Investigation of an Anomalously Accelerating Substitution in the Folding of a Prototypical Two-State Protein

Journal of Molecular Biology

Volumn 403, Issue 3, 2010, Pages 446-458

  Lawrence, Camille ^a   Kuge, Jennifer ^a   Ahmad, Kareem ^a   Plaxco, Kevin W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mutations; Point substitution; Protein folding; Transition state; Unfolding kinetics

Indexed keywords

ALKANE DERIVATIVE; ARGININE; CARBENE; CHYMOTRYPSIN INHIBITOR; CHYMOTRYPSIN INHIBITOR 2; PHENYLALANINE; UNCLASSIFIED DRUG; CHYMOTRYPSIN; PEPTIDE; SERINE PROTEINASE INHIBITOR; VEGETABLE PROTEIN;

ACCELERATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; HYDROPHOBICITY; KINETICS; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; WILD TYPE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; POINT MUTATION; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

CHYMOTRYPSIN; HUMANS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PLANT PROTEINS; POINT MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SERINE PROTEINASE INHIBITORS;

EID: 77957750946     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.08.049     Document Type: Article

References (94)

1. Anfinsen C.B. Principles that govern the folding of protein chains. Science 1973, 181:223-230.
2. Wittung-Stafshede P., Lee J.C., Winkler J.R., Gray H.B. Cytochrome b562 folding triggered by electron transfer: approaching the speed limit for formation of a four-helix-bundle protein. Proc. Natl Acad. Sci. USA 1999, 96:6587-6590.
3. Chiti F., Taddei N., White P.M., Bucciantini M., Magherini F., Stefani M., et al. Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding. Nat. Struct. Mol. Biol. 1999, 6:1005-1009.
4. Garvey E.P., Matthews C.R. Effects of multiple replacements at a single position on the folding and stability of dihydrofolate reductase from Escherichia coli. Biochemistry 1989, 28:2083-2093.
5. Matouschek A., Kellis J.T., Serrano L., Fersht A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 1989, 340:122-126.
6. Matouschek A., Fersht A.R. Protein engineering in analysis of protein folding pathways and stability. Methods Enzymol. 1991, 202:82-112.
7. Plaxco K.W., Simons K.T., Ruczinski I., Baker D. Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics. Biochemistry 2000, 39:11177-11183.
8. Mok Y., Elisseeva E.L., Davidson A.R., Forman-Kay J.D. Dramatic stabilization of an SH3 domain by a single substitution: roles of the folded and unfolded states. J. Mol. Biol. 2001, 307:913-928.
9. Northey J.G., Maxwell K.L., Davidson A.R. Protein folding kinetics beyond the Φ value: using multiple amino acid substitutions to investigate the structure of the SH3 domain folding transition state. J. Mol. Biol. 2002, 320:389-402.
10. Fersht A.R., Sato S. Φ-Value analysis and the nature of protein-folding transition states. Proc. Natl Acad. Sci. USA 2004, 101:7976-7981.
11. De Los Rios M.A., Daneshi M., Plaxco K.W. Experimental investigation of the frequency and substitution dependence of negative Φ-values in two-state proteins. Biochemistry 2005, 44:12160-12167.
12. Makarov D.E., Plaxco K.W. The topomer search model: a simple, quantitative theory of two-state protein folding kinetics. Protein Sci. 2003, 12:17.
13. Gillespie B., Plaxco K.W. Using protein folding rates to test protein folding theories. Annu. Rev. Biochem. 2004, 73:837-859.
14. Zhu Y., Fu X., Wang T., Tamura A., Takada S., Saven J.G., Gai F. Guiding the search for a protein's maximum rate of folding. Chem. Phys. 2004, 307:99-109.
