Intrinsic disorder and functional proteomics

Biophysical Journal

Volumn 92, Issue 5, 2007, Pages 1439-1456

  Radivojac, Predrag ^a   Iakoucheva, Lilia M ^b   Oldfield, Christopher J ^a   Obradovic, Zoran ^c   Uversky, Vladimir N ^d,e   Dunker, A Keith ^d  

^a INDIANA UNIVERSITY   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c TEMPLE UNIVERSITY   (United States)

^d INDIANA UNIVERSITY   (United States)

^e INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; HISTONE; TRANSCRIPTION FACTOR; VOLTAGE GATED POTASSIUM CHANNEL;

AMINO ACID SEQUENCE; BIOINFORMATICS; CELLULAR DISTRIBUTION; COMPUTER PROGRAM; DNA REPAIR; FUNCTIONAL PROTEOMICS; HUMAN; MATHEMATICAL COMPUTING; MOLECULAR BIOLOGY; NONHUMAN; PREDICTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; WART VIRUS;

EID: 33847795359     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.094045     Document Type: Article

References (208)

1. Pauling, L., R. B. Corey, and R. H. Branson. 1951. The structure of proteins: two hydrogen-bonded configurations of the polypeptide chain. Proc. Natl. Acad. Sci. USA. 37:205-210.
2. Fischer, E. 1894. Einfluss der configuration auf die wirkung der enzyme. Ber. Dt. Chem. Ges. 27:2985-2993.
3. Kendrew, J. C., G. Bodo, H. M. Dintzis, R. G. Parrish, H. Wyckoff, and D. C. Phillips. 1958. A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature. 181:662-666.
4. Kendrew, J. C., R. E. Dickerson, and B. E. Strandberg. 1960. Structure of myoglobin: a three-dimensional Fourier synthesis at 2 Å resolution. Nature. 206:757-763.
5. Blake, C. C., D. F. Koenig, G. A. Mair, A. C. North, D. C. Phillips, and V. R. Sarma. 1965. Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Ångström resolution. Nature. 206:757-761.
6. Anson, M. L., and A. E. Mirsky. 1925. On some general properties of proteins. J. Gen. Physiol. 9:169-179.
7. Anfinsen, C. B. 1973. Principles that govern the folding of protein chains. Science. 181:223-230.
8. Wu, H. 1931. Studies on denaturation of proteins. XIII. A theory of denaturation. Chin. J. Physiol. 1:219-234.
9. Mirsky, A. E., and L. Pauling. 1936. On the structure of native, denatured and coagulated proteins. Proc. Natl. Acad. Sci. USA. 22:439-447.
10. Dunker, A. K., 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. 2001. Intrinsically disordered protein. J. Mol. Graph. Model. 19:26-59.
11. Daughdrill, G. W., G. J. Pielak, V. N. Uversky, M. S. Cortese, and A. K. Dunker. 2005. Natively disordered protein. In Protein Folding Handbook. J. Buchner and T. Kiefhaber, editors. Wiley-VCH: Verlag, Weinheim, Germany. 271-353.
12. Weinreb, P. H., W. Zhen, A. W. Poon, K. A. Conway, and P. T. Lansbury, Jr. 1996. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry. 35:13709-13715.
13. Wright, P. E., and H. J. Dyson. 1999. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293:321-331.
14. Halle, B. 2002. Flexibility and packing in proteins. Proc. Natl. Acad. Sci. USA. 99:1274-1279.
15. Obradovic, Z., K. Peng, S. Vucetic, P. Radivojac, C. J. Brown, and A. K. Dunker. 2003. Predicting intrinsic disorder from amino acid sequence. Proteins. 53:566-572.
16. Uversky, V. N., C. J. Oldfield, and A. K. Dunker. 2005. Showing your ID: intrinsic disorder as an ID for recognition, regulation, and cell signaling. J. Mol. Recogn. 18:343-384.
17. Ringe, D., and G. A. Petsko. 1986. Study of protein dynamics by x-ray diffraction. Methods Enzymol. 131:389-433.
18. Dyson, H. J., and P. E. Wright. 2002. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv. Protein Chem. 62:311-340.
19. Bracken, C., L. M. Iakoucheva, P. R. Romero, and A. K. Dunker. 2004. Combining prediction, computation and experiment for the characterization of protein disorder. Curr. Opin. Struct. Biol. 14:570-576.
20. Dyson, H. J., and P. E. Wright. 2004. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104:3607-3622.
21. Dyson, H. J., and P. E. Wright. 2005. Elucidation of the protein folding landscape by NMR. Methods Enzymol. 394:299-321.
22. Fasman, G. D. 1996. Circular Dichroism and the Conformational Analysis of Biomolecules. Plenum Press, New York.
23. Adler, A. J., N. J. Greenfield, and G. D. Fasman. 1973. Circular dichroism and optical rotatory dispersion of proteins and polypeptides. Methods Enzymol. 27:675-735.
24. Provencher, S. W., and J. Glockner. 1981. Estimation of globular protein secondary structure from circular dichroism. Biochemistry. 20:33-37.
