An inverse correlation between loop length and stability in a four-helix-bundle protein

Folding and Design

Volumn 2, Issue 1, 1997, Pages 67-75

  Nagi, Athena D ^a   Regan, Lynne ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Entropy; Four helix bundle; Loop closure; Polymer models; Protein stability

Indexed keywords

DITERPENE; ROP;

ARTICLE; AUDIOVISUAL EQUIPMENT; CHEMICAL MODEL; CHEMISTRY; MOLECULAR CLONING; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; STATISTICS; THERMODYNAMICS; ULTRACENTRIFUGATION;

CLONING, MOLECULAR; DITERPENES; MODELS, CHEMICAL; MODELS, STRUCTURAL; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; STATISTICS; THERMODYNAMICS; ULTRACENTRIFUGATION;

EID: 0030623398     PISSN: 13590278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1359-0278(97)00007-2     Document Type: Article

References (53)

1. Dyson, H.J., Ranee, M., Houghten, R.A., Lerner, R.A. & Wright, P.E. (1988). Folding of immunogenic peptide fragments of proteins in water solution I. Sequence requirements for the formation of a reverse turn. J. Mol. Biol. 201, 161-200.
2. Chou, P.Y. & Fasman, G.D. (1974). Conformational parameters for amino acids in helical, beta-sheet and random coil regions calculated from proteins. Biochemistry 13, 211-222.
3. Rose, G., Gierasch, L. & Smith, J. (1985). Turns in peptides and proteins. Adv. Protein Chem. 37, 1-109.
4. Wright, P.E., Dyson, H.J. & Lerner, R.A. (1988). Conformation of peptide fragments of proteins in aqueous solution: implications for initiation of protein folding. Biochemistry 27, 7167-7175.
5. Milburn, P.J., Konishi, Y., Meinwald, Y.C. & Scheraga, H.A. (1987). Chain reversals in model peptides: studies of cystine-containing cyclic peptides. 1. Conformational free energies of cyclization of hexapeptides of sequence Ac-Cys-X-Pro-Gly-Y-Cys-NHMe. J. Am. Chem. Soc. 109, 4486-4496.
6. Falcomer, C.M., et al., & Scheraga, H.A. (1992). Chain reversals in model peptides: studies of cystine-containing cyclic peptides. 3. Conformational free energies of cyclization of tetrapeptides of sequence Ac-Cys-Pro-X-Cys-NHMe. J. Am. Chem. Soc. 114, 4036-4042.
7. Hutchinson, E.G. & Thornton, J.M. (1994). A revised set of potentials for β-turn formation in proteins. Protein Sci. 3, 2207-2216.
8. Scully, J. & Hermans, J. (1994). Backbone flexibility and stability of reverse turn conformation in a model system. J. Mol. Biol. 235, 682-694.
9. Sibanda, B.L. & Thornton, J.M. (1985). β-hairpin families in globular proteins. Nature 316, 170-174.
10. Sibanda, B.L. & Thornton, J.M. (1993). Accommodating sequence changes in β-hairpins in proteins. J. Mol. Biol. 229, 428-447.
11. Fetrow, J.S. (1995). Omega loops: nonregular secondary structures significant in protein function and stability. FASEB J. 9, 708-717.
12. Leszczynski, J. & Rose, G. (1986). Loops in globular proteins: a novel category of secondary structure. Science 234, 849-855.
13. Tramontano, A., Chothia, C. & Lesk, A.M. (1989). Structural determinants of the conformations of medium-sized loops in proteins. Proteins 6, 382-394.
14. Martin, A.C.R., Toda, K., Stirk, H.J. & Thornton, J.M. (1995). Long loops in proteins. Protein Eng. 8, 1093-1101.
15. Ramachandran, G.N. & Sassiekharan, V. (1968). Conformation of polypeptides and proteins. Adv. Protein Chem. 28, 283-437.
16. Toma, S., et al., & Fontana, A. (1991). Grafting of a calcium-binding loop of thermolysin to Bacillus subtilis neutral protease. Biochemistry 30,97-106.
17. Wolfson, A.J., Kanaoka, M., Lau, F.T.K. & Ringe, D. (1991). Insertions of an elastase-binding loop into interleukin-1β. Protein Eng. 4, 313-317.
18. 2+-binding chimera of human lysozyme and bovine ot-lactalbumin that can form a molten globule. J. Biol. Chem. 270, 10514-10524.
19. Hynes, T.R., Kautz, R.A., Goodman, M.A., Gill, J.F. & Fox, R.O. (1989). Transfer of a β-turn structure to a new protein context. Nature 339, 73-76.
20. Riechmann, L, Clark, M., Waldmann, H. & Winter, G. (1988). Reshaping human antibodies for therapy. Nature 332, 323-327.
21. Jones, P.T., Dear, P.M., Foote, J., Neuberger, M.S. & Winter, G. (1986). Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321, 522-525.
22. Barbas, C.F.I., Languino, L.R. & Smith, J.W. (1993). High-affinity selfreactive human antibodies by design and selection: targeting the integrin ligand binding site. Proc. Natl. Acad. Sci. USA 90, 10003-10007.
23. Fetrow, J.S., Cardillo, T.S. & Sherman, F. (1989). Deletions and replacements of omega loops in yeast iso-1-cytochrome c. Proteins 6, 372-381.
24. Ybe, J. & Hecht, M. (1996). Sequence replacements in the central βturn of plastocyanin. Protein Sci. 5, 814-824.
