Estimation of Helix-Helix Association Free Energy from Partial Unfolding of Bacterioopsin

Biochemistry

Volumn 43, Issue 2, 2004, Pages 550-559

  Nannepaga, Suraj John ^a   Gawalapu, Ravikumar ^a   Velasquez, Daniel ^a   Renthal, Robert ^a,b  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENTS; DISSOCIATION; ETHANOL; EXTRAPOLATION; FLUORESCENCE; FREE ENERGY; LIGHT SCATTERING; MICELLES; PROTEINS; RESONANCE;

ASSOCIATION CONSTANT;

BIOCHEMISTRY;

ALCOHOL; BACTERIOPSIN; CHYMOTRYPSIN; DANSYL CHLORIDE; DETERGENT; MEMBRANE PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL REACTION KINETICS; DISSOCIATION; ENERGY TRANSFER; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUOROMETRY; LIGHT SCATTERING; MEASUREMENT; MICELLE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; THERMODYNAMICS;

BACTERIORHODOPSINS; DANSYL COMPOUNDS; ETHANOL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUCOSIDES; HALOBACTERIUM SALINARUM; KINETICS; LIGHT; LYSINE; MICELLES; MODELS, CHEMICAL; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SCATTERING, RADIATION; SOLVENTS; TRYPTOPHAN;

EID: 0347724021     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034875c     Document Type: Article

References (55)

