Protein disorder in the human diseasome: Unfoldomics of human genetic diseases

BMC Genomics

Volumn 10, Issue SUPPL. 1, 2009, Pages

  Midic, Uros ^a   Oldfield, Christopher J ^b   Keith, A Keith ^c   Obradovic, Zoran ^a   Uversky, Vladimir N ^c,d  

^a TEMPLE UNIVERSITY   (United States)

^b Indiana University   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; CONFERENCE PAPER; GENETIC DISORDER; HUMAN; MOLECULAR RECOGNITION; PREDICTION; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS; SEQUENCE ANALYSIS; ARTICLE; BIOLOGY; METABOLISM; PROTEIN CONFORMATION; PROTEIN DATABASE; STRUCTURE ACTIVITY RELATION;

PROTEIN;

ALGORITHMS; ALTERNATIVE SPLICING; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; HUMANS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS; PROTEOMICS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 67650385638     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-S1-S12     Document Type: Conference Paper

References (139)

1. Dunker AK Lawson JD Brown CJ Williams RM Romero P Oh JS Oldfield CJ Campen AM Ratliff CM Hipps KW et al Intrinsically disordered protein J Mol Graph Model 2001, 19(1):26-59. 11381529
2. Schweers O Schonbrunn-Hanebeck E Marx A Mandelkow E Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure J Biol Chem 1994, 269(39):24290-24297. 7929085
3. Weinreb PH Zhen W Poon AW Conway KA Lansbury PT Jr NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded Biochemistry 1996, 35(43):13709-13715. 8901511
4. Wright PE Dyson HJ Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm J Mol Biol 1999, 293(2):321-331. 10550212
5. Daughdrill GW Pielak GJ Uversky VN Cortese MS Dunker AK Natively disordered proteins Handbook of Protein Folding Weinheim, Germany: Wiley-VCH, Verlag GmbH & Co. KGaA Buchner J, Kiefhaber T 2005, 271-353.
6. Uversky VN Protein folding revisited. A polypeptide chain at the folding-misfolding-nonfolding cross-roads: Which way to go? Cell Mol Life Sci 2003, 60(9):1852-1871. 14523548
7. Crick SL Jayaraman M Frieden C Wetzel R Pappu RV Fluorescence correlation spectroscopy shows that monomeric polyglutamine molecules form collapsed structures in aqueous solutions Proc Natl Acad Sci USA 2006, 103(45):16764-16769. 1629004 17075061
8. Tran HT Mao A Pappu RV Role of backbone-solvent interactions in determining conformational equilibria of intrinsically disordered proteins J Am Chem Soc 2008, 130(23):7380-7392. 18481860
9. Romero P Obradovic Z Li X Garner EC Brown CJ Dunker AK Sequence complexity of disordered protein Proteins 2001, 42(1):38-48. 11093259
10. Radivojac P Iakoucheva LM Oldfield CJ Obradovic Z Uversky VN Dunker AK Intrinsic disorder and functional proteomics Biophys J 2007, 92(5):1439-1456. 1796814 17158572
11. Creighton TE The protein folding problem Science 1988, 240(4850):267-344. 3353718
12. Williams RM Obradovic Z Mathura V Braun W Garner EC Young J Takayama S Brown CJ Dunker AK The protein non-folding problem: Amino acid determinants of intrinsic order and disorder Pac Symp Biocomput 2001, 89-100. 11262981
13. Uversky VN Natively unfolded proteins: A point where biology waits for physics Protein Sci 2002, 11(4):739-756. 2373528 11910019
14. Uversky VN Gillespie JR Fink AL Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 2000, 41(3):415-427. 11025552
15. Dosztanyi Z Csizmok V Tompa P Simon I IUPred: Web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content Bioinformatics 2005, 21(16):3433-3434. 15955779
16. Oldfield CJ Cheng Y Cortese MS Brown CJ Uversky VN Dunker AK Comparing and combining predictors of mostly disordered proteins Biochemistry 2005, 44(6):1989-2000. 15697224
17. Ferron F Longhi S Canard B Karlin D A practical overview of protein disorder prediction methods Proteins 2006, 65(1):1-14. 16856179
18. Sickmeier M Hamilton JA LeGall T Vacic V Cortese MS Tantos A Szabo B Tompa P Chen J Uversky VN DisProt: The Database of Disordered Proteins Nucleic Acids Res 2007, 35:DAtabase D786-793. 1751543 17145717
19. Romero P Obradovic Z Kissinger C Villafranca JE Dunker AK Identifying disordered regions in proteins from amino acid sequence 1997 Proceedings of International Conference on Neural Networks 1997, 1:90-95.
