Exploring the binding diversity of intrinsically disordered proteins involved in one-to-many binding

Protein Science

Volumn 22, Issue 3, 2013, Pages 258-273

  Hsu, Wei Lun ^a   Oldfield, Christopher J ^a   Xue, Bin ^b   Meng, Jingwei ^a   Huang, Fei ^a   Romero, Pedro ^a   Uversky, Vladimir N ^b,c   Dunker, A Keith ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

Binding site; Hub protein; Intrinsically disordered protein; Linear motif; Molecular recognition feature; MoRF; Protein protein interaction

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN A4; ANGIOTENSIN; BECLIN 1; BIM PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; CELL NUCLEUS RECEPTOR; GLYCOPROTEIN; HISTONE H3; HISTONE H4; NUCLEAR RECEPTOR 0B2; NUCLEAR RECEPTOR COACTIVATOR 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR BINDING PROTEIN; PROTEIN BAK; PROTEIN GRIM; PROTEIN P53; PROTEIN RAD9; RHODOPSIN; RNA POLYMERASE II; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; STEROID RECEPTOR COACTIVATOR 1; TROPONIN I; UNCLASSIFIED DRUG; VASOPRESSIN;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DATA BANK; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT;

ANIMALS; DATABASES, PROTEIN; HUMANS; MODELS, MOLECULAR; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SPLICING; PROTEIN UNFOLDING; RNA POLYMERASE II; SURFACE PROPERTIES;

EID: 84877896151     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2207     Document Type: Article

References (89)

