Sequence determinants of thermodynamic stability in a WW domain - An all-β-sheet protein

Protein Science

Volumn 18, Issue 8, 2009, Pages 1806-1813

  Jäger, Marcus ^a,b   Dendle, Maria ^a   Kelly, Jeffery W ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ala scanning; Beta sheet; Gly scanning; Protein folding; Protein stability; Side chain mutagenesis; WW domain

Indexed keywords

ALANINE; PEPTIDYLPROLYL ISOMERASE PIN1;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; HUMAN; HYDROPHOBICITY; LIGAND BINDING; MUTATION; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; HUMANS; MUTATION; PEPTIDYLPROLYL ISOMERASE; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 67749090874     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.172     Document Type: Article

References (52)

1. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223-230.
2. Heinz DW, Baase WA, Matthews BW (1992) Folding and function of a T4 lysozyme containing 10 consecutive alanines illustrate the redundancy of information in an amino acid sequence. Proc Natl Acad Sci USA 89:3751-3755.
3. Cunningham BC, Wells JA (1989) High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244:1081-1085.
4. Kuroda Y, Kim PS (2000) Folding of bovine pancreatic trypsin inhibitor (BPTI) variants in which almost half the residues are alanine. J Mol Biol 298:493-501.
5. Matthews BW (1995) Studies on protein stability with T4 lysozyme. Adv Protein Chem 46:249-278.
6. Deechongkit S, Nguyen H, Powers ET, Dawson PE, Gruebele M, Kelly JW (2004) Context-dependent contributions of backbone hydrogen bonding to beta-sheet folding energetics. Nature 430:101-105.
7. Jager M, Nguyen H, Crane JC, Kelly JW, Gruebele M (2001) The folding mechanism of a beta-sheet: the WW domain. J Mol Biol 311:373-393.
8. Powers ET, Deechongkit S, Kelly JW (2006) Backbone-backbone H-bonds make context-dependent contributions to protein folding kinetics and thermodynamics: lessons from amide-to-ester mutations. Adv Protein Chem 72:39-78.
9. Nguyen H, Jager M, Moretto A, Gruebele M, Kelly JW (2003) Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation. Proc Natl Acad Sci USA 100:3948-3953.
10. 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.
11. Sauer RT, Milla ME, Waldburger CD, Brown BM, Schildbach JF (1996) Sequence determinants of folding and stability for the P22 Arc repressor dimer. FASEB J 10:42-48.
12. Milla ME, Brown BM, Sauer RT (1994) Protein stability effects of a complete set of alanine substitutions in Arc repressor. Nat Struct Biol 1:518-523.
13. Yu MH, Weissman JS, Kim PS (1995) Contribution of individual side-chains to the stability of BPTI examined by alanine-scanning mutagenesis. J Mol Biol 249:388-397.
14. Deechongkit S, Nguyen H, Jager M, Powers ET, Gruebele M, Kelly JW (2006) Beta-sheet folding mechanisms from perturbation energetics. Curr Opin Struct Biol 16:94-101.
15. Jager M, Deechongkit S, Koepf EK, Nguyen H, Gao J, Powers ET, Gruebele M, Kelly JW (2008) Understanding the mechanism of beta-sheet folding from a chemical and biological perspective. Biopolymers 90:751-758.
16. Koepf EK, Petrassi HM, Sudol M, Kelly JW (1999) WW: an isolated three-stranded antiparallel beta-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.
17. Nguyen H, Jager M, Kelly JW, Gruebele M (2005) Engineering a beta-sheet protein toward the folding speed limit. J Phys Chem B 109:15182-15186.
18. Ferguson N, Johnson CM, Macias M, Oschkinat H, Fersht A (2001) Ultrafast folding of WW domains without structured aromatic clusters in the denatured state. Proc Natl Acad Sci USA 98:13002-13007.
19. 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.
20. Liu F, Du D, Fuller AA, Davoren JE, Wipf P, Kelly JW, Gruebele M (2008) An experimental survey of the transition between two-state and downhill protein folding scenarios. Proc Natl Acad Sci USA 105:2369-2374.
21. Kuznetsov SV, Hilario J, Keiderling TA, Ansari A (2003) Spectroscopic studies of structural changes in two beta-sheet-forming peptides show an ensemble of structures that unfold noncooperatively. Biochemistry 42:4321-4332.
22. Syud FA, Stanger HE, Mortell HS, Espinosa JF, Fisk JD, Fry CG, Gellman SH (2003) Influence of strand number on antiparallel beta-sheet stability in designed three- and four-stranded beta-sheets. J Mol Biol 326:553-568.
23. Stanger HE, Syud FA, Espinosa JF, Giriat I, Muir T, Gellman SH (2001) Length-dependent stability and strand length limits in antiparallel beta-sheet secondary structure. Proc Natl Acad Sci USA 98:12015-12020.
