Structural disorder within Henipavirus nucleoprotein and phosphoprotein: From predictions to experimental assessment

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Habchi, Johnny ^a   Mamelli, Laurent ^a   Darbon, Hervé ^a   Longhi, Sonia ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS NUCLEOPROTEIN; VIRUS PHOSPHOPROTEIN; NUCLEOCAPSID PROTEIN; PHOSPHOPROTEIN; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTALLIZATION; EXPERIMENTAL DESIGN; GEL FILTRATION; HENIPAVIRUS; LIGHT SCATTERING; MATHEMATICAL COMPUTING; MOLECULAR CLONING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PREDICTION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; CHEMISTRY; GEL CHROMATOGRAPHY; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

BACTERIA (MICROORGANISMS); HENIPAVIRUS; PARAMYXOVIRIDAE;

CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; HENIPAVIRUS; MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOCAPSID PROTEINS; PHOSPHOPROTEINS; VIRAL PROTEINS;

EID: 77955399035     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011684     Document Type: Article

References (138)

1. Eaton BT, Mackenzie JS, Wang LF (2007) Henipaviruses. In: Fields BN, Knipe DM, Howley PM, eds. Fields Virology. 5th ed. Philadelphia: Lippincott-Raven. pp 1587-1600.
2. Drexler JF, Corman VM, Gloza-Rausch F, Seebens A, Annan A, et al. (2009) Henipavirus RNA in African bats. PLoS ONE 4: e6367.
3. Wang LF, Yu M, Hansson E, Pritchard LI, Shiell B, et al. (2000) The exceptionally large genome of Hendra virus: support for creation of a new genus within the family Paramyxoviridae. J Virol 74: 9972-9979.
4. Eaton BT, Broder CC, Middleton D, Wang LF (2006) Hendra and Nipah viruses: different and dangerous. Nat Rev Microbiol 4: 23-35.
5. Karlin D, Longhi S, Canard B (2002) Substitution of two residues in the measles virus nucleoprotein results in an impaired self-association. Virology 302: 420-432.
6. Longhi S, Receveur-Brechot V, Karlin D, Johansson K, Darbon H, et al. (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.
7. Schoehn G, Mavrakis M, Albertini A, Wade R, Hoenger A, et al. (2004) The 12 A structure of trypsin-treated measles virus N-RNA. J Mol Biol 339: 301-312.
8. Bhella D (2007) Measles virus nucleocapsid structure, conformational flexibility and the rule of six. In: Longhi S, ed. Measles virus nucleoprotein. Hauppage, NY: Nova Publishers Inc.
9. Bhella D, Ralph A, Murphy LB, Yeo RP (2002) Significant differences in nucleocapsid morphology within the Paramyxoviridae. J Gen Virol 83: 1831-1839.
10. Bhella D, Ralph A, Yeo RP (2004) Conformational flexibility in recombinant measles virus nucleocapsids visualised by cryo-negative stain electron microscopy and real-space helical reconstruction. J Mol Biol 340: 319-331.
11. Halpin K, Bankamp B, Harcourt BH, Bellini WJ, Rota PA (2004) Nipah virus conforms to the rule of six in a minigenome replication assay. J Gen Virol 85: 701-707.
12. Park MS, Shaw ML, Munoz-Jordan J, Cros JF, Nakaya T, et al. (2003) Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J Virol 77: 1501-1511.
13. Sleeman K, Bankamp B, Hummel KB, Lo MK, BelliniWJ, et al. (2008) The C, V and W proteins of Nipah virus inhibit minigenome replication. J Gen Virol 89: 1300-1308.
14. Lou Z, Xu Y, Xiang K, Su N, Qin L, et al. (2006) Crystal structures of Nipah and Hendra virus fusion core proteins. Febs J 273: 4538-4547.
15. Bowden TA, Crispin M, Harvey DJ, Aricescu AR, Grimes JM, et al. (2008) Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J Virol 82: 11628-11636.
16. Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, et al. (2008) Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 15: 567-572.
17. Bowden TA, Crispin M, Harvey DJ, Jones EY, Stuart DI Dimeric (2010) Architecture of the Hendra Virus Attachment Glycoprotein: Evidence for a Conserved Mode of Assembly. J Virol.
