Intimate view of a kinetic protein folding intermediate: Residue-resolved structure, interactions, stability, folding and unfolding rates, homogeneity

Journal of Molecular Biology

Volumn 334, Issue 3, 2003, Pages 501-513

  Krishna, Mallela M G ^a   Lin, Yan ^a   Mayne, Leland ^a   Walter Englander, S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cytochrome c; EX1; Hydrogen exchange; Protein folding; Pulse labeling

Indexed keywords

CYTOCHROME C;

AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENERGY; MOLECULAR INTERACTION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON TRANSPORT; STRUCTURE ANALYSIS;

EID: 0242578172     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.09.070     Document Type: Article

References (81)

1. Wolynes P.G., Onuchic J.N., Thirumalai D. Navigating the folding routes. Science. 267:1995;1619-1620.
2. Shakhnovich E.I. Theoretical studies of protein-folding thermodynamics and kinetics. Curr. Opin. Struct. Biol. 7:1997;29-40.
3. Dill K.A., Chan H.S. From Levinthal to pathways to funnels. Nature Struct. Biol. 4:1997;10-19.
4. Wallace L.A., Matthews C.R. Sequential vs. parallel protein-folding mechanisms: experimental tests for complex folding reactions. Biophys. Chem. 101-102:2002;113-131.
5. Levinthal C. Are there pathways for protein folding. J. Chim. Phys. 65:1968;44-45.
6. Kim P.S., Baldwin R.L. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59:1990;631-660.
7. Englander S.W. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29:2000;213-238.
8. Roder H., Elöve G.A., Englander S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and proton NMR. Nature. 335:1988;700-704.
9. Udgaonkar J.B., Baldwin R.L. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature. 335:1988;694-699.
10. Udgaonkar J.B., Baldwin R.L. Early folding intermediate of ribonuclease A. Proc. Natl Acad. Sci. USA. 87:1990;8197-8201.
11. Elöve G.A., Roder H. Structure and stability of cytochrome c folding intermediates. Georgiou G., Bernardez-Clark E.D. Protein Refolding. 1991;50-63 American Chemical Society, Washington, DC.
12. Englander S.W., Mayne L. Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21:1992;243-265.
13. Baldwin R.L. Pulsed H/D-exchange studies of folding intermediates. Curr. Opin. Struct. Biol. 3:1993;84-91.
14. Dobson C.M., Evans P.A., Radford S.E. Understanding how proteins fold: the lysozyme story so far. Trends Biochem. Sci. 19:1994;31-37.
15. Evans P.A., Radford S.E. Probing the structure of folding intermediates. Curr. Opin. Struct. Biol. 4:1994;100-106.
16. Woodward C.K. Hydrogen exchange rates and protein folding. Curr. Opin. Struct. Biol. 4:1994;112-116.
17. Dyson H.J., Wright P.E. Insights into protein folding from NMR. Annu. Rev. Phys. Chem. 47:1996;369-395.
18. Li R., Woodward C. The hydrogen exchange core and protein folding. Protein Sci. 8:1999;1571-1591.
19. Bai Y., Sosnick T.R., Mayne L., Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science. 269:1995;192-197.
20. Bai Y., Englander S.W. Future directions in folding: the multi-state nature of protein structure. Proteins: Struct. Funct. Genet. 24:1996;145-151.
21. Chamberlain A.K., Marqusee S. Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms. Advan. Protein Chem. 53:2000;283-328.
22. Xu Y., Mayne L., Englander S.W. Evidence for an unfolding and refolding pathway in cytochrome c. Nature Struct. Biol. 5:1998;774-778.
23. Milne J.S., Xu Y., Mayne L.C., Englander S.W. Experimental study of the protein folding landscape: unfolding reactions in cytochrome c. J. Mol. Biol. 290:1999;811-822.
24. Bai Y. Kinetic evidence for an on-pathway intermediate in the folding of cytochrome c. Proc. Natl Acad. Sci. USA. 96:1999;477-480.
25. Rumbley J., Hoang L., Mayne L., Englander S.W. An amino acid code for protein folding. Proc. Natl Acad. Sci. USA. 98:2001;105-112.
26. Hoang L., Bédard S., Krishna M.M.G., Lin Y., Englander S.W. Cytochrome c folding pathway: kinetic native-state hydrogen exchange. Proc. Natl Acad. Sci. USA. 99:2002;12173-12178.
27. Krishna M.M.G., Lin Y., Rumbley J.N., Englander S.W. Cooperative omega loops in cytochrome c: role in folding and function. J. Mol. Biol. 331:2003;29-36.
