Disorder and order in unfolded and disordered peptides and proteins: A view derived from tripeptide conformational analysis. II. Tripeptides with short side chains populating asx and β-type like turn conformations

Proteins: Structure, Function and Bioinformatics

Volumn 81, Issue 6, 2013, Pages 968-983

  Rybka, Karin ^a   Toal, Siobhan E ^b   Verbaro, Daniel J ^b   Mathieu, Daniel ^a   Schwalbe, Harald ^a   Schweitzer Stenner, Reinhard ^b  

^a GOETHE UNIVERSITY   (Germany)

^b DREXEL UNIVERSITY   (United States)

Author keywords

Conformational distributions; J coupling constants; Tripeptides; Turn conformations; Unfolded state of proteins and peptides; Vibrational and NMR spectroscopy

Indexed keywords

ASPARTIC ACID; TRIPEPTIDE;

ARTICLE; ENTHALPY; ENTROPY; HYDROGEN BOND; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON TRANSPORT; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

MOLECULAR CONFORMATION; OLIGOPEPTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; THERMODYNAMICS;

EID: 84878156947     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24226     Document Type: Article

References (66)

1. Dyson HJ, Wright PE. Peptide conformation and protein folding. Curr Opin Struct Biol 1993; 3: 60-65.
2. Dyson HJ, Wright PE. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv Protein Chem 2002; 62: 311-340.
3. Dyson HJ, Rance M, Houghten RA, Lerner RA, Wright PE. Folding of immunogenic peptide fragments of proteins in water solution. I. Sequence requirements for the formation of a reverse turn. J Mol Biol 1988; 201: 161-200.
4. Dyson HJ, Wright PE. Defining solution conformations of small linear peptides. Annu Rev Biophys Biophys Chem 1991; 20: 519-538.
5. Kriwacki RW, Hengst L, Tennant L, Reed SI, Wright PE. Structural studies of p21Waf1/Cip1Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc Natl Acad Sci USA 1996; 123: 6142.
6. Alexandrescu AT, Abeygunawardana C, Shortle D. Structure and dynamics of a denaturared 131-residue fragment of staphylococcal nuclease: a heteronuclear NMR Study. Biochemistry 1994; 33: 1063-1072.
7. Dill KA, Shortle D. Denatured state of proteins. Annu Rev Biochem 1991; 60: 795-825.
8. Bernado P, Mylonas E, Petoukhov MV, Blackledge M, Svergun DI. Structural characterization of flexible proteins using small-angle x-ray scattering. J Am Chem Soc 2007; 129: 5656-5664.
9. Bernado P, Bertoncini CW, Griesinger C, Zweckstetter M, Blackledge M. Defining long-range order and local disorder in native a-synuclein using residua dipolar couplings. J Am Chem Soc 2005; 127: 17968-17969.
10. Shi Z, Woody RW, Kallenbach NR. Is polyproline II a major backbone conformation in unfolded proteins? Adv Protein Chem 2002; 62: 163-240.
11. Duddy WJ, Nissink JMM, Allen FH, Milner-White EJ. Mimicry by asx and ST-turns of the four main types of β-turn in proteins. Prot Sci 2004; 13: 3051-3055.
12. Wright PE, Dyson HJ, Lerner RA. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. Biochemistry 1988; 27: 7167-7175.
13. Ohnishi S, Lee AL, Egdell MH, Shortle D. Direct demonstration of structural similarity between native and denatured Eglin C. Biochemistry 2004; 43: 4064-4070.
14. Shortle D. The expanded denaturated state: an ensemble of conformations trapped in a locally encoded topological space. Adv Protein Chem 2002; 62: 1-23.
15. Bernado P, Blanchard L, Timminis P, Marion D, Rugrok RWH, Blackledge M. A structural model for unfolded proteins from dipolar couplings and small-angle x-ray scattering. Proc Natl Acad Sci USA 2005; 102: 17002-17007.
16. Logan TM, Thériault Y, Fesik SW. Structural characterization of the FK506 binding protein unfolded in urea and guanidine hydrochloride. J Mol Biol 1994; 236: 637-684.
17. Pan H, Barbar E, Barany G, Woodward C. Extensive nonrandom structure in reduced and unfolded bovine pancreatic trypsin inhibitor. Biochemistry 1995; 34: 13974-13981.
18. Mukrasch MD, Markwick P, Biernat J, von Bergen M, Bernado P, Greisinger C, Mandelkow E, Zweckstetter M, Blackledge M. Highly populated turn conformations in natively unfolded tau protein identified from residual dipolar couplings and molecular simulation. J Am Chem Soc 2007; 129: 5235-5243.
19. Bystroff C, Baker D. Prediction of local structure in proteins using a library of sequence-structure motifs. J Mol Biol 1998; 281: 565-577.