18. Karlin D, Longhi S, Receveur V, Canard B (2002) The N-terminal domain of the phosphoprotein of morbilliviruses belongs to the natively unfolded class of proteins. Virology 296: 251-262.
19. Bourhis J, Johansson K, Receveur-Bréchot V, Oldfield CJ, Dunker AK, et al. (2004) The C-terminal domain of measles virus nucleoprotein belongs to the classof intrinsically disordered proteins that fold upon binding to their pohysiological partner. Virus Research 99: 157-167.
20. Bourhis JM, Receveur-Bréchot V, Oglesbee M, Zhang X, Buccellato M, et al. (2005) The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded. Protein Sci 14: 1975-1992.
21. Bourhis JM, Canard B, Longhi S (2005) Désordre structural au sein du complexe réplicatif du virus de la rougeole: implications fonctionnelles. Virologie 9: 367-383.
22. Bourhis JM, Canard B, Longhi S (2006) Structural disorder within the replicative complex of measles virus: functional implications. Virology 344: 94-110.
23. Bourhis JM, Longhi S (2007) Measles virus nucleoprotein: structural organization and functional role of the intrinsically disordered C-terminal domain. In: Longhi S, ed. Measles virus nucleoprotein. Hauppage, NY: Nova Publishers Inc. pp 1-35.
24. Longhi S (2009) Nucleocapsid structure and function. Curr Top Microbiol Immunol 329: 103-128.
25. Bernard C, Gely S, Bourhis JM, Morelli X, Longhi S, et al. (2009) Interaction between the C-terminal domains of N and P proteins of measles virus investigated by NMR. FEBS Lett 583: 1084-1089.
26. Karlin D, Ferron F, Canard B, Longhi S (2003) Structural disorder and modular organization in Paramyxovirinae N and P. J Gen Virol 84: 3239-3252.
27. Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293: 321-331.
28. Dunker AK, Oldfield CJ, Meng J, Romero P, Yang JY, et al. (2008) The unfoldomics decade: an update on intrinsically disordered proteins. BMC Genomics 9 Suppl 2: S1.
29. Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Function and structure of inherently disordered proteins. Curr Opin Struct Biol 18: 756-764.
30. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, et al. (2001) Intrinsically disordered protein. J Mol Graph Model 19: 26-59.
31. Dunker AK, Obradovic Z (2001) The protein trinity-linking function and disorder. Nat Biotechnol 19: 805-806.
32. Uversky VN (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11: 739-756.
33. Uversky VN (2003) Protein folding revisited. A polypeptide chain at the folding-misfolding-nonfolding cross-roads: which way to go? Cell Mol Life Sci 60: 1852-1871.
34. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208.
35. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, et al. (2007) Intrinsic disorder and functional proteomics. Biophys J 92: 1439-1456.
36. Lieutaud P, Canard B, Longhi S (2008) MeDor: a metaserver for predicting protein disorder. BMC Genomics 9: S25.
37. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, et al. (2001) Sequence complexity of disordered proteins. Proteins 42: 38-48.
38. Brown CJ, Takayama S, Campen AM, Vise P, Marshall TW, et al. (2002) Evolutionary rate heterogeneity in proteins with long disordered regions. J Mol Evol 55: 104-110.
39. Liu J, Tan H, Rost B (2002) Loopy proteins appear conserved in evolution. J Mol Biol 322: 53-64.
40. Ferron F, Rancurel C, Longhi S, Cambillau C, Henrissat B, et al. (2005) VaZyMolO: a tool to define and classify modularity in viral proteins. J Gen Virol 86: 743-749.
41. Bourhis JM, Canard B, Longhi S (2007) Predicting protein disorder and induced folding: from theoretical principles to practical applications. Curr Protein Pept Sci 8: 135-149.
42. Johansson K, Bourhis JM, Campanacci V, Cambillau C, Canard B, et al. (2003) Crystal structure of the measles virus phosphoprotein domain responsible for the induced folding of the C-terminal domain of the nucleoprotein. J Biol Chem 278: 44567-44573.
43. Blanchard L, Tarbouriech N, Blackledge M, Timmins P, Burmeister WP, et al. (2004) Structure and dynamics of the nucleocapsid-binding domain of the Sendai virus phosphoprotein in solution. Virology 319: 201-211.