28. Shastry M.C.R., Roder H. Evidence for barrier-limited protein folding kinetics on the microsecond time scale. Nature Struct. Biol. 5:1998;385-392.
29. Krantz B.A., Mayne L., Rumbley J., Englander S.W., Sosnick T.R. Fast and slow intermediate accumulation and the initial barrier mechanism in protein folding. J. Mol. Biol. 324:2002;359-371.
30. Akiyama S., Takahashi S., Ishimori K., Morishima I. Stepwise formation of α-helices during cytochrome c folding. Nature Struct. Biol. 7:2000;514-520.
31. Elöve G.A., Bhuyan A.K., Roder H. Kinetic mechanism of cytochrome c folding: involvement of the heme and its ligands. Biochemistry. 33:1994;6925-6935.
32. Sosnick T.R., Mayne L., Hiller R., Englander S.W. The barriers in protein folding. Nature Struct. Biol. 1:1994;149-156.
33. Englander S.W., Sosnick T.R., Mayne L.C., Shtilerman M., Qi P.X., Bai Y. Fast and slow folding in cytochrome c. Accts Chem. Res. 31:1998;737-744.
34. Weissman J.S., Kim P.S. A kinetic explanation for the rearrangement pathway of BPTI folding. Nature Struct. Biol. 2:1995;1123-1130.
35. 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.
36. Bilsel O., Zitzewitz J.A., Bowers K.E., Matthews C.R. Folding mechanism of the α-subunit of tryptophan synthase, an α/β barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry. 38:1999;1018-1029.
37. Bhuyan A.K., Udgaonkar J.B. Folding of horse cytochrome c in the reduced state. J. Mol. Biol. 312:2001;1135-1160.
38. Ridge J.A., Baldwin R.L., Labhardt A.M. Nature of fast and slow refolding reactions of iron(III) cytochrome c. Biochemistry. 20:1981;1622-1630.
39. Osterhout J.J., Nall B.T. Slow refolding kinetics in yeast iso-2 cytochrome c. Biochemistry. 24:1985;7999-8005.
40. Wood L.C., White T.B., Ramdas L., Nall B.T. Replacement of a conserved proline eliminates the absorbance-detected slow folding phase of iso-2-cytochrome c. Biochemistry. 27:1988;8562-8568.
41. Nawrocki J.P., Chu R.-A., Pannell L.K., Bai Y. Intermolecular aggregations are responsible for the slow kinetics observed on the folding of cytochrome c at neutral pH. J. Mol. Biol. 293:1999;991-995.
42. Hvidt A. A discussion of the pH dependence of the hydrogen-deuterium exchange of proteins. C.R. Trav. Lab. Carlsberg. 34:1964;299-317.
43. Bai Y., Milne J.S., Mayne L., Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17:1993;75-86.
44. Connelly G.P., Bai Y., Jeng M.-F., Englander S.W. Isotope effects in peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17:1993;87-92.
45. Hoang L., Maity H., Krishna M.M.G., Lin Y., Englander S.W. Folding units govern the cytochrome c alkaline transition. J. Mol. Biol. 331:2003;37-43.
46. Arrington C.B., Robertson A.D. Kinetics and thermodynamics of conformational equilibria in native proteins by hydrogen exchange. Methods Enzymol. 323:2000;104-124.
47. 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.
48. Feng H., Takei J., Lipsitz R., Tjandra N., Bai Y. Specific non-native hydrophobic interactions in a hidden folding intermediate: implications for protein folding. Biochemistry. 2003;. in the press.
49. Dyson H.J., Rance M., Houghten R.A., Lerner R.A., Wright P.E. Folding of immunogenic peptide fragments of proteins in water solution. I. Sequence requirements for the formation of a reverse turn. J. Mol. Biol. 201:1988;161-200.
50. Dyson H.J., Bolinger L., Feher V.A., Osterhout J.T. Jr, Yao J., Wright P.E. Sequence requirements for stabilization of a peptide reverse turn in water solution. Proline is not essential for stability. Eur. J. Biochem. 255:1998;462-471.
51. Colón W., Elöve G.A., Wakem P., Sherman F., Roder H. Side chain packing of the N- and C-terminal helices play a critical role in the kinetics of cytochrome c folding. Biochemistry. 35:1996;5538-5549.
52. Lifson S., Roig A. On the theory of the helix-coil transition in polypeptides. J. Chem. Phys. 34:1961;1963-1974.
53. Qian H., Schellman J.A. Helix-coil theories: a comparative study for finite length polypeptides. J. Phys. Chem. 96:1992;3987-3994.
54. Chakrabartty A., Kortemme T., Baldwin R.L. Helix propensities of the amino acids measured in alanine-based peptides without helix-stabilizing side-chain interactions. Protein Sci. 3:1994;843-852.