20. Romero P Obradovic Z Kissinger CR Villafranca JE Garner E Guilliot S Dunker AK Thousands of proteins likely to have long disordered regions Pac Symp Biocomput 1998, 437-448. 9697202
21. Ward JJ Sodhi JS McGuffin LJ Buxton BF Jones DT Prediction and functional analysis of native disorder in proteins from the three kingdoms of life J Mol Biol 2004, 337(3):635-645. 15019783
22. Iakoucheva LM Brown CJ Lawson JD Obradovic Z Dunker AK Intrinsic disorder in cell-signaling and cancer-associated proteins J Mol Biol 2002, 323(3):573-584. 12381310
23. Xie H Vucetic S Iakoucheva LM Oldfield CJ Dunker AK Uversky VN Obradovic Z Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions J Proteome Res 2007, 6(5):1882-1898. 2543138 17391014
24. Vucetic S Xie H Iakoucheva LM Oldfield CJ Dunker AK Obradovic Z Uversky VN 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 2007, 6(5):1899-1916. 2588346 17391015
25. Xie H Vucetic S Iakoucheva LM Oldfield CJ Dunker AK Obradovic Z Uversky VN Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins J Proteome Res 2007, 6(5):1917-1932. 2588348 17391016
26. Dunker AK Cortese MS Romero P Iakoucheva LM Uversky VN Flexible nets. The roles of intrinsic disorder in protein interaction networks Febs J 2005, 272(20):5129-5148. 16218947
27. Cortese MS Uversky VN Keith Dunker A Intrinsic disorder in scaffold proteins: Getting more from less Prog Biophys Mol Biol 2008, 98(1):85-106. 18619997
28. Oldfield CJ Meng J Yang JY Yang MQ Uversky VN Dunker AK Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners BMC Genomics 2008, 9(Suppl 1):S1. 2386051 18366598
29. Radivojac P Vucetic S O'Connor TR Uversky VN Obradovic Z Dunker AK Calmodulin signaling: Analysis and prediction of a disorder-dependent molecular recognition Proteins 2006, 63(2):398-410. 16493654
30. Uversky VN Oldfield CJ Dunker AK Showing your ID: Intrinsic disorder as an ID for recognition, regulation and cell signaling J Mol Recognit 2005, 18(5):343-384. 16094605
31. Dunker AK Garner E Guilliot S Romero P Albrecht K Hart J Obradovic Z Kissinger C Villafranca JE Protein disorder and the evolution of molecular recognition: Theory, predictions and observations Pac Symp Biocomput 1998, 473-484. 9697205
32. Romero PR Zaidi S Fang YY Uversky VN Radivojac P Oldfield CJ Cortese MS Sickmeier M LeGall T Obradovic Z Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms Proc Natl Acad Sci USA 2006, 103(22):8390-8395. 1482503 16717195
33. Dunker AK Brown CJ Lawson JD Iakoucheva LM Obradovic Z Intrinsic disorder and protein function Biochemistry 2002, 41(21):6573-6582. 12022860
34. Oldfield CJ Cheng Y Cortese MS Romero P Uversky VN Dunker AK Coupled folding and binding with alpha-helix-forming molecular recognition elements Biochemistry 2005, 44(37):12454-12470. 16156658
35. Mohan A Oldfield CJ Radivojac P Vacic V Cortese MS Dunker AK Uversky VN Analysis of molecular recognition features (MoRFs) J Mol Biol 2006, 362(5):1043-1059. 16935303
36. Vacic V Oldfield CJ Mohan A Radivojac P Cortese MS Uversky VN Dunker AK Characterization of molecular recognition features, MoRFs, and their binding partners J Proteome Res 2007, 6(6):2351-2366. 2570643 17488107
37. Cheng Y Oldfield CJ Romero P Uversky VN Dunker AK Mining α-helix-forming molecular recognition features α-MoRFs with cross species sequence alignments Biochemistry 2007, 46(47):13468-13477. 2570644 17973494
38. Uversky VN Oldfield CJ Dunker AK Intrinsically disordered proteins in human diseases: Introducing the D2 concept Ann Rev Biophys Biomol Structure 2008, 37:215-246.
