Equilibrium Φ-analysis of a molten globule: The 1-149 apoflavodoxin fragment

Journal of Molecular Biology

Volumn 356, Issue 2, 2006, Pages 354-366

  Lopez Llano J ^a   Campos, L A ^a   Bueno, M ^a   Sancho, J ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

Equilibrium phi analysis; Molten globule; Protein folding; Protein fragment; Protein stability

Indexed keywords

APOFLAVODOXIN; FLAVODOXIN; MUTANT PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; MATHEMATICAL ANALYSIS; MUTATIONAL ANALYSIS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE;

EID: 30744471639     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.10.086     Document Type: Article

References (76)

1. K. Kuwajima The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure Proteins: Struct. Funct. Genet. 6 1989 87 103
2. O.B. Ptitsyn Molten globule and protein folding Advan. Protein Chem. 47 1995 83 229
3. I. Nishii, M. Kataoka, and Y. Goto Thermodynamic stability of the molten globule states of apomyoglobin J. Mol. Biol. 250 1995 223 238
4. J.M. Matthews, R.S. Norton, A. Hammacher, and R.J. Simpson The single mutation Phe173→Ala induces a molten globule-like state in murine interleukin-6 Biochemistry 39 2000 1942 1950
5. H. Roder, G.A. Elove, and S.W. Englander Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR Nature 335 1988 700 704
6. K. Kuwajima The molten globule state of alpha-lactalbumin FASEB J. 10 1996 102 199
7. W. Colon, and H. Rode Kinetic intermediates in the formation of the cytochrome c molten globule Nature Struct. Biol. 3 1996 1019 1025
8. B. Zhou, K. Tian, and G. Jing An in vitro peptide folding model suggests the presence of the molten globule state during nascent peptide folding Protein Eng. 13 2000 35 39
9. P. Bai, and Z. Peng Cooperative folding of the isolated alpha-helical domain of hen egg-white lysozyme J. Mol. Biol. 314 2001 321 329
10. M. Arai, K. Ito, T. Inobe, M. Nakao, K. Maki, and K. Kamagata Fast compaction of alpha-lactalbumin during folding studied by stopped-flow X-ray scattering J. Mol. Biol. 321 2002 121 132
11. 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
12. J.A. Morrow, D.M. Hatters, B. Lu, P. Hochtl, K.A. Oberg, B. Rupp, and K.H. Weisgraber Apolipoprotein E4 forms a molten globule. A potential basis for its association with disease J. Biol. Chem. 277 2002 50380 50385
13. F.M. Hughson, D. Barrick, and R.L. Baldwin Probing the stability of a partly folded apomyoglobin intermediate by site-directed mutagenesis Biochemistry 30 1991 4113 4118
14. M.S. Kay, and R.L. Baldwin Packing interactions in the apomyglobin folding intermediate Nature Struct. Biol. 3 1996 439 445
15. L.C. Wu, and P.S. Kim Hydrophobic sequence minimization of the alpha-lactalbumin molten globule Proc. Natl Acad. Sci. USA 94 1997 14314 14319
16. Y. Luo, M.S. Kay, and R.L. Baldwin Cooperativity of folding of the apomyoglobin pH 4 intermediate studied by glycine and proline mutations Nature Struct. Biol. 4 1997 925 930
17. M.S. Kay, C.H. Ramos, and R.L. Baldwin Specificity of native-like interhelical hydrophobic contacts in the apomyoglobin intermediate Proc. Natl Acad. Sci. USA 96 1999 2007 2012
18. Y. Luo, and R.L. Baldwin The 28-111 disulfide bond constrains the alpha-lactalbumin molten globule and weakens its cooperativity of folding Proc. Natl Acad. Sci. USA 96 1999 11283 11287
19. Y. Luo, and R.L. Baldwin How Ala→Gly mutations in different helices affect the stability of the apomyoglobin molten globule Biochemistry 40 2001 5283 5289
20. E.A. Dolginova, E. Roth, I. Silman, and L.M. Weiner Chemical modification of Torpedo acetylcholinesterase by disulfides: appearance of a "molten globule" state Biochemistry 31 1992 12248 12254
21. D. Andersson, P. Hammarström, and U. Carlsson Cofactor-induced refolding: refolding of molten globule carbonic anhydrase induced by Zn(II) and Co(II) Biochemistry 40 2001 2653 2661
22. J. Sancho, and A.R. Fersht Dissection of an enzyme by protein engineering. The N and C-terminal fragments of barnase form a native-like complex with restored enzymic activity J. Mol. Biol. 224 1992 741 747
