Protein folding: Binding of conformationally fluctuating building blocks via population selection

Critical Reviews in Biochemistry and Molecular Biology

Volumn 36, Issue 5, 2001, Pages 399-433

  Tsai, Chung Jung ^a   Ma, Buyong ^b   Kumar, Sandeep ^b   Wolfson, Haim ^c   Nussinov, Ruth ^a,c  

^a SAIC FREDERICK INC   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

Binding; Conformational ensembles; Dynamic landscapes; Folding; Funnels; Induced conformational change

Indexed keywords

AMYLOID; CHAPERONE; CHAPERONIN; DIHYDROFOLATE REDUCTASE; POLYPEPTIDE; PROTEIN;

CONFORMATIONAL TRANSITION; IN VITRO STUDY; IN VIVO STUDY; KINETICS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STABILITY; REVIEW;

EID: 0001450617     PISSN: 10409238     EISSN: None     Source Type: Journal    
DOI: 10.1080/20014091074228     Document Type: Review

References (122)

1. Kim, P. S. and Baldwin, R. L. 1982. Specific intermediates in the folding reactions of small proteins, and the mechanism of protein folding. Annu. Rev. Biochem. 51:459-489.
2. Kim, P. S. and Baldwin, R. L. 1990. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 59:631-660.
3. Udgaonkar, J. B. and Baldwin, R. L. 1988. NMR evidence for an early frameork interdediates on the folding pathway of ribonuclease A. Nature 335:694-699.
4. Wetlaufer D. B. 1973. Nucleation, rapid folding and globular intrachain regions in proteins. Proc Natl Acad Sci USA 70:697-701.
5. Shakhnovitch, E., Abkevitch, V. and Ptitsyn, O. 1996. Conserved residues and the mechanism of protein folding. Nature 379:96-98.
6. Fersht, A. R. 1997. Nucleation mechanism in protein folding. Curr Opin Struct Biol 7:3-9.
7. Karplus, M. and Weaver, D. L. 1994. Protein folding dynamics: the diffusion-collision model and experimental data. Prot Sci 3:650-668.
8. Rackovsky, S. and Scheraga, H. A. 1977. Hydrophobicity, hydrophilicity and the radial and orientational distributions of residues in native proteins. Proc Natl Acad Sci USA 74:5248-5251.
9. Dill, K. A. 1985. Theory for the folding and stability of globular proteins. Biochemistry 24:1501-1509.
10. Dill, K. A. 1990. Dominant forces in protein folding. Biochemistry 29:7135-7155.
11. Baldwin, R.L. and Rose, G.D. 1999. Is protein folding hierarchic? I. Local structure and peptide folding. TIBS 24:26-33.
12. Baldwin, R.L. and Rose, G. D. 1999. Is protein folding hierarchic? II. Folding intermediates and transition states. TIBS 24:77-84.
13. Chiti, F., Taddei, N., Webster, P., Hamada, D., Fiaschi, T., Ramponi, G., and Dobson, C.M. 1999. Acceleration of the folding of acylphosphatase by stabilization of local secondary structures. Nat Struct Biol 6:380-386.
14. Hamada, D., Chiti, F., Guijarro, I., Kataoka, M., Taddei, N., and Dobson, C. M. 2000. Evidence concerning rate-limiting steps in protein folding from the effects of trifluooethanol. Nat Struct Biol 7:58-61.
15. Sabelko, J, Ervin, J and Gruebele, M. 1999. Observations of strange kinetics in protein folding. Proc Natl Acad Sci USA 96:6031-6036.
16. Ionescu, R.M. and Matthews, C.M. 1999. Folding under the influence. Nat Struct Biol 6:304-307.
17. Gualfetti, P. J., Bilsel, O., and Mattews, C. R. 1999. The progressive development of structure and stability during the equilibrium folding of the α subunit of tryptophan synthase from E. coli. Protein Sci 8:1623-1635.
18. Park, S.H., O'Neil, K.T., and Roder, H. 1997. An early intermediate in the folding reaction of the B1 domain of protein G contains a native-like core. Biochemistry 36:14277-14283.
