Thermodynamic consequences of incorporating 4-substituted proline derivatives into a small helical protein

Biochemistry

Volumn 49, Issue 19, 2010, Pages 4255-4263

  Zheng, Tong Yuan ^a   Lin, Yu Ju ^a   Horng, Jia Cherng ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYPROLINES; AROMATIC INTERACTIONS; ELECTRON-WITHDRAWING SUBSTITUENTS; HELICAL PROTEINS; HELIX CONFORMATION; HYDROPHOBIC EFFECT; N-TERMINALS; NATIVE STRUCTURES; NMR MEASUREMENTS; PROLINE DERIVATIVES; PROLINE RESIDUES; STEREOELECTRONIC EFFECT; SUBDOMAIN; THERMAL UNFOLDING; VILLIN HEADPIECE; WILD TYPES;

HYDROPHOBICITY; PROTEINS; UREA;

AROMATIC COMPOUNDS;

4 FLUOROPROLINE; 4 METHOXYPROLINE; HYDROXYPROLINE; PROLINE DERIVATIVE; PROTEIN; RECOMBINASE; UNCLASSIFIED DRUG; UREA; VILLIN;

ARTICLE; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; CONFORMATION; DENATURATION; MUTANT; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN STABILITY; THERMODYNAMICS; WILD TYPE;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; HYDROXYPROLINE; MODELS, MOLECULAR; NEUROFILAMENT PROTEINS; PEPTIDE FRAGMENTS; PROLINE; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 77952369160     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100323v     Document Type: Article

References (38)