25. Woody, R. W. 1995. Circular dichroism. Methods Enzymol. 246:34-71.
26. Uversky, V. N., J. R. Gillespie, and A. L. Fink. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins. 41:415-427.
27. Smyth, E., C. D. Syme, E. W. Blanch, L. Hecht, M. Vasak, and L. D. Barron. 2001. Solution structure of native proteins with irregular folds from Raman optical activity. Biopolymers. 58:138-151.
28. Uversky, V. N. 1999. A multiparametric approach to studies of self-organization of globular proteins. Biochemistry (Mosc.). 64:250-266.
29. Receveur-Brechot, V., J. M. Bourhis, V. N. Uversky, B. Canard, and S. Longhi. 2006. Assessing protein disorder and induced folding. Proteins. 62:24-45.
30. Markus, G. 1965. Protein substrate conformation and proteolysis. Proc. Natl. Acad. Sci. USA. 54:253-258.
31. Mikhalyi, E. 1978. Application of Proteolytic Enzymes to Protein Structure Studies. CRC Press, Boca Raton, FL.
32. Hubbard, S. J., F. Eisenmenger, and J. M. Thornton. 1994. Modeling studies of the change in conformation required for cleavage of limited proteolytic sites. Protein Sci. 3:757-768.
33. Fontana, A., P. P. de Laureto, V. de Filippis, E. Scaramella, and M. Zambonin. 1997. Probing the partly folded states of proteins by limited proteolysis. Fold. Des. 2:R17-R26.
34. Fontana, A., P. P. de Laureto, B. Spolaore, E. Frare, P. Picotti, and M. Zambonin. 2004. Probing protein structure by limited proteolysis. Acta Biochim. Pol. 51:299-321.
35. Iakoucheva, L. M., A. L. Kimzey, C. D. Masselon, R. D. Smith, A. K. Dunker, and E. J. Ackerman. 2001. Aberrant mobility phenomena of the DNA repair protein XPA. Protein Sci. 10:1353-1362.
36. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27:527-533.
37. Privalov, P. L. 1979. Stability of proteins: small globular proteins. Adv. Protein Chem. 33:167-241.
38. Ptitsyn, O. 1995. Molten globule and protein folding. Adv. Protein Chem. 47:83-229.
39. Ptitsyn, O. B., and V. N. Uversky. 1994. The molten globule is a third thermodynamical state of protein molecules. FEBS Lett. 341:15-18.
40. Uversky, V. N., and O. B. Ptitsyn. 1996. All-or-none solvent-induced transitions between native, molten globule and unfolded states in globular proteins. Fold. Des. 1:117-122.
41. Westhof, E., D. Altschuh, D. Moras, A. C. Bloomer, A. Mondragon, A. Klug, and M. H. Van Regenmortel. 1984. Correlation between segmental mobility and the location of antigenic determinants in proteins. Nature. 311:123-126.
42. Berzofsky, J. A. 1985. Intrinsic and extrinsic factors in protein antigenic structure. Science. 229:932-940.
43. Kaltashov, I. A., and A. Mohimen. 2005. Estimates of protein surface areas in solution by electrospray ionization mass spectrometry. Anal. Chem. 77:5370-5379.
44. Uversky, V. N. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11:739-756.
45. Dunker, A. K., and Z. Obradovic. 2001. The protein trinity-linking function and disorder. Nat. Biotechnol. 19:805-806.
46. Iakoucheva, L. M., C. J. Brown, J. D. Lawson, Z. Obradovic, and A. K. Dunker. 2002. Intrinsic disorder in cell-signaling and cancer-associated proteins. J. Mol. Biol. 323:573-584.
47. Dunker, A. K., M. S. Cortese, P. Romero, L. M. Iakoucheva, and V. N. Uversky. 2005. Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J. 272:5129-5148.
48. Dunker, A. K., C. J. Brown, J. D. Lawson, L. M. Iakoucheva, and Z. Obradovic. 2002. Intrinsic disorder and protein function. Biochemistry. 41:6573-6582.
49. Dunker, A. K., C. J. Brown, and Z. Obradovic. 2002. Identification and functions of usefully disordered proteins. Adv. Protein Chem. 62:25-49.
50. Sim, K. L., T. Uchida, and S. Miyano. 2001. ProDDO: a database of disordered proteins from the Protein Data Bank (PDB). Bioinformatics. 17:379-380.
51. Vucetic, S., Z. Obradovic, V. Vacic, P. Radivojac, K. Peng, L. M. Iakoucheva, M. S. Cortese, J. D. Lawson, C. J. Brown, J. G. Sikes, C. D. Newton, and A. K. Dunker. 2005. DisProt: a database of protein disorder. Bioinformatics. 21:137-140.
52. Sickmeier, M., 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. 2006. DisProt: the database of disordered proteins. Nucleic Acids Res. In press.
53. Radivojac, P., Z. Obradovic, D. K. Smith, G. Zhu, S. Vucetic, C. J. Brown, J. D. Lawson, and A. K. Dunker. 2004. Protein flexibility and intrinsic disorder. Protein Sci. 13:71-80.
54. Romero, P., Z. Obradovic, C. R. Kissinger, J. E. Villafranca, and A. K. Dunker. 1997. Identifying disordered regions in proteins from amino acid sequences. IEEE Int. Conf. Neural Netw. 1:90-95.
