Structure and hydration of the M-state of the bacteriorhodopsin mutant D96N studied by neutron diffraction

Journal of Molecular Biology

Volumn 275, Issue 4, 1998, Pages 625-634

  Weik, M ^a   Zaccai, G ^a,b   Dencher, N A ^c   Oesterhelt, D ^d   Hauss T ^c,e  

^a CEA GRENOBLE   (France)

^b INSTITUT LAUE LANGEVIN   (France)

^c DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e HAHN MEITNER INSTITUT   (Germany)

Author keywords

Bacteriorhodopsin; Neutron diffraction; Photocycle; Purple membrane; Water

Indexed keywords

BACTERIORHODOPSIN; HYDROGEN; MUTANT PROTEIN; SCHIFF BASE; WATER;

ARTICLE; DIFFRACTION; HUMIDITY; HYDRATION; MEMBRANE; NEUTRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; PURPLE MEMBRANE;

EID: 0032579445     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1488     Document Type: Article

References (44)

1. Bevington, P. R. (1969). Data Reduction and Error Analysis for the Physical Sciences, McGraw-Hill, New York.
2. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S. & Karplus, M. (1983). CHARMM: A program for macromolecular energy minimization and dynamics calculations. J. Comput. Chem. 4, 187-217.
3. Brown, L. S., Váró, G., Needleman, R. & Lanyi, J. K. (1995). Functional significance of a protein conformation change at the cytoplasmic end of helix F during the bacteriorhodopsin photocycle. Biophys. J. 69, 2103-2111.
4. Cao, Y., Váró, G., Chang, M., Ni, B., Needleman, R. & Lanyi, J. K. (1991). Water is required for the proton transfer from aspartate-96 to the bacteriorhodopsin Schiff base. Biochemistry, 30, 10972-10979.
5. Dencher, N. A., Dresselhaus, D., Zaccai, G. & Büldt, G. (1989). Structural changes in bacteriorhodopsin during proton translocation revealed by neutron diffraction. Proc. Natl Acad. Sci. USA, 86, 7876-7879.
6. Dencher, N. A., Heberle, J., Büldt, G., Höltje, H.-D. & Höltje, M. (1992). Active and passive proton transfer steps through bacteriorhodopsin are controlled by a light-triggered hydrophobia gate. In Structure and Functions of Retinal Proteins (Rigaud, J. L., ed.), pp. 213-216, John Libbey Eurotext.
7. Ferrand, M., Zaccai, G., Nina, M., Smith, J., Etchbest, C. & Roux, B. (1993). Structure and dynamics of bacteriorhodopsin. Comparison of simulation and experiment. FEBS Letters, 327, 256-260.
8. Glaeser, R. M., Baldwin, J., Ceska, T. A. & Henderson, R. (1986). Electron diffraction analysis of the M412 intermediate of bacteriorhodopsin. Biophys. J. 50, 913-920.
9. Grigorieff, N., Beckman, E. & Zemlin, F. (1995). Lipid location in deoxycholate-treated purple membrane at 2.6 Å. J. Mol. Biol. 254, 404-415.
10. Grigorieff, N., Ceska, T. A., Downing, K. H., Baldwin, J. M. & Henderson, R. (1996). Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259, 393-421.
11. Hauss, T., Büldt, G., Heyn, M. P. & 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.
12. Henderson, R. & Moffat, J. K. (1971). The difference Fourier technique in protein crystallography: errors and their treatment. Acta Crystallog. 27, 1414-1420.
13. Henderson, R., Baldwin, J. M., Downing, K. H., Lepault, J. & Zemlin, F. (1986). Structure of purple membrane from Halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution. Ultramicroscopy, 19, 147-178.
14. Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E. & Downing, K. H. (1990). Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy. J. Mol. Biol. 213, 899-929.
15. Heyn, M. P., Westerhausen, J., Wallat, I. & Seiff, F. (1988). High-sensitivity neutron diffraction of membranes: location of the Schiff base end of the chromophore of bacteriorhodopsin. Proc. Natl Acad. Sci. USA, 85, 2146-2150.
16. Jacrot, B. (1976). The study of biological structures by neutron scattering from solution. Rep. Prog. Phys. 39, 911-953.
17. Jubb, J. S., Worcester, D. L., Crespi, H. L. & Zaccai, G. (1984). Retinal location in purple membrane of Halobacterium halobium: a neutron diffraction study of membranes labelled in vivo with denatured retinal. EMBO J. 3, 1455-1461.
18. Kamikubo, H., Kataoka, M., Varo, G., Oka, T., Tokunaga, F., Needleman, R. & Lanyi, J. K. (1996). Structure of the N intermediate of bacteriorhodopsin revealed by X-ray diffraction. Proc. Natl Acad. Sci. USA, 93, 1386-1390.
19. Koch, M. H. J., Dencher, N. A., Oesterhelt, D., Plöhn, H.-J., Rapp, G. & Büldt, G. (1991). Time-resolved X-ray diffraction studies of structural changes associated with the photocycle of bacteriorhodopsin. EMBO J. 10, 521-526.
