Redesign of a WW domain peptide for selective recognition of single-stranded DNA

Biochemistry

Volumn 50, Issue 13, 2011, Pages 2575-2584

  Stewart, Amanda L ^a   Park, Jessica H ^a   Waters, Marcey L ^a  

^a University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUPLEX DNA; POLYPROLINE HELIXES; PROTEIN-DNA INTERACTIONS; SELECTIVE RECOGNITION; SINGLE-STRANDED DNA; STRUCTURAL STUDIES; WW DOMAIN;

DIMERS; DNA; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; NUCLEIC ACIDS;

PEPTIDES;

DOUBLE STRANDED DNA; POLYPROLINE; PROLINE DERIVATIVE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA HAIRPIN; DNA STRUCTURE; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN;

CARRIER PROTEINS; CIRCULAR DICHROISM; DIMERIZATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; FLUORESCENCE POLARIZATION; HUMANS; KINETICS; LIGANDS; MUTANT PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PEPTIDES; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN REFOLDING; PROTEIN STABILITY; TEMPERATURE;

EID: 79953225853     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101116a     Document Type: Article

References (62)

1. Bochkarev, A., Pfuetzner, R. A., Edwards, A. M., and Frappier, L. (1997) Structure of the single-stranded-DNA-binding domain of replication protein A bound to DNA Nature 385, 176-181 (Pubitemid 27034221)
2. Wold, M. S. (1997) Replication protein A: A heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism Annu. Rev. Biochem. 66, 61-92 (Pubitemid 27274652)
3. Theobald, D. L., Mitton-Fry, R. M., and Wuttke, D. S. (2003) Nucleic acid recognition by OB-fold proteins Annu. Rev. Biophys. Biomol. Struct. 32, 115-133 (Pubitemid 37056224)
4. Bochkarev, A. and Bochkareva, E. (2004) From RPA to BRCA2: Lessons from single-stranded DNA binding by the OB-fold Curr. Opin. Struct. Biol. 14, 36-42 (Pubitemid 38249590)
5. Anderson, E. M., Halsey, W. A., and Wuttke, D. S. (2003) Site-directed mutagenesis reveals the thermodynamic requirements for single-stranded DNA recognition by the telomere-binding protein Cdc13 Biochemistry 42, 3751-3758 (Pubitemid 36402668)
6. Mitton-Fry, R. M., Anderson, E. M., Hughes, T. R., Lundblad, V., and Wuttke, D. S. (2002) Conserved structure for single-stranded telomeric DNA recognition Science 296, 145-147 (Pubitemid 34280074)
7. Max, K. E. A., Zeeb, M., Bienert, R., Balbach, J., and Heinemann, U. (2007) Common mode of DNA binding to cold shock domains: Crystal structure of hexathymidine bound to the domain-swapped form of a major cold shock protein from Bacillus caldolyticus FEBS J. 274, 1265-1279
8. Max, K. E. A., Zeeb, M., Bienert, R., Balbach, J., and Heinemann, U. (2006) T-rich DNA single strands bind to a preformed site on the bacterial cold shock protein Bs -CspB J. Mol. Biol. 360, 702-714 (Pubitemid 43975118)
9. Hillier, B. J., Rodriguez, H. M., and Gregoret, L. M. (1998) Coupling protein stability and protein function in Escherichia coli CspA Folding Des. 3, 87-93 (Pubitemid 28166180)
10. Newkirk, K., Feng, W., Jiang, W., Tejero, R., Emerson, S. D., Inouye, M., and Montelione, G. T. (1994) Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: Identification of a binding epitope for DNA Proc. Natl. Acad. Sci. U.S.A. 91, 5114-5118 (Pubitemid 24177803)
11. Schindelin, H., Marahiel, M. A., and Heinemann, U. (1993) Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein Nature 364, 164-168 (Pubitemid 23238202)
