Role of extracellular glutamic acids in the stability and energy landscape of bacteriorhodopsin

Biophysical Journal

Volumn 95, Issue 7, 2008, Pages 3407-3418

  Sapra, K Tanuj ^a   Doehner, Jana ^a,d   Renugopalakrishnan, V ^b   Padrós, Esteve ^c   Muller, Daniel J ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; GLUTAMIC ACID;

ARTICLE; BIOMECHANICS; CHEMISTRY; EXTRACELLULAR SPACE; GENETICS; HALOBACTERIUM SALINARUM; KINETICS; METABOLISM; MUTATION; PROTEIN DENATURATION; THERMODYNAMICS;

BACTERIORHODOPSINS; BIOMECHANICS; EXTRACELLULAR SPACE; GLUTAMIC ACID; HALOBACTERIUM SALINARUM; KINETICS; MUTATION; PROTEIN DENATURATION; THERMODYNAMICS;

EID: 48649083203     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.131904     Document Type: Article

References (67)

1. Oesterhelt, D., and W. Stoeckenius. 1973. Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci. USA. 70:2853-2857.
2. Henderson, R., and P. N. T. Unwin. 1975. Three-dimensional model of purple membrane obtained by electron microscopy. Nature. 257:28-32.
3. Büldt, G., K. Konno, K. Nakanishi, H. J. Ploehn, B. N. Rao, and N. A. Dencher. 1991. Heavy-atom labeled retinal analogues located in bacteriorhodopsin by x-ray diffraction. Photochem. Photobiol. 54:873-879.
4. Jubb, J. S., D. L. Worcester, H. L. Crespi, and G. Zaccai. 1984. Retinal location in purple membrane of Halobacterium halobium: a neutron diffraction study of membranes labeled in vivo with deuterated retinal. EMBO J. 3:1455-1461.
5. Oesterhelt, D. 1973. Reversible dissociation of the purple complex in bacteriorhodopsin and identification of 13-cis and all-trans-retinal as its chromophores. Eur. J. Biochem. 40:453-463.
6. Lanyi, J. K. 2004. Bacteriorhodopsin. Annu. Rev. Physiol. 66:665-688.
7. Kedrov, A., H. Janovjak, K. T. Sapra, and D. J. Muller. 2007. Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 36:233-260.
8. Evans, E. 1998. Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Faraday Discuss. 111:1-16.
9. Evans, E. 2001. Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:105-128.
10. Sapra, K. T., P. S. Park, K. Palczewski, and D. J. Muller. 2008. Mechanical properties of bovine rhodopsin and bacteriorhodopsin: possible roles in folding and function. Langmuir. 24:1330-1337.
11. Dietz, H., F. Berkemeier, M. Bertz, and M. Rief. 2006. Anisotropic deformation response of single protein molecules. Proc. Natl. Acad. Sci. USA. 103:12724-12728.
12. Sanz, C., M. Marquez, A. Peralvarez, S. Elouatik, F. Sepulcre, E. Querol, T. Lazarova, and E. Padros. 2001. Contribution of extracellular Glu residues to the structure and function of bacteriorhodopsin. Presence of specific cation-binding sites. J. Biol. Chem. 276:40788-40794.
13. Luecke, H., H.-T. Richter, and J. K. Lanyi. 1998. Proton transfer pathways in bacteriorhodopsin at 2.3 Angstrom resolution. Science. 280:1934-1937.
14. Lanyi, J. K. 1997. Mechanisms of ion transport across membranes. J. Biol. Chem. 272:31209-31212.
15. Brown, L. S., J. Sasaki, H. Kandori, A. Maeda, R. Needleman, and J. K. Lanyi. 1995. Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol. Chem. 270:27122-27126.
16. Bondar, A. N., M. Elstner, S. Suhai, J. C. Smith, and S. Fischer. 2004. Mechanism of primary proton transfer in bacteriorhodopsin. Structure. 12:1281-1288.
17. Sampogna, R. V., and B. Honig. 1996. Electrostatic coupling between retinal isomerization and the ionization state of Glu-204: a general mechanism for proton release in bacteriorhodopsin. Biophys. J. 71:1165-1171.
18. as of Asp-85 and Glu-204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry. 35:4054-4062.
19. Sanz, C., T. Lazarova, F. Sepulcre, R. Gonzalez-Moreno, J. L. Bourdelande, E. Querol, and E. Padros. 1999. Opening the Schiff base moiety of bacteriorhodopsin by mutation of the four extracellular Glu side chains. FEBS Lett. 456:191-195.