1. Jeong H, Mason SP, Barabasi AL, Oltvai ZN (2001) Lethality and centrality in protein networks. Nature 411:41-42. (Pubitemid 32428180)
2. Barabasi AL, Oltvai ZN (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5:101-113. (Pubitemid 38160277)
3. Hasty J, Collins JJ (2001) Protein interactions. Unspinning the web. Nature 411:30-31.
4. Pauling L (1940) A theory of the structure and process of formation of antibodies. J Am Chem Soc 62: 2643-2657.
5. Dunker AK, Garner E, Guilliot S, Romero P, Albrecht K, Hart J, Obradovic Z, Kissinger C, Villafranca JE (1998) Protein disorder and the evolution of molecular recognition: theory, predictions and observations. Pac Symp Biocomput 473-484.
6. Kriwacki RW, Hengst L, Tennant L, Reed SI, Wright PE (1996) Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc Natl Acad Sci USA 93: 11504-11509.
7. James LC, Roversi P, Tawfik DS (2003) Antibody multispecificity mediated by conformational diversity. Science 299:1362-1367. (Pubitemid 36254643)
8. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) Flexible nets. The roles of intrinsic disorder in protein interaction networks. FEBS J 272: 5129-5148. (Pubitemid 41503146)
9. Haynes C, Oldfield CJ, Ji F, Klitgord N, Cusick ME, Radivojac P, Uversky VN, Vidal M, Iakoucheva LM (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput Biol 2:e100.
10. Dosztanyi Z, Chen J, Dunker AK, Simon I, Tompa P (2006) Disorder and sequence repeats in hub proteins and their implications for network evolution. J Proteome Res 5:2985-2995. (Pubitemid 44749217)
11. Boxem M, Maliga Z, Klitgord N, Li N, Lemmens I, Mana M, de Lichtervelde L, Mul JD, van de Peut D, Devos M, Simonis N, Yildirim MA, Cokol M, Kao HL, de Smet AS, Wang HD, Schlaitz AL, Hao T, Milstein S, Fan CY, Tipsword M, Drew K, Galli M, Rhrissorrakrai K, Drechsel D, Koller D, Roth FP, Iakoucheva LM, Dunker AK, Bonneau R, Gunsalus KC, Hill DE, Piano F, Tavernier J, van den Heuvel S, Hyman AA, Vidal M (2008) A protein domain-based interactome network for C-elegans early embryogenesis. Cell 134:534-545.
12. Ekman D, Light S, Bjorklund AK, Elofsson A (2006) What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae? Genome Biol 7:R45.
13. Patil A, Nakamura H (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.
14. Singh GP, Dash D (2007) Intrinsic disorder in yeast transcriptional regulatory network. Proteins 68: 602-605. (Pubitemid 47068300)
15. Singh GP, Ganapathi M, Dash D (2007) Role of intrinsic disorder in transient interactions of hub proteins. Proteins 66:761-765.
16. Kim PM, Sboner A, Xia Y, Gerstein M (2008) The role of disorder in interaction networks: a structural analysis. Mol Syst Biol 4:179. (Pubitemid 351441045)
17. Bjorklund AK, Light S, Hedin L, Elofsson A (2008) Quantitative assessment of the structural bias in protein-protein interaction assays. Proteomics 8: 4657-4667.
18. Higurashi M, Ishida T, Kinoshita K (2008) Identification of transient hub proteins and the possible structural basis for their multiple interactions. Protein Sci 17:72-78.
19. Kahali B, Ahmad S, Ghosh TC (2009) Exploring the evolutionary rate differences of party hub and date hub proteins in Saccharomyces cerevisiae protein-protein interaction network. Gene 429:18-22.
20. Manna B, Bhattacharya T, Kahali B, Ghosh TC (2009) Evolutionary constraints on hub and non-hub proteins in human protein interaction network: insight from protein connectivity and intrinsic disorder. Gene 434: 50-55.
21. Patil A, Kinoshita K, Nakamura H (2010) Domain distribution and intrinsic disorder in hubs in the human protein-protein interaction network. Protein Sci 19: 1461-1468.
22. Patil A, Kinoshita K, Nakamura H (2010) Hub promiscuity in protein-protein interaction networks. Intl J Mol Sci 11:1930-1943.
23. Uversky VN, Dunker AK (2010) Understanding protein non-folding. Biochim Biophys Acta 1804:1231-1264.
24. Wright PE, Dyson HJ (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol 293:321-331. (Pubitemid 29516173)
25. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z (2001) Intrinsically disordered protein. J Mol Graph Model 19:26-59. (Pubitemid 32411501)
26. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41:6573-6582. (Pubitemid 34547347)
27. Dunker AK, Brown CJ, Obradovic Z (2002) Identification and functions of usefully disordered proteins. Adv Prot Chem 62:25-49. (Pubitemid 35204867)
28. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533. (Pubitemid 35279598)
29. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337:635-645. (Pubitemid 38326883)
30. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208. (Pubitemid 40314921)
31. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Uversky VN, Obradovic Z (2007) Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 6:1882-1898. (Pubitemid 46814512)
32. Vucetic S, Xie H, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) 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 6:1899-1916. (Pubitemid 46814513)
33. Xie H, Vucetic S, Iakoucheva LM, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN (2007) Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 6: 1917-1932. (Pubitemid 46814514)
34. Puntervoll P, Linding R, Gemund C, Chabanis-Davidson S, Mattingsdal M, Cameron S, Martin DM, Ausiello G, Brannetti B, Costantini A, Ferre F, Maselli V, Via A, Cesareni G, Diella F, Superti-Furga G, Wyrwicz L, Ramu C, McGuigan C, Gudavalli R, Letunic I, Bork P, Rychlewski L, Kuster B, Helmer-Citterich M, Hunter WN, Aasland R, Gibson TJ (2003) ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res 31: 3625-3630. (Pubitemid 37448491)
35. Gould CM, Diella F, Via A, Puntervoll P, Gemund C, Chabanis-Davidson S, Michael S, Sayadi A, Bryne JC, Chica C, Seiler M, Davey NE, Haslam N, Weatheritt RJ, Budd A, Hughes T, Pas J, Rychlewski L, Trave G, Aasland R, Helmer-Citterich M, Linding R, Gibson TJ (2010) ELM: the status of the 2010 eukaryotic linear motif resource. Nucleic Acids Res 38:D167-D180.
36. Fuxreiter M, Tompa P, Simon I (2007) Local structural disorder imparts plasticity on linear motifs. Bioinformatics 23:950-956. (Pubitemid 47050581)
37. Davey NE, Shields DC, Edwards RJ (2006) SLiMDisc: short, linear motif discovery, correcting for common evolutionary descent. Nucleic Acids Res 34:3546-3554.
38. Edwards RJ, Davey NE, Shields DC (2007) SLiMFinder: a probabilistic method for identifying over-represented, convergently evolved, short linear motifs in proteins. PLoS One 2:e967.
39. Callaghan AJ, Aurikko JP, Ilag LL, Gunter Grossmann J, Chandran V, Kuhnel K, Poljak L, Carpousis AJ, Robinson CV, Symmons MF, Luisi BF (2004). Studies of the RNA degradosome-organizing domain of the Escherichia coli ribonuclease RNase E. J Mol Biol 340: 965-979. (Pubitemid 38968695)
40. Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362: 1043-1059. (Pubitemid 44353519)
41. Obenauer JC, Yaffe MB (2004) Computational prediction of protein-protein interactions. Methods Mol Biol 261:445-468.
42. Valencia A, Pazos F, Computational methods to predict protein interaction partners. In: Panchenko A, Przytycka TM, Eds. (2008) Protein-protein interactions and networks. London: Springer-Verlag, pp 67-81.
43. Obenauer JC, Cantley LC, Yaffe MB (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31:3635-3641. (Pubitemid 37442212)
44. Kadaveru K, Vyas J, Schiller MR (2008) Viral infection and human disease -insights from minimotifs. Frontiers Biosci 13:6455-6471.
45. Mi T, Merlin JC, Deverasetty S, Gryk MR, Bill TJ, Brooks AW, Lee LY, Rathnayake V, Ross CA, Sargeant DP, Strong CL, Watts P, Rajasekaran S, Schiller MR (2012) Minimotif Miner 3.0: database expansion and significantly improved reduction of false-positive predictions from consensus sequences. Nucleic Acids Res 40:D252-D260.
46. Garner E, Romero P, Dunker AK, Brown C, Obradovic Z (1999) Predicting binding regions within disordered proteins. Genome Inform Ser Workshop Genome Inform 10:41-50.
47. Oldfield CJ, Cheng Y, Cortese MS, Romero P, Uversky VN, Dunker AK (2005) Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry 44:12454-12470. (Pubitemid 41324337)
48. Oldfield CJ, Meng J, Yang JY, Yang MQ, Uversky VN, Dunker AK (2008) Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9:S1.
