Intrinsically disordered regions of p53 family are highly diversified in evolution

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 4, 2013, Pages 725-738

  Xue, Bin ^a   Brown, Celeste J ^b   Dunker, A Keith ^c   Uversky, Vladimir N ^a,d  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

Intrinsically disordered proteins; p53 family; Protein evolution; Protein DNA interaction; Protein protein interactions

Indexed keywords

PROTEIN P53; PROTEIN P63; PROTEIN P73;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; DNA BINDING; ENTROPY; HUMAN; INTRINSICALLY DISORDERED PROTEIN; MISSENSE MUTATION; MOLECULAR RECOGNITION; NONHUMAN; OLIGOMERIZATION; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN DEFECT; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; UNFOLDED PROTEIN RESPONSE;

AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE CHECKPOINTS; CONSERVED SEQUENCE; DATABASES, PROTEIN; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; GENETIC VARIATION; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; TUMOR SUPPRESSOR PROTEIN P53;

INVERTEBRATA; VERTEBRATA;

EID: 84874071407     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.01.012     Document Type: Article

References (152)

1. C.W. Anderson, and E. Appella Signaling to the p53 tumor suppressor through pathways activated by genotoxic and nongenotoxic stress R.A. Bradshaw, E.A. Dennis, Handbook of Cell Signaling 2004 Academic Press New York 237 247
2. A.C. Joerger, and A.R. Fersht Structural biology of the tumor suppressor p53 Annu. Rev. Biochem. 77 2008 557 582
3. L. Collavin, A. Lunardi, and G. Del Sal p53-Family proteins and their regulators: hubs and spokes in tumor suppression Cell Death Differ. 17 2010 901 911
4. J.F. Armstrong, M.H. Kaufman, D.J. Harrison, and A.R. Clarke High-frequency developmental abnormalities in p53-deficient mice Curr. Biol. 5 1995 931 936
5. M. Hollstein, D. Sidransky, B. Vogelstein, and C.C. Harris p53 mutations in human cancers Science 253 1991 49 53
6. D.P. Lane Cancer. p53, guardian of the genome Nature 358 1992 15 16
7. V.N. Uversky, C.J. Oldfield, U. Midic, H. Xie, B. Xue, S. Vucetic, L.M. Iakoucheva, Z. Obradovic, and A.K. Dunker Unfoldomics of human diseases: linking protein intrinsic disorder with diseases BMC Genomics 10 Suppl. 1 2009 S7
8. T. Soussi, and C. Beroud Assessing TP53 status in human tumours to evaluate clinical outcome Nat. Rev. Cancer 1 2001 233 240
9. A.C. Joerger, H.C. Ang, D.B. Veprintsev, C.M. Blair, and A.R. Fersht Structures of p53 cancer mutants and mechanism of rescue by second-site suppressor mutations J. Biol. Chem. 280 2005 16030 16037
10. J.M. Canadillas, H. Tidow, S.M. Freund, T.J. Rutherford, H.C. Ang, and A.R. Fersht Solution structure of p53 core domain: structural basis for its instability Proc. Natl. Acad. Sci. U.S.A. 103 2006 2109 2114
11. Y. Wang, A. Rosengarth, and H. Luecke Structure of the human p53 core domain in the absence of DNA Acta Crystallogr. D Biol. Crystallogr. 63 2007 276 281
12. P.E. Wright, and H.J. Dyson Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm J. Mol. Biol. 293 1999 321 331
13. A.K. Dunker, J.D. Lawson, C.J. Brown, R.M. Williams, P. Romero, J.S. Oh, C.J. Oldfield, A.M. Campen, C.M. Ratliff, K.W. Hipps, J. Ausio, M.S. Nissen, R. Reeves, C. Kang, C.R. Kissinger, R.W. Bailey, M.D. Griswold, W. Chiu, E.C. Garner, and Z. Obradovic Intrinsically disordered protein J. Mol. Graph. Model. 19 2001 26 59
14. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41 2000 415 427
15. A.K. Dunker, C.J. Brown, and Z. Obradovic Identification and functions of usefully disordered proteins Adv. Protein Chem. 62 2002 25 49
16. A.K. Dunker, Z. Obradovic, P. Romero, E.C. Garner, and C.J. Brown Intrinsic protein disorder in complete genomes Genome Inform. Ser. Workshop Genome Inform. 11 2000 161 171
17. J.J. Ward, J.S. Sodhi, L.J. McGuffin, B.F. Buxton, and D.T. Jones Prediction and functional analysis of native disorder in proteins from the three kingdoms of life J. Mol. Biol. 337 2004 635 645
18. C.J. Oldfield, Y. Cheng, M.S. Cortese, C.J. Brown, V.N. Uversky, and A.K. Dunker Comparing and combining predictors of mostly disordered proteins Biochemistry 44 2005 1989 2000
19. Z.P. Feng, X. Zhang, P. Han, N. Arora, R.F. Anders, and R.S. Norton Abundance of intrinsically unstructured proteins in P. falciparum and other apicomplexan parasite proteomes Mol. Biochem. Parasitol. 150 2006 256 267
20. P. Tompa, Z. Dosztanyi, and I. Simon Prevalent structural disorder in E. coli and S. cerevisiae proteomes J. Proteome Res. 5 2006 1996 2000
21. C.A. Galea, A.A. High, J.C. Obenauer, A. Mishra, C.G. Park, M. Punta, A. Schlessinger, J. Ma, B. Rost, C.A. Slaughter, and R.W. Kriwacki Large-scale analysis of thermostable, mammalian proteins provides insights into the intrinsically disordered proteome J. Proteome Res. 8 2009 211 226
22. P.V. Burra, L. Kalmar, and P. Tompa Reduction in structural disorder and functional complexity in the thermal adaptation of prokaryotes PLoS One 5 2010 e12069
23. B. Xue, R.W. Williams, C.J. Oldfield, A.K. Dunker, and V.N. Uversky Archaic chaos: intrinsically disordered proteins in Archaea BMC Syst. Biol. 4 Suppl. 1 2010 S1
24. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
25. E. Schad, P. Tompa, and H. Hegyi The relationship between proteome size, structural disorder and organism complexity Genome Biol. 12 2011 R120
26. B. Xue, A.K. Dunker, and V.N. Uversky Orderly order in protein intrinsic disorder distribution: Disorder in thirty five hundred proteomes from viruses and the three domains of life J. Biomol. Struct. Dyn. 30 2012 131 142
27. C.J. Oldfield, Y. Cheng, M.S. Cortese, P. Romero, V.N. Uversky, and A.K. Dunker Coupled folding and binding with alpha-helix-forming molecular recognition elements Biochemistry 44 2005 12454 12470
28. Z. Obradovic, K. Peng, S. Vucetic, P. Radivojac, C.J. Brown, and A.K. Dunker Predicting intrinsic disorder from amino acid sequence Proteins 53 Suppl. 6 2003 566 572
29. A.K. Dunker, C.J. Brown, J.D. Lawson, L.M. Iakoucheva, and Z. Obradovic Intrinsic disorder and protein function Biochemistry 41 2002 6573 6582
30. V.N. Uversky, C.J. Oldfield, and A.K. Dunker Intrinsically disordered proteins in human diseases: introducing the D2 concept Annu. Rev. Biophys. 37 2008 215 246
31. L. Breydo, J.W. Wu, and V.N. Uversky Alpha-synuclein misfolding and Parkinson's disease Biochim. Biophys. Acta 1822 2012 261 285
32. V.N. Uversky Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation J. Neurochem. 103 2007 17 37
33. J.M. George The synucleins Genome Biol. 3 2002 (REVIEWS3002)
34. F. Vonderviszt, S. Kanto, S. Aizawa, and K. Namba Terminal regions of flagellin are disordered in solution J. Mol. Biol. 209 1989 127 133
