Tuning the Photocycle Kinetics of Bacteriorhodopsin in Lipid Nanodiscs

Biophysical Journal

Volumn 109, Issue 9, 2015, Pages 1899-1906

  Lee, Tsung Yen ^a   Yeh, Vivien ^b,c   Chuang, Julia ^c   Chung Chan, Jerry Chun ^b   Chu, Li Kang ^a   Yu, Tsyr Yan ^c  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c INSTITUTE OF ATOMIC AND MOLECULAR SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

1,2-DIOLEOYL-SN-GLYCERO-3-PHOSPHOGLYCEROL; 1,2-OLEOYLPHOSPHATIDYLCHOLINE; ARTIFICIAL MEMBRANE; BACTERIORHODOPSIN; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLGLYCEROL; MICELLE; NANOMATERIAL; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL;

ARTIFICIAL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; HALOBACTERIUM SALINARUM; MICELLE; PURPLE MEMBRANE; SPECTROSCOPY;

BACTERIORHODOPSINS; DIMYRISTOYLPHOSPHATIDYLCHOLINE; HALOBACTERIUM SALINARUM; MEMBRANES, ARTIFICIAL; MICELLES; MOLECULAR STRUCTURE; NANOSTRUCTURES; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; PURPLE MEMBRANE; SPECTRUM ANALYSIS;

EID: 84947439769     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.09.012     Document Type: Article

References (49)

