Effects of Domain Dissection on the Folding and Stability of the 43 kDa Protein PGK Probed by NMR

Journal of Molecular Biology

Volumn 330, Issue 5, 2003, Pages 1189-1201

  Reed, Michelle A C ^a   Hounslow, Andrea M ^a   Sze, K H ^b   Barsukov, Igor G ^c   Hosszu, Laszlo L P ^d   Clarke, Anthony R ^d   Craven, C Jeremy ^a   Waltho, Jonathan P ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

Author keywords

Assignment; Folding; Kinetic intermediate; NMR; Phosphoglycerate kinase

Indexed keywords

AMIDE; PHOSPHOGLYCERATE KINASE; PROTEIN; PROTEIN P43; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CONTROLLED STUDY; EQUILIBRIUM CONSTANT; GEOBACILLUS STEAROTHERMOPHILUS; KINETICS; MOLECULAR PROBE; MONTE CARLO METHOD; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; SIMULATION;

GEOBACILLUS STEAROTHERMOPHILUS;

EID: 0038351770     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00625-9     Document Type: Article

References (45)

1. Clarke A.R., Waltho J.P. Protein folding and intermediates. Curr. Opin. Biotechnol. 8:1997;400-410.
2. Roder H., Shastry M.C.R. Methods for exploring early events in protein folding. Curr. Opin. Struct. Biol. 9:1999;620-662.
3. Dyson H.J., Wright P.E. Insights into protein folding from NMR. Annu. Rev. Phys. Chem. 47:1996;369-395.
4. Brockwell D.J., Smith D.A., Radford S.E. Protein folding mechanisms: new methods and emerging ideas. Curr. Opin. Struct. Biol. 10:2000;16-25.
5. Dalby P.A., Oliveberg M., Fersht A.R. Folding intermediates of wild-type and mutants of barnase. I. Use of phi-value analysis and m-values to probe the cooperative nature of the folding pre-equilibrium. J. Mol. Biol. 276:1998;625-646.
6. Qi P.X., Sosnick T.R., Englander S.W. The burst phase in ribonuclease A folding and solvent dependence of the unfolded state. Nature Struct. Biol. 5:1998;882-884.
7. 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.
8. Englander S.W., Sosnick T.R., Mayne L.C., Shtilerman M., Qi P.X., Bai Y.W. Fast and slow folding in cytochrome c. Accts Chem. Res. 31:1998;737-744.
9. Shastry M.C.R., Sauder J.M., Roder H. Kinetic and structural analysis of submillisecond folding events in cytochrome c. Accts Chem. Res. 31:1998;717-725.
10. Parker M.J., Dempsey C.E., Hosszu L.L.P., Waltho J.P., Clarke A.R. Topology, sequence evolution and folding dynamics of an immunoglobulin domain. Nature Struct. Biol. 5:1998;194-198.
11. Fersht A.R. A kinetically significant intermediate in the folding of barnase. Proc. Natl Acad. Sci. USA. 97:2000;14121-14126.
12. Takei L., Chu R.A., Bai Y.W. Absence of stable intermediates on the folding pathway of barnase. Proc. Natl Acad. Sci. USA. 97:2000;10796-10801.
13. Hosszu L.L.P., Craven C.J., Parker M.J., Lorch M., Spencer J., Clarke A.R., Waltho J.P. Structure of a kinetic protein folding intermediate by equilibrium amide exchange. Nature Struct. Biol. 4:1997;801-804.
14. Heidary D.K., Gross L.A., Roy M., Jennings P.A. Evidence for an obligatory intermediate in the folding of interleukin-1beta. Nature Struct. Biol. 4:1997;725-731.
15. Capaldi A.P., Shastry M.C.R., Kleanthous C., Roder H., Radford S.E. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nature Struct. Biol. 8:2001;68-72.
16. Capaldi A.P., Ferguson S.J., Radford S.E. The Greek key protein apo-pseudoazurin folds through an obligate on-pathway intermediate. J. Mol. Biol. 286:1999;1621-1632.
17. 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. 8:1999;45-49.
18. Kuwata K., Shastry R., Cheng H., Hoshino M., Batt C.A., Goto Y., Roder H. Structural and kinetic characterization of early folding events in beta-lactoglobulin. Nature Struct. Biol. 8:2001;151-155.
19. Capaldi A.P., Kleanthous C., Radford S.E. Im7 folding mechanism: misfolding on a path to the native state. Nature Struct. Biol. 9:2002;209-216.
20. Sosnick T.R., Mayne L., Hiller R., Englander S.W. The barriers in protein-folding. Nature Struct. Biol. 1:1994;149-156.
