Characterization of membrane protein non-native states. 2. the SDS-unfolded states of rhodopsin

Biochemistry

Volumn 49, Issue 30, 2010, Pages 6329-6340

  Dutta, Arpana ^a   Kim, Tai Yang ^b   Moeller, Martina ^b   Wu, Jenny ^a,b   Alexiev, Ulrike ^b   Klein Seetharaman, Judith ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL CHARACTERIZATION; CHEMICAL DENATURANTS; CIRCULAR DICHROISM; CONCENTRATION RANGES; DENATURED STATE; EXPERIMENTAL EVIDENCE; FLEXIBLE SURFACES; G PROTEIN COUPLED RECEPTORS; INTERFACE REGIONS; INTERMEDIATE STATE; MAMMALIAN MEMBRANES; MEMBRANE PROTEINS; MICELLAR STRUCTURES; MIXED MICELLES; NON-NATIVE STATE; RESIDUAL STRUCTURE; SECONDARY STRUCTURES; SODIUM DODECYL SULFATE; STRUCTURAL CHANGE; TERTIARY STRUCTURES; TIME-RESOLVED FLUORESCENCE SPECTROSCOPY; TRANSIENT STABILITY; TRYPTOPHAN RESIDUES;

ABSORPTION SPECTROSCOPY; AMINO ACIDS; BIOLOGICAL MEMBRANES; DENATURATION; DICHROISM; FLUORESCENCE SPECTROSCOPY; INDICATORS (CHEMICAL); MAMMALS; PROTEINS; SODIUM; SODIUM SULFATE; SPHERES;

DIFFUSERS (OPTICAL);

CYSTEINE; RHODOPSIN; TRYPTOPHAN;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; LIGHT SCATTERING; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STEADY STATE;

ANIMALS; CATTLE; CYSTEINE; MEMBRANE PROTEINS; MICELLES; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RHODOPSIN; SODIUM DODECYL SULFATE; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

MAMMALIA;

EID: 77955018405     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100339x     Document Type: Article

References (42)

