Synergistic interactions between aqueous and membrane domains of a designed protein determine its fold and stability

Journal of Molecular Biology

Volumn 348, Issue 5, 2005, Pages 1225-1233

  Cristian, Lidia ^a   Nanda, Vikas ^a   Lear, James D ^a   DeGrado, William F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Coiled coils; Helical bundles; Membrane proteins; Polar interactions; Thiol disulfide exchange

Indexed keywords

ASPARAGINE; DIMER; MEMBRANE PROTEIN; MEMBRANE PROTEIN MS 1; MONOMER; UNCLASSIFIED DRUG; VALINE; WATER;

AQUEOUS SOLUTION; ARTICLE; HYBRID; INTERMETHOD COMPARISON; MICELLE; OLIGOMERIZATION; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEDIMENTATION; SOLUBILITY; THERMODYNAMICS; ULTRACENTRIFUGATION;

EID: 18144370753     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.03.053     Document Type: Article

References (41)

1. J.L. Popot, and D.M. Engelman Helical membrane protein folding, stability, and evolution Annu. Rev. Biochem. 69 2000 881 922
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. F. Marassi, and S. Opella NMR structural studies of membrane proteins Curr. Opin. Struct. Biol. 8 1998 640 648
4. P. Booth, and A. Curran Membrane protein folding Curr. Opin. Struct. Biol. 9 1999 115 121
5. A. Arora, and L.K. Tamm Biophysical approaches to membrane protein structure determination Curr. Opin. Struct. Biol. 11 2001 540 547
6. C. Choma, H. Gratkowski, J.D. Lear, and W.F. Degrado Asparagine-mediated self association of a model transmembrane helix Nature Struct. Biol. 7 2000 161 166
7. C.M. Deber, L.P. Liu, and C. Wang Perspective: peptides as mimics of transmembrane segments in proteins J. Pept. Res. 54 1999 200 205
8. W.C. Wimley, and S.H. White Designing transmembrane alpha-helices that insert spontaneously Biochemistry 39 2000 4342 4432
9. M.A. Lemmon, and D.M. Engelman Specificity and promiscuity in membrane helix interactions FEBS Letters 346 1994 17 20
10. W. Degrado, H. Gratkowski, and J. Lear How do helix-helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo-oligomeric helical bundles Protein Sci. 12 2003 647 665
11. M. Bennett, J.A. Yeagle, M. Maciejewski, J. Ocampo, and P.L. Yeagle Stability of loops in the structure of lactose permease Biochemistry 43 2004 12829 12837
12. M. Katragadda, J.L. Alderfer, and P.L. Yeagle Solution structure of the loops of bacteriorhodopsin closely resembles the crystal structure Biochim. Biophys. Acta 1466 2000 1 6
13. T. Haltia, and E. Freire Forces and factors that contribute to the structural stability of membrane proteins Biochim. Biophys. Acta 1228 1995 1 27
14. T. Kahn, J. Sturtevant, and D. Engelman Thermodynamic measurements of contributions of helix-connecting loops and of retinal to the stability of bacteriorhodopsin Biochemistry 31 1992 8829 8839
15. Discher, B., Lear, J., Moser, C., Dutton, P. (2002). De novo design of functional membrane peptides. Biophys. J. 82, 458A.
16. B.M. Discher, R.L. Koder, C.C. Moser, and P.L. Dutton Hydrophilic to amphiphilic design in redox protein maquettes Curr. Opin. Chem. Biol. 7 2003 741 748
17. H. Gratkowski, Q.-H. Dai, J. Wand, W.F. Degrado, and J.D. Lear Cooperativity and specificity of association of a designed transmembrane peptide Biophys. J. 83 2002 1613 1619
18. E.K. O'Shea, R. Rutkowski, and P.S. Kim Evidence that the leucine zipper is a coiled coil Science 243 1989 538 542
19. E.K. O'Shea, J.D. Klemm, P.S. Kim, and T. Alber X-ray structure of the GCN4 leucine zipper. A two-stranded, parallel coiled coil Science 254 1991 539 544
20. P.B. Harbury, P.S. Kim, and T. Alber Crystal structure of an isoleucine-zipper trimer Nature 371 1994 80 83