55. Padmanabhan S., York E.J., Stewart J.M., Baldwin R.L. Helix propensities of basic amino acids increase with the length of the side-chain. J. Mol. Biol. 257:1996;726-734.
56. Muñoz V., Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. Nature Struct. Biol. 1:1994;399-409.
57. Lacroix E., Viguera A.R., Serrano L. Elucidating the folding problem of α-helices: local motifs, long-range electrostatics, ionic strength dependence and prediction of NMR parameters. J. Mol. Biol. 284:1998;173-191.
58. 2H and temperature. Biochemistry. 24:1985;7396-7407.
59. 2 of the Linderstrøm-Lang model for protein amide hydrogen exchange. A study of individual amides in hen egg-white lysozyme. J. Mol. Biol. 230:1993;651-660.
60. Arrington C.B., Robertson A.D. Microsecond to minute dynamics revealed by EX1-type hydrogen exchange at nearly every backbone hydrogen bond in a native protein. J. Mol. Biol. 296:2000;1307-1317.
61. Canet D., Last A.M., Tito P., Sunde M., Spencer A., Archer D.B., et al. Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme. Nature Struct. Biol. 9:2002;308-315.
62. Yan S., Kennedy S.D., Koide S. Thermodynamic and kinetic exploration of the energy landscape of Borrelia budgdorferi OspA by native-state hydrogen exchange. J. Mol. Biol. 323:2002;363-375.
63. Sivaraman T., Arrington C.B., Robertson A.D. Kinetics of unfolding and folding from amide hydrogen exchange in native ubiquitin. Nature Struct. Biol. 8:2001;331-333.
64. Duan Y., Kollman P.A. Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science. 282:1998;740-744.
65. Penel S., Doig A.J. Rotamer strain energy in protein helices - quantification of a major force opposing protein folding. J. Mol. Biol. 305:2001;961-968.
66. Chowdary S., Zhang W., Wu C., Xiong G., Duan Y. Breaking non-native hydrophobic clusters is the rate-limiting step in the folding of an alanine-based peptide. Biopolymers. 68:2003;63-75.
67. Kussell E., Shimada J., Shakhnovich E.I. Side-chain dynamics and protein folding. Proteins: Struct. Funct. Genet. 52:2003;303-321.
68. Chin D.-H., Woody R.W., Rohl C.A., Baldwin R.L. Circular dichroism spectra of short, fixed-nucleus alanine helices. Proc. Natl Acad. Sci. USA. 99:2002;15416-15421.
69. Krantz B.A., Moran L.B., Kentsis A., Sosnick T.R. D/H amide kinetic isotope effects reveal when hydrogen bonds form during protein folding. Nature Struct. Biol. 7:2000;62-71.
70. Krantz B.A., Srivastava A.K., Nauli S., Baker D., Sauer R.T., Sosnick T.R. Understanding protein hydrogen bond formation with kinetic H/D amide isotope effects. Nature Struct. Biol. 9:2002;458-463.
71. Shtilerman M., Lorimer G.H., Englander S.W. Chaperonin function: folding by forced unfolding. Science. 284:1999;822-825.
72. Wildegger G., Kiefhaber T. Three-state model for lysozyme folding: triangular folding mechanism with an energetically trapped intermediate. J. Mol. Biol. 270:1997;294-304.
73. Wu Y., Matthews C.R. Parallel channels and rate-limiting steps in complex protein folding reactions: prolyl isomerization and the alpha subunit of Trp synthase, a TIM barrel protein. J. Mol. Biol. 323:2002;309-325.
74. Englander S.W., Mayne L., Rumbley J.N. Submolecular cooperativity produces multi-state protein unfolding and refolding. Biophys. Chem. 101-102:2002;57-65.
75. Rumbley J.N., Hoang L., Englander S.W. Recombinant equine cytochrome c in Escherichia coli: high-level expression, characterization, and folding and assembly mutants. Biochemistry. 41:2002;13894-13901.
76. Linderstrøm-Lang K. Deuterium exchange and protein structure. Neuberger A. Symposium on Protein Structure. 1958;23-24 Methuen, London.
77. Hvidt A., Nielsen S.O. Hydrogen exchange in proteins. Advan. Protein Chem. 21:1966;287-386.
78. Krishna M.M.G., Hoang L., Lin Y., Englander S.W. Hydrogen exchange methods to study protein folding. Methods. 2003;. in the press.
79. Bevington P.R., Robinson D.K. Data Reduction and Error Analysis for the Physical Sciences. 2nd edit. 1994;McGraw-Hill, New York.
80. Bushnell G.W., Louie G.V., Brayer G.D. High-resolution three-dimensional structure of horse heart cytochrome c. J. Mol. Biol. 214:1990;585-595.
81. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;945-949.