Chapter 3 Use of Protein Engineering Techniques to Elucidate Protein Folding Pathways

Progress in Nucleic Acid Research and Molecular Biology

Volumn 84, Issue , 2008, Pages 57-113

  Mallam, Anna L ^a   Jackson, Sophie E ^a  

^a Department of Chemistry ^*  (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

ANIMAL; CHEMISTRY; GENETICS; HUMAN; ISOMERISM; METABOLISM; METHODOLOGY; POINT MUTATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; REVIEW;

ANIMALS; HUMANS; ISOMERISM; POINT MUTATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 66149191304     PISSN: 00796603     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6603(08)00403-0     Document Type: Review

References (255)

1. Matthews C.R., Crisanti M.M., Manz J.T., and Gepner G.L. Effect of a single amino-acid substitution on the folding of the alpha-subunit of tryptophan synthase. Biochemistry 22 (1983) 1445-1452
2. Beasty A.M., Hurle M.R., Manz J.T., Stackhouse T., Onuffer J.J., and Matthews C.R. Effects of the phenylalanine-22-]leucine, glutamic acid-49-]methionine, glycine-234-]aspartic acid, and glycine-234-]lysine mutations on the folding and stability of the alpha-subunit of tryptophan synthase from Escherichia coli. Biochemistry 25 (1986) 2965-2974
3. Hurle M.R., Tweedy N.B., and Matthews C.R. Synergism in folding of a double mutant of the alpha-subunit of tryptophan synthase. Biochemistry 25 (1986) 6356-6360
4. Tweedy N.B., Hurle M.R., Chrunyk B.A., and Matthews C.R. Multiple replacements at position-211 in the alpha-subunit of tryptophan synthase as a probe of the folding unit association reaction. Biochemistry 29 (1990) 1539-1545
5. Beasty A.M., Hurle M.R., Manz J.T., Stackhouse T., and Matthews C.R. Mutagenesis as a probe of protein folding and stability. Protein Engineering. (1987), Alan R. Liss, New York 91-102
6. Matthews C.R. Effect of point mutations on the folding of globular-proteins. Methods Enzymol. 154 (1987) 498-511
7. Matthews C.R., and Hurle M.R. Mutant sequences as probes of protein folding mechanisms. Bioessays 6 (1987) 254-257
8. Perry K.M., Onuffer J.J., Touchette N.A., Herndon C.S., Gittelman M.S., Matthews C.R., Chen J.T., Mayer R.J., Taira K., Benkovic S.J., Howell E.E., and Kraut J. Effect of single amino-acid replacements on the folding and stability of dihydrofolate-reductase from Escherichia coli. Biochemistry 26 (1987) 2674-2682
9. Garvey E.P., and Matthews C.R. Effects of multiple replacements at a single position on the folding and stability of dihydrofolate-reductase from Escherichia coli. Biochemistry 28 (1989) 2083-2093
10. Perry K.M., Onuffer J.J., Gittelman M.S., Barmat L., and Matthews C.R. Long-range electrostatic interactions can influence the folding, stability, and cooperativity of dihydrofolate-reductase. Biochemistry 28 (1989) 7961-7968
11. Crisanti M.M., and Matthews C.R. Characterization of the slow steps in the folding of the alpha-subunit of tryptophan synthase. Biochemistry 20 (1981) 2700-2706
12. Matthews C.R., and Crisanti M.M. Urea-induced unfolding of the alpha-subunit of tryptophan synthase-Evidence for a multistate process. Biochemistry 20 (1981) 784-792
13. Touchette N.A., Perry K.M., and Matthews C.R. Folding of dihydrofolate-reductase from Escherichia coli. Biochemistry 25 (1986) 5445-5452
14. Matouschek A., Kellis J.T., Serrano L., Bycroft M., and Fersht A.R. Transient folding intermediates characterized by protein engineering. Nature 346 (1990) 440-445
15. Matouschek A., Kellis J.T., Serrano L., and Fersht A.R. Mapping the transition-state and pathway of protein folding by protein engineering. Nature 340 (1989) 122-126
16. Serrano L., Matouschek A., and Fersht A.R. The folding of an enzyme. III. Structure of the transition-state for unfolding of barnase analyzed by a protein engineering procedure. J. Mol. Biol. 224 (1992) 805-818
17. Matouschek A., and Fersht A.R. Protein engineering in analysis of protein folding pathways and stability. Methods Enzymol. 202 (1991) 82-112
18. Fersht A.R., Matouschek A., and Serrano L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224 (1992) 771-782
19. Fersht A.R., Kellis J.T., Matouschek A., and Serrano L. Folding pathway enigma-Reply. Nature 343 (1990) 602
20. Jackson S.E., and Fersht A.R. Folding of chymotrypsin inhibitor-2.1. Evidence for a 2-state transition. Biochemistry 30 (1991) 10428-10435
21. Jackson S.E., Elmasry N., and Fersht A.R. Structure of the hydrophobic core in the transition-state for folding of chymotrypsin inhibitor-2-A critical test of the protein engineering method of analysis. Biochemistry 32 (1993) 11270-11278
22. Otzen D.E., Itzhaki L.S., Elmasry N.F., Jackson S.E., and Fersht A.R. Structure of the transition-state for the folding/unfolding of the barley chymotrypsin inhibitor-2 and its implications for mechanisms of protein-folding. Proc. Natl. Acad. Sci. USA 91 (1994) 10422-10425
23. Itzhaki L.S., Otzen D.E., and Fersht A.R. The structure of the transition-state for folding of chymotrypsin inhibitor-2 analyzed by protein engineering methods-Evidence for a nucleation-condensation mechanism for protein-folding. J. Mol. Biol. 254 (1995) 260-288
24. Khorasanizadeh S., Peters I.D., and Roder H. Evidence for a three-state model of protein folding from kinetic analysis of ubiquitin variants with altered core residues. Nat. Struct. Biol. 3 (1996) 193-205
25. Jackson S.E. Ubiquitin: A small protein folding paradigm. Org. Biomol. Chem. 4 (2006) 1845-1853
26. Went H.M., and Jackson S.E. Ubiquitin folds through a highly polarized transition state. Protein Eng. Des. Sel. 18 (2005) 229-237
27. Campbell-Valois F.X., and Michnick S.W. The transition state of the ras binding domain of raf is structurally polarized based on phi-values but is energetically diffuse. J. Mol. Biol. 365 (2007) 1559-1577
