The folding of spectrin domains I: Wild-type domains have the same stability but very different kinetic properties

Journal of Molecular Biology

Volumn 344, Issue 1, 2004, Pages 195-205

  Scott, Kathryn A ^a   Batey, Sarah ^a   Hooton, Karen A ^a   Clarke, Jane ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

helix bundle; homologue; protein folding; residual structure; spectrin

Indexed keywords

FODRIN; ISOPROTEIN; SPECTRIN;

ARTICLE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; WILD TYPE;

GALLUS GALLUS;

EID: 7044226061     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.09.037     Document Type: Article

References (59)

1. K.W. Plaxco, K.T. Simons, and D. Baker Contact order, transition state placement and the refolding rates of single domain proteins J. Mol. Biol. 277 1998 985 994
2. K.W. Plaxco, K.T. Simons, I. Ruczinski, and B. David Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics Biochemistry 39 2000 11177 11183
3. M. Lindberg, J. Tangrot, and M. Oliveberg Complete change of the protein folding transition state upon circular permutation Nature Struct. Biol. 9 2002 818 822
4. K. Gunasekaran, S.J. Eyles, A.T. Hagler, and L.M. Gierasch Keeping it in the family: folding studies of related proteins Curr. Opin. Struct. Biol. 11 2001 83 93
5. S. Gianni, N.R. Guydosh, F. Khan, T.D. Caldas, U. Mayor, and G.W.N. White Unifying features in protein-folding mechanisms Proc. Natl Acad. Sci. USA 100 2003 13286 13291
6. Scott, K.A., Randles, L.G., Clarke, J. (2004). The folding of spectrin domains II. Φ-value analysis of R16. J. Mol. Biol. 344 (this issue).
7. D.W. Speicher, and V.T. Marchesi Erythrocyte spectrin is comprised of many homologous triple helical segments Nature 311 1984 177 180
8. E. Winograd, D. Hume, and D. Branton Phasing the conformational unit of spectrin Proc. Natl Acad. Sci. USA 88 1991 10788 10791
9. Y. Yan, E. Winograd, A. Viel, T. Cronin, S.C. Harrison, and D. Branton Crystal-structure of the repetitive segments of spectrin Science 262 1993 2027 2030
10. J. Pascual, M. Pfuhl, G. Rivas, A. Pastore, and M. Saraste The spectrin repeat folds into a three-helix bundle in solution FEBS Letters 383 1996 201 207
11. J. Pascual, M. Pfuhl, D. Walther, M. Saraste, and M. Nilges Solution structure of the spectrin repeat: a left-handed antiparallel triple-helical coiled-coil J. Mol. Biol. 273 1997 740 751
12. A. Bateman, L. Coin, R. Durbin, R.D. Finn, V. Hollich, and S. Griffiths-Jones The Pfam protein families database Nucl. Acids Res. 32 2004 D138 D141
13. R.I. MacDonald, and J.A. Cummings Stabilities of folding of clustered, two-repeat fragments of spectrin reveal a potential hinge in the human erythroid spectrin tetramer Proc. Natl Acad. Sci. USA 101 2004 1502 1507
14. R.I. MacDonald, and E.V. Pozharski Free energies of urea and of thermal unfolding show that two tandem repeats of spectrin are thermodynamically more stable than a single repeat Biochemistry 40 2001 3974 3984
15. N. Menhart, T. Mitchell, D. Lusitani, N. Topouzian, and L.W.M. Fung Peptides with more than one 106-amino acid sequence motif are needed to mimic the structural stability of spectrin J. Biol. Chem. 271 1996 30410 30416
16. J. Ylanne, K. Scheffzek, P. Young, and M. Saraste Crystal structure of the alpha-actinin rod reveals an extensive torsional twist Structure 9 2001 597 604
17. V.L. Grum, D.N. Li, R.I. MacDonald, and A. Mondragon Structures of two repeats of spectrin suggest models of flexibility Cell 98 1999 523 535
18. M. Rief, J. Pascual, M. Saraste, and H.E. Gaub Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles J. Mol. Biol. 286 1999 553 561
19. P.F. Lenne, A.J. Raae, S.M. Altmann, M. Saraste, and J.K.H. Horber States and transitions during forced unfolding of a single spectrin repeat FEBS Letters 476 2000 124 128
20. E. Paci, and M. Karplus Unfolding proteins by external forces and temperature: the importance of topology and energetics Proc. Natl Acad. Sci. USA 97 2000 6521 6526
21. R.I. MacDonald, A. Musacchio, R.A. Holmgren, and M. Saraste Invariant tryptophan at a shielded site promotes folding of the conformational unit of spectrin Proc. Natl Acad. Sci. USA 91 1994 1299 1303
22. T. Mitchell, N. Menhart, M. Meerson, N. Topouzian, and L.W.M. Fung Spectrin domain stability as measured solvent denaturation: Implications for minimum domain Biophys. J. 70 1996 TU232 TU232
23. R. Law, P. Carl, S. Harper, P. Daleheimer, D.W. Speicher, and D.E. Discher Cooperativity in forced unfolding of tandem spectrin repeats Biophys. J. 84 2003 533 544
24. R. Law, G. Liao, S. Harper, G. Yang, D.W. Speicher, and D.E. Discher Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains Biophys. J. 85 2003 3286 3293
25. I.E. Sanchez, and T. Kiefhaber Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding J. Mol. Biol. 325 2003 367 376
26. M.A. Seeliger, S.E. Breward, and L.S. Itzhaki 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
27. D.E. Otzen, and M. Oliveberg 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