55. Lise, S., and D. T. Jones. 2005. Sequence patterns associated with disordered regions in proteins. Proteins. 58:144-150.
56. Berman, H., T. N. Bhat, P. Bourne, Z. Feng, G. Gilliand, and H. Weissig. 2000. The Protein DataBank and the challenge of structural genomics. Nat. Struct. Biol. 7:957-959 (Structural Genomics supplement).
57. Romero, P., Z. Obradovic, X. Li, E. C. Garner, C. J. Brown, and A. K. Dunker. 2001. Sequence complexity of disordered protein. Proteins. 42:38-48.
58. Li, X., P. Romero, M. Rani, A. K. Dunker, and Z. Obradovic. 1999. Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10:30-40.
59. Wootton, J. C. 1993. Statistic of local complexity in amino acid sequences and sequence databases. Comput. Chem. 17:149-163.
60. Wootton, J. C. 1994. Non-globular domains in protein sequences: automated segmentation using complexity measures. Comput. Chem. 18:269-285.
61. Wootton, J. C. 1994. Sequences with "unusual" amino acid compositions. Curr. Opin. Struct. Biol. 4:413-421.
62. Wootton, J. C. 1997. Evaluating the effectiveness of sequence analysis algorithms using measures of relevant information. Comput. Chem. 21:191-202.
63. Wootton, J. C., and S. Federhen. 1996. Analysis of compositionally biased regions in sequence databases. Methods Enzymol. 266:554-571.
64. Romero, P., Z. Obradovic, and A. K. Dunker. 1999. Folding minimal sequences: the lower bound for sequence complexity of globular proteins. FEBS Lett. 462:363-367.
65. Weathers, E. A., M. E. Paulaitis, T. B. Woolf, and J. H. Hoh. 2007. Insights into protein structure and function from disorder-complexity space. Proteins. 66:16-28.
66. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
67. Prilusky, J., C. E. Felder, T. Zeev-Ben-Mordehai, E. H. Rydberg, O. Man, J. S. Beckmann, I. Silman, and J. L. Sussman. 2005. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics. 21:3435-3438.
68. Linding, R., L. J. Jensen, F. Diella, P. Bork, T. J. Gibson, and R. B. Russell. 2003. Protein disorder prediction: implications for structural proteomics. Structure. 11:1453-1459.
69. Liu, J., H. Tan, and B. Rost. 2002. Loopy proteins appear conserved in evolution. J. Mol. Biol. 322:53-64.
70. Liu, J., and B. Rost. 2003. NORSp: predictions of long regions without regular secondary structure. Nucleic Acids Res. 31:3833-3835.
71. Vucetic, S., P. Radivojac, Z. Obradovic, C. J. Brown, and A. K. Dunker. 2001. Methods for improving protein disorder prediction. In International Joint INNS-IEEE Conference on Neural Networks. Washington, DC. 2718-2723.
72. Vucetic, S., C. J. Brown, A. K. Dunker, and Z. Obradovic. 2003. Flavors of protein disorder. Proteins. 52:573-584.
73. Weathers, E. A., M. E. Paulaitis, T. B. Woolf, and J. H. Hoh. 2004. Reduced amino acid alphabet is sufficient to accurately recognize intrinsically disordered protein. FEBS Lett. 576:348-352.
74. Stoffer, D. A., and L. G. Volkert. 2005. A neural network for predicting protein disorder using amino acid hydropathy values. In IEEE Symposium on Computational Intelligence in Bioinformatics and Computational Biology. San Diego, CA. 482-490.
75. Garbuzynskiy, S. O., M. Y. Lobanov, and O. V. Galzitskaya. 2004. To be folded or to be unfolded? Protein Sci. 13:2871-2877.
76. Melamud, E., and J. Moult. 2003. Evaluation of disorder predictions in CASP5. Proteins. 53(Suppl 6):561-565.
77. Jin, Y., and R. L. Dunbrack, Jr. 2005. Assessment of disorder predictions in CASP6. Proteins. 61(Suppl 7):167-175.
78. Ferron, F., S. Longhi, B. Canard, and D. Karlin. 2006. A practical overview of protein disorder prediction methods. Proteins. 65:1-14.
79. Peng, K., S. Vucetic, P. Radivojac, C. J. Brown, A. K. Dunker, and Z. Obradovic. 2005. Optimizing long intrinsic disorder predictors with protein evolutionary information. J. Bioinform. Comput. Biol. 3:35-60.
80. Obradovic, Z., K. Peng, S. Vucetic, P. Radivojac, and A. K. Dunker. 2005. Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins. 61(Suppl 7):176-182.
81. Peng, K., P. Radivojac, S. Vucetic, A. K. Dunker, and Z. Obradovic. 2006. Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics. 7:208.
82. Jones, D. T., and J. J. Ward. 2003. Prediction of disordered regions in proteins from position specific score matrices. Proteins. 53:573-578.
83. Ward, J. J., J. S. Sodhi, L. J. McGuffin, B. F. Buxton, and D. T. Jones. 2004. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337:635-645.