28. Murzin A.G., Brenner S.E., Hubbard T., and Chothia C. Scop-A structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247 (1995) 536-540
29. Gu H.D., Kim D., and Baker D. Contrasting roles for symmetrically disposed beta-turns in the folding of a small protein. J. Mol. Biol. 274 (1997) 588-596
30. Kim D.E., Yi Q., Gladwin S.T., Goldberg J.M., and Baker D. The single helix in protein L is largely disrupted at the rate-limiting step in folding. J. Mol. Biol. 284 (1998) 807-815
31. Gu H., Doshi N., Kim D.E., Simons K.T., Santiago J.V., Nauli S., and Baker D. Robustness of protein folding kinetics to surface hydrophobic substitutions. Protein Sci. 8 (1999) 2734-2741
32. Kim D.E., Fisher C., and Baker D. A breakdown of symmetry in the folding transition state of protein L. J. Mol. Biol. 298 (2000) 971-984
33. McCallister E.L., Alm E., and Baker D. Critical role of beta-hairpin formation in protein G folding. Nat. Struct. Biol. 7 (2000) 669-673
34. Nauli S., Kuhlman B., and Baker D. Computer-based redesign of a protein folding pathway. Nat. Struct. Biol. 8 (2001) 602-605
35. Schymkowitz J.W.H., Rousseau F., Irvine L.R., and Itzhaki L.S. The folding pathway of the cell-cycle regulatory protein p13suc1: Clues for the mechanism of domain swapping. Structure 8 (2000) 89-100
36. Rousseau F., Schymkowitz J.W.H., Wilkinson H.R., and Itzhaki L.S. The structure of the transition state for folding of domain-swapped dimeric p13suc1. Structure 10 (2002) 649-657
37. Seeliger M.A., Breward S.E., and Itzhaki L.S. Weak cooperativity in the core causes a switch in folding mechanism between two proteins of the cks family. J. Mol. Biol. 325 (2003) 189-199
38. Viguera A.R., Villegas V., Aviles F.X., and Serrano L. Favourable native-like helical local interactions can accelerate protein folding. Fold. Des. 2 (1997) 23-33
39. Villegas V., Martinez J.C., Aviles F.X., and Serrano L. Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain. J. Mol. Biol. 283 (1998) 1027-1036
40. Chiti F., Taddei N., White P.M., Bucciantini M., Magherini F., Stefani M., and Dobson C.M. Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding. Nat. Struct. Biol. 6 (1999) 1005-1009
41. Ternstrom T., Mayor U., Akke M., and 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
42. Otzen D.E., and Oliveberg M. Conformational plasticity in folding of the split beta-alpha-beta protein S6: Evidence for burst-phase disruption of the native state. J. Mol. Biol. 317 (2002) 613-627
43. ‡). Proc. Natl. Acad. Sci. USA 101 (2004) 7606-7611
44. Raschke T.M., and Marqusee S. The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. Nat. Struct. Biol. 4 (1997) 298-304
45. Raschke T.M., Kho J., and Marqusee S. Confirmation of the hierarchical folding of RNase H: A protein engineering study. Nat. Struct. Biol. 6 (1999) 825-831
46. Spudich G., and Marqusee S. A change in the apparent m value reveals a populated intermediate under equilibrium conditions in Escherichia coli ribonuclease HI. Biochemistry 39 (2000) 11677-11683
47. Spudich G.M., Miller E.J., and Marqusee S. Destabilization of the Escherichia coli RNase H kinetic intermediate: Switching between a two-state and three-state folding mechanism. J. Mol. Biol. 335 (2004) 609-618
48. 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
49. Mayor U., Grossmann J.G., Foster N.W., Freund S.M.V., and Fersht A.R. The denatured state of engrailed homeodomain under denaturing and native conditions. J. Mol. Biol. 333 (2003) 977-991
50. Religa T.L., Johnson C.M., Vu D.M., Brewer S.H., Dyer R.B., and Fersht A.R. The helix-turn-helix motif as an ultrafast independently folding domain: The pathway of folding of Engrailed homeodomain. Proc. Natl. Acad. Sci. USA 104 (2007) 9272-9277
51. Mayor U., et al. The complete folding pathway of a protein from nanoseconds to microseconds. Nature 421 (2003) 863-867
52. Huang G.S., and Oas T.G. Submillisecond folding of monomeric lambda-repressor. Proc. Natl. Acad. Sci. USA 92 (1995) 6878-6882
53. Burton R.E., Huang G.S., Daugherty M.A., Calderone T.L., and Oas T.G. The energy landscape of a fast-folding protein mapped by Ala→Gly substitutions. Nat. Struct. Biol. 4 (1997) 305-310
54. Burton R.E., Huang G.S., Daugherty M.A., Fullbright P.W., and Oas T.G. Microsecond protein folding through a compact transition state. J. Mol. Biol. 263 (1996) 311-322
55. Burton R.E., Myers J.K., and Oas T.G. Protein folding dynamics: Quantitative comparison between theory and experiment. Biochemistry 37 (1998) 5337-5343
56. Myers J.K., and Oas T.G. Contribution of a buried hydrogen bond to lambda repressor folding kinetics. Biochemistry 38 (1999) 6761-6768
57. Kapp G.T., Richardson J.S., and Oas T.G. Kinetic role of helix caps in protein folding is context-dependent. Biochemistry 43 (2004) 3814-3823
58. Arora P., Oas T.G., and Myers J.K. Fast and faster: A designed variant of the B-domain of protein A folds in 3 mu sec. Protein Sci. 13 (2004) 847-853
59. Kragelund B.B., Osmark P., Neergaard T.B., Schiodt J., Kristiansen K., Knudsen J., and Poulsen F.M. The formation of a native-like structure containing eight conserved hydrophobic residues is rate limiting in two-state protein folding of ACBP. Nat. Struct. Biol. 6 (1999) 594-601
60. Teilum K., Thormann T., Caterer N.R., Poulsen H.I., Jensen P.H., Knudsen J., Kragelund B.B., and Poulsen F.M. Different secondary structure elements as scaffolds for protein folding transition states of two homologous four-helix bundles. Protein Struct. Funct. Bioinform. 59 (2005) 80-90
61. Ferguson N., Li W., Capaldi A.P., Kleanthous C., and Radford S.E. Using chimeric immunity proteins to explore the energy landscape for alpha-helical protein folding. J. Mol. Biol. 307 (2001) 393-405
