Probing the energy landscape of the membrane protein bacteriorhodopsin

Structure

Volumn 12, Issue 5, 2004, Pages 871-879

  Janovjak, Harald ^a   Struckmeier, Jens ^c   Hubain, Maurice ^a   Kedrov, Alexej ^a   Kessler, Max ^b   Müller, Daniel J ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c Veeco Metrology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; MEMBRANE PROTEIN;

ALPHA HELIX; ARTICLE; ATOMIC FORCE MICROSCOPY; ENERGY; MONTE CARLO METHOD; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; SPECTROSCOPY;

BACTERIORHODOPSINS; HALOBACTERIUM SALINARUM; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY; SPECTRUM ANALYSIS;

BACTERIA (MICROORGANISMS);

EID: 2342646040     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2004.03.016     Document Type: Article

References (45)

1. Allen S.J., Kim J.M., Khorana H.G., Lu H., Booth P.J. Structure and function in bacteriorhodopsin. the effect of the interhelical loops on the protein folding kinetics J. Mol. Biol. 308:2001;423-435
2. Baldwin J.M. The probable arrangement of the helices in G protein-coupled receptors. EMBO J. 12:1993;1693-1703
3. Bell G.I. Models for the specific adhesion of cells to cells. Science. 200:1978;618-627
4. Belrhali H., Nollert P., Royant A., Menzel C., Rosenbusch J.P., Landau E.M., Pebay-Peyroula E. Protein, lipid and water organization in bacteriorhodopsin crystals. a molecular view of the purple membrane at 1.9 A resolution Struct. Fold. Des. 7:1999;909-917
5. Best R.B., Li B., Steward A., Daggett V., Clarke J. Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophys. J. 81:2001;2344-2356
6. Best R.B., Fowler S.B., Toca-Herrera J.L., Clarke J. A simple method for probing the mechanical unfolding pathway of proteins in detail. Proc. Natl. Acad. Sci. USA. 99:2002;12143-12148
7. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Phys. Rev. Lett. 56:1986;930-933
8. Booth P.J., Templer R.H., Curran A.R., Allen S.J. Can we identify the forces that drive the folding of integral membrane proteins? Biochem. Soc. Trans. 29:2001;408-413
9. Carrion-Vazquez M., Oberhauser A.F., Fowler S.B., Marszalek P.E., Broedel S.E., Clarke J., Fernandez J.M. Mechanical and chemical unfolding of a single protein. a comparison Proc. Natl. Acad. Sci. USA. 96:1999;3694-3699
10. Engelman D.M., Steitz T.A. The spontaneous insertion of proteins into and across membranes. the helical hairpin hypothesis Cell. 23:1981;411-422
11. Essen L., Siegert R., Lehmann W.D., Oesterhelt D. Lipid patches in membrane protein oligomers. crystal structure of the bacteriorhodopsin-lipid complex Proc. Natl. Acad. Sci. USA. 95:1998;11673-11678
12. Evans E.B. Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophys. Chem. 82:1999;83-97
13. Evans E., Ludwig F. Dynamic strengths of molecular anchoring and material cohesion in fluid biomembranes. J. Phys. Condens. Matter. 12:2000;A315-A320
14. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1997;1541-1555
15. Florin E.L., Rief M., Lehmann H., Ludwig M., Dornmair C., Moy V.T., Gaub H.E. Sensing specific molecular-interactions with the atomic force microscope. Biosens. Bioelectron. 10:1995;895-901
16. Grigorieff N., Ceska T.A., Downing K.H., Baldwin J.M., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:1996;393-421
17. Haltia T., Freire E. Forces and factors that contribute to the structural stability of membrane proteins. Biochim. Biophys. Acta. 1241:1995;295-322
18. Helmreich E.J., Hofmann K.P. Structure and function of proteins in G-protein-coupled signal transfer. Biochim. Biophys. Acta. 1286:1996;285-322
19. Heymann B., Grubmüller H. Dynamic force spectroscopy of molecular adhesion bonds. Phys. Rev. Lett. 84:2000;6126-6129