19. Zitzewitz, J.A., Gualfetti, P.J., Perkons, I.A., Wasta, S.A., and Matthews, C.R. 1999. Identifying the structural boundaries of independent folding domains in the α subunit of tryptophan synthase, a β/α barrel protein. Protein Sci 8:1200-1209.
20. Gegg, C.V., Bowers, K.E., and Matthews, C.R. 1997. Probing minimal independent folding units in dihydrofolate reductase by molecular dissection. Protein Sci 6:1885-1892.
21. Dyson, H. J., Merutka, G., Waltho, J. P., Lerner, R. A., and Wright, P. E. 1992. Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding I. Myohemerythrin. J Mol Biol 226:795-817.
22. Dyson, H. J., Sayre, J. R., Merutka, G., Shin, H.-C., Lerner, R. A., and Wright, P. E. 1992. Folding of peptide fragments comprising the complete sequence of proteins. Models for initiation of protein folding II. Plastocyanin. J Mol Biol 226:819-835.
23. Prat-Gay, G. 1996. Association of complementary fragments and the elucidation of protein folding pathways. Prot Eng 9:843-847.
24. Yokota, A., Takenaka, H., Oh, T., Noda, Y., and Segawa, S.-I. 1998. Thermodynamics of the reconstitution of tuna cytochrome c from two peptides. Protein Sci 7:1717-1727.
25. Sancho, J. and Fersht, A. R. 1992. Dissection of an enzyme by protein engineering. The N and C-terminal fragments of barnase from a native-like complex with restored enzymic activity. J Mol Biol 224:741-747.
26. Yang, X.-M., Yu, W.-F., Li, J.-H., Fuchs, J., Rizo, J., and Tasayco, M. L. 1998. NMR evidence for the reassembly of an α/β domain after cleavage of an α-helix: implications for protein design. J Am Chem Soc 120:7985-7986.
27. Kobayashi, N., Honda, S., Yoshii, H., Uedaira, H., and Munekata, E. 1995. Complement assembly of two fragments of the streptococcal protein G B1 domain in aqueous solution. FEBS Lett 366:99-103.
28. Neira, J.L. and Fersht, A.R. 1999. Exploring the folding funnel of a polypeptide chain by biophysical studies on protein fragments. J Mol Biol 285:1309-1333.
29. Honda, S., Kobayashi, N., Munekata, E., and Uedaira, H. 1999. Fragment reconstitution of a small protein: folding energetics of the reconstituted immunoglobulin binding domain B1 of streptococcal protein G. Biochemistry 38:1203-1213.
30. Prat-Gay, G. and Fersht, A. 1994. Generation of a family of protein fragments for structure-folding studies. I. Folding complementation of two fragments of chymotrypsin inhibitor-2 formed by cleavage at its unique methionine residue. Biochemistry 33:7957-7963.
31. Tasayco, M.L. and Chao, K. 1995. NMR study of the reconstitution of the beta-sheet of thioredoxin by fragment cmplementation. Proteins 22:41-44.
32. Georgescu, R. E., Braswell, E. H., Zhu, D. and Tasayco, M. L. 1999. Energetics of assembling an artificial heterodimer with an α/β motif: cleaved versus uncleaved Escherichia coli thioredoxin. Biochemistry 38:13355-13366.
33. Burton, R.E., Myers, J.K. and Oas, T.G. 1998. Protein folding dynamics: quantitative comparison between theory and experiment. Biochemistry 37:5337-5343.
34. Tsuji, T., Yoshida, K., Satoh, A., Kohno, T., Kobayashi, K., and Yanagawa, H. 1999. Foldability of barnase mutants obtained by permutaion of modules or secondary structure units. J Mol Biol, 268:1581-1596.
35. Rothwarf, D. M. and Scheraga, H. A. 1996. Role of non-native aromatic and hydrophobic interactions in the folding of hen egg white lysozyme. Biochemistry 35:13797-13807.
