, 939-947.
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. 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.
36. Hessling, B., Souvignir, G., and Gerwert, K. (1993) A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates. Biophys. J. 65, 1929-1941.
37. Sasaki, J., Lanyi, J. K., Needleman, R., Yoshizawa, T., and Maeda, A. (1994) Complete identification of C=O stretching vibrational bands of protonated aspartic acid residues in the difference infrared spectra of M and N intermediates of bacteriorhodopsin. Biochemistry 33, 3178-3184.
38. Maeda, A., Tomson, F. L., Gennis, R. B., Kandori, H., Ebrey, T. G., and Balashov, S. P. (2000) Relocation of internal bound water in bacteriorhodopsin during the photoreaction of M at low temperature: an FTIR study. Biochemistry 39, 10154-10162.
39. Siebert, F., and Mäntele, W. (1983) Investigation of the primary photochemistry of bacteriorhodopsin by low temperature Fourier-transform infrared spectroscopy. Eur. J. Biochem. 130, 565-573.
40. Maeda, A., Sasaki, J., Pfefferlé, J.-M., Shichida, Y., and Yoshizawa, T. (1991) Fourier transform infrared spectral studies on the Schiff base mode of all-trans bacteriorhodopsin and its photointermediates, K and L. Photochem. Photobiol. 54, 911-921.
41. Smith, S. O., Braiman, M. S., Myers, A. B., Pardoen, J. A., Courtin, J. M. L., Winkel, C., Lugtenburg, J., and Mathies, R. A. (1987) Vibrational analysis of the all-trans-retinal chromophore in light-adapted bacteriorhodopsin. J. Am. Chem. Soc. 109, 3108-3125.
42. McMaster, E., and Lewis, A. (1988) Evidence for light-induced lysine conformational changes during the primary event of the bacteriorhodopsin photocycle. Biochem. Biophys. Res. Commun. 156, 86-91.
43. Gat, Y., Grossjean, M., Pinevsky, I., Takei, H., Rothman, Z., Sigrist, H., Lewis, A., and Sheves, M. (1992) Participation of bacteriorhodopsin active-site lysine backbone in vibrations associated with retinal photochemistry. Proc. Natl. Acad. Sci. U.S.A. 89, 2434-2438.
44. Yamazaki, Y., Kandori, H., Needleman, R., Lanyi, J. K., and Maeda, A. (1998) Interaction of the protonated Schiff base with the peptide backbone of valine 49 and the intervening water molecule in the N photointermediate of bacteriorhodopsin. Biochemistry 37, 1559-1564.
45. Hatanaka, M., Sasaki, J., Kandori, H., Ebrey, T. G., Needleman, R., Lanyi, J. K., and Maeda, A. (1995) Effects of arginine-82 on the interactions of internal water molecules in bacteriorhodopsin. Biochemistry 35, 6308-6312.
46. Wang, J., and El-Sayed, M. A. (2000) Proton polarizability of hydrogen-bonded network and its role in proton transfer in bacteriorhodopsin. J. Phys. Chem. A 104, 4333-4337.
47. Zundel, G. (2000) Hydrogen bonds with large proton polarizability and proton transfer processes in electrochemistry and biology. Adv. Chem. Phys. 111, 1-217.
48. 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.
49. Brown, L. S., Needleman, R., and Lanyi, J. K. (2000) Origins of deuterium kinetic isotope effects on the proton transfers of the bacteriorhodopsin photocycle. Biochemistry 39, 938-945.
50. Luecke, H., Schobert, B., Richter, H.-T., Cartailler, J.-P., and Lanyi, J. K. (1999) Structural changes in bacteriorhodopsin during ion transport at 2 angstrom resolution. Science 286, 255-260.
51. Takei, H., Gat, Y., Rothman, Z., Lewis, A., and Sheves, M. (1994) Active site lysine backbone undergoes conformational changes in the bacteriorhodopsin photocycle. J. Biol. Chem. 269, 7387-7389.
52. Luecke, H., Schobert, B., Cartailler, J.-P., Richter, H.-T., Rosengarth, A., Needleman, R., and Lanyi, J. K. (2000) Coupling photoisomerization of retinal to directional transport in bacteriorhodopsin. J. Mol. Biol. 300, 1237-1255.
53. Takeda, K., Matsui, Y., Kamiya, N., Adachi, S., Okumura, H., and Kouyama, T. (2004) Crystal structure of the M intermediate of bacteriorhodopsin: Allosteric structural changes mediated by sliding movement of a transmembrane helix. J. Mol. Biol. 341, 1023-1037.
54. Barth, A., and Zscherp, C. (2002) What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430.
55. Liu, X.-M., Sonar, S., Lee, C.-P., Coleman, M., RajBhandary, U. L., and Rothschild, K. J. (1995) Site-directed isotope labeling and FTIR spectroscopy: assignment of tyrosine bands in the bR → M difference spectrum of bacteriorhodopsin. Biophys. Chem. 56, 63-70.
56. Rothschild, K. J., Roepe, P., Ahl, P. L., Earnest, T. N., Bogomolni, R. A., Das Gupta, S. K., Mulliken, C. M., and Herzfeld, J. (1986) Evidence for a tyrosine protonation change during the primary phototransition of bacteriorhodopsin at low temperature. Proc. Natl. Acad. Sci. U.S.A. 83, 347-351.
57. Sonar, S., Marti, T., Rath, P., Fischer, W., Coleman, M., Nilsson, A., Khorana, H. G., and Rothschild, K. J. (1994) A predicted proton pathway in the bacteriorhodopsin mutant Tyr57→ Asp. J. Biol. Chem. 269, 28851-28858.
58. Sudo, Y., and Spudich, J. L. (2006) Three strategically placed hydrogen-bonding residues convert a proton pump into sensory receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 116129-16134.
59. DeLano, W. (2002) PYMOL, DeLano Scientific, San Carlos, CA).