12. Schnuchel, A., Wiltscheck, R., Czisch, M., Herrier, M., Willimsky, G., Graumann, P., Marahiel, M. A., and Holak, T. A. (1993) Structure in solution of the major cold-shock protein from Bacillus subtilis Nature 364, 169-171 (Pubitemid 23238203)
13. Butterfield, S. M., Cooper, W. J., and Waters, M. L. (2005) Minimalist protein design: A beta-hairpin peptide that binds ssDNA J. Am. Chem. Soc. 127, 24-25 (Pubitemid 40094346)
14. Butterfield, S. M. and Waters, M. L. (2003) A designed beta-hairpin peptide for molecular recognition of ATP in water J. Am. Chem. Soc. 125, 9580-9581 (Pubitemid 36975908)
15. Butterfield, S. M., Sweeney, M. M., and Waters, M. L. (2005) The recognition of nucleotides with model beta-hairpin receptors: Investigation of critical contacts and nucleotide selectivity J. Org. Chem. 70, 1105-1114 (Pubitemid 40261347)
16. Stewart, A. L. and Waters, M. L. (2009) Structural effects on ss- and dsDNA recognition by a beta-hairpin peptide ChemBioChem 10, 539-544
17. Jager, M., Zhang, Y., Bieschke, J., Nguyen, H., Dendle, M., Bowman, M. E., Noel, J. P., Gruebele, M., and Kelly, J. W. (2006) Structure-function- folding relationship in a WW domain Proc. Natl. Acad. Sci. U.S.A. 103, 10648-10653 (Pubitemid 44078031)
18. Fernandez-Escamilla, A. M., Ventura, S., Serrano, L., and Jimenez, M. A. (2006) Design and NMR conformational study of a β-sheet peptide based on Betanova and WW domains Protein Sci. 15, 2278-2289 (Pubitemid 44496382)
19. Karanicolas, J. and Brooks, C. L. (2003) The structural basis for biphasic kinetics in the folding of the WW domain from a formin-binding protein: Lessons for protein design? Proc. Natl. Acad. Sci. U.S.A. 100, 3954-3959 (Pubitemid 36418138)
20. Kraemer-Pecore, C. M., Lecomte, J. T. J., and Desjarlais, J. R. (2003) A de novo redesign of the WW domain Protein Sci. 12, 2194-2205 (Pubitemid 37163353)
21. Jiang, X., Kowalski, J., and Kelly, J. W. (2001) Increasing protein stability using a rational approach combining sequence homology and structural alignment: Stabilizing the WW domain Protein Sci. 10, 1454-1465 (Pubitemid 32568112)
22. Jager, M., Nguyen, H., Crane, J. C., Kelly, J. W., and Gruebele, M. (2001) The folding mechanism of a β-sheet: The WW domain J. Mol. Biol. 311, 373-393
23. Macias, M. J., Gervais, V., Civera, C., and Oschkinat, H. (2000) Structural analysis of WW domains and design of a WW prototype Nat. Struct. Biol. 7, 375-379 (Pubitemid 30249999)
24. Koepf, E. K., Petrassi, M., Ratnaswamy, G., Huff, M. E., Sudol, M., and Kelly, J. W. (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
25. Nguyen, H., Jager, M., Moretto, A., Gruebele, M., and Kelly, J. W. (2003) Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation Proc. Natl. Acad. Sci. U.S.A. 100, 3948-3953 (Pubitemid 36418137)
26. Jager, M., Dendle, M., Fuller, A. A., and Kelly, J. W. (2007) A cross-strand Trp-Trp pair stabilizes the hPin1 WW domain at the expense of function Protein Sci. 16, 2306-2313 (Pubitemid 47481667)
27. Kato, Y., Miyakawa, T., Kurita, J., and Tanokura, M. (2006) Structure of FBP11 WW1-PL ligand complex reveals the mechanism of proline-rich ligand recognition by group II/III WW domains J. Biol. Chem. 281, 40321-40329 (Pubitemid 46041837)
