Structure of the bacteriorhodopsin mutant F219L N intermediate revealed by electron crystallography

EMBO Journal

Volumn 19, Issue 10, 2000, Pages 2152-2160

  Vonck, Janet ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Bacteriorhodopsin; Conformational change; Electron crystallography; Proton pump; Trapped intermediates

Indexed keywords

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

CELL MEMBRANE; CONFORMATIONAL TRANSITION; CRYSTALLOGRAPHY; CYTOPLASM; HALOBACTERIUM; ISOMERISM; PRIORITY JOURNAL; PROTEIN STRUCTURE; PURPLE MEMBRANE; REVIEW;

BACTERIA (MICROORGANISMS); HALOBACTERIA; HALOBACTERIUM;

EID: 0034658269     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.10.2152     Document Type: Review

References (60)

1. Ames, J.B. and Mathies, R.A. (1990) The role of back-reactions and proton uptake during the N to O transition in bacteriorhodopsin's photocycle: a kinetic resonance Raman study. Biochemistry, 29, 7181-7190.
2. Baldwin, J.M. and Henderson, R. (1984) Measurement and evaluation of electron diffraction patterns from two-dimensional crystals. Ultramicroscopy, 14, 319-336.
3. 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 molecular view of the purple membrane at 1.9 Å resolution. Structure, 7, 909-917.
4. Booy, F.P. and Pawley, J.B. (1993) Cryo-crinkling: what happens to carbon films on copper grids at low temperature. Ultramicroscopy, 48, 273-280.
5. Brown, L.S., Yamazaki, Y., Maeda, A., Sun, L., Needleman, R. and Lanyi, J.K. (1994) The proton transfers in the cytoplasmic domain of bacteriorhodopsin are facilitated by a cluster of interacting residues. J. Mol. Biol., 239, 401-414.
6. Bullough, P.A. and Henderson, R. (1999) The projection structure of the low temperature K intermediate of the bacteriorhodopsin photocycle determined by electron diffraction. J. Mol. Biol., 286, 1663-1671.
7. Cao, Y., Váró, G., Chang, M., Ni, B., Needleman, R. and Lanyi, J.K. (1991) Water is required for proton transfer from aspartate-96 to the bacteriorhodopsin Schiff base. Biochemistry, 30, 10972-10979.
8. a of Asp-96 which follows a protein backbone conformational change. Biochemistry, 31, 1981-1990.
9. Ceska, T.A. and Henderson, R. (1990) Analysis of high-resolution electron diffraction patterns from purple membrane labelled with heavy-atoms. J. Mol. Biol., 213, 539-560.
10. Dencher, N.A., Dresselhaus, D., Zaccai, G. and Büldt, G. (1989) Structural changes in bacteriorhodopsin during proton translocation revealed by neutron diffraction. Proc. Natl Acad. Sci. USA, 86, 7876-7879.
11. Edman, K., Nollert, P., Royant, A., Belrhali, H., Pebay-Peyroula E., Hajdu, J., Neutze, R. and Landau, E.M. (1999) High-resolution X-ray structure of an early intermediate in the bacteriorhodopsin photocycle. Nature, 401, 822-826.
12. Esnouf, R.M. (1997) An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J. Mol. Graph. Model., 15, 132-134.
13. Esnouf, R.M. (1999) Further additions to MolScript version 1.4. including reading and contouring of electron-density maps. Acta Crystallogr. D, 55, 938-940.
14. Essen, L.O., Siegert, R., Lehmann, W.D. and Oesterhelt, D. (1998) Lipid patches in membrane protein oligomers - crystal structure of the bacteriorhodopsin-lipid complex. Proc. Natl Acad. Sci. USA, 95, 11673-11678.
15. Fukuda, K. and Kouyama, T. (1992) Photoreaction of bacteriorhodopsin at high pH: origins of the slow decay component of M. Biochemistry, 31, 11740-11747.
16. Glaeser, R.M. and Downing, K.H. (1990) The 'specimen flatness' problem in high-resolution electron crystallography of biological macromolecules. In Peachy, L.D. and Williams, D.B. (eds). XIIth International Congress for Electron Microscopy. San Francisco Press, Inc., Seattle, WA, Vol. 1, pp. 98-99.
17. Grigorieff, N., Ceska, T.A., Downing, K.H., Baldwin, J.M. and Henderson, R. (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol., 259, 393-421.