44. Kingston RL, Gay LS, Baase WS, Matthews BW (2008) Structure of the nucleocapsid-binding domain from the mumps virus polymerase; an example of protein folding induced by crystallization. J Mol Biol 379: 719-731.
45. Uversky VN, Gillespie JR, Fink AL (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41: 415-427.
46. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27: 527-533.
47. Receveur-Bréchot V, Bourhis JM, Uversky VN, Canard B, Longhi S (2006) Assessing protein disorder and induced folding. Proteins: Structure, Function and Bioinformatics 62: 24-45.
48. Fontana A, Polverino de Laureto P, De Filippis V, Scaramella E, Zambonin M (1997) Probing the partly folded states of proteins by limited proteolysis. Fold Des 2: R17-26.
49. Hubbard SJ (1998) The structural aspects of limited proteolysis of native proteins. Biochim Biophys Acta 1382: 191-206.
50. Uversky VN (2002) What does it mean to be natively unfolded? Eur J Biochem 269: 2-12.
51. Uversky VN (1993) Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule. Biochemistry 32: 13288-13298.
52. Wu J, Yang JT, Wu CS (1992) Beta-II conformation of all-beta proteins can be distinguished from unordered form by circular dichroism. Anal Biochem 200: 359-364.
53. Tell G, Perrone L, Fabbro D, Pellizzari L, Pucillo C, et al. (1998) Structural and functional properties of the N transcriptional activation domain of thyroid transcription factor-1: similarities with the acidic activation domains. Biochem J 329: 395-403.
54. Hua QX, Jia WH, Bullock BP, Habener JF, Weiss MA (1998) Transcriptional activator-coactivator recognition: nascent folding of a kinase-inducible transactivation domain predicts its structure on coactivator binding. Biochemistry 37: 5858-5866.
55. Dahlman-Wright K, McEwan IJ (1996) Structural studies of mutant glucocorticoid receptor transactivation domains establish a link between transactivation activity in vivo and alpha-helix-forming potential in vitro. Biochemistry 35: 1323-1327.
56. Brocca S, Samalikova M, Uversky VN, Lotti M, Vanoni M, et al. (2009) Order propensity of an intrinsically disordered protein, the cyclin-dependent-kinase inhibitor Sic1. Proteins 76: 731-746.
57. Soulages JL, Kim K, Walters C, Cushman JC (2002) Temperature-induced extended helix/random coil transitions in a group 1 late embryogenesisabundant protein from soybean. Plant Physiol 128: 822-832.
58. Uversky VN (2010) Analyzing intrinsically disordered proteins by size exclusion chromatography. In: Uversky VN, Longhi S, eds. Instrumental analysis of intrinsically disordered proteins. Hoboken, New Jersey: John Wiley & Sons. pp 525-544.
59. Csizmok V, Szollosi E, Friedrich P, Tompa P (2006) A novel two-dimensional electrophoresis technique for the identification of intrinsically unstructured proteins. Mol Cell Proteomics 5: 265-273.
60. Oldfield CJ, Cheng Y, Cortese MS, Romero P, Uversky VN, et al. (2005) Coupled Folding and Binding with alpha-Helix-Forming Molecular Recognition Elements. Biochemistry 44: 12454-12470.
61. Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, et al. (2006) Analysis of Molecular Recognition Features (MoRFs). J Mol Biol 362: 1043-1059.
62. Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, et al. (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6: 2351-2366.
63. Fuxreiter M, Tompa P, Simon I (2007) Local structural disorder imparts plasticity on linear motifs. Bioinformatics 23: 950-956.
64. Fuxreiter M, Simon I, Friedrich P, Tompa P (2004) Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J Mol Biol 338: 1015-1026.
65. Lacy ER, Filippov I, Lewis WS, Otieno S, Xiao L, et al. (2004) p27 binds cyclin-CDK complexes through a sequential mechanism involving bindinginduced protein folding. Nat Struct Mol Biol 11: 358-364.
66. Sivakolundu SG, Bashford D, Kriwacki RW (2005) Disordered p27Kip1 exhibits intrinsic structure resembling the Cdk2/cyclin A-bound conformation. J Mol Biol 353: 1118-1128.
