Secondary and tertiary structure of bacteriorhodopsin in the SDS denatured state

Biochemistry

Volumn 51, Issue 6, 2012, Pages 1051-1060

  Krishnamani, Venkatramanan ^a,c   Hegde, Balachandra G ^b   Langen, Ralf ^b   Lanyi, Janos K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DENATURED STATE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; END-TO-END DISTANCES; IN-VITRO; INTERHELICAL DISTANCE; NATIVE STATE; PULSED ELECTRON; SDS MICELLES; SECONDARY AND TERTIARY STRUCTURES; SECONDARY STRUCTURES; SODIUM DODECYL SULFATE MICELLES; SPIN RESONANCE; TERTIARY STRUCTURES;

ELECTRON SPIN RESONANCE SPECTROSCOPY; PARAMAGNETISM; SODIUM; SODIUM SULFATE;

MICELLES;

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; BACTERIORHODOPSIN; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DODECYL SULFATE SODIUM;

ARTICLE; DOUBLE ELECTRON ELECTRON SPIN RESONANCE; ELECTRON SPIN RESONANCE; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SPIN LABELING;

BACTERIORHODOPSINS; MICELLES; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; SODIUM DODECYL SULFATE; SPIN TRAPPING;

EID: 84856853534     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201769z     Document Type: Article

References (62)