18. Han, B.-G., Vonck, J. and Glaeser, R.M. (1994a) The bacteriorhodopsin photocycle: direct structural study of two substates of the M-intermediate. Biophys. J., 67, 1179-1186.
19. Han, B.-G., Wolf, S.G., Vonck, J. and Glaeser, R.M. (1994b) Specimen flatness in electron crystallography of glucose-embedded biological materials is significantly affected by the choice of carbon evaporation stock. Ultramicroscopy, 55, 1-5.
20. Haupts, U., Tittor, J. and Oesterhelt, D. (1999) Closing in on bacteriorhodopsin: progress in understanding the photocycle. Annu. Rev. Biophys. Biomol. Struct., 28, 367-399.
21. Hauss, T., Büldt, G., Heyn, M.P. and Dencher, N.A. (1994) Light-induced isomerization causes an increase in the chromophore tilt in the M intermediate of bacteriorhodopsin: a neutron diffraction study. Proc. Natl Acad. Sci. USA, 91, 11854-11858.
22. Henderson, R., Baldwin, J.M., Ceska, T.A., Zemlin, F., Beckmann, E. and Downing, K.H. (1990) A model for the structure of bacteriorhodopsin based on high resolution electron cryomicroscopy. J. Mol. Biol., 213, 899-929.
23. Hendler, R.W., Dancsházy, Z., Bose, S., Shrager, R.I. and Tokaji, Z. (1994) Influence of excitation energy on the bacteriorhodopsin photocycle. Biochemistry, 33, 4604-4610.
24. Hendrickson, F.M., Burkard, F. and Glaeser, R.M. (1998) Structural characterization of the L-to-M transition of the bacteriorhodopsin photocycle. Biophys. J., 75, 1446-1454.
25. Jones, T.A. and Kjeldgaard, M. (1993) O - The Manual. Uppsala University, Uppsala, Sweden.
26. Kamikubo, H., Kataoka, M., Váró, G., Oka, T., Tokunaga, F., Needleman, R. and Lanyi, J.K. (1996) Structure of the N intermediate of bacteriorhodopsin revealed by X-ray diffraction. Proc. Natl Acad. Sci. USA, 93, 1386-1390.
27. Kamikubo, H., Oka, T., Imamoto, Y., Tokunaga, F., Lanyi, J.K. and Kataoka, M. (1997) The last phase of the reprotonation switch in bacteriorhodopsin: the transition between the M-type and the N-type protein conformation depends on hydration. Biochemistry, 36, 12282-12287.
28. Kataoka, M., Kamikubo, H., Tokunaga, F., Brown, L.S., Yamazaki, Y., Maeda, A., Sheves, M., Needleman, R. and Lanyi, J.K. (1994) Energy coupling in an ion pump. The reprotonation switch of bacteriorhodopsin. J. Mol. Biol., 243, 621-638.
29. Kimura, Y., Vassylyev, D.G., Miyazawa, A., Kidera, A., Matsushima, M., Mitsuoka, K., Murata, K., Hirai, T. and Fujiyoshi, Y. (1997) Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature, 389, 206-211.
30. Koch, M.H.J., Dencher, N.A., Oesterhelt, D., Plöhn, H.-J., Rapp, G. and Büldt, G. (1991) Time-resolved X-ray diffraction study of structural changes associated with the photocycle of bacteriorhodopsin. EMBO J., 10, 521-526.
31. Korenstein, R., Hess, B. and Markus, M. (1979) Cooperativity in the photocycle of purple membrane of Halobacterium halobium with a mechanism of free energy transduction. FEBS Lett., 102, 155-161.
32. Kouyama, T. and Nasuda-Kouyama, A. (1989) Turnover rate of the proton pumping cycle of bacteriorhodopsin: pH and light-intensity dependences. Biochemistry, 28, 5963-5970.
33. 350) at high pH and its M-like photoproduct. Biochemistry, 27, 5855-5863.
34. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
35. Lanyi, J.K. (1998) Understanding structure and function in the light-driven proton pump bacteriorhodopsin. J. Struct. Biol., 124, 164-178.
36. Lindahl, M. and Henderson, R. (1997) Structure of the bacteriorhodopsin D85N/D96N double mutant showing substantial structural changes and a highly twinned, disordered lattice. Ultramicroscopy, 70, 95-106.
37. Luecke, H., Richter, H.-T. and Lanyi, J.K. (1998) Proton transfer pathways in bacteriorhodopsin at 2.3 Å resolution. Science, 280, 1934-1937.
38. Luecke, H., Schobert, B., Richter, H.T., Cartailler, J.P. and Lanyi, J.K. (1999a) Structural changes in bacteriorhodopsin during ion transport at 2 Å resolution. Science, 286, 255-260.