21. P.B. Harbury, T. Zhang, P.S. Kim, and T. Alber A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants Science 262 1993 1401 1407
22. N.L. Ogihara, M.S. Weiss, W.F. Degrado, and D. Eisenberg The crystal structure of the designed trimeric coiled coil coil-vald: implications for engineering crystals and supramolecular assemblies Protein Sci. 6 1997 80 88
23. J.A. Boice, D. G.R., D. W.F., and F. R. Thermodynamic analysis of a designed three-stranded coiled coil Biochemistry 35 1996 14480 14485
24. S. Betz, R. Fairman, K. O'Neil, J. Lear, and W. Degrado Design of two-stranded and three-stranded coiled-coil peptides Philos. Trans. Roy. Soc. ser. B 348 1995 81 88
25. L. Gonzalez Jr, D.N. Woolfson, and T. Alber Buried polar residues and structural specificity in the GCN4 leucine zipper Nature Struct. Biol. 3 1996 1011 1018
26. K.J. Lumb, and P.S. Kim A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil Biochemistry 34 1995 8642 8648
27. L. Gonzalez Jr, R.A. Brown, D. Richardson, and T. Alber Crystal structures of a single coiled-coil peptide in two oligomeric states reveal the basis for structural polymorphism Nature Struct. Biol. 3 1996 1002 1009
28. L. Cristian, J.D. Lear, and W.F. Degrado Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers Proc. Natl Acad. Sci. USA 100 2003 14772 14777
29. M.G. Oakley, and P.S. Kim A buried polar interaction can direct the relative orientation of helices in a coiled coil Biochemistry 37 1998 12603 112610
30. Summa, C.M. (2002). Computational methods and their applications for de novo functional protein design and membrane protein solubilization, PhD Thesis, University Of Pennsylvania.
31. G.R. Dieckmann, and W.F. Degrado Modeling transmebrane helical oligomers Curr. Opin. Struct. Biol. 7 1997 486 494
32. S.J. Weiner, P.A. Kollman, D.A. Case, U.C. Singh, C. Ghio, and G. Alagona A new force field for molecular mechanical simulation of nucleic acids and proteins J. Am. Chem. Soc. 106 1984 765 784
33. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus Charmm - a program for macromolecular energy. Minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
34. R.L.J. Dunbrack, and F.E. Cohen Bayesian statistical analysis of protein side-chain rotamer preferences Protein Sci. 6 1997 1661 1681
35. J. Desmet, M. Demaeyer, B. Hazes, and I. Lasters The dead-end elimination theorem and its use in protein side-chain positioning Nature 356 1992 539 542
36. R.F. Goldstein Efficient rotamer elimination applied to protein side-chains and related spin glasses Biophys. J. 66 1994 1335 1340
37. L. Cristian, J.D. Lear, and W.F. Degrado Determination of membrane protein stability via thermodynamic coupling of folding to thiol-disulfide interchange Protein Sci. 12 2003 1732 1740
38. A. Furst The XL-I analytical ultracentrifuge with Rayleigh interference optics Eur. Biophys. J. 25 1997 307 310
39. C. Tanford, and J.A. Reynolds Characterization of membrane proteins in detergent solution Biochim. Biophys. Acta 457 1976 133 170
40. T. Laue, B.D. Shaw, T.M. Ridgeway, and S.L. Pelletier Computer-aided interpretation of analytical sedimentation data for proteins S.E. Harding A.J. Rowe J.C. Horton Analytical Ultracentrifugation In Biochemistry And Polymer Science 1992 The Royal Society Of Chemistry Cambridge, UK 90 125
41. G.G. Kochendoerfer, D. Salom, J.D. Lear, R. Wilk-Orescan, S.B.H. Kent, and W.F. Degrado Total chemical synthesis of the integral membrane protein influenza A virus M2: role of its C-terminal domain in tetramer assembly Biochemistry 38 1999 11905 11913