62. Capaldi A.P., Kleanthous C., and Radford S.E. Im7 folding mechanism: Misfolding on a path to the native state. Nat. Struct. Biol. 9 (2002) 209-216
63. Friel C.T., Capaldi A.P., and Radford S.E. Structural analysis of the rate-limiting transition states in the folding of lm7 and lm9: Similarities and differences in the folding of homologous proteins. J. Mol. Biol. 326 (2003) 293-305
64. Spence G.R., Capaldi A.P., and Radford S.E. Trapping the on-pathway folding intermediate of Im7 at equilibrium. J. Mol. Biol. 341 (2004) 215-226
65. Whittaker S.B.M., Spence G.R., Grossmann J.G., Radford S.E., and Moore G.R. NMR analysis of the conformational properties of the trapped on-pathway folding intermediate of the bacterial immunity protein Im7. J. Mol. Biol. 366 (2007) 1001-1015
66. Friel C.T., Beddard G.S., and Radford S.E. Switching two-state to three-state kinetics in the helical protein Im9 via the optimisation of stabilising non-native interactions by design. J. Mol. Biol. 342 (2004) 261-273
67. Cranz-Mileva S., Friel C.T., and Radford S.E. Helix stability and hydrophobicity in the folding mechanism of the bacterial immunity protein Im9. Protein Eng. Des. Sel. 18 (2005) 41-50
68. Morton V.L., Friel C.T., Allen L.R., Paci E., and Radford S.E. The effect of increasing the stability of non-native interactions on the folding landscape of the bacterial immunity protein Im9. J. Mol. Biol. 371 (2007) 554-568
69. Hackenberger C.P.R., Friel C.T., Radford S.E., and Imperiali B. Semisynthesis of a glycosylated lm7 analogue for protein folding studies. J. Am. Chem. Soc. 127 (2005) 12882-12889
70. Scott K.A., and Clarke J. Spectrin R16: Broad energy barrier or sequential transition states?. Protein Sci. 14 (2005) 1617-1629
71. Scott K.A., Randles L.G., and Clarke J. The folding of spectrin domains II: Phi-value analysis of R16. J. Mol. Biol. 344 (2004) 207-221
72. Scott K.A., Randles L.G., Moran S.J., Daggett V., and Clarke J. The folding pathway of spectrin R17 from experiment and simulation: Using experimentally validated MD simulations to characterize states hinted at by experiment. J. Mol. Biol. 359 (2006) 159-173
73. Grantcharova V.P., Riddle D.S., Santiago J.V., and Baker D. Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat. Struct. Biol. 5 (1998) 714-720
74. Riddle D.S., Grantcharova V.P., Santiago J.V., Alm E., Ruczinski I., and Baker D. Experiment and theory highlight role of native state topology in SH3 folding. Nat. Struct. Biol. 6 (1999) 1016-1024
75. Grantcharova V.P., Riddle D.S., and Baker D. Long-range order in the src SH3 folding transition state. Proc. Natl. Acad. Sci. USA 97 (2000) 7084-7089
76. Martinez J.C., and Serrano L. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nat. Struct. Biol. 6 (1999) 1010-1016
77. Viguera A.R., Vega C., and Serrano L. Unspecific hydrophobic stabilization of folding transition states. Proc. Natl. Acad. Sci. USA 99 (2002) 5349-5354
78. Fernandez-Escamilla A.M., Cheung M.S., Vega M.C., Wilmanns M., Onuchic J.N., and Serrano L. Solvation in protein folding analysis: Combination of theoretical and experimental approaches. Proc. Natl. Acad. Sci. USA 101 (2004) 2834-2839
79. Guerois R., and Serrano L. The SH3-fold family: Experimental evidence and prediction of variations in the folding pathways. J. Mol. Biol. 304 (2000) 967-982
80. Northey J.G.B., Di Nardo A.A., and Davidson A.R. Hydrophobic core packing in the SH3 domain folding transition state. Nat. Struct. Biol. 9 (2002) 126-130
81. Northey J.G.B., Maxwell K.L., and Davidson A.R. Protein folding kinetics beyond the Phi value: Using multiple amino acid substitutions to investigate the structure of the SH3 domain folding transition state. J. Mol. Biol. 320 (2002) 389-402
82. Di Nardo A.A., Korzhnev D.M., Stogios P.J., Zarrine-Afsar A., Kay L.E., and Davidson A.R. Dramatic acceleration of protein folding by stabilization of a non-native backbone conformation. Proc. Natl. Acad. Sci. USA 101 (2004) 7954-7959
83. Korzhnev D.M., Salvatella X., Vendruscolo M., Di Nardo A.A., Davidson A.R., Dobson C.M., and Kay L.E. Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430 (2004) 586-590
84. Neudecker P., Zarrine-Afsar A., Choy W.Y., Muhandiram D.R., Davidson A.R., and Kay L.E. Identification of a collapsed intermediate with non-native long-range interactions on the folding pathway of a pair of Fyn SH3 domain mutants by NMR relaxation dispersion spectroscopy. J. Mol. Biol. 363 (2006) 958-976
85. Neudecker P., Zarrine-Afsar A., Davidson A.R., and Kay L.E. Phi-Value analysis of a three-state protein folding pathway by NMR relaxation dispersion spectroscopy. Proc. Natl. Acad. Sci. USA 104 (2007) 15717-15722
86. 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
87. Garcia-Mira M.M., and Schmid F.X. Key role of coulombic interactions for the folding transition state of the cold shock protein. J. Mol. Biol. 364 (2006) 458-468
88. Crane J.C., Koepf E.K., Kelly J.W., and Gruebele M. Mapping the transition state of the WW domain beta-sheet. J. Mol. Biol. 298 (2000) 283-292
89. Nguyen H., Jager M., Kelly J.W., and Gruebele M. Engineering beta-sheet protein toward the folding speed limit. J. Phys. Chem. B 109 (2005) 15182-15186
90. Jager M., Nguyen H., Crane J.C., Kelly J.W., and Gruebele M. The folding mechanism of a beta-sheet: The WW domain. J. Mol. Biol. 311 (2001) 373-393
91. Jager M., et al. Structure-function-folding relationship in a WW domain. Proc. Natl. Acad. Sci. USA 103 (2006) 10648-10653
92. Schreiber C., Buckle A.M., and Fersht A.R. Stability and function-Two constraints in the evolution of barstar and other proteins. Structure 2 (1994) 945-951