67. Van Hoy M, Leuther KK, Kodadek T, Johnston SA (1993) The acidic activation domains of the GCN4 and GAL4 proteins are not alpha helical but form beta sheets. Cell 72: 587-594.
68. Belle V, Rouger S, Costanzo S, Liquiere E, Strancar J, et al. (2008) Mapping alpha-helical induced folding within the intrinsically disordered C-terminal domain of the measles virus nucleoprotein by site-directed spin-labeling EPR spectroscopy. Proteins: Structure, Function and Bioinformatics 73: 973-988.
69. Callebaut I, Labesse G, Durand P, Poupon A, Canard L, et al. (1997) Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell Mol Life Sci 53: 621-645.
70. Morin B, Bourhis JM, Belle V, Woudstra M, Carrière F, et al. (2006) Assessing induced folding of an intrinsically disordered protein by site-directed spinlabeling EPR spectroscopy. J Phys Chem B 110: 20596-20608.
71. Gely S, Lowry DF, Bernard C, Ringkjobing-Jensen M, Blackledge M, et al. (2010) Solution structure of the C-terminal X domain of the measles virus phosphoprotein and interaction with the intrinsically disordered C-terminal domain of the nucleoprotein. J Mol Recognit, in press.
72. Kavalenka A, Urbancic I, Belle V, Rouger S, Costanzo S, et al. (2010) Conformational analysis of the partially disordered measles virus NTAIL-XD complex by SDSL EPR spectroscopy. Biophys J 98: 1055-1064.
73. Houben K, Marion D, Tarbouriech N, Ruigrok RW, Blanchard L (2007) Interaction of the C-terminal domains of sendai virus N and P proteins: comparison of polymerase-nucleocapsid interactions within the paramyxovirus family. J Virol 81: 6807-6816.
74. Jordan IK, Sutter BA, McClure MA (2000) Molecular evolution of the Paramyxoviridae and Rhabdoviridae multiple-protein-encoding P gene. Mol Biol Evol 17: 75-86.
75. Narechania A, Terai M, Burk RD (2005) Overlapping reading frames in closely related human papillomaviruses result in modular rates of selection within E2. J Gen Virol 86: 1307-1313.
76. Rancurel C, Khosravi M, Dunker KA, Romero PR, Karlin D (2009) Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol.
77. Kovacs E, Tompa P, Liliom K, Kalmar L Dual coding in alternative reading frames correlates with intrinsic protein disorder. Proc Natl Acad Sci U S A 107: 5429-5434.
78. Boumlic A, Nomine Y, Charbonnier S, Dalagiorgou G, Vassilaki N, et al. Prevalence of intrinsic disorder in the hepatitis C virus ARFP/Core+1/S protein. Febs J 277: 774-789.
79. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) Flexible nets. Febs J 272: 5129-5148.
80. Uversky VN, Oldfield CJ, Dunker AK (2005) Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J Mol Recognit 18: 343-384.
81. Haynes C, Oldfield CJ, Ji F, Klitgord N, Cusick ME, et al. (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput Biol 2: e100.
82. Dunker AK, Garner E, Guilliot S, Romero P, Albrecht K, et al. (1998) Protein disorder and the evolution of molecular recognition: theory, predictions and observations. Pac Symp Biocomput 3: 473-484.
83. Dunker AK, Brown CJ, Obradovic Z (2002) Identification and functions of usefully disordered proteins. Adv Protein Chem 62: 25-49.
84. Uversky VN, Li J, Souillac P, Jakes R, Goedert M, et al. (2002) Biophysical properties of the synucleins and their propensities to fibrillate: inhibition of alpha-synuclein assembly by beta- and gamma- synucleins. J Biol Chem 25: 25.
85. Gunasekaran K, Tsai CJ, Kumar S, Zanuy D, Nussinov R (2003) Extended disordered proteins: targeting function with less scaffold. Trends Biochem Sci 28: 81-85.
86. Fink AL (2005) Natively unfolded proteins. Curr Opin Struct Biol 15: 35-41.
87. Zhang X, Glendening C, Linke H, Parks CL, Brooks C, et al. (2002) Identification and characterization of a regulatory domain on the carboxyl terminus of the measles virus nucleocapsid protein. J Virol 76: 8737-8746.