15. Larson S.M., Ruczinski I., Davidson A.R., Baker D., Plaxco K.W. Residues participating in the protein folding nucleus do not exhibit preferential evolutionary conservation. J. Mol. Biol. 2002, 316:225-233.
16. Kellis J.T., Nyberg K., Sali D., Fersht A.R. Contribution of hydrophobic interactions to protein stability. Nature 1988, 333:784-786.
17. Matsumura M., Becktel W.J., Matthews B.W. Hydrophobic stabilization in T4 lysozyme determined directly by multiple substitutions of Ile3. Nature 1988, 334:406-410.
18. Kellis J.T., Nyberg K., Fersht A.R. Energetics of complementary side chain packing in a protein hydrophobic core. Biochemistry 1989, 28:4914-4922.
19. Shortle D., Stites W.E., Meeker A.K. Contributions of the large hydrophobic amino acids to the stability of staphylococcal nuclease. Biochemistry 1990, 29:8033-8041.
20. Eriksson A.E., Baase WA., Zhang X.J., Heinz D.W., Blaber M., Baldwin E.P., Matthews B.W. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 1992, 255:178-183.
21. Jackson S.E., Moracci M., elMasry N., Johnson C.M., Fersht A.R. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry 1993, 32:11259-11269.
22. Dürr E., Jelesarov I. Thermodynamic analysis of cavity creating mutations in an engineered leucine zipper and energetics of glycerol-induced coiled coil stabilization. Biochemistry 2000, 39:4472-4482.
23. Otzen D.E., Itzhaki L.S., ElMasry N.F., Jackson S.E., 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 1994, 91:10422-10425.
24. Raleigh D.P., Plaxco K.W. The protein folding transition state: what are Φ-values really telling us?. Protein Pept. Lett. 2005, 12:117-122.
25. Font J., Benito A., Lange R., Ribó M., Vilanova M. The contribution of the residues from the main hydrophobic core of ribonuclease A to its pressure-folding transition state. Protein Sci. 2006, 15:1000-1009.
26. Sánchez I.E., Kiefhaber T. Origin of unusual φ-values in protein folding: evidence against specific nucleation sites. J. Mol. Biol. 2003, 334:1077-1085.
27. Friel C.T., Capaldi A.P., Radford S.E. Structural analysis of the rate-limiting transition states in the folding of Im7 and Im9: similarities and differences in the folding of homologous proteins. J. Mol. Biol. 2003, 326:293-305.
28. Martinez J.C., Pisabarro M.T., Serrano L. Obligatory steps in protein folding and the conformational diversity of the transition state. Nat. Struct. Mol. Biol. 1998, 5:721-729.
29. Martinez J.C., Serrano L. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nat. Struct. Mol. Biol. 1999, 6:1010-1016.
30. Itzhaki L.S., Otzen D.E., Fersht A.R. The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 1995, 254:260-288.
31. Jackson S.E., Fersht A.R. Folding of chymotrypsin inhibitor 2: 1. Evidence for a two-state transition. Biochemistry 1991, 30:10428-10435.
32. Ladurner A.G., Itzhaki L.S., Daggett V., Fersht A.R. Synergy between simulation and experiment in describing the energy landscape of protein folding. Proc. Natl Acad. Sci. USA 1998, 95:8473-8478.
33. Maxwell K.L., Wildes D., Zarrine-Afsar A., De Los Rios M.A., Brown A.G., Friel C.T., et al. Protein folding: defining a "standard" set of experimental conditions and a preliminary kinetic data set of two-state proteins. Protein Sci. 2005, 14:602-616.
34. Ruczinski I., Sosnick T.R., Plaxco K.W. Methods for the accurate estimation of confidence intervals on protein folding Φ-values. Protein Sci. 2006, 15:2257-2264.
