Effects of solubilization on the structure and function of the sensory rhodopsin II/transducer complex

Journal of Molecular Biology

Volumn 356, Issue 5, 2006, Pages 1207-1221

  Klare, Johann P ^a   Bordignon, Enrica ^b   Doebber, Meike ^b   Fitter, Jörg ^c   Kriegsmann, Jana ^c   Chizhov, Igor ^d   Steinhoff, Heinz Jürgen ^b   Engelhard, Martin ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Detergents; Membrane proteins; Phoborhodopsin; Phototaxis; Site directed spin labeling EPR

Indexed keywords

DETERGENT; LIPID; MEMBRANE PROTEIN; RECEPTOR PROTEIN; SENSORY RHODOPSIN;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM TRANSDUCTION; ELECTRON SPIN RESONANCE; FLUORESCENCE SPECTROSCOPY; LASER; LOW TEMPERATURE; NONHUMAN; PHOTOLYSIS; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; ROOM TEMPERATURE; SOLUBILIZATION; STOICHIOMETRY;

ARCHAEA; BACTERIA (MICROORGANISMS); NATRONOMONAS PHARAONIS;

EID: 32044442292     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.12.015     Document Type: Article

References (64)

1. E. Wallin, and G. von Heijne Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms Protein Sci. 7 1998 1029 1038
2. C.R. Sanders, and J.K. Myers Disease-related misassembly of membrane proteins Annu. Rev. Biophys. Biomol. Struct. 33 2004 25 51
3. S. Geibel, T. Friedrich, P. Ormos, P.G. Wood, G. Nagel, and E. Bamberg The voltage-dependent proton pumping in bacteriorhodopsin is characterized by optoelectric behavior Biophys. J. 81 2001 2059 2068
4. 2+-ATPase from sarcoplasmic reticulum J. Biol. Chem. 264 1989 4907 4915
5. P. Banerjee, J.B. Joo, J.T. Buse, and G. Dawson Differential solubilization of lipids along with membrane proteins by different classes of detergents Chem. Phys. Lip. 77 1995 65 78
6. L. Haneskog, L. Andersson, E. Brekkan, A.K. Englund, K. Keiichi, and L. Liljas Monomeric human red cell glucose transporter (Glut1) in non-ionic detergent solution and a semi-elliptical torus model for detergent binding to membrane proteins Biochim. Biophys. Acta 1282 1996 39 47
7. A.K. Mukhopadhyay, S. Bose, and R.W. Hendler Membrane-mediated control of the bacteriorhodopsin photocycle Biochemistry 33 1994 10889 10895
8. M.K. Joshi, S. Dracheva, A.K. Mukhopadhyay, S. Bose, and R.W. Hendler Importance of specific native lipids in controlling the photocycle of bacteriorhodopsin Biochemistry 37 1998 14463 14470
9. S. Dracheva, S. Bose, and R.W. Hendler Chemical and functional studies on the importance of purple membrane lipids in bacteriorhodopsin photocycle behaviour FEBS Letters 382 1996 209 212
10. C.R. Sanders, A. Kuhn Hoffmann, D.N. Gray, M.H. Keyes, and C.D. Ellis French swimwear for membrane proteins ChemBioChem 5 2004 423 426
11. A.M. Seddon, P. Curnow, and P.J. Booth Membrane proteins, lipids and detergents: not just a soap opera Biochim. Biophys. Acta 1666 2004 105 117
12. R.M. Garavito, and S. Ferguson-Miller Detergents as tools in membrane biochemistry J. Biol. Chem. 276 2001 32403 32406
13. U. Haupts, J. Tittor, and D. Oesterhelt Closing in on bacteriorhodopsin: progress in understanding the molecule Annu. Rev. Biophys. Biomol. Struct. 28 1999 367 399
14. G. Schäfer, M. Engelhard, and V. Müller Bioenergetics of the Archaea Microbiol. Mol. Biol. Rev. 63 1999 570 620
15. J.L. Spudich, C.-S. Yang, K.-H. Jung, and E.N. Spudich Retinylidene proteins: structures and functions from Archaea to humans Annu. Rev. Cell Dev. Biol. 16 2000 365 392
16. J.L. Spudich, and H. Luecke Sensory rhodopsin II: functional insights from structure Curr. Opin. Struct. Biol. 12 2002 540 546
17. J.P. Klare, V.I. Gordeliy, J. Labahn, G. Buldt, H.J. Steinhoff, and M. Engelhard The archaeal sensory rhodopsin II/transducer complex: a model for transmembrane signal transfer FEBS Letters 564 2004 219 224
18. I. Chizhov, G. Schmies, R.P. Seidel, J.R. Sydor, B. Lüttenberg, and M. Engelhard The photophobic receptor from Natronobacterium pharaonis: temperature and pH dependencies of the photocycle of sensory rhodopsin II Biophys. J. 75 1998 999 1009
19. A.A. Wegener, I. Chizhov, M. Engelhard, and H.-J. Steinhoff Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II J. Mol. Biol. 301 2000 881 891