93. Deechongkit S., Nguyen H., Powers E.T., Dawson P.E., Gruebele M., and Kelly J.W. Context-dependent contributions of backbone hydrogen bonding to beta-sheet folding energetics. Nature 430 (2004) 101-105
94. Ferguson N., et al. Using flexible loop mimetics to extend Phi-value analysis to secondary structure interactions. Proc. Natl. Acad. Sci. USA 98 (2001) 13008-13013
95. Petrovich M., Jonsson A.L., Ferguson N., Daggett V., and Fersht A.R. phi-Analysis at the experimental limits: Mechanism of beta-hairpin formation. J. Mol. Biol. 360 (2006) 865-881
96. Hamill S.J., Steward A., and Clarke J. The folding of an immunoglobulin-like Greek key protein is defined by a common-core nucleus and regions constrained by topology. J. Mol. Biol. 297 (2000) 165-178
97. Cota E., Steward A., Fowler S.B., and Clarke J. The folding nucleus of a fibronectin type III domain is composed of core residues of the immunoglobulin-like fold. J. Mol. Biol. 305 (2001) 1185-1194
98. Fowler S.B., and Clarke J. Mapping the folding pathway of an immunoglobulin domain: Structural detail from phi value analysis and movement of the transition state. Structure 9 (2001) 355-366
99. Wright C.F., Christodoulou J., Dobson C.M., and Clarke J. The importance of loop length in the folding of an immunoglobulin domain. Protein Eng. Des. Sel. 17 (2004) 443-453
100. Lappalainen I., Hurley M.G., and Clarke J. Plasticity within the obligatory folding nucleus of an immunoglobulin-like domain. J. Mol. Biol. 375 (2008) 547-559
101. Billings K.S., Best R.B., Rutherford T.J., and Clarke J. Crosstalk between the protein surface and hydrophobic core in a core-swapped fibronectin type III domain. J. Mol. Biol. 375 (2008) 560-571
102. Lorch M., Mason J.M., Clarke A.R., and Parker M.J. Effects of core mutations on the folding of a beta-sheet protein: Implications for backbone organization in the I-State. Biochemistry 38 (1999) 1377-1385
103. Lorch M., Mason J.M., Sessions R.B., and Clarke A.R. Effects of mutations on the thermodynamics of a protein folding reaction: Implications for the mechanism of formation of the intermediate and transition states. Biochemistry 39 (2000) 3480-3485
104. Poso D., Sessions R.B., Lorch M., and Clarke A.R. Progressive stabilization of intermediate and transition states in protein folding reactions by introducing surface hydrophobic residues. J. Biol. Chem. 275 (2000) 35723-35726
105. Fersht A.R. Relationship of Leffler (Bronsted) alpha values and protein folding Phi values to position of transition-state structures on reaction coordinates. Proc. Natl. Acad. Sci. USA 101 (2004) 14338-14342
106. Fersht A.R., Itzhaki L.S., El Masry N.F., Matthews J.M., and Otzen D.E. Single versus parallel pathways of protein-folding and fractional formation of structure in the transition-state. Proc. Natl. Acad. Sci. USA 91 (1994) 10426-10429
107. Sosnick T.R., Krantz B.A., Dothager R.S., and Baxa M. Characterizing the protein folding transition state using psi analysis. Chem. Rev. 106 (2006) 1862-1876
108. Krantz B.A., and Sosnick T.R. Engineered metal binding sites map the heterogeneous folding landscape of a coiled coil. Nat. Struct. Biol. 8 (2001) 1042-1047
109. Krantz B.A., Dothager R.S., and Sosnick T.R. Discerning the structure and energy of multiple transition states in protein folding using psi-analysis. J. Mol. Biol. 337 (2004) 463-475
110. Krantz B.A., Dothager R.S., and Sosnick T.R. Discerning the structure and energy of multiple transition states in protein folding using psi-analysis. J. Mol. Biol. 347 (2004) 463-475
111. Moran L.B., Schneider J.P., Kentsis A., Reddy G.A., and Sosnick T.R. Transition state heterogeneity in GCN4 coiled coil folding studied by using multisite mutations and crosslinking. Proc. Natl. Acad. Sci. USA 96 (1999) 10699-10704
112. Fersht A.R. Phi value versus psi analysis. Proc. Natl. Acad. Sci. USA 101 (2004) 17327-17328
113. Lin L.N., and Brandts J.F. Further evidence suggesting that slow phase in protein unfolding and refolding is due to proline isomerization-Kinetic study of carp parvalbumins. Biochemistry 17 (1978) 4102-4110
114. Brandts J.F., Brennan M., and Lin L.N. Unfolding and refolding occur much faster for a proline-free protein than for most proline-containing proteins. Proc. Natl. Acad. Sci. USA 74 (1977) 4178-4181
115. Brandts J.F., Halvorson H.R., and Brennan M. Consideration of possibility that slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry 14 (1975) 4953-4963
116. Engel J., and Bachinger H.P. Structure, stability and folding of the collagen triple helix. Collagen 247 (2005) 7-33
117. Kiefhaber T., Grunert H.P., Hahn U., and Schmid F.X. Replacement of a cis proline simplifies the mechanism of ribonuclease-T1 folding. Biochemistry 29 (1990) 6475-6480
118. Schreiber G., and Fersht A.R. The refolding of cis-peptidylprolyl and trans-peptidylprolyl isomers of barstar. Biochemistry 32 (1993) 11195-11203
119. Schultz D.A., Schmid F.X., and Baldwin R.L. Cis proline mutants of ribonuclease-a.2. Elimination of the slow-folding forms by mutation. Protein Sci. 1 (1992) 917-924
120. Munoz V., Lopez E.M., Jager M., and Serrano L. Kinetic characterization of the chemotactic protein from Escherichia coli, chey-Kinetic-analysis of the inverse hydrophobic effect. Biochemistry 33 (1994) 5858-5866
121. Eyles S.J., and Gierasch L.M. Multiple roles of prolyl residues in structure and folding. J. Mol. Biol. 301 (2000) 737-747
122. Burns-Hamuro L.L., Dalessio P.M., and Ropson I.J. Replacement of proline with valine does not remove an apparent proline isomerization-dependent folding event in CRABP I. Protein Sci. 13 (2004) 1670-1676
123. Kamen D.E., and Woody R.W. Identification of proline residues responsible for the slow folding kinetics in pectate lyase C by mutagenesis. Biochemistry 41 (2002) 4724-4732