39. Cheng Y LeGall T Oldfield CJ Dunker AK Uversky VN Abundance of intrinsic disorder in protein associated with cardiovascular disease Biochemistry 2006, 45(35):10448-10460. 16939197
40. Uversky VN Amyloidogenesis of natively unfolded proteins Current Alzheimer Research 2008, 5(3):260-287. 18537543
41. Uversky VN Intrinsic disorder in proteins associated with neurodegenerative diseases Protein Folding and Misfolding: Neurodegenerative Diseases New York, USA: Springer Ovádi J, Orosz F 2008, 21-75.
42. Jimenez-Sanchez G Childs B Valle D Human disease genes Nature 2001, 40(6822):853-855. 11237009
43. Peltonen L McKusick VA Genomics and medicine. Dissecting human disease in the postgenomic era Science 2001, 291(5507):1224-1229. 11233446
44. Rual JF Venkatesan K Hao T Hirozane-Kishikawa T Dricot A Li N Berriz GF Gibbons FD Dreze M Ayivi-Guedehoussou N et al Towards a proteome-scale map of the human protein-protein interaction network Nature 2005, 437(7062):1173-1178. 16189514
45. Stelzl U Worm U Lalowski M Haenig C Brembeck FH Goehler H Stroedicke M Zenkner M Schoenherr A Koeppen S et al A human protein-protein interaction network: A resource for annotating the proteome Cell 2005, 122(6):957-968. 16169070
46. Lim J Hao T Shaw C Patel AJ Szabo G Rual JF Fisk CJ Li N Smolyar A Hill DE et al A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration Cell 2006, 125(4):801-814. 16713569
47. Goh KI Cusick ME Valle D Childs B Vidal M Barabasi AL The human disease network Proc Natl Acad Sci USA 2007, 104(21):8685-8690. 1885563 17502601
48. Peng K Radivojac P Vucetic S Dunker AK Obradovic Z Length-dependent prediction of protein intrinsic disorder BMC Bioinformatics 2006, 7:208. 1479845 16618368
49. Dunker AK Obradovic Z Romero P Garner EC Brown CJ Intrinsic protein disorder in complete genomes Genome Inform Ser Workshop Genome Inform 2000, 11:161-171. 11700597
50. Mann HB Whitney DR On a test of whether one of two random variables is stochastically larger than the other Annals of Mathematical Statistics 1947, 18:50-60.
51. Wilcoxon F Individual comparisons by ranking methods Biometrics Bulletin 1945, 1:80-83.
52. Benjamini Y Y H Controlling the false discovery rate: A practical and powerful approach to multiple testing Journal of the Royal Statistical Society Series B (Methodological) 1995, 57(1):289-300.
53. Benjamini Y Yekutieli D The control of the false discovery rate in multiple testing under dependency Annals of Statistics 2001, 29:1165-1188.
54. Tukey JW The problem of multiple comparisons Princeton University 1953 unpublished report.
55. Kramer CY Extension of multiple range tests to group means with unequal numbers of replications Biometrics Bulletin 1956, 12:307-310.
