Protein, lipid and water organization in bacteriorhodopsin crystals: A molecular view of the purple membrane at 1.9 Å resolution

Structure

Volumn 7, Issue 8, 1999, Pages 909-917

  Belrhali, Hassan ^a   Nollert, Peter ^b,f   Royant, Antoine ^a,c   Menzel, Christoph ^d   Rosenbusch, Jurg P ^b   Landau, Ehud M ^b   Pebay Peyroula, Eva ^c,e  

^a EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIV GRENOBLE ALPES   (France)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cubic phase crystallization; Matrix assisted laser desorption ionization mass spectrometry; Membrane protein structure; Purple membrane; X ray crystallography

Indexed keywords

ADENOSINE TRIPHOSPHATE; ASPARTIC ACID; BACTERIORHODOPSIN; GLUTAMIC ACID; LIPID; LYSINE; NITROGEN; PROTEIN; PROTON; PROTON PUMP; RETINAL; SCHIFF BASE; WATER;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HALOBACTERIUM SALINARUM; HYDROGEN BOND; LIGHT; LIPID ANALYSIS; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; PURPLE MEMBRANE; TEMPERATURE;

EID: 0033567092     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(99)80118-X     Document Type: Article

References (36)

1. Simons, K. & Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
2. Oesterhelt, D. & Stoeckenius, W. (1971). Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat. New Biol. 233, 149-152.
3. Henderson, R. & Unwin, P.N.T. (1975). Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 28-32.
4. 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.
5. Kimura, Y., et al., & Fujiyoshi, Y. (1997). Structure of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature 389, 206-211.
6. Kates, M. (1993). Membranes lipids of archaea. In The Biochemistry of Archaea. (Kates, M., Kushner, D.J. & Matheson, A.T., eds), pp. 261-295, Elsevier Science Publishers BV, Amsterdam, The Netherlands.
7. Henderson, R., Jubb, J.S. & Whytock, S. (1978). Specific labeling of the protein and lipid on the extracellular surface of purple membrane. J. Mol. Biol. 123, 259-274.
8. Sternberg, B., L'Hostis, C., Whiteway, C.A. & Watts, A. (1992). The essential role of specific Halobacterium halobium polar lipids in 2D-array formation of bacteriorhodopsin. Biochim. Biophys. Acta 1108, 21-30.
9. Landau, E.M. & Rosenbusch, J.P. (1996). Lipidic cubic phases: A novel concept for the crystallization of membrane proteins. Proc. Natl Acad. Sci. USA 93, 14532-14535.
10. Rummel, G., et al., & Rosenbusch, J.P. (1998). Lipidic cubic phases: New matrices for the three-dimensional crystallization of membrane proteins. J. Struct. Biol. 121, 1-11.
11. Pebay-Peyroula, E., Rummel, G., Rosenbusch, J.P. & Landau, E.M. (1997). X-ray structure of bacteriorhodopsin at 2.5 Å resolution from microcrystals grown in lipidic cubic phases. Science 277, 1676-1681.
12. Heberle, J., Büldt, G., Koglin, E., Rosenbusch, J.P. & Landau, E.M. (1998). Assessing the functionality of a membrane protein in a three-dimensional crystal. J. Mol. Biol. 281, 587-592.
13. Papadopoulos, G., Dencher, N., Zaccai, G. & Büldt, G. (1990). Water molecules and exchangeable hydrogen ions at the active center of bacteriorhodopsin localized by neutron diffraction: Elements of the proton pathway. J. Mol. Biol. 214, 15-19.
14. Luecke, H., Richter, H.-T. & Lanyi, J.K. (1998). Proton transfer pathways in bacteriorhodopsin at 2.3 Å resolution. Science 280, 1934-1937.
15. Essen, L.-O., Siegert, R., Lehmann, W.D. & Oesterhelt, D. (1998). Lipid patches in membrane protein oligomers: Crystal structure of the bacteriorhodopsin-lipid complex. Proc. Natl Acad. Sci. USA 95, 11673-11678.
16. Subramaniam, S., et al., & Henderson, R. (1999) Protein conformational changes in the bacteriorhodopsin photocycle. J. Mol. Biol. 287, 145-161.
17. Weik, M., Zaccai, G., Dencher, N.A., Oesterhelt, D. & 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.
18. Sass, H.J., et al., & 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.
19. Patzelt, H., et al., & Oesterhelt, D. (1997). Towards structural investigations on isotope labeled bacteriorhodopsin in detergent micelles by solution-state NMR spectroscopy. J. Biomol. NMR 10, 95-106.
20. Weik, M., Patzelt, H., Zaccai, G. & Oesterhelt, D. (1998). Localization of glycolipids in membranes by in vivo labeling and neutron diffraction. Mol. Cell 1, 411-419.
21. Nollert, P. & Landau, E.M. (1998). Enzymic release of crystals from lipidic cubic phases. Biochem. Soc. Trans. 26, 709-713.
22. Harvey, D.J. (1995). Matrix-assisted laser desorption/ionization mass spectrometry of phospholipids. J. Mass Spec. 30, 1333-1346.
23. Edlhom., O., Berger, O. & Jähnig, F. (1995). Structure and fluctuations of bacteriorhodopsin in the purple membrane: A molecular dynamics study. J. Mol. Biol. 250, 94-111.
24. 2H labeling and neutron scattering. Proc. Natl Acad. Sci. USA 95, 4970-4975.
25. Lehnert, U., Réat, V., Weik, M., Zaccai, G. & Pfister, C. (1998). Correlation between thermal motions and functional conformational changes in bacteriorhodopsin: A neutron scattering study at different hydration levels. Biophys. J. 75, 1945-1952.
26. Burmeister, W.P., et al., & Wakatsuki, S. (1998). Diamonds, a multilayer and a sagitally focusing crystal as optical elements on the ID14/Quadriga-3 beamline at ESRF. Proceedings of SPIE, the International Society for Optical Engineering 3448 188-196.
27. Kabsch, W. (1988). Evaluation of single crystal X-ray diffraction data from a positive-sensitive detector. J. Appl. Crystallogr. 21, 916-924.
28. Collaborative Computational Project, No. 4. (1994). The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
29. Yeates, T.O. (1997). Detecting and overcoming crystal twinning. Methods Enzymol. 276, 344-358.
30. Brünger, A.T., et al., & Warren, G.L. (1998). Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921.
31. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in the models. Acta Crystallogr. A 47, 110-119.
32. Kraulis, P.J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
33. Karas, M., Ehring, H., Nordhoff, E., Stahl, B., Strupat, K. & Hillenkamp, F. (1993). Matrix-assisted laser desorption/ionization mass spectrometry with additives to 2,5-dihydroxybenzoic acid. Org. Mass Spec. 28, 1476-1481.
34. Little, D.P., Cornish, T.J., O'Donnel, M.J., Braun, A., Cotter, R.J. & Köster, H. (1997). MALDI on a chip: Analysis of arrays of low-femtomol quantities of synthetic oligonucleotides and DNA diagnostics products dispensed by a piezoelectric pipet. Anal. Chem. 69, 4540-4546.
35. Karas, M. & Hillenkamp, F. (1998). Laser desorption/ionization of proteins with molecular masses exceeding 10000 daltons. Anal. Chem. 60, 2299-2301.
36. Menzel, C., Berkenkamp, S. & Hillenkamp, F. (1999). Infrared matrix-assisted laser desorption/ionization mass spectrometry with a transversely excited atmospheric pressure carbon dioxide laser at 10.6 μm wavelength with static and delayed ion extraction. Rap. Commun. Mass Spec. 13, 26-32.