49. Dosztanyi Z, Meszaros B, Simon I (2009) ANCHOR: web server for predicting protein binding regions in disordered proteins. Bioinformatics 25:2745-2746.
50. Disfani FM, Hsu WL, Mizianty MJ, Oldfield CJ, Xue B, Dunker A, Uversky V, Kurgan L (2012) MoRFpred, a computational tool for sequence-based prediction and characterization of disorder-to-order transitioning binding sites in proteins. Bioinformatics 28:i75-i83.
51. Bourhis J-M, Johansson K, Receveur-Brechot V, Oldfield CJ, Dunker KA, Canard B, Longhi S (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. (Pubitemid 38121665)
52. Hsu WL, Oldfield C, Meng J, Huang F, Xue B, Uversky VN, Romero P, Dunker AK (2012) Intrinsic protein disorder and protein-protein interactions. Pac Symp Biocomput 116-127.
53. Oldfield CJ, Meng J, Yang JY, Uversky VN, Dunker AK (2007) Intrinsic disorder in protein-protein interaction networks: case studies of complexes involving p53 and 14-3-3. BIOCOMP 07:553-566.
54. Doolittle RF (1886) Of Urfs and Orfs: a primer on how to analyze derived amino acid sequences. Mill Valley, California: University Science Books.
55. Disfani FM, Hsu WL, Mizianty MJ, Oldfield CJ, Xue B, Dunker AK, Uversky VN, Kurgan L (2012) MoRFpred, a computational tool for sequence-based prediction and characterization of short disorder-toorder transitioning binding regions in proteins. Bioinformatics 28:i75-i83.
56. Darimont BD, Wagner RL, Apriletti JW, Stallcup MR, Kushner PJ, Baxter JD, Fletterick RJ, Yamamoto KR (1998) Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev 12: 3343-3356. (Pubitemid 28520983)
57. Shiau AK, Barstad D, Radek JT, Meyers MJ, Nettles KW, Katzenellenbogen BS, Katzenellenbogen JA, Agard DA, Greene GL (2002) Structural characterization of a subtype-selective ligand reveals a novel mode of estrogen receptor antagonism. Nat Struct Biol 9: 359-364. (Pubitemid 34462554)
58. Xu RX, Lambert MH, Wisely BB, Warren EN, Weinert EE, Waitt GM, Williams JD, Collins JL, Moore LB, Willson TM, Moore JT (2004) A structural basis for constitutive activity in the human CAR/RXRalpha heterodimer. Mol Cell 16:919-928. (Pubitemid 40018402)
59. Estebanez-Perpina E, Moore JM, Mar E, Delgado-Rodrigues E, Nguyen P, Baxter JD, Buehrer BM, Webb P, Fletterick RJ, Guy RK (2005) The molecular mechanisms of coactivator utilization in ligand-dependent transactivation by the androgen receptor. J Biol Chem 280:8060-8068. (Pubitemid 40349704)
60. Soisson SM, Parthasarathy G, Adams AD, Sahoo S, Sitlani A, Sparrow C, Cui J, Becker JW (2008) Identification of a potent synthetic FXR agonist with an unexpected mode of binding and activation. Proc Natl Acad Sci USA 105:5337-5342. (Pubitemid 351753864)
61. Xue Y, Chao E, Zuercher WJ, Willson TM, Collins JL, Redinbo MR (2007) Crystal structure of the PXR-T1317 complex provides a scaffold to examine the potential for receptor antagonism. Bioorg Med Chem 15: 2156-2166. (Pubitemid 46176620)
62. Rosonina E, Blencowe BJ (2004) Analysis of the requirement for RNA polymerase II CTD heptapeptide repeats in pre-mRNA splicing and 30-end cleavage. RNA 10:581-589. (Pubitemid 38405936)
63. Zhang Y, Kim Y, Genoud N, Gao J, Kelly JW, Pfaff SL, Gill GN, Dixon JE, Noel JP (2006) Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1. Mol Cell 24:759-770. (Pubitemid 44839215)
64. Meinhart A, Cramer P (2004) Recognition of RNA polymerase II carboxy-terminal domain by 30-RNA-processing factors. Nature 430:223-226. (Pubitemid 38902432)
65. Fabrega C, Shen V, Shuman S, Lima CD (2003). Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II. Mol Cell 11:1549-1561. (Pubitemid 36776541)
66. Huang Y, Fang J, Bedford MT, Zhang Y, Xu RM (2006) Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312:748-751.
67. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714-717. (Pubitemid 47236857)
68. Ruthenburg AJ, Wang W, Graybosch DM, Li H, Allis CD, Patel DJ, Verdine GL (2006) Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex. Nat Struct Mol Biol 13:704-712. (Pubitemid 44175163)
69. Ramon-Maiques S, Kuo AJ, Carney D, Matthews AG, Oettinger MA, Gozani O, Yang W (2007) The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2. Proc Natl Acad Sci USA 104:18993-18998.
