The Contribution of a Covalently Bound Cofactor to the Folding and Thermodynamic Stability of an Integral Membrane Protein

Journal of Molecular Biology

Volumn 403, Issue 4, 2010, Pages 630-642

  Curnow, Paul ^a   Booth, Paula J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Bacteriorhodopsin; Cofactor; Folding; Membrane protein; Retinal

Indexed keywords

APOPROTEIN; BACTERIORHODOPSIN; INTEGRAL MEMBRANE PROTEIN; MEMBRANE PROTEIN; POLYPEPTIDE; RETINAL; RHODOPSIN; UNCLASSIFIED DRUG; DETERGENT; LIPID; MICELLE; MO 113; OXADIAZOLE DERIVATIVE; RECOMBINANT PROTEIN;

ARTICLE; COVALENT BOND; MICELLE; MOLECULAR DYNAMICS; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; THERMOSTABILITY; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HALOBACTERIUM SALINARUM; KINETICS; PROTEIN DENATURATION; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS;

BACTERIORHODOPSINS; DETERGENTS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HALOBACTERIUM SALINARUM; KINETICS; LIPIDS; MEMBRANE PROTEINS; MICELLES; MUTAGENESIS, SITE-DIRECTED; OXADIAZOLES; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; RECOMBINANT PROTEINS; RETINALDEHYDE; THERMODYNAMICS;

EID: 77957922696     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.09.003     Document Type: Article

References (46)

