Reversible unfolding of β-sheets in membranes: A calorimetric study

Journal of Molecular Biology

Volumn 342, Issue 3, 2004, Pages 703-711

  Wimley, William C ^a   White, Stephen H ^b  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

membrane proteins; membrane induced folding; nucleation; protein folding; barrel

Indexed keywords

AMINO ACID; HEXAPEPTIDE; MEMBRANE PROTEIN; WATER;

ARTICLE; BETA SHEET; CALORIMETRY; CONCENTRATION RESPONSE; DIFFERENTIAL SCANNING CALORIMETRY; ENERGY TRANSFER; ENTHALPY; HEATING; HYDROGEN BOND; ISOTHERM; MATHEMATICAL MODEL; MEMBRANE; PARTITION COEFFICIENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; TEMPERATURE; THERMAL ANALYSIS; THERMODYNAMICS; THERMOSTABILITY; TITRIMETRY;

EID: 4444260314     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.06.093     Document Type: Article

References (50)

1. T. Haltia, and E. Freire Forces and factors that contribute to the structural stability of membrane proteins Biochim. Biophys. Acta 1241 1995 295 322
2. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365
3. B.P. Atanasov, P.L. Privalov, and N.N. Khechinashvili Calorimetric investigations on heat denaturation of cyanmetmyoglobin Mol. Biol. 6 1972 26 32
4. P.L. Privalov, N.N. Khechinashvili, and B.P. Atanasov Thermodynamic analysis of thermal transitions in globular proteins. I. Calorimetric study of chymotrypsinogen, ribonuclease and myoglobin Biopolymers 10 1971 1865 1890
5. P.L. Privalov, and N.N. Khechinashvili Calorimetric investigation of thermal denaturation of chymotrypsinogen Mol. Biol. 5 1971 573 579
6. P.L. Privalov, and E.I. Tiktopulo Thermal conformational transformation of tropocollagen. I. Calorimetric study Biopolymers 9 1970 127 139
7. P.L. Privalov, and N.N. Khechinashvili A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study J. Mol. Biol. 86 1974 665 684
8. P.L. Privalov, and S.J. Gill Stability of protein structure and hydrophobic interaction Advan. Protein Chem. 39 1988 191 234
9. P.L. Privalov, and G.I. Makhatadze Contribution of hydration to protein folding thermodynamics. 2. The entropy and Gibbs energy of hydration J. Mol. Biol. 232 1993 660 679
10. G.I. Makhatadze, and P.L. Privalov Contribution of hydration to protein folding thermodynamics. 1. The enthalpy of hydration J. Mol. Biol. 232 1993 639 659
11. A.-S. Yang, K.A. Sharp, and B. Honig Analysis of the heat capacity dependence of protein folding J. Mol. Biol. 227 1992 889 900
12. M.B. Jackson, and J.M. Sturtevant Phase transitions of the purple membranes of Halobacterium halobium Biochemistry 17 1978 911 915
13. C.D. Heyes, and M.A. El Sayed Effect of temperature, pH, and metal ion binding on the secondary structure of bacteriorhodopsin: FT-IR study of the melting and premelting transition temperatures Biochemistry 40 2001 11819 11827
14. C.D. Heyes, and M.A. El Sayed The role of the native lipids and lattice structure in bacteriorhodopsin protein conformation and stability as studied by temperature-dependent Fourier transform-infrared spectroscopy J. Biol. Chem. 277 2002 29437 29443
15. I. Echabe, T. Haltia, E. Freire, F.M. Goni, and J.L. Arrondo Subunit III of cytochrome c oxidase influences the conformation of subunits I and II: an infrared study Biochemistry 34 1995 13565 13569
16. P.E. Morin, and E. Freire Direct calorimetric analysis of the enzymatic activity of yeast cytochrome c oxidase Biochemistry 30 1991 8494 8500
17. P.E. Morin, D. Diggs, and E. Freire Thermal stability of membrane-reconstituted yeast cytochrome c oxidase Biochemistry 29 1990 781 788
18. J.S. Landin, M. Katragadda, and A.D. Albert Thermal destabilization of rhodopsin and opsin by proteolytic cleavage in bovine rod outer segment disk membranes Biochemistry 40 2001 11176 11183
19. R.F. Epand, R.M. Epand, and C.Y. Jung Ligand-modulation of the stability of the glucose transporter GLUT 1 Protein Sci. 10 2001 1363 1369
20. J.R. Lepock, A.M. Rodahl, C. Zhang, M.L. Heynen, B. Waters, and K.H. Cheng Thermal denaturation of the Ca2(+)-ATPase of sarcoplasmic reticulum reveals two thermodynamically independent domains Biochemistry 29 1990 681 689
21. I.T. Arkin, S.I. Sukharev, P. Blount, C. Kung, and A.T. Brünger Helicity, membrane incorporation, orientation and thermal stability of the large conductance mechanosensitive ion channel from E. coli Biochim. Biophys. Acta 1369 1998 131 140
