Structural analysis of an equilibrium folding intermediate in the apoflavodoxin native ensemble by small-angle X-ray scattering

Journal of Molecular Biology

Volumn 406, Issue 4, 2011, Pages 604-619

  Ayuso Tejedor, Sara ^a   García Fandiño, Rebeca ^b,c   Orozco, Modesto ^b,d   Sancho, Javier ^a,e   Bernadó, Pau ^b  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c UNIVERSITY OF A CORUÑA   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e CSIC   (Spain)

Author keywords

flavodoxin; folding intermediate; protein folding; restrained molecular dynamics; small angle X ray scattering

Indexed keywords

APOFLAVODOXIN; FLAVODOXIN; HOLOFLAVODOXIN; UNCLASSIFIED DRUG;

ANABAENA; ARTICLE; CALORIMETRY; CHEMICAL STRUCTURE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE; SIMULATION; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; THERMOSTABILITY; WILD TYPE; X RAY CRYSTALLOGRAPHY;

NOSTOC SP. PCC 7119;

EID: 79951675082     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.12.027     Document Type: Article

References (91)

1. Bernado P., Blackledge M., and Sancho J. Sequence-specific solvent accessibilities of protein residues in unfolded protein ensembles Biophys. J. 91 2006 4536 4543 (Pubitemid 44904238)
2. Bernado P., Blanchard L., Timmins P., Marion D., Ruigrok R.W., and Blackledge M. A structural model for unfolded proteins from residual dipolar couplings and small-angle X-ray scattering Proc. Natl Acad. Sci. USA 102 2005 17002 17007 (Pubitemid 41692673)
3. Fitzkee N.C., and Rose G.D. Reassessing random-coil statistics in unfolded proteins Proc. Natl Acad. Sci. USA 101 2004 12497 12502 (Pubitemid 39122052)
4. Goldenberg D.P. Computational simulation of the statistical properties of unfolded proteins J. Mol. Biol. 326 2003 1615 1633 (Pubitemid 36269097)
5. Jha A.K., Colubri A., Freed K.F., and Sosnick T.R. Statistical coil model of the unfolded state: resolving the reconciliation problem Proc. Natl Acad. Sci. USA 102 2005 13099 13104 (Pubitemid 41324985)
6. Zhou H.X. Polymer models of protein stability, folding, and interactions Biochemistry 43 2004 2141 2154
7. Estrada J., Bernado P., Blackledge M., and Sancho J. ProtSA: a web application for calculating sequence specific protein solvent accessibilities in the unfolded ensemble BMC Bioinf. 10 2009 104
8. Meier S., Blackledge M., and Grzesiek S. Conformational distributions of unfolded polypeptides from novel NMR techniques J. Chem. Phys. 128 2008 052204
9. Kohn J.E., Millett I.S., Jacob J., Zagrovic B., Dillon T.M., and Cingel N. Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl Acad. Sci. USA 101 2004 12491 12496 (Pubitemid 39122051)
10. Mohana-Borges R., Goto N.K., Kroon G.J., Dyson H.J., and Wright P.E. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings J. Mol. Biol. 340 2004 1131 1142 (Pubitemid 38968706)
11. Brockwell D.J., and Radford S.E. Intermediates: ubiquitous species on folding energy landscapes? Curr. Opin. Struct. Biol. 17 2007 30 37 (Pubitemid 46240814)
12. Cremades N., Velazquez-Campoy A., Martinez-Julvez M., Neira J.L., Perez-Dorado I., and Hermoso J. Discovery of specific flavodoxin inhibitors as potential therapeutic agents against Helicobacter pylori infection ACS Chem. Biol. 4 2009 928 938
13. Bahar I., Chennubhotla C., and Tobi D. Intrinsic dynamics of enzymes in the unbound state and relation to allosteric regulation Curr. Opin. Struct. Biol. 17 2007 633 640 (Pubitemid 350180409)
14. Dobson C.M. Protein folding and misfolding Nature 426 2003 884 890 (Pubitemid 38056880)
