Sequence Composition Effects on Denatured State Loop Formation in Iso-1-cytochrome c Variants: Polyalanine versus Polyglycine Inserts

Journal of Molecular Biology

Volumn 371, Issue 3, 2007, Pages 577-584

  Tzul, Franco O ^a   Kurchan, Eydiejo ^a   Bowler, Bruce E ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

denatured states; loop formation; protein folding; sequence composition; side chain sterics

Indexed keywords

ALANINE DERIVATIVE; CYTOCHROME C; GLYCINE; GLYCINE DERIVATIVE; GUANIDINE; HEME; HISTIDINE; ISOCYTOCHROME C1; POLYALANINE; POLYGLYCINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; DENATURATION; MATHEMATICAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; THERMODYNAMICS;

EID: 34447624167     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.04.060     Document Type: Article

References (49)

1. Tanford C. Protein denaturation. Adv. Protein Chem. 23 (1968) 121-282
2. Fleming P.J., and Rose G.D. Conformational properties of unfolded proteins. In: Buchner J., and Kiefhaber T. (Eds). Protein Folding Handbook, part I (2005), Wiley-VCH, Weinheim, Germany 710-736
3. Garcia P., Serrano L., Durand D., Rico M., and Bruix M. NMR and SAXS characterization of the denatured state of the chemotactic protein CheY: implications for protein folding initiation. Protein Sci. 10 (2001) 1100-1112
4. Klein-Seetharaman J., Oikawa M., Grimshaw S.B., Wirmer J., Duchardt E., Ueda T., et al. Long-range interactions within a non-native protein. Science 295 (2002) 1719-1722
5. Bond C.J., Wong K., Clarke J., Fersht A.R., and Daggett V. Characterization of residual structure in the thermally denatured state of barnase by simulation and experiment: description of the folding pathway. Proc. Natl Acad. Sci. USA 94 (1997) 13409-13413
6. Shortle D., and Ackerman M.S. Persistence of native-like topology in a denatured protein in 8 M urea. Science 293 (2001) 487-489
7. Kazmirski S.L., Wong K., Freund M.V., Tan Y., Fersht A.R., and Daggett V. Protein folding from a highly disordered denatured state: the folding pathway of chymotrypsin 2 inhibitor at atomic resolution. Proc. Natl Acad. Sci. USA 98 (2001) 4349-4354
8. Dill K., and Shortle D. Denatured states of proteins. Annu. Rev. Biochem. 60 (1991) 795-825
9. Shortle D. Structural analysis of non-native states of proteins by NMR methods. Curr. Opin. Struct. Biol. 6 (1996) 24-30
10. Kohn J.E., Millett I.S., Jacob J., Zagrovic B., Dillon T.M., Cingel N., et al. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl Acad. Sci. USA 101 (2004) 12491-12496
11. Bowler B.E. Thermodynamics of protein denatured states. Mol. BioSyst. 3 (2007) 88-99
12. Cho J., Sato S., and Raleigh D. Thermodynamics and kinetics in protein folding: a single point mutant significantly stabilizes the N-terminal domain of L9 by modulating non-native interactions in the denatured state. J. Mol. Biol. 338 (2004) 827-837
13. Cho J., and Raleigh D. Mutational analysis demonstrates that specific electrostatic interactions can play a key role in the denatured state ensemble of proteins. J. Mol. Biol. 353 (2005) 174-185
14. Anil B., Craig-Shapiro R., and Raleigh D.P. Design of a hyperstable protein by rational consideration of unfolded state interactions. J. Am. Chem. Soc. 128 (2006) 3144-3145
15. Whitten S.T., and Garcia-Moreno E.B. pH dependence of the stability of staphylococcal nuclease: evidence of substantial electrostatic interactions in the denatured state. Biochemistry 39 (2000) 14292-14304
16. Grimsley G.R., Shaw K.L., Fee L.R., Alston R.W., Huyghues-Despointes B.M., Thurlkill R.L., et al. Increasing protein stability by altering long-range Coulombic interactions. Protein Sci. 8 (1999) 1843-1849
17. Pace C.N., Alston R.W., and Shaw K.L. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci. 9 (2000) 1395-1398
18. Trefethen J.M., Pace C.N., Scholtz J.M., and Brems D.N. Charge-charge interactions in the denatured state influence the folding kinetics of ribonuclease Sa. Protein Sci. 14 (2005) 1934-1938
19. Dill K.A., and Chan H.S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4 (1997) 10-19
20. Eaton W.A., Munoz V., Thompson P.A., Henry E.R., and Hofrichter J. Kinetics and dynamics of loops, α-helices, β-hairpins, and fast folding proteins. Acc. Chem. Res. 31 (1998) 745-753
21. Chan H.S., and Dill K.A. Intrachain loops in polymers: effects of excluded volume. J. Chem. Phys. 90 (1989) 492-509
22. Weikl T.R., and Dill K.A. Folding rates and low-entropy-loss routes of two-state proteins. J. Mol. Biol. 329 (2003) 585-598
