Lipidic cubic phases: New matrices for the three-dimensional crystallization of membrane proteins

Journal of Structural Biology

Volumn 121, Issue 2, 1998, Pages 82-91

  Rummel, Gabriele ^a   Hardmeyer, Ariane ^a   Widmer, Christine ^a   Chiu, Mark L ^a   Nollert, Peter ^a   Locher, Kaspar P ^a   Pedruzzi, Ivo ^a   Landau, Ehud M ^a   Rosenbusch, Jurg P ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Bacteriorhodopsin; Cubic phase preparation; Lipidic matrices; Membrane protein crystallization; Phase diagrams

Indexed keywords

BACTERIORHODOPSIN; LIPID; LYSOZYME; MEMBRANE PROTEIN; MONOACYLGLYCEROL; WATER;

ARTICLE; CRYSTALLIZATION; LIPID BILAYER; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

EID: 0031829172     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.1997.3952     Document Type: Article

References (70)

1. Abrahams J. P., Leslie A. G. W., Lutter R., Walker J. E. Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature. 370:1994;621-628.
2. Allen J. P., Feher G., Yeates T. O., Komiya H., Rees D. C. Structure of the reaction center fromRhodobacter sphaeroides. Proc. Natl. Acad. Sci. USA. 84:1987;5730-5734.
3. Bax A. Multidimensional NMR methods for protein studies. Curr. Opin. Struct. Biol. 4:1997;738-744.
4. Bloom M., Evans E., Mouritsen O. G. Physical properties of the fluid lipid bilayer component of cell membranes: a perspective. Quart. Rev. Biophysics. 24:1992;293-397.
5. Briggs J., Chung H., Caffrey M. The temperature-composition phase diagram and mesophase structure characterization of the monoolein/water system. J. Physique II. 6:1996;723-752.
6. Buchheim W., Larsson K. Cubic lipid-protein-water phases. J. Coll. Interface Sci. 117:1987;582-583.
7. Bult C. J., White O., Olsen G. J., Zhou L., Fleischmann R. D., Sutton G. G., Blake J. A., FitzGerald L. M., Clayton R. A., Gocayne J. D., Kerlavage A. R., Dougherty B. A., Tomb J. F., Adams M. D., Reich C. I., Overbeek R., Kirkness E. F., Weinstock K. G., Merrick J. M., Glodek A., Scott J. L., Geoghagen N. S. M., Venter J. C. Complete genome sequence of the methanogenic archaeon. Methanococcus jannaschii, Science. 273:1996;1058-1073.
8. Cantor R. S. The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry. 36:1997;2339-2344.
9. Chang C.-H., El-Kabbani O., Tiede D., Norris J., Schiffer M. Structure of the membrane-bound protein photosynthetic reaction center fromRhodopseudomonas sphaeroides. Biochemistry. 30:1991;5352-5360.
10. Chung H., Caffrey M. The curvature elastic-energy function of the lipid-water cubic mesophase. Nature. 368:1994;224-226.
11. Cowan S. W., Garavito R. M., Jansonius J. N., Jenkins J., Karlsson R., Koenig N., Pai E. F., Pauptit R. A., Rizkallah P. J., Rosenbusch J. P., Rummel G., Schirmer T. The structure of OmpF porin in a tetragonal crystal form. Structure. 3:1995;1041-1050.
12. Cowan S. W., Rosenbusch J. P. Folding pattern diversity of integral membrane proteins. Science. 264:1994;914-916.
13. Cowan S. W., Schirmer T., Rummel G., Steiert M., Ghosh R., Pauptit R. A., Jansonius J. N., Rosenbusch J. P. Crystal Structures Explain Functional Properties of twoE. coli. Nature. 358:1992;727-733.
14. Cribier S., Gulik A., Fellmann P., Vargas R., Devaux P. F., Luzzati V. Cubic Phases of Lipid-containing Systems. J. Mol. Biol. 229:1993;517-525.
15. de Kruijff B. Lipids beyond the bilayer. Nature. 386:1997;129-130.
16. Deisenhofer J., Epp O., Miki K., Huber R., Michel H. Structure of the protein subunits in the photosynthetic reaction centre ofRhodopseudomonas viridis. Nature. 318:1985;618-624.
17. Ericsson B., Larsson K., Fontell K. A Cubic Protein-Monoolein-Water Phase. Biochim. Biophys. Acta. 729:1983;23-27.
18. Eriksson P.-O., Lindblom G., Arvidson G. NMR studies of micellar aggregates in 1-acyl-sn. J. Phys. Chem. 91:1987;846-853.