84. Ward, J. J., L. J. McGuffin, K. Bryson, B. F. Buxton, and D. T. Jones. 2004. The DISOPRED server for the prediction of protein disorder. Bioinformatics. 20:2138-2139.
85. Linding, R., R. B. Russell, V. Neduva, and T. J. Gibson. 2003. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31:3701-3708.
86. Dosztanyi, Z., V. Csizmok, P. Tompa, and I. Simon. 2005. The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J. Mol. Biol. 347:827-839.
87. Dosztanyi, Z., V. Csizmok, P. Tompa, and I. Simon. 2005. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics. 21:3433-3434.
88. Yang, Z. R., R. Thomson, P. McNeil, and R. M. Esnouf. 2005. RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics. 21:3369-3376.
89. Coeytaux, K., and A. Poupon. 2005. Prediction of unfolded segments in a protein sequence based on amino acid composition. Bioinformatics. 21:1891-1900.
90. Cheng, J., M. J. Sweredoski, and P. Baldi. 2005. Accurate prediction of protein disordered regions by mining protein structure data. Data Mining Knowl. Disc. 11:213-222.
91. Vullo, A., O. Bortolami, G. Pollastri, and S. C. E. Tossato. 2006. Spritz: a server for the prediction of intrinsically disordered regions in protein sequences using kernel machines. Nucleic Acids Res. 34(Web server issue):W164-168.
92. Gu, J., M. Gribskov, and P. E. Bourne. 2006. Wiggle-predicting functionally flexible regions from primary sequence. PLoS Comput. Biol. 2:e90.
93. Gunasekaran, K., C. J. Tsai, and R. Nussinov. 2004. Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers. J. Mol. Biol. 341:1327-1341.
94. Mohan, A., C. J. Oldfield, P. Radivojac, V. Vacic, M. S. Cortese, A. K. Dunker, and V. N. Uversky. 2006. Analysis of Molecular Recognition Features (MoRFs). J. Mol. Biol. 362:1043-1059.
95. Oldfield, C. J., Y. Cheng, M. S. Cortese, P. Romero, V. N. Uversky, and A. K. Dunker. 2005. Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry. 44:12454-12470.
96. Romero, P., Z. Obradovic, C. R. Kissinger, J. E. Villafranca, S. Guilliot, E. Garner, and A. K. Dunker. 1998. Thousands of proteins likely to have long disordered regions. Pac. Symp. Biocomput. 3:437-448.
97. Romero, P., Z. Obradovic, and A. K. Dunker. 2000. Intelligent data analysis for protein disorder prediction. Artif. Intel. Rev. 14:447-484.
98. Bairoch, A., R. Apweiler, C. H. Wu, W. C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, M. Magrane, M. J. Martin, D. A. Natale, C. O'Donovan, N. Redaschi, and L. S. Yeh. 2005. The Universal Protein Resource (UniProt). Nucleic Acids Res. 33:D154-D159.
99. Garner, E., P. Cannon, P. Romero, Z. Obradovic, and A. K. Dunker. 1999. Predicting disordered regions in protein from amino acid sequence: common themes despite differing structural characterization. Genome Inform. Ser. Workshop Genome Inform. 9:201-213.
100. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, and G. Sherlock. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25:25-29.
101. Xie, H., S. Vucetic, L.M. Iakoucheva, C.J. Oldfield, A.K. Dunker, Z. Obradovic, and V.N. Uversky. 2007. Functional anthology of intrinsic disorder. I. Biological processes and functions of proteins with long disordered regions. J. Proteome Res. In press.
102. Xie, H., S. Vucetic, L.M. Iakoucheva, C.J. Oldfield, A.K. Dunker, Z. Obradovic, and V.N. Uversky. 2007. Functional anthology of intrinsic disorder. II. Cellular components, domains, technical terms, developmental processes and coding sequence diversities correlated with long disordered regions. J. Proteome Res. In press.
103. Xie, H., S. Vucetic, L.M. Iakoucheva, C.J. Oldfield, A.K. Dunker, Z. Obradovic, and V.N. Uversky. 2007. Functional anthology of intrinsic disorder. III. Ligands, posttranslational modifications and diseases associated with intrinsically disordered proteins. J. Proteome Res. In press.
104. Garner, E., P. Romero, A. K. Dunker, C. Brown, and Z. Obradovic. 1999. Predicting binding regions within disordered proteins. Genome Inform. Ser. Workshop Genome Inform. 10:41-50.
105. Fletcher, C. M., and G. Wagner. 1998. The interaction of eIF4E with 4E-BP1 is an induced fit to a completely disordered protein. Protein Sci. 7:1639-1642.
106. Mader, S., H. Lee, A. Pause, and N. Sonenberg. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15:4990-4997.
107. Fuxreiter, M., I. Simon, P. Friedrich, and P. Tompa. 2004. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol. 338:1015-1026.
108. Bienkiewicz, E. A., J. N. Adkins, and K. J. Lumb. 2002. Functional consequences of preorganized helical structure in the intrinsically disordered cell-cycle inhibitor p27(Kip1). Biochemistry. 41:752-759.
109. Lacy, E. R., I. Filippov, W. S. Lewis, S. Otieno, L. Xiao, S. Weiss, L. Hengst, and R. W. Kriwacki. 2004. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat. Struct. Mol. Biol. 11:358-364.