124. Maki K., Ikura T., Hayano T., Takahashi N., and Kuwajima K. Effects of proline mutations on the folding of staphylococcal nuclease. Biochemistry 38 (1999) 2213-2223
125. Kuwajima K., Okayama N., Yamamoto K., Ishihara T., and Sugai S. The Pro117 to glycine mutation of staphylococcal nuclease simplifies the unfolding folding kinetics. FEBS Lett. 290 (1991) 135-138
126. Rousseau F., Schymkowitz J.W.H., del Pino M.S., and Itzhaki L.S. Stability and folding of the cell cycle regulatory protein, p13(suc1). J. Mol. Biol. 284 (1998) 503-519
127. Main E.R., Jackson S.E., and Regan L. The folding and design of repeat proteins: Reaching a consensus. Curr. Opin. Struct. Biol. 13 (2003) 482-489
128. Main E.R., Lowe A.R., Mochrie S.G., Jackson S.E., and Regan L. A recurring theme in protein engineering: The design, stability and folding of repeat proteins. Curr. Opin. Struct. Biol. 15 (2005) 464-471
129. Barrick D., Ferreiro D.U., and Komives E.A. Folding landscapes of ankyrin repeat proteins: Experiments meet theory. Curr. Opin. Struct. Biol. 18 (2008) 27-34
130. Low C., Weininger U., Zeeb M., Zhang W., Laue E.D., Schmid F.X., and Balbach J. Folding mechanism of an ankyrin repeat protein: Scaffold and active site formation of human CDK inhibitor p19(INK4d). J. Mol. Biol. 373 (2007) 219-231
131. Tang K.S., Fersht A.R., and Itzhaki L.S. Sequential unfolding of ankyrin repeats in tumor suppressor p16. Structure 11 (2003) 67-73
132. Mosavi L.K., Cammett T.J., Desrosiers D.C., and Peng Z.Y. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 13 (2004) 1435-1448
133. Interlandi G., Settanni G., and Caflisch A. Unfolding transition state and intermediates of the tumor suppressor p16INK4a investigated by molecular dynamics simulations. Proteins 64 (2006) 178-192
134. Lowe A.R., and Itzhaki L.S. Rational redesign of the folding pathway of a modular protein. Proc. Natl. Acad. Sci. USA 104 (2007) 2679-2684
135. Truhlar M.E., and Komives E.A. LRR domain folding: Just put a cap on it!. Structure 16 (2008) 655-657
136. Courtemanche N., and Barrick D. The leucine-rich repeat domain of internalin B folds along a polarized N-terminal pathway. Structure 16 (2008) 705-714
137. Mello C.C., and Barrick D. An experimentally determined protein folding energy landscape. Proc. Natl. Acad. Sci. USA 101 (2004) 14102-14107
138. Zhang B., and Peng Z. A minimum folding unit in the ankyrin repeat protein p16(INK4). J. Mol. Biol. 299 (2000) 1121-1132
139. Zweifel M.E., and Barrick D. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. II. Solution stability and cooperativity of unfolding. Biochemistry 40 (2001) 14357-14367
140. Tripp K.W., and Barrick D. The tolerance of a modular protein to duplication and deletion of internal repeats. J. Mol. Biol. 344 (2004) 169-178
141. Street T.O., Bradley C.M., and Barrick D. Predicting coupling limits from an experimentally determined energy landscape. Proc. Natl. Acad. Sci. USA 104 (2007) 4907-4912
142. Ferreiro D.U., Cho S.S., Komives E.A., and Wolynes P.G. The energy landscape of modular repeat proteins: Topology determines folding mechanism in the ankyrin family. J. Mol. Biol. 354 (2005) 679-692
143. Werbeck N.D., and Itzhaki L.S. Probing a moving target with a plastic unfolding intermediate of an ankyrin-repeat protein. Proc. Natl. Acad. Sci. USA 104 (2007) 7863-7868
144. Kajander T., Cortajarena A.L., and Regan L. Consensus design as a tool for engineering repeat proteins. Methods Mol. Biol. 340 (2006) 151-170
145. Binz H.K., Stumpp M.T., Forrer P., Amstutz P., and Pluckthun A. Designing repeat proteins: Well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J. Mol. Biol. 332 (2003) 489-503
146. Kohl A., Binz H.K., Forrer P., Stumpp M.T., Pluckthun A., and Grutter M.G. Designed to be stable: Crystal structure of a consensus ankyrin repeat protein. Proc. Natl. Acad. Sci. USA 100 (2003) 1700-1705
147. Main E.R., Xiong Y., Cocco M.J., D'Andrea L., and Regan L. Design of stable alpha-helical arrays from an idealized TPR motif. Structure 11 (2003) 497-508
148. Mosavi L.K., Minor Jr. D.L., and Peng Z.Y. Consensus-derived structural determinants of the ankyrin repeat motif. Proc. Natl. Acad. Sci. USA 99 (2002) 16029-16034
149. Stumpp M.T., Forrer P., Binz H.K., and Pluckthun A. Designing repeat proteins: Modular leucine-rich repeat protein libraries based on the mammalian ribonuclease inhibitor family. J. Mol. Biol. 332 (2003) 471-487
150. Wetzel S.K., Settanni G., Kenig M., Binz H.K., and Pluckthun A. Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J. Mol. Biol. 376 (2008) 241-257
151. Parmeggiani F., Pellarin R., Larsen A.P., Varadamsetty G., Stumpp M.T., Zerbe O., Caflisch A., and Pluckthun A. Designed armadillo repeat proteins as general peptide-binding scaffolds: Consensus design and computational optimization of the hydrophobic core. J. Mol. Biol. 376 (2008) 1282-1304
152. Tripp K.W., and Barrick D. Folding by consensus. Structure 11 (2003) 486-487
153. Tripp K.W., and Barrick D. Enhancing the stability and folding rate of a repeat protein through the addition of consensus repeats. J. Mol. Biol. 365 (2007) 1187-1200
154. Ferreiro D.U., Cervantes C.F., Truhlar S.M., Cho S.S., Wolynes P.G., and Komives E.A. Stabilizing IkappaBalpha by "consensus" design. J. Mol. Biol. 365 (2007) 1201-1216
155. Main E.R., Stott K., Jackson S.E., and Regan L. Local and long-range stability in tandemly arrayed tetratricopeptide repeats. Proc. Natl. Acad. Sci. USA 102 (2005) 5721-5726
156. Goldenberg D.P., and Creighton T.E. Circular and circularly permuted forms of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 165 (1983) 407-413
157. Luger K., Hommel U., Herold M., Hofsteenge J., and Kirschner K. Correct folding of circularly permuted variants of a beta alpha barrel enzyme in vivo. Science 243 (1989) 206-210