1. Popot, J.-L., and Engelman, D. M. (2000) Helical membrane protein folding, stability, and evolution, Annu. Rev. Biochem. 69, 881-922.
2. Rees, D. C., DeAntonio, L., and Eisenberg, D. (1989) Hydrophobic organization of membrane proteins, Science 245, 510-513.
3. Liao, M. J., London, E., and Khorana, H. G. (1983) Regeneration of the native bacteriorhodopsin structure from two chymotryptic fragments, J. Biol. Chem. 258, 9949-9955.
4. Liao, M.-J., Huang, K.-S., and Khorana, H. G. (1984) Regeneration of native bacteriorhodopsin structure from fragments, J. Biol. Chem. 259, 4200-4204.
5. Sigrist, H., Wenger, R. H., Kislig, E., and Wuthrich, M. (1988) Refolding of bacteriorhodopsin. Protease V8 fragmentation and chromophore reconstitution from proteolytic V8 fragments, Eur. J. Biochem. 177, 125-133.
6. Gilles-Gonzalez, M. A., Engelman, D. M., and Khorana, H. G. (1991) Structure-function studies of bacteriorhodopsin XV. Effects of deletions in loops B-C and E-F on bacteriorhodopsin chromophore and structure, J. Biol. Chem. 266, 8545-8550.
7. Kahn, T. W., and Engelman, D. M. (1992) Bacteriorhodopsin can be refolded from two independently stable transmembrane helices and the complementary five-helix fragment, Biochemistry 31, 6144-6151.
8. Marti, T. (1998) Refolding of bacteriorhodopsin from expressed polypeptide fragments, J. Biol. Chem. 273, 9312-9322.
9. Kim, J.-M., Booth, P. J., Allen, S. J., and Khorana, H. G. (2001) Structure and function in bacteriorhodopsin: the role of the interhelical loops in the folding and stability of bacteriorhodopsin, J. Mol. Biol. 308, 409-422.
10. Zhou, F. X., Cocco, M. J., Russ, W. P., Brunger, A. T., and Engelman, D. M. (2000) Interhelical hydrogen bonding drives strong interactions in membrane proteins, Nat. Struct. Biol. 7, 154-160.
11. Zhou, F. X., Merianos, H. J., Brunger, A. T., and Engelman, D. M. (2001) Polar residues drive association of polyleucine transmembrane helices, Proc. Natl. Acad. Sci. U.S.A. 98, 2250-2255.
12. Dawson, J. P., Weinger, J. S., and Engelman, D. M. (2002) Motifs of serine and threonine can drive association of transmembrane helices, J. Mol. Biol. 316, 799-805.
13. Lemmon, M. A., and Engelman, D. M. (1992) Specificity and promiscuity in membrane helix interactions, FEBS Lett. 346, 17-20.
14. Mall, S., Broadbridge, R., Sharma, R. P., East, J. M., and Lee, A. G. (2001) Self-association of model transmembrane α-helices is modulated by lipid structure, Biochemistry 40, 12379-12386.
15. Yano, Y., Takemoto, T., Kobayashi, S., Yasui, H., Sakurai, H., Ohashi, W., Niwa, M., Futaki, S., Sugiura, Y., and Matsuzaki, K. (2002) Topological stability and self-association of a completely hydrophobic model transmembrane helix in lipid bilayers, Biochemistry 41, 3073-3080.
16. Renthal, R., and Velasquez, D. (2002) Self-association of helical peptides in a lipid environment, J. Protein Chem. 21, 255-264.
17. Tanford, C. (1970) Protein denaturation. C. Theoretical models for the mechanism of denaturation, Adv. Protein Chem. 24, 1-95.
18. Schellman, J. A. (1978) Solvent denaturation, Biopolymers 17, 1305-1322.
19. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves, Methods Enzymol. 131, 266-280.
20. Brouillette, C. G., Muccio, D. D., and Finney, T. K. (1987) pH dependence of bacteriorhodopsin thermal unfolding, Biochemistry 26, 7431-7438.
21. Taneva, S. G., Caaveiro, J. M. M., Muga, A., and Goni, F. M. (1995) A pathway for the thermal destabilization of bacteriorhodopsin, FEBS Lett. 367, 297-300.
22. Brouillette, C. G., McMichens, R. B., Stern, L. J., and Khorana, H. G. (1989) Structure and thermal stability of monomeric bacteriorhodopsin in mixed phospholipid/detergent micelles, Proteins 5, 38-46.
23. Booth, P. J. (2000) Unraveling the folding of bacteriorhodopsin, Biochim. Biophys. Acta 1460, 4-14.
24. Chen, G. Q., and Gouaux, E. (1999) Probing the folding and unfolding of wild-type and mutant forms of bacteriorhodopsin in micellar solutions: evaluation of reversible unfolding conditions, Biochemistry 38, 15380-15387.
25. 1H heteronuclear NMR spectroscopy, Eur. J. Biochem. 219, 571-583.
26. Lau, F. W. and Bowie, J. U. (1997) A method for assessing the stability of a membrane protein, Biochemistry 36, 5884-5892.
27. Tanford, C. (1980) The hydrophobic effect, 2nd ed., p 93, J. Wiley and Sons, NY.
28. Huang, K. S., Bayley, H., Liao, M. J., London, E., and Khorana, H. G. (1981) Refolding of an integral membrane protein. Denaturation, renaturation, and reconstitution of intact bacteriorhodopsin and two proteolytic fragments, J. Biol. Chem. 256, 3802-3809.