20. J.P. Klare, E. Bordignon, M. Engelhard, and H.-J. Steinhoff Sensory rhodopsin II and bacteriorhodopsin: light activated helix F movement Photochem. Photobiol. Sci. 3 2004 543 547
21. W.D. Hoff, K.-H. Jung, and J.L. Spudich Molecular mechanism of photosignalling by archaeal sensory rhodopsins Annu. Rev. Biophys. Biomol. Struct. 26 1997 223 258
22. Y. Sudo, M. Iwamoto, K. Shimono, and N. Kamo Pharaonis phoborhodopsin binds to its cognate truncated transducer even in the presence of a detergent with a 1:1 stoichiometry Photochem. Photobiol. 74 2001 489 494
23. Y. Sudo, H. Okuda, M. Yamabi, Y. Fukuzaki, M. Mishima, N. Kamo, and C. Kojima Linker region of a halobacterial transducer protein interacts directly with its sensor retinal protein Biochemistry 44 2005 6144 6152
24. S. Hippler-Mreyen, J.P. Klare, A.A. Wegener, R. Seidel, C. Herrmann, and G. Schmies Probing the sensory rhodopsin II binding domain of its cognate transducer by calorimetry and electrophysiology J. Mol. Biol. 330 2003 1203 1213
25. Y. Sudo, M. Iwamoto, K. Shimono, and N. Kamo Association between a photo-intermediate of a M-lacking mutant D75N of pharaonis phoborhodopsin and its cognate transducer J. Photochem. Photobiol. B 67 2002 171 176
26. Y. Sudo, M. Iwamoto, K. Shimono, and N. Kamo Tyr-199 and charged residues of pharaonis phoborhodopsin are important for the interaction with its transducer Biophys. J. 83 2002 427 432
27. Y. Furutani, K. Kamada, Y. Sudo, K. Shimono, N. Kamo, and H. Kandori Structural changes of the complex between pharaonis phoborhodopsin and its cognate transducer upon formation of the M photointermediate Biochemistry 44 2005 2909 2915
28. C.S. Yang, O. Sineshchekov, E.N. Spudich, and J.L. Spudich The cytoplasmic membrane-proximal domain of the HtrII transducer interacts with the E-F loop of photoactivated natronomonas pharaonis sensory rhodopsin II J. Biol. Chem. 279 2004 42970 42976
29. V.I. Gordeliy, J. Labahn, R. Moukhametzianov, R. Efremov, J. Granzin, and R. Schlesinger Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex Nature 419 2002 484 487
30. A.A. Wegener, J.P. Klare, M. Engelhard, and H.-J. Steinhoff Structural insights into the early steps of receptor-transducer signal transfer in archaeal phototaxis EMBO J. 20 2001 5312 5319
31. Y. Sudo, M. Yamabi, M. Iwamoto, K. Shimono, and N. Kamo Interaction of Natronobacterium pharaonis phoborhodopsin (sensory rhodopsin II) with its cognate transducer probed by increase in the thermal stability Photochem. Photobiol. 78 2003 511 516
32. J. Sasaki, and J.L. Spudich The transducer protein HtrII modulates the lifetimes of sensory rhodopsin II photointermediates Biophys. J. 75 1998 2435 2440
33. Y. Sudo, M. Iwamoto, K. Shimono, M. Sumi, and N. Kamo Photo-induced proton transport of pharaonis phoborhodopsin (sensory rhodopsin II) Is Ceased by association with the transducer Biophys. J. 80 2001 916 922
34. V. Buschmann, K.D. Weston, and M. Sauer Spectroscopic study and evaluation of red-absorbing fluorescent dyes Bioconjug. Chem. 14 2003 195 204
35. N. Marme, J.-P. Knemeyer, M. Sauer, and J. Wolfrum Inter- and intramolecular fluorescence quenching of organic dyes by tryptophan Bioconjug. Chem. 14 2003 1133 1139
36. J.R. Maddock, and L. Shapiro Polar location of the chemoreceptor complex in the Escherichia coli cell Science 259 1993 1717 1723
37. T.S. Shimizu, N. Le Novere, M.D. Levin, A.J. Beavil, B.J. Sutton, and D. Bray Molecular model of a lattice of signalling proteins involved in bacterial chemotaxis Nature Cell Biol. 2 2000 792 796
38. R. Henderson, and P.N.T. Unwin Three-dimensional model of purple membrane obtained by electron microscopy Nature 257 1975 28 32
39. S.H. Kim, W. Wang, and K.K. Kim Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity Proc. Natl Acad. Sci. USA 99 2002 11611 11615
40. W.L. Hubbell, H.S. Mchourab, C. Altenbach, and M.A. Lietzow Watching Proteins move using site-directed spin labeling Structure 4 1996 779 783
41. W.L. Hubbell, A. Gross, R. Langen, and M.A. Lietzow Recent advances in site-directed spin labeling of proteins Curr. Opin. Struct. Biol. 8 1998 649 656
