Differential stiffness and lipid mobility in the leaflets of purple membranes

Biophysical Journal

Volumn 90, Issue 6, 2006, Pages 2075-2085

  Voïtchovsky, Kislon ^a   Contera, Sonia Antoranz ^a   Kamihira, Miya ^b,c   Watts, Anthony ^b   Ryan, J F ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF SHIZUOKA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHLORIDE; INORGANIC SALT; MEMBRANE LIPID;

ARTICLE; ATOMIC FORCE MICROSCOPY; CYTOPLASM; LIPID METABOLISM; NUCLEAR MAGNETIC RESONANCE; PH; PURPLE MEMBRANE; SOLID STATE; CELL SURFACE; CHEMISTRY; CONFORMATION; ELASTICITY; MECHANICAL STRESS; MEMBRANE FLUIDITY; METHODOLOGY;

CELL SURFACE EXTENSIONS; ELASTICITY; MEMBRANE FLUIDITY; MEMBRANE LIPIDS; MICROSCOPY, ATOMIC FORCE; MOLECULAR CONFORMATION; PURPLE MEMBRANE; SALTS; STRESS, MECHANICAL;

EID: 33645545806     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.072405     Document Type: Article

References (62)

1. Houslay, M. D., and K. K. Stanley. 1982. Dynamics of Biological Membranes. Wiley Interscience, New York.
2. Op den Kamp, J. A. F. 1979. Lipid asymmetry in membranes. Annu. Rev. Biochem. 48:47-71.
3. Rothman, J. E., and J. Lenard. 1977. Membrane asymmetry. Science. 195:743-753.
4. Bergelson, L. D., and L. I. Barsukov. 1977. Topological asymmetry of phospholipids in membranes. Science. 197:224-230.
5. 2H-NMR study. Biochim. Biophys. Acta. 1106:317-324.
6. Renthal, R., and C. H. Cha. 1984. Charge asymmetry of the purple membrane measured by uranyl quenching of dansyl fluorescence. Biophys. J. 45:1001-1006.
7. Müller, D. J., C. A. Schoenenberger, G. Buldt, and A. Engel. 1996. Immuno-atomic force microscopy of purple membrane. Biophys. J. 70:1796-1802.
8. Cartailler, J. P., and H. Luecke. 2003. X-ray and crystallographic analysis of lipid-protein interactions in the bacteriorhodopsin purple membrane. Annu. Rev. Biophys. Biomol. Struct. 32:285-310.
9. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:899-911.
10. Lanyi, J. K. 1995. Bacteriorhodopsin as a model for proton pumps. Nature. 375:461-463.
11. Krebs, M. P., and T. A. Isenbarger. 2000. Structural determinants of purple membrane assembly. Biochim. Biophys. Acta. 1460:15-26.
12. Lee, A. G. 2003. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta. 1612:1-40.
13. Kates, M., S. C. Kushwaha, and G. D. Sprott. 1982. Lipids of purple membrane from extreme halophiles and of methanogenic bacteria. Methods Enzymol. 88:98-111.
14. Corcelli, A., V. M. T. Lattanzio, G. Mascolo, P. Papadia, and F. Fanizzi. 2002. Lipid-protein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane. J. Lipid Res. 43:132-140.
15. Corcelli, A., V. M. T. Lattanzio, G. Mascolo, P. Papadia, and F. Fanizzi. 2002. Lipid-protein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane. J. Lipid Res. 43:132-140.
16. Sternberg, B., C. L'Hostis, C. A. Whiteway, and A. Watts. 1992. The essential role of specific Halobacterium halobium polar lipids in 2D-array formation of bacteriorhodopsin. Biochim. Biophys. Acta 1108:21-30.
17. Grigorieff, N., E. Beckmann, and F. Zemlin. 1995. Lipid location in deoxycholate-treated purple membrane at 2.6 Å. J. Mol. Biol. 254:404-415.
18. Pebay-Peyroula, E., G. Rummel, J. P. Rosenbusch, and E. M. Landau. 1997. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science. 277:1676-1681.
19. Belrhali, H., P. Nollert, A. Royant, C. Menzel, J. P. Rosenbusch, E. M. Landau, and E. Pebay-Peyroula. 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.