1. Bhattacharyya, R. and Chakrabarti, P. (2003) Stereospecific interactions of proline residues in protein structures and complexes J. Mol. Biol. 331, 925-940
2. Jäger, 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
3. 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
4. Neidigh, J. W., Fesinmeyer, R. M., and Andersen, N. H. (2002) Designing a 20-residue protein Nat. Struct. Biol. 9, 425-430
5. Neidigh, J. W., Fesinmeyer, R. M., Prickett, K. S., and Andersen, N. H. (2001) Exendin-4 and glucagon-like-peptide-1: NMR structural comparisons in the solution and micelle-associated states Biochemistry 40, 13188-13200
6. Vermeulen, W., Van Troys, M., Bourry, D., Dewitte, D., Rossenu, S., Goethals, M., Borremans, F. A. M., Vandekerckhove, J., Martins, J. C., and Ampe, C. (2006) Identification of the PXW sequence as a structural gatekeeper of the headpiece C-terminal subdomain fold J. Mol. Biol. 359, 1277-1292
7. McKnight, C. J., Doering, D. S., Matsudaira, P. T., and Kim, P. S. (1996) A thermostable 35-residue subdomain within villin headpiece J. Mol. Biol. 260, 126-134
8. McKnight, C. J., Matsudaira, P. T., and Kim, P. S. (1997) NMR structure of the 35-residue villin headpiece subdomain Nat. Struct. Biol. 4, 180-184
9. Vardar, D., Buckley, D. A., Frank, B. S., and McKnight, C. J. (1999) NMR structure of an F-actin-binding "headpiece" motif from villin J. Mol. Biol. 294, 1299-1310
10. Bi, Y., Cho, J. H., Kim, E. Y., Shan, B., Schindelin, H., and Raleigh, D. P. (2007) Rational design, structural and thermodynamic characterization of a hyperstable variant of the villin headpiece helical subdomain Biochemistry 46, 7497-7505
11. Chiu, T. K., Kubelka, J., Herbst-Irmer, R., Eaton, W. A., Hofrichter, J., and Davies, D. R. (2005) High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein Proc. Natl. Acad. Sci. U.S.A. 102, 7517-7522
12. Wang, M., Tang, Y., Sato, S., Vugmeyster, L., McKnight, C. J., and Raleigh, D. P. (2003) Dynamic NMR line-shape analysis demonstrates that the villin headpiece subdomain folds on the microsecond time scale J. Am. Chem. Soc. 125, 6032-6033
13. Tang, Y. F., Goger, M. J., and Raleigh, D. P. (2006) NMR characterization of a peptide model provides evidence for significant structure in the unfolded state of the villin headpiece helical subdomain Biochemistry 45, 6940-6946
14. Xiao, S. F., Bi, Y., Shan, B., and Ralelgh, D. P. (2009) Analysis of core packing in a cooperatively folded miniature protein: the ultrafast folding villin headpiece helical subdomain Biochemistry 48, 4607-4616
15. 5-phenylalanine mutations on the folding of a small protein J. Am. Chem. Soc. 128, 15932-15933
16. Zheng, H., Comeforo, K., and Gao, J. M. (2009) Expanding the fluorous arsenal: tetrafluorinated phenylalanines for protein design J. Am. Chem. Soc. 131, 18-19
17. Reiersen, H. and Rees, A. R. (2001) The hunchback and its neighbours: proline as an environmental modulator Trends Biochem. Sci. 26, 679-684
18. Hutchinson, E. G. and Thornton, J. M. (1994) A revised set of potentials for β-turn formation in proteins Protein Sci. 3, 2207-2216
19. Wilmot, C. M. and Thornton, J. M. (1988) Analysis and prediction of the different types of β-turn in proteins J. Mol. Biol. 203, 221-232
20. Richardson, J. S. and Richardson, D. C. (1988) Amino acid preferences for specific locations at the ends of α helices Science 240, 1648-1652
21. DeRider, M. L., Wilkens, S. J., Waddell, M. J., Bretscher, L. E., Weinhold, F., Raines, R. T., and Markley, J. L. (2002) Collagen stability: insights from NMR spectroscopic and hybrid density functional computational investigations of the effect of electronegative substituents on prolyl ring conformations J. Am. Chem. Soc. 124, 2497-2505
22. Shoulders, M. D. and Raines, R. T. (2009) Collagen structure and stability Annu. Rev. Biochem. 78, 929-958
23. Bretscher, L. E., Jenkins, C. L., Taylor, K. M., DeRider, M. L., and Raines, R. T. (2001) Conformational stability of collagen relies on a stereoelectronic effect J. Am. Chem. Soc. 123, 777-778
24. Shoulders, M. D., Satyshur, K. A., Forest, K. T., and Raines, R. T. (2010) Stereoelectronic and steric effects in side chains preorganize a protein main chain Proc. Natl. Acad. Sci. U.S.A. 107, 559-564
25. Chiang, Y. C., Lin, Y. J., and Horng, J. C. (2009) Stereoelectronic effects on the transition barrier of polyproline conformational interconversion Protein Sci. 18, 1967-1977
26. Horng, J. C. and Raines, R. T. (2006) Stereoelectronic effects on polyproline conformation Protein Sci. 15, 74-83
27. Kümin, M., Sonntag, L. S., and Wennemers, H. (2007) Azidoproline containing helices: stabilization of the polyproline II structure by a functionalizable group J. Am. Chem. Soc. 129, 466-467
28. Kim, W., McMillan, R. A., Snyder, J. P., and Conticello, V. P. (2005) A stereoelectronic effect on turn formation due to proline substitution in elastin-mimetic polypeptides J. Am. Chem. Soc. 127, 18121-18132
29. Naduthambi, D. and Zondlo, N. J. (2006) Stereoelectronic tuning of the structure and stability of the Trp cage miniprotein J. Am. Chem. Soc. 128, 12430-12431
30. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 239, 266-280
31. Wüthrich, K. (1986) NMR of amino acid residues and mononucleotides, in NMR of Proteins and Nucleic Acids, pp 13-25, Wiley, New York.
32. Aune, K. C., Salahuddin, A., Zarlengo, M. H., and Tanford, C. (1967) Evidence for residual structure in acid- and heat-denatured proteins J. Biol. Chem. 242, 4486-4489
33. Deshpande, R. A., Khan, M. I., and Shankar, V. (2003) Equilibrium unfolding of RNase Rs from Rhizopus stolonifer: pH dependence of chemical and thermal denaturation Biochim. Biophys. Acta 1648, 184-194
34. Farruggia, B. and Pic, G. A. (1999) Thermodynamic features of the chemical and thermal denaturations of human serum albumin Int. J. Biol. Macromol. 26, 317-323 (Pubitemid 29509940)
35. Tang, Y., Rigotti, D. J., Fairman, R., and Raleigh, D. P. (2004) Peptide models provide evidence for significant structure in the denatured state of a rapidly folding protein: the villin headpiece subdomain Biochemistry 43, 3264-3272
36. Janesko, B. G., Gallek, C. J., and Yaron, D. (2003) Using constrained schrödinger equations to separate resonant and inductive substituent effects: a new methodology for parametrizing simple models in chemistry J. Phys. Chem. A 107, 1655-1663
37. Alabugin, I. V. and Zeidan, T. A. (2002) Stereoelectronic effects and general trends in hyperconjugative acceptor ability of-bonds J. Am. Chem. Soc. 124, 3175-3185
38. Kotch, F. W., Guzei, I. A., and Raines, R. T. (2008) Stabilization of the collagen triple helix by O -methylation of hydroxyproline residues J. Am. Chem. Soc. 130, 2952-295