15. Dyson H.J., and Wright P.E. Unfolded proteins and protein folding studied by NMR Chem. Rev. 104 2004 3607 3622
16. Redfield C. Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins Methods 34 2004 121 132 (Pubitemid 38996781)
17. Vallurupalli P., Hansen D.F., Stollar E., Meirovitch E., and Kay L.E. Measurement of bond vector orientations in invisible excited states of proteins Proc. Natl Acad. Sci. USA 104 2007 18473 18477 (Pubitemid 350210721)
18. Korzhnev D.M., Salvatella X., Vendruscolo M., Di Nardo A.A., Davidson A.R., Dobson C.M., and Kay L.E. Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR Nature 430 2004 586 590 (Pubitemid 38998635)
19. Vendruscolo M. Determination of conformationally heterogeneous states of proteins Curr. Opin. Struct. Biol. 17 2007 15 20 (Pubitemid 46240813)
20. Doniach S. Changes in biomolecular conformation seen by small angle X-ray scattering Chem. Rev. 101 2001 1763 1778 (Pubitemid 35377802)
21. Bernado P., Mylonas E., Petoukhov M.V., Blackledge M., and Svergun D.I. Structural characterization of flexible proteins using small-angle X-ray scattering J. Am. Chem. Soc. 129 2007 5656 5664 (Pubitemid 46697655)
22. Mylonas E., Hascher A., Bernado P., Blackledge M., Mandelkow E., and Svergun D.I. Domain conformation of tau protein studied by solution small-angle X-ray scattering Biochemistry 47 2008 10345 10353
23. Hoffmann A., Kane A., Nettels D., Hertzog D.E., Baumgartel P., and Lengefeld J. Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy Proc. Natl Acad. Sci. USA 104 2007 105 110 (Pubitemid 46067992)
24. Kuzmenkina E.V., Heyes C.D., and Nienhaus G.U. Single-molecule Förster resonance energy transfer study of protein dynamics under denaturing conditions Proc. Natl Acad. Sci. USA 102 2005 15471 15476 (Pubitemid 41528081)
25. Choy W.Y., Mulder F.A., Crowhurst K.A., Muhandiram D.R., Millett I.S., and Doniach S. Distribution of molecular size within an unfolded state ensemble using small-angle X-ray scattering and pulse field gradient NMR techniques J. Mol. Biol. 316 2002 101 112 (Pubitemid 34729269)
26. Yan S., Gawlak G., Smith J., Silver L., Koide A., and Koide S. Conformational heterogeneity of an equilibrium folding intermediate quantified and mapped by scanning mutagenesis J. Mol. Biol. 338 2004 811 825 (Pubitemid 38507424)
27. Campos L.A., Bueno M., Lopez-Llano J., Jimenez M.A., and Sancho J. Structure of stable protein folding intermediates by equilibrium phi-analysis: the apoflavodoxin thermal intermediate J. Mol. Biol. 344 2004 239 255 (Pubitemid 39422385)
28. Ayuso-Tejedor S., Angarica V.E., Bueno M., Campos L.A., Abián O., and Bernado P. Design and structure of an equilibrium protein folding intermediate. A hint into dynamical regions of proteins J. Mol. Biol. 400 2010 922 934
29. Gsponer J., Hopearuoho H., Whittaker S.B., Spence G.R., Moore G.R., and Paci E. Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7 Proc. Natl Acad. Sci. USA 103 2006 99 104 (Pubitemid 43076111)
30. Koch M.H., Vachette P., and Svergun D.I. Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution Q. Rev. Biophys. 36 2003 147 227 (Pubitemid 37493573)
31. Svergun D.I., and Koch M.H.J. Small-angle scattering studies of biological macromolecules in solution Rep. Prog. Phys. 66 2003 1735 1782 (Pubitemid 37365734)
32. Petoukhov M.V., and Svergun D.I. Analysis of X-ray and neutron scattering from biomacromolecular solutions Curr. Opin. Struct. Biol. 17 2007 562 571 (Pubitemid 350041656)