158. Viguera A.R., Blanco F.J., and Serrano L. The order of secondary structure elements does not determine the structure of a protein but does affect its folding kinetics. J. Mol. Biol. 247 (1995) 670-681
159. Viguera A.R., Serrano L., and Wilmanns M. Different folding transition states may result in the same native structure. Nat. Struct. Biol. 3 (1996) 874-880
160. Martinez J.C., Viguera A.R., Berisio R., Wilmanns M., Mateo P.L., Filimonov V.V., and Serrano L. Thermodynamic analysis of alpha-spectrin SH3 and two of its circular permutants with different loop lengths: Discerning the reasons for rapid folding in proteins. Biochemistry 38 (1999) 549-559
161. Otzen D.E., and Fersht A.R. Folding of circular and permuted chymotrypsin inhibitor 2: Retention of the folding nucleus. Biochemistry 37 (1998) 8139-8146
162. Iwakura M., Nakamura T., Yamane C., and Maki K. Systematic circular permutation of an entire protein reveals essential folding elements. Nat. Struct. Biol. 7 (2000) 580-585
163. Arai M., Maki K., Takahashi H., and Iwakura M. Testing the relationship between foldability and the early folding events of dihydrofolate reductase from Escherichia coli. J. Mol. Biol. 328 (2003) 273-288
164. Hennecke J., Sebbel P., and Glockshuber R. Random circular permutation of DsbA reveals segments that are essential for protein folding and stability. J. Mol. Biol. 286 (1999) 1197-1215
165. Lindberg M., Tangrot J., and Oliveberg M. Complete change of the protein folding transition state upon circular permutation. Nat. Struct. Biol. 9 (2002) 818-822
166. Lindberg M.O., Tangrot J., Otzen D.E., Dolgikh D.A., Finkelstein A.V., and Oliveberg M. Folding of circular permutants with decreased contact order: General trend balanced by protein stability. J. Mol. Biol. 314 (2001) 891-900
167. Miller E.J., Fischer K.F., and Marqusee S. Experimental evaluation of topological parameters determining protein-folding rates. Proc. Natl. Acad. Sci. USA 99 (2002) 10359-10363
168. Lindberg M.O., Haglund E., Hubner I.A., Shakhnovich E.I., and Oliveberg M. Identification of the minimal protein-folding nucleus through loop-entropy perturbations. Proc. Natl. Acad. Sci. USA 103 (2006) 4083-4088
169. Olofsson M., Hansson S., Hedberg L., Logan D.T., and Oliveberg M. Folding of S6 structures with divergent amino acid composition: Pathway flexibility within partly overlapping foldons. J. Mol. Biol. 365 (2007) 237-248
170. Iwakura M., and Nakamura T. Effects of the length of a glycine linker connecting the N- and C-termini of a circularly permuted dihydrofolate reductase. Protein Eng. 11 (1998) 707-713
171. Lindberg M.O., and Oliveberg M. Malleability of protein folding pathways: A simple reason for complex behaviour. Curr. Opin. Struct. Biol. 17 (2007) 21-29
172. Han J.H., Batey S., Nickson A.A., Teichmann S.A., and Clarke J. The folding and evolution of multidomain proteins. Nat. Rev. Mol. Cell. Biol. 8 (2007) 319-330
173. Ekman D., Bjorklund A.K., Frey-Skott J., and Elofsson A. Multi-domain proteins in the three kingdoms of life: Orphan domains and other unassigned regions. J. Mol. Biol. 348 (2005) 231-243
174. Jackson S.E. How do small single-domain proteins fold?. Fold. Des. 3 (1998) R81-R91
175. Daggett V., and Fersht A. The present view of the mechanism of protein folding. Nat. Rev. Mol. Cell. Biol. 4 (2003) 497-502
176. Daggett V., and Fersht A.R. Is there a unifying mechanism for protein folding?. Trends Biochem. Sci. 28 (2003) 18-25
177. Zarrine-Afsar A., Larson S.M., and Davidson A.R. The family feud: Do proteins with similar structures fold via the same pathway?. Curr. Opin. Struct. Biol. 15 (2005) 42-49
178. Steward A., Toca-Herrera J.L., and Clarke J. Versatile cloning system for construction of multimeric proteins for use in atomic force microscopy. Protein Sci. 11 (2002) 2179-2183
179. Batey S., and Clarke J. Apparent cooperativity in the folding of multidomain proteins depends on the relative rates of folding of the constituent domains. Proc. Natl. Acad. Sci. USA 103 (2006) 18113-18118
180. Arora P., Hammes G.G., and Oas T.G. Folding mechanism of a multiple independently-folding domain protein: Double B domain of protein A. Biochemistry 45 (2006) 12312-12324
181. Hamill S.J., Meekhof A.E., and Clarke J. The effect of boundary selection on the stability and folding of the third fibronectin type III domain from human tenascin. Biochemistry 37 (1998) 8071-8079
182. Batey S., Randles L.G., Steward A., and Clarke J. Cooperative folding in a multi-domain protein. J. Mol. Biol. 349 (2005) 1045-1059
183. Batey S., Scott K.A., and Clarke J. Complex folding kinetics of a multidomain protein. Biophys. J. 90 (2006) 2120-2130
184. Osvath S., Kohler G., Zavodszky P., and Fidy J. Asymmetric effect of domain interactions on the kinetics of folding in yeast phosphoglycerate kinase. Protein Sci. 14 (2005) 1609-1616
185. Wenk M., Jaenicke R., and Mayr E.M. Kinetic stabilisation of a modular protein by domain interactions. FEBS Lett. 438 (1998) 127-130
186. Jager M., Gehrig P., and Pluckthun A. The scFv fragment of the antibody hu4D5-8: Evidence for early premature domain interaction in refolding. J. Mol. Biol. 305 (2001) 1111-1129
187. Batey S., and Clarke J. The folding pathway of a single domain in a multidomain protein is not affected by its neighbouring domain. J. Mol. Biol. 378 2 (2008) 297-301
188. Scott K.A., Steward A., Fowler S.B., and Clarke J. Titin; a multidomain protein that behaves as the sum of its parts. J. Mol. Biol. 315 (2002) 819-829
189. Steward A., Adhya S., and Clarke J. Sequence conservation in Ig-like domains: The role of highly conserved proline residues in the fibronectin type III superfamily. J. Mol. Biol. 318 (2002) 935-940
