Evaluating β-turn mimics as β-sheet folding nucleators

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

Volumn 106, Issue 27, 2009, Pages 11067-11072

  Fuller, Amelia A ^a   Du, Deguo ^a   Liu, Feng ^b   Davoren, Jennifer E ^c   Bhabha, Gira ^a   Kroon, Gerard ^a   Case, David A ^d   Dyson, H Jane ^a   Powers, Evan T ^a   Wipf, Peter ^c   Gruebele, Martin ^b   Kelly, Jeffery W ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

Beta sheet nucleator; Kinetic assessment of turn mimics; Pin WW domain; Protein folding

Indexed keywords

ALKENE; ALPHA AMINO ACID;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE; SIMULATION;

AMINO ACID SEQUENCE; HUMANS; KINETICS; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PEPTIDYLPROLYL ISOMERASE; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS; THERMODYNAMICS;

EID: 67650468079     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0813012106     Document Type: Article

References (51)

1. Rose GD, Gierasch LM, Smith JA (1985) Turns in peptides and proteins. Adv Protein Chem 37:1-109.
2. Rotondi KS, Gierasch LM (2006) Natural polypeptide scaffolds: β-sheets, β-turns, and β-hairpins. Biopolymers 84:13-22.
3. Grantcharova VP, Riddle DS, Santiago JV, Baker D (1998) Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat Struct Mol Biol 5:714-720.
4. Jäger M, Nguyen H, Crane JC, Kelly JW, Gruebele M (2001) The folding mechanism of a β-sheet: The WW domain. J Mol Biol 311:373-373.
5. Marcelino AMC, Gierasch LM (2008) Roles of β-turns in protein folding: From peptide models to protein engineering. Biopolymers 89:380-391.
6. Martinez JC, Pisabarro MT, Serrano L (1998) Obligatory steps in protein folding and the conformational diversity of the transition state. Nat Struct Biol 5:721-729.
7. Matouschek A, Kellis JT, Jr, Serrano L, Fersht AR (1989) Mapping the transition state and pathway of protein folding by protein engineering. Nature 340:122-126.
8. Nguyen H, Jäger M, Kelly JW, Gruebele M (2005) Engineering β-sheet protein toward the folding speed limit. J Phys Chem B 109:15182-15186.
9. Petrovich M, Jonsson AL, Ferguson N, Daggett V, Fersht AR (2006) -analysis at the experimental limits: mechanism of β-hairpin formation. J Mol Biol 360:865-881.
10. Sharpe T, Jonsson AL, Rutherford TJ, Daggett V, Fersht AR (2007) The role of the turn in β-hairpin formation during WW domain folding. Protein Sci 16:2233-2239.
11. Sibanda BL, Blundell TL, Thornton JM (1989) Conformation of β-hairpins in protein structures. A systematic classification with applications to modelling by homology, electron density fitting and protein engineering. J Mol Biol 206:759-777.
12. Sibanda BL, Thornton JM (1985) β-Hairpin families in globular proteins. Nature 316:170-174.
13. Venkatachalam CM (1968) Stereochemical criteria for polypeptides and proteins. V. Conformation of a system of three linked peptide units. Biopolymers 6:1425-1436.
14. Richardson JS, Getzoff ED, Richardson DC (1978) The βbulge: A common small unit of nonrepetitive protein structure. Proc Natl Acad Sci USA 75:2574-2578.
15. Oishi S, et al. (2006) Application of tri- and tetrasubstituted alkene dipeptide mimetics to conformational studies of cyclic RGD peptides. Tetrahedron 62:1416-1424.
16. Chung YJ, Christianson LA, Stanger HE, Powell DR, Gellman SH (1998) A β-peptide reverse turn that promotes hairpin formation. J Am Chem Soc 120:10555-10556.
17. Chung YJ, et al. (2000) Stereochemical control of hairpin formation in β-peptides containing dinipecotic acid reverse turn segments. J Am Chem Soc 122:3995-4004.
18. Diaz H, Espina JR, Kelly JW (1992) A dibenzofuran-based amino acid designed to nucleate antiparallel β-sheet structure: Evidence for intramolecular hydrogen bond formation. J Am Chem Soc 114:8316-8318.
19. Diaz H, Tsang KY, Choo D, Espina JR, Kelly JW (1993) Design, synthesis, and partial characterization of water-soluble β-sheets stabilized by a dibenzofuran-based amino acid. J Am Chem Soc 115:3790-3791.
20. Gardner RR, Liang GB, Gellman SH (1999) β-Turn and β-hairpin mimicry with tetrasubstituted alkenes. J Am Chem Soc 121:1806-1816.
21. Nagai U, Sato K (1985) Synthesis of a bicyclic dipeptide with the shape of β-turn central part. Tetrahedron Lett 26:647-650.
22. Schneider JP, Kelly JW (1995) Templates that induce α-helical, β-sheet, and loop conformations. Chem Rev 95:2169-2187.
23. Souers AJ, Ellman JA (2001) β-Turn mimetic library synthesis: Scaffolds and applications. Tetrahedron 57:7431-7448.