56. Mohan A Sullivan WJ Jr Radivojac P Dunker AK Uversky VN Intrinsic disorder in pathogenic and non-pathogenic microbes: Discovering and analyzing the unfoldomes of early-branching eukaryotes Mol Biosyst 2008, 4(4):328-340. 18354786
57. Lavery DN McEwan IJ Structural characterization of the native NH2-terminal transactivation domain of the human androgen receptor: A collapsed disordered conformation underlies structural plasticity and protein-induced folding Biochemistry 2008, 47(11):3360-3369. 18284208
58. Oldfield CJ Ulrich EL Cheng Y Dunker AK Markley JL Addressing the intrinsic disorder bottleneck in structural proteomics Proteins 2005, 59(3):444-453. 15789434
59. Balasubramanian S Schneider T Gerstein M Regan L Proteomics of Mycoplasma genitalium: Identification and characterization of unannotated and atypical proteins in a small model genome Nucleic Acids Res 2000, 28(16):3075-3082. 108442 10931922
60. Haynes C Oldfield CJ Ji F Klitgord N Cusick ME Radivojac P Uversky VN Vidal M Iakoucheva LM Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes PLoS Comput Biol 2006, 2(8):e100. 1526461 16884331
61. Patil A Nakamura H Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks FEBS Lett 2006, 580(8):2041-2045. 16542654
62. Dosztanyi Z Chen J Dunker AK Simon I Tompa P Disorder and sequence repeats in hub proteins and their implications for network evolution J Proteome Res 2006, 5(11):2985-2995. 17081050
63. Ekman D Light S Bjorklund AK Elofsson A What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae? Genome Biol 2006, 7(6):R45. 1779539 16780599
64. Singh GP Ganapathi M Sandhu KS Dash D Intrinsic unstructuredness and abundance of PEST motifs in eukaryotic proteomes Proteins 2006, 62(2):309-315. 16299712
65. Goedert M Filamentous nerve cell inclusions in neurodegenerative diseases: Tauopathies and alpha-synucleinopathies Philos Trans R Soc Lond B Biol Sci 1999, 354(1386):1101-1118. 1692614 10434313
66. Spillantini MG Goedert M The alpha-synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy Ann N Y Acad Sci 2000, 920:16-27. 11193145
67. Trojanowski JQ Lee VM Parkinson's disease and related alpha-synucleinopathies are brain amyloidoses Ann N Y Acad Sci 2003, 991:107-110. 12846979
68. Galvin JE Lee VM Trojanowski JQ Synucleinopathies: Clinical and pathological implications Arch Neurol 2001, 58(2):186-190. 11176955
69. Uversky VN alpha-Synuclein misfolding and neurodegenerative diseases Current Protein and Peptide Science 2008, 9(5):507-540.
70. Uversky VN Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation J Neurochem 2007, 103(1):17-37. 17623039
71. Kruger R Kuhn W Muller T Woitalla D Graeber M Kosel S Przuntek H Epplen JT Schols L Riess O Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat Genet 1998, 18(2):106-108. 9462735
72. Polymeropoulos MH Lavedan C Leroy E Ide SE Dehejia A Dutra A Pike B Root H Rubenstein J Boyer R et al Mutation in the alpha-synuclein gene identified in families with Parkinson's disease Science 1997, 276(5321):2045-2047. 9197268
73. Zarranz JJ Alegre J Gomez-Esteban JC Lezcano E Ros R Ampuero I Vidal L Hoenicka J Rodriguez O Atares B et al The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia Ann Neurol 2004, 55(2):164-173. 14755719
74. Farrer M Kachergus J Forno L Lincoln S Wang DS Hulihan M Maraganore D Gwinn-Hardy K Wszolek Z Dickson D et al Comparison of kindreds with parkinsonism and alpha-synuclein genomic multiplications Ann Neurol 2004, 55(2):174-179. 14755720
75. Singleton AB Farrer M Johnson J Singleton A Hague S Kachergus J Hulihan M Peuralinna T Dutra A Nussbaum R et al alpha-Synuclein locus triplication causes Parkinson's disease Science 2003, 302(5646):841. 14593171
76. 5Singleton A Gwinn-Hardy K Sharabi Y Li ST Holmes C Dendi R Hardy J Crawley A Goldstein DS Association between cardiac denervation and parkinsonism caused by alpha-synuclein gene triplication Brain 2004, 127(Pt 4):768-772. 14736756
77. Miller DW Hague SM Clarimon J Baptista M Gwinn-Hardy K Cookson MR Singleton AB Alpha-synuclein in blood and brain from familial Parkinson disease with SNCA locus triplication Neurology 2004, 62(10):1835-1838. 15159488
78. Dev KK Hofele K Barbieri S Buchman VL Putten van der H Part II: alpha-synuclein and its molecular pathophysiological role in neurodegenerative disease Neuropharmacology 2003, 45(1):14-44. 12814657
79. Dickson DW Alpha-synuclein and the Lewy body disorders Curr Opin Neurol 2001, 14(4):423-432. 11470957
80. Goedert M Alpha-synuclein and neurodegenerative diseases Nat Rev Neurosci 2001, 2(7):492-501. 11433374
81. Goedert M Parkinson's disease and other alpha-synucleinopathies Clin Chem Lab Med 2001, 39(4):308-312. 11388653
82. Uversky VN A protein-chameleon: Conformational plasticity of alpha-synuclein, a disordered protein involved in neurodegenerative disorders J Biomol Struct Dyn 2003, 21(2):211-234. 12956606
83. Jin J Li GJ Davis J Zhu D Wang Y Pan C Zhang J Identification of novel proteins interacting with both a-synuclein and DJ-1 Mol Cell Proteomics 2006.