25. Brunei, A.P., Huang, E.S., Huffine, M.E., Loeb, J.E., Weltman, R.J. & Hecht, M.H. (1993). The role of turns in the structure of an α-helical protein. Nature 364, 355-358.
26. Predki, P.F., Agrawal, V., Brünger, AT. & Regan, L (1996). Amino-acid substitutions in a surface turn modulate protein stability. Nat. Struct. Biol. 3, 54-58.
27. Zhou, H.X., Hoess, R.H. & DeGrado, W.F. (1996). In vitro evolution of thermodynamically stable turns. Nat. Struct. Biol. 3, 446-450.
28. Cooper, A., Eyles, S.J., Radford, S.E. & Dobson, C.M. (1992). Thermodynamic consequences of the removal of a disulphide bridge from hen lysozyme. J. Mol. Biol. 225, 939-943.
29. Matsumura, M., Gecktel, W.J., Levitt, M. & Matthews, B.W. (1989). Stabilization of phage T4 lysozyme by engineered disulfide bonds. Proc. Natl. Acad. Sci. USA 86, 6562-6566.
30. Ho, S.P. & DeGrado, W.F. (1987). Design of a 4-helix bundle protein: synthesis of peptides which self-associate into a helical protein. J. Am. Chem. Soc. 109, 6751-6758.
31. Predki, P.F. & Regan, L (1995). Redesigning the topology of a fourhelix-bundle protein: monomeric Rop. Biochemistry 34, 9834-9839.
32. Helms, LR. & Wetzel, R. (1995). Destabilizing loop swaps in the CDRs of an immunoglobulin VI domain. Protein Sci. 4, 2073-2081.
33. Banner, D., Kokkinidis, M. & Tsernoglou, D. (1987). Structure of the ColE1 Rop protein at 1.7 Å resolution. J. Mol. Biol. 196, 657-675.
34. Castagnoli, L., Scarpa, M., Kokkinidis, M., Banner, D.W., Tsernoglou, D. & Cesareni, G. (1989). Genetic and structural analysis of the ColE1 Rop (Rom) protein. EMBO J. 8, 621-629.
35. Chou, P.Y. & Fasman, G.D. (1978). Predictions of the secondary structure of proteins from their amino acid sequence. Adv. Enzymol. 47, 45-148.
36. Schimmel, P.R. & Flory, P.J. (1967). Conformation energy and configurational statistics of poly-L-proline. Prac. Natl. Acad. Sci. USA 58, 52-59.
37. Flory, P.J. & Schimmel, P.R. (1967). Dipole moments in relation to configuration of polypeptide chains. J. Am. Chem. Soc. 89, 6807-6813.
38. Munson, M., O'Brien, R., Sturtevant, J.M. & Regan, L. (1994). Redesigning the hydrophobic core of a four-helix-bundle protein. Protein Sci. 3, 2015-2022.
39. Lau, S.Y.M., Taneja, A.K. & Hodges, R.S. (1984). Synthesis of a model protein of defined secondary and quaternary structure. J. Biol. Chem. 259, 13252-13261.
40. Monera, O.D., Zhou, N.E., Kay, C.M. & Hodges, R.S. (1993). Comparison of antiparallel and parallel two-stranded α-helical coiled-coils. J. Biol. Chem. 268, 19218-19227.
41. Monera, O.D., Kay, C.M. & Hodges, R.S. (1991). Protein denaturation with guanidine hydrochloride or urea provides a different estimate of stability depending on the contributions of electrostatic interactions. Protein Sci. 3, 1984-1991.
42. Predki, P.F., Nayak, L.M., Gottlieb, M.B. & Regan, L. (1995). Dissecting RNA-protein interactions: RNA-RNA recognition by Rop. Cell 80, 41-50.
43. Thornton, J.M., Sibanda, B.L., Edwards, M.S. & Barlow, D.J. (1988). Analysis, design & modification of loop regions in proteins. Bioessays 8, 63-69.
44. Matthews, B.W., Nicholson, H. & Becktel, W.J. (1987). Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl. Acad. Sci. USA 84, 6663-6667.
45. Camacho, C.J. & Thirumalai, D. (1995). Modeling the role of disulfide bonds in protein folding: entropic barriers and pathways. Proteins 22, 27-40.
46. Pace, C.N., Grimsley, G.R., Thomson, J.A. & Barnett, B.J. (1988). Conformational stability and activity of ribonuclease T1 with zero, one and two intact disulfide bonds. J. Biol. Chem. 263, 11820-11825.
47. Jerala, R. (1992). Simultaneous synthesis of degenerate oligonucleotides of variable length. Biotechniques 13, 564-567.
48. Sambrook, J., Fritsch, E. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, New York.
49. Munson, M., Predki, P.F. & Regan, L. (1994). ColE1-compatible vectors for high-level expression of cloned DNAs from the T7 promoter. Gene 144, 59-62.
50. Santoro, M.M. & Bolen, D.W. (1988). Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl-alpha-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068.
51. Munson, M., et al., & Regan, L. (1996). What makes a protein a protein? Hydrophobic core designs that specify stability and structural properties. Protein Sci. 5, 1584-1594.
52. Cohn, EJ. & Edsall, J.T. (1943). Density and apparent specific volume of proteins. In Proteins, Amino Acids, and Peptides, pp. 370-381, Reinhold Publishing, Inc, New York, NY.
53. Chan, H.S. & Dill, K.A. (1988). Intrachain loops in polymers. J. Chem. Phys. 90, 492-509.