Crystallinity of purple membranes comprising the chloride-pumping bacteriorhodopsin variant D85T and its modulation by pH and salinity

Journal of Physical Chemistry B

Volumn 114, Issue 46, 2010, Pages 15424-15428

  Rhinow, Daniel ^a   Chizhik, Ivan ^b   Baumann, Roelf Peter ^b   Noll, Frank ^b   Hampp, Norbert ^b,c  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c Material Sciences Center   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ATOMIC FORCE MICROSCOPY; BIOLOGICAL MEMBRANES; CELL MEMBRANES; CHLORINE COMPOUNDS; CRYSTALLINE MATERIALS; CYTOLOGY; FUNCTIONAL GROUPS; PROTEINS; PROTONATION; PUMPS; X RAY SCATTERING;

AMINO ACID RESIDUES; BACTERIORHODOPSIN (BR); BINDING POCKETS; CHLORIDE BINDING; CHLORIDE ION CONCENTRATION; CRYSTALLINE ARRAYS; CRYSTALLINE DOMAINS; CRYSTALLINE LATTICE; CRYSTALLINITIES; FREEZE FRACTURE ELECTRON MICROSCOPY; HALORHODOPSIN; MEMBRANE PROTEINS; MODEL SYSTEM; NATIVE ENVIRONMENT; PH VALUE; PROTEIN-LIPID INTERACTIONS; PROTONATED; PROTONATION STATE; PURPLE MEMBRANES; SCHIFF-BASE; SMALL ANGLE X-RAY SCATTERING; SUBSTRATE BINDING; WILD TYPES;

MEMBRANES;

EID: 78649616253     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp108502p     Document Type: Article

References (38)