20. Watts, A. 1995. Bacteriorhodopsin: the mechanism of 2D-array formation and the structure of retinal in the protein. Biophys. Chem. 55:137-151.
21. Saito, H., Y. Yamamoto, S. Tuzi, and S. Yamaguchi. 2003. Backbone dynamics of membrane proteins in lipid bilayers: the effect of two-dimensional array formation as revealed by site-directed solid-state 13C NMR studies on [3-13C]Ala-and [1-13]Val-labeled bacteriorhodopsin. Biochim. Biophys. Acta. 1616:127-136.
22. Sato, H., K. Takeda, K. Tani, T. Hino, T. Okada, M. Nakasako, N. Kamiya, and T. Kouyama. 1999. Specific lipid-protein interactions in a novel honeycomb lattice structure of bacteriorhodopsin. Acta Crystallogr. D. 55:1251-1256.
23. Weik, M., H. Patzelt, G. Zaccai, and D. Oesterhelt. 1998. Localization of glycolipids in membranes by in vivo labeling and neutron diffraction. Mol. Cell. 1:411-419.
24. Henderson, R., J. S. Jubb, and S. Whytock. 1978. Specific labelling of the protein and lipid on the extracellular surface of purple membrane. J. Mol. Biol. 123:259-274.
25. Grigorieff, N., T. A. Ceska, K. H. Downing, J. M. Baldwin, and R. Henderson. 1996. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:393-421.
26. Möller, C., M. Allen, V. Elings, A. Engel, and D. J. Mudie;ller. 1999. Tapping-mode atomic force microscopy produces faithful high-resolution images of protein surfaces. Biophys. J. 77:1150-1158.
27. Müller, D. J., J. B. Heymann, F. Oesterhelt, C. Möller, H. Gaub, G. Buldt, and A. Engel. 2000. Atomic force microscopy of native purple membrane. Biochim. Biophys. Acta. 1460:27-38.
28. Subramaniam, S., M. Gerstein, D. Oesterhelt, and R. Henderson. 1993. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12:1-8.
29. Seelig, J. 1978. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim. Biophys. Acta. 515:105-140.
30. Watts, A. 1998. Solid-state NMR approaches for studying the interaction of peptides and proteins with membranes. Biochim. Biophys. Acta. 1376:297-318.
31. Ulrich, A. S., M. P. Heyn, and A. Watts. 1992. Structure determination of the cyclohexene ring of retinal in bacteriorhodopsin by solid-state deuterium nmr. Biochemistry. 31:10390-10399.
32. 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.
33. Müller, D. J., A. Engel, and M. Amrein. 1997. Adsorption of biological molecules to a solid support for scanning probe microscopy. J. Struct. Biol. 119:172-188.
34. Biscan, J., N. Kallay, and T. Smolic. 2000. Determination of isoelectric point of silicon nitride by adhesion method. Colloids Surf. A. 165:115-123.
35. Butt, H. J., and M. Jaschke. 1995. Calculation of thermal noise in atomic force microscopy. Nanotechnology. 6:1-7.
36. Hutter, J. L., and J. Bechhoefer. 1993. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64:1868-1873.
37. Sader, J. E. 1995. Parallel beam approximation for V-shaped atomic force microscope cantilevers. Rev. Sci. Instrum. 66:4583-4587.
38. Israelachvili, J. N. 1991. Intermolecular and Surface Forces. Academic Press, London.
39. Müller, D. J., D. Fotiadis, S. Scheuring, S. A. Müller, and A. Engel. 1999. Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscope. Biophys. J. 76:1101-1111.
40. San Paulo, A., and R. Garcia. 2001. Amplitude, deformation and phase shift in amplitude modulation atomic force microscopy: a numerical study for compliant materials. Surf. Sci. 471:71-79.
41. García, R., J. Tamayo, and A. San Paulo. 1999. Phase contrast and surface energy hysteresis in tapping mode scanning force microscopy. Surf. Interf. Anal. 27:312-316.