20. Brahmachari SK, Rajendra SB, Ananthanaryanan VS. Proline-containing β-turns in peptides and protein. II. Physicochemical studies on tripeptides with the pro-Gly sequence. Biopolymers 1982; 21: 1107.
21. Bashford D, Case DA, Choi C, Gippert GP. A computational study of the role of solvation effects in reverse turn formation in the tetrapeptides APGD and APGN. J Am Chem Soc 1997; 119: 4964-4971.
22. Kakinoki S, Hirano Y, Oka M. On the stability of polyproline I and II structures of proline oligopeptides. Polymer Bull 2005; 53: 109-115.
23. Oka M, Montelione GT, Scheraga HA. Chain-folding initiation structures in ribonuclease a: conformational free energy calculations on Ac-Asn-Pro-tyr-NHMe, Ac-Tyr-Pro-Asn-NHMe, and related peptides. J Am Chem Soc 1984; 106: 7959-7969.
24. Haque TS, Gellman SH. Insights on β-hairpin stability in aqueous solution from peptides with enforced type I' and type II' β-turns. J Am Chem Soc 1997; 119: 2303-2304.
25. Chandrasekhar K, Profy AT, Dyson HJ. Solution conformational preferences of immunogenic peptides derived from the principal neutralizing determinant of the HIV-1 envelope glycoprotein gp 120. Biochemistry 1991; 30:9187-9194.
26. Mcharfi M, Aubry A, boussard G, Marrand M. Backbone side-cahin interactions in petides. IV. β-turn conformations of Asp and Asn-containing dipeptides in solute and solid states. Eur Biophys J 1986; 14: 43-51.
27. Song B, Kibler P, Malde A, Kodukula K, Galande AK. Design of short linear peptides that show hydrogen bonding constraints in water. J Am Chem Soc 2010; 132: 4508-4509.
28. Hagarman A, Mathieu D, Toal S, Measey TJ, Schwalbe H, Schweitzer-Stenner R. Amino acids with hydrogen-bonding side chains have an intrinsic propensity to sample various turn conformations in aqueous solution. Chem Eur J 2011; 17: 6789-6797.
29. Duitch L, Toal S, Measey TJ, Schweitzer-Stenner R. Triaspartate: a model system for conformationally flexible ddd motifs in proteins. J Phys Chem B 2012; 116: 5160-5171.
30. Schweitzer-Stenner R, Hagarman A, Toal SE, Mathieu D, Schwalbe H. Disorder and order in unfolded peptides and proteins: a view derived from tripeptide conformational analysis, submitted for publication.
31. 1 torsion angle preferences. J Mol Biol 1998; 180: 867-877.
32. 15N NMR spectroscopy. J Mol Biol 1999; 288: 705-723.
33. Hähnke MJ, Richter C, Heinicke F, Schwalbe H. THe NH(COCA)HAHB NMR experiment for the stereospecific assignment of hβ-protons in non-native states of proteins. J Am Chem Soc 2010; 132: 918-919.
34. Meier S, Grzesiek S, Blackledge M. Mapping the conformational landscape of urea-denaturated ubiquitin using residual dipolar couplings. J Am Chem Soc 2007; 129: 9799-9807.
35. Sziegat F, Silvers R, Hähnke MJ, Jensen MR, Blackledge M, Wirmer-Bartoschek J, Schwalbe H. Disentangling the coil: modulation of conformationa and dynamic properties by site-directed mutation in the non-native state of hen egg white lysozyme. Biochemistry 2012; 51: 3361-3372.
36. Glasoe PK, Long FA. Use of glass electrodes to measure acidities in deuterium oxide. J Phys Chem 1960; 64: 188-190.
37. Jentzen W, Unger E, Karvounis G, Shelnutt JA, Dreybrodt W, Schweitzer-Stenner R. Conformational properties of nickel(II) octaethylporphyrin in solution. I. Resonance excitation profiles and temperature dependence of structure-sensitive Raman lines. J Phys Chem 1995; 100: 14184-14191.
38. Toal S, Omidi A, Schweitzer-Stenner R. Conformational changes of trialanine induced by direct interactions between alanine residues and alcohols in binary mixtures of water with glycerol and ethanol. J Am Chem Soc 2011; 133: 12728.
39. Schweitzer-Stenner R. Distribution of conformations sampled by the central amino acid residue in tripeptides inferred from amide I band profiles and nmr scalar coupling constants. J Phys Chem B 2009; 113: 2922-2932.
40. Hagarman A, Measey TJ, Mathieu D, Schwalbe H, Schweitzer-Stenner R. Intrinsic propensities of amino acid residues in gxg peptides inferred from amide I band profiles and NMR scalar coupling constants. J Am Chem Soc 2010; 132: 540.
41. Graf J, Nguyen PH, Stock G, Schwalbe H. Structure and dynamics of the homologous series of alanine peptides: a joint molecular dynamics/NMR study. J Am Chem Soc 2007; 129: 1179-1189.
42. Pachler KG. Nuclear magnetic resonance study of some α-amino acids-I coupling constants in alkaline and acidic medium. Spectrochim Acta 1963; 19: 2085-2092.