1. T.H. Bayburt, and S.G. Sligar Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers Protein Sci. 12 2003 2476 2481
2. S. Banerjee, T. Huber, and T.P. Sakmar Rapid incorporation of functional rhodopsin into nanoscale apolipoprotein bound bilayer (NABB) particles J. Mol. Biol. 377 2008 1067 1081
3. A. Nath, W.M. Atkins, and S.G. Sligar Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins Biochemistry 46 2007 2059 2069
4. A. Pandit, and N. Shirzad-Wasei W.J. de Grip Assembly of the major light-harvesting complex II in lipid nanodiscs Biophys. J. 101 2011 2507 2515
5. T.H. Bayburt, and S.A. Vishnivetskiy V.V. Gurevich Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding J. Biol. Chem. 286 2011 1420 1428
6. M.R. Whorton, and M.P. Bokoch R.K. Sunahara A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein Proc. Natl. Acad. Sci. USA 104 2007 7682 7687
7. N. Mitra, and Y. Liu E.C.Y. Yan Calcium-dependent ligand binding and G-protein signaling of family B GPCR parathyroid hormone 1 receptor purified in nanodiscs ACS Chem. Biol. 8 2013 617 625
8. F. Hagn, and M. Etzkorn G. Wagner Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins J. Am. Chem. Soc. 135 2013 1919 1925
9. M. Etzkorn, and T. Raschle G. Wagner Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility Structure 21 2013 394 401
10. T.H. Bayburt, Y.V. Grinkova, and S.G. Sligar Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins Nano Lett. 2 2002 853 856
11. T.H. Bayburt, and S.G. Sligar Membrane protein assembly into nanodiscs FEBS Lett. 584 2010 1721 1727
12. I.G. Denisov, and Y.V. Grinkova S.G. Sligar Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size J. Am. Chem. Soc. 126 2004 3477 3487
13. M. Wadsäter, and S. Maric M. Cardenas The effect of using binary mixtures of zwitterionic and charged lipids on nanodisc formation and stability Soft Matter 9 2013 2329 2337
14. I.G. Denisov, and M.A. McLean S.G. Sligar Thermotropic phase transition in soluble nanoscale lipid bilayers J. Phys. Chem. B 109 2005 15580 15588
15. V.M. Hernández-Rocamora, and B. Reija M. Vicente Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs J. Biol. Chem. 287 2012 30097 30104
16. D. Oesterhelt, and W. Stoeckenius Rhodopsin-like protein from the purple membrane of Halobacterium halobium Nat. New Biol. 233 1971 149 152
17. T.H. Bayburt, Y.V. Grinkova, and S.G. Sligar Assembly of single bacteriorhodopsin trimers in bilayer nanodiscs Arch. Biochem. Biophys. 450 2006 215 222
18. P.J.M. Johnson, and A. Halpin R.J. Dwayne Miller The photocycle and ultrafast vibrational dynamics of bacteriorhodopsin in lipid nanodiscs Phys. Chem. Chem. Phys. 16 2014 21310 21320
19. J.K. Lanyi Molecular mechanism of ion transport in bacteriorhodopsin: insights from crystallographic, spectroscopic, kinetic, and mutational studies J. Phys. Chem. B 104 2000 11441 11448
20. A.V. Sharkov, and A.V. Pakulev Y.A. Matveetz Primary events in bacteriorhodopsin probed by subpicosecond spectroscopy Biochim. Biophys. Acta 808 1985 94 102
21. L. Zimányi, and G. Váró J.K. Lanyi Pathways of proton release in the bacteriorhodopsin photocycle Biochemistry 31 1992 8535 8543
22. K.J. Rothschild FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model J. Bioenerg. Biomembr. 24 1992 147 167
23. G. Váró, and J.K. Lanyi Kinetic and spectroscopic evidence for an irreversible step between deprotonation and reprotonation of the Schiff base in the bacteriorhodopsin photocycle Biochemistry 30 1991 5008 5015
24. J.E. Morgan, and A.S. Vakkasoglu A. Maeda Coordinating the structural rearrangements associated with unidirectional proton transfer in the bacteriorhodopsin photocycle induced by deprotonation of the proton-release group: a time-resolved difference FTIR spectroscopic study Biochemistry 49 2010 3273 3281
25. P. Phatak, and N. Ghosh M. Elstner Amino acids with an intermolecular proton bond as proton storage site in bacteriorhodopsin Proc. Natl. Acad. Sci. USA 105 2008 19672 19677
26. K. Gerwert, G. Souvignier, and B. Hess Simultaneous monitoring of light-induced changes in protein side-group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier-transform infrared spectroscopy Proc. Natl. Acad. Sci. USA 87 1990 9774 9778
27. 640 photointermediate Biochemistry 22 1983 6141 6148
28. J. Riesle, and D. Oesterhelt J. Heberle D38 is an essential part of the proton translocation pathway in bacteriorhodopsin Biochemistry 35 1996 6635 6643
29. H.-T. Richter, and R. Needleman J.K. Lanyi Relationship of retinal configuration and internal proton transfer at the end of the bacteriorhodopsin photocycle Biochemistry 35 1996 15461 15466
30. J.K. Lanyi X-ray diffraction of bacteriorhodopsin photocycle intermediates Mol. Membr. Biol. 21 2004 143 150 (Review)
31. S. Dracheva, S. Bose, and R.W. Hendler Chemical and functional studies on the importance of purple membrane lipids in bacteriorhodopsin photocycle behavior FEBS Lett. 382 1996 209 212
32. J.-P. Cartailler, and H. Luecke X-ray crystallographic analysis of lipid-protein interactions in the bacteriorhodopsin purple membrane Annu. Rev. Biophys. Biomol. Struct. 32 2003 285 310
33. A. Corcelli, and V.M.T. Lattanzio F. Fanizzi Lipid-protein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane J. Lipid Res. 43 2002 132 140
34. Y. Yokoyama, and L. Negishi S. Mitaku Effect of lipid phase transition on molecular assembly and structural stability of bacteriorhodopsin reconstituted into phosphatidylcholine liposomes with different acyl-chain lengths J. Phys. Chem. B 114 2010 15706 15711
35. C.D. Heyes, and M.A. El-Sayed The role of the native lipids and lattice structure in bacteriorhodopsin protein conformation and stability as studied by temperature-dependent Fourier transform-infrared spectroscopy J. Biol. Chem. 277 2002 29437 29443
36. N.A. Dencher, and M.P. Heyn Formation and properties of bacteriorhodopsin monomers in the non-ionic detergents octyl-β-D-glucoside and Triton X-100 FEBS Lett. 96 1978 322 326
37. S.M. Barnett, and S. Dracheva I.W. Levin Lipid-induced conformational changes of an integral membrane protein: an infrared spectroscopic study of the effects of Triton X-100 treatment on the purple membrane of Halobacterium halobium ET1001 Biochemistry 35 1996 4558 4567
38. M.K. Joshi, and S. Dracheva R.W. Hendler Importance of specific native lipids in controlling the photocycle of bacteriorhodopsin Biochemistry 37 1998 14463 14470
39. C. Roos, and M. Zocher F. Bernhard Characterization of co-translationally formed nanodisc complexes with small multidrug transporters, proteorhodopsin and with the E. coli MraY translocase Biochim. Biophys. Acta 1818 2012 3098 3106
40. D. Oesterhelt, and W. Stoeckenius Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane Methods Enzymol. 31 1974 667 678
41. J. Wang, and S. Link M.A. El-Sayed Comparison of the dynamics of the primary events of bacteriorhodopsin in its trimeric and monomeric states Biophys. J. 83 2002 1557 1566
42. J. Heberle, and J. Riesle N.A. Dencher Proton migration along the membrane surface and retarded surface to bulk transfer Nature 370 1994 379 382
43. C.D. Heyes, and M.A. El-Sayed Proton transfer reactions in native and deionized bacteriorhodopsin upon delipidation and monomerization Biophys. J. 85 2003 426 434
44. M. Hoffmann, and M. Wanko M. Elstner Color tuning in rhodopsins: the mechanism for the spectral shift between bacteriorhodopsin and sensory rhodopsin II J. Am. Chem. Soc. 128 2006 10808 10818
45. C.G. Brouillette, and R.B. McMichens H.G. Khorana Structure and thermal stability of monomeric bacteriorhodopsin in mixed phospholipid/detergent micelles Proteins 5 1989 38 46
46. R. Casadio, and H. Gutowitz W. Stoeckenius Light-dark adaptation of bacteriorhodopsin in triton-treated purple membrane Biochim. Biophys. Acta 590 1980 13 23
47. J.Y. Cassim Unique biphasic band shape of the visible circular dichroism of bacteriorhodopsin in purple membrane: excitons, multiple transitions or protein heterogeneity? Biophys. J. 63 1992 1432 1442
48. G. Váró, R. Needleman, and J.K. Lanyi Protein structural change at the cytoplasmic surface as the cause of cooperativity in the bacteriorhodopsin photocycle Biophys. J. 70 1996 461 467
49. P. Scherrer, and U. Alexiev M.P. Heyn Covalently bound pH-indicator dyes at selected extracellular or cytoplasmic sites in bacteriorhodopsin. 1. Proton migration along the surface of bacteriorhodopsin micelles and its delayed transfer from surface to bulk Biochemistry 33 1994 13684 13692