33. Svergun D.I., and Koch M.H. Advances in structure analysis using small-angle scattering in solution Curr. Opin. Struct. Biol. 12 2002 654 660 (Pubitemid 35449075)
34. Segel D.J., Fink A.L., Hodgson K.O., and Doniach S. Protein denaturation: a small-angle X-ray scattering study of the ensemble of unfolded states of cytochrome c Biochemistry 37 1998 12443 12451 (Pubitemid 28427528)
35. Perez J., Vachette P., Russo D., Desmadril M., and Durand D. Heat-induced unfolding of neocarzinostatin, a small all-beta protein investigated by small-angle X-ray scattering J. Mol. Biol. 308 2001 721 743 (Pubitemid 32573705)
36. Akiyama S., Takahashi S., Kimura T., Ishimori K., Morishima I., Nishikawa Y., and Fujisawa T. Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle X-ray scattering Proc. Natl Acad. Sci. USA 99 2002 1329 1334 (Pubitemid 34136493)
37. Kimura T., Uzawa T., Ishimori K., Morishima I., Takahashi S., and Konno T. Specific collapse followed by slow hydrogen-bond formation of beta-sheet in the folding of single-chain monellin Proc. Natl Acad. Sci. USA 102 2005 2748 2753 (Pubitemid 40299864)
38. Uzawa T., Akiyama S., Kimura T., Takahashi S., Ishimori K., Morishima I., and Fujisawa T. Collapse and search dynamics of apomyoglobin folding revealed by submillisecond observations of alpha-helical content and compactness Proc. Natl Acad. Sci. USA 101 2004 1171 1176 (Pubitemid 38182661)
39. Arai M., Ikura T., Semisotnov G.V., Kihara H., Amemiya Y., and Kuwajima K. Kinetic refolding of beta-lactoglobulin. Studies by synchrotron X-ray scattering, and circular dichroism, absorption and fluorescence spectroscopy J. Mol. Biol. 275 1998 149 162 (Pubitemid 28022394)
40. Arai M., Ito K., Inobe T., Nakao M., Maki K., and Kamagata K. Fast compaction of alpha-lactalbumin during folding studied by stopped-flow X-ray scattering J. Mol. Biol. 321 2002 121 132 (Pubitemid 34948474)
41. Sancho J. Flavodoxins: sequence, folding, binding, function and beyond Cell. Mol. Life Sci. 63 2006 855 864
42. Cremades N., Bueno M., Toja M., and Sancho J. Towards a new therapeutic target: Helicobacter pylori flavodoxin Biophys. Chem. 115 2005 267 276 (Pubitemid 40327070)
43. Irun M.P., Garcia-Mira M.M., Sanchez-Ruiz J.M., and Sancho J. Native hydrogen bonds in a molten globule: the apoflavodoxin thermal intermediate J. Mol. Biol. 306 2001 877 888 (Pubitemid 33027707)
44. Genzor C.G., Perales-Alcon A., Sancho J., and Romero A. Closure of a tyrosine/tryptophan aromatic gate leads to a compact fold in apo flavodoxin Nat. Struct. Biol. 3 1996 329 332 (Pubitemid 26112630)
45. Bollen Y.J., Kamphuis M.B., and van Mierlo C.P. The folding energy landscape of apoflavodoxin is rugged: hydrogen exchange reveals nonproductive misfolded intermediates Proc. Natl Acad. Sci. USA 103 2006 4095 4100
46. Bueno M., Cremades N., Neira J.L., and Sancho J. Filling small, empty protein cavities: structural and energetic consequences J. Mol. Biol. 358 2006 701 712
47. Campos L.A., Garcia-Mira M.M., Godoy-Ruiz R., Sanchez-Ruiz J.M., and Sancho J. 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 (Pubitemid 39422384)
48. Campos L.A., and Sancho J. Native-specific stabilization of flavodoxin by the FMN cofactor: structural and thermodynamical explanation Proteins 63 2006 581 594
49. Guinier A. La Diffraction des Rayons X aux Très Faibles Angles: Applications à l'Etude des Phénomènes Ultra-microscopiques Ann. Phys. (Paris) 12 1939 161 237
50. Svergun D., Barberato C., and Koch M.H.J. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates J. Appl. Crystallogr. 28 1995 768 773 (Pubitemid 3014671)