20. 85 at alkaline pH in the photocycle of bacteriorhodopsin mutants containing E194Q. Biophys. J. 78:2022-2030.
21. Oesterhelt, D., and W. Stoeckenius. 1974. Isolation of the cell membrane of Halobacterium halobium and its fraction into red and purple membrane. Methods Enzymol. 31:667-678.
22. Oesterhelt, F., D. Oesterhelt, M. Pfeiffer, A. Engel, H. E. Gaub, and D. J. Müller. 2000. Unfolding pathways of individual bacteriorhodopsins. Science. 288:143-146.
23. Müller, D. J., M. Kessler, F. Oesterhelt, C. Möller, D. Oesterhelt, and H. E. Gaub. 2002. Stability of bacteriorhodopsin α-helices and loops analyzed by single-molecule force spectroscopy. Biophys. J. 83:3578-3588.
24. Kessler, M., and H. E. Gaub. 2006. Unfolding barriers in bacteriorhodopsin probed from the cytoplasmic and the extracellular side by AFM. Structure. 14:521-527.
25. Florin, E.-L., M. Rief, H. Lehmann, M. Ludwig, C. Dornmair, V. T. Moy, and H. E. Gaub. 1995. Sensing specific molecular interactions with the atomic force microscope. Biosens. Bioelectron. 10:895-901.
26. Butt, H.-J., and M. Jaschke. 1995. Calculation of thermal noise in atomic force microscopy. Nanotechnology. 6:1-7.
27. Janovjak, H., J. Struckmeier, M. Hubain, A. Kedrov, M. Kessler, and D. J. Müller. 2004. Probing the energy landscape of the membrane protein bacteriorhodopsin. Structure. 12:871-879.
28. Rief, M., M. Gautel, F. Oesterhelt, J. M. Fernandez, and H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112.
29. Dudko, O. K., G. Hummer, and A. Szabo. 2006. Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys. Rev. Lett. 96:108101-108104.
30. Dudko, O. K., A. E. Filippov, J. Klafter, and M. Urbakh. 2003. Beyond the conventional description of dynamic force spectroscopy of adhesion bonds. Proc. Natl. Acad. Sci. USA. 100:11378-11381.
31. Hummer, G., and A. Szabo. 2003. Kinetics from nonequilibrium single-molecule pulling experiments. Biophys. J. 85:5-15.
32. Best, R. B., S. B. Fowler, J. L. Toca-Herrera, and J. Clarke. 2002. A simple method for probing the mechanical unfolding pathway of proteins in detail. Proc. Natl. Acad. Sci. USA. 99:12143-12148.
33. Bell, G. I. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
34. Evans, E. 1999. Looking inside molecular bonds at biological interfaces with dynamic force spectroscopy. Biophys. Chem. 82:83-97.
35. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
36. Dietz, H., and M. Rief. 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. USA. 101:16192-16197.
37. Bieri, O., J. Wirz, B. Hellrung, M. Schutkowski, M. Drewello, and T. Kiefhaber. 1999. The speed limit for protein folding measured by triplet-triplet energy transfer. Proc. Natl. Acad. Sci. USA. 96:9597-9601.
38. Schlierf, M., and M. Rief. 2005. Temperature softening of a protein in single-molecule experiments. J. Mol. Biol. 354:497-503.
39. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer, Sunderland, MA.
40. Sapra, K. T., G. P. Balasubramanian, D. Labudde, J. U. Bowie, and D. J. Muller. 2008. Point mutations in membrane proteins reshape energy landscape and populate different unfolding pathways. J. Mol. Biol. 376:1076-1090.
41. Contera, S. A., V. Lemaitre, M. R. de Planque, A. Watts, and J. F. Ryan. 2005. Unfolding and extraction of a transmembrane α-helical peptide: dynamic force spectroscopy and molecular dynamics simulations. Biophys. J. 89:3129-3140.
42. Janovjak, H., A. Kedrov, D. A. Cisneros, K. T. Sapra, and D. J. Müller. 2006. Imaging and detecting molecular interactions of single transmembrane proteins. Neurobiol. Aging. 27:546-561.
43. Sapra, K. T., H. Besir, D. Oesterhelt, and D. J. Muller. 2006. Characterizing molecular interactions in different bacteriorhodopsin assemblies by single-molecule force spectroscopy. J. Mol. Biol. 355:640-650.