24. Tsang KY, Diaz H, Graciani N, Kelly JW (1994) Hydrophobic cluster formation is necessary for dibenzofuran-based amino acids to function as β-sheet nucleators. J Am Chem Soc 116:3988-4005.
25. Wipf P, Henninger TC, Geib SJ (1998) Methyl- and (trifluoromethyl)alkene peptide isosteres: Synthesis and evaluation of their potential as β-turn promoters and peptide mimetics. J Org Chem 63:6088-6089.
26. Nesloney CN, Kelly JW (1996) Progress towards understanding β-sheet structure. Bioorg Med Chem 4:739-766.
27. Koepf EK, et al. (1999) Characterization of the structure and function of W 3 F WW domain variants: Identification of a natively unfolded protein that folds upon ligand binding. Biochemistry 38:14338-14351.
28. Koepf EK, Petrassi HM, Sudol M, Kelly JW (1999) WW: An isolated three-stranded antiparallel β-sheet domain that unfolds and refolds reversibly; evidence for a structured hydrophobic cluster in urea and GdnHCl and a disordered thermal unfolded state. Protein Sci 8:841-853.
29. Crane JC, Koepf EK, Kelly JW, Gruebele M (2000) Mapping the transition state of the WW domain β-sheet. J Mol Biol 298:283-292.
30. Deechongkit S, et al. (2004) Context-dependent contributions of backbone hydrogen bonding to β-sheet folding energetics. Nature 430:101-105.
31. Jäger M, Nguyen H, Dendle M, Gruebele M, Kelly JW (2007) Influence of hPin1 WW N-terminal domain boundaries on function, protein stability, and folding. Protein Sci 16:1495-1501.
32. Jäger M, et al. (2006) Structure-function-folding relationship in a WW domain. Proc Natl Acad Sci USA 103:10648-10653.
33. Jiang X, Kowalski J, Kelly JW (2001) Increasing protein stability using a rational approach combining sequence homology and structural alignment: Stabilizing the WW domain. Protein Sci 10:1454-1465.
34. Kaul R, Angeles AR, Jä ger M, Powers ET, Kelly JW (2001) Incorporating β-turns and a turn mimetic out of context in loop 1 of theWWdomain affords cooperatively folded β-sheets. J Am Chem Soc 123:5206-5212.
35. Nguyen H, Jäger M, Moretto A, Gruebele M, Kelly JW (2003) Tuning the free-energy landscape of aWWdomain by temperature, mutation, and truncation. Proc Natl Acad Sci USA 100:3948-3953.
36. Kowalski JA, Liu K, Kelly JW (2002) NMR solution structure of the isolated Apo Pin1 WW domain: comparison to the x-ray crystal structures of Pin1. Biopolymers 63:111-121.
37. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89:875-886.
38. Liu F, et al. (2008) An experimental survey of the transition between two-state and downhill protein folding scenarios. Proc Natl Acad Sci USA 105:2369-2374.
39. Eliel EL, Wilen SH (1994) Stereochemistry of Organic Compounds (Wiley-Interscience, New York).
40. Baca M, Alewood PF, Kent SBH (1993) Structural-Engineering of the HIV-1 Protease Molecule with a β-Turn Mimic of Fixed Geometry. Protein Sci 2:1085-1091.
41. Viles JH, et al. (1998) Design, synthesis and structure of a zinc finger with an artificial β-turn. J Mol Biol 279:973-986.
42. Choo DW, Schneider JP, Graciani NR, Kelly JW (1996) Nucleated antiparallel β-sheet that folds and undergoes self-assembly:Atemplate promoted folding strategy toward controlled molecular architectures. Macromolecules 29:355-366.
43. Kaul R, Deechongkit S, KellyJW(2002) Synthesis of a negatively charged dibenzofuranbased β-turn mimetic and its incorporation into the WW miniprotein-enhanced solubility without a loss of thermodynamic stability. J Am Chem Soc 124:11900-11907.
44. Arnold U, et al. (2002) Protein prosthesis: A semisynthetic enzyme with a β-peptide reverse turn. J Am Chem Soc 124:8522-8523.
45. Yang WY, Gruebele M (2004) Folding lambda-repressor at its speed limit. Biophys J 87:596-608.
46. Naganathan AN, Doshi U, Munoz V (2007) Protein folding kinetics: Barrier effects in chemical and thermal denaturation experiments. J Am Chem Soc 129:5673-5682.
47. Bach AC, II, Markwalder JA, Ripka WC (1991) Synthesis and NMR conformational analysis of a β-turn mimic incorporated into gramicidin S. A general approach to evaluate β-turn peptidomimetics. Int J Pept Prot Res 38:314-323.
48. Fu Y, Gao J, Bieschke J, Dendle MA, Kelly JW (2006) Amide-to-E-olefin versus amideto-ester backbone H-bond perturbations: Evaluating the O-O repulsion for extracting H-bond energies. J Am Chem Soc 128:15948-15949.
49. Case DA, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26:1668-1688.
50. Pace CN, et al. (2001) Tyrosine hydrogen bonds make a large contribution to protein stability. J Mol Biol 312:393-404.
51. Ervin J, Sabelko J, GruebeleM(2000) Submicrosecond real-time fluorescence sampling: application to protein folding. J Photochem Photobio B 54:1-15.