Relocation of water molecules between the Schiff base and the Thr46-Asp96 region during light-driven unidirectional proton transport by bacteriorhodopsin: An FTIR study of the N intermediate

Biochemistry

Volumn 44, Issue 16, 2005, Pages 5960-5968

  Maeda, Akio ^a,b   Gennis, Robert B ^a   Balashov, Sergei P ^c   Ebrey, Thomas G ^b  

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

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOURIER TRANSFORM INFRARED SPECTROSCOPY; MOLECULAR VIBRATIONS; PROTEINS; PROTONS; WATER;

BACTERIORHODOPSIN; PROTON TRANSFER; WATER MOLECULES; WATER VIBRATION;

BACTERIA;

ASPARTIC ACID; BACTERIORHODOPSIN; PROTON PUMP; SCHIFF BASE; THREONINE; WATER;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; MOLECULAR INTERACTION; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STABILITY; PROTON TRANSPORT; VIBRATION;

AMINO ACID SUBSTITUTION; BACTERIORHODOPSINS; CRYSTALLOGRAPHY, X-RAY; HALOBACTERIUM SALINARUM; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTAGENESIS, SITE-DIRECTED; PHOTOCHEMISTRY; PROTEIN CONFORMATION; PROTONS; SCHIFF BASES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; WATER;

EID: 17644426679     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047469h     Document Type: Article

References (43)

