Glutamic Acid Residues of Bacteriorhodopsin at the Extracellular Surface as Determinants for Conformation and Dynamics as Revealed by Site-Directed Solid-State 13C NMR

Biophysical Journal

Volumn 86, Issue 3, 2004, Pages 1673-1681

  Saitô, Hazime ^a   Yamaguchi, Satoru ^a   Ogawa, Keiji ^a   Tuzi, Satoru ^a   Márquez, Mercedes ^b   Sanz, Carolina ^b   Padrós, Esteve ^b  

^a UNIVERSITY OF HYOGO   (Japan)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; BACTERIORHODOPSIN; CARBON 13; GLUTAMIC ACID; MEMBRANE PROTEIN; VALINE;

ARTICLE; BACTERIAL MEMBRANE; CARBON NUCLEAR MAGNETIC RESONANCE; HALOBACTERIUM SALINARUM; ISOTOPE LABELING; MUTANT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PURPLE MEMBRANE;

BACTERIA (MICROORGANISMS); HALOBACTERIUM SALINARUM;

EID: 1542315401     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74236-8     Document Type: Article

References (53)

1. Ariki, M., and J. K. Lanyi. 1986. Characterization of metal ion-binding sites in bacteriorhodopsin. J. Biol. Chem. 261:8167-8174.
2. 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.
3. Bloembergen, N. 1957. Proton relaxation times in paramagnetic solutions. J. Chem. Phys. 27:572-573.
4. Brown, L. S., Y. Gat, M. Sheves, Y. Yamazaki, A. Maeda, R. Needleman, and J. K. Lanyi. 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.
5. Brown, L. S., R. Needleman, and J. K. Lanyi. 1999. Functional roles of aspartic acid residues at the cytoplasmic surface of bacteriorhodopsin. Biochemistry. 38:6855-6861.
6. 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.
7. Chang, C. H., J. G. Chen, R. Govindjee, and T. Ebrey. 1985. Cation binding by bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 82:396-400.
8. Checover, S., Y. Marantz, E. Nachliel, M. Gutman, M. Pfeffer, J. Tittor, D. Oesterhelt, and N. A. Dencher. 2001. Dynamics of the proton transfer reaction on the cytoplasmic surface of bacteriorhodopsin. Biochemistry. 40:4281-4292.
9. Checover, S., E. Nachliel, N. A. Dencher, and M. Gutman. 1997. Mechanism of proton entry into the cytoplasmic section of the proton-conducting channel of bacteriorhodopsin. Biochemistry. 40:4281-4292.
10. Dencher, N. A., K.-D. Kohl, and M. P. Heyn. 1983. Photochemical cycle and light-dark adaptation of monomeric and aggregated bacteriorhodopsin in various lipid environments. Biochemistry. 22:1323-1334.
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. Eliash, T., L. Weiner, M. Ottolenghi, and M. Sheves. 2001. Specific binding sites for cations in bacteriorhodopsin. Biophys. J. 81:1155-1162.
13. Fu, X., M. Blesser, M. Ottoleghi, T. Eliash, N. Friedman, and M. Sheves. 1997. Titration kinetics of Asp-85 in bacteriorhodopsin: exclusion of the retinal pocket as the color-controlling cation binding site. FEBS Lett. 416:167-170.
14. 13C NMR. Biochemistry. 39:14472-14480.
15. Kusnetzow, A., D. L. Singh, C. H. Martin, I. L. Barani, and R. R. Birge. 1999. Nature of chromophore binding site of bacteriorhodopsin: the potential role of Arg82 as a principal counterion. Biophys. J. 76:2370-2389.
16. Lanyi, J. K. 1993. Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim. Biophys. Acta. 1183:241-261.
17. Lanyi, J. K. 1997. Mechanism of ion transport across membranes. bacteriorhodopsin as a prototype for proton pumps. J. Biol. Chem. 272:31209-31212.
18. 85 at alkaline pH in the photocycle of bacteriorhodopsin mutants containing E194Q. Biophys. J. 78:2022-2030.
19. Luecke, H., H. T. Richter, and J. K. Lanyi. 1998. Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. Science. 280:1934-1937.
20. Mathies, P. A., S. W. Lin, J. B. Ames, and W. T. Pollard. 1991. From femoseconds to biology: mechanism of bacteriorhodopsin's light-driven proton pump. Annu. Rev. Biophys. Biophys. Chem. 20:491-518.
21. 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.
22. Onishi, H., E. M. McCance, and N. E. Gibbons. 1965. A synthetic medium for extremely halophilic bacteria. Can. J. Microbiol. 11:365-373.