1. Levinthal, C. (1968) Are There Pathways for Protein Folding J.Chim. Phys. Phys.-Chim. Biol. 65, 44-45
2. Flory, P. J. and Volkenstein, M. (1969) Statistical mechanics of chain molecules Biopolymers 8, 699-700
3. Pappu, R. V., Srinivasan, R., and Rose, G. D. (2000) The Flory isolated-pair hypothesis is not valid for polypeptide chains: implications for protein folding Proc. Natl. Acad. Sci. U. S. A. 97, 12565-12570
4. Marqusee, S., Robbins, V. H., and Baldwin, R. L. (1989) Unusually stable helix formation in short alanine-based peptides Proc. Natl. Acad. Sci. U. S. A. 86, 5286-5290
5. Srinivasan, R. and Rose, G. D. (1999) A physical basis for protein secondary structure Proc. Natl. Acad. Sci. U. S. A. 96, 14258-14263 (Pubitemid 30000638)
6. Klimov, D. K. and Thirumalai, D. (2005) Symmetric connectivity of secondary structure elements enhances the diversity of folding pathways J. Mol. Biol. 353, 1171-1186 (Pubitemid 41503281)
7. Dill, K. A. and Shortle, D. (1991) Denatured states of proteins Annu. Rev. Biochem. 60, 795-825
8. Shortle, D. R. (1996) Structural analysis of non-native states of proteins by NMR methods Curr. Opin. Struct. Biol. 6, 24-30 (Pubitemid 26073941)
9. Lanyi, J. K. and Schobert, B. (2003) Mechanism of proton transport in bacteriorhodopsin from crystallographic structures of the K, L, M1, M2, and M2′ intermediates of the photocycle J. Mol. Biol. 328, 439-450 (Pubitemid 36407586)
10. Haupts, U., Tittor, J., and Oesterhelt, D. (1999) Closing in on bacteriorhodopsin: progress in understanding the molecule Annu. Rev. Biophys. Biomol. Struct. 28, 367-399 (Pubitemid 29319263)
11. 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
12. Huang, K. S., Bayley, H., and Khorana, H. G. (1980) Delipidation of bacteriorhodopsin and reconstitution with exogenous phospholipid Proc. Natl. Acad. Sci. U. S. A. 77, 323-327 (Pubitemid 10126039)
13. Booth, P. J., Flitsch, S. L., Stern, L. J., Greenhalgh, D. A., Kim, P. S., and Khorana, H. G. (1995) Intermediates in the folding of the membrane protein bacteriorhodopsin Nat. Struct. Biol. 2, 139-143 (Pubitemid 26040650)
14. Booth, P. J., Farooq, A., and Flitsch, S. L. (1996) Retinal binding during folding and assembly of the membrane protein bacteriorhodopsin Biochemistry 35, 5902-5909 (Pubitemid 26143684)
15. Sugiyama, Y. and Mukohata, Y. (1996) Dual roles of DMPC and CHAPS in the refolding of bacterial opsins in vitro J Biochem. 119, 1143-1149 (Pubitemid 26202629)
16. Booth, P. J. (1997) Folding alpha-helical membrane proteins: kinetic studies on bacteriorhodopsin Folding Des. 2, R85-92
17. Booth, P. J., Riley, M. L., Flitsch, S. L., Templer, R. H., Farooq, A., Curran, A. R., Chadborn, N., and Wright, P. (1997) Evidence that bilayer bending rigidity affects membrane protein folding Biochemistry 36, 197-203 (Pubitemid 27024693)
18. Riley, M. L., Wallace, B. A., Flitsch, S. L., and Booth, P. J. (1997) Slow alpha helix formation during folding of a membrane protein Biochemistry 36, 192-196 (Pubitemid 27024692)
19. Curran, A. R., Templer, R. H., and Booth, P. J. (1999) Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer Biochemistry 38, 9328-9336
20. 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. 299, 233-243
21. Allen, S. J., Kim, J. M., Khorana, H. G., Lu, H., and Booth, P. J. (2001) Structure and function in bacteriorhodopsin: the effect of the interhelical loops on the protein folding kinetics J. Mol. Biol. 308, 423-435 (Pubitemid 33043579)
22. Lu, H., Marti, T., and Booth, P. J. (2001) Proline residues in transmembrane alpha helices affect the folding of bacteriorhodopsin J.Mol. Biol. 308, 437-446 (Pubitemid 33043580)
23. Compton, E. L., Farmer, N. A., Lorch, M., Mason, J. M., Moreton, K. M., and Booth, P. J. (2006) Kinetics of an individual transmembrane helix during bacteriorhodopsin folding J. Mol. Biol. 357, 325-338 (Pubitemid 43339334)
24. Pan, Y., Brown, L., and Konermann, L. (2011) Kinetic folding mechanism of an integral membrane protein examined by pulsed oxidative labeling and mass spectrometry J. Mol. Biol. 410, 146-158
25. Krishnamani, V. and Lanyi, J. K. (2011) Structural Changes in Bacteriorhodopsin during In Vitro Refolding from a Partially Denatured State Biophys. J. 100, 1559-1567
26. London, E. and Khorana, H. G. (1982) Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures J. Biol. Chem. 257, 7003-7011
27. Polet, H. and Steinhardt, J. (1968) Binding-induced alterations in ultraviolet absorption of native serum albumin Biochemistry 7, 1348-1356
28. Pan, Y., Brown, L., and Konermann, L. (2011) Hydrogen/deuterium exchange mass spectrometry and optical spectroscopy as complementary tools for studying the structure and dynamics of a membrane protein Int. J. Mass Spectrom. 302, 3-11
29. Pan, Y., Brown, L., and Konermann, L. (2010) Site-directed mutagenesis combined with oxidative methionine labeling for probing structural transitions of a membrane protein by mass spectrometry J.Am. Soc. Mass Spectrom. 21, 1947-1956
30. Pervushin, K. V., Arseniev, A. S., Kozhich, A. T., and Ivanov, V. T. (1991) Two-dimensional NMR study of the conformation of (34-65)bacterioopsin polypeptide in SDS micelles J. Biomol. NMR 1, 313-322
31. Pervushin, K. V., Orekhov, V., Popov, A. I., Musina, L., and Arseniev, A. S. (1994) Three-dimensional structure of (1-71)bacterioopsin solubilized in methanol/chloroform and SDS micelles determined by 15N-1H heteronuclear NMR spectroscopy Eur. J. Biochem. 219, 571-583 (Pubitemid 24053676)