43. Grdadolnik J, Grdadolnik SG, Avbelj F. Determination of conformational preferences of dipeptides using vibrational spectroscopy. J Phys Chem B 2008; 112: 2712-2718.
44. Grdadolnik J, Mohacek-Grosev V, Baldwin RL, Avbelj F. Populations of the three makor backbone conformations in 19 amino acid dipeptides. Proc Natl Acad Sci USA 2011; 108: 1794-1798.
45. He L, Navarro AE, Shi Z, Kallenbach NR. End effects influence short model peptide conformation. J Am Chem Soc 2011; 134: 1571-1576.
46. Hu H, Elstner M, Hermans J. Comparison of a QM/MM force field and molecular mechanics force fields in simulations of alanine and glycine "dipeptides" (Ace-Ala-NMe and Ace-Gly-Nme) in water in relation to the problem of modeling the unfolded peptide backbone in solution. Proteins 2003; 50: 451-463.
47. Ioannou F, Archontis G, Leontidis E. Specific interactions of sodium salts with alanine dipeptide and tetrapeptide in water: insights from molecular dynamics. J Phys Chem B 2011; 115: 13389-13400.
48. Ishizuka R, Huber GA, McCammon JA. Solvation effect on the conformation of alanine dipeptide: integral equation approach. J Phys Chem Lett 2011; 1: 2279-2283.
49. Kim YS, Wang J, Hochstrasser RM. Two-dimensional infrared spectroscopy of the alanine dipeptide in aqueous solution. J Phys Chem B 2005; 109: 7511-7521.
50. Kwac K, Lee K-K, Han JB, Oh K-I, Cho M. Classical and quantum mechanical/molecular mechanical molecular dynamics simulations of alanine dipeptide in water: comparison with IR and vibrational circular dichroism spectra. J Chem Phys 2008; 128: 105106.
51. Lee O, Roberts GM, Diem M. IR vibrational CD in alanyl tripeptide: indication of a stable solution conformer. Biopolymers 1989; 28: 1759-1770.
52. Choi J-H, Cho M. Amide I vibrational circular dichroism of dipeptide: conformation dependence and fragment analysis. J Chem Phys 2004; 120: 4383-4392.
53. Cruz V, Ramos J, Martinez-Salazar J. Water-mediated conformations of the alanine dipeptide as revealed by distributed umbrella sampling simulations, quantum mechanics based calculations, and experimental data. J Phys Chem B 2011; 115: 4880-4886.
54. Poon CD, Samulsi ET, Weise CF, Weisshaar JC. Do bridging water molecules dictate the structure of a model dipeptide in aqueous solution? J Am Chem Soc 2000; 122: 5612-5613.
55. Ramachandran GN, Ramachandran C, Sasisekharan V. Stereochemistry of polypeptide chain configurations. J Mol Biol 1963; 7: 95-99.
56. Brant DA, Flory PJJ. The configuration of random polypeptide chains. II. Theory. J Am Chem Soc 1965; 87: 2791-2800.
57. Toal SE, Verbaro DJ, Meral D, Urbanč B, Schweitzer-Stenner R. The pH-independence of trialanine and the effects of termini blocking in short peptides: a combined vibrational, NMR, UVCD, and molecular dynamics study, submitted for publication.
58. Measey T, Hagarman A, Eker F, Griebenow K, Schweitzer-Stenner R. Side chain dependence of intensity and wavenumber position of amide I' in IR and visible Raman spectra of XA and AX dipeptides. J Phys Chem B 2005; 109: 8195-8205.
59. Chakrabati P, Pal D. The inter-relationship of side-chain and main-chain conformations in proteins. Prog Biophys Mol Biol 2001; 76: 1-102.
60. 3J couplings. J Biomol NMR 2007; 37: 287-301.
61. Eker F, Griebenow K, Schweitzer-Stenner R. Stable conformations of tripeptides in aqueous solution studied by UV circular dichroism spectroscopy. J Am Chem Soc 2003; 125: 8178-8185.
62. Shi Z, Olson CA, Rose GD, Baldwin RL, Kallenbach NR. Polyproline II structure in a sequence of seven alanine residues. Proc Natl Acad Sci USA 2002; 99: 9190-9195.
63. Chen K, Liu Z, Zhou C, Shi Z, Kallenbach NR. Neighbor effect on PPII conformation in alanine peptides. J AM Chem Soc 2005; 127: 10146-10147.
64. Chen K, Liu ZG, Kallenbach NR. The polyproline II conformation in short alanine peptides is noncooperative. Proc Natl Acad Sci USA 2004; 101: 15352-15357.
65. Yang WY, Larios E, Gruebele M. On the extended β-conformation of polypeptides at high temperatures. J Am Chem Soc 2003; 125: 16220-16227.
66. Kaur H, Sasidhar YU. For the SEQUENCE YKGQ, the turn and extended conformational forms are separated by small barriers and the turn propensity persists even at high temperatures: implications for protein folding. J Phys Chem B 2012; 116: 3850-3860.