Effect of H helix destabilizing mutations on the kinetic and equilibrium folding of apomyoglobin

Journal of Molecular Biology

Volumn 285, Issue 1, 1999, Pages 269-282

  Cavagnero, Silvia ^a   Dyson, H Jane ^a   Wright, Peter E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Myoglobin; NMR hydrogen deuterium exchange; Protein folding; Protein folding intermediate

Indexed keywords

APOPROTEIN; MYOGLOBIN;

ARTICLE; CIRCULAR DICHROISM; KINETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY;

EID: 0033534586     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2273     Document Type: Article

References (63)

1. Alexandrescu A. T., Abeygunawardana C., Shortle D. Structure and dynamics of a denatured 131-residue fragment of staphylococcal nuclease: a heteronuclear NMR study. Biochemistry. 33:1994;1063-1072.
2. 1H NMR assignments of its pH-denatured state. Proc. Natl Acad. Sci. USA. 91:1994;9412-9416.
3. Baldwin R. L. Finding intermediates in protein folding. BioEssays. 16:1994;207-210.
4. Baldwin R. L. On-pathway versus off-pathway folding intermediates. Fold. Design. 1:1996;R1-R8.
5. Ballew R. M., Sabelko J., Gruebele M. Direct observation of fast protein folding: The initial collapse of apomyoglobin. Proc. Natl Acad. Sci. USA. 93:1996;5759-5764.
6. Barrick D., Baldwin R. L. Three-state analysis of sperm whale apomyoglobin folding. Biochemistry. 32:1993;3790-3796.
7. Bashford D., Cohen F. E., Karplus M., Kuntz I. D., Weaver D. L. Diffusion-collision model for the folding kinetics of myoglobin. Proteins: Struct. Funct. Genet. 4:1988;211-227.
8. Blaber M., Zhang X., Lindstrom J. D., Pepiot S. D., Baase W. A., Matthews B. W. Determination of α-helix propensity within the context of a folded protein. Sites 44 and 131 in bacteriophage T4 lysozyme. J. Mol. Biol. 235:1994;600-624.
9. Burton R. E., Huang G. S., Daugherty M. A., Calderone T. L., Oas T. G. The energy landscape of a fast-folding protein mapped by Ala-Gly substitutions. Nature Struct. Biol. 4:1997;305-310.
10. Clarke J., Fersht A. R. An evaluation of the use of hydrogen exchange at equilibrium to probe intermediates on the protein folding pathway. Fold. Design. 1:1996;243-254.
11. Dill K. A., Chan H. S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4:1997;10-18.
12. Dyson H. J., Wright P. E. Peptide conformation and protein folding. Curr. Opin. Struct. Biol. 3:1993;60-65.
13. Dyson H. J., Wright P. E. Insights into protein folding from NMR. Annu. Rev. Phys. Chem. 47:1996;369-395.
14. Dyson H. J., Merutka G., Waltho J. P., Lerner R. A., Wright P. E. Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding. I. Myohemerythrin. J. Mol Biol. 226:1992a;795-817.
15. Dyson H. J., Sayre J. R., Merutka G., Shin H.-C., Lemer R. A., Wright P. E. Folding of peptide fragments comprising the complete sequence of proteins: models for the initiation of protein folding. II. Plastocyanin. J. Mol Biol. 226:1992b;819-835.
16. Eliezer D., Jennings P. A., Wright P. E., Doniach S., Hodgson K. O., Tsuruta H. The radius of gyration of an apomyoglobin folding intermediate. Science. 270:1995;487-488.
17. Eliezer D., Yao J., Dyson H. J., Wright P. E. Structural and dynamic characterization of partially folded states of myoglobin and implications for protein folding. Nature Struct. Biol. 5:1998;148-155.
18. Evans P. A., Topping K. D., Woolfson D. N., Dobson C. M. Hydrophobic clustering in nonnative states of a protein: interpretation of chemical shifts in NMR spectra of denatured states of lysozyme. Protein: Struct. Funct. Genet. 9:1991;248-266.