1. Popot, J. L. and Engelman, D. M. (1990) Membrane protein folding and oligomerization: the two-stage model Biochemistry 29, 4031-4037
2. Klein-Seetharaman, J. (2005) Dual role of interactions between membranous and soluble portions of helical membrane receptors for folding and signaling Trends Pharmacol. Sci. 26, 183-189
3. Rader, A. J., Anderson, G., Isin, B., Khorana, H. G., Bahar, I., and Klein-Seetharaman, J. (2004) Identification of core amino acids stabilizing rhodopsin Proc. Natl. Acad. Sci. U.S.A. 101, 7246-7251
4. Tastan, O., Yu, E., Ganapathiraju, M., Aref, A., Rader, A. J., and Klein-Seetharaman, J. (2007) Comparison of stability predictions and simulated unfolding of rhodopsin structures Photochem. Photobiol. 83, 351-363
5. Park, P. S., Palczewski, K., and Muller, D. J. (2008) Mechanical properties of bovine rhodopsin and bacteriorhodopsin: possible roles in folding and function Langmuir 24, 1330-1337
6. Oprian, D. D., Molday, R. S., Kaufman, R. J., and Khorana, H. G. (1987) Expression of a synthetic bovine rhodopsin gene in monkey kidney cells Proc. Natl. Acad. Sci. U.S.A. 84, 8874-8878
7. Moller, M. and Alexiev, U. (2009) Surface charge changes upon formation of the signaling state in visual rhodopsin Photochem. Photobiol. 85, 501-508
8. Scherrer, P., Alexiev, U., Heyn, M. P., Marti, T., and Khorana, H. G. (1992) Structures and Functions of Retinal Proteins, Vol. 221, Colloque INSERM/John Libbey Eurotext Ltd.
9. Wald, G. and Brown, P. K. (1953) The molar extinction of rhodopsin J. Gen. Physiol. 37, 189-200
10. Grassetti, D. R. and Murray, J. F., Jr. (1967) Determination of sulfhydryl groups with 2,2′- or 4,4′-dithiodipyridine Arch. Biochem. Biophys. 119, 41-49
11. Kim, T. Y., Winkler, K., and Alexiev, U. (2007) Picosecond multidimensional fluorescence spectroscopy: a tool to measure real-time protein dynamics during function Photochem. Photobiol. 83, 378-384
12. Farrens, D. L. and Khorana, H. G. (1995) Structure and function in rhodopsin. Measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy J. Biol. Chem. 270, 5073-5076
13. Wald, G. and Brown, P. K. (1950) The synthesis of rhodopsin from retinene(1) Proc. Natl. Acad. Sci. U.S.A. 36, 84-92
14. Chen, Y. S. and Hubbell, W. L. (1978) Reactions of the sulfhydryl groups of membrane-bound bovine rhodopsin Membr. Biochem. 1, 107-130
15. Bucci, S. and Fagotti, C. (1991) Small-angle neutron-scattering study of ionic-nonionic mixed micelles Langmuir 7, 824-826
16. Turro, N. J. and Yekta, A. (1978) Luminescent probes for detergent solutions. A simple procedure for determination of the mean aggregation number of micelles J. Am. Chem. Soc. 100, 5951-5952
17. Tummino, P. J. and Gafni, A. (1993) Determination of the aggregation number of detergent micelles using steady-state fluorescence quenching Biophys. J. 64, 1580-1587
18. Alexiev, U., Rimke, I., and Pohlmann, T. (2003) Elucidation of the nature of the conformational changes of the EF-interhelical loop in bacteriorhodopsin and of the helix VIII on the cytoplasmic surface of bovine rhodopsin: a time-resolved fluorescence depolarization study J. Mol. Biol. 328, 705-719
19. Kirchberg, K., Kim, T. Y., Haase, S., and Alexiev, U. (2010) Functional interaction structures of the photochromic retinal protein rhodopsin Photochem. Photobiol. Sci. 9, 226-233
20. Krishna, A. G., Menon, S. T., Terry, T. J., and Sakmar, T. P. (2002) Evidence that helix 8 of rhodopsin acts as a membrane-dependent conformational switch Biochemistry 41, 8298-8309
21. Lehmann, N., Alexiev, U., and Fahmy, K. (2007) Linkage between the intramembrane H-bond network around aspartic acid 83 and the cytosolic environment of helix 8 in photoactivated rhodopsin J. Mol. Biol. 366, 1129-1141
22. Schroder, G. F., Alexiev, U., and Grubmuller, H. (2005) Simulation of fluorescence anisotropy experiments: probing protein dynamics Biophys. J. 89, 3757-3770
23. Kim, T. Y., Moeller, M., Winkler, K., Kirchberg, K., and Alexiev, U. (2009) Dissection of environmental changes at the cytoplasmic surface of light-activated bacteriorhodopsin and visual rhodopsin: sequence of spectrally silent steps Photochem. Photobiol. 85, 570-577
24. Dornmair, K., Kiefer, H., and Jahnig, F. (1990) Refolding of an integral membrane protein. OmpA of Escherichia coli J. Biol. Chem. 265, 18907-18911
25. Lau, F. W. and Bowie, J. U. (1997) A method for assessing the stability of a membrane protein Biochemistry 36, 5884-5892
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. Otzen, D. E. (2003) Folding of DsbB in mixed micelles: a kinetic analysis of the stability of a bacterial membrane protein J. Mol. Biol. 330, 641-649
28. Tanford, C. (1991) The Hydrophobic Effect. Formation of Micelles and Biological Membranes, 2 nd ed., Wiley and Sons, New York.
29. Mascher, E. and Lundahl, P. (1989) Sodium dodecyl sulphate-protein complexes: Changes in size or shape below the critical micelle concentration, as monitored by high-performance agarose gel chromatography J. Chromatogr. 476, 147-158
30. Ibel, K., May, R. P., Kirschner, K., Szadkowski, H., Mascher, E., and Lundahl, P. (1990) Protein-decorated micelle structure of sodium-dodecyl- sulfate-protein complexes as determined by neutron scattering Eur. J. Biochem. 190, 311-318
31. Jirgensons, B. (1967) Effects of n-propyl alcohol and detergents on the optical rotatory dispersion of alpha-chymotrypsinogen, beta-casein, histone fraction F1, and soybean trypsin inhibitor J. Biol. Chem. 242, 912-918
32. Mattice, W. L., Riser, J. M., and Clark, D. S. (1976) Conformational properties of the complexes formed by proteins and sodium dodecyl sulfate Biochemistry 15, 4264-4272
33. Rao, J. K. and Argos, P. (1981) Structural stability of halophilic proteins Biochemistry 20, 6536-6543
34. Otzen, D. E. (2002) Protein unfolding in detergents: effect of micelle structure, ionic strength, pH, and temperature Biophys. J. 83, 2219-2230
35. Otzen, D. E. and Oliveberg, M. (2002) Burst-phase expansion of native protein prior to global unfolding in SDS J. Mol. Biol. 315, 1231-1240
36. Alexiev, U., Mollaaghababa, R., Khorana, H. G., and Heyn, M. P. (2000) Evidence for long range allosteric interactions between the extracellular and cytoplasmic parts of bacteriorhodopsin from the mutant R82A and its second site revertant R82A/G231C J. Biol. Chem. 275, 13431-13440
37. Heyne, K., Herbst, J., Dominguez-Herradon, B., Alexiev, U., and Diller, R. (2000) Reaction control in bacteriorhodopsin: impact of Arg82 and Asp85 on the fast retinal isomerization, studied in the second site revertant Arg82Ala/Gly231Cys and various purple and blue forms of bacteriorhodopsin J. Phys. Chem. B 104, 6053-6058
38. Alexiev, U., Scherrer, P., Marti, T., Khorana, H. G., and Heyn, M. P. (1995) Time-resolved surface charge change on the cytoplasmic side of bacteriorhodopsin FEBS Lett. 373, 81-84
39. Cai, K., Klein-Seetharaman, J., Farrens, D., Zhang, C., Altenbach, C., Hubbell, W. L., and Khorana, H. G. (1999) Single-cysteine substitution mutants at amino acid positions 306-321 in rhodopsin, the sequence between the cytoplasmic end of helix VII and the palmitoylation sites: sulfhydryl reactivity and transducin activation reveal a tertiary structure Biochemistry 38, 7925-7930
40. Klein-Seetharaman, J., Hwa, J., Cai, K., Altenbach, C., Hubbell, W. L., and Khorana, H. G. (1999) Single-cysteine substitution mutants at amino acid positions 55-75, the sequence connecting the cytoplasmic ends of helices I and II in rhodopsin: reactivity of the sulfhydryl groups and their derivatives identifies a tertiary structure that changes upon light-activation Biochemistry 38, 7938-7944
41. Croonen, Y., Gelade, E., Van der Zegel, M., Van der Auweraer, M., Vandendriessche, H., De Schryver, F. C., and Almgren, M. (1983) Influence of salt, detergent concentration, and temperature on the fluorescence quenching of 1-methylpyrene in sodium dodecyl sulfate with m-dicyanobenzene J. Phys. Chem. 87, 1426-1431
42. Sreerama, N. a. W., R.W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287, 252-260