29. Mitaku, S., Ikuta, K., Itoh, H., Katoaka, R., Naka, M., Yamada, M., and Suwa, M. (1988) Denaturation of bacteriorhodopsin by organic solvents, Biophys. Chem. 30, 69-79.
30. Renthal, R., Cothran, M., Dawson, N., and Harris, G. (1987) Fluorescent labeling of purple membrane: implications for helix connections, Biochim. Biophys. Acta 897, 384-394.
31. Oesterhelt, D., and Stoeckenius, W. (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane, Methods Enzymol. 31, 667-678.
32. Harris, G., Renthal, R., Tuley, J., and Robinson, N. (1979) Dansylation of bacteriorhodopsin near the retinal attachment site, Biochem. Biophys. Res. Commun. 91, 926-931.
33. Gerber, G. E., Anderegg, R. J., Herlihy, W. C., Gray, C. P., Biemann, K., and Khorana, H. G. (1979) Partial primary structure of bacteriorhodopsin: sequencing methods for membrane proteins, Proc. Natl. Acad. Sci. U.S.A. 76, 227-231.
34. Katre, N. V., Wolber, P. K., Stoeckenius, W., and Stroud, R. M. (1981) Attachment site(s) of retinal in bacteriorhodopsin, Proc. Natl. Acad. Sci. U.S.A. 78, 4068-4072.
35. Renthal, R., and Alaniz, C. (1999) Conformational change in bacterio-opsin on binding to retinal, Biophys. Chem. 78, 241-245.
36. Renthal, R., and Haas, P. (1996) Effect of transmembrane helix packing on tryptophan and tyrosine environments in detergent-solubilized bacterio-opsin, J. Protein Chem. 15, 281-289.
37. Melhuish, W. H. (1973) Absolute spectrofluorometry, in Accuracy in Spectrophotometry and Luminescence Measurements, Natl. Bur. Stand., Spec. Publ. 378, 137-150.
38. Stryer, L. (1978) Fluorescence energy transfer as a spectroscopic ruler, Annu. Rev. Biochem. 47, 819-846.
39. Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P., Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 A resolution, J. Mol. Biol. 291, 899-911.
40. Essen, L.-O., Siegert, R., Lehmann, W. D., and Oesterhelt, D. (1998) Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex, Proc. Natl. Acad. Sci. U.S.A. 95, 11673-11678.
41. London, E., and Khorana, H. G. (1982) Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures, J. Biol. Chem. 257, 7003-7011.
42. Walter, A., Kuehl, G., Barnes, K., and VanderWaerdt, G. (2000) The vesicle-to-micelle transition of phosphatidylcholine vesicles induced by nonionic detergents: effects of sodium chloride, sucrose and urea, Biochim. Biophys. Acta 1508, 20-33.
43. 13C NMR, J. Biochem. 127, 861-869.
44. Braiman, M. S., Stern, L. J., Chao, B. H., and Khorana, H. G. (1987) Structure-function studies on bacteriorhodopsin. IV. Purification and renaturation of bacterio-opsin polypeptide expressed in Escherichia coli, J. Biol. Chem. 262, 9271-9276.
45. Lustig, A., Engel, A., Tsiotis, G., Landau, E. M., and Baschong, W. (2000) Molecular weight determination of membrane proteins by sedimentation equilibrium at the sucrose or nycodenz-adjusted density of the hydrated detergent micelle, Biochim. Biophys. Acta 1464, 199-206.
46. Riley, L. M., Wallace, B. A., Flitsch, S. L., and Booth, P. J. (1997) Slow α helix formation during folding of a membrane protein, Biochemistry 36, 192-196.
47. Mao, D., and Wallace, B. A. (1984) Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles, Biochemistry 23, 2667-2673.
48. Muccio, D. D., and DeLucas, L. J. (1985) Isolation of detergent-solubilized monomers of bacteriorhodopsin by size-exclusion high-performance liquid chromatography, J. Chromatogr. A 326, 243-250.
49. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants, Biochemistry 27, 8063-8068.
50. Baskakov, I. V., and Bolen, D. W. (1998) Monitoring the sizes of denatured ensembles of staphylococcal nuclease proteins: implications regarding m values, intermediates, and thermodynamics, Biochemistry 37, 18010-18017.
51. Ramos, C. H. I., Kay, M. S., and Baldwin, R. L. (1999) Putative interhelix ion pairs involved in the stability of myoglobin, Biochemistry 38, 9783-9790.
52. Lu, H., and Booth, P. J. (2000) The final stages of folding of the membrane protein bacteriorhodopsin occur by kinetically indistinguishable parallel folding paths that are mediated by pH, J. Mol. Biol. (2000) 233-243.
53. Privalov, P. L. (1989) Thermodynamic problems of protein structure, Annu. Rev. Biophys. Biophys. Chem. 18, 47-69.
54. Popot, J.-L., and de Vitry, C. (1990) On the microassembly of integral membrane proteins, Annu. Rev. Biophys. Biophys. Chem. 19, 369-403.
55. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.