32. Torres, J., Sepulcre, F., and Padros, E. (1995) Conformational changes in bacteriorhodopsin associated with protein-protein interactions: a functional alpha I-alpha II helix switch? Biochemistry 34, 16320-16326 (Pubitemid 26006475)
33. Pannier, M., Veit, S., Godt, A., Jeschke, G., and Spiess, H. W. (2000) Dead-time free measurement of dipole-dipole interactions between electron spins J. Magn. Reson. 142, 331-340
34. Rabenstein, M. D. and Shin, Y. K. (1995) Determination of the distance between two spin labels attached to a macromolecule Proc. Natl. Acad. Sci. U. S. A. 92, 8239-8243
35. Krebs, M. P., Mollaaghababa, R., and Khorana, H. G. (1993) Gene replacement in Halobacterium halobium and expression of bacteriorhodopsin mutants Proc. Natl. Acad. Sci. U. S. A. 90, 1987-1991 (Pubitemid 23069982)
36. Krebs, M. P., Hauss, T., Heyn, M. P., Rajbhandary, U. L., and Khorana, H. G. (1991) Expression of the Bacterioopsin Gene in Halobacterium-Halobium Using a Multicopy Plasmid Proc. Natl. Acad. Sci. U. S. A. 88, 859-863 (Pubitemid 21916123)
37. Peck, R. F., DasSarma, S., and Krebs, M. P. (2000) Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker Mol. Microbiol. 35, 667-676 (Pubitemid 30085283)
38. Cline, S. W. and Doolittle, W. F. (1987) Efficient transfection of the archaebacterium Halobacterium halobium J. Bacteriol. 169, 1341-1344 (Pubitemid 17043411)
39. Oesterhelt, D. and Stoeckenius, W. (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane, in Methods in Enzymology (Sidney Fleischer, L. P., Ed.) pp 667-678, Academic Press, New York.
40. Misch, D. W. and Misch, M. S. (1975) Effect of Dimethyl-Sulfoxide on a Lysosomal Membrane Ann. N. Y. Acad. Sci. 243, 54-59
41. Aracava, Y., Schreier, S., Phadke, R., Deslauriers, R., and Smith, I. C. P. (1981) Spin Label Reduction Kinetics, a Procedure to Study the Effect of Drugs on Membrane-Permeability-the Effects of Monosodium Urate, Dimethylsulfoxide and Amphotericin-B J. Biochem. Biophys. Methods 5, 83-94 (Pubitemid 11023622)
42. Steinhoff, H. J., Pfeiffer, M., Rink, T., Burlon, O., Kurz, M., Riesle, J., Heuberger, E., Gerwert, K., and Oesterhelt, D. (1999) Azide reduces the hydrophobic barrier of the bacteriorhodopsin proton channel Biophys. J. 76, 2702-2710 (Pubitemid 29264629)
43. Allen, S. J., Curran, A. R., Templer, R. H., Meijberg, W., and Booth, P. J. (2004) Folding kinetics of an alpha helical membrane protein in phospholipid bilayer vesicles J. Mol. Biol. 342, 1279-1291 (Pubitemid 39207902)
44. Curnow, P. and Booth, P. J. (2007) Combined kinetic and thermodynamic analysis of alpha-helical membrane protein unfolding Proc. Natl. Acad. Sci. U. S. A. 104, 18970-18975
45. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J., Timmel, C. R., Hilger, D., and Jung, H. (2006) DeerAnalysis2006-a comprehensive software package for analyzing pulsed ELDOR data Appl. Magn. Reson. 30, 473-498
46. 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 (Pubitemid 19128899)
47. Kratky, O. and Porod, G. (1949) Rontgenuntersuchung Geloster Fadenmolekule Recl. Trav. Chim. Pays-Bas 68, 1106-1122
48. Gobush, W., Yamakawa, H., Stockmay, W. H., and Magee, W. S. (1972) Statistical Mechanics of Wormlike Chains. 1. Asymptotic Behavior J. Chem. Phys. 57, 2839-2842
49. Yamakawa, H. and Stockmay, W., H. (1972) Statistical Mechanics of Wormlike Chains. 2. Excluded Volume Effects J. Chem. Phys. 57, 2843-2854
50. Zhou, H. X. (2004) Polymer models of protein stability, folding, and interactions Biochemistry 43, 2141-2154
51. Blaurock, A. E. and Stoecken., W. (1971) Structure of Purple Membrane Nature (London), New Biol. 233, 152-&
52. Henderson, R. and Unwin, P. N. T. (1975) 3-Dimensional Model of Purple Membrane Obtained by Electron-Microscopy Nature 257, 28-32
53. Zhou, H. X. (2001) Loops in proteins can be modeled as worm-like chains J. Phys. Chem. B 105, 6763-6766
54. Hawkins, C. A., de Alba, E., and Tjandra, N. (2005) Solution structure of human saposin C in a detergent environment J. Mol. Biol. 346, 1381-1392 (Pubitemid 40248836)
55. Braun, R., Engelman, D. M., and Schulten, K. (2004) Molecular dynamics simulations of micelle formation around dimeric glycophorin A transmembrane helices Biophys. J. 87, 754-763 (Pubitemid 39095058)
56. Sorin, E. J. and Pande, V. S. (2005) Exploring the helix-coil transition via all-atom equilibrium ensemble simulations Biophys. J. 88, 2472-2493 (Pubitemid 40976118)
57. Fersht, A. R. (1997) Nucleation mechanisms in protein folding Curr. Opin. Struct. Biol. 7, 3-9 (Pubitemid 27092374)
58. Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P., and Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 A resolution J. Mol. Biol. 291, 899-911
59. Derosa, M., Gambacorta, A., and Gliozzi, A. (1986) Structure, Biosynthesis, and Physicochemical Properties of Archaebacterial Lipids Microbiol. Rev. 50, 70-80 (Pubitemid 16122596)
60. Hunt, J. F., Earnest, T. N., Bousche, O., Kalghatgi, K., Reilly, K., Horvath, C., Rothschild, K. J., and Engelman, D. M. (1997) A biophysical study of integral membrane protein folding Biochemistry 36, 15156-15176 (Pubitemid 27527981)
61. Hawkins, C. A., de Alba, E., and Tjandra, N. (2005) Solution structure of human saposin C in a detergent environment J. Mol. Biol. 346, 1381-1392 (Pubitemid 40248836)
62. Yonath, A., Podjarny, A., Honig, B., Sielecki, A., and Traub, W. (1977) Crystallographic studies of protein denaturation and renaturation. 2. Sodium dodecyl sulfate induced structural changes in triclinic lysozyme Biochemistry 16, 1418-1424 (Pubitemid 8083113)