110. Lee, H., K. H. Mok, R. Muhandiram, K. H. Park, J. E. Suk, D. H. Kim, J. Chang, Y. C. Sung, K. Y. Choi, and K. H. Han. 2000. Local structural elements in the mostly unstructured transcriptional activation domain of human p53. J. Biol. Chem. 275:29426-29432.
111. Longhi, S., V. Receveur-Brechot, D. Karlin, K. Johansson, H. Darbon, D. Bhella, R. Yeo, S. Finet, and B. Canard. 2003. The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J. Biol. Chem. 278:18638-18648.
112. Callaghan, A. J., J. P. Aurikko, L. L. Ilag, J. Gunter Grossmann, V. Chandran, K. Kuhnel, L. Poljak, A. J. Carpousis, C. V. Robinson, M. F. Symmons, and B. F. Luisi. 2004. Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J. Mol. Biol. 340:965-979.
113. Bourhis, J. M., K. Johansson, V. Receveur-Brechot, C. J. Oldfield, K. A. Dunker, B. Canard, and S. Longhi. 2004. The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their physiological partner. Virus Res. 99:157-167.
114. Vacic, V., C.J. Oldfield, A. Mohan, P. Radivojac, M.S. Cortese, V.N. Uversky, and A.K. Dunker. 2007. Characterization of molecular recognition features, MoRFs, and MoRF-binding proteins. J. Mol. Biol. In press.
115. Chin, D., and A. R. Means. 2000. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10:322-328.
116. Van Eldik, L. J., and D. M. Watterson, editors. 1998. Calmodulin and Signal Transduction. Academic Press, San Diego, CA.
117. 2+-dependent cell signaling through calmodulin-activated protein phosphatase and protein kinases. Minireview series. J. Biol. Chem. 276:2311-2312.
118. Vetter, S. W., and E. Leclerc. 2003. Novel aspects of calmodulin target recognition and activation. Eur. J. Biochem. 270:404-414.
119. Yap, K., J. Kim, K. Truong, M. Sherman, T. Yuan, and M. Ikura. 2000. Calmodulin target database. J. Struct. Funct. Genomics. 1:8-14.
120. James, P., T. Vorherr, and E. Carafoli. 1995. Calmodulin-binding domains: just two faced ormulti-faceted? Trends Biochem. Sci. 20:38-42.
121. Yuan, T., H. J. Vogel, C. Sutherland, and M. P. Walsh. 1998. Characterization of the Ca21-dependent and -independent interactions between calmodulin and its binding domain of inducible nitric oxide synthase. FEBS Lett. 431:210-214.
122. Radivojac, P., S. Vucetic, T. R. O'Connor, V. N. Uversky, Z. Obradovic, and A. K. Dunker. 2006. Calmodulin signaling: analysis and prediction of a disorder-dependent molecular recognition. Proteins. 63:398-410.
123. Iakoucheva, L. M., P. Radivojac, C. J. Brown, T. R. O'Connor, J. G. Sikes, Z. Obradovic, and A. K. Dunker. 2004. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32:1037-1049.
124. Daily, K. M., P. Radivojac, and A. K. Dunker. 2005. Intrinsic disorder and protein modifications: building an SVM predictor for methylation. In IEEE Symposium on Computational Intelligence in Bioinformatics and Computational Biology, CIBCB 2005. San Diego, CA, 475-481.
125. Radivojac, P., N. V. Chawla, A. K. Dunker, and Z. Obradovic. 2004. Classification and knowledge discovery in protein databases. J. Biomed. Inform. 37:224-239.
126. Beltrao, P., and L. Serrano. 2005. Comparative genomics and disorder prediction identify biologically relevant SH3 protein interactions. PLoS Comput. Biol. 1:e26.
127. Puntervoll, P., R. Linding, C. Gemund, S. Chabanis-Davidson, M. Mattingsdal, S. Cameron, D. M. Martin, G. Ausiello, B. Brannetti, A. Costantini, F. Ferre, V. Maselli, A. Via, G. Cesareni, F. Diella, G. Superti-Furga, L. Wyrwicz, C. Ramu, C. McGuigan, R. Gudavalli, I. Letunic, P. Bork, L. Rychlewski, B. Kuster, M. Helmer-Citterich, W. N. Hunter, R. Aasland, and T. J. Gibson. 2003. ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res. 31:3625-3630.
128. Goh, C. S., N. Lan, S. M. Douglas, B. Wu, N. Echols, A. Smith, D. Milburn, G. T. Montelione, H. Zhao, and M. Gerstein. 2004. Mining the structural genomics pipeline: identificationof protein properties that affect high-throughput experimental analysis. J. Mol. Biol. 336:115-130.
129. Adams, M., A. Joachimiak, R. Kim, G. T. Montelione, and J. Norvell. 2004. Meeting review: 2003 NIH protein structure initiative workshop in protein production and crystallization for structural and functional genomics. J. Struct. Funct. Genomics. 5:1-2.
130. Chandonia, J. M., S. H. Kim, and S. E. Brenner. 2006. Target selection and deselection at the Berkeley Structural Genomics Center. Proteins. 62:356-370.