1. Wilson C.J., Apiyo D., Wittung-Stafshede P. Role of cofactors in metalloprotein folding. Q. Rev. Biophys. 2004, 37:285-314.
2. Higgins C.L., Muralidhara B.K., Wittung-Stafshede P. How do cofactors modulate protein folding?. Protein Pept. Lett. 2005, 12:165-170.
3. Wittung-Stafshede P. Role of cofactors in protein folding. Acc. Chem. Res. 2002, 35:201-208.
4. Gibson N.J., Cassim J.Y. Nature of forces stabilizing the transmembrane protein bacteriorhodopsin in purple membrane. Biophys. J. 1989, 56:769-780.
5. Booth P.J., Farooq A., Flitsch S.L. Retinal binding during folding and assembly of the membrane protein bacteriorhodopsin. Biochemistry 1996, 35:5902-5909.
6. Curnow P., Booth P.J. Combined kinetic and thermodynamic analysis of α-helical membrane protein unfolding. Proc. Natl Acad. Sci. USA 2007, 104:18970-18975.
7. Huang K.S., Bayley H., Liao M.J., London E., Khorana H.G. Refolding of an integral membrane protein. J. Biol. Chem. 1981, 256:3802-3809.
8. London E., Khorana H.G. Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures. J. Biol. Chem. 1982, 257:7003-7011.
9. Faham S., Yang D., Bare E., Yohannan S., Whitelegge J.P., Bowie J.U. Side-chain contributions to membrane protein stability and structure. J. Mol. Biol. 2004, 335:297-305.
10. Booth P.J., Curnow P. Folding scene investigation: membrane proteins. Curr. Opin. Struct. Biol. 2009, 19:8-13.
11. Booth P.J., Flitsch S.L., Stern L.J., Greenhalgh D.A., Kim P.S., Khorana H.G. Intermediates in the folding of the membrane protein bacteriorhodopsin. Nat. Struct. Biol. 1995, 2:139-143.
12. Riley M.L., Wallace B.A., Flitsch S.L., Booth P.J. Slow α-helix formation during folding of a membrane protein. Biochemistry 1997, 36:192-196.
13. DeLano W.L. The PyMOL Molecular Graphics System 2002, http://www.pymol.org.
14. Curnow P., Booth P.J. The transition state for integral membrane protein folding. Proc. Natl Acad. Sci. USA 2009, 106:773-778.
15. Majumdar D.S., Smirnova I., Kasho V., Nir E., Kong X., Weiss S., Kaback H.R. Single-molecule FRET reveals sugar-induced conformational dynamics in LacY. Proc. Natl Acad. Sci. USA 2007, 104:12640-12645.
16. Rehorek M., Dencher N.A., Heyn M.P. Fluorescence energy transfer from diphenylhexatriene to bacteriorhodopsin in lipid vesicles. Biophys. J. 1983, 43:39-45.
17. Wu C.W., Stryer L. Proximity relationships in rhodopsin. Proc. Natl Acad. Sci. USA 1972, 69:1104-1108.
18. Kalisky O., Felteson J., Ottolenghi M. Photochemistry and fluorescence of bacteriorhodopsin excited in its 280-nm absorption band. Biochemistry 1981, 20:205-209.
19. Nannepaga S.J., Gawalapu R., Valasquez D., Renthal R. Estimation of helix-helix association free energy from partial unfolding of bacterioopsin. Biochemistry 2004, 43:550-559.
20. Valluru N., Silva F., Dhage M., Rodriguez G., Alloor S.R., Renthal R. Transmembrane helix-helix association: relative stabilities at low pH. Biochemistry 2006, 45:4371-4377.
21. Fersht A.R. Structure and Mechanism in Protein Science 1998, W. H. Freeman and Co., New York, NY.
22. Cladera J., Torres J., Padros E. Analysis of conformational changes in bacteriorhodopsin upon retinal removal. Biophys. J. 1996, 70:2882-2887.
23. Vogel H., Gartner W. The secondary structure of bacteriorhodopsin determined by Raman and circular dichroism spectroscopy. J. Biol. Chem. 1987, 262:11464-11469.
24. Becher B., Cassim J.Y. Effects of bleaching and regeneration on the purple membrane structure of Halobacterium halobium. Biophys. J. 1977, 19:285-297.
25. 13C nuclear magnetic resonance. Biochemistry 1996, 35:7520-7527.
26. 13C NMR. J. Biochem. 2000, 127:861-869.
27. Pan Y., Brown L., Konermann L. Mapping the structure of an integral membrane protein under semi-denaturing conditions by laser-induced oxidative labeling and mass spectrometry. J. Mol. Biol. 2009, 394:968-981.
28. Krebs M.P., Isenbarger T.A. Structural determinants of purple membrane assembly. Biochim. Biophys. Acta 2000, 1460:15-26.
29. Gerber G.E., Gray C.P., Wildenauer D., Khorana H.G. Orientation of bacteriorhodopsin in Halobacterium halobium as studied by selective proteolysis. Proc. Natl Acad. Sci. USA 1977, 74:5426-5430.
30. Kahn T.W., Sturtevant J.N., Engelman D.M. Thermodynamic measurements of the contributions of helix-connecting loops and of retinal to the stability of bacteriorhodopsin. Biochemistry 1992, 31:8829-8839.
31. Cladera J., Galisteo M.L., Sabes M., Mateo P.L., Padros E. The role of retinal in the thermal stability of the purple membrane. Eur. J. Biochem. 1992, 207:581-585.
32. Myers J.K., Pace C.N., Scholtz J.M. Denaturant m-values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 1995, 4:2138-2148.
33. 5. Biochemistry 1999, 38:14352-14362.
34. 5 using equilibrium and kinetic fluorescence measurements. Biochemistry 1999, 38:9533-9540.
35. Engelman D.M., Chen Y., Chin C.N., Curran A.R., Dixon A.M., Dupuy A.D., et al. Membrane protein folding: beyond the two-stage model. FEBS Lett. 2003, 555:122-125.
36. Joh N.H., Min A., Faham S., Whitelegge J.P., Yang D., Woods V.L., Bowie J.U. Modest stabilization by most hydrogen-bonded side-chain interactions in membrane proteins. Nature 2008, 453:1266-1270.
37. Joh N.H., Oberai A., Yang D., Whitelegge J.P., Bowie J.U. Similar energetic contributions of packing in the core of membrane and water-soluble proteins. J. Am. Chem. Soc. 2009, 131:10846-10847.
38. Manning M., Colon W. Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a role for rigidity and a bias toward β-sheet structure. Biochemistry 2004, 43:11248-11254.
39. Krebs M.P., Hauss T., Heyn M.P., RajBhandary U.L., Khorana H.G. Expression of the bacterioopsin gene in Halobacterium halobium using a multicopy plasmid. Proc. Natl Acad. Sci. USA 1991, 88:859-863.
40. Krebs M.P., Mollaaghababa R., Khorana H.G. Gene replacement in Halobacterium halobium and expression of bacteriorhodopsin mutants. Proc. Natl Acad. Sci. USA 1993, 90:1987-1991.
41. Cline S.W., Doolittle F.W. Efficient transfection of the archaebacterium Halobacterium halobium. J. Bacteriol. 1987, 169:1341-1344.
42. Whitelegge J.P., Gundersen C.B., Faull K.Y. Electrospray-ionization mass spectroscopy of intact intrinsic membrane proteins. Protein Sci. 1998, 7:1423-1430.
43. Oesterhelt D., Schuhmann L., Gruber H. Light-dependent reaction of bacteriorhodopsin with hydroxylamine in cell suspensions of Halobacterium halobium: demonstration of an apo-membrane. FEBS Lett. 1974, 44:257-261.
44. Brouillete C.G., McMichens R.B., Stern L.J., Khorana H.G. Structure and thermal stability of monomeric bacteriorhodopsin in mixed phospholipid/detergent mixtures. Proteins: Struct. Funct. Genet. 1989, 5:38-46.
45. Sehgal P., Mogensen J.E., Otzen D.E. Using micellar mole fractions to assess membrane protein stability in mixed micelles. Biochim. Biophys. Acta 2005, 1716:59-68.
46. Zarrine-Afsar A., Davidson A.R. The analysis of protein folding kinetic data produced in protein engineering experiments. Methods 2004, 34:41-50.