44. Saito, H., S. Yamaguchi, K. Ogawa, S. Tuzi, M. Marquez, C. Sanz, and E. Padros. 2004. Glutamic acid residues of bacteriorhodopsin at the extracellular surface as determinants for conformation and dynamics as revealed by site-directed solid-state 13CNMR. Biophys. J. 86:1673-1681.
45. Janovjak, H., M. Kessler, D. Oesterhelt, H. E. Gaub, and D. J. Müller. 2003. Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J. 22:5220-5229.
46. Kedrov, A., M. Krieg, C. Ziegler, W. Kuhlbrandt, and D. J. Müller. 2005. Locating ligand binding and activation of a single antiporter. EMBO Rep. 6:668-674.
47. 2+ in native bovine rhodopsin. J. Biol. Chem. 282:11377-11385.
48. Janovjak, H., H. Knaus, and D. J. Muller. 2007. Transmembrane helices have rough energy surfaces. J. Am. Chem. Soc. 129:246-247.
49. Nagy, J. K., and C. R. Sanders. 2004. Destabilizing mutations promote membrane protein misfolding. Biochemistry. 43:19-25.
50. Astier, Y., H. Bayley, and S. Howorka. 2005. Protein components for nanodevices. Curr. Opin. Chem. Biol. 9:576-584.
51. Bayley, H., and L. Jayasinghe. 2004. Functional engineered channels and pores. Mol. Membr. Biol. 21:209-220.
52. Leifert, W. R., A. L. Aloia, O. Bucco, R. V. Glatz, and E. J. McMurchie. 2005. G-protein-coupled receptors in drug discovery: nanosizing using cell-free technologies and molecular biology approaches. J. Biomol. Screen. 10:765-779.
53. Onuchic, J. N., P. G. Wolynes, Z. Luthey-Schulten, and N. D. Socci. 1995. Toward an outline of the topography of a realistic protein-folding funnel. Proc. Natl. Acad. Sci. USA. 92:3626-3630.
54. Wolynes, P. G., J. N. Onuchic, and D. Thirumalai. 1995. Navigating the folding routes. Science. 267:1619-1620.
55. Dill, K. A., and H. S. Chan. 1997. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4:10-19.
56. Bryngelson, J. D., J. N. Onuchic, N. D. Socci, and P. G. Wolynes. 1995. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins. 21:167-195.
57. Jahn, T. R., and S. E. Radford. 2005. The Yin and Yang of protein folding. FEBS J. 272:5962-5970.
58. Boehr, D. D., D. McElheny, H. J. Dyson, and P. E. Wright. 2006. The dynamic energy landscape of dihydrofolate reductase catalysis. Science. 313:1638-1642.
59. Frederick, K. K., M. S. Marlow, K. G. Valentine, and A. J. Wand. 2007. Conformational entropy in molecular recognition by proteins. Nature. 448:325-329.
60. Faham, S., D. Yang, E. Bare, S. Yohannan, J. P. Whitelegge, and J. U. Bowie. 2004. Side-chain contributions to membrane protein structure and stability. J. Mol. Biol. 335:297-305.
61. Yohannan, S., S. Faham, D. Yang, J. P. Whitelegge, and J. U. Bowie. 2004. The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc. Natl. Acad. Sci. USA. 101:959-963.
62. Oliveberg, M., and P. G. Wolynes. 2006. The experimental survey of protein-folding energy landscapes. Q. Rev. Biophys. 38:245-288.
63. Belrhali, H., P. Nollert, A. Royant, C. Menzel, J. P. Rosenbusch, E. M. Landau, and E. Pebay-Peyroula. 1999. Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 A resolution. Struct. Fold. Des. 7:909-917.
64. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 A resolution. J. Mol. Biol. 291:899-911.
65. Dencher, N. A., H. J. Saas, and G. Buldt. 2000. Water and bacteriorhodopsin: structure, dynamics and function. Biochim. Biophys. Acta. 1460:192-203.
66. 2H labeling and neutron scattering. Proc. Natl. Acad. Sci. USA. 95:4970-4975.
67. Thavasi, V., T. Lazarova, S. Filipek, M. Kolinski, E. Querol, A. Kumar, S. Ramakrishna, E. Padrós, V. Renugopalakrishnan. Study on the feasibility of bacteriorhodopsin as bio-photosensitizer in excitonic solar cell: a first report. J. Nanosci. and Nanotechnol. 2008. In press.