Tuning the heterogeneous early folding dynamics of phosphoglycerate kinase

Journal of Molecular Biology

Volumn 333, Issue 1, 2003, Pages 187-199

  Osváth, Szabolcs ^a,c   Sabelko, Jobiah J ^a   Gruebele, Martin ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Downhill folding; Energy landscape; Logarithmic oscillation; Phosphoglycerate kinase; Temperature jump

Indexed keywords

PHOSPHOGLYCERATE KINASE; PROLINE; TRYPTOPHAN; TYROSINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIS ISOMER; ENERGY; ENZYME ANALYSIS; ENZYME KINETICS; FLUORESCENCE; LASER; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR PROBE; OSCILLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; SPECTROSCOPY; THERMODYNAMICS;

MUS;

EID: 18844481606     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.011     Document Type: Article

References (64)

1. Kim P.S., Baldwin R.L. Specific intermediates in the folding reactions of small proteins and the mechanism of protein folding. Annu. Rev. Biochem. 51:1982;459-489.
2. 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.
3. Hagen S.J., Eaton W.A. Two-state expansion and collapse of a polypeptide. J. Mol. Biol. 297:2000;781-789.
4. Sabelko J., Ervin J., Gruebele M. Observation of strange kinetics in protein folding. Proc. Natl Acad. Sci. USA. 96:1999;6031-6036.
5. Parker M.J., Marqusee S. The cooperativity of burst phase reactions explored. J. Mol. Biol. 293:1999;1195-1210.
6. Segel D.J., Bachmann A., Hofrichter J., Hodgson K.O., Doniach S., Kiefhaber T. Characterization of transient intermediates in lysizyme folding with time-resolved small-angle X-ray scattering. J. Mol. Biol. 288:1999;489-499.
7. Capaldi A.P., Shastry M.C.R., Kleanthous C., Roder H., Radforth S.E. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nature Struct. Biol. 8:2001;68-72.
8. Qin Z., Ervin K., Larios E., Gruebele M., Kihara H. Formation of a compact structured ensemble without fluorescence signature early during ubiquitin unfolding. J. Phys. Chem. ser. B. 106:2002;13040-13046.
9. Portman J.J., Takada S., Wolynes P.G. Microscopic theory of protein folding rates. I. Fine structure of the free energy profile and folding routes from a variational approach. J. Chem. Phys. 114:2001;5069-5081.
10. Onuchic J.N., Luthey-Schulten Z., Wolynes P.G. Theory of protein folding: the energy landscape perspective. Annu. Rev. Phys. Chem. 48:1997;545-600.
11. Kiefhaber T. Kinetic traps in lysozyme folding. Proc. Natl Acad. Sci. USA. 92:1995;9029-9033.
12. Pappenberger G., Saudan C., Becker M., Merbach A.E., Kiefhaber T. Denaturant-induced movement of the transition state of protein folding revealed by high-pressure stopped-flow measurements. Proc. Natl Acad. Sci. USA. 97:2000;17-22.
13. Jäger M., Nguyen H., Crane J., Kelly J., Gruebele M. The folding mechanism of a β-sheet: the WW domain. J. Mol. Biol. 311:2001;373-393.
14. Snow C., Nguyen H., Pande V., Gruebele M. Absolute comparison of simulated and experimental protein folding dynamics. Nature. 420:2002;102-106.
15. Yang W.Y., Gruebele M. Folding at the speed limit. Nature. 423:2003;193-197.
16. Khorasanizadeh S., Peters I., Roder H. Evidence for a three-state model of protein folding from kinetic analysis of ubiquitin variants with altered core residues. Nature Struct. Biol. 3:1996;193-205.
17. Bachmann A., Kiefhaber T. Apparent two-state tendamistat folding is a sequential process along a defined route. J. Mol. Biol. 306:2001;375-386.
18. Ternstrom T., Mayor U., Akke M., Oliveberg M. From snapshot to movie: phi analysis of protein folding transition states taken one step further. Proc. Natl Acad. Sci. USA. 96:1999;14854-14859.
19. Walkenhorst W.F., Green S.M., Roder H. Kinetic evidence for folding and unfolding intermediates in staphylococcal nuclease. Biochemistry. 36:1997;5795-5805.
20. Shlesinger M.F., Zaslavsky G.M., Klafter J. Strange kinetics. Nature. 363:1993;31-37.
