Specificity of the Initial Collapse in the Folding of the Cold Shock Protein

Journal of Molecular Biology

Volumn 360, Issue 5, 2006, Pages 1067-1080

  Magg, Christine ^a   Kubelka, Jan ^b   Holtermann, Georg ^c   Haas, Elisha ^d   Schmid, Franz X ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^d BAR ILAN UNIVERSITY   (Israel)

Author keywords

fluorescence energy transfer; folding intermediates; folding kinetics; intra molecular distances; protein folding

Indexed keywords

AMMONIUM SULFATE; BACTERIAL PROTEIN; COLD SHOCK PROTEIN; ETHYLENE GLYCOL; WATER;

ARTICLE; BACILLUS; ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN VARIANT; SOLUTE; TEMPERATURE;

BACILLUS CALDOLYTICUS;

EID: 33745955427     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.05.073     Document Type: Article

References (65)

1. Schindler T., Herrler M., Marahiel M.A., and Schmid F.X. Extremely rapid folding in the absence of intermediates: the cold-shock protein from Bacillus subtilis. Nature Struct. Biol. 2 (1995) 663-673
2. Ferguson N., and Fersht A.R. Early events in protein folding. Curr. Opin. Struct. Biol. 13 (2003) 75-81
3. Horng J.C., Moroz V., and Raleigh D.P. Rapid cooperative two-state folding of a miniature alpha-beta protein and design of a thermostable variant. J. Mol. Biol. 326 (2003) 1261-1270
4. Huang G.S., and Oas T.G. Submillisecond folding of monomeric lambda repressor. Proc. Natl Acad. Sci. USA 92 (1995) 6878-6882
5. Jackson S.E. How do small single-domain proteins fold?. Fold. Des. 3 (1998) R81-R91
6. Mayor U., Johnson C.M., Daggett V., and Fersht A.R. Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation. Proc. Natl Acad. Sci. USA 97 (2000) 13518-13522
7. Eaton W.A., Munoz V., Hagen S.J., Jas G.S., Lapidus L.J., Henry E.R., and Hofrichter J. Fast kinetics and mechanisms in protein folding. Annu. Rev. Biophys. Biomol. Struct. 29 (2000) 327-359
8. Gillespie B., and Plaxco K.W. Using protein folding rates to test protein folding theories. Annu. Rev. Biochem. 73 (2004) 837-859
9. Krantz B.A., Mayne L., Rumbley J., Englander S.W., and Sosnick T.R. Fast and slow intermediate accumulation and the initial barrier mechanism in protein folding. J. Mol. Biol. 324 (2002) 359-371
10. Millett I.S., Doniach S., and Plaxco K.W. Toward a taxonomy of the denatured state: Small angle scattering studies of unfolded proteins. Unfolded Proteins 62 (2002) 241-262
11. Millett I.S., Townsley L.E., Chiti F., Doniach S., and Plaxco K.W. Equilibrium collapse and the kinetic 'foldability' of proteins. Biochemistry 41 (2002) 321-325
12. Kimura T., Uzawa T., Ishimori K., Morishima I., Takahashi S., Konno T., et al. Specific collapse followed by slow hydrogen-bond formation of beta-sheet in the folding of single-chain monellin. Proc. Natl Acad. Sci. USA 102 (2005) 2748-2753
13. Uzawa T., Akiyama S., Kimura T., Takahashi S., Ishimori K., Morishima I., and Fujisawa T. Collapse and search dynamics of apomyoglobin folding revealed by submillisecond observations of alpha-helical content and compactness. Proc. Natl Acad. Sci. USA 101 (2004) 1171-1176
14. Segel D.J., Bachmann A., Hofrichter J., Hodgson K.O., Doniach S., and Kiefhaber T. Characterization of transient intermediates in lysozyme folding with time-resolved small-angle X-ray scattering. J. Mol. Biol. 288 (1999) 489-499
15. Arai M., Ito K., Inobe T., Nakao M., Maki K., Kamagata K., et al. Fast compaction of alpha-lactalbumin during folding studied by stopped-flow X-ray scattering. J. Mol. Biol. 321 (2002) 121-132
16. Qin Z., Ervin J., Larios E., Gruebele M., and Kihara H. Formation of a compact structured ensemble without fluorescence signature early during ubiquitin folding. J. Phys. Chem. 106 (2002) 13040-13046
17. Akiyama S., Takahashi S., Kimura T., Ishimori K., Morishima I., Nishikawa Y., and Fujisawa T. Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle X-ray scattering. Proc. Natl Acad. Sci. USA 99 (2002) 1329-1334
