The Effect of the Polyproline II (PPII) Conformation on the Denatured State Entropy

Overview

Journal Protein Sci

Specialty Biochemistry

Date 2003 Feb 20

PMID 12592015

Citations 23

Authors

Josephine C Ferreon

Vincent J Hilser

Affiliations

Soon will be listed here.

Abstract

Polyproline II (PPII) is reported to be a dominant conformation in the unfolded state of peptides, even when no prolines are present in the sequence. Here we use isothermal titration calorimetry (ITC) to investigate the PPII bias in the unfolded state by studying the binding of the SH3 domain of SEM-5 to variants of its putative PPII peptide ligand, Sos. The experimental system is unique in that it provides direct access to the conformational entropy change of the substituted amino acids. Results indicate that the denatured ensemble can be characterized by at least two thermodynamically distinct states, the PPII conformation and an unfolded state conforming to the previously held idea of the denatured state as a random collection of conformations determined largely by hard-sphere collision. The probability of the PPII conformation in the denatured states for Ala and Gly were found to be significant, approximately 30% and approximately 10%, respectively, resulting in a dramatic reduction in the conformational entropy of folding.

Citing Articles

Structural and dynamic characterization of the C-terminal tail of ErbB2: Disordered but not random.

Pinet L, Wang Y, Deville C, Lescop E, Guerlesquin F, Badache A Biophys J. 2021; 120(10):1869-1882.

PMID: 33741354 PMC: 8204338. DOI: 10.1016/j.bpj.2021.03.005.

Structural and Energetic Characterization of the Denatured State from the Perspectives of Peptides, the Coil Library, and Intrinsically Disordered Proteins.

Paiz E, Lewis K, Whitten S Molecules. 2021; 26(3).

PMID: 33530506 PMC: 7865441. DOI: 10.3390/molecules26030634.

Rapid Quantification of Protein-Ligand Binding via F NMR Lineshape Analysis.

Stadmiller S, Aguilar J, Waudby C, Pielak G Biophys J. 2020; 118(10):2537-2548.

PMID: 32348722 PMC: 7231920. DOI: 10.1016/j.bpj.2020.03.031.

Involvement of Local, Rapid Conformational Dynamics in Binding of Flexible Recognition Motifs.

Bukowski G, Horness R, Thielges M J Phys Chem B. 2019; 123(40):8387-8396.

PMID: 31535866 PMC: 8066399. DOI: 10.1021/acs.jpcb.9b07036.

Sequence Reversal Prevents Chain Collapse and Yields Heat-Sensitive Intrinsic Disorder.

English L, Tischer A, Demeler A, Demeler B, Whitten S Biophys J. 2018; 115(2):328-340.

PMID: 30021108 PMC: 6050754. DOI: 10.1016/j.bpj.2018.06.006.

References

Kelly M, Chellgren B, Rucker A, Troutman J, Fried M, Miller A . Host-guest study of left-handed polyproline II helix formation. Biochemistry. 2001; 40(48):14376-83. DOI: 10.1021/bi011043a. View

Scholtz J, Pace C . Protein conformational stabilities can be determined from hydrogen exchange rates. Nat Struct Biol. 1999; 6(10):910-2. DOI: 10.1038/13273. View

Shi Z, Olson C, Rose G, Baldwin R, Kallenbach N . Polyproline II structure in a sequence of seven alanine residues. Proc Natl Acad Sci U S A. 2002; 99(14):9190-5. PMC: 123116. DOI: 10.1073/pnas.112193999. View

Pappu R, Rose G . A simple model for polyproline II structure in unfolded states of alanine-based peptides. Protein Sci. 2002; 11(10):2437-55. PMC: 2373714. DOI: 10.1110/ps.0217402. View

EDELHOCH H . Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry. 1967; 6(7):1948-54. DOI: 10.1021/bi00859a010. View

TIFFANY M, Krimm S . New chain conformations of poly(glutamic acid) and polylysine. Biopolymers. 1968; 6(9):1379-82. DOI: 10.1002/bip.1968.360060911. View

Ramachandran G, Sasisekharan V . Conformation of polypeptides and proteins. Adv Protein Chem. 1968; 23:283-438. DOI: 10.1016/s0065-3233(08)60402-7. View

TIFFANY M, Krimm S . Effect of temperature on the circular dichroism spectra of polypeptides in the extended state. Biopolymers. 1972; 11(11):2309-16. DOI: 10.1002/bip.1972.360111109. View

Drake A, Siligardi G, Gibbons W . Reassessment of the electronic circular dichroism criteria for random coil conformations of poly(L-lysine) and the implications for protein folding and denaturation studies. Biophys Chem. 1988; 31(1-2):143-6. DOI: 10.1016/0301-4622(88)80019-x. View

10.

Wiseman T, Williston S, Brandts J, Lin L . Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem. 1989; 179(1):131-7. DOI: 10.1016/0003-2697(89)90213-3. View

11.

Gill S, von Hippel P . Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem. 1989; 182(2):319-26. DOI: 10.1016/0003-2697(89)90602-7. View

12.

MacArthur M, Thornton J . Influence of proline residues on protein conformation. J Mol Biol. 1991; 218(2):397-412. DOI: 10.1016/0022-2836(91)90721-h. View

13.

Dukor R, Keiderling T . Reassessment of the random coil conformation: vibrational CD study of proline oligopeptides and related polypeptides. Biopolymers. 1991; 31(14):1747-61. DOI: 10.1002/bip.360311409. View

14.

Blaber M, Zhang X, Lindstrom J, Pepiot S, Baase W, Matthews B . Determination of alpha-helix propensity within the context of a folded protein. Sites 44 and 131 in bacteriophage T4 lysozyme. J Mol Biol. 1994; 235(2):600-24. DOI: 10.1006/jmbi.1994.1016. View

15.

Wittekind M, Mapelli C, Farmer 2nd B, Suen K, Goldfarb V, Tsao J . Orientation of peptide fragments from Sos proteins bound to the N-terminal SH3 domain of Grb2 determined by NMR spectroscopy. Biochemistry. 1994; 33(46):13531-9. DOI: 10.1021/bi00250a004. View

16.

Lim W, Richards F, Fox R . Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature. 1994; 372(6504):375-9. DOI: 10.1038/372375a0. View

17.

Lee K, Xie D, Freire E, Amzel L . Estimation of changes in side chain configurational entropy in binding and folding: general methods and application to helix formation. Proteins. 1994; 20(1):68-84. DOI: 10.1002/prot.340200108. View

18.

Gomez J, Freire E . Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin. J Mol Biol. 1995; 252(3):337-50. DOI: 10.1006/jmbi.1995.0501. View

19.

DAquino J, Gomez J, Hilser V, Lee K, Amzel L, Freire E . The magnitude of the backbone conformational entropy change in protein folding. Proteins. 1996; 25(2):143-56. DOI: 10.1002/(SICI)1097-0134(199606)25:2<143::AID-PROT1>3.0.CO;2-J. View

20.

Wilson G, Hecht L, Barron L . Residual structure in unfolded proteins revealed by Raman optical activity. Biochemistry. 1996; 35(38):12518-25. DOI: 10.1021/bi961314v. View