51. Svergun D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25 1992 495 503 (Pubitemid 23564996)
52. Jolliffe I.T. Principal Component Analysis Springer edit. (Springer) 2002 Springer New York, NY
53. Tauler R., Smilde A., and Kowalski B. Selectivity, local rank, 3-way data-analysis and ambiguity in multivariate curve resolution J. Chemom. 9 1995 31 58
54. Tauler R. Multivariate curve resolution applied to second order data Chemom. Intell. Lab. Syst. 30 1995 133 146
55. de Juan A., and Tauler R. Chemometrics applied to unravel multicomponent processes and mixtures-revisiting latest trends in multivariate resolution Anal. Chim. Acta 500 2003 195 210 (Pubitemid 37487780)
56. de Juan A., and Tauler R. Multivariate curve resolution (MCR) from 2000: progress in concepts and applications Crit. Rev. Anal. Chem. 36 2006 163 176 (Pubitemid 44889524)
57. Jaumot J., Gargallo R., de Juan A., and Tauler R. A graphical user-friendly interface for MCR-ALS: a new tool for multivariate curve resolution in MATLAB Chemom. Intell. Lab. Syst. 76 2005 101 110 (Pubitemid 40342915)
58. Bueno M., Campos L.A., Estrada J., and Sancho J. Energetics of aliphatic deletions in protein cores Protein Sci. 15 2006 1858 1872 (Pubitemid 44141504)
59. Lopez-Llano J., Campos L.A., Bueno M., and Sancho J. Equilibrium phi-analysis of a molten globule: the 1-149 apoflavodoxin fragment J. Mol. Biol. 356 2006 354 366 (Pubitemid 43099976)
60. Religa T.L., Markson J.S., Mayor U., Freund S.M., and Fersht A.R. Solution structure of a protein denatured state and folding intermediate Nature 437 2005 1053 1056 (Pubitemid 41486989)
61. Paci E., Lindorff-Larsen K., Dobson C.M., Karplus M., and Vendruscolo M. Transition state contact orders correlate with protein folding rates J. Mol. Biol. 352 2005 495 500 (Pubitemid 41225462)
62. Salvatella X., Dobson C.M., Fersht A.R., and Vendruscolo M. Determination of the folding transition states of barnase by using PhiI-value-restrained simulations validated by double mutant PhiIJ-values Proc. Natl Acad. Sci. USA 102 2005 12389 12394 (Pubitemid 41266369)
63. Varnai P., Dobson C.M., and Vendruscolo M. Determination of the transition state ensemble for the folding of ubiquitin from a combination of Phi and Psi analyses J. Mol. Biol. 377 2008 575 588
64. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486 (Pubitemid 126706801)
65. Lopez-Llano J., Maldonado S., Bueno M., Lostao A., Angeles-Jimenez M., Lillo M.P., and Sancho J. The long and short flavodoxins: I. The role of the differentiating loop in apoflavodoxin structure and FMN binding J. Biol. Chem. 279 2004 47177 47183 (Pubitemid 39518374)
66. Lostao A., Daoudi F., Irun M.P., Ramon A., Fernandez-Cabrera C., Romero A., and Sancho J. How FMN binds to Anabaena apoflavodoxin: a hydrophobic encounter at an open binding site J. Biol. Chem. 278 2003 24053 24061 (Pubitemid 36830238)
67. Hall D.A., Vander Kooi C.W., Stasik C.N., Stevens S.Y., Zuiderweg E.R., and Matthews R.G. Mapping the interactions between flavodoxin and its physiological partners flavodoxin reductase and cobalamin-dependent methionine synthase Proc. Natl Acad. Sci. USA 98 2001 9521 9526 (Pubitemid 32769336)
68. Boynton T.O., Daugherty L.E., Dailey T.A., and Dailey H.A. Identification of Escherichia coli HemG as a novel, menadione-dependent flavodoxin with protoporphyrinogen oxidase activity Biochemistry 48 2009 6705 6711
69. Martinez-Julvez M., Cremades N., Bueno M., Perez-Dorado I., Maya C., and Cuesta-Lopez S. Common conformational changes in flavodoxins induced by FMN and anion binding: the structure of Helicobacter pylori apoflavodoxin Proteins 69 2007 581 594 (Pubitemid 47623873)