190. Robertsson J., Petzold K., Lofvenberg L., and Backman L. Folding of spectrin's SH3 domain in the presence of spectrin repeats. Cell. Mol. Biol. Lett. 10 (2005) 595-612
191. Jaenicke R., and Lilie H. Folding and association of oligomeric and multimeric proteins. Adv. Protein Chem. 53 (2000) 329-401
192. Milla M.E., Brown B.M., Waldburger C.D., and Sauer R.T. P22 Arc repressor: Transition state properties inferred from mutational effects on the rates of protein unfolding and refolding. Biochemistry 34 (1995) 13914-13919
193. Milla M.E., and Sauer R.T. P22 Arc repressor: Folding kinetics of a single-domain, dimeric protein. Biochemistry 33 (1994) 1125-1133
194. Doyle S.M., Bilsel O., and Teschke C.M. SecA folding kinetics: A large dimeric protein rapidly forms multiple native states. J. Mol. Biol. 341 (2004) 199-214
195. Mallam A.L., and Jackson S.E. Probing Nature's knots: The folding pathway of a knotted homodimeric protein. J. Mol. Biol. 359 (2006) 1420-1436
196. Mallam A.L., and Jackson S.E. The dimerization of an alpha/beta-knotted protein is essential for structure and function. Structure 15 (2007) 111-122
197. Shao X., Hensley P., and Matthews C.R. Construction and characterization of monomeric tryptophan repressor: A model for an early intermediate in the folding of a dimeric protein. Biochemistry 36 (1997) 9941-9949
198. Mallam A.L., Onuoha S.C., Grossmann J.G., and Jackson S.E. Knotted fusion proteins reveal unexpected possibilities in protein folding. Mol. Cell 30 5 (2008) 642-648
199. Randles L.G., Batey S., Steward A., and Clarke J. Distinguishing specific and nonspecific interdomain interactions in multidomain proteins. Biophys. J. 94 (2008) 622-628
200. Khorasanizadeh S., Peters I.D., Butt T.R., and Roder H. Folding and stability of a tryptophan-containing mutant of ubiquitin. Biochemistry 32 (1993) 7054-7063
201. Vallee-Belisle A., and Michnick S.W. Multiple tryptophan probes reveal that ubiquitin folds via a late misfolded intermediate. J. Mol. Biol. 374 (2007) 791-805
202. Krantz B.A., and Sosnick T.R. Distinguishing between two-state and three-state models for ubiquitin folding. Biochemistry 39 (2000) 11696-11701
203. Ghaemmaghami S., Word J.M., Burton R.E., Richardson J.S., and Oas T.G. Folding kinetics of a fluorescent variant of monomeric lambda repressor. Biochemistry 37 (1998) 9179-9185
204. Dimitriadis G., Drysdale A., Myers J.K., Arora P., Radford S.E., Oas T.G., and Smith D.A. Microsecond folding dynamics of the F13W G29A mutant of the B domain of staphylococcal protein A by laser-induced temperature jump. Proc. Natl. Acad. Sci. USA 101 (2004) 3809-3814
205. Smith C.J., Clarke A.R., Chia W.N., Irons L.I., Atkinson T., and Holbrook J.J. Detection and characterization of intermediates in the folding of large proteins by the use of genetically inserted tryptophan probes. Biochemistry 30 (1991) 1028-1036
206. Staniforth R.A., Burston S.G., Smith C.J., Jackson G.S., Badcoe I.G., Atkinson T., Holbrook J.J., and Clarke A.R. The energetics and cooperativity of protein folding-A simple experimental-analysis based upon the solvation of internal residues. Biochemistry 32 (1993) 3842-3851
207. Clark P.L., Weston B.F., and Gierasch L.M. Probing the folding pathway of a beta-clam protein with single-tryptophan constructs. Fold. Des. 3 (1998) 401-412
208. Clark P.L., Liu Z.P., Zhang J.H., and Gierasch L.M. Intrinsic tryptophans of CRABPI as probes of structure and folding. Protein Sci. 5 (1996) 1108-1117
209. Dalessio P.M., Fromholt S.E., and Ropson I.J. The role of Trp-82 in the folding of intestinal fatty acid binding protein. Protein Struct. Funct. Bioinform. 61 (2005) 176-183
210. Dalessio P.M., Boyer J.A., McGettigan J.L., and Ropson I.J. Swapping core residues in homologous proteins swaps folding mechanism. Biochemistry 44 (2005) 3082-3090
211. Yeh S.R., Ropson I.J., and Rousseau D.L. Hierarchical folding of intestinal fatty acid binding protein. Biochemistry 40 (2001) 4205-4210
212. Chattopadhyay K., Saffarian S., Elson E.L., and Frieden C. Measurement of microsecond dynamic motion in the intestinal fatty acid binding protein by using fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA 99 (2002) 14171-14176
213. Scheraga H.A., Wedemeyer W.J., and Welker E. Bovine pancreatic ribonuclease A: Oxidative and conformational folding studies. Ribonucleases, Pt A 341 (2001) 189-221
214. Narayan M., Welker E., Wedemeyer W.J., and Scheraga H.A. Oxidative folding of proteins. Acc. Chem. Res. 33 (2000) 805-812
215. Wedemeyer W.J., Welker E., Narayan M., and Scheraga H.A. Disulfide bonds and protein folding. Biochemistry 39 (2000) 4207-4216
216. Goldenberg D.P. Native and nonnative intermediates in the Bpti folding pathway. Trends Biochem. Sci. 17 (1992) 257-261
217. Mason J.M., Gibbs N., Sessions R.B., and Clarke A.R. The influence of intramolecular bridges on the dynamics of a protein folding reaction. Biochemistry 41 (2002) 12093-12099
218. Mason J.M., Cliff M.J., Sessions R.B., and Clarke A.R. Low energy pathways and non-native interactions-The influence of artificial disulfide bridges on the mechanism of folding. J. Biol. Chem. 280 (2005) 40494-40499
219. Kufer S.K., Dietz H., Albrecht C., Blank K., Kardinal A., Rief M., and Gaub H.E. Covalent immobilization of recombinant fusion proteins with hAGT for single molecule force spectroscopy. Eur. Biophys. J. 35 (2005) 72-78
220. Best R.B., Brockwell D.J., Toca-Herrera J.L., Blake A.W., Smith D.A., Radford S.E., and Clarke J. Force mode atomic force microscopy as a tool for protein folding studies. Anal. Chim. Acta 479 (2003) 87-105
221. Forman J.R., and Clarke J. Mechanical unfolding of proteins: Insights into biology, structure and folding. Curr. Opin. Struct. Biol. 17 (2007) 58-66