131. Oldfield, C. J., E. L. Ulrich, Y. Cheng, A. K. Dunker, and J. L. Markley. 2005. Addressing the intrinsic disorder bottleneck in structural proteomics. Proteins. 59:444-453.
132. Bandaru, V., W. Cooper, S. S. Wallace, and S. Doublie. 2004. Overproduction, crystallization and preliminary crystallographic analysis of a novel human DNA-repair enzyme that recognizes oxidative DNA damage. Acta Crystallogr. D Biol. Crystallogr. 60:1142-1144.
133. Idicula-Thomas, S., A. J. Kulkarni, B. D. Kulkarni, V. K. Jayaraman, and P. V. Balaji. 2006. A support vector machine-based method for predicting the propensity of a protein to be soluble or to form inclusion body on overexpression in Escherichia coli. Bioinformatics. 22:278-284.
134. Smialowski, P., T. Schmidt, J. Cox, A. Kirschner, and D. Frishman. 2006. Will my protein crystallize? A sequence-based predictor. Proteins. 62:343-355.
135. Ferron, F., S. Longhi, B. Henrissat, and B. Canard. 2002. Viral RNA-polymerases-a predicted 2′-O-ribose methyltransferase domain shared by all Mononegavirales. Trends Biochem. Sci. 27:222-224.
136. Karlin, D., F. Ferron, B. Canard, and S. Longhi. 2003. Structural disorder and modular organization in Paramyxovirinae N and P. J. Gen. Virol. 84:3239-3252.
137. Ferron, F., C. Rancurel, S. Longhi, C. Cambillau, B. Henrissat, and B. Canard. 2005. VaZyMolO: a tool to define and classify modularity in viral proteins. J. Gen. Virol. 86:743-749.
138. Iakoucheva, L. M., A. L. Kimzey, C. D. Masselon, J. E. Bruce, E. C. Garner, C. J. Brown, A. K. Dunker, R. D. Smith, and E. J. Ackerman. 2001. Identification of intrinsic order and disorder in the DNA repair protein XPA. Protein Sci. 10:560-571.
139. Adkins, J. N., and K. J. Lumb. 2002. Intrinsic structural disorder and sequence features of the cell cycle inhibitor p57(Kip2). Proteins. 46:1-7.
140. Chang, B. S., A. J. Minn, S. W. Muchmore, S. W. Fesik, and C. B. Thompson. 1997. Identification of a novel regulatory domain in Bcl-X(L) and Bcl-2. EMBO J. 16:968-977.
141. Campbell, K. M., A. R. Terrell, P. J. Laybourn, and K. J. Lumb. 2000. Intrinsic structural disorder of the C-terminal activation domain from the bZIP transcription factor Fos. Biochemistry. 39:2708-2713.
142. Sunde, M., K. C. McGrath, L. Young, J. M. Matthews, E. L. Chua, J. P. Mackay, and A. K. Death. 2004. TC-1 is a novel tumorigenic and natively disordered protein associated with thyroid cancer. Cancer Res. 64:2766-2773.
143. Uversky, V. N., A. Roman, C. J. Oldfield, and A. K. Dunker. 2006. Protein intrinsic disorder and human papillomaviruses: increased amount of disorder in E6 and E7 oncoproteins from high risk HPVs. J. Proteome Res. 5:1829-1842.
144. zur Hausen, H. 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer. 2:342-350.
145. Longworth, M. S., and L. A. Laimins. 2004. Pathogenesis of human papillomaviruses in differentiating epithelia. Microbiol. Mol. Biol. Rev. 68:362-372.
146. Munger, K., A. Baldwin, K. M. Edwards, H. Hayakawa, C. L. Nguyen, M. Owens, M. Grace, and K. Huh. 2004. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 78:11451-11460.
147. Munoz, N., F. X. Bosch, S. de Sanjose, R. Herrero, X. Castellsague, K. V. Shah, P. J. Snijders, and C. J. Meijer. 2003. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348:518-527.
148. Tommasino, M., and L. Crawford. 1995. Human papillomavirus E6 and E7: proteins that deregulate the cell cycle. Bioessays. 17:509-518.
149. Ohlenschlager, O., T. Seiboth, H. Zengerling, L. Briese, A. Marchanka, R. Ramachandran, M. Baum, M. Korbas, W. Meyer-Klaucke, M. Durst, and M. Gorlach. 2006. Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7. Oncogene. 25:5953-5959.
150. Cheng, Y., T. LeGall, C. J. Oldfield, A. K. Dunker, and V. N. Uversky. 2006. Abundance of intrinsic disorder in protein associated with cardiovascular disease. Biochemistry. 45:10448-10460.
151. Rogers, S., R. Wells, and M. Rechsteiner. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 234:364-368.
152. Rechsteiner, M., and S. W. Rogers. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21:267-271.
153. Yaglom, J., M. H. Linskens, S. Sadis, D. M. Rubin, B. Futcher, and D. Finley. 1995. p34Cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol. 15:731-741.
