A method for the reversible trapping of proteins in non-native conformations

Biochemistry

Volumn 47, Issue 51, 2008, Pages 13620-13634

  Milanesi, Lilia ^a   Jelinska, Clare ^a   Hunter, Christopher A ^a   Hounslow, Andrea M ^a   Staniforth, Rosemary A ^a   Waltho, Jonathan P ^a,b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC DISULFIDES; CHEMICAL CLEAVAGES; CYSTEINE RESIDUES; DISULFIDE EXCHANGES; FUNCTIONALIZATION; GENERAL APPROACHES; HIGH YIELDS; INTRAMOLECULAR CYCLIZATION; MACROCYCLIZATION; MALEIMIDE GROUPS; NATIVE CONFORMATIONS; NATIVE STATES; PHOSPHOGLYCERATE KINASES; PROTEIN SURFACES; REVERSIBLE SWITCHES; SYNTHETIC REAGENTS; TERMINAL DOMAINS;

AROMATIC COMPOUNDS; CONFORMATIONS; CROSSLINKING; NUCLEAR MAGNETIC RESONANCE; PROTEINS; SULFUR COMPOUNDS;

PROTEIN FOLDING;

CYSTEINE; DISULFIDE; MALEIMIDE; PHOSPHOGLYCERATE KINASE; THIOL;

AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CROSS LINKING; CYCLIZATION; ELECTROSPRAY MASS SPECTROMETRY; FLUORESCENCE SPECTROSCOPY; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; SURFACE PROPERTY;

BIOCHEMISTRY; CIRCULAR DICHROISM; CROSS-LINKING REAGENTS; DIMERIZATION; DISULFIDES; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CONFORMATION; PHOSPHOGLYCERATE KINASE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SPECTROMETRY, FLUORESCENCE; TEMPERATURE;

EID: 58149174070     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801362f     Document Type: Article

References (62)

