Molecular mechanisms of the anomalous thermal aggregation of green fluorescent protein

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 12, 2011, Pages 1930-1939

  Melnik, Bogan S ^a   Molochkov, Nikolay V ^b   Prokhorov, Dmitry A ^a   Uversky, Vladimir N ^c,d   Kutyshenko, Viktor P ^b  

^a INSTITUTE OF PROTEIN RESEARCH   (Russian Federation)

^b INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Carbonic anhydrase II; Green fluorescent protein; NMR; Protein association; Protein solvent interaction; Spin diffusion

Indexed keywords

CARBONATE DEHYDRATASE II; GREEN FLUORESCENT PROTEIN; WATER;

ARTICLE; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE;

ANIMALS; CATTLE; CHEMICAL PRECIPITATION; DIFFUSION; GREEN FLUORESCENT PROTEINS; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SOLVENTS; TEMPERATURE; THERMODYNAMICS; WATER;

BOVINAE;

EID: 81755184322     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.07.017     Document Type: Article

References (130)

1. M. Zimmer Green fluorescent protein (GFP): applications, structure, and related photophysical behavior Chem. Rev. 102 2002 759 781 (Pubitemid 35377613)
2. S. Delagrave, R.E. Hawtin, C.M. Silva, M.M. Yang, and D.C. Youvan Red-shifted excitation mutants of the green fluorescent protein Biotechnology (N Y) 13 1995 151 154
3. R. Heim, D.C. Prasher, and R.Y. Tsien Wavelength mutations and posttranslational autoxidation of green fluorescent protein Proc. Natl. Acad. Sci. U. S. A. 91 1994 12501 12504
4. R. Heim, and R.Y. Tsien Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer Curr. Biol. 6 1996 178 182
5. M. Ormo, A.B. Cubitt, K. Kallio, L.A. Gross, R.Y. Tsien, and S.J. Remington Crystal structure of the Aequorea victoria green fluorescent protein Science 273 1996 1392 1395 (Pubitemid 26296528)
6. A. Crameri, E.A. Whitehorn, E. Tate, and W.P. Stemmer Improved green fluorescent protein by molecular evolution using DNA shuffling Nat. Biotechnol. 14 1996 315 319
7. M.V. Matz, A.F. Fradkov, Y.A. Labas, A.P. Savitsky, A.G. Zaraisky, M.L. Markelov, and S.A. Lukyanov Fluorescent proteins from nonbioluminescent Anthozoa species Nat. Biotechnol. 17 1999 969 973 (Pubitemid 29474851)
8. A.F. Fradkov, Y. Chen, L. Ding, E.V. Barsova, M.V. Matz, and S.A. Lukyanov Novel fluorescent protein from Discosoma coral and its mutants possesses a unique far-red fluorescence FEBS Lett. 479 2000 127 130 (Pubitemid 30616419)
9. M.V. Matz, K.A. Lukyanov, and S.A. Lukyanov Family of the green fluorescent protein: journey to the end of the rainbow Bioessays 24 2002 953 959 (Pubitemid 35180850)
10. Y.A. Labas, N.G. Gurskaya, Y.G. Yanushevich, A.F. Fradkov, K.A. Lukyanov, S.A. Lukyanov, and M.V. Matz Diversity and evolution of the green fluorescent protein family Proc. Natl. Acad. Sci. U. S. A. 99 2002 4256 4261 (Pubitemid 34285973)
11. J. Wiedenmann, C. Elke, K.D. Spindler, and W. Funke Cracks in the beta-can: fluorescent proteins from Anemonia sulcata (Anthozoa, Actinaria) Proc. Natl. Acad. Sci. U. S. A. 97 2000 14091 14096 (Pubitemid 32016535)
12. K.A. Lukyanov, A.F. Fradkov, N.G. Gurskaya, M.V. Matz, Y.A. Labas, A.P. Savitsky, M.L. Markelov, A.G. Zaraisky, X. Zhao, Y. Fang, W. Tan, and S.A. Lukyanov Natural animal coloration can be determined by a nonfluorescent green fluorescent protein homolog J. Biol. Chem. 275 2000 25879 25882
13. N.G. Gurskaya, A.F. Fradkov, A. Terskikh, M.V. Matz, Y.A. Labas, V.I. Martynov, Y.G. Yanushevich, K.A. Lukyanov, and S.A. Lukyanov GFP-like chromoproteins as a source of far-red fluorescent proteins FEBS Lett. 507 2001 16 20 (Pubitemid 33000290)