84. Perutz MF Glutamine repeats and inherited neurodegenerative diseases: molecular aspects Curr Opin Struct Biol 1996, 6(6):848-858. 8994886
85. Zoghbi HY Orr HT Polyglutamine diseases: Protein cleavage and aggregation Curr Opin Neurobiol 1999, 9(5):566-570. 10508741
86. Ross CA Wood JD Schilling G Peters MF Nucifora FC Jr Cooper JK Sharp AH Margolis RL Borchelt DR Polyglutamine pathogenesis Philos Trans R Soc Lond B Biol Sci 1999, 354(1386):1005-1011. 1692617 10434299
87. 1386Preisinger E Jordan BM Kazantsev A Housman D Evidence for a recruitment and sequestration mechanism in Huntington's disease Philos Trans R Soc Lond B Biol Sci 1999, 354(1386):1029-1034. 1692605 10434302
88. Wanker EE Protein aggregation and pathogenesis of Huntington's disease: mechanisms and correlations Biol Chem 2000, 381(9-10):937-942. 11076024
89. Perutz MF Pope BJ Owen D Wanker EE Scherzinger E Aggregation of proteins with expanded glutamine and alanine repeats of the glutamine-rich and asparagine-rich domains of Sup35 and of the amyloid beta-peptide of amyloid plaques Proc Natl Acad Sci USA 2002, 99(8):5596-5600. 122815 11960015
90. McCampbell A Taylor JP Taye AA Robitschek J Li M Walcott J Merry D Chai Y Paulson H Sobue G et al CREB-binding protein sequestration by expanded polyglutamine Hum Mol Genet 2000, 9(14):2197-2202. 10958659
91. McCampbell A Fischbeck KH Polyglutamine and CBP: Fatal attraction? Nat Med 2001, 7(5):528-530. 11329046
92. Chen S Berthelier V Yang W Wetzel R Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity J Mol Biol 2001, 311(1):173-182. 11469866
93. Chen S Berthelier V Hamilton JB O'Nuallain B Wetzel R Amyloid-like features of polyglutamine aggregates and their assembly kinetics Biochemistry 2002, 41(23):7391-7399. 12044172
94. Faber PW Barnes GT Srinidhi J Chen J Gusella JF MacDonald ME Huntingtin interacts with a family of WW domain proteins Hum Mol Genet 1998, 7(9):1463-1474. 9700202
95. Boutell JM Thomas P Neal JW Weston VJ Duce J Harper PS Jones AL Aberrant interactions of transcriptional repressor proteins with the Huntington's disease gene product, huntingtin Hum Mol Genet 1999, 8(9):1647-1655. 10441327
96. Steffan JS Kazantsev A Spasic-Boskovic O Greenwald M Zhu YZ Gohler H Wanker EE Bates GP Housman DE Thompson LM The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription Proc Natl Acad Sci USA 2000, 97(12):6763-6768. 18731 10823891
97. Schaeper U Boyd JM Verma S Uhlmann E Subramanian T Chinnadurai G Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation Proc Natl Acad Sci USA 1995, 92(23):10467-10471. 40632 7479821
98. Vousden KH Lu X Live or let die: The cell's response to p53 Nat Rev Cancer 2002, 2(8):594-604. 12154352
99. Anderson CW Appella E Signaling to the p53 tumor suppressor through pathways activated by genotoxic and nongenotoxic stress Handbook of Cell Signaling New York: Academic Press Bradshaw RA, Dennis EA 2003, 237-247.
