Folding mechanism of an extremely thermostable (βα) 8-barrel enzyme: A high kinetic barrier protects the protein from denaturation

Biochemistry

Volumn 51, Issue 16, 2012, Pages 3420-3432

  Carstensen, Linn ^a   Zoldák, Gabriel ^b   Schmid, Franz Xaver ^c   Sterner, Reinhard ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLASES; FOLDING MECHANISM; GLUTAMINASE; HIGH-ENERGY BARRIERS; IMIDAZOLE GLYCEROL PHOSPHATES; KINETIC BARRIER; NATIVE PROTEINS; REFOLDING; SEQUENTIAL PROCESS; STOPPED FLOW; SYNTHASES; THERMOTOGA MARITIMA; TIME CONSTANTS; TWO-STATE MODEL;

GLYCEROL; KINETICS;

PROTEINS;

ADENYLATE CYCLASE; GLUTAMINASE; HISF PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; BINDING SITE; ENZYME MECHANISM; KINETICS; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; THERMODYNAMICS;

AMINOHYDROLASES; CIRCULAR DICHROISM; ENZYME STABILITY; KINETICS; MODELS, MOLECULAR; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STRUCTURE, SECONDARY; TEMPERATURE; THERMODYNAMICS; THERMOTOGA MARITIMA;

EID: 84860182968     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300189f     Document Type: Article

References (63)