28. M. Oliveberg Characterisation of the transition states for protein folding: towards a new level of mechanistic detail in protein engineering analysis Curr. Opin. Struct. Biol. 11 2001 94 100
29. M. Oliveberg Alternative explanations for "multistate" kinetics in protein folding: transient aggregation and changing transition-state ensembles Accts Chem. Res. 31 1998 765 772
30. J.F. Brandts, H.R. Halvorson, and M. Brennan Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues Biochemistry 14 1975 4953 4963
31. F.X. Schmid, and R.L. Baldwin Acid catalysis of the formation of the slow-folding species of RNas A: evidence that the reaction is proline isomerization Proc. Natl Acad. Sci. USA 10 1978 4764 4768
32. P.S. Kim, and R.L. Baldwin Intermediates in the folding reactions of small proteins Ann. Rev. Biochem. 59 1990 631 660
33. F. Chiti, N. Taddei, E. Giannoni, N.A.J. van Nuland, G. Ramponi, and C.M. Dobson Development of enzymatic activity during protein folding - detection of a spectroscopically silent native-like intermediate of muscle acylphosphatase J. Biol. Chem. 274 1999 20151 20158
34. H. Lilie, R. Rudolph, and J. Buchner Association of antibody chains at different stages of folding: prolyl isomerisation occurs after formation of quaternary structure J. Mol. Biol. 248 1995 190 201
35. F.X. Schmid Mechanism of folding of ribnuclease A. Slow refolding is a sequential reaction via structural intermediates Biochemistry 22 1983 4690 4696
36. G. Pappenberger, H. Aygun, J.W. Engels, U. Reimer, G. Fischer, and T. Kiefhaber Nonprolyl cis peptide bonds in unfolded proteins cause complex folding kinetics Nature Struct. Biol. 8 2001 452 458
37. M. Silow, and M. Oliveberg High-energy channeling in protein folding Biochemistry 36 1997 7633 7637
38. A. Matouschek, D.E. Otzen, L.S. Itzhaki, S.E. Jackson, and A.R. Fersht Movement of the position of the transition state in protein folding Biochemistry 34 1995 13656 13662
39. M. Oliveberg, Y.J. Tan, M. Silow, and A.R. Fersht The changing nature of the protein folding transition state: Implications for the shape of the free-energy profile for folding J. Mol. Biol. 277 1998 933 943
40. D.E. Otzen, O. Kristensen, M. Proctor, and M. Oliveberg Structural changes in the transition state of protein folding: alternative interpretations of curved chevron plots Biochemistry 38 1999 6499 6511
41. T. Ternstrom, U. Mayor, M. Akke, and M. Oliveberg 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. A. Bachmann, and T. Kiefhaber Apparent two-state tendamistat folding is a sequential process along a defined route J. Mol. Biol. 306 2001 375 386
43. V. Munoz, and L. Serrano Development of the multiple sequence approximation within the agadir model of alpha-helix formation. Comparison with Zimm-Bragg and Lifson-Roig formalisms Biopolymers 41 1997 495 509
44. E. Lacroix, A.R. Viguera, and L. Serrano Elucidating the folding problem of alpha-helices: local motifs, long-range electrostatics, ionic-strength dependence and prediction of NMR parameters J. Mol. Biol. 284 1998 173 191
45. V. Munoz, and L. Serrano Elucidating the folding problem of helical peptides using empirical parameters. III. Temperature and pH dependence J. Mol. Biol. 245 1995 297 308
46. V. Munoz, and L. Serrano Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides J. Mol. Biol. 245 1995 275 296
47. J. Clarke, E. Cota, S.B. Fowler, and S.J. Hamill Folding studies of immunoglobulin-like beta-sandwich proteins suggest that they share a common folding pathway Struct. Fold. Des. 7 1999 1145 1153
48. K.A. Scott, A. Steward, S.B. Fowler, and J. Clarke Titin; a multidomain protein that behaves as the sum of its parts J. Mol. Biol. 315 2002 819 829
49. G. Calloni, N. Taddei, K.W. Plaxco, G. Ramponi, M. Stefani, and F. Chiti Comparison of the folding processes of distantly related proteins. Importance of hydrophobic content in folding J. Mol. Biol. 330 2003 577 591
50. D. Baker A surprising simplicity to protein folding Nature 405 2000 39 42
51. N. Ferguson, and A.R. Fersht Early events in protein folding Curr. Opin. Struct. Biol. 13 2003 75 81
52. C.T. Friel, A.P. Capaldi, and S.E. Radford 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
53. S.B. Fowler, and J. Clarke 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
54. C.F. Wright, K. Lindorff-Larsen, L.G. Randles, and J. Clarke Parallel protein-unfolding pathways revealed and mapped Nature Struct. Biol. 10 2003 658 662
55. S.J. Hamill, A.E. Meekhof, and J. Clarke 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
56. S.J. Hamill, A. Steward, and J. Clarke 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
57. E. Cota, A. Steward, S.B. Fowler, and J. Clarke 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
58. B. Miroux, and J.E. Walker Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels J. Mol. Biol. 260 1996 289 298
59. C.N. Pace Determination and analysis of urea and guanidinium hydrochloride denaturation curves Methods Enzymol. 131 1986 266 280