14. N.G. Gurskaya, A.P. Savitsky, Y.G. Yanushevich, S.A. Lukyanov, and K.A. Lukyanov Color transitions in coral's fluorescent proteins by site-directed mutagenesis BMC Biochem. 2 2001 6
15. A. Terskikh, A. Fradkov, G. Ermakova, A. Zaraisky, P. Tan, A.V. Kajava, X. Zhao, S. Lukyanov, M. Matz, S. Kim, I. Weissman, and P. Siebert "Fluorescent timer": protein that changes color with time Science 290 2000 1585 1588
16. Y.G. Yanushevich, D.B. Staroverov, A.P. Savitsky, A.F. Fradkov, N.G. Gurskaya, M.E. Bulina, K.A. Lukyanov, and S.A. Lukyanov A strategy for the generation of non-aggregating mutants of Anthozoa fluorescent proteins FEBS Lett. 511 2002 11 14 (Pubitemid 34127814)
17. B.J. Bevis, and B.S. Glick Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed) Nat. Biotechnol. 20 2002 83 87 (Pubitemid 34044920)
18. F.V. Subach, G.H. Patterson, S. Manley, J.M. Gillette, J. Lippincott-Schwartz, and V.V. Verkhusha Photoactivatable mCherry for high-resolution two-color fluorescence microscopy Nat. Methods 6 2009 153 159
19. F.V. Subach, G.H. Patterson, M. Renz, J. Lippincott-Schwartz, and V.V. Verkhusha Bright monomeric photoactivatable red fluorescent protein for two-color super-resolution sptPALM of live cells J. Am. Chem. Soc. 132 2010 6481 6491
20. K.S. Morozova, K.D. Piatkevich, T.J. Gould, J. Zhang, J. Bewersdorf, and V.V. Verkhusha Far-red fluorescent protein excitable with red lasers for flow cytometry and superresolution STED nanoscopy Biophys. J. 99 2010 L13 L15
21. F.V. Subach, L. Zhang, T.W. Gadella, N.G. Gurskaya, K.A. Lukyanov, and V.V. Verkhusha Red fluorescent protein with reversibly photoswitchable absorbance for photochromic FRET Chem. Biol. 17 2010 745 755
22. U. Lauf, P. Lopez, and M.M. Falk Expression of fluorescently tagged connexins: a novel approach to rescue function of oligomeric DsRed-tagged proteins FEBS Lett. 498 2001 11 15 (Pubitemid 32522882)
23. V.V. Verkhusha, H. Otsuna, T. Awasaki, H. Oda, S. Tsukita, and K. Ito An enhanced mutant of red fluorescent protein DsRed for double labeling and developmental timer of neural fiber bundle formation J. Biol. Chem. 276 2001 29621 29624
24. H. Mizuno, A. Sawano, P. Eli, H. Hama, and A. Miyawaki Red fluorescent protein from Discosoma as a fusion tag and a partner for fluorescence resonance energy transfer Biochemistry 40 2001 2502 2510 (Pubitemid 32171724)
25. O.V. Stepanenko, V.V. Verkhusha, I.M. Kuznetsova, V.N. Uversky, and K.K. Turoverov Fluorescent proteins as biomarkers and biosensors: throwing color lights on molecular and cellular processes Curr. Protein Pept. Sci. 9 2008 338 369
26. D.A. Shagin, E.V. Barsova, Y.G. Yanushevich, A.F. Fradkov, K.A. Lukyanov, Y.A. Labas, T.N. Semenova, J.A. Ugalde, A. Meyers, J.M. Nunez, E.A. Widder, S.A. Lukyanov, and M.V. Matz GFP-like proteins as ubiquitous metazoan superfamily: evolution of functional features and structural complexity Mol. Biol. Evol. 21 2004 841 850 (Pubitemid 38529726)
27. R.Y. Tsien The green fluorescent protein Annu. Rev. Biochem. 67 1998 509 544 (Pubitemid 28411137)
28. N.C. Shaner, P.A. Steinbach, and R.Y. Tsien A guide to choosing fluorescent proteins Nat. Methods 2 2005 905 909 (Pubitemid 43108726)
29. R.M. Wachter, M.A. Elsliger, K. Kallio, G.T. Hanson, and S.J. Remington Structural basis of spectral shifts in the yellow-emission variants of green fluorescent protein Structure 6 1998 1267 1277 (Pubitemid 28485959)
30. F. Yang, L.G. Moss, and G.N. Phillips Jr. The molecular structure of green fluorescent protein Nat. Biotechnol. 14 1996 1246 1251 (Pubitemid 26332784)