36. Shortle, D. R. 1996 Structural analysis of non-native states of proteins by NMR methods. Curr Opin Struct Biol 6:24-30.
37. Shao, X. and Matthews, C. R. 1998. Single-tryptophan mutants of monomeric tryptophan repressor: optical spectroscopy reveals nonnative structure in a model for an early folding intermediates. Biochemistry 37:7850-7858.
38. Houry, W. A., Frishman, D., Eckerson, C., Lottspeich, F., and Hartl, F. U. 1999. Identification of in vivo substrates of the chaperonin GroEl. Nature 402:147-154.
39. Netzer, W. J. and Hartl, F. U. 1998. Protein folding in the cytosol: chaperone-dependent and -independent mechanisms. Trends Biochem Sci 23:68-73.
40. Baker, D., Shiau, A. K., and Agard, D. A. 1993. The role of pro regions in protein folding. Curr Opin Cell Biol 5:966-970.
41. Shinde, U. P., Liu, J. J. and Inoye, M. 1997. Protein memory through altered folding mediated by intramolecular chaperones. Nature 389:520-522.
42. Sauter, N. K., Mau, T., Rader, S. D., and Agard, D. A. 1998. Structure of α-lytic protease complexed with its proregion. Nature Struct Biol 5:945-950.
43. Sohl, J. S., Jaswal, S. S., and Agard, D. A. 1998. Unfolded conformations of α-lytic protease are more stable than its native state. Nature 395:817-819.
44. Wang, L., Ruan, B., Ruvinov, S., and Bryan, P. N. 1998. Engineering the independent folding of subtilisin BPN' prodomain: correlation of pro-domain stability with the rate of subtilisin folding. Biochemistry 37:3165-3171.
45. Anderson, D. E., Peters, R. J., Wilk, B., and Agard, D. A. 1999. α-lytic protease precursor: characterization of a structured folding intermediate. Biochemistry 38:4728-4735.
46. Cunningham, E. L., Jaswal, S. J., Sohl, J. L., and Agard, D. A. 1999. Kinetic stability as a mechanism for protease longevity. Proc Natl Acad Sci USA 96:1108-11014.
47. Ellis, R. J. 1998. Steric chaperones. Trends Biochem Sci 23:43-45.
48. Baker, D., Sohl, J. L., and Agard, D. A. 1992. A protein folding reaction under kinetic control. Nature 356:263-265.
49. Wright, P.E. and Dyson, H.J. 1999. Intrinsically unstructured proteins: reassessing the protein structure-function paradigm. J Mol Biol 293:321-331.
50. II-ras protein. Biochemistry 37:14881-14890.
51. Uversky, V.N., Gillespie, J.R., and Fink, A.L. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41:415-427.
52. Serio, T. R., Gashikar, A. G., Kowal, A. S., Sawicki, G. J., Moslehi, J. J., Serpell, L., Arnsdorf, M. F., and Lindquist, S. L. 2000. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289:1317-1321.
53. Kelly, J. W. 2000. Mechanism of amyloidogenesis. Nat Struct Biol 7:824-826.
54. Alm, E. and Baker, D. 1999. Matching theory and experiment in protein folding. Curr Opin Struct Biol 9:189-196.
55. Plaxco, K. W., Simons, K. T. and Baker, D. 1998. Contact order, transition state placement and the refolding rates of single domain proteins. J Mol Biol 277:985-994.
56. Perl, D., Welker, C., Schindler, T., Schroder, K., Marahiel, M.A., Jaenicke, R., and Schmid, F.X. 1998. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nat Struct Biol, 5:229-235.
57. Kiefhaber, T. 1995. Kinetic traps in lysozyme folding. Proc Natl Acad Sci USA 92:9029-9033.
58. Capaldi, A. P., Ferguson, S. J., and Radford, S. E. 1999. The Greek key protein apo-pseudoazurin folds through an obligate on-pathway intermediate. J Mol Biol 286:1621-1632.
59. Lopez-Hernandez, E. and Serrano, L. 1996. Structure of the transition state for folding of the 129 aa protein Che Y resembles that of a smaller protein, CI-2? Fold Design, 1:43-55.