100. Hollstein M Sidransky D Vogelstein B Harris CC p53 mutations in human cancers Science 1991, 253(5015):49-53. 1905840
101. Vogelstein B Lane D Levine AJ Surfing the p53 network Nature 2000, 408(6810):307-310. 11099028
102. Zambetti GP The p53 mutation "gradient effect" and its clinical implications J Cell Physiol 2007, 213(2):370-373. 17671971
103. Hainaut P Hollstein M p53 and human cancer: The first ten thousand mutations Adv Cancer Res 2000, 77:81-137. 10549356
104. Dawson R Muller L Dehner A Klein C Kessler H Buchner J The N-terminal domain of p53 is natively unfolded J Mol Biol 2003, 332(5):1131-1141. 14499615
105. Lee H Mok KH Muhandiram R Park KH Suk JE Kim DH Chang J Sung YC Choi KY Han KH Local structural elements in the mostly unstructured transcriptional activation domain of human p53 J Biol Chem 2000, 275(38):29426-29432. 10884388
106. Zhao R Gish K Murphy M Yin Y Notterman D Hoffman WH Tom E Mack DH Levine AJ Analysis of p53-regulated gene expression patterns using oligonucleotide arrays Genes Dev 2000, 14(8):981-993. 316542 10783169
107. Szabo CI King MC Inherited breast and ovarian cancer Hum Mol Genet 1995, 4: Spec No 1811-1817. 8541881
108. Ferla R Calo V Cascio S Rinaldi G Badalamenti G Carreca I Surmacz E Colucci G Bazan V Russo A Founder mutations in BRCA1 and BRCA2 genes Ann Oncol 2007, 18(Suppl 6):vI93-98. 17591843
109. Deng CX Brodie SG Roles of BRCA1 and its interacting proteins Bioessays 2000, 22(8):728-737. 10918303
110. Mark WY Liao JC Lu Y Ayed A Laister R Szymczyna B Chakrabartty A Arrowsmith CH Characterization of segments from the central region of BRCA1: An intrinsically disordered scaffold for multiple protein-protein and protein-DNA interactions? J Mol Biol 2005, 345(2):275-287. 15571721
111. Orban TI Olah E Emerging roles of BRCA1 alternative splicing Mol Pathol 2003, 56(4):191-197. 1187320 12890739
112. Delattre O Zucman J Plougastel B Desmaze C Melot T Peter M Kovar H Joubert I de Jong P Rouleau G et al Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours Nature 1992, 359(6391):162-165. 1522903
113. May WA Gishizky ML Lessnick SL Lunsford LB Lewis BC Delattre O Zucman J Thomas G Denny CT Ewing sarcoma 11;22 translocation produces a chimeric transcription factor that requires the DNA-binding domain encoded by FLI1 for transformation Proc Natl Acad Sci USA 1993, 90(12):5752-5756. 46800 8516324
114. Hahm KB Repression of the gene encoding the TGF-beta type II receptor is a major target of the EWS-FLI1 oncoprotein Nat Genet 1999, 23(4):481. 10581042
115. Nakatani F Tanaka K Sakimura R Matsumoto Y Matsunobu T Li X Hanada M Okada T Iwamoto Y Identification of p21WAF1/CIP1 as a direct target of EWS-Fli1 oncogenic fusion protein J Biol Chem 2003, 278(17):15105-15115. 12560328
116. Abaan OD Levenson A Khan O Furth PA Uren A Toretsky JA PTPL1 is a direct transcriptional target of EWS-FLI1 and modulates Ewing's Sarcoma tumorigenesis Oncogene 2005, 24(16):2715-2722. 15782144
117. Nishimori H Sasaki Y Yoshida K Irifune H Zembutsu H Tanaka T Aoyama T Hosaka T Kawaguchi S Wada T et al The Id2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors Oncogene 2002, 21(54):8302-8309. 12447693
118. Watanabe G Nishimori H Irifune H Sasaki Y Ishida S Zembutsu H Tanaka T Kawaguchi S Wada T Hata J et al Induction of tenascin-C by tumor-specific EWS-ETS fusion genes Genes Chromosomes Cancer 2003, 36(3):224-232. 12557222
119. Thompson AD Braun BS Arvand A Stewart SD May WA Chen E Korenberg J Denny C EAT-2 is a novel SH2 domain containing protein that is up regulated by Ewing's sarcoma EWS/FLI1 fusion gene Oncogene 1996, 13(12):2649-2658. 9000139