21. Volk M., Kholodenko Y., Lu H.S.M., Gooding E.A., DeGrado W.F., Hochstrasser R.M. Peptide conformational dynamics and vibrational stark effects following photoinitiated disulfide cleavage. J. Phys. Chem. 101:1997;8607-8616.
22. Skorobogatiy M., Guo H., Zuckerman M. Non-Arrhenius modes in the relaxation of model proteins. J. Chem. Phys. 109:1998;2528-2535.
23. Nymeyer H., García A.E., Onuchic J.N. Folding funnels and frustration in off-lattice minimalist protein landscapes. Proc. Natl Acad. Sci. USA. 95:1998;5921-5928.
24. Metzler R., Klafter J., Jortner J., Volk M. Multiple time scales for dispersive kinetics in early events of peptide folding. Chem. Phys. Letters. 293:1998;477-484.
25. Metzler R., Klafter J., Jortner J. Hierarchies and logarithmic oscillations in the temporal relaxation patterns of proteins and other complex systems. Proc. Natl Acad. Sci. USA. 96:1999;11085-11089.
26. Brandts J.F., Hu C.Q., Lin L.-N. A simple model for proteins with interacting domains. Applications to scanning calorimetry data. Biochemistry. 28:1989;8588-8596.
27. McHarg J., Kelly S.M., Price N.C., Cooper A., Littlechild J.A. Site-directed mutagenesis of proline 204 in the "hinge" region of yeast phosphoglycerate kinase. Eur. J. Biochem. 259:1999;939-945.
28. Missiakas D., Betton J.-M., Minard P., Yon J.M. Unfolding-refolding of the domains in yeast phosphoglycerate kinase: comparison with the isolated engineered domains. Biochemistry. 29:1990;8683-8689.
29. Ritco-Vonsovici M., Minard P., Desmadril M., Yon J.M. Is the continuity of the domains required for the correct folding of a two-domain protein. Biochemistry. 34:1995;16543-16551.
30. Pecorari F., Guilbert C., Minard P., Desmadril M., Yon J.M. Folding and functional complementation of engineered fragments from yeast phosphoglycerate kinase. Biochemistry. 35:1996;3465-3476.
31. Adams B., Fowler R., Hudson M., Pain R.H. The role of the C-terminal lysine in the hinge bending mechanism of yeast phosphoglyceratre kinase. FEBS Letters. 385:1996;101-104.
32. Vas M., Sinev M.A., Kotova N., Semisotnov G.V. Reactivation of 3-phosphoglycerate kinase from its proteolytic fragments. Eur. J. Biochem. 189:1990;575-579.
33. Szilágyi A.N., Kotova N.V., Semisotnov G.V., Vas M. Incomplete refolding of a fragment of the N-terminal domain of pig muscle 3-phosphoglycerate kinase that lacks a subdomain. Eur. J. Biochem. 268:2001;1851-1860.
34. Szilágyi A.N., Vas M. Sequential domain refolding of pig muscle 3-phosphoglycerate kinase: kinetic analysis of reactivation. Fold. Des. 3:1998;565-575.
35. 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 revealed by equilibrium amide exchange. Nature Struct. Biol. 4:1997;801-804.
36. Ritco-Vonsovici M., Mouratou B., Minard P., Desmadril M., Yon J.M., Andrieux M., et al. Role of the C-terminal helix in the folding and stability of yeast phosphoglycerate kinase. Biochemistry. 34:1995;833-841.
37. Beechem J.M., Sherman M.A., Mas M.T. Sequential domain unfolding in phosphoglycerate kinase: fluorescence intensity and anisotropy stopped-flow kinetics of several tryptophan mutants. Biochemistry. 34:1995;13943-13948.
38. Chardot T., Mitraki A., Amigues Y., Desmadril M., Betton J.M., Yon J.M. The effect of phosphate on the unfolding-refolding of phosphoglycerate kinase induced by guanidine hydrochloride. FEBS Letters. 228:1988;65-68.
39. Damaschun G., Damaschun H., Gast K., Misselwitz R., Müller J.J., Pfeil W., Zirwer D. Cold denaturation-induced conformational changes in phosphoglycerate kinase from yeast. Biochemistry. 32:1993;7739-7746.
40. Gast K., Damaschun G., Damaschun H., Misselqitz R., Zirwer D. Cold denaturation of yeast phosphoglycerate kinase: kinetics of changes in secondary structure and compactness on unfolding and refolding. Biochemistry. 32:1993;7747-7752.
41. Griko Y.V., Venyaminov S.Y., Privalov P.L. Heat and cold denaturation of phosphoglycerate kinase (interaction of domains). FEBS Letters. 244:1989;276-278.
42. Damaschun G., Damaschun H., Gast K., Zirwer D. Denatured states of yeast phosphoglycerate kinase. Biochemistry (Moscow). 63:1998;259-275.