1. Murzin, A. G., Brenner, S. E., Hubbard, T., and Chothia, C. (1995) SCOP: A structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247, 536-540
2. Caetano-Anollés, G., Kim, H. S., and Mittenthal, J. E. (2007) The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture Proc. Natl. Acad. Sci. U.S.A. 104, 9358-9363
3. Wierenga, R. K. (2001) The TIM-barrel fold: A versatile framework for efficient enzymes FEBS Lett. 492, 193-198
4. 8-barrel enzyme fold Chem. Rev. 105, 4038-4055
5. Nagano, N., Orengo, C. A., and Thornton, J. M. (2002) One fold with many functions: The evolutionary relationships between TIM barrel families based on their sequences, structures and functions J. Mol. Biol. 321, 741-765
6. Pujadas, G. and Palau, J. (1999) TIM barrel fold: Structural, functional and evolutionary characteristics in natural and designed molecules Biologica (Bratislava, Slovakia) 54, 231-253
7. Raine, A. R., Scrutton, N. S., and Mathews, F. S. (1994) On the evolution of alternate core packing in eightfold (βα)-barrels Protein Sci. 3, 1889-1892
8. Reardon, D. and Farber, G. (1995) The structure and evolution of αβ-barrel proteins FASEB J. 9, 497-503
9. 8-barrels: Implications for the evolution of metabolic pathways J. Mol. Biol. 303, 627-641
10. 8-barrel proteins: Fragment complementation of phosphoribosylanthranilate isomerase Biochemistry 31, 3617-3625
11. 8-barrel protein: Generation of variability by recombination FEBS Lett. 560, 167-172
12. Bertolaet, B. L. and Knowles, J. R. (1995) Complementation of fragments of triosephosphate isomerase defined by exon boundaries Biochemistry 34, 5736-5743
13. Gualfetti, P. J., Bilsel, O., and Matthews, C. R. (1999) The progressive development of structure and stability during the equilibrium folding of the α-subunit of tryptophan synthase from Escherichia coli Protein Sci. 8, 1623-1635
14. Bilsel, O., Zitzewitz, J. A., Bowers, K. E., and Matthews, C. R. (1999) Folding mechanism of the α-subunit of tryptophan synthase, an βα-barrel protein: Global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels Biochemistry 38, 1018-1029
15. 8-barrels J. Mol. Biol. 320, 1119-1133
16. Gu, Z., Zitzewitz, J. A., and Matthews, C. R. (2007) Mapping the structure of folding cores in TIM barrel proteins by hydrogen exchange mass spectrometry: The roles of motif and sequence for the indole-3-glycerol phosphate synthase from Sulfolobus solfataricus J. Mol. Biol. 368, 582-594
17. Gu, Z., Rao, M. K., Forsyth, W. R., Finke, J. M., and Matthews, C. R. (2007) Structural analysis of kinetic folding intermediates for a TIM barrel protein, indole-3-glycerol phosphate synthase, by hydrogen exchange mass spectrometry and Gō model simulation J. Mol. Biol. 374, 528-546
18. 8-barrel of unknown function from B. subtilis J. Mol. Biol. 372, 236-253
19. Mukaiyama, A., Takano, K., Haruki, M., Morikawa, M., and Kanaya, S. (2004) Kinetically robust monomeric protein from a hyperthermophile Biochemistry 43, 13859-13866
20. Perl, D., Welker, C., Schindler, T., Schroder, K., Marahiel, M., Janicke, 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
21. Dams, T. and Jaenicke, R. (1999) Stability and folding of dihydrofolate reductase from the hyperthermophilic bacterium Thermotoga maritima Biochemistry 38, 9169-9178
22. Deutschman, W. and Dahlquist, F. (2001) Thermodynamic basis for the increased thermostability of CheY from the hyperthermophile Thermotoga maritima Biochemistry 40, 13107-13113
23. Lang, D., Thoma, R., Henn-Sax, M., Sterner, R., and Wilmanns, M. (2000) Structural evidence for evolution of the βα-barrel scaffold by gene duplication and fusion Science 289, 1546-1550
24. 8-barrel proteins in histidine and tryptophan biosynthesis: A paradigm to study enzyme evolution ChemBioChem 12, 1487-1494
25. Beismann-Driemeyer, S. and Sterner, R. (2001) Imidazole glycerol phosphate synthase from Thermotoga maritima: Quaternary structure, steady-state kinetics, and reaction mechanism of the bienzyme complex J. Biol. Chem. 276, 20387-20396
26. 8-barrel of the imidazole glycerol phosphate synthase bienzyme complex Structure 10, 185-193
27. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77, 51-59
28. Thoma, R., Obmolova, G., Lang, D. A., Schwander, M., Jenö, P., Sterner, R., and Wilmanns, M. (1999) Efficient expression, purification and crystallisation of two hyperthermostable enzymes of histidine biosynthesis FEBS Lett. 454, 1-6
29. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131, 266-280
30. Santoro, M. M. and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants Biochemistry 27, 8063-8068
31. McDaniel, D. H. and Smoot, C. R. (1956) Approximations in the kinetics of consecutive reactions J. Phys. Chem. 60, 966-969
32. Casado, J., González, J., and Moreno, M. (1987) Consecutive reactions in chemical kinetics: A method for the treatment of experimental data React. Kinet. Catal. Lett. 33, 357-362
33. Myers, J. K., Pace, C. N., and Martin Scholtz, J. (1995) Denaturant m -values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding Protein Sci. 4, 2138-2148
34. Silow, M. and Oliveberg, M. (1997) Transient aggregates in protein folding are easily mistaken for folding intermediates Proc. Natl. Acad. Sci. U.S.A. 94, 6084-6086
35. Stryer, L. (1965) The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites J. Mol. Biol. 13, 482-495