23. J. Sancho, J.L. Neira, and A.R. Fersht An N-terminal fragment of barnase has residual helical structure similar to that in a refolding intermediate J. Mol. Biol. 224 1992 749 758
24. S. Maldonado, M.A. Jimenez, G.M. Langdon, and J. Sancho Cooperative stabilization of a molten globule apoflavodoxin fragment Biochemistry 37 1998 10589 10596
25. L.A. Campos, M. Bueno, J. López-Llano, and J. Sancho Structure of stable protein folding intermediates by equilibrium φ-analysis: the apoflavodoxin thermal intermediate J. Mol. Biol. 344 2004 239 255
26. L.A. Campos, M.M. Garcia-Mira, R. Godoy-Ruiz, J.M. Sanchez-Ruiz, and J. Sancho Do proteins always benefit from a stability increase? Relevant and residual stabilisation in a three-state protein by charge optimisation J. Mol. Biol. 344 2004 223 237
27. 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
28. 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 1376 1388
29. J. Fernandez-Recio, A. Vazquez, C. Civera, P. Sevilla, and J. Sancho The tryptophan/histidine interaction in alpha-helices J. Mol. Biol. 267 1997 184 197
30. 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
31. S. Maldonado, M.P. Irun, L.A. Campos, J.A. Rubio, A. Luquita, and A. Lostao Salt-induced stabilization of apoflavodoxin at neutral pH is mediated through cation-specific effects Protein Sci. 11 2002 1260 1273
32. J. Lopez-Llano, S. Maldonado, M. Bueno, A. Lostao, M.A. Jimenez, M.P. Lillo, and J. Sancho The long and short flavodoxins. I: Role of the differentiating loop in apoflavodoxin structure and FMN binding J. Biol. Chem. 279 2004 47177 47183
33. J. Lopez-Llano, S. Maldonado, S. Jain, A. Lostao, R. Godoy-Ruiz, and J.M. Sanchez-Ruiz The long and short flavodoxins. II: role of the differentiating loop in apoflavodoxin stability and folding mechanism J. Biol. Chem. 279 2004 47184 47191
34. J. Fernandez-Recio, C.G. Genzor, and J. Sancho Apoflavodoxin folding mechanism: an alpha/beta protein with an essentially off-pathway intermediate Biochemistry 40 2001 15234 15245
35. J.K. Myers, C.N. Pace, and J.M. Scholtz Helix propensities are identical in proteins and peptides Biochemistry 36 1997 10923 10929
36. D.N. Ermolenko, J.M. Richardson, and G.I. Makhatadze Noncharged amino acid residues at the solvent-exposed positions in the middle and at the C terminus of the alpha-helix have the same helical propensity Protein Sci. 12 2003 1169 1176
37. R. Aurora, and G.D. Rose Helix capping Protein Sci. 7 1998 21 38
38. S. Penel, R.G. Morrison, R.J. Mortishire-Smith, and A.J. Doig Periodicity in alpha-helix lengths and C-capping preferences J. Mol. Biol. 293 1999 1211 1219
39. M. Petukhov, K. Uegaki, N. Yumoto, and L. Serrano Amino acid intrinsic alpha-helical propensities III: positional dependence at several positions of C terminus Protein Sci. 11 2002 766 777
40. T. Alber, J.A. Bell, D.P. Sun, H. Nicholson, J.A. Wozniak, S. Cook, and B.W. Matthews Replacements of Pro86 in phage T4 lysozyme extend an alpha-helix but do not alter protein stability Science 239 1988 631 635
41. V.E. Bychkova, R.H. Pain, and O.B. Ptitsyn The "molten globule" state is involved in the translocation of proteins across membranes? FEBS Letters 238 1988 231 234
42. 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
43. V.E. Bychkova, R. Berni, G.L. Rossi, V.P. Kutyshenko, and O.B. Ptitsyn Retinol-binding protein is in the molten globule state at low pH Biochemistry 31 1992 7566 7571
44. V.N. Uversky, N.V. Narizhneva, T.V. Ivanova, M.D. Kirkitadze, and A.Yu. Tomashevski Ligand-free form of human alpha-fetoprotein: evidence for the molten globule state FEBS Letters 410 1997 280 284
45. 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
46. V.E. Bychkova, and O.B. Ptitsyn Folding intermediates are involved in genetic diseases? FEBS Letters 359 1995 6 8
47. S. Ramboarina, and C. Redfield Structural characterisation of the human alpha-lactalbumin molten globule at high temperature J. Mol. Biol. 330 2003 1177 1188