43. Gast K., Damaschun G., Desmadril M., Minard P., Müller-Frohne M., Pfeil W., Zirwer D. Cold denaturation of yeast phosphoglycerate kinase: which domain is more stable? FEBS Letters. 358:1995;247-250.
44. Ptitsyn O.B., Pain R.H., Semisotnov G.V., Zerovnik E., Razgulyaev O.I. Evidence for a molten globule state as a general intermediate in protein folding. FEBS Letters. 232:1990;20-24.
45. Lillo M.P., Szpikowska B.K., Mas M.T., Sutin J.D., Beechem J.M. Real-time measurement of multiple intramolecular distances during protein folding reactions: a multisite stopped-flow fluorescence energy-transfer study of yeast phosphoglycerate kinase. Biochemistry. 36:1997;11273-11281.
46. 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.
47. Lillo P., Mas M.T., Beechem J.M. Characterization of the 3-D structure and psec/nsec rotational dynamics of the rapidly collapsed folded state in yeast phosphoglycerate kinase. Biophys. J. 74:1998;. Tu-Pos-130.
48. Thesis Sabelko J. Millisecond and Submillisecond Folding Kinetics of Horse Apomyoglobin and Yeast Phosphoglycerate Kinase. 2000;University of Illinois, Urbana-Champaign.
49. Osváth S., Gruebele M. Proline can have opposite effect on the fast and slow protein folding phases. Biophys. J. 85:2003;1215-1222.
50. Sherman M.A., Beechem J.M., Mas M.T. Probing intradomain and interdomain conformational changes during equilibrium unfolding of phosphoglycerate kinase: fluorescence and circular dichroism study of tryptophan mutants. Biochemistry. 34:1995;13934-13942.
51. Yang J.T., Wu C.C., Martinez H.M. Calculation of protein conformation from circular dichroism. Methods Enzymol. 130:1986;208-269.
52. Ervin J., Larios E., Osvath S., Schulten K., Gruebele M. What causes hyperfluorescence: folding intermediates or conformationally flexible native states? Biophys. J. 83:2002;473-483.
53. Yang W., Pitera J., Swope W., Gruebele M. Heterogeneous folding of the trpzip hairpin: full atom simulation and experiment. Nature Struct. Biol. 2003;. In the press.
54. Onuchic J.N., Wolynes P.G., Luthey-Schulten Z., Socci N.D. Toward an outline of the topography of a realistic protein folding funnel. Proc. Natl Acad. Sci. USA. 92:1995;3626-3630.
55. Mas M.T., Resplandor Z.E., Riggs A.D. Site-directed mutagenesis of glutamate-190 in the hinge region of yeast 3-phosphoglycerate kinase: implications for the mechanism of domain movement. Biochemistry. 26:1987;5369-5377.
56. Hitzeman R.A., Clarke L., Carbon J. Isolation and characterization of the yeast 3-phosphoglycerokinase gene (PGK) by an immunological screening technique. J. Biol. Chem. 255:1980;12073-12080.
57. Edelhoch H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry. 6:1967;1948-1954.
58. Johnson W.C.J. Secondary structure of protein through circular dichroism spectroscopy. Annu. Rev. Biophys. Biophys. Chem. 17:1988;145-166.
59. Ballew R.M., Sabelko J., Gruebele M. Observation of distinct nanosecond and microsecond protein folding events. Nature Struct. Biol. 3:1996;923-926.
60. Gruebele M., Sabelko J., Ballew R., Ervin J. Laser temperature-jump induced protein refolding. Accts Chem. Res. 31:1998;699-707.
61. Ballew R.M., Sabelko J., Reiner C., Gruebele M. A single-sweep, nanosecond time resolution laser temperature-jump apparatus. Rev. Sci. Instrum. 67:1996;3694-3699.
62. Ervin J., Sabelko J., Gruebele M. Submicrosecond real-time fluorescence detection: application to protein folding. J. Photochem. Photobiol. sect. B. 54:2000;1-15.
63. Semisotnov G.V., Vas M., Chemeris V.V., Kashparova N.J., Ktotova N.V., Razgulyaev O.I., Sienv M.A. Refolding kinetics of pig muscle and yeast 3-phosphoglycerate kinase and of their proteolytic fragments. Eur. J. Biochem. 202:1991;1083-1090.
64. Szpikowska B.K., Beechem J.M., Sherman M.A., Mas M.T. Equilibrium unfolding of yeast phosphoglycerate kinase and its mutants lacking one or both tryptophans: a circular dichroism and steady-state and time resolved fluorescence study. Biochemistry. 33:1994;2217-2225.