35. J.W. Chen, P. Romero, V.N. Uversky, and A.K. Dunker Conservation of intrinsic disorder in protein domains and families: II. Functions of conserved disorder J. Proteome Res. 5 2006 888 898
36. J.W. Chen, P. Romero, V.N. Uversky, and A.K. Dunker Conservation of intrinsic disorder in protein domains and families: I. A database of conserved predicted disordered regions J. Proteome Res. 5 2006 879 887
37. P. Tompa, M. Fuxreiter, C.J. Oldfield, I. Simon, A.K. Dunker, and V.N. Uversky Close encounters of the third kind: disordered domains and the interactions of proteins Bioessays 31 2009 328 335
38. C.J. Brown, S. Takayama, A.M. Campen, P. Vise, T.W. Marshall, C.J. Oldfield, C.J. Williams, and A.K. Dunker Evolutionary rate heterogeneity in proteins with long disordered regions J. Mol. Evol. 55 2002 104 110
39. S.C. Chen, T.J. Chuang, and W.H. Li The relationships among microRNA regulation, intrinsically disordered regions, and other indicators of protein evolutionary rate Mol. Biol. Evol. 28 2011 2513 2520
40. Y.S. Lin, W.L. Hsu, J.K. Hwang, and W.H. Li Proportion of solvent-exposed amino acids in a protein and rate of protein evolution Mol. Biol. Evol. 24 2007 1005 1011
41. A.K. Dunker, E. Garner, S. Guilliot, P. Romero, K. Albrecht, J. Hart, Z. Obradovic, C. Kissinger, and J.E. Villafranca Protein disorder and the evolution of molecular recognition: theory, predictions and observations Pac. Symp. Biocomput. 1998 473 484
42. W.L. Shaiu, T. Hu, and T.S. Hsieh The hydrophilic, protease-sensitive terminal domains of eucaryotic DNA topoisomerases have essential intracellular functions Pac. Symp. Biocomput. 1999 578 589
43. E.W. Sayers, R.B. Gerstner, D.E. Draper, and D.A. Torchia Structural preordering in the N-terminal region of ribosomal protein S4 revealed by heteronuclear NMR spectroscopy Biochemistry 39 2000 13602 13613
44. R. Wissmann, T. Baukrowitz, H. Kalbacher, H.R. Kalbitzer, J.P. Ruppersberg, O. Pongs, C. Antz, and B. Fakler NMR structure and functional characteristics of the hydrophilic N terminus of the potassium channel beta-subunit Kvbeta1.1 J. Biol. Chem. 274 1999 35521 35525
45. C.J. Brown, A.K. Johnson, A.K. Dunker, and G.W. Daughdrill Evolution and disorder Curr. Opin. Struct. Biol. 21 2011 441 446
46. J. Nilsson, M. Grahn, and A.P. Wright Proteome-wide evidence for enhanced positive Darwinian selection within intrinsically disordered regions in proteins Genome Biol. 12 2011 R65
47. L.B. Chemes, J. Glavina, L.G. Alonso, C. Marino-Buslje, G. de Prat-Gay, and I.E. Sanchez Sequence evolution of the intrinsically disordered and globular domains of a model viral oncoprotein PLoS One 7 2012 e47661
48. G.W. Daughdrill, P. Narayanaswami, S.H. Gilmore, A. Belczyk, and C.J. Brown Dynamic behavior of an intrinsically unstructured linker domain is conserved in the face of negligible amino acid sequence conservation J. Mol. Evol. 65 2007 277 288
49. H.A. Moesa, S. Wakabayashi, K. Nakai, and A. Patil Chemical composition is maintained in poorly conserved intrinsically disordered regions and suggests a means for their classification Mol. Biosyst. 8 2012 3262 3273
50. M. Osada, M. Ohba, C. Kawahara, C. Ishioka, R. Kanamaru, I. Katoh, Y. Ikawa, Y. Nimura, A. Nakagawara, M. Obinata, and S. Ikawa Cloning and functional analysis of human p51, which structurally and functionally resembles p53 Nat. Med. 4 1998 839 843
