Structure of stable protein folding intermediates by equilibrium φ-analysis: The apoflavodoxin thermal intermediate

Journal of Molecular Biology

Volumn 344, Issue 1, 2004, Pages 239-255

  Campos, Luis A ^a   Bueno, Marta ^a   Lopez Llano, Jon ^a   Jiménez, María Ángeles ^b   Sancho, Javier ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

Author keywords

equilibrium intermediate; protein folding; protein stability; thermal unfolding; analysis

Indexed keywords

FLAVODOXIN;

ANALYTIC METHOD; ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON TRANSPORT; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; TEMPERATURE DEPENDENCE; THREE DIMENSIONAL IMAGING; X RAY CRYSTALLOGRAPHY;

EID: 7044231161     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.08.081     Document Type: Article

References (55)

1. J. Baum, C.M. Dobson, P.A. Evans, and C. Hanley Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig alpha-lactalbumin Biochemistry 28 1989 7 13
2. D. Hamada, M. Hoshino, M. Kataoka, A.L. Fink, and Y. Goto Intermediate conformational states of apocytochrome c Biochemistry 32 1993 10351 10358
3. V.N. Uversky, and O.B. Ptitsyn "Partly folded" state, a new equilibrium state of protein molecules: four-state guanidinium chloride-induced unfolding of beta-lactamase at low temperature Biochemistry 33 1994 2782 2791
4. H. Zhu, S.A. Celinski, J.M. Scholtz, and J.C. Hu An engineered leucine zipper a position mutant with an unusual three-state unfolding pathway Protein Sci. 10 2001 24 33
5. I. Pedroso, M.P. Irun, C. Machicado, and J. Sancho Four-state equilibrium unfolding of an scFv antibody fragment Biochemistry 41 2002 9873 9884
6. S.A. Hobart, D.W. Meinhold, R. Osuna, and W. Colon From two-state to three-state: the effect of the P61A mutation on the dynamics and stability of the factor for inversion stimulation results in an altered equilibrium denaturation mechanism Biochemistry 41 2002 13744 13754
7. B.R. Rami, G. Krishnamoorthy, and J.B. Udgaonkar Dynamics of the core tryptophan during the formation of a productive molten globule intermediate of barstar Biochemistry 42 2003 7986 8000
8. L.A. Campos, and J. Sancho The active site of pepsin is formed in the intermediate conformation dominant at mildly acidic pH FEBS Letters 538 2003 89 95
9. S.M. Martins, A. Chapeaurouge, and S.T. Ferreira Folding intermediates of the prion protein stabilized by hydrostatic pressure and low temperature J. Biol. Chem. 278 2003 50449 50455
10. R.J. Ellis, and S.M. van der Vies Molecular chaperones Annu. Rev. Biochem. 60 1991 321 347
11. N. Plesofsky-Vig, and R. Brambl Disruption of the gene for hsp30, an alpha-crystallin-related heat shock protein of Neurospora crassa, causes defects in thermotolerance Proc. Natl Acad. Sci. USA 92 1995 5032 5036
12. D.A. Parsell, A.S. Kowal, M.A. Singer, and S. Lindquist Protein disaggregation mediated by heat-shock protein Hsp104 Nature 372 2002 475 478
13. P.J. Thomas, B.H. Qu, and P.L. Pedersen Defective protein folding as a basis of human disease Trends Biochem. Sci. 20 1995 456 459
14. S.B. Prusiner Prions Proc. Natl Acad. Sci. USA 95 1998 13363 13383
15. F.G. van der Goot, J.M. Gonzalez-Manas, J.H. Lakey, and F. Pattus A "molten-globule" membrane-insertion intermediate of the pore-forming domain of colicin A Nature 354 1991 408 410
16. V.E. Bychkova, R. Berni, G.L. Rossi, P. Kutyshenko, and O.B. Ptitsyn Retinol-binding protein is in the molten globule state at low pH Biochemistry 31 1992 7566 7571
17. V.N. Uversky, N.V. Narizhneva, T.V. Ivanova, M.D. Kirkitadze, and A.Y. Tomashevski Ligand-free form of human-fetoprotein: evidence for the molten globule state FEBS Letters 410 1997 280 284
18. S. Cai, and B.R. Singh Role of the disulfide cleavage induced molten globule state of type A botulinum neurotoxin in its endopeptidase activity Biochemistry 40 2001 15327 15333
19. A.T. Alexandrescu, P.A. Evans, M. Pitkeathly, J. Baum, and C.M. Dobson Structure and dynamics of the acid-denatured molten globule state of alpha-lactalbumin: a two-dimensional NMR study Biochemistry 32 1993 1707 1718
20. B.A. Schulman, P.S. Kim, C.M. Dobson, and C. Redfield A residue-specific NMR view of the non-cooperative unfolding of a molten globule Nature Struct. Biol. 4 1997 630 634
21. O. Zhang, J.D. Forman-Kay, D. Shortle, and L.E. Kay Triple-resonance NOESY-based experiments with improved spectral resolution: applications to structural characterization of unfolded, partially folded and folded proteins J. Biomol. NMR 9 1997 181 200
22. A.K. Chamberlain, and S. Marqusee Molten globule unfolding monitored by hydrogen exchange in urea Biochemistry 37 1998 1736 1742
23. D. Eliezer, J. Yao, J.H. Dyson, and P.E. Wright Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding Nature Struct. Biol. 5 1998 148 155
24. S. Ramboarina, and C. Redfield Structural characterisation of the human α-lactalbumin molten globule at high temperature J. Mol. Biol. 330 2003 1177 1188