70. Fillat M.F., Borrias W.E., and Weisbeek P.J. Isolation and overexpression in Escherichia coli of the flavodoxin gene from Anabaena PCC 7119 Biochem. J. 280 1991 187 191
71. Privalov P.L. Stability of proteins: small globular proteins Adv. Protein Chem. 33 1979 167 241
72. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., and Svergun D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36 2003 1277 1282
73. Malinowski E.R. Factor Analysis in Chemistry 3rd edit. 2002 Wiley-Interscience New York, NY
74. Blobel J., Bernado P., Svergun D.I., Tauler R., and Pons M. Low-resolution structures of transient protein-protein complexes using small-angle X-ray scattering J. Am. Chem. Soc. 131 2009 4378 4386
75. Alexandrescu A.T., Evans P.A., Pitkeathly M., Baum J., and Dobson C.M. Structure and dynamics of the acid-denatured molten globule state of alpha-lactalbumin: a two-dimensional NMR study Biochemistry 32 1993 1707 1718 (Pubitemid 23066443)
76. Chamberlain A.K., and Marqusee S. Molten globule unfolding monitored by hydrogen exchange in urea Biochemistry 37 1998 1736 1742 (Pubitemid 28099795)
77. Eliezer D., Yao J., Dyson H.J., and Wright P.E. Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding Nat. Struct. Biol. 5 1998 148 155 (Pubitemid 28086916)
78. Ramboarina S., and Redfield C. Structural characterisation of the human alpha-lactalbumin molten globule at high temperature J. Mol. Biol. 330 2003 1177 1188 (Pubitemid 36818912)
79. Schulman B.A., Kim P.S., Dobson C.M., and Redfield C. A residue-specific NMR view of the non-cooperative unfolding of a molten globule Nat. Struct. Biol. 4 1997 630 634 (Pubitemid 27323445)
80. Zhang O., Forman-Kay J.D., Shortle D., and Kay L.E. 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 (Pubitemid 127715708)
81. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., and Karplus M. CHARMM-a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
82. Lazaridis T., and Karplus M. Effective energy function for proteins in solution Proteins 35 1999 133 152 (Pubitemid 29165128)
83. Nose S. A unified formulation of the constant temperature molecular-dynamics methods J. Chem. Phys. 81 1984 511 519
84. Hoover W.G. Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
85. Paci E., and Karplus M. Forced unfolding of fibronectin type 3 modules: an analysis by biased molecular dynamics simulations J. Mol. Biol. 288 1999 441 459 (Pubitemid 29221813)
86. Geierhaas C.D., Best R.B., Paci E., Vendruscolo M., and Clarke J. Structural comparison of the two alternative transition states for folding of TI I27 Biophys. J. 91 2006 263 275 (Pubitemid 44015326)
87. Gelpi J.L., Kalko S.G., Barril X., Cirera J., de La Cruz X., Luque F.J., and Orozco M. Classical molecular interaction potentials: improved setup procedure in molecular dynamics simulations of proteins Proteins 45 2001 428 437 (Pubitemid 33108077)
88. Darden T., York D., and Pedersen L. Particle Mesh Ewald-an N•log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
89. Andersen H.C. Rattle-a velocity version of the shake algorithm for molecular-dynamics calculations J. Comput. Phys. 52 1983 24 34
90. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., and Villa E. Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
91. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., and Field M.J. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616 (Pubitemid 128576688)