51. A. Yang, M. Kaghad, Y. Wang, E. Gillett, M.D. Fleming, V. Dotsch, N.C. Andrews, D. Caput, and F. McKeon p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities Mol. Cell 2 1998 305 316
52. M. Kaghad, H. Bonnet, A. Yang, L. Creancier, J.C. Biscan, A. Valent, A. Minty, P. Chalon, J.M. Lelias, X. Dumont, P. Ferrara, F. McKeon, and D. Caput Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers Cell 90 1997 809 819
53. A. Yang, M. Kaghad, D. Caput, and F. McKeon On the shoulders of giants: p63, p73 and the rise of p53 Trends Genet. 18 2002 90 95
54. F. Murray-Zmijewski, D.P. Lane, and J.C. Bourdon p53/p63/p73 isoforms: an orchestra of isoforms to harmonise cell differentiation and response to stress Cell Death Differ. 13 2006 962 972
55. V.P. Sah, L.D. Attardi, G.J. Mulligan, B.O. Williams, R.T. Bronson, and T. Jacks A subset of p53-deficient embryos exhibit exencephaly Nat. Genet. 10 1995 175 180
56. V. Rotter, D. Schwartz, E. Almon, N. Goldfinger, A. Kapon, A. Meshorer, L.A. Donehower, and A.J. Levine Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome Proc. Natl. Acad. Sci. U.S.A. 90 1993 9075 9079
57. L.A. Donehower, M. Harvey, B.L. Slagle, M.J. McArthur, C.A. Montgomery Jr., J.S. Butel, and A. Bradley Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours Nature 356 1992 215 221
58. A. Yang, N. Walker, R. Bronson, M. Kaghad, M. Oosterwegel, J. Bonnin, C. Vagner, H. Bonnet, P. Dikkes, A. Sharpe, F. McKeon, and D. Caput p73-Deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours Nature 404 2000 99 103
59. M. Senoo, F. Pinto, C.P. Crum, and F. McKeon p63 is essential for the proliferative potential of stem cells in stratified epithelia Cell 129 2007 523 536
60. X. Su, M. Paris, Y.J. Gi, K.Y. Tsai, M.S. Cho, Y.L. Lin, J.A. Biernaskie, S. Sinha, C. Prives, L.H. Pevny, F.D. Miller, and E.R. Flores TAp63 prevents premature aging by promoting adult stem cell maintenance Cell Stem Cell 5 2009 64 75
61. A.A. Mills, B. Zheng, X.J. Wang, H. Vogel, D.R. Roop, and A. Bradley p63 is a p53 homologue required for limb and epidermal morphogenesis Nature 398 1999 708 713
62. A. Yang, R. Schweitzer, D. Sun, M. Kaghad, N. Walker, R.T. Bronson, C. Tabin, A. Sharpe, D. Caput, C. Crum, and F. McKeon p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development Nature 398 1999 714 718
63. M.S. Irwin, and W.G. Kaelin p53 family update: p73 and p63 develop their own identities Cell Growth Differ. 12 2001 337 349
64. M.S. Irwin, and W.G. Kaelin Jr. Role of the newer p53 family proteins in malignancy Apoptosis 6 2001 17 29
65. T. Ozaki, M. Naka, N. Takada, M. Tada, S. Sakiyama, and A. Nakagawara Deletion of the COOH-terminal region of p73alpha enhances both its transactivation function and DNA-binding activity but inhibits induction of apoptosis in mammalian cells Cancer Res. 59 1999 5902 5907
66. K.L. Harms, and X. Chen The C terminus of p53 family proteins is a cell fate determinant Mol. Cell. Biol. 25 2005 2014 2030
67. W.J. Lu, J.F. Amatruda, and J.M. Abrams p53 ancestry: gazing through an evolutionary lens Nat. Rev. Cancer 9 2009 758 762
