Defining the minimum size of a hydrophobic cluster in two-stranded α-helical coiled-coils: Effects on protein stability

Protein Science

Volumn 13, Issue 3, 2004, Pages 714-726

  Lu, Stephen M ^a   Hodges, Robert S ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Coiled coil; De novo design; Hydrophobic clusters; Protein stability

Indexed keywords

ALANINE; DISULFIDE; ISOLEUCINE; LEUCINE;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN STABILITY;

ALANINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; CONSENSUS SEQUENCE; DATABASES, PROTEIN; HEAT; HYDROPHOBICITY; ISOLEUCINE; LEUCINE; MODELS, MOLECULAR; PEPTIDES; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TROPOMYOSIN; ULTRACENTRIFUGATION; UREA;

EID: 1342268069     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03443204     Document Type: Article

References (51)

1. Akey, D.L., Malashkevich, V.N., and Kim, P.S. 2001. Buried polar residues in coiled-coil interfaces. Biochemistry. 40: 6352-6360.
2. Berger, B., Wilson, D.B., Wolf, E., Tonchev, T., Milla, M., and Kim, P.S. 1995. Predicting coiled coils by use of pairwise residue correlations. Proc. Natl. Acad. Sci. 92: 8259-8263.
3. Brown, J.H., Cohen, C., and Parry, D.A.D. 1996. Heptad breaks in α-helical coiled coils: Stutters and stammers. Proteins 26: 134-145.
4. Brown, J.H., Kim, K.H., Jun, G., Greenfield, N.J., Dominguez, R., Volkmann, N., Hitchcock-DeGregori, S.E., and Cohen, C. 2001. Deciphering the design of the tropomyosin molecule. Proc. Natl. Acad. Sci. 98: 8496-8501.
5. Burkhard, P., Stetefeld, J., and Strelkov, S.V. 2001. Coiled coils: A highly versatile protein folding motif. Trends Cell Biol. 11: 82-88.
6. Chakrabartty, A., Kortemme, T., and Baldwin, R.L. 1994. Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci. 3: 843-852.
7. Chen, Y.H., Yang, J.T., and Chau, K.H. 1974. Determination of the helix and β form of proteins in aqueous solution by circular dichroism. Biochemistry 13: 3350-3359.
8. Daggett, V. and Fersht, A.R. 2003. Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28: 18-25.
9. Dill, K.A. 1990. Dominant forces in protein folding. Biochemistry 29: 7133-7155.
10. Dragan, A.I. and Privalov, P.L. 2002. Unfolding of a leucine zipper is not a simple two-state transition. J. Mol. Biol. 321: 891-908.
11. Dürr, E. and Jelesarov, I. 2000. Thermodynamic analysis of cavity creating mutations in an engineered leucine zipper and energetics of glyercol-induced coiled-coil stabilization. Biochemistry 39: 4472-4482.
12. Harbury, P.B., Zhang, T., Kim, P.S., and Alber, T. 1993. A switch between two-, three-, and four-stranded coiled-coils in GCN4 leucine zipper mutants. Science 262: 1401-1407.
13. Hayes, D.B., Laue, T., and Philo, J. 2003. SEDNTERP v. 1.06. University of New Hampshire.
14. Hitchcock-DeGregori, S.E., Song, Y., and Greenfield, N. 2002. Functions of tropomyosin's periodic repeats. Biochemistry 41: 15036-15044.
15. Hodges, R.S., 1996. De novo design of α-helical proteins: Basic research to medical applications. Biochem. Cell Biol. 74: 133-154.
16. Hodges, R.S., Sodek, J., Smillie, L.B., and Jurasek, L. 1972. Tropomyosin: Amino acid sequence and coiled-coil structure. Cold Spring Harb. Symp. Quant. Biol. 37: 299-310.
17. α-NMR studies of folding equilibria in a two-stranded coiled-coil formed by residues 190-254 of α-tropomyosin. Biopolymers 59: 257-265.
18. Kauzmann, W. 1959. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 14: 1-63.
19. Kellis Jr., J.T., Nyberg, K., and Fersht, A.R. 1989. Energetics of complementary side-chain packing in a protein hydrophobic core. Biochemistry 28: 4914-4922.
20. Kohn, W.D., Kay, C.M., and Hodges, R.S. 1998. Orientation, positional, additivity, and oligomerization-state effects of interhelical ion pairs in α-helical coiled-coils. J. Mol. Biol. 283: 993-1012.
21. Kwok, S.C. and Hodges, R.S. 2003. Clustering of large hydrophobes in the hydrophobic core of two-stranded α-helical coiled-coils controls protein folding and stability. J. Biol. Chem. 278: 35248-35254.
22. Landis, C., Back, N., Homsher, E., and Tobacman, L.S. 1999. Effect of tropomyosin internal deletions on thin filament function. J. Biol. Chem. 274: 31279-31285.
23. Lau, S.Y., Taneja, A.K., and Hodges, R.S. 1984. Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and formation of two-stranded α-helical coiled-coils. J. Biol. Chem. 259: 13253-13261.
24. Lavigne, P., Kondejewski, L.H., Houston Jr., M.E., Sonnichsen, F.D., Lix, B., Skyes, B.D., Hodges, R.S., and Kay, C.M. 1995. Preferential heterodimeric parallel coiled-coil formation by synthetic Max and c-Myc leucine zippers: A description of putative electrostatic interactions responsible for the specificity of heterodimerization. J. Mol. Biol. 254: 505-520.