35. Ladurner A.G., Fersht A.R. Glutamine, alanine or glycine repeats inserted into the loop of a protein have minimal effects on stability and folding rates. J. Mol. Biol. 1997, 273:330-337.
36. Ladurner A.G., Itzhaki L.S., Fersht A.R. Strain in the folding nucleus of chymotrypsin inhibitor 2. Fold. Des. 1997, 2:363-368.
37. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157:105-132.
38. Hopp T.P., Woods K.R. Prediction of protein antigenic determinants from amino acid sequences. Proc. Natl Acad. Sci. USA 1981, 78:3824-3828.
39. Fauchère J., Pliska V. Hydrophobic parameters pi of amino acid side chains from partitioning of N-acetyl-amino-acid amides. Eur. J. Med. Chem. 1983, 18:369-375.
40. Roseman M.A. Hydrophilicity of polar amino acid side-chains is markedly reduced by flanking peptide bonds. J. Mol. Biol. 1988, 200:513-522.
41. Anil B., Sato S., Cho J., Raleigh D.P. Fine structure analysis of a protein folding transition state; distinguishing between hydrophobic stabilization and specific packing. J. Mol. Biol. 2005, 354:693-705.
42. Calloni G., Taddei N., Plaxco K.W., Ramponi G., Stefani M., Chiti F. Comparison of the folding processes of distantly related proteins. importance of hydrophobic content in folding. J. Mol. Biol. 2003, 330:577-591.
43. Di Nardo A.A., Korzhnev D.M., Stogios P.J., Zarrine-Afsar A., Kay L.E., Davidson A.R. Dramatic acceleration of protein folding by stabilization of a nonnative backbone conformation. Proc. Natl Acad. Sci. USA 2004, 101:7954-7959.
44. Zarrine-Afsar A., Wallin S., Neculai A.M., Neudecker P., Howell P.L., Davidson A.R., Chan H.S. Theoretical and experimental demonstration of the importance of specific nonnative interactions in protein folding. Proc. Natl Acad. Sci. USA 2008, 105:9999-10004.
45. Zarrine-Afsar A., Dahesh S., Davidson A.R. Protein folding kinetics provides a context-independent assessment of β-strand propensity in the Fyn SH3 domain. J. Mol. Biol. 2007, 373:764-774.
46. Riddle D.S., Santiago J.V., Bray-Hall S.T., Doshi N., Grantcharova V.P., Yi Q., Baker D. Functional rapidly folding proteins from simplified amino acid sequences. Nat. Struct. Mol. Biol. 1997, 4:805-809.
47. Kim D.E., Gu H., Baker D. The sequences of small proteins are not extensively optimized for rapid folding by natural selection. Proc. Natl Acad. Sci. USA 1998, 95:4982-4986.
48. Gillespie B., Vu D.M., Shah P.S., Marshall S.A., Dyer R., Mayo S.L., Plaxco K.W. NMR and temperature-jump measurements of de novo designed proteins demonstrate rapid folding in the absence of explicit selection for kinetics. J. Mol. Biol. 2003, 330:813-819.
49. Kubelka J., Chiu T.K., Davies D.R., Eaton W.A., Hofrichter J. Sub-microsecond protein folding. J. Mol. Biol. 2006, 359:546-553.
50. Radisky E., Lu C., Kwan G., Koshland D. Role of the intramolecular hydrogen bond network in the inhibitory power of chymotrypsin inhibitor 2. Biochemistry 2005, 44:6823-6830.
51. Boisen S., Andersen C.Y., Hejgaard J. Inhibitors of chymotrypsin and microbial serine proteases in barley grains. Physiol. Plant 1981, 52:167-176.
52. Hejgaard J., Dam J., Petersen L.C., Bjorn S.E. Primary structure and specificity of the major serine proteinase inhibitor of amaranth (Amaranthus caudatus L.) seeds. Biochim. Biophys. Acta 1994, 1204:68-74.
53. Wojtaszek J., Kolaczkowska A., Kowalska J., Nowak K., Wilusz T. LTCI, a novel chymotrypsin inhibitor of the potato I family from the earthworm Lumbricus terrestris. Purification, cDNA cloning, and expression. Comp. Biochem. Physiol. Part B 2006, 143:465-472.