19. Ermler U., Fritzsch G., Buchanan S. K., Michel H. Structure of the photosynthetic reaction center fromRhodobacter sphaeroides. Structure. 2:1994;925-936.
20. Fleischmann, R. D. Adams, M. D. White, O. Clayton, R. A. Kirkness, E. F. Kerlavage, A. R. Bult, C. J. Tomb, J. F. Dougherty, B. A. Merrick, J. M. et al. 1995, Whole-genome random sequence and assembly ofHaemophilus influenzae, Science, 269, 496, 512.
21. Fontell K. Cubic phases in surfactant and surfactant-like lipid systems. Colloid Polym. Sci. 268:1990;264-285.
22. Fulford A. J. C., Peel W. E. Lateral pressures in biomembranes estimated from the dynamics of fluorescent probes. Biochim. Biophys. Acta. 598:1980;237-246.
23. Garavito R. M., Rosenbusch J. P. Three-dimensional crystals of an integral membrane protein: An initial X-ray analysis. J. Cell. Biol. 86:1980;327-329.
24. Grigorieff T., Ceska T. A., Downing K. H., Baldwin J. M., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:1996;393-421.
25. Gruner S. M., Shyamsunder E. Is the mechanism of general anesthesia related to lipid membrane spontaneous curvature. Ann. N. Y. Acad. Sci. 625:1991;685-697.
26. Guillon T., Schaefer J. Detection of weak heteronuclear dipolar coupling by rotational-echo double-resonance NMR. Adv. Magn. Reson. 13:1989;57-83.
27. Helenius A., Simons K. Solubilization of membrane proteins by detergents. Biochim. Biophys. Acta. 415:1975;29-79.
28. Henderson R., Shotton D. J. Mol. Biol. 139:1980;99-102.
29. Henderson R., Unwin P. N. T. Three-dimensional model of purple membrane obtained by electron microscopy. Nature. 257:1975;28-32.
30. Hyde S., Anderson S., Larsson K., Blum Z., Landh T., Lidin S., Ninham B. W. The Language of Shape. 1997;Elsevier, Amsterdam.
31. Iwata S., Ostermeier C., Ludwig B., Michel H. Structure at 2.8Å resolution of cytochromecParacoccus denitrificans. Nature. 376:1995;660-668.
32. Jackson M. B., Sturtevant J. M. Phase Transitions of the Purple Membranes ofHalobacterium halobium. Biochemistry. 17:1978;911-915.
33. Kimura Y., Vassylyev D. G., Miyazawa A., Kidera A., Matsushima M., Mitsuoka K., Murata K., Hirai T., Fujiyoshi Y. Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature. 389:1997;206-211.
34. Komiya H., Yeates T. O., Rees D. C., Allen J. P., Feher G. Structure of the reaction center fromRhodobacter sphaeroides. Proc. Natl. Acad. Sci. USA. 85:1988;9012-9016.
35. Landau E. M., Rosenbusch J. P. Lipidic cubic phases: A novel concept for the crystallization of membrane proteins. Proc. Natl. Acad. Sci. USA. 93:1996;14532-14535.
36. Landau E. M., Rummel G., Cowan-Jacob S. W., Rosenbusch J. P. Crystallization of a polar protein and small molecules from the aqueous compartent of lipidic cubic phases. J. Phys. Chem. B. 101:1997;1935-1937.
37. Larsson K. Cubic Lipid-Water Phases: Structures and Biomembrane Aspects. J. Phys. Chem. 93:1989;7304-7314.
38. Leslie S. B., Puvvada S., Ratna B. R., Rudolph A. S. Encapsulation of hemoglobin in a bicontinuous cubic phase lipid. Biochim. Biophys. Acta. 1285:1996;246-254.
39. Lindblom G., Rilfors L. Cubic phases and isotropic structures formed by membrane lipids - possible biological relevance. Biochim. Biophys. Acta. 988:1989;221-256.
40. Locher K., Rosenbusch J. P. Oligomeric states and siderophore binding of the ligand-gated FhuA protein that forms channels acrossEscherichia coli. Eur. J. Biochem. 247:1997;770-775.
41. Luzzati V., Gulik-Krzywicki T., Tardieu A. Polymorphism of lecithins. Nature. 218:1968;1031-1034.
42. Luzzati V., Vargas R., Mariani P., Gulik A., Delacroix H. Cubic Phases of Lipid-containing systems. J. Mol. Biol. 229:1993;540-551.
43. Marsh D. Lateral pressure in membranes. Biochim. Biophys. Acta. 1286:1996;183-223.