68. B.I. Lee Kobayashi, K.W. Makabe, C. Manohar, G. Matassi, M. Medina, Y. Mochizuki, S. Mount, T. Morishita, S. Miura, A. Nakayama, S. Nishizaka, H. Nomoto, F. Ohta, K. Oishi, I. Rigoutsos, M. Sano, A. Sasaki, Y. Sasakura, E. Shoguchi, T. Shin-i, A. Spagnuolo, D. Stainier, M.M. Suzuki, O. Tassy, N. Takatori, M. Tokuoka, K. Yagi, F. Yoshizaki, S. Wada, C. Zhang, P.D. Hyatt, F. Larimer, C. Detter, N. Doggett, T. Glavina, T. Hawkins, P. Richardson, S. Lucas, Y. Kohara, M. Levine, N. Satoh, and D.S. Rokhsar The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins Science 298 2002 2157 2167
69. N.H. Putnam, M. Srivastava, U. Hellsten, B. Dirks, J. Chapman, A. Salamov, A. Terry, H. Shapiro, E. Lindquist, V.V. Kapitonov, J. Jurka, G. Genikhovich, I.V. Grigoriev, S.M. Lucas, R.E. Steele, J.R. Finnerty, U. Technau, M.Q. Martindale, and D.S. Rokhsar Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization Science 317 2007 86 94
70. S. Pankow, and C. Bamberger The p53 tumor suppressor-like protein nvp63 mediates selective germ cell death in the sea anemone Nematostella vectensis PLoS One 2 2007 e782
71. N. King, M.J. Westbrook, S.L. Young, A. Kuo, M. Abedin, J. Chapman, S. Fairclough, U. Hellsten, Y. Isogai, I. Letunic, M. Marr, D. Pincus, N. Putnam, A. Rokas, K.J. Wright, R. Zuzow, W. Dirks, M. Good, D. Goodstein, D. Lemons, W. Li, J.B. Lyons, A. Morris, S. Nichols, D.J. Richter, A. Salamov, J.G. Sequencing, P. Bork, W.A. Lim, G. Manning, W.T. Miller, W. McGinnis, H. Shapiro, R. Tjian, I.V. Grigoriev, and D. Rokhsar The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans Nature 451 2008 783 788
72. L. Mendoza, E. Orozco, M.A. Rodriguez, G. Garcia-Rivera, T. Sanchez, E. Garcia, and P. Gariglio Ehp53, an Entamoeba histolytica protein, ancestor of the mammalian tumour suppressor p53 Microbiology 149 2003 885 893
73. V.A. Belyi, P. Ak, E. Markert, H. Wang, W. Hu, A. Puzio-Kuter, and A.J. Levine The origins and evolution of the p53 family of genes Cold Spring Harb. Perspect. Biol. 2 2010 a001198
74. D.P. Lane, C.F. Cheok, C. Brown, A. Madhumalar, F.J. Ghadessy, and C. Verma Mdm2 and p53 are highly conserved from placozoans to man Cell Cycle 9 2010 540 547
75. A.J. Levine The evolution of the p53 family of genes Cell Cycle 11 2012 214 215
76. D.P. Lane, A. Madhumalar, A.P. Lee, B.H. Tay, C. Verma, S. Brenner, and B. Venkatesh Conservation of all three p53 family members and Mdm2 and Mdm4 in the cartilaginous fish Cell Cycle 10 2011 4272 4279
77. D. Bordo, and P. Argos Evolution of protein cores. Constraints in point mutations as observed in globin tertiary structures J. Mol. Biol. 211 1990 975 988
78. A.M. Dean, C. Neuhauser, E. Grenier, and G.B. Golding The pattern of amino acid replacements in alpha/beta-barrels Mol. Biol. Evol. 19 2002 1846 1864
79. J. Liu, H. Tan, and B. Rost Loopy proteins appear conserved in evolution J. Mol. Biol. 322 2002 53 64
80. P. Radivojac, Z. Obradovic, D.K. Smith, G. Zhu, S. Vucetic, C.J. Brown, J.D. Lawson, and A.K. Dunker Protein flexibility and intrinsic disorder Protein Sci. 13 2004 71 80
81. R.L. Jernigan, and A. Kloczkowski Packing regularities in biological structures relate to their dynamics Methods Mol. Biol. 350 2007 251 276
82. C. Schaefer, A. Schlessinger, and B. Rost Protein secondary structure appears to be robust under in silico evolution while protein disorder appears not to be Bioinformatics 26 2010 625 631
83. C.J. Brown, A.K. Johnson, and G.W. Daughdrill Comparing models of evolution for ordered and disordered proteins Mol. Biol. Evol. 27 2010 609 621