1. Oesterhelt, D.; Stoeckenius, W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium Nat. New Biol. 1971, 233, 149-152
2. Haupts, U.; Tittor, J.; Oesterhelt, D. Closing in on Bacteriorhodopsin: Progress in Understanding the Molecule Annu. Rev. Biophys. Biomol. Struct. 1999, 28, 367-399
3. Lanyi, J. K. Bacteriorhodopsin Annu. Rev. Physiol. 2004, 66, 665-688
4. Krebs, M. P.; Isenbarger, T. A. Structural Determinants of Purple Membrane Assembly Biochim. Biophys. Acta 2000, 1460, 15-26
5. Kolbe, M.; Hüseyin, B.; Essen, L.-O.; Oesterhelt, D. Structure of the light-driven chloride pump halorhodopsin at 1.8 A. resolution Science 2000, 288, 1390-1396
6. Luecke, H.; Schobert, B.; Lanyi, J. K.; Spudich, E. N.; Spudich, J. L. Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction Science 2001, 293, 1499-1503
7. Royant, A.; Nollert, P.; Edman, K.; Neutze, R.; Landau, E. M.; Pebay-Peyroula, E.; Navarro, J. X-ray structure of sensory rhodopsin II at 2.1 Å resolution Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 10131-10136
8. Gordeliy, V. I.; Labahn, J.; Moukhametzianov, R.; Efremov, R.; Granzin, J.; Schlesinger, Büldt, G.; Savopol, T.; Scheidig, A. J.; Klare, J. P.; Engelhard, M. Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex Nature 2002, 419, 484-487
9. Vogley, L.; Sineshekov, O. A.; Vishwa, D. T.; Sasaki, J.; Spudich, J.; Luecke, H. Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å Science 2004, 306, 1390-1393
10. Balashov, S. P.; Imasheva, E. S.; Boichenko, V. A.; Antón, J.; Wang, J. M.; Lanyi, J. K. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna Science 2005, 309, 2061-2064
11. Spudich, J. L. The multitalented microbial sensory rhodopsins Trends Microbiol. 2006, 14, 480-487
12. Grigorieff, N.; Ceska, T. A.; Downing, K. H.; Baldwin, J. M.; Henderson, R. Electron-crystallographic refinement of the structure of bacteriorhodopsin J. Mol. Biol. 1996, 259, 393-421
13. 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 1997, 389, 206-211
14. Essen, L.-O.; Siegert, R.; Lehmann, W. D.; Oesterhelt, D. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 11673-11678
15. Luecke, H.; Schobert, B.; Richter, H.-T.; Cartailler, J.-P.; Lanyi, J. Structure of bacteriorhodopsin at 1.55 Å resolution J. Mol. Biol. 1999, 291, 899-911
16. Sass, H. J.; Büldt, G.; Gessenich, R.; Hehn, D.; Neff, D.; Schlesinger, R.; Berendzen, J.; Ormos, P. Structural alterations for proton translocation in the M state of wild-type bacteriorhodopsin Nature 2000, 406, 649-653
17. Subramaniam, S.; Henderson, R. Molecular mechanism of vectorial proton translocation by bacteriorhodopsin Nature 2000, 406, 653-657
18. Sapra, K. T.; Hüseyin, B.; Oesterhelt, D.; Müller, D. J. Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy J. Mol. Biol. 2006, 355, 640-650
19. Lindahl, M.; Henderson, R. Structure of the bacteriorhodopsin D85N/D96N double mutant showing substantial structural changes and a highly twinned disordered lattice Ultramicroscopy 1997, 70, 95-106
20. Möller, C.; Büldt, G.; Dencher, N. A.; Engel, A.; Müller, D. J. Reversible loss of crystallinity on photobleaching purple membrane in the presence of hydroxylamine J. Mol. Biol. 2000, 301, 869-879
21. Sasaki, J.; Brown, L. S.; Chon, Y. S.; Kandori, H.; Maeda, A.; Needleman, R.; Lanyi, J. K. Conversion of bacteriorhodopsin into a chloride ion pump Science 1995, 269, 73-75
22. Tittor, J.; Haupts, U.; Haupts, C.; Oesterhelt, D.; Becker, A.; Bamberg, E. Chloride and proton transport in bacteriorhodopsin mutant D85T: Different Modes of Ion Translocation in a Retinal Protein J. Mol. Biol. 1997, 271, 405-416
23. Oesterhelt, D.; Stoeckenius, W. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane Methods Enzymol. 1974, 31, 667
24. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera-A visualization system for exploratory research and analysis J. Comput. Chem. 2004, 25, 1605-1612
25. Schranz, M.; Baumann, R.-P.; Rhinow, D.; Hampp, N. Dynamics of Bacteriorhodopsin in Solid-Supported Purple Membranes Studied with Tapping-Mode Atomic Force Microscopy J. Phys. Chem. B 2010, 114, 9047-9053
26. Tittor, J.; Schweiger, U.; Oesterhelt, D.; Bamberg, E. Inversion of proton translocation in bacteriorhodopsin mutants D85N, D85T, and D85,96N Biophys. J. 1994, 67, 1682-1690
27. Tittor, J.; Oesterhelt, D.; Bamberg, E. Bacteriorhodopsin mutants D85N, D85T and D85,96N as proton pumps Biophys. Chem. 1995, 56, 153-157
28. Turner, G. J.; Miercke, J. W.; Thorgeirsson, T. E.; Kliger, D. S.; Betlach, M. C.; Stroud, R. M. Bacteriorhodopsin D85N: Three spectroscopic species in equilibrium Biochemistry 1993, 32, 1332-1337
29. Brown, L.; Kamikubo, H.; Zimányi, L.; Kataoka, M.; Tokunaga, F.; Verdegem, P.; Lugtenburg, J.; Lanyi, J. K. A local electrostatic change is the cause of the large-scale protein conformation shift in bacteriorhodopsin Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 5040-5044
30. Rhinow, D.; Hampp, N. A. Light- and pH-dependent conformational changes in protein structure induce strong bending of purple membranes-active membranes studied by cryo-SEM J. Phys. Chem. B 2008, 112, 13116-13120
31. Baumann, R.-P.; Schranz, M.; Hampp, N. Bending of purple membranes in dependence on the pH analyzed by AFM and single molecule force spectroscopy Phys. Chem. Chem. Phys. 2010, 12, 4329-4335
32. Rhinow, D.; Hampp, N. Curvature of Purple Membranes Comprising Permanently Wedge-Shaped Bacteriorhodopsin Molecules Is Regulated by Lipid Content J. Phys. Chem. B 2010, 114, 549-556
33. Rouhani, S.; Cartailler, J. P.; Facciotti, M. T.; Walian, P.; Needleman, R.; Lanyi, J. K.; Glaeser, R. M.; Luecke, H. Crystal structure of the D85S mutant of bacteriorhodopsin: Model of an O-like photocycle intermediate J. Mol. Biol. 2001, 313, 615
34. Facciotti, M. T.; Cheung, V. S.; Nguyen, D.; Rouhani, S.; Glaeser, R. M. Crystal structure of the bromide-bound D85S mutant of bacteriorhodopsin: Principles of ion pumping Biophys. J. 2003, 85, 451-458
35. Heymann, J. A. W.; Havelka, W. A.; Oesterhelt, D. Homologous overexpression of a light-driven anion pump in an archaebacterium Mol. Microbiol. 1993, 7, 623-630
36. Havelka, W. A.; Henderson, R.; Heymann, J. A. W.; Oesterhelt, D. Projection structure of halorhodopsin from Halobacterium halobium at 6 Å resolution obtained from electron cryo-microscopy J. Mol. Biol. 1993, 234, 837-845
37. Persike, N.; Pfeiffer, M.; Guckenberger, R.; Radmacher, M.; Fritz, M. Direct observation of different surface structures on high-resolution images of native halorhodopsin J. Mol. Biol. 2001, 310, 773-780
38. Simons, K.; Toomre, D. Lipid rafts and signal transduction Nat. Rev. Mol. Cell. Biol. 2000, 1, 31-41