25. A.R. Fersht, A. Matouschek, and L. Serrano 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
26. A. Matouschek, J.T. Kellis Jr, L. Serrano, and A.R. Fersht Mapping the transition state and pathway of protein folding by protein engineering Nature 340 1989 122 126
27. A. Matouschek, J.T. Kellis Jr, L. Serrano, M. Bycroft, and A.R. Fersht Transient folding intermediates characterized by protein engineering Nature 346 1990 440 445
28. M.P. Irun, M.M. Garcia-Mira, J.M. Sanchez-Ruiz, and J. Sancho Native hydrogen bonds in a molten globule: the apoflavodoxin thermal intermediate J. Mol. Biol. 306 2001 877 888
29. C.G. Genzor, A. Perales-Alcon, J. Sancho, and A. Romero Closure of a tyrosine/tryptophan aromatic gate leads to a compact fold in apoflavodoxin Nature Struct. Biol. 3 1996 329 332
30. G.M. Langdon, M.A. Jimenez, C.G. Genzor, S. Maldonado, J. Sancho, and M. Rico Anabaena apoflavodoxin hydrogen exchange: on the stable exchange core of the alpha/beta(21345) flavodoxin-like family Proteins: Struct. Funct. Genet. 43 2001 476 488
31. Campos, L. A., Garcia-Mira, M. M., Godoy-Ruiz, R., Sanchez-Ruiz, J. M. & Sancho, J. (2004). Do proteins always benefit from a stability increase? Relevant and residual stabilization in a three-state protein by charge optimization. J. Mol. Biol., in press.
32. S. Vuilleumier, J. Sancho, R. Loewenthal, and A.R. Fersht Circular dichroism studies of barnase and its mutants: characterization of the contribution of aromatic side chains Biochemistry 32 1993 10303 10313
33. C.G. Genzor, A. Beldarrain, C. Gomez-Moreno, J.L. Lopez-Lacomba, M. Cortijo, and J. Sancho Conformational stability of apoflavodoxin Protein Sci. 5 1996 1373 1388
34. Pace, C. N., Shirley, B. A. & Thomson, J. A. (1989). Measuring the conformational stability of a protein. In Protein Structure: A Practical Approach, pp. 311-330, IRL Press, Oxford.
35. I.E. Sanchez, and T. Kiefhaber Origin of unusual phi-values in protein folding: evidence against specific nucleation sites J. Mol. Biol. 334 2003 1077 1085
36. A.R. Fersht, and S. Sato Phi-value analysis and the nature of protein-folding transition states Proc. Natl Acad. Sci. USA 101 2004 7976 7981
37. A. Lostao, M. El Harrous, F. Daoudi, A. Romero, A. Parody-Morreale, and J. Sancho Dissecting the energetics of the apoflavodoxin-FMN complex J. Biol. Chem. 275 2000 9518 9526
38. C.P. van Mierlo, W.M. van Dongen, F. Vergeldt, W.J. van Berkel, and E. Steensma The equilibrium unfolding of Azotobacter vinelandii apoflavodoxin II occurs via a relatively stable folding intermediate Protein Sci. 7 1998 2331 2344
39. D. Eliezer, J. Chung, H.J. Dyson, and P.E. Wright Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin Biochemistry 39 2000 2894 2901
40. S.W. Englander, and N.R. Kallenbach Hydrogen exchange and structural dynamics of proteins and nucleic acids Quart. Rev. Biophys. 16 1984 521 655
41. Y. Bai, J.S. Milne, L. Mayne, and S.W. Englander Primary structure effects on peptide group hydrogen exchange Proteins: Struct. Funct. Genet. 17 1993 75 86
42. S.W. Englander, T.R. Sosnick, J.J. Englander, and L. Mayne Mechanisms and uses of hydrogen exchange Curr. Opin. Struct. Biol. 6 1996 18 23
43. R. Li, and C. Woodward The hydrogen exchange core and protein folding Protein Sci. 8 1999 1571 1590
44. L.M. Gloss, and C.R. Matthews Urea and thermal equilibrium denaturation studies on the dimerization domain of Escherichia coli Trp repressor Biochemistry 36 1997 5612 5623
45. J. Sancho, M. Bueno, L.A. Campos, J. Fernandez-Recio, M.P. Irun, and J. Lopez The relevant stability of proteins with equilibrium intermediates Sci. World 2 2002 1209 1215
46. M.F. Fillat, W.E. Borrias, and P.J. Weisbeek Isolation and overexpression in Escherichia coli of the flavodoxin gene from Anabaena PCC 7119 Biochem. J. 280 1991 187 191
47. M.M. Santoro, and D.W. Bolen Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27 1988 8063 8068
48. M.P. Irun, S. Maldonado, and J. Sancho Stabilization of apoflavodoxin by replacing hydrogen-bonded charged Asp or Glu residues by the neutral isosteric Asn or Gln Protein Eng. 14 2001 173 181
49. P.L. Privalov Stability of proteins: small globular proteins Advan. Protein Chem. 33 1979 167 241
50. J.M. Beechem Global analysis of biochemical and biophysical data Methods Enzymol. 210 1992 37 54
51. R. Fraczkiewicz, and W. Braun Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules J. Comput. Chem. 19 1998 319 333
52. M. Rance Improved techniques for homonuclear rotating frame and isotropic mixing experiments J. Magn. Reson. 74 1987 557 564
53. J. Jeener, B.H. Meier, P. Bachmann, and R.R. Ernst Investigation of exchange processes by two-dimensional NMR spectroscopy J. Chem. Phys. 71 1979 4546 4553
54. A. Kumar, R.R. Ernst, and K. Wüthrich A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules Biochem. Biophys. Res. Commun. 95 1980 1 6
55. A.G. Redfield, and S.D. Kuntz Quadrature Fourier NMR detection: Simple multiplex for dual detection J. Magn. Reson. 19 1975 250 254