31. B.S. Melnik, T.V. Povarnitsyna, and T.N. Melnik Can the fluorescence of green fluorescent protein chromophore be related directly to the nativity of protein structure? Biochem. Biophys. Res. Commun. 390 2009 1167 1170
32. O.V. Stepanenko, V.V. Verkhusha, V.I. Kazakov, M.M. Shavlovsky, I.M. Kuznetsova, V.N. Uversky, and K.K. Turoverov Comparative studies on the structure and stability of fluorescent proteins EGFP, zFP506, mRFP1, "dimer2", and DsRed1 Biochemistry 43 2004 14913 14923 (Pubitemid 39587467)
33. C.A. Schiffer, and V. Dotsch The role of protein-solvent interactions in protein unfolding Curr. Opin. Biotechnol. 7 1996 428 432 (Pubitemid 26265624)
34. L. Costenaro, and C. Ebel Thermodynamic relationships between protein-solvent and protein-protein interactions Acta. Crystallogr. D Biol. Crystallogr. 58 2002 1554 1559 (Pubitemid 35181046)
35. Y. Kita, T. Arakawa, T.Y. Lin, and S.N. Timasheff Contribution of the surface free energy perturbation to protein-solvent interactions Biochemistry 33 1994 15178 15189
36. R. Murugan Competitive model on denaturant-mediated protein unfolding Biophys. J. 84 2003 770 774 (Pubitemid 36138755)
37. V.P. Denisov, B.H. Jonsson, and B. Halle Hydration of denatured and molten globule proteins Nat. Struct. Biol. 6 1999 253 260 (Pubitemid 29107228)
38. M. Tarek, and D.J. Tobias Single-particle and collective dynamics of protein hydration water: a molecular dynamics study Phys. Rev. Lett. 89 2002 275501
39. M. Gottschalk, K. Venu, and B. Halle Protein self-association in solution: the bovine pancreatic trypsin inhibitor decamer Biophys. J. 84 2003 3941 3958 (Pubitemid 36644147)
40. M. Lund, and B. Jonsson A mesoscopic model for protein-protein interactions in solution Biophys. J. 85 2003 2940 2947 (Pubitemid 37345784)
41. J. Brnjas-Kraljevic, G. Pifat, and S. Maricic Quaternary structure, hydration, and self-association of hemoglobin. A proton magnetic relaxation study Physiol Chem. Phys. 11 1979 371 376
42. V.P. Kutyshenko, and M. Cortijo Water-protein interactions in the molten-globule state of carbonic anhydrase b: an NMR spin-diffusion study Protein Sci. 9 2000 1540 1547 (Pubitemid 30659192)
43. V.P. Kutyshenko, D.A. Prokhorov, and V.S. Khristoforov A study of interactions of carbonic anhydrase B with water and urea. I. Spin-diffusion parameters that determine individual and cooperative properties of molecules Biofizika 50 2005 641 647
44. D.A. Prokhorov, V.P. Kutyshenko, and V.S. Khristoforov Carbonic anhydrase B interactions with water and urea Mol. Biol. (Mosk) 39 2005 497 503
45. S. Lindskog Structure and mechanism of carbonic anhydrase Pharmacol. Ther. 74 1997 1 20 (Pubitemid 27337350)
46. A. Liljas, K.K. Kannan, P.C. Bergsten, I. Waara, K. Fridborg, B. Strandberg, U. Carlbom, L. Jarup, S. Lovgren, and M. Petef Crystal structure of human carbonic anhydrase C Nat. New Biol. 235 1972 131 137
47. K.K. Kannan, B. Notstrand, K. Fridborg, S. Lovgren, A. Ohlsson, and M. Petef Crystal structure of human erythrocyte carbonic anhydrase B. Three-dimensional structure at a nominal 2.2-A resolution Proc. Natl. Acad. Sci. U. S. A. 72 1975 51 55
48. V. Kumar, and K.K. Kannan Enzyme-substrate interactions. Structure of human carbonic anhydrase I complexed with bicarbonate J. Mol. Biol. 241 1994 226 232
49. V. Kumar, K. Sankaran, and K.K. Kannan Crystallization and preliminary data of Indian buffalo erythrocyte carbonic anhydrase J. Mol. Biol. 190 1986 129 131
50. A.E. Eriksson, and A. Liljas Refined structure of bovine carbonic anhydrase III at 2.0 A resolution Proteins 16 1993 29 42 (Pubitemid 23129870)