120. Arvand A Bastians H Welford SM Thompson AD Ruderman JV Denny CT EWS/FLI1 up regulates mE2-C, a cyclin-selective ubiquitin conjugating enzyme involved in cyclin B destruction Oncogene 1998, 17(16):2039-2045. 9798675
121. May WA Arvand A Thompson AD Braun BS Wright M Denny CT EWS/FLI1-induced manic fringe renders NIH 3T3 cells tumorigenic Nat Genet 1997, 17(4):495-497. 9398859
122. Bailly RA Bosselut R Zucman J Cormier F Delattre O Roussel M Thomas G Ghysdael J DNA-binding and transcriptional activation properties of the EWS-FLI-1 fusion protein resulting from the t(11;22) translocation in Ewing sarcoma Mol Cell Biol 1994, 14(5):3230- 3241. 358690 8164678
123. Zwerner JP May WA PDGF-C is an EWS/FLI induced transforming growth factor in Ewing family tumors Oncogene 2001, 20(5):626-633. 11313995
124. Dauphinot L De Oliveira C Melot T Sevenet N Thomas V Weissman BE Delattre O Analysis of the expression of cell cycle regulators in Ewing cell lines: EWS-FLI-1 modulates p57KIP2and c-Myc expression Oncogene 2001, 20(25):3258-3265. 11423975
125. Deneen B Welford SM Ho T Hernandez F Kurland I Denny CT PIM3 proto-oncogene kinase is a common transcriptional target of divergent EWS/ETS oncoproteins Mol Cell Biol 2003, 23(11):3897-3908. 155223 12748291
126. Knoop LL Baker SJ The splicing factor U1C represses EWS/FLI-mediated transactivation J Biol Chem 2000, 275(32):24865-24871. 10827180
127. Knoop LL Baker SJ EWS/FLI alters 5′-splice site selection J Biol Chem 2001, 276(25):22317-22322. 11301318
128. Uren A Tcherkasskaya O Toretsky JA Recombinant EWS-FLI1 oncoprotein activates transcription Biochemistry 2004, 43(42):13579-13589. 15491164
129. Epstein J Cai J Glaser T Jepeal L Maas R Identification of a Pax paired domain recognition sequence and evidence for DNA-dependent conformational changes J Biol Chem 1994, 269(11):8355-8361. 8132558
130. Tompa P Intrinsically unstructured proteins Trends Biochem Sci 2002, 27(10):527-533. 12368089
131. Dunker AK Obradovic Z The protein trinity - linking function and disorder Nat Biotechnol 2001, 19(9):805-806. 11533628
132. Dyson HJ Wright PE Coupling of folding and binding for unstructured proteins Curr Opin Struct Biol 2002, 12(1):54-60. 11839490
133. Dyson HJ Wright PE Intrinsically unstructured proteins and their functions Nat Rev Mol Cell Biol 2005, 6(3):197-208. 15738986
134. Sigalov A Aivazian D Stern L Homooligomerization of the cytoplasmic domain of the T cell receptor zeta chain and of other proteins containing the immunoreceptor tyrosine-based activation motif Biochemistry 2004, 43(7):2049-2061. 14967045
135. Sigalov AB Multichain immune recognition receptor signaling: Different players, same game? Trends Immunol 2004, 25(11):583-589. 15489186
136. Sigalov AB Immune cell signaling: A novel mechanistic model reveals new therapeutic targets Trends Pharmacol Sci 2006, 27(10):518-524. 16908074
137. Sigalov AB Aivazian DA Uversky VN Stern LJ Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling subunits Biochemistry 2006, 45(51):15731-15739. 2528957 17176095
138. Sigalov AB Zhuravleva AV Orekhov VY Binding of intrinsically disordered proteins is not necessarily accompanied by a structural transition to a folded form Biochimie 2007, 89(3):419-421. 2692994 17174464
139. Garner E Romero P Dunker AK Brown C Obradovic Z Predicting Binding Regions within Disordered Proteins Genome Inform Ser Workshop Genome Inform 1999, 10:41-50. 11072341