44. McDermott G., Prince S. M., Freer A. A., Hawthornethwaite-Lawless A. M., Papiz M. Z., Cogdell R. J., Isaacs N. W. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature. 374:1995;517-521.
45. McDowell L. M., Schaefer J. High resolution NMR of biological solids. Curr. Op. Struct. Biol. 6:1996;624-629.
46. McPherson A. Preparation and analysis of protein crystals. 1982;John Wiley and Sons, New York.
47. Michel H., Oesterhelt D. Three dimensional crystals of membrane proteins: bacteriorhodopsin. Proc. Natl. Acad. Sci. U. S. AU. S. 77:1980;1283-1285.
48. Newman M. J., Foster D. L., Wilson T. H., Kaback R. Purification and reconstitution of functional lactose carrier fromEscherichia coli. J. Biol. Chem. 256:1981;11804-11808.
49. Oschkinat H., Miller T., Dieckmann T. Protein Structure determined with three and four-dimensional NMR spectroscopy. Angew. Chemie Engl. Ed. 33:1994;277-293.
50. Page M. G. P., Rosenbusch J. P., Yamato I. The effects of pH on proton sugar symport activity of the lactose permease purified fromEscherichia coli. J. Biol. Chem. 263:1988;15897-15905.
51. Pebay-Peroula E., Rummel G., Rosenbusch J. P., Landau E. M. High resolution X-ray structure of bacteriorhodopsin from microcrystals grown in lipidic cubic phases. Science. 277:1997;1676-1680.
52. +++. Biochemistry. 34:1995;4412-4420.
53. Razumas V., Larsson K., Miezis Y., Nylander T. A cubic monoolein-cytochromec. J. Phys. Chem. 100:1996;11766-11774.
54. Rilfors L., Eriksson P.-O., Arvidson G., Lindblom G. Relationship between three-dimensional arrays of "lipidic particles" and bicontinuous cubic lipid phases. Biochemistry. 25:1986;7702-7711.
55. Rosenbusch J. P. Characterization of the major envelope protein fromEscherichiacoli. J. Biol. Chem. 249:1974;8019-8029.
56. Rosenbusch J. P., Müller R. Solubilization of Lipo-protein Complexes. 1977;European Press, Ghent. p. 59-68.
57. Schirmer T., Keller T. A., Wang Y.-F., Rosenbusch J. P. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science. 267:1995;512-514.
58. Service R. F. Brightness speeds search for structures great and small. Science. 277:1997;1217-1219.
59. Sober H. A., Harte R. A. Sober E. K. Handbook of Biochemistry. 1968;J-195 CRC, Cleveland.
60. Song L., Hobaugh M. R., Shustak C., Cheley S., Bayley H., Gouaux J. E. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science. 274:1996;1859-1866.
61. Tanford C., Reynolds J. A. Characterization of membrane proteins in detergent solutions. Biochim. Biophys. Acta. 457:1976;133-170.
62. Torchia D. A. Solid state nuclear magnetic resonance studies of protein internal dynamics. Annu. Rev. Biophys. Bioeng. 13:1989;125-144.
63. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi A., Shinzawa-Itoh K., Nakashima R., Yaono R., Yoshikawa S. The whole structures of the 13-subunit oxidised cytochrome c oxidase at 2.8 Å Science. 272:1996;1136-1144.
64. Vargas R., Mariani P., Gulik A., Luzzati V. Cubic Phases of Lipid-containing Systems. J. Mol. Biol. 225:1992;137-145.
65. Walker J. E., Saraste M. Membrane protein structure. Curr. Opin. Struct. Biol. 6:1996;457-459.
66. Weiss M. S., Abele U., Weckesser J., Welte W., Schiltz E., Schulz G. E. Molecular Architecture and Electrostatic Properties of a Bacterial Porin. Science. 254:1991;1627-1630.
67. Weiss M. S., Schulz G. E. Structure of Porin Refined at 1.8 Å Resolution. J. Mol. Biol. 227:1992;493-509.
68. Wüthrich K. Protein Structure determined in Solution by NMR spectroscopy. Science. 243:1989;45-50.
69. Xia D., Yu C.-A., Kim H., Xia J.-Z., Kachurin A. M., Zhang L., Yu L., Deisenhofer J. Crystal Structure of the Cytochrome bc1 Complex from Bovine Heart Mitochondria. Science. 277:1997;60-66.
70. Zulauf M., Rosenbusch J. P. Micelle clusters of octyl-oligooxyethylenes. J. Phys. Chem. 87:1983;856-862.