51. P.A. Boriack-Sjodin, R.W. Heck, P.J. Laipis, D.N. Silverman, and D.W. Christianson Structure determination of murine mitochondrial carbonic anhydrase V at 2.45-A resolution: implications for catalytic proton transfer and inhibitor design Proc. Natl. Acad. Sci. U. S. A. 92 1995 10949 10953
52. J.S. Richardson The anatomy and taxonomy of protein structure Adv. Protein Chem. 34 1981 167 339
53. A. Yazgan, and R.W. Henkens Role of zinc (II) in the refolding of guanidine hydrochloride denatured bovine carbonic anhydrase Biochemistry 11 1972 1314 1318
54. K.P. Wong, and C. Tanford Denaturation of bovine carbonic anhydrase B by guanidine hydrochloride. A process involving separable sequential conformational transitions J. Biol. Chem. 248 1973 8518 8523
55. R.W. Henkens, B.B. Kitchell, S.C. Lottich, P.J. Stein, and T.J. Williams Detection and characterization using circular dichroism and fluorescence spectroscopy of a stable intermediate conformation formed in the denaturation of bovine carbonic anhydrase with guanidinium chloride Biochemistry 21 1982 5918 5923
56. K.P. Wong, and L.M. Hamlin Acid denaturation of bovine carbonic anhydrase B Biochemistry 13 1974 2678 2683
57. D.A. Dolgikh, L.V. Abaturov, Brazhnikov, Iu.O. Lebedev, and Iu.N. Chirgadze Acid form of carbonic anhydrase: "molten globule" with a secondary structure Dokl. Akad. Nauk SSSR 272 1983 1481 1484
58. U. Carlsson, L.E. Henderson, and S. Lindskog Denaturation and reactivation of human carbonic anhydrases in guanidine hydrochloride and urea Biochim. Biophys. Acta 310 1973 376 387
59. L.G. Martensson, B.H. Jonsson, P.O. Freskgard, A. Kihlgren, M. Svensson, and U. Carlsson Characterization of folding intermediates of human carbonic anhydrase II: probing substructure by chemical labeling of SH groups introduced by site-directed mutagenesis Biochemistry 32 1993 224 231 (Pubitemid 23033340)
60. L.G. Martensson, P. Jonasson, P.O. Freskgard, M. Svensson, U. Carlsson, and B.H. Jonsson Contribution of individual tryptophan residues to the fluorescence spectrum of native and denatured forms of human carbonic anhydrase II Biochemistry 34 1995 1011 1021
61. M. Svensson, P. Jonasson, P.O. Freskgard, B.H. Jonsson, M. Lindgren, L.G. Martensson, M. Gentile, K. Boren, and U. Carlsson Mapping the folding intermediate of human carbonic anhydrase II. Probing substructure by chemical reactivity and spin and fluorescence labeling of engineered cysteine residues Biochemistry 34 1995 8606 8620
62. B.P. Ko, A. Yazgan, P.L. Yeagle, S.C. Lottich, and R.W. Henkens Kinetics and mechanism of refolding of bovine carbonic anhydrase. A probe study of the formation of the active site Biochemistry 16 1977 1720 1725 (Pubitemid 8081475)
63. L.F. McCoy Jr., and K.P. Wong Denaturation of cobalt-carbonic anhydrase B from bovine erythrocyte Biopolymers 18 1979 2893 2904 (Pubitemid 10194971)
64. L.F. McCoy Jr., E.S. Rowe, and K.P. Wong Multiparameter kinetic study on the unfolding and refolding of bovine carbonic anhydrase B Biochemistry 19 1980 4738 4743
65. P.J. Stein, and R.W. Henkens Detection of intermediates in protein folding of carbonic anhydrase with fluorescence emission and polarization J. Biol. Chem. 253 1978 8016 8018 (Pubitemid 9086278)
66. N.A. Rodionova, G.V. Semisotnov, V.P. Kutyshenko, V.N. Uverskii, and I.A. Bolotina Staged equilibrium of carbonic anhydrase unfolding in strong denaturants Mol. Biol. (Mosk) 23 1989 683 692 (Pubitemid 19245358)