222. Fisher T.E., Marszalek P.E., and Fernandez J.M. Stretching single molecules into novel conformations using the atomic force microscope. Nat. Struct. Biol. 7 (2000) 719-724
223. Fisher T.E., Oberhauser A.F., Carrion-Vazquez M., Marszalek P.E., and Fernandez J.M. The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24 (1999) 379-384
224. Carrion-Vazquez M., Oberhauser A.F., Fisher T.E., Marszalek P.E., Li H.B., and Fernandez J.M. Mechanical design of proteins-studied by single-molecule force spectroscopy and protein engineering. Prog. Biophys. Mol. Biol. 74 (2000) 63-91
225. Best R.B., Fowler S.B., Toca-Herrera J.L., and Clarke J. A simple method for probing the mechanical unfolding pathway of proteins in detail. Proc. Natl. Acad. Sci. USA 99 (2002) 12143-12148
226. Ng S.P., Rounsevell R.W.S., Steward A., Geierhaas C.D., Williams P.M., Paci E., and Clarke J. Mechanical unfolding of TNfn3: The unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation. J. Mol. Biol. 350 (2005) 776-789
227. Kim Y.G., Ho S.O., Gassman N.R., Korlann Y., Landorf E.V., Collart F.R., and Weiss S. Efficient site-specific labeling of proteins via cysteines. Bioconjug. Chem. 19 (2008) 786-791
228. Jager M., Nir E., and Weiss S. Site-specific labeling of proteins for single-molecule FRET by combining chemical and enzymatic modification. Protein Sci. 15 (2006) 640-646
229. Jager M., Michalet X., and Weiss S. Protein-protein interactions as a tool for site-specific labeling of proteins. Protein Sci. 14 (2005) 2059-2068
230. Deniz A.A., et al. Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc. Natl. Acad. Sci. USA 97 (2000) 5179-5184
231. 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
232. Kuzmenkina E.V., Heyes C.D., and Nienhaus G.U. Single-molecule FRET study of denaturant induced unfolding of RNase H. J. Mol. Biol. 357 (2006) 313-324
233. 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
234. Groll J., Amirgoulova E.V., Ameringer T., Heyes C.D., Rocker C., Nienhaus G.U., and Moller M. Biofunctionalized, ultrathin coatings of cross-linked star-shaped poly (ethylene oxide) allow reversible folding of immobilized proteins. J. Am. Chem. Soc. 126 (2004) 4234-4239
235. Tezuka-Kawakami T., Gell C., Brockwell D.J., Radford S.E., and Smith D.A. Urea-induced unfolding of the immunity protein Im9 monitored by spFRET. Biophys. J. 91 (2006) L42-L44
236. Rhoades E., Gussakovsky E., and Haran G. Watching proteins fold one molecule at a time. Proc. Natl. Acad. Sci. USA 100 (2003) 3197-3202
237. Huang F., Sato S., Sharpe T.D., Ying L.M., and Fersht A.R. Distinguishing between cooperative and unimodal downhill protein folding. Proc. Natl. Acad. Sci. USA 104 (2007) 123-127
238. Lipman E.A., Schuler B., Bakajin O., and Eaton W.A. Single-molecule measurement of protein folding kinetics. Science 301 (2003) 1233-1235
239. Schuler B., and Eaton W.A. Protein folding studied by single-molecule FRET. Curr. Opin. Struct. Biol. 18 (2008) 16-26
240. Hamadani K.M., and Weiss S. Nonequilibrium single molecule protein folding in a coaxial mixer. Biophysic. J. 95 (2008) 352-365
241. Kinoshita M., Kamagata K., Maeda A., Goto Y., Komatsuzaki T., and Takahashi S. Development of a technique for the investigation of folding dynamics of single proteins for extended time periods. Proc. Natl. Acad. Sci. USA 104 (2007) 10453-10458
242. Chirico G., Cannone F., and Diaspro A. Unfolding time distribution of GFP by single molecule fluorescence spectroscopy. Eur. Biophys. J. 35 (2006) 663-674
243. Baldini G., Cannone F., Chirico G., Collini M., Campanini B., Bettati S., and Mozzarelli A. Evidence of discrete substates and unfolding pathways in green fluorescent protein. Biophysic. J. 92 (2007) 1724-1731
244. Orte A., Craggs T.D., White S.S., Jackson S.E., and Klenerman D. Evidence of an intermediate and parallel pathways in protein unfolding from single-molecule fluorescence. J. Am. Chem. Soc. 130 (2008) 7898-7907
245. Michalet X., Weiss S., and Jager M. Single-molecule fluorescence studies of protein folding and conformational dynamics. Chem. Rev. 106 (2006) 1785-1813
246. Nienhaus G.U. Exploring protein structure and dynamics under denaturing conditions by single-molecule FRET analysis. Macromol. Biosci. 6 (2006) 907-922
247. Borgia A., Williams P.M., and Clarke J. Single-molecule studies of protein folding. Annu. Rev. Biochem. 77 (2008) 101-125
248. Sato S., Religa T.L., Daggett V., and Fersht A.R. Testing protein-folding simulations by experiment: B domain of protein A. Proc. Natl. Acad. Sci. USA 101 (2004) 6952-6956
249. Schaeffer R.D., Fersht A., and Daggett V. Combining experiment and simulation in protein folding: Closing the gap for small model systems. Curr. Opin. Struct. Biol. 18 (2008) 4-9
250. Clementi C. Coarse-grained models of protein folding: Toy models or predictive tools?. Curr. Opin. Struct. Biol. 18 (2008) 10-15
251. Matysiak S., and Clementi C. Mapping folding energy landscapes with theory and experiment. Arch. Biochem. Biophys. 469 (2008) 29-33
252. Vendruscolo M., and Paci E. Protein folding: Bringing theory and experiment closer together. Curr. Opin. Struct. Biol. 13 (2003) 82-87
253. Improta S., Krueger J.K., Gautel M., Atkinson R.A., Lefevre J.F., Moulton S., Trewhella J., and Pastore A. The assembly of immunoglobulin-like modules in titin: Implications for muscle elasticity. J. Mol. Biol. 284 (1998) 761-777
254. Mallam A.L., Onuoha S.C., Grossmann J.G., and Jackson S.E. Knotted fusion proteins reveal unexpected possibilities in protein folding. Mol. Cell 30 (2008) 642-648
255. Went H.M., Benitez-Cardoza C.G., and Jackson S.E. Is an intermediate state populated on the folding pathway of ubiquitin?. FEBS Letters 567 (2004) 333-338