42. L.J. Berliner Spin Labeling: The Next Millennium 1998 Academic Press New York
43. H.-J. Steinhoff Methods for study of protein dynamics and protein-protein interaction in proteinubiquitination by electron paramagnetic resonance spectroscopy Front. Biosci. 7 2002 c97 c110
44. C. Altenbach, T. Marti, H.G. Khorana, and W.L. Hubbell Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants Science 248 1990 1088 1092
45. M. Pfeiffer, T. Rink, K. Gerwert, D. Oesterhelt, and H.-J. Steinhoff Site-directed spin-labeling reveals the orientation of the amino acid side-chains in the E-F loop of bacteriorhodopsin J. Mol. Biol. 287 1999 163 171
46. E. Bordignon, J.P. Klare, M. Doebber, A.A. Wegener, S. Martell, M. Engelhard, and H.-J. Steinhoff Structural analysis of a HAMP domain: the linker region of the phototransducer in complex with sensory rhodopsin II J. Biol. Chem. 280 2005 38767 38775
47. H.S. Mchaourab, M.A. Lietzow, K. Hideg, and W.L. Hubbell Motion of spin-labeled side chains in T4 Lysozyme. Correlation with protein structure and dynamics Biochemistry 35 1996 7692 7704
48. W.L. Hubbell, D.S. Cafiso, and C. Altenbach Identifying conformational changes with site-directed spin labeling Nature Struct. Biol. 7 2000 735 739
49. R. Medina, D. Perdomo, and J. Bubis The hydrodynamic properties of dark- and light-activted states of n-dodecyl β-d-maltoside-solubilized bovine rhodopsin support the dimeric structure of both conformations J. Biol. Chem. 279 2004 39565 39573
50. O. Meyer, M. Ollivon, and M.T. Paternostre Solubilization steps of dark-adapted purple membrane by Triton X-100: a spectroscopic study FEBS Letters 305 1992 249 253
51. H.-J. Steinhoff, A. Savitsky, C. Wegener, M. Pfeiffer, M. Plato, and K. Möbius High-field EPR studies of the structure and conformational changes of site-directed spin labeled bacteriorhodopsin Biochim. Biophys. Acta 1457 2000 253 262
52. M. Plato, H.-J. Steinhoff, C. Wegener, J.T. Törring, A. Savitsky, and K. Möbius Molecular orbital study of polarity and hydrogen bonding effects on the g and hyperfine tensors of site directed NO spin labelled bacteriorhodopsin Mol. Phys. 100 2002 3711 3721
53. 13C NMR Biochim. Biophys. Acta 1375 1998 84 92
54. A.M. Stanley, and K.G. Fleming The transmembrane domains of ErbB receptors do not dimerize strongly in micelles J. Mol. Biol. 347 2005 759 772
55. J.M. Gonzalez-Manas, G. Montoya, C. Rodriguez-Fernandez, J.I.G. Gurtubay, and F.M. Goni The interaction of Triton X-100 with purple membrane: effect of light-dark adaptation Biochim. Biophys. Acta 1019 1990 167 169
56. I. Kovacs, K. Hollos-Nagy, and G. Varo Dark adaptation and spectral changes in Triton X-100-treated bacteriorhodopsin J. Photochem. Photobiol. B 27 1995 21 25
57. J. Liang, L. Adamian, and J. Jackups The membrane-water interface region of membrane proteins: structural bias and the anti-snorkeling effect Trends Biochem. Sci. 30 2005 355 357
58. S.R. Hubbard, and J.H. Till Protein tyrosine kinase structure and function Annu. Rev. Biochem. 69 2000 373 398
59. I.P. Hohenfeld, A.A. Wegener, and M. Engelhard Purification of Histidine tagged bacteriorhodopsin pharaonis halorhodopsin and pharaonis sensory rhodopsin II functionally expressed in Escherichia coli FEBS Letters 442 1999 198 202
60. S.N. Ho, H.D. Hunt, R.M. Horton, J.K. Pullen, and L.R. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 59
61. M. Kates, S.C. Kushawa, and G.D. Sprott Lipids of purple membrane from extreme halophiles and of methanogenic bacteria Methods Enzymol. 88 1982 98 111
62. K. Shimono, M. Iwamoto, M. Sumi, and N. Kamo Functional expression of pharaonis phoborhodopsin in Escherichia coli FEBS Letters 420 1997 54 56
63. C. Altenbach, D.A. Greenhalgh, H.G. Khorana, and W.L. Hubbell A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin Proc. Natl Acad. Sci. USA 91 1994 1667 1671
64. H.-J. Steinhoff, N. Radzwill, W. Thevis, V. Lenz, D. Brandenburg, and A. Antson Determination of interspin distances between spin labels attached to insulin: comparison of electron paramagnetic resonance data with the X-ray structure Biophys. J. 73 1997 3287 3298