88. Zhang X, Bourhis JM, Longhi S, Carsillo T, Buccellato M, et al. (2005) Hsp72 recognizes a P binding motif in the measles virus N protein C-terminus. Virology 337: 162-174.
89. Couturier M, Buccellato M, Costanzo S, Bourhis JM, Shu Y, et al. (2009) High Affinity Binding between Hsp70 and the C-Terminal Domain of the Measles Virus Nucleoprotein Requires an Hsp40 Co-Chaperone. J Mol Recognit, in press.
90. ten Oever BR, Servant MJ, Grandvaux N, Lin R, Hiscott J (2002) Recognition of the Measles Virus Nucleocapsid as a Mechanism of IRF-3 Activation. J Virol 76: 3659-3669.
91. Colombo M, Bourhis JM, Chamontin C, Soriano C, Villet S, et al. (2009) The interaction between the measles virus nucleoprotein and the Interferon Regulator Factor 3 relies on a specific cellular environment. Virol J 6: 59.
92. Laine D, Bourhis J, Longhi S, Flacher M, Cassard L, et al. (2005) Measles virus nucleoprotein induces cell proliferation arrest and apoptosis through NTAIL/ NR and NCORE/FcgRIIB1 interactions, respectively. J Gen Virol 86: 1771-1784.
93. Laine D, Trescol-Biémont M, Longhi S, Libeau G, Marie J, et al. (2003) Measles virus nucleoprotein binds to a novel cell surface receptor distinct from FcgRII via its C-terminal domain: role in MV-induced immunosuppression. J Virol 77: 11332-11346.
94. Sato H, Masuda M, Miura R, Yoneda M, Kai C (2006) Morbillivirus nucleoprotein possesses a novel nuclear localization signal and a CRM1- independent nuclear export signal. Virology 352: 121-130.
95. Iwasaki M, Takeda M, Shirogane Y, Nakatsu Y, Nakamura T, et al. (2009) The matrix protein of measles virus regulates viral RNA synthesis and assembly by interacting with the nucleocapsid protein. J Virol.
96. De BP, Banerjee AK (1999) Involvement of actin microfilaments in the transcription/replication of human parainfluenza virus type 3: possible role of actin in other viruses. Microsc Res Tech 47: 114-123.
97. Moyer SA, Baker SC, Horikami SM (1990) Host cell proteins required for measles virus reproduction. J Gen Virol 71: 775-783.
98. Chen M, Cortay JC, Gerlier D (2003) Measles virus protein interactions in yeast: new findings and caveats. Virus Res 98: 123-129.
99. Liston P, DiFlumeri C, Briedis DJ (1995) Protein interactions entered into by the measles virus P, V, and C proteins. Virus Res 38: 241-259.
100. Curran J, Pelet T, Kolakofsky D (1994) An acidic activation-like domain of the Sendai virus P protein is required for RNA synthesis and encapsidation. Virology 202: 875-884.
101. Curran J, Marq JB, Kolakofsky D (1995) An N-terminal domain of the Sendai paramyxovirus P protein acts as a chaperone for the NP protein during the nascent chain assembly step of genome replication. J Virol 69: 849-855.
102. Watanabe N, Kawano M, Tsurudome M, Nishio M, Ito M, et al. (1996) Binding of the V proteins to the nucleocapsid proteins of human parainfluenza type 2 virus. Med Microbiol Immunol (Berl) 185: 89-94.
103. Chinchar VG, Portner A (1981) Functions of Sendai virus nucleocapsid polypeptides: enzymatic activities in nucleocapsids following cleavage of polypeptide P by Staphylococcus aureus protease V8. Virology 109: 59-71.
104. Deshpande KL, Portner A (1985) Monoclonal antibodies to the P protein of Sendai virus define its structure and role in transcription. Virology 140: 125-134.
105. Tarbouriech N, Curran J, Ebel C, Ruigrok RW, Burmeister WP (2000) On the domain structure and the polymerization state of the sendai virus P protein. Virology 266: 99-109.
106. Bernado P, Blanchard L, Timmins P, Marion D, Ruigrok RW, et al. (2005) A structural model for unfolded proteins from residual dipolar couplings and small-angle x-ray scattering. Proc Natl Acad Sci U S A 102: 17002-17007.