54. Demirel M.C., Atilgan A.R., Jernigan R.L., Erman B., Bahar I. Identification of kinetically hot residues in proteins. Protein Sci. 1998, 7:2522-2532.
55. Poupon A., Mornon J. Predicting the protein folding nucleus from a sequence. FEBS Lett. 1999, 452:283-289.
56. Plaxco K.W., Simons K.T., Baker D. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 1998, 277:985-994.
57. Ivankov D.N., Garbuzynskiy S.O., Alm E., Plaxco K.W., Baker D., Finkelstein A.V. Contact order revisited: influence of protein size on the folding rate. Protein Sci. 2003, 12:2057-2062.
58. Nguyen H., Jäger M., Kelly J.W., Gruebele M. Engineering a β-sheet protein toward the folding speed limit. J. Phys. Chem. B 2005, 109:15182-15186.
59. Jäger M., Zhang Y., Bieschke J., Nguyen H., Dendle M., Bowman M.E., et al. Structure-function-folding relationship in a WW domain. Proc. Natl Acad. Sci. USA 2006, 103:10648-10653.
60. Scott K.A., Steward A., Fowler S.B., Clarke J. Titin; a multidomain protein that behaves as the sum of its parts. J. Mol. Biol. 2002, 315:819-829.
61. Carrion-Vazquez M., Oberhauser A.F., Fowler S.B., Marszalek P.E., Broedel S.E., Clarke J., Fernandez J.M. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl Acad. Sci. USA 1999, 96:3694-3699.
62. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
63. Boeckmann B., Bairoch A., Apweiler R., Blatter M.C., Estreicher A., Gasteiger E., et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003, 31:365-370.
64. Pruitt K.D., Tatusova T., Maglott D.R. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 2007, 35:D61-D65.
65. Marchler-Bauer A., Anderson J.B., Derbyshire M.K., DeWeese-Scott C., Gonzales N.R., Gwadz M., et al. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 2007, 35:D237-D240.
66. Kragelund B.B., Osmark P., Neergaard T.B., Schiodt J., Kristiansen K., Knudsen J., 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. Mol. Biol. 1999, 6:594-601.
67. Fernandez-Escamilla A.M., Cheung M.S., Vega M.C., Wilmanns M., Onuchic J.N., Serrano L. Solvation in protein folding analysis: combination of theoretical and experimental approaches. Proc. Natl Acad. Sci. USA 2004, 101:2834-2839.
68. Viguera A.R., Vega C., Serrano L. Unspecific hydrophobic stabilization of folding transition states. Proc. Natl Acad. Sci. USA 2002, 99:5349-5354.
69. Cobos E.S., Filimonov V.V., Vega M.C., Mateo P.L., Serrano L., Martinez J.C. A thermodynamic and kinetic analysis of the folding pathway of an SH3 domain entropically stabilised by a redesigned hydrophobic core. J. Mol. Biol. 2003, 328:221-233.
70. Viguera A.R., Serrano L., Wilmanns M. Different folding transition states may result in the same native structure. Nat. Struct. Mol. Biol. 1996, 3:874-880.
71. Burton R.E., Huang G.S., Daugherty M.A., Calderone T.L., Oas T.G. The energy landscape of a fast-folding protein mapped by Ala→Gly substitutions. Nat. Struct. Mol. Biol. 1997, 4:305-310.
72. Wilson C.J., Wittung-Stafshede P. Role of structural determinants in folding of the sandwich-like protein Pseudomonas aeruginosa azurin. Proc. Natl Acad. Sci. USA 2005, 102:3984-3987.
73. Jackson S.E., elMasry N., 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 1993, 32:11270-11278.
74. Rodriguez H.M., Vu D.M., Gregoret L.M. Role of a solvent-exposed aromatic cluster in the folding of Escherichia coli CspA. Protein Sci. 2000, 9:1993-2000.