18. Plaxco K.W., Millett I.S., Segel D.J., Doniach S., and Baker D. Chain collapse can occur concomitantly with the rate-limiting step in protein folding. Nature Struct. Biol. 6 (1999) 554-556
19. Jacob J., Krantz B., Dothager R.S., Thiyagarajan P., and Sosnick T.R. Early collapse is not an obligate step in protein folding. J. Mol. Biol. 338 (2004) 369-382
20. Bilsel O., and Matthews C.R. Molecular dimensions and their distributions in early folding intermediates. Curr. Opin. Struct. Biol. 16 (2006) 86-93
21. Wu P., and Brand L. Resonance energy transfer: methods and applications. Anal. Biochem. 218 (1994) 1-13
22. Ratner V., Sinev M., and Haas E. Determination of intramolecular distance distribution during protein folding on the millisecond timescale. J. Mol. Biol. 299 (2000) 1363-1371
23. Navon A., Ittah V., Landsman P., Scheraga H.A., and Haas E. Distributions of intramolecular distances in the reduced and denatured states of bovine pancreatic ribonuclease A. Folding initiation structures in the C-terminal portions of the reduced protein. Biochemistry 40 (2001) 105-118
24. Lillo M.P., Szpikowska B.K., Mas M.T., Sutin J.D., and 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
25. Lakowicz, J. R. (1999). Principles of Fluorescence Spectroscopy, Kluwer/Pleum Publishers, New York.
26. Haas E. The study of protein folding and dynamics by determination of intramolecular distance distributions and their fluctuations using ensemble and single-molecule FRET measurements. Chemphyschem. 6 (2005) 858-870
27. Magg C., and Schmid F.X. Rapid collapse precedes the fast two-state folding of the cold shock protein. J. Mol. Biol. 335 (2004) 1309-1323
28. Kuzmenkina E.V., Heyes C.D., and Nienhaus G.U. Single-molecule Forster resonance energy transfer study of protein dynamics under denaturing conditions. Proc. Natl Acad. Sci. USA 102 (2005) 15471-15476
29. Schuler B., Lipman E.A., and Eaton W.A. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419 (2002) 743-747
30. Lipman E.A., Schuler B., Bakajin O., and Eaton W.A. Single-molecule measurements of protein folding kinetics. Science 301 (2003) 1233-1235
31. Sadqi M., Lapidus L.J., and Munoz V. How fast is protein hydrophobic collapse?. Proc. Natl Acad. Sci. USA 100 (2003) 12117-12122
32. Laurence T.A., Kong X., Jager M., and Weiss S. Probing structural heterogeneities and fluctuations of nucleic acids and denatured proteins. Proc. Natl Acad. Sci. USA 102 (2005) 17348-17353
33. Schindelin H., Jiang W., Inouye M., and Heinemann U. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc. Natl Acad. Sci. USA 91 (1994) 5119-5123
34. Schindler T., and Schmid F.X. Thermodynamic properties of an extremely rapid protein folding reaction. Biochemistry 35 (1996) 16833-16842
35. Perl D., Welker C., Schindler T., Schröder K., Marahiel M.A., Jaenicke R., and Schmid F.X. Conservation of rapid two-state folding in mesophilic, thermophilic, and hyperthermophilic cold shock proteins. Nature Struct. Biol. 5 (1998) 229-235
36. Garcia-Mira M.M., Boehringer D., and Schmid F.X. The folding transition state of the cold shock protein is strongly polarized. J. Mol. Biol. 339 (2004) 555-569
37. Timasheff S.N. The control of protein stability and association by weak interactions with water - how do solvents affect these processes. Annu. Rev. Biophys. Biomol. Struct. 22 (1993) 67-97
38. Timasheff S.N. Protein hydration, thermodynamic binding, and preferential hydration. Biochemistry 41 (2002) 13473-13482
39. Auton M., and Bolen D.W. Predicting the energetics of osmolyte-induced protein folding/unfolding. Proc. Natl Acad. Sci. USA 102 (2005) 15065-15068
40. Gekko K., and Morikawa T. Preferential hydration of bovine serum albumin in polyhydric alcohol-water mixtures. J. Biochem. (Tokyo) 90 (1981) 39-50
41. Liu Y., and Bolen D.W. The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemistry 34 (1995) 12884-12891
42. Nozaki Y., and Tanford C. The solubility of amino acids and related compounds in aqueous thylene glycol solutions. J. Biol. Chem. 240 (1965) 3568-3575