20. Hunt J.F., Earnest T.N., Bousche O., Kalghatgi K., Reilly K., Horvath C., Rothschild K.J., Engelman D.M. A biophysical study of integral membrane protein folding. Biochemistry. 36:1997;15156-15176
21. Janovjak H., Kessler M., Oesterhelt D., Gaub H., Muller D.J. Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J. 22:2003;5220-5229
22. Kolbe M., Besir H., Essen L.O., Oesterhelt D. Structure of the light-driven chloride pump halorhodopsin at 1.8 A resolution. Science. 288:2000;1390-1396
23. Lanyi J.K. Progress toward an explicit mechanistic model for the light-driven pump, bacteriorhodopsin. FEBS Lett. 464:1999;103-107
24. Leckband D., Israelachvili J. Intermolecular forces in biology. Q. Rev. Biophys. 34:2001;105-267
25. Lodish H., Berk A., Zipursky L.S., Matsudaira P., Baltimore D., Darnell J.E. Molecular Cell Biology. Fourth Edition:1999;W.H. Freeman and Company, New York
26. Luecke H., Schobert B., Richter H.T., Cartailler J.P., Lanyi J.K. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:1999;899-911
27. Marti T. Refolding of bacteriorhodopsin from expressed polypeptide fragments. J. Biol. Chem. 273:1998;9312-9322
28. Merkel R., Nassoy P., Leung A., Ritchie K., Evans E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:1999;50-53
29. Mitsuoka K., Hirai T., Murata K., Miyazawa A., Kidera A., Kimura Y., Fujiyoshi Y. 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
30. Möller C., Fotiadis D., Suda K., Engel A., Kessler M., Muller D.J. Determining molecular forces that stabilize human aquaporin-1. J. Struct. Biol. 142:2003;369-378
31. Müller D.J., Schabert F.A., Büldt G., Engel A. Imaging purple membranes in aqueous solutions at sub-nanometer resolution by atomic force microscopy. Biophys. J. 68:1995;1681-1686
32. Müller D.J., Amrein M., Engel A. Adsorption of biological molecules to a solid support for scanning probe microscopy. J. Struct. Biol. 119:1997;172-188
33. Müller D.J., Kessler M., Oesterhelt F., Möller C., Oesterhelt D., Gaub H. Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy. Biophys. J. 83:2002;3578-3588
34. Oesterhelt D., Stoeckenius W. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31:1974;667-678
35. Oesterhelt F., Oesterhelt D., Pfeiffer M., Engel A., Gaub H.E., Müller D.J. Unfolding pathways of individual bacteriorhodopsins. Science. 288:2000;143-146
36. Palczewski K., Kumasaka T., Hori T., Behnke C.A., Motoshima H., Fox B.A., Le Trong I., Teller D.C., Okada T., Stenkamp R.E., et al. Crystal structure of rhodopsin. A G protein-coupled receptor Science. 289:2000;739-745
37. Popot J.L., Engelman D.M. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:2000;881-922
38. Popot J.L., Gerchman S.E., Engelman D.M. Refolding of bacteriorhodopsin in lipid bilayers. A thermodynamically controlled two-stage process. J. Mol. Biol. 198:1987;655-676
39. Radford S.E. Protein folding. progress made and promises ahead Trends Biochem. Sci. 25:2000;611-618
40. Rief M., Gautel M., Oesterhelt F., Fernandez J.M., Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1997;1109-1112
41. Rief M., Fernandez J.M., Gaub H.E. Elastically coupled two-level systems as a model for biopolymer extensibility. Phys. Rev. Lett. 81:1998;4764-4767
42. 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-A resolution. Proc. Natl. Acad. Sci. USA. 98:2001;10131-10136
43. Subramaniam S. The structure of bacteriorhodopsin. an emerging consensus Curr. Opin. Struct. Biol. 9:1999;462-468
44. White S.H., Wimley W.C. Membrane protein folding and stability. physical principles Annu. Rev. Biophys. Biomol. Struct. 28:1999;319-365
45. Williams P.M., Fowler S.B., Best R.B., Toca-Herrera J.L., Scott K.A., Steward A., Clarke J. Hidden complexity in the mechanical properties of titin. Nature. 422:2003;446-449