48. Y.O. Kamatari, R. Kitahara, H. Yamada, S. Yokoyama, and K. Akasaka High-pressure NMR spectroscopy for characterizing folding intermediates and denatured states of proteins Methods 34 2004 133 143
49. M.M. Krishna, L. Hoang, Y. Lin, and S.W. Englander Hydrogen exchange methods to study protein folding Methods 34 2004 51 64
50. C. Redfield Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins Methods 34 2004 121 132
51. 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
52. 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
53. 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
54. D.A. Dolgikh, L.V. Abaturov, I.A. Bolotina, E.V. Brazhnikov, V.E. Bychkova, and R.I. Gilmanshin Compact state of a protein molecule with pronounced small-scale mobility: bovine alpha-lactalbumin Eur. Biophys. J. 13 1985 109 121
55. V.N. Uversky, and O.B. Ptitsyn All-or-none solvent-induced transitions between native, molten globule and unfolded states in globular proteins Fold. Des. 1 1996 117 122
56. M. Jamin, and R.L. Baldwin Refolding and unfolding kinetics of the equilibrium folding intermediate of apomyoglobin Nature Struct. Biol. 3 1996 613 618
57. F. Edwin, Y.V. Sharma, and M.V. Jagannadham Stabilization of molten globule state of papain by urea Biochem. Biophys. Res. Commun. 290 2002 1441 1446
58. M. Ferrer, G. Barany, and C. Woodward Partially folded, molten globule and molten coil states of bovine pancreatic trypsin inhibitor Nature Struct. Biol. 2 1995 211 217
59. V.N. Uversky Cracking the folding code. Why do some proteins adopt partially folded conformations, whereas other don't? FEBS Letters 514 2002 181 183
60. T. Kiefhaber, and R.L. Baldwin Intrinsic stability of individual alpha helices modulates structure and stability of the apomyoglobin molten globule form J. Mol. Biol. 252 1995 122 132
61. L.C. Wu, Z.Y. Peng, and P.S. Kim Bipartite structure of the alpha-lactalbumin molten globule Nature Struct. Biol. 2 1995 281 286
62. D. Barrick, and R.L. Baldwin Stein and Moore Award address. The molten globule intermediate of apomyoglobin and the process of protein folding Protein Sci. 2 1993 869 876
63. J.P. Waltho, V.A. Feher, G. Merutka, H.J. Dyson, and P.E. Wright Peptide models of protein folding initiation sites. 1. Secondary structure formation by peptides corresponding to the G- and H-helices of myoglobin Biochemistry 32 1993 6337 6347
64. J.H. Carra, E.A. Anderson, and P.L. Privalov Thermodynamics of staphylococcal nuclease denaturation. II. The A-state Protein Sci. 3 1994 952 959
65. W. Colon, G.A. Elove, L.P. Wakem, F. Sherman, and H. Roder Side chain packing of the N- and C-terminal helices plays a critical role in the kinetics of cytochrome c folding Biochemistry 35 1996 5538 5549
66. J.L. Marmorino, M. Lehti, and G.J. Pielak Native tertiary structure in an A-state J. Mol. Biol. 275 1998 379 388
67. M. Mizuguchi, K. Masaki, M. Demura, and K. Nitta Local and long-range interactions in the molten globule state: a study of chimeric proteins of bovine and human alpha-lactalbumin J. Mol. Biol. 298 2000 985 995
68. 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
69. F.W. Studier, A.H. Rosenberg, J.J. Dunn, and J.W. Dubendorff Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol. 185 1990 60 89
70. F. Sanger, S. Nicklen, and A.R. Coulson DNA sequencing with chain-terminating inhibitors Proc. Natl Acad. Sci. USA 74 1977 5463 5467
71. E. Monsellier, and H. Bedouelle Quantitative measurement of protein stability from unfolding equilibria monitored with the fluorescence maximum wavelength Protein Eng. Des. Sel. 18 2005 445 456
72. P.L. Privalov Stability of proteins: small globular proteins Advan. Protein Chem. 33 1979 167 241
73. C.N. Pace, B.A. Shirley, and J.A. Thomson Measuring the conformational stability of a protein T.E. Creighton Protein Structure: A Practical Approach 1989 IRL Press Oxford 311 330
74. C.N. Pace Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131 1986 266 280
75. 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
76. J.M. Beechem Global analysis of biochemical and biophysical data Methods Enzymol. 210 1992 37 54