154. Berset, C., P. Griac, R. Tempel, J. La Rue, C. Wittenberg, and S. Lanker. 2002. Transferable domain in the G(1) cyclin Cln2 sufficient to switch degradation of Sic1 from the E3 ubiquitin ligase SCF(Cdc4) to SCF(Grr1). Mol. Cell. Biol. 22:4463-4476.
155. Bordone, L., and C. Campbell. 2002. DNA ligase III is degraded by calpain during cell death induced by DNA-damaging agents. J. Biol. Chem. 277:26673-26680.
156. Gregory, M. A., and S. R. Hann. 2000. c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells. Mol. Cell. Biol. 20:2423-2435.
157. Singh, G. P., M. Ganapathi, K. S. Sandhu, and D. Dash. 2006. Intrinsic unstructuredness and abundance of PEST motifs in eukaryotic proteomes. Proteins. 62:309-315.
158. Babon, J. J., E. J. McManus, S. Yao, D. P. DeSouza, L. A. Mielke, N. S. Sprigg, T. A. Willson, D. J. Hilton, N. A. Nicola, M. Baca, S. E. Nicholson, and R. S. Norton. 2006. The structure of SOCS3 reveals the basis of the extended SH2 domain function and identifies an unstructured insertion that regulates stability. Mol. Cell. 22:205-216.
159. Kalderon, D., B. L. Roberts, W. D. Richardson, and A. E. Smith. 1984. A short amino acid sequence able to specify nuclear location. Cell. 39:499-509.
160. Dingwall, C., and R. A. Laskey. 1991. Nuclear targeting sequences - a consensus? Trends Biochem. Sci. 16:478-481.
161. Conti, E., and E. Izaurralde. 2001. Nucleocytoplasmic transport enters the atomic age. Curr. Opin. Cell Biol. 13:310-319.
162. Mosammaparast, N., and L. F. Pemberton. 2004. Karyopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol. 14:547-556.
163. Lee, B. J., A. E. Cansizoglu, K. E. Suel, T. H. Louis, Z. Zhang, and Y. M. Chook. 2006. Rules for nuclear localization sequence recognition by karyopherin β2. Cell. 126:543-558.
164. Breman, J. G. 2001. The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am. J. Trop. Med. Hyg. 64:1-11.
165. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, I. T. Paulsen, K. James, J. A. Eisen, K. Rutherford, S. L. Salzberg, A. Craig, S. Kyes, M. S. Chan, V. Nene, S. J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M. W. Mather, A. B. Vaidya, D. M. Martin, A. H. Fairlamb, M. J. Fraunholz, D. S. Roos, S. A. Ralph, G. I. McFadden, L. M. Cummings, G. M. Subramanian, C. Mungall, J. C. Venter, D. J. Carucci, S. L. Hoffman, C. Newbold, R. W. Davis, C. M. Fraser, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 419:498-511.
166. Feng, Z. P., X. Zhang, P. Han, N. Arora, R. F. Anders, and R. S. Norton. 2006. Abundance of intrinsically unstructured proteins in P. falciparum and other apicomplexan parasite proteomes. Mol. Biochem. Parasitol. 150:256-267.
167. Bezanilla, F. 2000. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 80:555-592.
168. Sigworth, F. J. 1994. Voltage gating of ion channels. Q. Rev. Biophys. 27:1-40.
169. Yellen, G. 1998. The moving parts of voltage-gated ion channels. Q. Rev. Biophys. 31:239-295.
170. Armstrong, C. M., and F. Bezanilla. 1977. Inactivation of the sodium channel. II. Gating current experiments. J. Gen. Physiol. 70:567-590.
171. Bezanilla, F., and C. M. Armstrong. 1977. Inactivation of the sodium channel. I. Sodium current experiments. J. Gen. Physiol. 70:549-566.
172. Antz, C., M. Geyer, B. Fakler, M. K. Schott, H. R. Guy, R. Frank, J. P. Ruppersberg, and H. R. Kalbitzer. 1997. NMR structure of inactivation gates from mammalian voltage-dependent potassium channels. Nature. 385:272-275.
173. 2+- and voltage-activated potassium channels. J. Biol. Chem. 276:42116-42121.
174. Hoshi, T., W. N. Zagotta, and R. W. Aldrich. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 250:533-538.
175. Zagotta, W. N., T. Hoshi, and R. W. Aldrich. 1990. Restoration of inactivation in mutants of Shaker potassium channels by a peptide derived from ShB. Science. 250:568-571.
176. Magidovich, E., S. J. Fleishman, and O. Yifrach. 2006. Intrinsically disordered C-terminal segments of voltage-activated potassium channels: a possible fishing rod-like mechanism for channel binding to scaffold proteins. Bioinformatics. 22:1546-1550.
177. Wolffe, A. 1998. Chromatin: Structure and Function. Academic Press, New York.
178. Hansen, J. C. 2002. Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct. 31:361-392.
179. Arents, G., and E. N. Moudrianakis. 1995. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA. 92:11170-11174.
180. Bustin, M., F. Catez, and J. H. Lim. 2005. The dynamics of histone H1 function in chromatin. Mol. Cell. 17:617-620.
181. van Holde, K. 1988. Chromatin. Springer-Verlag, New York.
182. Munishkina, L. A., A. L. Fink, and V. N. Uversky. 2004. Conformational prerequisites for formation of amyloid fibrils from histones. J. Mol. Biol. 342:1305-1324.