60. Choe, S.E., Matsudaira, P.T., Osterhout, J., Wagner, G., and Shakhnovitch, E.I. 1998. Folding kinetics of villin 14T, a protein domain with a central β-sheet and two hydrophobic cores. Biochemistry 37:14508-14518.
61. Matagne, A., Radford, S. E., and Dobson, C. M. 1997. Fast and slow tracks in lysozyme folding: insight into the role of domains in the folding process. J Mol Biol 267:1068-1074.
62. van Nuland, N.A.J., et al. 1998. Slow folding of muscle acylphosphatase in the absence of intermediates. J Mol Biol, 283:883-891.
63. Bilsel, O., Zitzewitz, J. A., Bowers, K. E. and Matthews, R. C. 1999. Folding mechanism of the -subunit of tryptophan synthase, an /β barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry 38:1018-1029.
64. Panchenko, A.R., Luthey-Schulten, Z., Cole, R., and Wolynes, P.G. 1997. The foldon universe: A survey of structural similarity and self-recognition of independently folding units. J Mol Biol 272:95-105.
65. Hansmann, U. H. E., Okamoto, Y., and Onuchic, J. N. 1999. The folding funnel landscape for the peptide metenkephalin. Proteins 34:472-483.
66. Frauenfelder, H. and Leeson, D. T. 1998. The energy landscape in non-biological molecules. Nat Struct Biol 5:757-759.
67. Shoemaker, B. A. and Wolynes, P. G. 1999. Exploring structures in protein folding funnels with free energy functions: the denatured ensemble. J Mol Biol 267:657-674.
68. Shoemaker Wang, J. and Wolynes, P. G. 1999. Exploring structures in protein folding funnels with free energy functions: the transition state ensemble. J Mol Biol 267:675-694.
69. Pande, V.S., Grosberg, A.Y., Tanaka, T., and Rokhsar, D.S. 1998. Pathways for protein folding: Is a new view needed? Curr Opin Struct Biol 8:66-79.
70. Pande, V. S. and Rokhsar, D. S. 1999. Molecular dynamics simulations of unfolding and refolding of βhairpin fragements of protein G. Proc Natl Acad Sci USA 96:9062-9067.
71. Tsai, C.J., Xu, D., and Nussinov, R. 1998. Protein folding via binding, and vice versa. Fold Design 3:R71-R80.
72. Tsai, C.J., Kumar, S., Ma, B., and Nussinov R. 1999. Folding funnels, binding funnels and protein function. Protein Sci 8:1181-1190.
73. Tsai, C-J, Maizel, J. V., and Nussinov, R. 1999. Distinguishing between sequential and non-sequentially folded proteins: implications for folding and misfolding. Protein Sci 37:73-87.
74. Tsai, C.J., Ma, B., and Nussinov, R. 1999. Folding and binding cascades: shifts in energy landscapes. Proc Natl Acad Sci USA 96:9970-9972.
75. Tsai, C.J., Maizel, J.V., and Nussinov, R. 2000. Anatomy of protein structures: visualizing how a 1D protein chain folds into a 3D shape. Proc Natl Acad Sci USA 97:12038-12043.
76. Kumar, S., Ma, B., Tsai, C.-J., Wolfson, H. and Nussinov, R. 1999. Folding funnels and conformational transitions via hinge-bending motions. Cell Biochem Biophys 31:23-46.
77. Kumar, S., Ma, B., Tsai, C.J., Sinha, N. and Nussinov, R. 2000. Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci 9:10-19.
78. Ma, B., Kumar, S., Tsai, C-J. and Nussinov, R. 1999. Folding funnels and binding mechanisms. Protein Eng 12:713-720.
79. Ma, B., Tsai, C.J., and Nussinov, R. 2000. Binding and folding: in search of intramolecular chaperone-like building block fragments. Protein Eng 13:617-627.
80. Alm, E. and Baker, D. 1999. Prediction of protein-folding mechanisms from free-energy landscapes derived from native structures. Proc Natl Acad Sci USA 96:11305-11310.