67. N.A. Bushmarina, I.M. Kuznetsova, A.G. Biktashev, K.K. Turoverov, and V.N. Uversky Partially folded conformations in the folding pathway of bovine carbonic anhydrase II: a fluorescence spectroscopic analysis ChemBioChem 2 2001 813 821 (Pubitemid 33722673)
68. V.N. Uverskii, and O.B. Ptitsyn Three-stage equilibrium unfolding of small globular proteins by denaturing agents. I. Carboanhydrase B Mol. Biol. (Mosk) 30 1996 1124 1134
69. V.N. Uversky, and O.B. Ptitsyn Further evidence on the equilibrium "pre-molten globule state": four-state guanidinium chloride-induced unfolding of carbonic anhydrase B at low temperature J. Mol. Biol. 255 1996 215 228
70. A.K. Dunker, E. Garner, S. Guilliot, P. Romero, K. Albrecht, J. Hart, Z. Obradovic, C. Kissinger, and J.E. Villafranca Protein disorder and the evolution of molecular recognition: theory, predictions and observations Pac. Symp. Biocomput. 1998 473 484
71. P. Romero, Z. Obradovic, C.R. Kissinger, J.E. Villafranca, E. Garner, S. Guilliot, and A.K. Dunker Thousands of proteins likely to have long disordered regions Pac. Symp. Biocomput. 1998 437 448
72. P.E. Wright, and H.J. Dyson Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm J. Mol. Biol. 293 1999 321 331 (Pubitemid 29516173)
73. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41 2000 415 427
74. A.K. Dunker, J.D. Lawson, C.J. Brown, R.M. Williams, P. Romero, J.S. Oh, C.J. Oldfield, A.M. Campen, C.M. Ratliff, K.W. Hipps, J. Ausio, M.S. Nissen, R. Reeves, C. Kang, C.R. Kissinger, R.W. Bailey, M.D. Griswold, W. Chiu, E.C. Garner, and Z. Obradovic Intrinsically disordered protein J. Mol. Graph. Model. 19 2001 26 59 (Pubitemid 32411501)
75. A.K. Dunker, and Z. Obradovic The protein trinity-linking function and disorder Nat. Biotechnol. 19 2001 805 806
76. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533 (Pubitemid 35279598)
77. A.K. Dunker, C.J. Brown, J.D. Lawson, L.M. Iakoucheva, and Z. Obradovic Intrinsic disorder and protein function Biochemistry 41 2002 6573 6582 (Pubitemid 34547347)
78. A.K. Dunker, C.J. Brown, and Z. Obradovic Identification and functions of usefully disordered proteins Adv. Protein Chem. 62 2002 25 49 (Pubitemid 35204867)
79. L.M. Iakoucheva, C.J. Brown, J.D. Lawson, Z. Obradovic, and A.K. Dunker Intrinsic disorder in cell-signaling and cancer-associated proteins J. Mol. Biol. 323 2002 573 584 (Pubitemid 35283681)
80. V.N. Uversky Natively unfolded proteins: a point where biology waits for physics Protein Sci. 11 2002 739 756 (Pubitemid 34241284)
81. V.N. Uversky What does it mean to be natively unfolded? Eur. J. Biochem. 269 2002 2 12 (Pubitemid 34107333)
82. V.N. Uversky Protein folding revisited. A polypeptide chain at the folding-misfolding-nonfolding cross-roads: which way to go? Cell Mol. Life Sci. 60 2003 1852 1871 (Pubitemid 37222583)
83. H.J. Dyson, and P.E. Wright Coupling of folding and binding for unstructured proteins Curr. Opin. Struct. Biol. 12 2002 54 60 (Pubitemid 34142721)
84. A.L. Fink Natively unfolded proteins Curr. Opin. Struct. Biol. 15 2005 35 41 (Pubitemid 40249507)
85. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 2005 197 208 (Pubitemid 40314921)
86. P. Tompa The interplay between structure and function in intrinsically unstructured proteins FEBS Lett. 579 2005 3346 3354 (Pubitemid 40804685)
87. A.K. Dunker, M.S. Cortese, P. Romero, L.M. Iakoucheva, and V.N. Uversky Flexible nets. The roles of intrinsic disorder in protein interaction networks FEBS J. 272 2005 5129 5148 (Pubitemid 41503146)
88. V.N. Uversky, C.J. Oldfield, and A.K. Dunker Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling J. Mol. Recognit. 18 2005 343 384 (Pubitemid 41341287)
