Bacteriorhodopsin folds into the membrane against an external force

Journal of Molecular Biology

Volumn 357, Issue 2, 2006, Pages 644-654

  Kessler, Max ^a   Gottschalk, Kay E ^a   Janovjak, Harald ^b   Muller, Daniel J ^b   Gaub, Hermann E ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Bacteriorhodopsin; Folding; Helical hairpin; Membrane insertion; Single molecule force spectroscopy

Indexed keywords

BACTERIORHODOPSIN; MEMBRANE PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CARBOXY TERMINAL SEQUENCE; ENERGY; EXTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 33344474603     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.12.065     Document Type: Article

References (43)

1. A. Krogh, B. Larsson, G. von Heijne, and E.L. Sonnhammer Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 305 2001 567 580
2. D.O. Daley, M. Rapp, E. Granseth, K. Melen, D. Drew, and G. von Heijne Global topology analysis of the Escherichia coli inner membrane proteome Science 308 2005 1321 1323
3. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365
4. P.J. Booth, A.R. Curran, R.H. Templer, H. Lu, and W. Meijberg Manipulating the folding of membrane proteins: using the bilayer to our advantage Biochem. Soc. Symp. 68 2001 27 33
5. D.A. Cisneros, D. Oesterhelt, and D.J. Muller Probing origins of molecular interactions stabilizing the membrane proteins halorhodopsin and bacteriorhodopsin Structure (Camb) 13 2005 235 242
6. A. Kedrov, C. Ziegler, H. Janovjak, W. Kuhlbrandt, and D.J. Muller Controlled unfolding and refolding of a single sodium-proton antiporter using atomic force microscopy J. Mol. Biol. 340 2004 1143 1152
7. F. Kienberger, G. Kada, H. Mueller, and P. Hinterdorfer Single molecule studies of antibody-antigen interaction strength versus intra-molecular antigen stability J. Mol. Biol. 347 2005 597 606
8. G. Buldt, J. Heberle, N.A. Dencher, and H.J. Sass Structure, dynamics, and function of bacteriorhodopsin J. Protein Chem. 17 1998 536 538
9. N.A. Dencher, H.J. Sass, and G. Buldt Water and bacteriorhodopsin: structure, dynamics, and function Biochim. Biophys. Acta 1460 2000 192 203
10. H. Belrhali, P. Nollert, A. Royant, C. Menzel, J.P. Rosenbusch, E.M. Landau, and E. Pebay-Peyroula Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution Struct. Fold. Des. 7 1999 909 917
11. L. Essen, R. Siegert, W.D. Lehmann, and D. Oesterhelt Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex Proc. Natl Acad. Sci. USA 95 1998 11673 11678
12. N. Grigorieff, T.A. Ceska, K.H. Downing, J.M. Baldwin, and R. Henderson Electron-crystallographic refinement of the structure of bacteriorhodopsin J. Mol. Biol. 259 1996 393 421
13. H. Luecke, B. Schobert, H.T. Richter, J.P. Cartailler, and J.K. Lanyi Structure of bacteriorhodopsin at 1.55 Å resolution J. Mol. Biol. 291 1999 899 911
14. K. Mitsuoka, T. Hirai, K. Murata, A. Miyazawa, A. Kidera, Y. Kimura, and Y. Fujiyoshi The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: implication of the charge distribution J. Mol. Biol. 286 1999 861 882
15. F. Oesterhelt, D. Oesterhelt, M. Pfeiffer, A. Engel, H.E. Gaub, and D.J. Muller Unfolding pathways of individual bacteriorhodopsins Science 288 2000 143 146
16. D.J. Muller, M. Kessler, F. Oesterhelt, C. Moller, D. Oesterhelt, and H. Gaub Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy Biophys. J. 83 2002 3578 3588
17. M. Rief, M. Gautel, F. Oesterhelt, J.M. Fernandez, and H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112
18. M. Carrion-Vazquez, A.F. Oberhauser, S.B. Fowler, P.E. Marszalek, S.E. Broedel, J. Clarke, and J.M. Fernandez Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl Acad. Sci. USA 96 1999 3694 3699
19. M. Rief, M. Gautel, and H.E. Gaub Unfolding forces of titin and fibronectin domains directly measured by AFM Advan Exp. Med. Biol. 481 2000 129 136