36. Jones, B. E., Jennings, P. A., Pierre, R. A., and Matthews, C. R. (1994) Development of nonpolar surfaces in the folding of Escherichia coli dihydrofolate reductase detected by 1-anilinonaphthalene-8-sulfonate binding Biochemistry 33, 15250-15258
37. Lorenz, T. and Reinstein, J. (2008) The influence of proline isomerization and off-pathway intermediates on the folding mechanism of eukaryotic UMP/CMP kinase J. Mol. Biol. 381, 443-455
38. Hammond, G. S. (1955) A correlation of reaction rates J. Am. Chem. Soc. 77, 334-338
39. Oliveberg, M., Tan, Y.-J., Silow, M., and Fersht, A. R. (1998) The changing nature of the protein folding transition state: Implications for the shape of the free-energy profile for folding J. Mol. Biol. 277, 933-943
40. Silow, M. and Oliveberg, M. (1997) High-energy channeling in protein folding Biochemistry 36, 7633-7637
41. Zoldak, G., Carstensen, L., Scholz, C., and Schmid, F. X. (2009) Consequences of domain insertion on the stability and folding mechanism of a protein J. Mol. Biol. 386, 1138-1152
42. 8-barrel enzyme into two folded halves Nat. Struct. Biol. 8, 32-36
43. Sterner, R. and Liebl, W. (2001) Thermophilic adaptation of proteins Crit. Rev. Biochem. Mol. Biol. 36, 39-106
44. Bachmann, A. and Kiefhaber, T. (2001) Apparent two-state Tendamistat folding is a sequential process along a defined route J. Mol. Biol. 306, 375-386
45. Ptitsyn, O. B. (1995) Molten globule and protein folding Adv. Protein Chem. 47, 83-229
46. Wensley, B. G., Gärtner, M., Choo, W. X., Batey, S., and Clarke, J. (2009) Different members of a simple three-helix bundle protein family have very different folding rate constants and fold by different mechanisms J. Mol. Biol. 390, 1074-1085
47. Friel, C. T., Capaldi, A. P., and Radford, S. E. (2003) 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, 293-305
48. Olofsson, M., Hansson, S., Hedberg, L., Logan, D. T., and Oliveberg, M. (2007) Folding of S6 structures with divergent amino acid composition: Pathway flexibility within partly overlapping foldons J. Mol. Biol. 365, 237-248
49. Lappalainen, I., Hurley, M. G., and Clarke, J. (2008) Plasticity within the obligatory folding nucleus of an immunoglobulin-like domain J. Mol. Biol. 375, 547-559
50. Lam, A. R., Borreguero, J. M., Ding, F., Dokholyan, N. V., Buldyrev, S. V., Stanley, H. E., and Shakhnovich, E. (2007) Parallel folding pathways in the SH3 domain protein J. Mol. Biol. 373, 1348-1360
51. Wu, Y., Vadrevu, R., Kathuria, S., Yang, X., and Matthews, C. R. (2007) A tightly packed hydrophobic cluster directs the formation of an off-pathway sub-millisecond folding intermediate in the α subunit of tryptophan synthase, a TIM barrel protein J. Mol. Biol. 366, 1624-1638
52. Rudolph, R., Siebendritt, R., and Kiefhaber, T. (1992) Reversible unfolding and refolding behavior of a monomeric aldolase from Staphylococcus aureus Protein Sci. 1, 654-666
53. 8-barrel N-(5′-phosphoribosyl)anthranilate isomerase from Escherichia coli Biochemistry 33, 6350-6355
54. Kathuria, S. V., Day, I. J., Wallace, L. A., and Matthews, C. R. (2008) Kinetic traps in the folding of βα-repeat proteins: CheY initially misfolds before accessing the native conformation J. Mol. Biol. 382, 467-484
55. Hills, R. D., Jr., Kathuria, S. V., Wallace, L. A., Day, I. J., Brooks, C. L., III, and Matthews, C. R. (2010) Topological frustration in βα-repeat proteins: Sequence diversity modulates the conserved folding mechanisms of α/β/α sandwich proteins J. Mol. Biol. 398, 332-350
56. Höcker, B., Schmidt, S., and Sterner, R. (2002) A common evolutionary origin of two elementary enzyme folds FEBS Lett. 510, 133-135
57. Bharat, T. A. M., Eisenbeis, S., Zeth, K., and Höcker, B. (2008) A βα-barrel built by the combination of fragments from different folds Proc. Natl. Acad. Sci. U.S.A. 105, 9942-9947
58. Wu, Y. and Matthews, C. R. (2002) Parallel channels and rate-limiting steps in complex protein folding reactions: Prolyl isomerization and the α-subunit of Trp synthase, a TIM barrel protein J. Mol. Biol. 323, 309-325
59. Wu, Y. and Matthews, C. R. (2002) A cis -prolyl peptide bond isomerization dominates the folding of the α-subunit of trp synthase, a TIM barrel protein J. Mol. Biol. 322, 7-13
60. Wu, Y. and Matthews, C. R. (2003) Proline replacements and the simplification of the complex, parallel channel folding mechanism for the α-subunit of Trp synthase, a TIM barrel protein J. Mol. Biol. 330, 1131-1144
61. Saab-Rincon, G., Froebe, C. L., and Matthews, C. R. (1993) Urea-induced unfolding of the α-subunit of tryptophan synthase: One-dimensional proton NMR evidence for residual structure near histidine-92 at high denaturant concentration Biochemistry 32, 13981-13990
62. Wilmanns, M., Hyde, C. C., Davies, D. R., Kirschner, K., and Jansonius, J. N. (1991) Structural conservation in parallel (βα)-barrel enzymes that catalyze three sequential reactions in the pathway of tryptophan biosynthesis Biochemistry 30, 9161-9169
63. Rojsajjakul, T., Wintrode, P., Vadrevu, R., Robert Matthews, C., and Smith, D. L. (2004) Multi-state unfolding of the α-subunit of tryptophan synthase, a TIM barrel protein: Insights into the secondary structure of the stable equilibrium intermediates by hydrogen exchange mass spectrometry J. Mol. Biol. 341, 241-253