89. P. Radivojac, L.M. Iakoucheva, C.J. Oldfield, Z. Obradovic, V.N. Uversky, and A.K. Dunker Intrinsic disorder and functional proteomics Biophys. J. 92 2007 1439 1456 (Pubitemid 46393458)
90. M. Sickmeier, J.A. Hamilton, T. LeGall, V. Vacic, M.S. Cortese, A. Tantos, B. Szabo, P. Tompa, J. Chen, V.N. Uversky, Z. Obradovic, and A.K. Dunker DisProt: the database of disordered proteins Nucleic Acids Res. 35 2007 D786 D793
91. T. Le Gall, P.R. Romero, M.S. Cortese, V.N. Uversky, and A.K. Dunker Intrinsic disorder in the Protein Data Bank J. Biomol. Struct. Dyn. 24 2007 325 342
92. S. Vucetic, H. Xie, L.M. Iakoucheva, C.J. Oldfield, A.K. Dunker, Z. Obradovic, and V.N. Uversky Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions J. Proteome Res. 6 2007 1899 1916 (Pubitemid 46814513)
93. H. Xie, S. Vucetic, L.M. Iakoucheva, C.J. Oldfield, A.K. Dunker, Z. Obradovic, and V.N. Uversky Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins J. Proteome Res. 6 2007 1917 1932 (Pubitemid 46814514)
94. H. Xie, S. Vucetic, L.M. Iakoucheva, C.J. Oldfield, A.K. Dunker, V.N. Uversky, and Z. Obradovic Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions J. Proteome Res. 6 2007 1882 1898 (Pubitemid 46814512)
95. M.S. Cortese, V.N. Uversky, and A. Keith Dunker Intrinsic disorder in scaffold proteins: getting more from less Prog. Biophys. Mol. Biol. 98 2008 85 106
96. A.K. Dunker, C.J. Oldfield, J. Meng, P. Romero, J.Y. Yang, J.W. Chen, V. Vacic, Z. Obradovic, and V.N. Uversky The unfoldomics decade: an update on intrinsically disordered proteins BMC Genomics 9 Suppl 2 2008 S1
97. A.K. Dunker, I. Silman, V.N. Uversky, and J.L. Sussman Function and structure of inherently disordered proteins Curr. Opin. Struct. Biol. 18 2008 756 764
98. A.K. Dunker, and V.N. Uversky Signal transduction via unstructured protein conduits Nat. Chem. Biol. 4 2008 229 230 (Pubitemid 351414840)
99. M. Fuxreiter, P. Tompa, I. Simon, V.N. Uversky, J.C. Hansen, and F.J. Asturias Malleable machines take shape in eukaryotic transcriptional regulation Nat. Chem. Biol. 4 2008 728 737
100. V.N. Uversky, C.J. Oldfield, and A.K. Dunker Intrinsically disordered proteins in human diseases: introducing the D2 concept Annu. Rev. Biophys. 37 2008 215 246
101. F. Ferron, S. Longhi, B. Canard, and D. Karlin A practical overview of protein disorder prediction methods Proteins 65 2006 1 14 (Pubitemid 44320610)
102. Z. Dosztanyi, M. Sandor, P. Tompa, and I. Simon Prediction of protein disorder at the domain level Curr. Protein Pept. Sci. 8 2007 161 171 (Pubitemid 46681753)
103. Z. Dosztanyi, and P. Tompa Prediction of protein disorder Methods Mol. Biol. 426 2008 103 115
104. L. Li, V.N. Uversky, A.K. Dunker, and S.O. Meroueh A computational investigation of allostery in the catabolite activator protein J. Am. Chem. Soc. 129 2007 15668 15676
105. S. Liang, L. Li, W.-Y. Hsu, Y. Zhou, A.K. Dunker, V.N. Uversky, and S.O. Meroueh Exploring the molecular design of protein interaction sites with molecular dynamics simulations and free energy calculations Biochemistry 48 2009 399 414
106. V.P. Kutyshenko, D.A. Prokhorov, M.A. Timchenko, Y.A. Kudrevatykh, L.V. Gushchina, V.S. Khristoforov, V.V. Filimonov, and V.N. Uversky Solution structure and dynamics of the chimeric SH3 domains, SHH- and SHA-"Bergeracs" Biochim. Biophys. Acta. 1794 2009 1813 1822
107. F. Khan, K. Stott, and S. Jackson 1H, 15N and 13C backbone assignment of the green fluorescent protein (GFP) J. Biomol. NMR 26 2003 281 282