183. Hansen, J. C., X. Lu, E. D. Ross, and R. W. Woody. 2006. Intrinsic protein disorder, amino acid composition, and histone terminal domains. J. Biol. Chem. 281:1853-1856.
184. Dyson, H. J., and P. E. Wright. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6:197-208.
185. Haynes, C., C. J. Oldfield, F. Ji, N. Klitgord, M. E. Cusick, P. Radivojac, V. N. Uversky, M. Vidal, and L. M. Iakoucheva. 2006. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol. 2:e100.
186. Ekman, D., S. Light, A. K. Bjorklund, and A. Elofsson. 2006. What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae? Genome Biol. 7:R45.
187. Patil, A., and H. Nakamura. 2006. Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett. 580:2041-2045.
188. Dosztányi, Z., J. Chen, A. K. Dunker, I. Simon, and P. Tompa. 2006. Disorder and sequence repeats in hub proteins and their implications for network evolution. J. Proteome Res. 5:2985-2995.
189. Haynes, C., and L. M. Iakoucheva. 2006. Serine/arginine-rich splicing factors belong to a class of intrinsically disordered proteins. Nucleic Acids Res. 34:305-312.
190. Bustos, D. M., and A. A. Iglesias. 2006. Intrinsic disorder is a key characteristic in partners that bind 14-3-3 proteins. Proteins. 63:35-42.
191. Rittinger, K., J. Budman, J. Xu, S. Volinia, L. C. Cantley, S. J. Smerdon, S. J. Gamblin, and M. B. Yaffe. 1999. Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell. 4:153-166.
192. Spolar, R. S., and M. T. Record II. 1994. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:777-784.
193. Kalodimos, C. G., N. Biris, A. M. Bonvin, M. M. Levandoski, M. Guennuegues, R. Boelens, and R. Kaptein. 2004. Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science. 305:386-389.
194. Dyson, H. J., and P. E. Wright. 2002. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 12:54-60.
195. Liu, J., N. B. Perumal, C. J. Oldfield, E. W. Su, V. N. Uversky, and A. K. Dunker. 2006. Intrinsic disorder in transcription factors. Biochemistry. 45:6873-6888.
196. Minezaki, Y., K. Homma, A. R. Kinjo, and K. Nishikawa. 2006. Human transcription factors contain a high fraction of intrinsically disordered regions essential for transcriptional regulation. J. Mol. Biol. 359:1137-1149.
197. Ritter, L. M., T. Arakawa, and A. F. Goldberg. 2005. Predicted and measured disorder in peripherin/RDS, a retinal tetraspanin. Protein Pept. Lett. 12:677-686.
198. Kukhtina, V., D. Kottwitz, H. Strauss, B. Heise, N. Chebotareva, V. Tsetlin, and F. Hucho. 2006. Intracellular domain of nicotinic acetylcholine receptor: the importance of being unfolded. J. Neurochem. 97:S63-S67.
199. Yiu, C. P., R. L. Beavil, and H. Y. Chan. 2006. Biophysical characterization reveals structural disorder in the nucleolar protein, Dribble. Biochem. Biophys. Res. Commun. 343:311-318.
200. Hinds, M. G., C. Smits, R. Fredericks-Short, J. M. Risk, M. Bailey, D. C. Huang, and C. L. Day. 2007. Bim, Bad and Bmf: intrinsically unstructured BH3-only proteins that undergo a localized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death Differ. 14:128-136.
201. Nardini, M., D. Svergun, P. V. Konarev, S. Spano, M. Fasano, C. Bracco, A. Pesce, A. Donadini, C. Cericola, F. Secundo, A. Luini, D. Corda, and M. Bolognesi. 2006. The C-terminal domain of the transcriptional corepressor CtBP is intrinsically unstructured. Protein Sci. 15:1042-1050.
202. Loftus, S. R., D. Walker, M. J. Mate, D. A. Bonsor, R. James, G. R. Moore, and C. Kleanthous. 2006. Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9. Proc. Natl. Acad. Sci. USA. 103:12353-12358.
203. 2+ regulation of striated muscle. J. Mol. Biol. 361:625-633.
204. Keramisanou, D., N. Biris, I. Gelis, G. Sianidis, S. Karamanou, A. Economou, and C. G. Kalodimos. 2006. Disorder-order folding transitions underlie catalysis in the helicase motor of SecA. Nat. Struct. Mol. Biol. 13:594-602.
205. Roy, S., S. Schnell, and P. Radivojac. 2006. Unraveling the nature of the segmentation clock: intrinsic disorder of clock proteins and their interaction map. Comput. Biol. Chem. 30:241-248.
206. Dyson, H. J., and P. E. Wright. 2006. According to current textbooks, a well-defined three-dimensional structure is a prerequisite for the function of a protein. Is this correct? IUBMB Life. 58:107-109.
207. George, R. A., and J. Heringa. 2002. SnapDRAGON: a method to delineate protein structural domains from sequence data. J. Mol. Biol. 316:839-851.
208. Obenauer, J. C., L. C. Cantley, and M. B. Yaffe. 2003. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31:3635-3641.