39. Luecke, H., Schobert, B., Richter, H.T., Cartailler, J.P. and Lanyi, J.K. (1999b) Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol., 291, 899-911.
40. Merritt, E.A. and Bacon, D.J. (1997) Raster3D: photorealistic molecular graphics. Methods Enzymol., 277, 505-524.
41. Mitsuoka, K., Hirai, T., Murata, K., Miyazawa, A., Kidera, A., Kimura, Y. and Fujiyoshi, Y. (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.
42. Mukhopadhyay, A.K., Bose, S. and Hendler, R.W. (1994) Membrane-mediated control of the bacteriorhodopsin photocycle. Biochemistry, 33, 10889-10895.
43. Nakasako, M., Kataoka, M., Amemiya, Y. and Tokunaga, F. (1991) Crystallographic characterization by X-ray diffraction of the M-intermediate from the photocycle of bacteriorhodopsin at room temperature. FEBS Lett., 292, 73-75.
44. Otto, H., Marti, T., Holz, M., Mogi, T., Lindau, M., Khorana, H.G. and Heyn, M.P. (1989) Aspartic acid-96 is the internal proton donor in the reprotonation of the Schiff base of bacteriorhodopsin. Proc. Natl Acad. Sci. USA, 86, 9228-9232.
45. Pebay-Peyroula, E., Rummel, G., Rosenbusch, J.P. and Landau, E.M. (1997) X-ray structure of bacteriorhodopsin at 2.5 Å from microcrystals grown in lipidic cubic phases. Science, 277, 1676-1681.
46. Perkins, G.A., Burkard, F., Liu, E. and Glaeser, R.M. (1993) Glucose alone does not completely hydrate bacteriorhodopsin in glucose-embedded purple membrane. J. Microsc., 169, 61-65.
47. Radionov, A.N. and Kaulen, A.D. (1995) Cooperative phenomena in the photocycle of D96N mutant bacteriorhodopsin. FEBS Lett., 377, 330-332.
48. Rothschild, K.J. (1992) FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model. J. Bioenerg. Biomembr., 24, 147-167.
49. Rothschild, K.J., Braiman, M.S., He, Y.-W., Marti, T. and Khorana, H.G. (1990) Vibrational spectroscopy of bacteriorhodopsin mutants. Evidence for the interaction of aspartic acid 212 with tyrosine 185 and possible role in the proton pump mechanism. J. Biol. Chem., 265, 16985-16991.
50. N intermediate with unprotonated Schiff base but N-like protein structure. J. Biol. Chem., 267, 20782-20786.
51. Sass, H.J., Schachowa, I.W., Rapp, G., Koch, M.H.J., Oesterhelt, D., Dencher, N.A. and Büldt, G. (1997) The tertiary structural changes in bacteriorhodopsin occur between M states: X-ray diffraction and Fourier transform infrared spectroscopy. EMBO J., 16, 1484-1491.
52. Shrager, R.I., Hendler, R.W. and Bose, S. (1995) The ability of actinic light to modify the bacteriorhodopsin photocycle. Heterogeneity or photocooperativity? Eur. J. Biochem., 229, 589-595.
53. Subramaniam, S., Gerstein, M., Oesterhelt, D. and Henderson, R. (1993) Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J., 8, 1-12.
54. Subramaniam, S., Lindahl, M., Bullough, P., Faruqi, A.R., Tittor, J., Oesterhelt, D., Brown, L., Lanyi, J. and Henderson, R. (1999) Protein conformational changes in the bacteriorhodopsin photocycle. J. Mol. Biol. 287, 145-161.
55. Tokaji, Z. (1998) Quantitative model for the cooperative interaction of the bacteriorhodopsin molecules in purple membrane. FEBS Lett., 423, 343-346.
56. Tokaji, Z. and Dancsházy, Z. (1991) Light-induced, long-lived perturbation of the photocycle of bacteriorhodopsin. FEBS Lett., 281, 170-172.
57. Váró, G., Needleman, R. and Lanyi, J.K. (1996) Protein structural change at the cytoplasmic surface as the cause of cooperatively in the hacteriorhodopsin photocycle. Biophys. J., 70, 461-467.
58. Vonck, J. (1996) A three-dimensional difference map of the N intermediate in the bacteriorhodopsin photocycle: part of the F helix tilts in the M to N transition. Biochemistry, 35, 5870-5878.
59. Weik, M., Zaccai, G., Dencher, N.A., Oesterhelt, D. and Hauss, T. (1998) Structure and hydration of the M-state of the bacteriorhodopsin mutant D96N studied by neutron diffraction. J. Mol. Biol., 275, 625-634.
60. 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.