28. Pires, J. R., Parthier, C., do Aido-Machado, R., Wiedemann, U., Otte, L., Bohm, G., Rudolph, R., and Oschkinat, H. (2005) Structural basis for APPTPPPLPP peptide recognition by the FBP11WW1 domain J. Mol. Biol. 348, 399-408 (Pubitemid 40462104)
29. Ball, L. J., Kuhne, R., Schneider-Mergener, J., and Oschkinat, H. (2005) Recognition of proline-rich motifs by protein-protein-interaction domains Angew. Chem., Int. Ed. 44, 2852-2869 (Pubitemid 40689661)
30. Kato, Y., Nagata, K., Takahashi, M., Lian, L., Herrero, J. J., Sudol, M., and Tanokura, M. (2004) Common mechanism of ligand recognition by group II/III WW domains: Redefining their functional classification J. Biol. Chem. 279, 31833-31841 (Pubitemid 39037856)
31. Bedford, M. T., Chan, D. C., and Leder, P. (1997) FBP WW domains and the Abl SH3 domain bind to a specific class of proline-rich ligands EMBO J. 16, 2376-2383 (Pubitemid 27258637)
32. Otte, L., Wiedemann, U., Schlegel, B., Pires, J. R., Beyermann, M., Schmieder, P., Krause, G., Volkmer-Engert, R., Schneider-Mergener, J., and Oschkinat, H. (2003) WW domain sequence activity relationships identified using ligand recognition propensities of 42 WW domains Protein Sci. 12, 491-500 (Pubitemid 36241107)
33. Zarrinpar, A. and Lim, W. A. (2000) Converging on proline: The mechanism of WW domain peptide recognition Nat. Struct. Biol. 7, 611-613 (Pubitemid 30636665)
34. Espinosa, J. F., Syud, F. A., and Gellman, S. H. (2005) An autonomously folding β-hairpin derived from the human YAP65 WW domain: Attempts to define a minimum ligand-binding motif Peptide Sci. 80, 303-311 (Pubitemid 40791060)
35. Dalby, P. A., Hoess, R. H., and DeGrado, W. F. (2000) Evolution of binding affinity in a WW domain probed by phage display Protein Sci. 9, 2366-2376 (Pubitemid 32105719)
36. Chan, D. C., Bedford, M. T., and Leder, P. (1996) Formin binding proteins bear WWP/WW domains that bind proline-rich peptides and functionally resemble SH3 domains EMBO J. 15, 1045-1054 (Pubitemid 26077833)
37. Macias, M. J., Hyvonen, M., Baraldi, E., Schultz, J., Sudol, M., Saraste, M., and Oschkinat, H. (1996) Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide Nature 382, 646-649 (Pubitemid 26268960)
38. Chen, H. I. and Sudol, M. (1995) The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules Proc. Natl. Acad. Sci. U.S.A. 92, 7819-7823
39. Lim, W. A., Fox, R. O., and Richards, F. M. (1994) Stability and peptide binding affinity of an SH3 domain from the Caenorhabditis elegans signaling protein Sem-5 Protein Sci. 3, 1261-1266 (Pubitemid 24278207)
40. Lohman, T. M. and Mascotti, D. P. (1992) Nonspecific ligand-DNA equilibrium binding parameters determined by fluorescence methods Methods Enzymol. 212, 424-458
41. C.Y. Huang, C Y. (1982) Determination of binding stoichiometry by the continuous variation method: The job plot Methods Enzymol. 87, 509-525
42. Wang, Y., Hamasaki, K., and Rando, R. R. (1997) Specificity of aminoglycoside binding to RNA constructs derived from the 16S rRNA decoding region and the HIV-RRE activator region Biochemistry 36, 768-779 (Pubitemid 27110956)
43. Wuthrich, K. ((1986)) NMR of Proteins and Nucleic Acids, Wiley-Interscience, New York.
44. Syud, F. A., Espinosa, J. F., and Gellman, S. H. (1999) NMR-based quantification of β-sheet populations in aqueous solution through use of reference peptides for the folded and unfolded states J. Am. Chem. Soc. 121, 11577-11578 (Pubitemid 30010494)