81. Jackson, S.E. 1998. How do small single domain proteins fold? Fold Design 3:R81-R91.
82. Llinas, M. and Marqusee, S. 1998. Subdomain interactions as a determinant in the folding and stability of T4 lysozyme. Protein Sci 7:96-104.
83. Sham, Y.Y., Ma. B., Tsai, C.J. and Nussinov, R. 2001. Molecular dynamic simulation of Escherichia coli dihydrofolate reductase and its protein fragments: relative stabilities in experiment and simulations. Protein Sci 10:135-148.
84. Bennett, M. J., Schlunegger, M. P., and Eisenberg, D. 1995. 3D domain swapping: A mechanism for oligomer assembly. Protein Sci 4:2455-2468.
85. Munioz, V. and Eaton, W. 1999. A simple model for calculating the kinetics of protein folding from three-dimensional structures. Proc Natl Acad Sci USA 96:1131-1136.
86. Galzitskaya, O. V. and Finkelstein, A. V. 1999. A theoretical search for folding/unfolding nuclei in three-dimensional protein structures. Proc Natl Acad Sci USA 96:11299-11304.
87. Riddle, D.S., Santiago, J.V., Bray-Hall, S.T., Doshi, N., Grantcharova, V.P., Yi, O., and Baker, D. 1997. Functional rapidly folding proteins from simplified amino acid sequences. Nat Struct Biol, 4:805-809.
88. Martinez, J.C., Pisabarro, M.T., and Serrano, L. 1998. Obligatory steps in protein folding and the conformational diversity of the transition state. Nat Struct Biol 5:721-729.
89. Polverino de Laureto, P., Scaramella, E., Frigo, M., Wondrich, F.G., De Filippis, V., Zambonin, M., and Fontana, A. 1999. Limited proteolysis of bovine α-lactalbumin: isolation and characterization of protein domains. Protein Sci 8:2290-2303.
90. Fontana, A., Zambonin, M., Polverino de Laureto, P., De Filippis, V., Clementi, A., and Scaramella, E. 1997. Probing the conformational state of apomyoglobin by limited proteolysis. J Mol Biol 266:223-230.
91. Oas, T. G. and Kim, P. S. 1988. A peptide model of protein folding intermediate. Nature 336:42-48.
92. Tasayco, M.L. and Carey, J. 1992. Ordered self-assembly of polypeptide fragments to form native-like dimeric trp represoor. Science 255:594-597.
93. Wu, L. C., Grandori, R., and Carey, J. 1994. Autonomous subdomains in protein folding. Protein Sci 3:359-371.
94. Jones, B.E. and Matthews, C. R. 1995. Early intermediates in the folding of dihydrofolate reductase from Escherichia coli detected by hydrogen exchange and NMR. Protein Sci 4:167-177.
95. Goldberg, M.S., Zhang, J., Sondek, S., Matthews, C.R., Fox, R.O., and Horwich, A.L. 1997. Native-like structure of a protein-folding intermediate bound to the chaperonin GroEL. Proc Natl Acad Sci USA 94:1080-1085.
96. Clark, A.C. and Frieden, C. 1999. The chaperonin GroEL binds to late-folding non-native conformations present in native Escherichia coli and murine dihydrofolate reductases. J Mol Biol 285:1777-1788.
97. Bystroff, C., Oatley, S.J., and Kraut, J. 1990. Crystal structures of Escherichia coli dihydrofolate reductase: the NADP+ holoenzyme and the folate-NADP+ ternary complex, substrate binding and a model for the transition state. Biochemistry 30:8067-8074.
98. Sawaya, M.R. and Kraut, J. 1997. Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry 36:585-603.
99. Bernstein, F.C., Koetzle, T.F., Williams, G.J.B., Meyer, E.F. Jr, Brice, M.D., Rodgers, J.R., Kennard, O., Shimanouchi, T., and Tasumi, M. 1977. The protein databank: a computer-based archival file for macromolecular structures. J Mol Biol 112:535-542.