108. J. Georgescu, T. Rehm, J. Wiehler, B. Steipe, and T.A. Holak Backbone H(N), N, C(alpha) and C(beta) assignment of the GFPuv mutant J. Biomol. NMR 25 2003 161 162
109. H. Fukuda, M. Arai, and K. Kuwajima Folding of green fluorescent protein and the cycle3 mutant Biochemistry 39 2000 12025 12032
110. W.W. Ward, and S.H. Bokman Reversible denaturation of Aequorea green-fluorescent protein: physical separation and characterization of the renatured protein Biochemistry 21 1982 4535 4540
111. J.M. Armstrong, D.V. Myers, J.A. Verpoorte, and J.T. Edsall Purification and properties of human erythrocyte carbonic anhydrases J. Biol. Chem. 241 1966 5137 5149
112. C.N. Pace Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131 1986 266 280 (Pubitemid 16002205)
113. T.E. Creighton Electrophoretic analysis of the unfolding of proteins by urea J. Mol. Biol. 129 1979 235 264
114. T.E. Creighton, and R.H. Pain Unfolding and refolding of Staphylococcus aureus penicillinase by urea-gradient electrophoresis J. Mol. Biol. 137 1980 431 436
115. T.E. Creighton Kinetic study of protein unfolding and refolding using urea gradient electrophoresis J. Mol. Biol. 137 1980 61 80
116. T.E. Creighton Detection of folding intermediates using urea-gradient electrophoresis Methods Enzymol. 131 1986 156 172 (Pubitemid 16002201)
117. G.H. Caines, and T. Schleich Incorporation of saturation transfer into the formalism for rotating-frame spin-lattice proton NMR relaxation in the presence of an off-resonance-irradiation field J. Magn. Res. 95 1991 457 476
118. J. Grad, and R.G. Bryant Nuclear magnetic cross-relaxation spectroscopy J. Magn. Res. 90 1990 1 8
119. B. Xue, R.L. Dunbrack, R.W. Williams, A.K. Dunker, and V.N. Uversky PONDR-FIT: a meta-predictor of intrinsically disordered amino acids Biochim. Biophys. Acta 1804 2010 996 1010
120. P. Romero, Z. Obradovic, X. Li, E.C. Garner, C.J. Brown, and A.K. Dunker Sequence complexity of disordered protein Proteins 42 2001 38 48
121. K. Peng, S. Vucetic, P. Radivojac, C.J. Brown, A.K. Dunker, and Z. Obradovic Optimizing long intrinsic disorder predictors with protein evolutionary information J. Bioinform. Comput. Biol. 3 2005 35 60 (Pubitemid 40305483)
122. K. Peng, P. Radivojac, S. Vucetic, A.K. Dunker, and Z. Obradovic Length-dependent prediction of protein intrinsic disorder BMC Bioinforma. 7 2006 208
123. J. Prilusky, C.E. Felder, T. Zeev-Ben-Mordehai, E.H. Rydberg, O. Man, J.S. Beckmann, I. Silman, and J.L. Sussman FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded Bioinformatics 21 2005 3435 3438 (Pubitemid 41222454)
124. Z. Dosztanyi, V. Csizmok, P. Tompa, and I. Simon The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins J. Mol. Biol. 347 2005 827 839 (Pubitemid 40357923)
125. A. Campen, R.M. Williams, C.J. Brown, J. Meng, V.N. Uversky, and A.K. Dunker TOP-IDP-scale: a new amino acid scale measuring propensity for intrinsic disorder Protein Pept. Lett. 15 2008 956 963
126. J. Kyte, and R.F. Doolittle A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 157 1982 105 132
127. K. Wuthrich NMR in Biological Research: Peptides and Proteins 1976 American Press/Elsevier New York
128. D.A. Prokhorov, A.A. Timchenko, V.N. Uversky, V.S. Khristoforov, H. Kihara, K. Kimura, and V.P. Kutyshenko Dynamics of oligomer formation by denatured carbonic anhydrase II Biochim. Biophys. Acta 1784 2008 834 842
129. F.G. Prendergast, and K.G. Mann Chemical and physical properties of aequorin and the green fluorescent protein isolated from Aequorea forskalea Biochemistry 17 1978 3448 3453 (Pubitemid 8405366)
130. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637