75. Vu D.M., Reid K.L., Rodriguez H.M., Gregoret L.M. Examination of the folding of E. coli CspA through tryptophan substitutions. Protein Sci. 2001, 10:2028-2036.
76. Horng J., Cho J., Raleigh D.P. Analysis of the pH-dependent folding and stability of histidine point mutants allows characterization of the denatured state and transition state for protein folding. J. Mol. Biol. 2005, 345:163-173.
77. Hamill S.J., Steward A., 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. 2000, 297:165-178.
78. Northey J.G., Di Nardo A.A., Davidson A.R. Hydrophobic core packing in the SH3 domain folding transition state. Nat. Struct. Mol. Biol. 2002, 9:126-130.
79. Di Nardo A.A., Korzhnev D.M., Stogios P.J., Zarrine-Afsar A., Kay L.E., Davidson A.R. Dramatic acceleration of protein folding by stabilization of a nonnative backbone conformation. Proc. Natl Acad. Sci. USA 2004, 101:7954-7959.
80. De Los Rios M.A., Muralidhara B.K., Wildes D., Sosnick T.R., Marqusee S., Wittung-Stafshede P., et al. On the precision of experimentally determined protein folding rates and Φ-values. Protein Sci. 2006, 15:553-563.
81. Villegas V., Martinez J.C., Aviles F.X., Serrano L. Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain. J. Mol. Biol. 1998, 283:1027-1036.
82. McCallister E.L., Alm E., Baker D. Critical role of β-hairpin formation in protein G folding. Nat. Struct. Mol. Biol. 2000, 7:669-673.
83. Kim D.E., Fisher C., Baker D. A breakdown of symmetry in the folding transition state of protein L. J. Mol. Biol. 2000, 298:971-984.
84. Gu H., Doshi N., Kim D., Simons K., Santiago J., Nauli S., Baker D. Robustness of protein folding kinetics to surface hydrophobic substitutions. Protein Sci. 1999, 8:2734-2741.
85. Otzen D.E., Oliveberg M. Conformational plasticity in folding of the split β-α-β protein S6: evidence for burst-phase disruption of the native state. J. Mol. Biol. 2002, 317:613-627.
86. Guerois R., Serrano L. The SH3-fold family: experimental evidence and prediction of variations in the folding pathways. J. Mol. Biol. 2000, 304:967-982.
87. Fowler S.B., Clarke J. Mapping the folding pathway of an immunoglobulin domain: structural detail from Φ value analysis and movement of the transition state. Structure 2001, 9:355-366.
88. Grantcharova V.P., Riddle D.S., Santiago J.V., Baker D. Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat. Struct. Mol. Biol. 1998, 5:714-720.
89. Riddle D.S., Grantcharova V.P., Santiago J.V., Alm E., Ruczinski I., Baker D. Experiment and theory highlight role of native state topology in SH3 folding. Nat. Struct. Mol. Biol. 1999, 6:1016-1024.
90. Went H.M., Jackson S.E. Ubiquitin folds through a highly polarized transition state. Protein Eng. Des. Sel. 2005, 18:229-237.
91. Kubelka J., Henry E.R., Cellmer T., Hofrichter J., Eaton W.A. Chemical, physical, and theoretical kinetics of an ultrafast folding protein. Proc. Natl Acad. Sci. USA 2008, 105:18655-18662.
92. Pozdnyakova I., Guidry J., Wittung-Stafshede P. Studies of Pseudomonas aeruginosa azurin mutants: cavities in beta-barrel do not affect refolding speed. Biophys. J. 2002, 82:2645-2651.
93. Wilson C.J., Wittung-Stafshede P. Snapshots of a dynamic folding nucleus in zinc-substituted Pseudomonas aeruginosa azurin. Biochemistry 2005, 44:10054-10062.
94. Williamson M.S., Forde J., Kreis M. Molecular cloning of two isoinhibitor forms of chymotrypsin inhibitor 1 (CI-1) from barley endosperm and their expression in normal and mutant barleys. Plant Mol. Biol. 1988, 10:521-535.