23. Ovchinnikov, Y. A. 1982. Rhodopsin and bacteriorhodopsin: structure-function relationships. FEBS Lett. 148:179-191.
24. Riesle, J., D. Oesterhelt, N. A. Dencher, and J. Heberle. 1996. D38 is an essential part of the proton translocation pathway in bacteriorhodopsin. Biochemistry. 35:6635-6643.
25. Rothwell, W. P., and J. S. Waugh. 1981. Transverse relaxation of dipolar coupled spin systems under rf irradiation: detecting motions in solid. J. Chem. Phys. 74:2721-2732.
26. 13C chemical shifts: a new means of conformational characterization as obtained by high-resolution solid-state NMR. Magn. Reson. Chem. 24:835-852.
27. Saitô, H., and I. Ando. 1989. High-resolution solid-state NMR studies of synthetic and biological macromolecules. Annu. Rep. NMR Spectrosc. 21:209-290.
28. Saitô, H., S. Tuzi, and A. Naito. 1998. Empirical versus nonempirical evaluation of secondary structure of fibrous and membrane protein by solid-state NMR: a practical approach. Annu. Rep. NMR Spectrosc. 36:79-121.
29. 13C NMR. Biochim. Biophys. Acta. 1460:39-48.
30. 13C NMR: lessons from bacteriorhodopsin as an intact protein. Annu. Rep. NMR Spectrosc. 47:39-108.
31. 13C NMR. Biochim. Biophys. Acta. 1565:97-106.
32. 13C NMR: conformational elucidation, surface dynamics and information transfer from the surface to inner residues. Spectrosc. Int. J. 16:107-120.
33. 13C]amino-acid residues. Magn. Reson. Chem. 4:218-230.
34. 13C] Val-labeled bacteriorhodopsin. Biochim. Biophys. Acta 1616:127-136.
35. Sanz, C., T. 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. 4556:191-195.
36. Sanz, C., M. Márquez, A. Perálvarez, S. Elouatik, F. Sepulcre, E. Querol, T. Lazarova, and E. Padrós. 2001. Contribution of extracellular Glu residues to the structure and function of bacteriorhodopsin. Presence of specific cation-binding sites. J. Biol. Chem. 276:40788-40794.
37. Solomon, I. 1955. Relaxation processes in a system of two spins. Phys. Rev. 99:559-565.
38. Stoeckenius, W., and R. A. Bogomolni. 1982. Bacteriorhodopsin and related pigments of halobacteria. Annu. Rev. Biochem. 52:587-616.
39. Suwelack, D., W. P. Rothwell, and J. S. Waugh. 1980. Slow molecular motion detected in the NMR spectra of rotating solids. J. Chem. Phys. 73:2559-2569.
40. Szundi, L., and W. Stoeckenius. 1987. Effect of lipid surface charges on the purple-to-blue transition of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 84:3681-3684.
41. Szundi, L., and W. Stoeckenius. 1989. Surface pH controls purple-to-blue transition of bacteriorhodopsin. Biophys. J. 56:369-383.
42. 13C]Ala-labeled protein: Arg82 may function as an information mediator. Biophys. J. 77:1577-1584.
43. 2+ ion. Biophys. J. 81:425-434.
44. 13C]Leu and Val-labelled bacteriorhodopsin. Conformation and dynamics of transmembrane helices, loop and termini, and hydration-induced conformational change. Eur. J. Biochem. 218:837-844.
45. 13C NMR. J. Mol. Struct. 654:205-214.
46. 13C nuclear magnetic resonance. Biochemistry. 35:7520-7527.
47. 13C NMR. Biophys. J. 76:1523-1531.
48. 13C NMR. J. Biochem. (Tokyo). 127:861-869.
49. 13CAla-labeled proteins: detection of millisecond or microsecond motions in interhelical loops and C-terminal α-helix. J. Biochem. (Tokyo). 129:373-382.
50. 13C-NMR. Eur. J. Biochem. 268:2218-2228.
51. Yamazaki, Y., M. Hatanaka, H. Kandori, J. Sasaki, W. F. Karsten, J. Raap, J. Lugtenburg, M. Bizounok, J. Herzfeld, R. Needleman, and J. K. Lanyi. 1995. Interaction of tryptophan-182 with the retinal 9-methyl group in the L intermediate of bacteriorhodopsin. Biochemistry. 34:7088-7093.
52. Yamazaki, Y., S. Tuzi, H. Saitô, H. Kandori, R. Needleman, J. K. Lanyi, and A. Maeda. 1996. Water structural changes at the proton uptake site (the Thr46-Asp96 domain) in the L-intermediate of bacteriorhodopsin. Biochemistry. 35:4063-4068.
53. 13C NMR. Eur. Biophys. J. 32:1-11.