1. 15 s-trans retinal chromophore, Proc. Natl. Acad. Sci. U.S.A. 85, 2156-2160.
2. 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.
3. Maeda, A., Sasaki, J., Shichida, Y., Yoshizawa, T., Chang, M., Ni, B., Needleman, R., and Lanyi, J. K. (1992) Structures of Asp-96 in the L and N intermediates of bacteriorhodopsin: Analysis by Fourier transform infrared spectroscopy, Biochemistry 31, 4684-4690.
4. a of the chromophore's Schiff base can restore its light-induced deprotnation in the inactive Tyr-57→Asn mutant of bacteriorhodopsin, J. Biol. Chem. 269, 14353-14354.
5. a increase of the chromophore counterion in bacteriorhodopsin: Implication for ion transport mechanism of retinal proteins, Biophys. J. 70, 939-947.
6. Váró, G., and Lanyi, J. K. (1991) Thermodynamics and energy coupling in the bacteriorhodopsin photocycle, Biochemistry 30, 5016-5022,
7. 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.
8. Yamazaki, Y., Hatanaka, M., Kandori, H., Sasaki, J., Karstens, W. F. J., Raap, J., Lugtenburg, J., Bizounok, M., Herzfeld, J., Needleman, R., Lanyi, J. K., and Maeda, A. (1995) Water structural changes at the proton uptake site (the Thr46-Asp96 domain) in the L intermediate of bacteriorhodopsin, Biochemistry 34, 7088-7093.
9. Maeda, A., Balashov, S. P., Lugtenburg, J., Verhoeven, M. A., 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.
10. 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.
11. Maeda, A. (2001) Internal water molecules as mobile polar groups for light-induced proton translocation in bacteriorhodopsin and rhodopsin as studied by difference FTIR spectroscopy, Biochemsitry (Moscow) 66, 1256-1268.
12. Maeda, A., Sasaki, J., Shichida, Y., and Yoshizawa, T. (1992) Water structural changes in the bacteriorhodopsin photocycle: Analysis by Fourier-transform infrared spectroscopy, Biochemistry 31, 462-467.
13. Maeda, A., Herzfeld, J., Belenky, M., Needleman, R., Gennis, R. B., Balashov, S. P., and Ebrey, T. G. (2003) Water-mediated hydrogen-bonded network on the cytoplasmic side of the Schiff base of the L photointermediate of bacteriorhodopsin, Biochemistry 42, 14122-14129.
14. Maeda, A., Tomson, F. L. Gennis, R. B., Ebrey, T. G., and Balashov, S. P. (1999) Chromophore-protein-water interactions in the L intermediate of bacteriorhodopsin: FTIR study of the photoreaction of L at 80 K, Biochemistry 38, 8800-8807.
15. Maeda, A., Tomson, F. L., Gennis, R. B., Balashov, S. P., and Ebrey, T. G. (2003) Water molecule rearrangements around Leu93 and Trp182 in the formation of the L intermediate in bacteriorhodopsin's photocycle, Biochemistry 42, 2535-2541.
16. Kouyama, T., Nishikawa, T., Tokuhisa, T., and Okumura, H. (2004) Crystal structure of the L intermediate of bacteriorhodopsin: Evidence for vertical translocation of a water molecule during the proton pumping cycle, J. Mol. Biol. 335, 531-546.
17. Fodor, S. P. A., Ames, J. B., Gebhard, R., van den Berg, E. M. M., Stoeckenius, W., Lugtenburg, J., and Mathies, R. (1988) Chromophore structure in bacteriorhodopsin's N intermediate: implication for the proton pumping mechanism, Biochemistry 27, 7097-7101.
18. 13N NMR investigations of the N intermediate of bacteriorhodopsin, Biochemistry 33, 8853-8857.
19. Balashov, S. P., Lu, M., Imasheva, E. S., Govindjee, R., Ebrey, T. G., Othersen, B., III, Chen, Y., Crouch, R. K., and Menick, D. R. (1999) The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH, Biochemistry 38, 2026-2039.
20. 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.
21. a of the retinal Schiff base during the photocycle of bacteriorhodopsin, Proc. Natl. Acad. Sci. U.S.A. 93, 1731-1734.
22. Schobert, B., Brown, L. S., and Lanyi, J. K. (2003) Crystallographic structures of the M and N intermediates of bacteriorhodopsin: Assembly of a hydrogen-bonded chain of water molecules between Asp-96 and the retinal Schiff base, J. Mol. Biol. 330, 553-570.
23. 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.
24. Balashov, S. P., Imasheva, E. S., Litvin, F. F., and Lozier, R. H. (1990) The N intermediate of bacteriorhodopsin at low temperatures, FEBS Lett. 271, 93-96.
25. Balashov, S. P., Imasheva, E. S., Karneyeva, N. V., Litvin, F. F., and Ebrey, T. G. (1992) in Structures and Functions of Retinal Proteins (Rigaud, J. L., Ed.) p 119, John Libbey Eurotext Ltd., Paris.
26. Brown, L. S., Gat, Y., Sheves, M., Yamazaki, Y., Maeda, A., Needleman, R., and Lanyi, J. K. (1994) The retinal Schiff base-counterion complex of bacteriorhodopsin: Changed geometry during the photocycle is a cause of proton transfer to aspartate 85, Biochemistry 33, 12001-12011.
27. Yamazaki, Y., Tuzi, S., Saitô, H., Kandori, H., Needleman, R., Lanyi, J. K., and Maeda, A. (1996) Hydrogen bonds of water and C=O groups coordinate long-range structural changes in the L photointermediate of bacteriorhodopsin, Biochemistry 35, 4063-4068.
28. Pfefferlé, J.-M., Maeda, A., Sasaki, J., and Yoshizawa, T. (1991) Fourier transform infrared study of the N intermediate of bacteriorhodopsin, Biochemistry 30, 6548-6556.
29. Ormos, P., Chu, K., and Mourant, J. (1992) Infrared study of the L, M, and N intermediates of bacteriorhodopsin using the photoreaction of M, Biochemistry 31, 6933-6937.
30. Weidlich, O., and Siebert, F. (1993) Time-resolved step-scan FTIR investigations of the transition from KL to L in the bacteriorhodopsin photocycle: Idnetification of chromophore twist by assigning hydrogen-out-of-plane (HOOP) bending vibrations, Appl. Spectrosc. 47, 1394-1399.
31. Maeda, A. (1995) Application of FTIR spectroscopy to the structural study on the function of bacteriorhodopsin, Isr. J. Chem. 35, 387-400.
32. Dioumaev, A. K., Brown, L. S., Needleman, R., and Lanyi, J. K. (2001) Coupling of the reisomerization of the retinal, proton uptake, and reprotonation of Asp-96 in the N intermediate of bacteriorhodopsin, Biochemistry 40, 11308-11317.
33. Gerwert, K., and Siebert, F. (1986) Evidence for light-induced 13-cis, 14-s-cis isomerization in bacteriorhodopsin obtained by FTIR difference spectroscopy using isotopically labelled retinals, EMBO J. 5, 805-811.
34. Lanyi, J. (2004) What is the real crystallographic structure of the L photointermediate of Bacteriorhodopsin?, Biochim. Biophys. Acta 1658, 14-22
35. 2′ intermediates of the photocycle, J. Mol. Biol. 328, 439-450.
36. Edman, K., Royant, A., Larsson, G., Jacobson, F., Taylor, T., van der Spoel, D., Landau, E. M., Pebay-Peyroula, E., and Neutze, R. (2004) Deformation of helix C in the low temperature L-intermediate of bacteriorhodopsin, J. Biol. Chem. 279, 2147-2158.
37. Yamazaki, Y., Sasaki, J., Hatanaka, M., Kandori, H., Maeda, A., Needleman, R., Shinada, T., Yoshihara, K., Brown, L. S., and Lanyi, J. K. (1995) Interaction of tryptophan-182 with the retinal 9-methyl group in the L intermediate of bacteriorhodopsin, Biochemistry 34, 977-982.
38. 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.
39. Friedman, R., Nachiel, E., and Gutman, M. (2003) The role of small intraprotein cavities in the catalytic cycle of bacteriorhodopsin, Biophys. J. 85, 886-896.
40. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin, Biochim. Biophys. Acta 1460, 177-191.
41. Facciotti, M. T., Rouhani, S., Burkard, F. T., Betancourt, F. M., Downing, K. H., Rose, R. B., McDermott, G., and Glaeser, R. M. (2001) Structure of an early intermediate in the M-state phase of the bacteriorhodopsin photocycle, Biophys. J. 81, 3422-3455.
42. Sass, H. J., Büldt, G., Gessenich, R., Hehn, D., Neff, D., Schlessinger, R., Berendzen, J., and Ormos, P. (2000) Structural alterations fro proton translocation in the M state of wild-type bacteriorhodopsin, Nature 406, 549-653.
43. 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.