22. T.E. Creighton Protein Folding 1992 W. H. Freeman and Company, New York
23. C.M. Bishop, W.F. Walkenhorst, and W.C. Wimley Folding of β-sheet membrane proteins: specificity and promiscuity in peptide model systems J. Mol. Biol. 309 2001 975 988
24. W.C. Wimley, K. Hristova, A.S. Ladokhin, L. Silvestro, P.H. Axelsen, and S.H. White Folding of β-sheet membrane proteins: a hydrophobic hexapeptide model J. Mol. Biol. 277 1998 1091 1110
25. A.S. Ladokhin, and S.H. White Folding of amphipathic α-helices on membranes: energetics of helix formation by melittin J. Mol. Biol. 285 1999 1363 1369
26. T. Wieprecht, O. Apostolov, M. Beyermann, and J. Seelig Thermodynamics of the alpha-helix-coil transition of amphipathic peptides in a membrane environment: implications for the peptide-membrane binding equilibrium J. Mol. Biol. 294 1999 785 794
27. M.R. Wenk, and J. Seelig Magainin 2 amide interaction with lipid membranes: calorimetric detection of peptide binding and pore formation Biochemistry 37 1998 3909 3916
28. S.H. White, W.C. Wimley, A.S. Ladokhin, and K. Hristova Protein folding in membranes: determining the energetics of peptide-bilayer interactions Methods Enzymol. 295 1998 62 87
29. W.C. Wimley, and S.H. White Membrane partitioning: distinguishing bilayer effects from the hydrophobic effect Biochemistry 32 1993 6307 6312
30. Y. Li, X. Han, and L.K. Tamm Thermodynamics of fusion peptide-membrane interactions Biochemistry 42 2003 7245 7251
31. G.E. Schulz β-Barrel membrane proteins Curr. Opin. Struct. Biol. 10 2000 443 447
32. J. Deisenhofer, O. Epp, K. Miki, R. Huber, and H. Michel X-ray structure analysis of a membrane protein complex: electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis J. Mol. Biol. 180 1984 385 398
33. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nature Struct. Biol. 3 1996 842 848
34. M.E. Selsted, M.J. Novotny, W.L. Morris, Y.-Q. Tang, W. Smith, and J.S. Cullor Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils J. Biol. Chem. 267 1992 4292 4295
35. W.M. Yau, W.C. Wimley, K. Gawrisch, and S.H. White The preference of tryptophan for membrane interfaces Biochemistry 37 1998 14713 14718
36. S.H. White, and W.C. Wimley Hydrophobic interactions of peptides with membrane interfaces Biochim. Biophys. Acta 1376 1998 339 352
37. D. Marsh CRC Handbook of Lipid Bilayers 1990 CRC Press, Boca Raton
38. G.I. Makhatadze, M.M. Lopez, and P.L. Privalov Heat capacities of protein functional groups Biophys. Chem. 64 1997 93 101
39. E. Terzi, G. Hölzemann, and J. Seelig Reversible random coil-β-sheet transition of the Alzheimer β-amyloid fragment Biochemistry 33 1994 1345 1350
40. J.M. Scholtz, S. Marqusee, R.L. Baldwin, E.J. York, J.M. Stewart, M. Santoro, and D.W. Bolen Calorimetric determination of the enthalpy change for the β-helix to coil transition of an alanine peptide in water Proc. Natl Acad. Sci. USA 88 1991 2854 2858
41. W.C. Wimley, K. Hristova, A.S. Ladokhin, L. Silvestro, P.H. Axelsen, and S.H. White Folding of β-sheet membrane proteins: a hydrophobic hexapeptide model J. Mol. Biol. 277 1998 1091 1110
42. C.M. Bishop, W.F. Walkenhorst, and W.C. Wimley Folding of β-sheet membrane proteins: specificity and promiscuity in peptide model systems J. Mol. Biol. 309 2001 975 988
43. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365
44. W.M. Yau, W.C. Wimley, K. Gawrisch, and S.H. White The preference of tryptophan for membrane interfaces Biochemistry 37 1998 14713 14718
45. W.C. Wimley Toward genomic identification of beta-barrel membrane proteins: composition and architecture of known structures Protein Sci. 11 2002 301 312
46. M.C. Wiener, and S.H. White Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. III. Complete structure Biophys. J. 61 1992 434 447
47. D.A. Doyle, and B.A. Wallace Crystal structure of the gramicidin/potassium thiocyanate complex J. Mol. Biol. 266 1997 963 977
48. R.R. Ketchem, B. Roux, and T.A. Cross High-resolution polypeptide structure in a lamellar phase lipid environment from solid state NMR derived orientational constraints Structure 5 1997 1655 1669
49. L.D. Mayer, M.J. Hope, and P.R. Cullis Vesicles of variable sizes produced by a rapid extrusion procedure Biochim. Biophys. Acta 858 1986 161 168
50. W.C. Wimley, and S.H. White Quantitation of electrostatic and hydrophobic membrane interactions by equilibrium dialysis and reverse-phase HPLC Anal. Biochem. 213 1993 213 217