20. H. Li, A.F. Oberhauser, S.B. Fowler, J. Clarke, and J.M. Fernandez Atomic force microscopy reveals the mechanical design of a modular protein Proc. Natl Acad. Sci. USA 97 2000 6527 6531
21. C. Gergely, J. Voegel, P. Schaaf, B. Senger, M. Maaloum, J.K. Horber, and J. Hemmerle Unbinding process of adsorbed proteins under external stress studied by atomic force microscopy spectroscopy Proc. Natl Acad. Sci. USA 97 2000 10802 10807
22. S.M. Altmann, R.G. Grunberg, P.F. Lenne, J. Ylanne, A. Raae, and K. Herbert Pathways and intermediates in forced unfolding of spectrin repeats Structure (Camb) 10 2002 1085 1096
23. I. Schwaiger, A. Kardinal, M. Schleicher, A.A. Noegel, and M. Rief A mechanical unfolding intermediate in an actin-crosslinking protein Nature Struct. Mol. Biol. 11 2004 81 85
24. H. Clausen-Schaumann, M. Rief, C. Tolksdorf, and H.E. Gaub Mechanical stability of single DNA molecules Biophys. J. 78 2000 1997 2007
25. A. Kedrov, H. Janovjak, C. Ziegler, W. Kuhlbrandt, and D.J. Muller Observing folding pathways and kinetics of a single sodium-proton antiporter from Escherichia coli J. Mol. Biol. 355 2006 2 8
26. T. Wieprecht, M. Beyermann, and J. Seelig Thermodynamics of the coil-alpha-helix transition of amphipathic peptides in a membrane environment: the role of vesicle curvature Biophys. Chem. 96 2002 191 201
27. A.S. Ladokhin, and S.H. White Folding of amphipathic alpha-helices on membranes: energetics of helix formation by melittin J. Mol. Biol. 285 1999 1363 1369
28. M. Soekarjo, M. Eisenhawer, A. Kuhn, and H. Vogel Thermodynamics of the membrane insertion process of the M13 procoat protein, a lipid bilayer traversing protein containing a leader sequence Biochemistry 35 1996 1232 1241
29. A.S. Ladokhin, and S.H. White Interfacial folding and membrane insertion of a designed helical peptide Biochemistry 43 2004 5782 5791
30. G. Hummer, and A. Szabo Free energy reconstruction from non-equilibrium single-molecule pulling experiments Proc. Natl Acad. Sci. USA 98 2001 3658 3661
31. D.M. Engelman, Y. Chen, C.N. Chin, A.R. Curran, A.M. Dixon, and A.D. Dupuy Membrane protein folding: beyond the two stage model FEBS Letters 555 2003 122 125
32. J.L. Popot, and D.M. Engelman Membrane protein folding and oligomerization: the two-stage model Biochemistry 29 1990 4031 4037
33. J.L. Popot, and D.M. Engelman Helical membrane protein folding, stability, and evolution Annu. Rev. Biochem. 69 2000 881 922
34. J.F. Hunt, P. Rath, K.J. Rothschild, and D.M. Engelman Spontaneous, pH-dependent membrane insertion of a transbilayer alpha-helix Biochemistry 36 1997 15177 15192
35. H. Janovjak, D.J. Muller, and A.D. Humphris Molecular force modulation spectroscopy revealing the dynamic response of single bacteriorhodopsins Biophys. J. 88 2005 1423 1431
36. S. Faham, D. Yang, E. Bare, S. Yohannan, J.P. Whitelegge, and J.U. Bowie Side-chain contributions to membrane protein structure and stability J. Mol. Biol. 335 2004 297 305
37. 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
38. D.J. Muller, M. Amrein, and A. Engel Adsorption of biological molecules to a solid support for scanning probe microscopy J. Struct. Biol. 119 1997 172 188
39. H.-J. Butt, and M. Jaschke Calculation of thermal noise in atomic force microscopy Nanotechnology 6 1995 1 7
40. E.L. Florin, M. Rief, H. Lehmann, M. Ludwig, C. Dornmair, V.T. Moy, and H.E. Gaub Sensing specific molecular interactions with the atomic force microscope Biosens. Bioelectr. 10 1995 895 901
41. C. Bustamante, J.F. Marko, E.D. Siggia, and S. Smith Entropic elasticity of lambda-phage DNA Science 265 1994 1599 1600
42. P.J. Booth, and A.R. Curran Membrane protein folding Curr. Opin. Struct. Biol. 9 1999 115 121
43. P.J. Booth Unravelling the folding of bacteriorhodopsin Biochim. Biophys. Acta 1460 2000 4 14