70. Forneris F, Binda C, Adamo A, Battaglioli E, Mattevi A (2007) Structural basis of LSD1-CoREST selectivity in histone H3 recognition. J Biol Chem 282:20070-20074. (Pubitemid 47099979)
71. Clements A, Poux AN, Lo WS, Pillus L, Berger SL, Marmorstein R (2003) Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol Cell 12:461-473. (Pubitemid 37238932)
72. Macdonald N, Welburn JP, Noble ME, Nguyen A, Yaffe MB, Clynes D, Moggs JG, Orphanides G, Thomson S, Edmunds JW, Clayton AL, Endicott JA, Mahadevan LC (2005) Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Mol Cell 20:199-211. (Pubitemid 41484166)
73. Couture JF, Collazo E, Ortiz-Tello PA, Brunzelle JS, Trievel RC (2007) Specificity and mechanism of JMJD2A, a trimethyllysine-specific histone demethylase. Nat Struct Mol Biol 14:689-695. (Pubitemid 47220059)
74. Zhang X, Yang Z, Khan SI, Horton JR, Tamaru H, Selker EU, Cheng X (2003) Structural basis for the product specificity of histone lysine methyltransferases. Mol Cell 12:177-185. (Pubitemid 36957834)
75. Cheng Y, Oldfield CJ, Meng J, Romero P, Uversky VN, Dunker AK (2007) Mining alpha-helix-forming molecular recognition features with cross species sequence alignments. Biochemistry 46:13468-13477. (Pubitemid 350209945)
76. Fares MA, Ruiz-Gonzalez MX, Labrador JP (2011) Protein coadaptation and the design of novel approaches to identify protein-protein interactions. IUBMB Life 63:264-271.
77. Diella F, Haslam N, Chica C, Budd A, Michael S, Brown NP, Trave G, Gibson TJ (2008) Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front Biosci 13:6580-6603.
78. Gfeller D, Butty F, Wierzbicka M, Verschueren E, Vanhee P, Huang HM, Ernst A, Dar N, Stagljar I, Serrano L, Sidhu SS, Bader GD, Kim PM (2011) The multiplespecificity landscape of modular peptide recognition domains. Mol Syst Biol 7:484.
79. Davey NE, Van Roey K, Weatheritt RJ, Toedt G, Uyar B, Altenberg B, Budd A, Diella F, Dinkel H, Gibson TJ (2012) Attributes of short linear motifs. Mol Biosyst 8: 268-281.
80. Dinkel H, Michael S, Weatheritt RJ, Davey NE, Van Roey K, Altenberg B, Toedt G, Uyar B, Seiler M, Budd A, Jodicke L, Dammert MA, Schroeter C, Hammer M, Schmidt T, Jehl P, McGuigan C, Dymecka M, Chica C, Luck K, Via A, Chatr-Aryamontri A, Haslam N, Grebnev G, Edwards RJ, Steinmetz MO, Meiselbach H, Diella F, Gibson TJ (2012) ELM -the database of eukaryotic linear motifs. Nucleic Acids Res 40: D242-D251.
81. Buljan M, Chalancon G, Eustermann S, Wagner GP, Fuxreiter M, Bateman A, Babu MM (2012) Tissue-specific splicing of disordered segments that embed binding motifs rewires protein interaction networks. Mol Cell 46:871-883.
82. Ellis JD, Barrios-Rodiles M, Colak R, Irimia M, Kim T, Calarco JA, Wang X, Pan Q, O'Hanlon D, Kim PM, Wrana JL, Blencowe BJ (2012) Tissue-specific alternative splicing remodels protein-protein interaction networks. Mol Cell 46:884-892.
83. Romero PR, Zaidi S, Fang YY, Uversky VN, Radivojac P, Oldfield CJ, Cortese MS, Sickmeier M, LeGall T, Obradovic Z, Dunker AK (2006) Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci USA 103:8390-8395. (Pubitemid 43838465)
84. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK (2004) The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res 32:1037-1049. (Pubitemid 38854704)
85. Gao J, Thelen JJ, Dunker AK, Xu D (2010) Musite, a tool for global prediction of general and kinase-specific phosphorylation sites. Mol Cell Proteomics 9: 2586-2600.
86. Gao J, Xu D (2012) Correlation between posttranslational modification and intrinsic disorder in protein. Pac Symp Biocomput 94-103.
87. Cheng Y, LeGall T, Oldfield CJ, Mueller JP, Van YY, Romero P, Cortese MS, Uversky VN, Dunker AK (2006) Rational drug design via intrinsically disordered protein. Trends Biotechnol 24:435-442. (Pubitemid 44374778)
88. Carugo O, Argos P (1997) Protein-protein crystal-packing contacts. Protein Sci 6:2261-2263. (Pubitemid 27449306)
89. Henrick K, Thornton JM (1998) PQS: a protein quaternary structure file server. Trends Biochem Sci 23: 358-361. (Pubitemid 28461869)