21. Fersht A. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. 1999;W.H. Freeman, New York.
22. Matouschek A., Kellis J.T., Serrano L., Bycroft M., Fersht A.R. Transient folding intermediates characterized by protein engineering. Nature. 346:1990;440-445.
23. Clarke J., Itzhaki L.S. Hydrogen exchange and protein folding. Curr. Opin. Struct. Biol. 8:1998;112-118.
24. Li R.H., Woodward C. The hydrogen exchange core and protein folding. Protein Sci. 8:1999;1571-1590.
25. Staniforth R.A., Dean J.L.E., Zhong Q., Zerovnik E., Clarke A.R., Waltho J.P. The major transition state in folding need not involve the immobilization of side chains. Proc. Natl Acad. Sci. USA. 97:2000;5790-5795.
26. Davies G.J., Gamblin S.J., Littlechild J.A., Dauter Z., Wilson K.S., Watson H.C. Structure of the ADP complex of the 3-phosphoglycerate kinase from Bacillus stearothermophilus at 1.65 Å Acta Crystallog., sect. D. 50:1994;202-209.
27. Parker M.J., Spencer J., Jackson G.S., Burston S.G., Hosszu L.L.P., Craven C.J., et al. Domain behavior during the folding of a thermostable phosphoglycerate kinase. Biochemistry. 35:1996;15740-15752.
28. Parker M.J., Sessions R.B., Badcoe I.G., Clarke A.R. The development of tertiary interactions during the folding of a large protein. Fold. Des. 1:1996;145-156.
29. Hosszu L.L.P., Craven C.J., Spencer J., Parker M.J., Clarke A.R., Kelly M., Waltho J.P. Is the structure of the N-domain of phosphoglycerate kinase affected by isolation from the intact molecule? Biochemistry. 36:1997;333-340.
30. Pervushin K.V., Wider G., Wuthrich K. Single transition-to-single transition polarization transfer (ST2-PT) in [N-15,H-1]-TROSY. J. Biomol. NMR. 12:1998;345-348.
31. Yang D.W., Kay L.E. TROSY triple-resonance four-dimensional NMR spectroscopy of a 46 ns tumbling protein. J. Am. Chem. Soc. 121:1999;2571-2575.
32. Yang D.W., Kay L.E. Improved (HN)-H-1-detected triple resonance TROSY-based experiments. J. Biomol. NMR. 13:1999;3-10.
33. Bernstein B.E., Michels P.A.M., Hol W.G.J. Synergistic effects of substrate-induced conformational changes in phosphoglycerate kinase activation. Nature. 385:1997;275-278.
34. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR. 13:1999;289-302.
35. Bai Y.W., Milne J.S., Mayne L., Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17:1993;75-86.
36. Tugarinov V., Muhandiram R., Ayed A., Kay L.E. Four-dimensional NMR spectroscopy of a 723-residue protein: chemical shift assignments and secondary structure of malate synthase G. J. Am. Chem. Soc. 124:2002;10025-10035.
37. Gardner K.H., Zhang X.C., Gehring K., Kay L.E. Solution NMR studies of a 42 kDa Escherichia coli maltose binding protein beta-cyclodextrin complex: chemical shift assignments and analysis. J. Am. Chem. Soc. 120:1998;11738-11748.
38. Seavey B.R., Farr E.A., Westler W.M., Markley J.L. A relational database for sequence-specific protein NMR data. J. Biomol. NMR. 1:1991;217-236.
39. Moseley H.N.B., Montelione G.T. Automated analysis of NMR assignments and structures for proteins. Curr. Opin. Struct. Biol. 9:1999;635-642.
40. Mcfeeters R.L., Swapna G.V.T., Montelione G.T., Oswald R.E. Semi-automated backbone resonance assignments of the extracellular ligand binding domain of an ionotrophic glutamate receptor. J. Biomol. NMR. 22:2002;297-298.
41. α chemical shifts and their (i, i-1) sequential connectivities. J. Biomol. NMR. 23:2002;263-270.
42. Sambrook S., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. 15N labelling of proteins for NMR studies. J. Biomol. NMR. 5:1995;339-344.
44. Grzesiek S., Bax A. Amino-acid type determination in the sequential assignment procedure of uniformly C-13/N-15-enriched proteins. J. Biomol. NMR. 3:1993;185-204.
45. Wishart D.S., Bigam C.G., Holm A., Hodges R.S., Sykes B.D. H-1, C-13 and N-15 random coil NMR chemical shifts of the common amino acids. 1. Investigations of nearest neighbor effects. J. Biomol. NMR. 5:1995;67-81.