19. Fiebig K. M., Schwalbe H., Buck M., Smith L. J., Dobson C. M. Toward a description of the conformations of denatured states of proteins. Comparison of a random coil model with NMR measurements. J. Phys. Chem. 100:1996;2661-2666.
20. Fink A. L., Calciano L. J., Goto Y., Kurotsu T., Palleros D. R. Classification of acid denaturation of proteins: Intermediates and unfolded states. Biochemistry. 33:1994;12504-12511.
21. Frank M. K., Clore G. M., Gronenborn A. M. Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy. Protein Sci. 4:1995;2605-2615.
22. Griko Y. V., Privalov P. L., Venyaminov S. Y., Kutyshenko V. P. Thermodynamic study of the apomyoglobin structure. J. Mol. Biol. 202:1988;127-138.
23. Grzesiek S., Bax A. Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114:1992;6291-6293.
24. 15N-enriched proteins. J. Biomol. NMR. 3:1993;185-204.
25. Hargrove M. S., Krzywda S., Wilkinson A. J., Dou Y., Ikeda-Saito M., Olson J. S. Stability of myoglobin: a model for the folding of heme proteins. Biochemistry. 33:1994;11767-11775.
26. Higuchi R., Krummel B., Saiki R. K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucl. Acids Res. 16:1988;7351-7367.
27. Horovitz A., Matthews J. M., Fersht A. R. α-helix stability in proteins. II. Factors that influence stability at an internal position. J. Mol. Biol. 227:1992;560-568.
28. Hughson F. M., Baldwin R. L. Use of site-directed mutagenesis to destabilize native apomyoglobin relative to folding intermediates. Biochemistry. 28:1989;4415-4422.
29. Hughson F. M., Wright P. E., Baldwin R. L. Structural characterization of a partly folded apomyoglobin intermediate. Science. 249:1990;1544-1548.
30. Irace G., Balestrieri C., Parlato G., Servillo L., Colonna G. Tryptophanyl fluorescence heterogeneity of apomyoglobins. Correlation with the presence of two distinct structural domains. Biochemistry. 20:1981;792-799.
31. Jamin M., Baldwin R. L. Two forms of the pH 4 folding intermediate of apomyoglobin. J. Mol. Biol. 276:1998;491-504.
32. Jennings P. A., Wright P. E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science. 262:1993;892-896.
33. Jennings P. A., Stone M. J., Wright P. E. Overexpression of myoglobin and assignment of the amide, Cα and Cβ resonances. J. Biomol. NMR. 6:1995;271-276.
34. Karplus M., Weaver D. L. Protein folding dynamics: The diffusion-collision model and experimental data. Protein Sci. 3:1994;650-668.
35. Kay L. E., Ikura M., Tschudin R., Bax A. Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J. Magn. Reson. 89:1990;496-514.
36. Kuriyan J., Wilz S., Karplus M., Petsko G. A. X-ray structure and refinement of carbon-monoxy (Fe ll)-myoglobin at 1.5 Å resolution. J. Mol. Biol. 192:1986;133-154.
37. Lakowicz J. R., Maliwal B. P., Cherek H., Balter A. Rotational freedom of tryptophan residues in proteins and peptides. Biochemistry. 22:1983;1741-1752.
38. Logan T. M., Thériault Y., Fesik S. W. Structural characterization of the FK506 binding protein unfolded in urea and guanidine hydrochloride. J. Mol. Biol. 236:1994;637-648.
39. Luo Y., Kay M. S., Baldwin R. L. Cooperativity of folding of the apomyoglobin pH 4 intermediate studied by glycine and proline mutations. Nature Struct. Biol. 4:1997;925-930.
40. Matouschek A., Kellis J. T., Serrano L., Bycroft M., Fersht A. R. Transient folding intermediates characterized by protein engineering. Nature. 346:1990;440-445.
41. Mu ñ V., Serrano L. Development of the multiple sequence approximation within the AGADIR model of α-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers. 41:1997;495-509.
42. Myers J. K., Pace C. N., Scholtz J. M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4:1995;2138-2148.