100. Kumar, S., Sham, Y. Y., Tsai, C.-J., and Nussinov, R. 2001. Protein folding and function: the N-terminal fragment in adenylate kinase. Biophys J, in press.
101. Clark, A.C. and Frieden, C. 1999. Native Escherichia coli and murine dihydrofolate reductases contain late-folding non-native structures. J Mol Biol 285:1765-1776.
102. Clark, A. C. and Frieden, C. 1997. GroEL-mediated folding of structurally homologous dihydrofolate reductases. J Mol Biol 268:512-525.
103. Pfeil W. 1998. Protein Stability and Folding: A Collection of Thermodynamic Data. Springer-Verlag, Berlin. 657 pp.
104. Clark, A.C, Hugo, E., and Frieden, C. 1996. Determination of regions in the dihydrofolate reductase structure that interact with the molecular chaperonin GroEL. Biochemistry 35:5893-5901.
105. Xu, D., Lin, S. L., and Nussinov, R. 1997. Protein binding vs. protein folding: the role of hydrophilic bridges in protein associations. J Mol Biol 265:68-84.
106. Chen, L. and Sigler, P.B. 1999. The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 99:757-768.
107. Chatellier, J., Buckle, A.M., and Fersht, A.R. 1999. GroEL recognizes sequential and non-sequential linear structural motifs compatible with extended β-strands and α-helices. J Mol Biol 292:163-172.
108. Tanaka, N. and Fersht, A.R. 1999. Identification of substrate binding site of GroEL minichaperone in solution. J Mol Biol 292:173-180.
109. Eilers, M., Hwang, S., and Schatz, G. 1988. Unfolding and refolding of a purified precursor protein during import into isolated mitochondria. EMBO J 7:1139-1145.
110. Ostermann, J., Horwich, A.L., Neupert, W., and Hartl, F.U. 1989. Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341:125-130.
111. Shtilerman, M., Lorimer, G.H., and Englander, S.W. 1999. Chaperonin function: folding by forced unfolding. Science 284:822-825.
112. Demarest, S.J., Fairman, R., and Raleigh, D.P. 1998. Peptide models of local and long-range interactions in the molten globule state of human α-lactalbumin. J Mol Biol 283:279-291.
113. Sprang, S. R. 1997 G protein mechanisms: insights from structural analysis. Annu Rev Biochem 66:639-678.
114. Rumbley, J., Hoang, L., Mayne, L., and Englander, S. W. 2001. An amino acid code for protein folding. Proc Natl Acad Sci USA 98:105-112.
115. Laurents, D. V., Bruix, M., Jamin, M., and Baldwin, R. L. 1998. A pulse-chase-competition experiment to determine if a folding intermediate is on or off pathway: application to ribonuclease A. J Mol Biol 283:669-678.
116. Bai, Y. 1999. Kinetic evidence for an on-pathway intermediate in the folding of cytochrome c. Proc Natl Acad Sci USA 96:477-480.
117. Bai, Y. 2000. Kinetic evidence of an on-pathway intermediate in the folding of lysozyme. Protein Sci 9:194-196.
118. Bai, Y., Sosnick, T. R., Mayne, L., and Englander, S. W. 1995. Protein folding intermediates: native state hydrogen exchange. Science 269:192-197.
119. Bai, Y. and Englander, S. W. 2000. Future directions in folding: the multistate nature of protein structure. Proteins 24:145-151.
120. Milne, J. S., Mayne, L., Roder, H., Wand, A. J., and Englander, S. W. 1998. Protein Sci 7:739-745.
121. Chamberlain, A. K., Fischer, K. F., Reardon, D., Handel, T. M., and Marqusee, A. S. 1999. Folding of an isolated ribonuclease H core fragment. Protein Sci 8:2251-2257.
122. Freire, E. 1999. The propagation of binding interactions to remote sites in proteins: analysis of the binding of the monoclonal antibody D1.3 to lysozyme. Proc Natl Acad Sci USA 96:10118-10122.