45. The amino acid numbering for the mutant peptides is 1-30.
46. Allen, M. D., Yamasaki, K., Ohme-Takagi, M., Tateno, M., and Suzuki, M. (1998) A novel mode of DNA recognition by a β-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA EMBO J. 17, 5484-5496 (Pubitemid 28427062)
47. Ohki, I., Shimotake, N., Fujita, N., Jee, J.-G., Ikegami, T., Nakao, M., and Shirakawa, M. (2001) Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA Cell 105, 487-497 (Pubitemid 32520854)
48. Luscombe, N. M., Laskowski, R. A., and Thornton, J. M. (2001) Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level Nucleic Acids Res. 29, 2860-2874 (Pubitemid 32685051)
49. Moodie, S. L., Mitchell, J. B. O., and Thornton, J. M. (1996) Protein recognition of adenylate: An example of a fuzzy recognition template J. Mol. Biol. 263, 486-500 (Pubitemid 26375531)
50. Cooper, W. J. and Waters, M. L. (2005) Turn residues in beta-hairpin peptides as points for covalent modification Org. Lett. 7, 3825-3828 (Pubitemid 41305651)
51. d of 145 μM. See ref 28.
52. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1991) Relationship between nuclear magnetic resonance chemical shift and protein secondary structure J. Mol. Biol. 222, 311-333 (Pubitemid 121004009)
53. Maynard, A. J., Sharman, G. J., and Searle, M. S. (1998) Origin of β-hairpin stability in solution: Structural and thermodynamic analysis of the folding of a model peptide supports hydrophobic stabilization in water J. Am. Chem. Soc. 120, 1996-2007 (Pubitemid 28179171)
54. Searle, M. S., Griffiths-Jones, S. R., and Skinner-Smith, H. (1999) Energetics of weak interactions in a β-hairpin peptide: Electrostatic and hydrophobic contributions to stability from lysine salt bridges J. Am. Chem. Soc. 121, 11615-11620 (Pubitemid 30032737)
55. Sharman, G. J. and Searle, M. S. (1997) Dissecting the effects of cooperativity on the stabilisation of a de novo designed three stranded anti-parallel β-sheet Chem. Commun. 1955-1956 (Pubitemid 127495608)
56. Sharman, G. J. and Searle, M. S. (1998) Cooperative interaction between the three strands of a designed antiparallel β-sheet J. Am. Chem. Soc. 120, 5291-5300 (Pubitemid 28328892)
57. Griffiths-Jones, S. R. and Searle, M. S. (2000) Structure, folding, and energetics of cooperative interactions between the β-strands of a de novo designed three-stranded antiparallel β-sheet peptide J. Am. Chem. Soc. 122, 8350-8356
58. Kortemme, T., Ramirez-Alvarado, M., and Serrano, L. (1998) Design of a 20-amino acid, three-stranded β-sheet protein Science 281, 253-256 (Pubitemid 28334507)
59. Kaul, R., Angeles, A. R., Jager, M., Powers, E. T., and Kelly, J. W. (2001) Incorporating β-turns and a turn mimetic out of context in loop 1 of the WW domain affords cooperatively folded β-sheets J. Am. Chem. Soc. 123, 5206-5212 (Pubitemid 32910663)
60. Nguyen, H., Jager, M., Kelly, J. W., and Gruebele, M. (2005) Engineering a beta-sheet protein toward the folding speed limit J. Phys. Chem. B 109, 15182-15186 (Pubitemid 41260759)
61. Zondlo, N. J. and Schepartz, A. (1999) Highly specific DNA recognition by a designed miniature protein J. Am. Chem. Soc. 121, 6938-6939 (Pubitemid 29374495)
62. Smith, T. J., Stains, C. I., Meyer, S. C., and Ghosh, I. (2006) Inhibition of β-amyloid fibrillization by directed evolution of a β-sheet presenting miniature protein J. Am. Chem. Soc. 128, 14456-14457 (Pubitemid 44749835)