42. Cleveland, J. P., B. Anczykowski, A. E. Schmid, and V. B. Elings. 1998. Energy dissipation in tapping-mode atomic force microscopy. Appl. Phys. Lett. 72:2613-2615.
43. Stark, M., C. Moller, D. J. Muller, and R. Guckenberger. 2001. From images to interactions: high-resolution phase imaging in tapping-mode atomic force microscopy. Biophys. J. 80:3009-3018.
44. Neugebauer, D. C., H. P. Zingsheim, and D. Oesterhelt. 1983. Biogenesis of purple membrane in halobacteria. Methods Enzymol. 97:218-226.
45. Fisher, K. A., K. Yanagimoto, and W. Stoeckenius. 1978. Oriented adsorption of purple membrane to cationic surfaces. J. Cell Biol. 77:611-621.
46. Zaccai, G. 1987. Structure and hydration of purple membranes in different conditions. J. Mol. Biol. 194:569-572.
47. Gale, P., and A. Watts. 1991. Characterization of phospholipid compositions and physical properties of DMPC/bacteriorhodopsin vesicles produced by a detergent-free method. Biochem. Biophys. Res. Commun. 180:939-944.
48. Blaurock, A. E., and W. Stoeckenius. 1971. Structure of the purple membrane. Nat. New Biol. 233:152-155.
49. Henderson, R., and P. N. Unwin. 1975. Three-dimensional model of purple membrane. Nature. 257:28-32.
50. Essen, L. O., R. Siegert, W. D. Lehmann, and D. Oesterhelt. 1998. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex. Proc. Natl. Acad. Sci. USA. 95:11673-11678.
51. Antoranz Contera, S., V. Lemaître, M. R. R. de Planque, A. Watts, and J. F. Ryan. 2005. Unfolding and extraction of a transmembrane α-helical peptide: dynamic force spectroscopy and molecular dynamics simulations. Biophys. J. 89:3129-3140.
52. Blaurock, A. E., and G. I. King. 1977. Asymmetric structure of the purple membrane. Science. 196:1101-1104.
53. Cornell, B. A., C. A. Morris, V. L. B. Braach-Maksvytis, and F. Separovic. 1987. The effect of bacteriorhodopsin on the dynamics of lipid bilayers: a study by solid state 13-C nuclear magnetic resonance. In Retinal Proteins: Proceedings of the International Conference, USSR, 1986. Yu. A. Ovchinnikov, editor. Brill Academic Publishers, Leiden, The Netherlands. 285-293.
54. Chadwick, R. S. 2002. Axisymmetric indentation of a thin incompressible elastic layer. SIAM J. Appl. Math. 62:1520-1530.
55. Haltia, T., and E. Freire. 1995. Forces and factors that contribute to the structural stability of membrane proteins. Bioenergetics. 1228:1-27.
56. Lopez, F., S. Lobasso, M. Colella, A. Agostiano, and A. Corcelli. 1999. Light-dependent and biochemical properties of two different bands of bacteriorhodopsin isolated on phenyl-sepharose CL-4B. Photochem. Photobiol. 69:599-604.
57. Hertz, H. 1882. Über die Berührung Fester Elasticher Körper. Journal für die reine und angewandte Mathematik. 92:156-171.
58. Sneddon, I. N. 1965. The relation between load and penetration in the axisymmetric Boussinesq problem for a punch of arbitrary profile. Internat. J. Engin. Sci. 3:47-57.
59. Domke, J., and M. Radmacher. 1998. Measuring the elastic properties of thin polymer films with the atomic force microscope. Langmuir. 14:3320-3325.
60. Benz, M., T. Gutsmann, N. Chen, R. Tadmor, and J. Israelachvili. 2004. Correlation of AFM and SFA measurements concerning the stability of supported lipid bilayers. Biophys. J. 86:870-879.
61. Cevc, G., and D. Marsh. 1987. Phospholipid Bilayers: Physical Principles and Models. Wiley, New York.
62. Dimitriadis, E. K., F. Horkay, J. Maresca, B. Kachar, and R. S. Chadwick. 2002. Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys. J. 82:2798-2810.