24. Kortemme T, Ramirez-Alvarado M, Serrano L (1998) Design of a 20-amino acid, three-stranded beta-sheet protein. Science 281:253-256.
25. Deechongkit S, Kelly JW (2002) The effect of backbone cyclization on the thermodynamics of beta-sheet unfolding: stability optimization of the PIN WW domain. J Am Chem Soc 124:4980-4986.
26. Kaul R, Angeles AR, Jager M, Powers ET, Kelly JW (2001) Incorporating beta-turns and a turn mimetic out of context in loop 1 of the WW domain affords cooperatively folded beta-sheets. J Am Chem Soc 123:5206-5212.
27. Deechongkit S, Dawson PE, Kelly JW (2004) Toward assessing the position-dependent contributions of backbone hydrogen bonding to beta-sheet folding thermodynamics employing amide-to-ester perturbations. J Am Chem Soc 126:16762-16771.
28. Deechongkit S, You SL, Kelly JW (2004) Synthesis of all nineteen appropriately protected chiral alpha-hydroxy acid equivalents of the alpha-amino acids for Boc solid-phase depsi-peptide synthesis. Org Lett 6:497-500.
29. Crane JC, Koepf EK, Kelly JW, Gruebele M (2000) Mapping the transition state of the WW domain beta-sheet. J Mol Biol 298:283-292.
30. Macias MJ, Hyvonen M, Baraldi E, Schultz J, Sudol M, Saraste M, Oschkinat H (1996) Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature 382:646-649.
31. Jager M, Zhang Y, Bieschke J, Nguyen H, Dendle M, Bowman ME, Noel JP, Gruebele M, Kelly JW (2006) Structure-function-folding relationship in a WW domain. Proc Natl Acad Sci USA 103:10648-10653.
32. Jager 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.
33. Jager M, Dendle M, Fuller AA, Kelly JW (2007) A crossstrand Trp Trp pair stabilizes the hPin1 WW domain at the expense of function. Protein Sci 16:2306-2313.
34. Macias MJ, Gervais V, Civera C, Oschkinat H (2000) Structural analysis of WW domains and design of a WW prototype. Nat Struct Biol 7:375-379.
35. Myers JK, Morris DP, Greenleaf AL, Oas TG (2001) Phosphorylation of RNA polymerase II CTD fragments results in tight binding to the WW domain from the yeast prolyl isomerase Ess1. Biochemistry 40:8479-8486.
36. 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.
37. Sharpe T, Jonsson AL, Rutherford TJ, Daggett V, Fersht AR (2007) The role of the turn in beta-hairpin formation during WW domain folding. Protein Sci 16:2233-2239.
38. Peng T, Zintsmaster JS, Namanja AT, Peng JW (2007) Sequence-specific dynamics modulate recognition specificity in WW domains. Nat Struct Mol Biol 14:325-331.
39. Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol 7:639-643.
40. Lubs H, Abidi FE, Echeverri R, Holloway L, Meindl A, Stevenson RE, Schwartz CE (2006) Golabi-Ito-Hall syndrome results from a missense mutation in the WW domain of the PQBP1 gene. J Med Genet 43:e30.
41. Petrovich M, Jonsson AL, Ferguson N, Daggett V, Fersht AR (2006) Phi-analysis at the experimental limits: mechanism of beta-hairpin formation. J Mol Biol 360:865-881.
42. Socolich M, Lockless SW, Russ WP, Lee H, Gardner KH, Ranganathan R (2005) Evolutionary information for specifying a protein fold. Nature 437:512-518.
43. Russ WP, Lowery DM, Mishra P, Yaffe MB, Ranganathan R (2005) Natural-like function in artificial WW domains. Nature 437:579-583.
44. Sudol M, The WW domain. In: Cesareni G, Ed. (2005) Modular protein domains. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA, pp 59-72.
45. Koepf EK, Petrassi HM, Ratnaswamy G, Huff ME, Sudol M, Kelly JW (1999) Characterization of the structure and function of W -> F WW domain variants: identification of a natively unfolded protein that folds upon ligand binding. Biochemistry 38:14338-14351.
46. Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol 7:639-643.
47. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319:916-919.
48. Brown BM, Sauer RT (1999) Tolerance of Arc repressor to multiple-alanine substitutions. Proc Natl Acad Sci USA 96:1983-1988.
49. Schafmeister CE, LaPorte SL, Miercke LJ, Stroud RM (1997) A designed four helix bundle protein with native-like structure. Nat Struct Biol 4:1039-1046.
50. Riddle DS, Santiago JV, Bray-Hall ST, Doshi N, Grantcharova VP, Yi Q, Baker D (1997) Functional rapidly folding proteins from simplified amino acid sequences. Nat Struct Biol 4:805-809.
51. Gaspar C, Jannatipour M, Dion P, Laganiere J, Sequeiros J, Brais B, Rouleau GA (2000) CAG tract of MJD-1 may be prone to frameshifts causing polyalanine accumulation. Hum Mol Genet 9:1957-1966.
52. Gautam AM, Pearson CI, Smilek DE, Steinman L, McDevitt HO (1992) A polyalanine peptide with only five native myelin basic protein residues induces autoimmune encephalomyelitis. J Exp Med 176:605-609.