43. 1H NMR assignments for the amino-terminal domain of the phage 434 repressor in the urea-unfolded form. Proc. Natl Acad. Sci. USA. 89:1992;4397-4401.
44. O'Neil K. T., DeGrado W. F. A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science. 250:1990;646-651.
45. Pace C. N. Measuring and increasing protein stability. Trends Technol. 8:1990;93-98.
46. Pan H., Barbar E., Barany G., Woodward C. Extensive nonrandom structure in reduced and unfolded bovine pancreatic trypsin inhibitor. Biochemistry. 34:1995;13974-13981.
47. Pappu R. V., Weaver D. L. The early folding kinetics of apomyoglobin. Protein Sci. 7:1998;480-490.
48. Reymond M. T., Merutka G., Dyson H. J., Wright P. E. Folding propensities of peptide fragments of myoglobin. Protein Sci. 6:1997;706-716.
49. Richardson J. S., Richardson D. C. Amino acid preferences for specific locations at the ends of α helices. Science. 240:1988;1648-1652.
50. Santoro M. M., Bolen D. W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry. 27:1988;8063-8068.
51. Saven J. G., Wolynes P. G. Local conformational signals and the statistical thermodynamics of collapsed helical proteins. J. Mol. Biol. 257:1996;199-216.
52. Schulman B. A., Kim P. S. Proline scanning mutagenesis of a molten globule reveals non-cooperative formation of a protein's overall topology. Nature Struct. Biol. 3:1996;682-687.
53. Shin H.-C., Merutka G., Waltho J. P., Tennant L. L., Dyson H. J., Wright P. E. Peptide models of protein folding initiation sites. 3. The G-H helical hairpin of myoglobin. Biochemistry. 32:1993a;6356-6364.
54. Shin H.-C., Merutka G., Waltho J. P., Wright P. E., Dyson H. J. Peptide models of protein folding initiation sites. 2. The G-H turn region of myoglobin acts as a helix stop signal. Biochemistry. 32:1993b;6348-6355.
55. Shortle D., Abeygunawardana C. NMR analysis of the residual structure in the denatured state of an unusual mutant of staphylococcal nuclease. Structure. 1:1993;121-134.
56. Smith L. J., Bolin K. A., Schwalbe H., MacArthur M. W., Thornton J. M., Dobson C. M. Analysis of main chain torsion angles in proteins: Prediction of NMR coupling constants for native and random coil conformations. J. Mol. Biol. 255:1996a;494-506.
57. Smith L. J., Fiebig K. M., Schwalbe H., Dobson C. M. The concept of a random coil. Residual structure in peptides and denatured proteins. Fold. Design. 1:1996b;R95-RI06.
58. Sosnick T. R., Mayne L., Englander S. W. Molecular collapse: the rate-limiting step in two-state cytochrome c folding. Proteins: Struct. Funct. Genet. 24:1996;413-426.
59. Tsui V., Garcia C., Cavagnero S., Siuzdak G., Dyson H. J., Wright P. E. Quench-flow experiments combined with mass spectrometry show apomyoglobin folds through an obligatory intermediate. Protein Sci. 1998.
60. Waltho J. P., Feher V. A., Merutka G., Dyson H. J., Wright P. E. Peptide models of protein folding initiation sites. 1. Secondary structure formation by peptides corresponding to the G- and H-helices of myoglobin. Biochemistry. 32:1993;6337-6347.
61. Wright P. E., Dyson H. J., Lerner R. A. Conformation of peptide fragments of proteins in aqueous solution: implications for initiation of protein folding. Biochemistry. 27:1988;7167-7175.
62. 15N resonance assignments of the N-terminal SH3 domain of drk in folded and unfolded states using enhanced-sensitivity pulse field gradient NMR techniques. J. Biomol. NMR. 4:1994;845-858.
63. Zhang O., Kay L. E., Shortle D., Forman-Kay J. D. Comprehensive NOE characterization of a partly folded large fragment of staphylococcal nuclease Δ131Δ, using NMR methods with improved resolution. J. Mol. Biol. 272:1997;9-20.