1. Anfinsen, C. B. (1973) Principles that govern folding of protein chains. Science 181, 223-230.
2. Shakhnovich, E. (2006) Protein folding thermodynamics and dynamics: Where physics, chemistry, and biology meet. Chem. Rev. 106, 1559-1588.
3. Oliveberg, M., and Wolynes, P. G. (2005) The experimental survey of protein-folding energy landscapes. Q. Rev. Biophys. 38, 245-288.
4. Daggett, V., and Fersht, A. (2003) The present view of the mechanism of protein folding. Nat. Rev. Mol. Cell Biol. 4, 497-502.
5. Baker, D. (2000) A surprising simplicity to protein folding. Nature 405, 39-42.
6. Tulla-Puche, J., Getun, I. V., Woodward, C., and Barany, G. (2004) Native-like conformations are sampled by partially folded and disordered variants of bovine pancreatic trypsin inhibitor. Biochemistry 43, 1591-1598.
7. Jaenicke, R. (1999) Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71, 155-241.
8. Darby, N. J., Morin, P. E., Talbo, G., and Creighton, T. E. (1995) Refolding of bovine pancreatic trypsin-inhibitor via non-native disulfide intermediates. J. Mol. Biol. 249, 463-477.
9. Ptitsyn, O. B. (1987) Protein folding: Hypotheses and experiments. J. Protein Chem. 6, 273-293.
10. Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366.
11. Jackson, G. S., Hosszu, L. L. P., Power, A., Hill, A. F., Kenney, J., Saibil, H., Craven, C. J., Waltho, J. P., Clarke, A. R., and Collinge, J. (1999) Reversible conversion of monomeric human prion protein between native and fibrilogenic conformations. Science 283, 1935-1937.
12. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383.
13. Dill, K. A., and Shortle, D. (1991) Denatured states of proteins. Annu. Rev. Biochem. 60, 795-825.
14. Nishimura, C., Dyson, H. J., and Wright, P. E. (2008) The kinetic and equilibrium molten globule intermediates of apoleghemoglobin differ in structure. J. Mol. Biol. 378, 715-725.
15. Staniforth, R. A., Giannini, S., Higgins, L. D., Conroy, M. J., Hounslow, A. M., Jerala, R., Craven, C. J., and Waltho, J. P. (2001) Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily. EMBO J. 20, 4774-4781.
16. Fink, A. L. (1995) Compact intermediate states in protein-folding. Annu. Rev. Biophys. Biomol. Struct. 24, 495-522.
17. Ptitsyn, O. B. (1995) Molten globule and protein folding. Adv. Protein Chem. 47, 83-229.
18. Kuwajima, K. (1989) The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins: Struct., Funct., Genet. 6, 87-103.
19. Smith, D. P., Jones, S., Serpell, L. C., Sunde, M., and Radford, S. E. (2003) A systematic investigation into the effect of protein destabilisation on β2-microglobulin amyloid formation. J. Mol. Biol. 330, 943-954.
20. Mayor, U., Grossmann, J. G., Foster, N. W., Freund, S. M. V., and Fersht, A. R. (2003) The denatured state of engrailed homeodomain under denaturing and native conditions. J. Mol. Biol. 333, 977-991.
21. Kouvatsos, N., Meldrum, J. K., Searle, M. S., and Thomas, N. R. (2006) Coupling ligand recognition to protein folding in an engineered variant of rabbit ileal lipid binding protein. Chem. Commun., 4623-4625.
22. Kohn, J. E., and Plaxco, K. W. (2005) Engineering a signal transduction mechanism for protein-based biosensors. Proc. Natl. Acad. Sci. U.S.A. 102, 10841-10845.
23. Creighton, T. E. (1974) Intermediates in refolding of reduced pancreatic trypsin-inhibitor. J. Mol. Biol. 87, 579.
24. Creighton, T. E. (1975) Interactions between cysteine residues as probes of protein conformation: Disulfide bond between cys-14 and cys-38 of pancreatic trypsin-inhibitor. J. Mol. Biol. 96, 767-776.
25. Kolano, C., Helbing, J., Kozinski, M., Sander, W., and Hamm, P. (2006) Watching hydrogen-bond dynamics in a β-turn by transient two-dimensional infrared spectroscopy. Nature 444, 469-472.
26. Lu, H. S. M., Volk, M., Kholodenko, Y., Gooding, E., Hochstrasser, R. M., and DeGrado, W. F. (1997) Aminothiotyrosine disulfide, an optical trigger for initiation of protein folding. J. Am. Chem. Soc. 119, 7173-7180.
27. Ghosh, K., Ozkan, S. B., and Dill, K. A. (2007) The ultimate speed limit to protein folding is conformational searching. J. Am. Chem. Soc. 129, 11920-11927.
28. Roder, H., Maki, K., and Cheng, H. (2006) Early events in protein folding explored by rapid mixing methods. Chem. Rev. 106, 1836-1861.
29. Myers, J. K., and Oas, T. G. (2002) Mechanisms of fast protein folding. Annu. Rev. Biochem. 71, 783-815.
30. Eaton, W. A., Munoz, V., Hagen, S. J., Jas, G. S., Lapidus, L. J., Henry, E. R., and Hofrichter, J. (2000) Fast kinetics and mechanisms in protein folding. Annu. Rev. Biophys. Biomol. Struct. 29, 327-359.
31. Mayor, U., Johnson, C. M., Daggett, V., and Fersht, A. R. (2000) Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation. Proc. Natl. Acad. Sci. U.S.A. 97, 13518-13522.
32. Chen, R. P. Y., Huang, J. J. T., Chen, H. L., Jan, H., Velusamy, M., Lee, C. T., Fann, W. S., Larsen, R. W., and Chan, S. I. (2004) Measuring the refolding of β-sheets with different turn sequences on a nanosecond time scale. Proc. Natl. Acad. Sci. U.S.A. 101, 7305-7310.
33. Huang, C. Y., He, S., DeGrado, W. F., McCafferty, D. G., and Gai, F. (2002) Light-induced helix formation. J. Am. Chem. Soc. 124, 12674-12675.
34. Kumita, J. R., Smart, O. S., and Woolley, G. A. (2000) Photocontrol of helix content in a short peptide. Proc. Natl. Acad. Sci. U.S.A. 97, 3803-3808.
35. Zhu, Y.; Wang, T., and Gai, F. (2005) Laser-induced T-jump method: A non-conventional photoreleasing approach to study protein folding. In Dynamic Studies in Biology (Goeldner, M., and Givens, R., Eds.) 1st ed., pp 461-479, Wiley-VCH, Weinheim, Germany.