107. Houben K, Blanchard L, Blackledge M, Marion D (2007) Intrinsic dynamics of the partly unstructured PX domain from the Sendai virus RNA polymerase cofactor P. Biophys J 93: 2830-2844.
108. Dedmon MM, Patel CN, Young GB, Pielak GJ (2002) FlgM gains structure in living cells. Proc Natl Acad Sci U S A 99: 12681-12684.
109. McNulty BC, Young GB, Pielak GJ (2006) Macromolecular crowding in the Escherichia coli periplasm maintains alpha-synuclein disorder. J Mol Biol 355: 893-897.
110. Bodart JF, Wieruszeski JM, Amniai L, Leroy A, Landrieu I, et al. (2008) NMR observation of Tau in Xenopus oocytes. J Magn Reson 192: 252-257.
111. Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN, Tawfik DS (2009) Do viral proteins possess unique biophysical features? Trends Biochem Sci 34: 53-59.
112. Cheng Y, Legall T, Oldfield CJ, Mueller JP, Van YY, et al. (2006) Rational drug design via intrinsically disordered protein. Trends Biotechnol 24: 435-442.
113. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
114. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
115. Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, et al. (2005) Protein structure prediction servers at University College London. Nucleic Acids Res 33: W36-38.
116. Dosztanyi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433-3434.
117. Coeytaux K, Poupon A (2005) Prediction of unfolded segments in a protein sequence based on amino acid composition. Bioinformatics 21: 1891-1900.
118. Yang ZR, Thomson R, McNeil P, Esnouf RM (2005) RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics 21: 3369-3376.
119. Galzitskaya OV, Garbuzynskiy SO, Lobanov MY (2006) FoldUnfold: web server for the prediction of disordered regions in protein chain. Bioinformatics 22: 2948-2949.
120. Garbuzynskiy SO, Lobanov MY, Galzitskaya OV (2004) To be folded or to be unfolded? Protein Sci 13: 2871-2877.
121. Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ, et al. (2003) Protein disorder prediction: implications for structural proteomics. Structure (Camb) 11: 1453-1459.
122. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, et al. (2005) FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21: 3435-3438.
123. Linding R, Russell RB, Neduva V, Gibson TJ (2003) GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res 31: 3701-3708.
124. Obradovic Z, Peng K, Vucetic S, Radivojac P, Brown CJ, et al. (2003) Predicting intrinsic disorder from amino acid sequence. Proteins 53 Suppl 6: 566-572.
125. Obradovic Z, Peng K, Vucetic S, Radivojac P, Dunker AK (2005) Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins 61: 176-182.
126. Chandonia JM, Karplus M (1999) New methods for accurate prediction of protein secondary structure. Proteins 35: 293-306.
127. Ferron F, Longhi S, Canard B, Karlin D (2006) A practical overview of protein disorder prediction methods. Proteins 65: 1-14.
128. Dosztanyi Z, Sandor M, Tompa P, Simon I (2007) Prediction of protein disorder at the domain level. Curr Protein Pept Sci 8: 161-171.
129. He B, Wang K, Liu Y, Xue B, Uversky VN, et al. (2009) Predicting intrinsic disorder in proteins: an overview. Cell Res.
130. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252: 1162-1164.
131. Kelley LA, MacCallum RM, Sternberg MJ (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J Mol Biol 299: 499-520.
132. Vacic V, Uversky VN, Dunker AK, Lonardi S (2007) Composition Profiler: a tool for discovery and visualization of amino acid composition differences. BMC Bioinformatics 8: 211.
133. Wootton JC (1994) Non-globular domains in protein sequences: automated segmentation using complexity measures. Comput Chem 18: 269-285.
134. Hwang TL, Shaka AJ (1998) Multiple-pulse mixing sequences that selectively enhance chemical exchange or cross-relaxation peaks in high-resolution NMR spectra. J Magn Reson 135: 280-287.
135. Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32: W668-673.
136. Whitmore L, Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89: 392-400.
137. Kawahara K, Tanford C (1966) Viscosity and density of aqueous solutions of urea and guanidine hydrochloride. J Biol Chem 241: 3228-3232.
138. Campen A, Williams RM, Brown CJ, Meng J, Uversky VN, et al. (2008) TOPIDP-scale: a new amino acid scale measuring propensity for intrinsic disorder. Protein Pept Lett 15: 956-963.