43. Jacob M.H., Saudan C., Holtermann G., Martin A., Perl D., Merbach A.E., and Schmid F.X. Water contributes actively to the rapid crossing of a protein unfolding barrier. J. Mol. Biol. 318 (2002) 837-845
44. Plumridge T.H., Steele G., and Waigh R.D. Geometry-based simulation of the hydration of small molecules. Phys. Chem. Comm. 3 (2000) 36-41
45. Wang X.B., Yang X., Nicholas J.B., and Wang L.S. Bulk-like features in the photoemission spectra of hydrated doubly charged anion clusters. Science 294 (2001) 1322-1325
46. Jacob M., Schindler T., Balbach J., and Schmid F.X. Diffusion control in an elementary protein folding reaction. Proc. Natl Acad. Sci. USA 94 (1997) 5622-5627
47. Möglich A., Krieger F., and Kiefhaber T. Molecular basis for the effect of urea and guanidinium chloride on the dynamics of unfolded polypeptide chains. J. Mol. Biol. 345 (2005) 153-162
48. Shastry M.C.R., and Roder H. Evidence for barrier-limited protein folding kinetics on the microsecond time scale. Nature Struct. Biol. 5 (1998) 385-392
49. Capaldi A.P., Shastry M.C.R., Kleanthous C., Roder H., and Radford S.E. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nature Struct. Biol. 8 (2001) 68-72
50. Maki K., Cheng H., Dolgikh D.A., Shastry M.C., and Roder H. Early events during folding of wild-type staphylococcal nuclease and a single-tryptophan variant studied by ultrarapid mixing. J. Mol. Biol. 338 (2004) 383-400
51. Roder H., Maki K., Cheng H., and Shastry M.C. Rapid mixing methods for exploring the kinetics of protein folding. Methods 34 (2004) 15-27
52. Weisbuch S., Gerard F., Pasdeloup M., Cappadoro J., Dupont Y., and Jamin M. Cooperative sub-millisecond folding kinetics of apomyoglobin pH 4 intermediate. Biochemistry 44 (2005) 7013-7023
53. Perl D., Holtermann G., and Schmid F.X. Role of the chain termini for the folding transition state of the cold shock protein. Biochemistry 40 (2001) 15501-15511
54. Ellison P.A., and Cavagnero S. Role of unfolded state heterogeneity and en-route ruggedness in protein folding kinetics. Protein Sci. 15 (2006) 564-582
55. Ratner V., Amir D., Kahana E., and Haas E. Fast collapse but slow formation of secondary structure elements in the refolding transition of E. coli adenylate kinase. J. Mol. Biol. 352 (2005) 683-699
56. Choy W.Y., Mulder F.A., Crowhurst K.A., Muhandiram D.R., Millett I.S., et al. Distribution of molecular size within an unfolded state ensemble using small-angle X-ray scattering and pulse field gradient NMR techniques. J. Mol. Biol. 316 (2002) 101-112
57. Baldwin R.L. A new perspective on unfolded proteins. Adv. Protein Chem. 62 (2002) 361-367
58. Pappu R.V., and Rose G.D. A simple model for polyproline II structure in unfolded states of alanine-based peptides. Protein Sci. 11 (2002) 2437-2455
59. Shi Z., Woody R.W., and Kallenbach N.R. Is polyproline II a major backbone conformation in unfolded proteins?. Adv. Protein Chem. 62 (2002) 163-240
60. Jacob M., Holtermann G., Perl D., Reinstein J., Schindler T., Geeves M.A., and Schmid F.X. Microsecond folding of the cold shock protein measured by a pressure- jump technique. Biochemistry 38 (1999) 2882-2891
61. Thompson P.A., Munoz V., Jas G.S., Henry E.R., Eaton W.A., and Hofrichter J. The helix-coil kinetics of a heteropeptide. J. Phys. Chem. B 104 (2000) 378-389
62. McCarney E.R., Werner J.H., Bernstein S.L., Ruczinski I., Makarov D.E., Goodwin P.M., and Plaxco K.W. Site-specific dimensions across a highly denatured protein; a single molecule study. J. Mol. Biol. 352 (2005) 672-682
63. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
64. Mueller U., Perl D., Schmid F.X., and Heinemann U. Thermal stability and atomic-resolution crystal structure of the Bacillus caldolyticus cold shock protein. J. Mol. Biol. 297 (2000) 975-988
65. Koradi R., Billeter M., and Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996) 51-55