23. Fersht A.R. Transition-state structure as a unifying basis in protein folding mechanisms: contact order, chain topology, stability and the extended nucleus mechanism. Proc. Natl Acad. Sci. USA 97 (2000) 1525-1529
24. Roder H., Elöve G.A., and Englander S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and protein NMR. Nature 335 (1988) 700-704
25. Krishna M.M.G., and Englander S.W. The N-terminal and C-terminal motif in protein folding and function. Proc. Natl Acad. Sci. USA 102 (2005) 1053-1058
26. Pierce M.M., and Nall B.T. Fast folding of cytochrome c. Protein Sci. 6 (1997) 618-627
27. Krieger F., Möglich A., and Kiefhaber T. Effect of proline and glycine residues on dynamics and barriers of loop formation in polypeptide chains. J. Am. Chem. Soc. 127 (2005) 3346-3352
28. Robinson C.R., and Sauer R.T. Optimizing the stability of single-chain proteins by linker length and composition mutagenesis. Proc. Natl Acad. Sci. USA 95 (1998) 5929-5934
29. Godbole S., Hammack B., and Bowler B.E. Measuring denatured state energetics: deviations from random coil behavior and implications for the folding of iso-1-cytochrome c. J. Mol. Biol. 296 (2000) 217-228
30. Godbole S., and Bowler B.E. A histidine variant of yeast iso-1-cytochrome c that strongly affects the energetics of the denatured state. J. Mol. Biol. 268 (1997) 816-821
31. Hammack B.N., Godbole S., and Bowler B.E. Cytochrome c folding traps are not due solely to histidine-heme ligation: direct demonstration of a role for N-terminal amino group-heme ligation. J. Mol. Biol. 275 (1998) 719-724
32. Hammack B.N., Smith C.R., and Bowler B.E. Denatured state thermodynamics: residual structure, chain stiffness and scaling factors. J. Mol. Biol. 311 (2001) 1091-1104
33. Smith C.R., Mateljevic N., and Bowler B.E. Effects of topology and excluded volume on protein denatured state conformational properties. Biochemistry 41 (2002) 10173-10181
34. Kurchan E., Roder H., and Bowler B.E. Kinetics of loop formation and breakage in the denatured state of iso-1-cytochrome c. J. Mol. Biol. 353 (2005) 730-743
35. Berghuis A.M., and Brayer G.D. Oxidation state-dependent conformational changes in cytochrome c. J. Mol. Biol. 223 (1992) 959-976
36. Deng W.P.D., and Nickoloff J.A. Site-directed mutagenesis of virtually any plasmid by eliminating a unique site. Anal. Biochem. 200 (1992) 81-88
37. Wandschneider E., Hammack B.N., and Bowler B.E. Evaluation of cooperative interactions between substructures of iso-1-cytochrome c using double mutant cycles. Biochemistry 42 (2003) 10659-10666
38. Pierce M.M., and Nall B.T. Coupled kinetics traps in cytochrome c folding: His-heme misligation and proline isomerization. J. Mol. Biol. 298 (2000) 955-969
39. Kristinsson R., and Bowler B.E. Communication of stabilizing energy between substructures of a protein. Biochemistry 44 (2005) 2349-2359
40. Cantor C.R., and Schimmel P.R. Biophysical Chemistry, Part III: The Behavior of Biological Molecules (1980), W. H. Freeman and Co., San Francisco 1205-1209
41. Flory P.J. Statistical Mechanics of Chain Molecules (1969), John Wiley & Sons, Inc., New York 392-396
42. Miller W.G., Brant D.A., and Flory P.J. Random coil configurations of polypeptide copolymers. J. Mol. Biol. 23 (1967) 67-80
43. Chan H.S., and Dill K.A. The effect of internal constraints on the configurations of chain molecules. J. Phys. Chem. 92 (1990) 3118-3135
44. Krieger F., Fierz B., Bieri O., Drewello M., and Kiefhaber T. Dynamics of unfolded polypeptide chains as models for the earliest steps in protein folding. J. Mol. Biol. 332 (2003) 265-274
45. Onishi S., Kamikubo H., Onitsuka M., Kataoka M., and Shortle D. Conformational preference of polyglycine in solution to elongated structure. J. Am. Chem. Soc. 128 (2006) 16338-16344
46. Anil B., Song B., Tang Y., and Raleigh D.P. Exploiting the right side of the Ramachandran plot: substitution of glycines by d-alanine can significantly increase protein stability. J. Am. Chem. Soc. 126 (2004) 13194-13195
47. Yeh S., and Rousseau D.L. Folding intermediates in cytochrome c. Nature Struct. Biol. 5 (1998) 222-228
48. Lee J.C., Chang I., Gray H.B., and Winkler J.R. The cytochrome c folding landscape revealed by electron-transfer kinetics. J. Mol. Biol. 320 (2002) 159-164
49. Lyubovitsky J.G., Gray H.B., and Winkler J.R. Mapping the cytochrome c folding landscape. J. Am. Chem. Soc. 124 (2002) 5481-5485