25. Lee, D.L., Ivaninskii, S., Burkhard, P., and Hodges, R.S. 2003. Unique stabilizing interactions identified in the two-stranded α-stranded coiled-coil: Crystal structure of a cortexillin I/GCN4 hybrid coiled-coil peptide. Protein Sci. 12: 1395-1405.
26. Levinthal, C. 1968. Are there pathways for protein folding? Journal de Chemie Physique 65: 44-45.
27. Liu, J., Cao, W., and Lu. M. 2002. Core side-chain packing and backbone conformation in Lpp-56 coiled-coil mutants. J. Mol. Biol. 318: 877-888.
28. Lupas, A. 1996. Coiled-coils: New structures and new functions. Trends Biochem. Sci. 21: 375-382.
29. Lupas, A., Van Dyke, M., and Stock, J. 1991. Predicting coiled coils from protein sequences. Science 252: 1162-1164.
30. Monera, O.D., Kay, C.M., and Hodges, R.S. 1994. 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.
31. O'Neil, K.T. and DeGrado, W.F. 1990. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250: 646-651.
32. Pace, N.C. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131: 266-280.
33. Paulucci, A.A., Hicks, L., Machado, A., Miranda, M.T.M., Kay, C.M., and Farah, C.S. 2002. Specific sequences determine the stability and cooperativity of folding of the C-terminal half of tropomyosin. Biochemistry 277: 39574-39584.
34. Perry, S.V. 2001. Vertebrate tropomyosin: Distribution, properties and function. J. Muscle Res. Cell Motil. 22: 5-49.
35. Santoro, M.M. and Bolen, D.W. 1988. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethane-sulfonyl α-chymotrypsin using different denaturants. Biochemistry 27: 8063-8068.
36. Sodek, J., Hodges, R.S., Smillie, L.B., and Jurasek, L. 1972. Amino-acid sequence of rabbit skeletal tropomyosin and its coiled-coil structure. Proc. Natl. Acad. Sci. 69: 3800-3804.
37. Strelkov, S.V. and Burkhard, P. 2002. Analysis of α-helical coiled-coils with the program TWISTER reveals a structural mechanism for stutter compensation. J. Struct. Biol. 137: 54-64.
38. Suarez, M.C., Lehrer, S.S., and Silva, J.L. 2001. Local heterogeneity in the pressure naturation of the coiled-coil tropomyosin because of subdomain folding units. Biochemistry 40: 1300-1307.
39. Thompson Kenar, K., Garcia-Moreno, B., and Freire, E. 1995. A calorimetric characterization of the salt dependence of the stability of the GCN4 leucine zipper. Protein Sci. 4: 1934-1938.
40. Tripet, B. and Hodges, R.S. 2001. STABLECOIL: An algorithm designed to predict the location and relative stability of coiled-coils in native protein sequences. In Peptides: The wave of the future (eds. M. Lebl and R. Houghten), pp. 365-366. American Peptide Society, San Diego.
41. Tripet, B., Wagschal, K., Lavigne, P., Mant, C.T., and Hodges, R.S. 2000. Effects of side-chain characteristics on stability and oligomerization state of a de novo-designed model coiled-coil: 20 amino acid substitutions in position d. J. Mol. Biol. 300: 377-402.
42. Wagschal, K., Tripet, B., and Hodges, R.S. 1999a. De novo design of a model peptide sequence to examine the effects of single amino acid substitutions in the hydrophobic core on both stability and oligomerization state of coiled-coils. J. Mol. Biol. 285: 785-803.
43. Wagschal, K., Tripet, B., Lavigne, P., Mant, C.T., and Hodges, R.S. 1999b. The role of position a in determining the stability and oligomerization state of α-helical coiled-coils: 20 amino acid stability coefficients in the hydrophobic core of proteins. Protein Sci. 8: 2312-2329.
44. Wendt, H., Berger, B., Baici, A., Thomas, R.M., and Bosshard, H.R. 1995. Kinetics of folding of leucine zipper domains. Biochemistry 34: 4097-4107.
45. Wolf, E., Kim, P.S., and Berger, B. 1997. Multicoil: A program for predicting two- and three-stranded coiled-coil. Protein Sci. 6: 1179-1189.
46. Yphantis, D.A., Johnson, M.L., and Lary, J.W. 1997. WINNONLIN v. 1.06. University of Connecticut.
47. Yu, Y., Monera, O.D., Hodges, R.S., and Privalov, P.L. 1996. Investigation of electrostatic interactions in two-stranded coiled-coils through residue shuffling. Biophys. Chem. 59: 299-314.
48. Zhou, N.E., Zhu, B.Y., Kay, C.M., and Hodges, R.S. 1992a. The two-stranded α-helical coiled-coil is an ideal model for studying protein stability and subunit interactions. Biopolymers 32: 419-426.
49. Zhou, N.E., Kay, C.M., and Hodges, R.S. 1992b. Synthetic model proteins: The relative contribution of leucine residues at non-equivalent positions of the 3-4 hydrophobic repeat to the stability of the two-stranded α-helical coiled-coil. Biochemistry 31: 5739-5746.
50. Zhou, N.E., Monera, O.D., Kay, C.M., and Hodges, R.S. 1994. α-Helical propensities of amino acids in the hydrophobic face of an amphiphathic α-helix. Protein Pept. Lett. 1: 114-119,
51. Zhu, B.Y., Zhou, N.E., Kay, CM., and Hodges, R.S. 1993. Packing and hydrophobicity effects in protein folding and stability. Effects of β-branched amino acids, valine and isoleucine, on the formation and stability of two-stranded α-helical coiled-coils/leucine zippers. Protein Sci. 2: 383-394.