20. Korenstein, R. & Hess, B. (1977). Hydration effects on the photocycle of bacteriorhodopsin in thin layers of purple membrane. Nature, 270, 184-186.
21. Lanyi, J. K. (1993). Proton translocation mechanism and energetics in the light-driven pump bacteriorhodopsin. Biochim. Biophys. Acta, 1183, 241-261.
22. Lechner, R. E., Dencher., N. A., Fitter, J. & Dippel, Th. (1994). Two-dimensional proton diffusion on purple membrane. Solid State Ionics, 70/71, 296-304.
23. Mathies, R. A., Lin, S. W., Ames, J. B. & Pollard, W. T. (1991). From femtoseconds to biology: mechanism of bacteriorhodopsin's light-driven proton pump. Annu. Rev. Biophys. Chem. 20, 491-518.
24. Nakasako, M., Kataoka, M., Amemiya, Y. & Tokunaga, F. (1991). Cristallographic characterization by X-ray diffraction of the M-intermediate from the photocycle of bacteriorhodopsin at room temperature. FEBS Letters, 292, 73-75.
25. O'Brien, F. E. M. (1948). The control of humidity by saturated salt solutions. J. Sci. Instr. 25, 73-76.
26. Oesterhelt, D. & Stoeckenius, W. (1971). Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature New Biol. 233, 149-152.
27. Oesterhelt, D. & Stoeckenius, W. (1974). Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. (Biomembranes Part A), 31 (69), 667-678.
28. Ottolenghi, M. & Sheves, M.(eds) (1995). Photophysics and photochemistry of retinalproteins. Isr. J. Chem. 35(34), 193-515.
29. Papadopoulos, G., Dencher, N. A., Zaccai, G. & Büldt, G. (1990). Water molecules and exchangeable hydrogen ions at the active centre of bacteriorhodopsin localized by neutron diffraction: elements of proton pathway? J. Mol. Biol. 214, 15-19.
30. Pebay-Peyroula, E., Rummel, G., Rosenbusch, J. & Landau, E. M. (1997). X-ray structure of bacteriorhodopsin at 2.5 Å from microcrystals grown in lipidic cubic phases. Science, 277, 1676-1681.
31. Plöhn, H. J. & Büldt, G. (1986). The determination of label positions in membrane proteins by neutron and anomalous X-ray diffraction of powder samples. J. Appl. Crystallog. 19, 255-261.
32. Popot, J. L., Engelman, D. M., Gurel, O. & Zaccai, G. (1989). Tertiary structure of bacteriorhodopsin. Positions and orientations of helices A and B in the structural map determined by neutron diffraction. J. Mol. Biol. 210, 829-847.
33. Sasaki, J., Shichida, Y., Lanyi, J. K. & Maeda, A. (1992). Protein changes associated with reprotonation of the Schiff base in the photocycle of Asp96-Asn bacteriorhodopsin. J. Biol. Chem. 267, 20782-20786.
34. Sass, H. J., Schachowa, I. W., Rapp, G., Koch, M. H. J., Oesterhelt, D., Dencher, N. A. & Büldt, G. (1997). The tertiary structure changes in bacteriorhodopsin occur between M states: X-ray diffraction and Fourier transform infrared spectroscopy. EMBO J. 16, 1484-1491.
35. Schulenberg, P. J., Gärtner, W. & Braslavsky, S. E. (1995). Time-resolved volume changes during the bacteriorhodopsin photocycle: a photothermal beam deflection study. J. Phys. Chem. 99, 9617-9624.
36. Subramaniam, S., Gerstein, M., Oesterhelt, D. & Henderson, R. (1993). Electron diffraction analysis of the structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12, 1-8.
37. Tittor, J., Schweiger, U., Oesterhelt, D. & Bamberg, E. (1994). Inversion of proton translocation in bacteriorhodopsin mutants D85N, D85T, and D85,96N. Biophys. J. 67, 1682-1690.
38. Váró, G. & Keszthelyi, L. (1985). Arrhenius parameters of the bacteriorhodopsin photocycle in dried oriented samples. Biophys. J. 47, 243-246.
39. Váró, G. & Lanyi, J. K. (1991). Kinetic and spectroscopic evidence for an irreversible step between deprotonation and reprotonation of the Schiff base in the bacteriorhodopsins photocycle. Biochemistry, 30, 5008-5015.
40. Váró, G. & Lanyi, J. K. (1995). Effects of hydrostatic pressure on the kinetics reveal a volume increase during the bacteriorhodopsin photocycle. Biochemistry, 34, 12161-12169.
41. Vonck, J. (1996). A three-dimensional difference map of the N intermediate in the bacteriorhodopsins photocycle: part of the F helix tilts in the M to N transition. Biochemistry, 35, 5870-5878.
42. Zaccai, G. (1987). Structure and hydration of purple membranes in different conditions. J. Mol. Biol. 194, 569-572.
43. Zaccai, G. & Gilmore, D. J. (1979). Areas of hydration in the purple membrane of Halobacterium halobium: a neutron diffraction study. J. Mol. Biol. 132, 181-191.
44. Zaccai, G. & Jacrot, B. (1983). Small angle neutron scattering. Ann. Rev. Biophys. Bioeng. 12, 139-157.