36. Hodgson, D. R. W., and Sanderson, J. M. (2004) The synthesis of peptides and proteins containing non-natural amino acids. Chem. Soc. Rev. 33, 422-430.
37. Volk, M. (2001) Fast initiation of peptide and protein folding processes. Eur. J. Org. Chem. 14, 2605-2621.
38. Shandiz, A. T., Capraro, B. R., and Sosnick, T. R. (2007) Intramolecular cross-linking evaluated as a structural probe of the protein folding transition state. Biochemistry 46, 13711-13719.
39. Weikl, T. R., and Dill, K. A. (2003) Folding kinetics of two-state proteins: Effect of circularization, permutation, and crosslinks. J. Mol. Biol. 332, 953-963.
40. Milanesi, L., Reid, G. D., Beddard, G. S., Hunter, C. A., and Waltho, J. P. (2004) Synthesis and photochemistry of a new class of photocleavable protein cross-linking reagents. Chem. - Eur. J. 10, 1705-1710.
41. Palmblad, M., Hakansson, K., Hakansson, P., Feng, X. D., Cooper, H. J., Giannakopulos, A. E., Green, P. S., and Derrick, P. J. (2000) A 9.4 T Fourier transform ion cyclotron resonance mass spectrometer: Description and performance. Eur. J. Mass Spectrom. 6, 267-275.
42. Mohamadi, F., Richards, N. G. J., Guida, W. C., Liskamp, R., Lipton, M., Caufield, C., Chang, G., Hendrickson, T., and Still, W. C. (1990) Macromodel: An integrated software system for modeling organic and bioorganic molecules using molecular mechanics. J. Comput. Chem. 11, 440-467.
43. Davies, G. J., Gamblin, S. J., Littlechild, J. A., Dauter, Z., Wilson, K. S., and Watson, H. C. (1994) Structure of the Adp complex of the 3-phosphoglycerate kinase from Bacillus stearothermophilus at 1.65 angstrom. Acta Crystallogr. D50, 202-209.
44. Cliff, M. J., Alizadeh, T., Jelinska, C., Craven, C. J., Staniforth, R. A., and Waltho, J. P. (2006) A thiol labelling competition experiment as a probe for sidechain packing in the kinetic folding intermediate of N-PGK. J. Mol. Biol. 364, 810-823.
45. Ellman, G. L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
46. Creighton, T. E. (1984) Disulfide bond formation in proteins. Methods Enzymol. 107, 305-329.
47. Parker, M. J., Spencer, J., and Clarke, A. R. (1995) An integrated kinetic-analysis of intermediates and transition-states in protein-folding reactions. J. Mol. Biol. 253, 771-786.
48. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free-energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl R-chymotrypsin using different denaturants. Biochemistry 27, 8063-8068.
49. Darby, N. J., Morin, P. E., Talbo, G., and Creighton, T. E. (1995) Refolding of bovine pancreatic trypsin-inhibitor via non-native disulfide intermediates. J. Mol. Biol. 249, 463-477.
50. Singh, R., and Kats, L. (1995) Catalysis of reduction of disulfide by selenol. Anal. Biochem. 232, 86-91.
51. Girouard, S., Houle, M. H., Grandbois, A., Keillor, J. W., and Michnick, S. W. (2005) Synthesis and characterization of dimaleimide fluorogens designed for specific labeling of proteins. J. Am. Chem. Soc. 127, 559-566.
52. Means, G. E., and Feeney, R. E. (1971) Chemical Modifications of Proteins, pp 110-114, Holden-Day, San Francisco.
53. Kolano, C., Helbing, J., Bucher, G., Sander, W., and Hamm, P. (2007) Intramolecular disulfide bridges as a phototrigger to monitor the dynamics of small cyclic peptides. J. Phys. Chem. B 111, 11297-11302.
54. Volk, M., Kholodenko, Y., Lu, H. S. M., Gooding, E. A., DeGrado, W. F., and Hochstrasser, R. M. (1997) Peptide conformational dynamics and vibrational stark effects following photoinitiated disulfide cleavage. J. Phys. Chem. B 101, 8607-8616.
55. Milanesi, L., Tomas, S., Hunter, C. A., Weinstein, J. A., Edge, R., Navaratnam, S., Waltho, J. P., and Best, J. (2008) A pulse radiolysis approach to fast reductive cleavage of a disulfide bond to uncage enzyme activity. Free Radical Biol. Med. 45, 1271-1278.
56. Hosszu, L. L. P., Craven, C. J., Spencer, J., Parker, M. J., Clarke, A. R., Kelly, M., and Waltho, J. P. (1997) Is the structure of the N-domain of phosphoglycerate kinase affected by isolation from the intact molecule? Biochemistry 36, 333-340.
57. Parker, M. J., Spencer, J., Jackson, G. S., Burston, S. G., Hosszu, L. L. P., Craven, C. J., Waltho, J. P., and Clarke, A. R. (1996) Domain behavior during the folding of a thermostable phosphoglycerate kinase. Biochemistry 35, 15740-15752.
58. Darby, N., and Creighton, T. E. (1995) Protein stability and folding: Theory and practice. In Methods in Molecular Biology (Shirley, B. A., Ed.) pp 219-252, Human Press Inc., Totowa, NJ.
59. Pascher, T., Chesick, J. P., Winkler, J. R., and Gray, H. B. (1996) Protein folding triggered by electron transfer. Science 271, 1558-1560.
60. Jones, C. M., Henry, E., Hu, Y., Cham, C.-K., Luck, S. D., Bhuyan, A., Roder, H., Hofrichter, J., and Eaton, W. A. (1993) Fast events in protein folding initiated by nanosecond laser photolysis. Proc. Natl. Acad. Sci. U.S.A. 90, 11860-11864.
61. Chakraborty, S., Ittah, V., Bai, P., Luo, L., Haas, E., and Peng, Z. Y. (2001) Structure and dynamics of the R-lactalbumin molten globule: Fluorescence studies using proteins containing a single tryptophan residue. Biochemistry 40, 7228-7238.
62. Reed, M. A. C., Jelinska, C., Syson, K., Cliff, M. J., Splevins, A., Alizadeh, T., Hounslow, A. M., Staniforth, R. A., Clarke, A. R., Craven, C. J., and Waltho, J. P. (2006) The Denatured State under Native Conditions: A Non-native-like Collapsed State of N-PGK. J. Mol. Biol. 357, 365-372.