Denatured states of low-complexity polypeptide sequences differ dramatically from those of foldable sequences

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 25, 2010, Pages 11364-11369

  Tzul, Franco O ^a,b   Bowler, Bruce E ^a  

^a UNIVERSITY OF MONTANA   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Chain stiffness; Protein folding; Residual structure

Indexed keywords

ALANINE; CYTOCHROME C; ENZYME VARIANT; GUANIDINE; HEME; HYDROCHLORIC ACID; POLYPEPTIDE; HISTIDINE; HISTONE; PEPTIDE; POLYALANINE; PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; ENZYME CONFORMATION; ENZYME DENATURATION; ENZYME KINETICS; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN FOLDING; RHODOPSEUDOMONAS PALUSTRIS; THERMODYNAMICS; YEAST; CHEMISTRY; CONFORMATION; KINETICS; METABOLISM; PH; PROTEIN CONFORMATION; PROTEIN DENATURATION; RHODOPSEUDOMONAS;

RHODOPSEUDOMONAS PALUSTRIS;

CYTOCHROMES C; HEME; HISTIDINE; HISTONES; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR CONFORMATION; PEPTIDES; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEINS; RHODOPSEUDOMONAS; THERMODYNAMICS;

EID: 77954942428     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1004572107     Document Type: Article

References (41)

1. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223-230.
2. Gassner NC, Baase WA, Matthews BW (1996) A test of the "jigsaw puzzle" model for protein folding by multiple methionine substitutions within the core of T4 lysozyme. Proc Natl Acad Sci USA 93:12155-12158.
3. Dyson HJ,Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6:197-208.
4. Wang S, Gu J, Larson SA, Whitten ST, Hilser VJ (2008) Denatured-state energy landscapes of a protein structural database reveal the energetic determinants of a framework model for folding. J Mol Biol 381:1184-1201.
5. Weinkam P, Pletneva EK, Gray HB, Winkler JR, Wolynes PG (2009) Electrostatic effects on funneled landscapes and structural diversity in denatured protein ensembles. Proc Natl Acad Sci USA 106:1796-1801.
6. O'Brien RP, Brooks BR, Thirumalai D (2009) Molecular origin of constant m-values, denatured state collapse, and residue-dependent transition midpoints in globular proteins. Biochemistry 48:3743-3754.
7. Kohn JE, Gillespie B, Plaxco KW (2009) Non-sequence-specific interactions can account for the compaction of proteins unfolded under "native" conditions. J Mol Biol 394:343-350.
8. Fierz B, Kiefhaber T (2005) Dynamics of unfolded polypeptide chains. Protein Folding Handbook, Part I, eds J Buchner and T Kiefhaber (Wiley-VCH, Weinheim), 2, pp 809-855.
9. Kulbeka J, Hofrichter J, Eaton WA (2004) The protein folding speed limit. Curr Opin Struct Biol 14:76-88.
10. Bieri O, et al. (1999) The speed limit for protein folding measured by triplet-triplet energy transfer. Proc Natl Acad Sci USA 96:9567-9601.
11. Lapidus LJ, Eaton WA, Hofrichter J (2000) Measuring the rate of intramolecular contact formation in polypeptides. Proc Natl Acad Sci USA 97:7220-7225.
12. Krieger F, Fierz B, Bieri O, Darwello M, Kiefhaber T (2003) Dynamics of unfolded polypeptide chains as model for the earliest steps in protein folding. J Mol Biol 332:265-274.
13. Krieger F, Möglich A, Kiefhaber T (2005) Effect of proline and glycine residues on dynamics and barriers of loop formation in polypeptide chains. J Am Chem Soc 127:3346-3352.
14. Cortajarena AL, et al. (2008) Non-random coil behavior as a consequence of extensive PPII structure in the denatured state. J Mol Biol 382:203-212.
15. Hammack BN, Smith CR, Bowler BE (2001) Denatured state thermodynamics: Residual structure, chain stiffness and scaling factors. J Mol Biol 311:1091-1104.
16. Wandschneider E, Bowler BE (2004) Conformational properties of the iso-1-cytochrome c denatured state: Dependence on guanidine hydrochloride concentration. J Mol Biol 339:185-197.
17. Rao KS, Tzul FO, Christian AK, Gordon TN, Bowler BE (2009) Thermodynamics of loop formation in the denatured state of Rhodopseudomonas palustris cytochrome c′: Scaling exponents and the reconciliation problem. J Mol Biol 392:1315-1325.
18. Kurchan E, Roder H, Bowler BE (2005) Kinetics of loop formation and breakage in the denatured state of iso-1-cytochrome c. J Mol Biol 353:730-743.
19. Moore GR, Pettigrew GW (1990) Cytochromes c Evolutionary, Structural and Physicochemical Aspects (Springer, Berlin).
20. Berghuis AM, Brayer GD (1992) Oxidation state-dependent conformational changes in cytochrome c. J Mol Biol 223:959-976.
21. 15N chemical shifts and 15N relaxation measurements for oxidized and reduced iso-1-cytochrome c. Biochemistry 38:4480-4492.
22. 15N]-labeled oxidized and reduced iso-1-cytochrome c. Biochemistry 38:4493-4503.
23. Tzul FO, Kurchan E, Bowler BE (2007) Sequence composition effects on denatured state loop formation in iso-1-cytochrome c variants: Polyalanine versus polyglycine inserts. J Mol Biol 371:577-584.
24. Tzul FO, Bowler BE (2009) Importance of contact persistence in denatured state loop formation: Kinetic insights into sequence effects on nucleation early in folding. J Mol Biol 390:124-134.
25. Jacobson H, Stockmayer WH (1950) Intramolecular reaction in polycondensations I. The theory of linear systems. J Chem Phys 18:1600-1606.
26. Kurchan E (2005) Kinetics and thermodynamics in the denatured state of cytochrome c. Ph.D. dissertation (University of Denver, Denver).
27. Bowler BE (2007) Thermodynamics of protein denatured states. Mol Biosyst 3:88-99.
28. Redner S (1980) Distribution functions in the interior of polymer chains. J Phys A-Math Gen 13:3525-3541.
29. Chan HS, Dill KA (1990) The effect of internal constraints on the configurations of chain molecules. J Chem Phys 92:3118-3135.
30. Davis LA, Schejter A, Hess GP (1973) Alkaline isomerization of oxidized cytochrome c. J Biol Chem 249:2624-2632.
31. Goldenberg DP (2003) Conformational simulation of the statistical properties of unfolded proteins. J Mol Biol 326:1615-1633.
32. Tsong TY (1974) The Trp-59 fluorescence of ferricytochrome c as a sensitive measure of the over-all protein conformation. J Biol Chem 249:1988-1990.
33. Schuler B, Eaton WA (2008) Protein folding studies by single-molecule FRET. Curr Opin Struct Biol 18:16-26.
34. Pletneva EV, Gray HB, Winkler JR (2005) Many faces of the unfolded state: Conformational heterogeneity in denatured yeast cytochrome c. J Mol Biol 345:855-867.
35. Fersht A (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (Freeman, New York).
36. Jacob M, Geeves M, Holtermann G, Schmid FX (1999) Diffusional barrier crossing in a two-state protein folding reaction. Nat Struct Biol 6:923-926.
37. Qiu L, Hagen SJ (2004) A limiting speed for protein folding at low solvent viscosity. J Am Chem Soc 126:3398-3399.
38. Qiu L, Hagen SJ (2005) Internal friction in the ultrafast folding of the tryptophan cage. Chem Phys 312:327-333.
39. Möglich A, Krieger F, Kiefhaber T (2005) Molecular basis for the effect of urea and guanidine hydrochloride on the dynamics of unfolded polypeptide chains. J Mol Biol 345:153-162.
40. Rosell FI, Mauk AG (2002) Spectroscopicpropertiesofamitochondrialcytochromec with a single thioether bond to the heme prosthetic group. Biochemistry 41:7811-7818.
41. Deng WPD, Nickoloff JA (1992) Site-directed mutagenesis of virtually any plasmid by eliminating a unique site. Anal Biochem 200:81-88.