84. P. Artimo, M. Jonnalagedda, K. Arnold, D. Baratin, G. Csardi, E. de Castro, S. Duvaud, V. Flegel, A. Fortier, E. Gasteiger, A. Grosdidier, C. Hernandez, V. Ioannidis, D. Kuznetsov, R. Liechti, S. Moretti, K. Mostaguir, N. Redaschi, G. Rossier, I. Xenarios, and H. Stockinger ExPASy: SIB bioinformatics resource portal Nucleic Acids Res. 40 2012 W597 W603
85. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402
86. B. Xue, R.L. Dunbrack, R.W. Williams, A.K. Dunker, and V.N. Uversky PONDR-FIT: a meta-predictor of intrinsically disordered amino acids Biochim. Biophys. Acta 1804 2010 996 1010
87. P. Romero, Z. Obradovic, C.R. Kissinger, J.E. Villafranca, and A.K. Dunker Identifying Disordered regions in proteins from amino acid sequences IEEE Int. Conf. Neural Netw. 1 1997 90 95
88. P. Romero, Z. Obradovic, X. Li, E.C. Garner, C.J. Brown, and A.K. Dunker Sequence complexity of disordered protein Proteins 42 2001 38 48
89. Z. Obradovic, K. Peng, S. Vucetic, P. Radivojac, and A.K. Dunker Exploiting heterogeneous sequence properties improves prediction of protein disorder Proteins 61 Suppl. 7 2005 176 182
90. K. Peng, P. Radivojac, S. Vucetic, A.K. Dunker, and Z. Obradovic Length-dependent prediction of protein intrinsic disorder BMC Bioinformatics 7 2006
91. S. Vucetic, C.J. Brown, A.K. Dunker, and Z. Obradovic Flavors of protein disorder Proteins 52 2003 573 584
92. K. Peng, S. Vucetic, P. Radivojac, C.J. Brown, A.K. Dunker, and Z. Obradovic Optimizing long intrinsic disorder predictors with protein evolutionary information J. Bioinform. Comput. Biol. 3 2005 35 60
93. J. Prilusky, C.E. Felder, T. Zeev-Ben-Mordehai, E.H. Rydberg, O. Man, J.S. Beckmann, I. Silman, and J.L. Sussman FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded Bioinformatics 21 2005 3435 3438
94. Z. Dosztanyi, V. Csizmok, P. Tompa, and I. Simon The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins J. Mol. Biol. 347 2005 827 839
95. A. Campen, R.M. Williams, C.J. Brown, J. Meng, V.N. Uversky, and A.K. Dunker TOP-IDP-scale: a new amino acid scale measuring propensity for intrinsic disorder Protein Pept. Lett. 15 2008 956 963
96. B. Xue, C.J. Oldfield, A.K. Dunker, and V.N. Uversky CDF it all: consensus prediction of intrinsically disordered proteins based on various cumulative distribution functions FEBS Lett. 583 2009 1469 1474
97. Y. Cheng, C.J. Oldfield, J. Meng, P. Romero, V.N. Uversky, and A.K. Dunker Mining alpha-helix-forming molecular recognition features with cross species sequence alignments Biochemistry 46 2007 13468 13477
98. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533
99. A.K. Dunker, M.S. Cortese, P. Romero, L.M. Iakoucheva, and V.N. Uversky Flexible nets. The roles of intrinsic disorder in protein interaction networks FEBS J. 272 2005 5129 5148
100. P. Radivojac, L.M. Iakoucheva, C.J. Oldfield, Z. Obradovic, V.N. Uversky, and A.K. Dunker Intrinsic disorder and functional proteomics Biophys. J. 92 2007 1439 1456
101. V.N. Uversky, C.J. Oldfield, and A.K. Dunker Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signalling J. Mol. Recognit. 18 2005 343 384
102. H.J. Dyson, and P.E. Wright Coupling of folding and binding for unstructured proteins Curr. Opin. Struct. Biol. 12 2002 54 60
103. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 2005 197 208
104. A. Mohan, C.J. Oldfield, P. Radivojac, V. Vacic, M.S. Cortese, A.K. Dunker, and V.N. Uversky Analysis of molecular recognition features (MoRFs) J. Mol. Biol. 362 2006 1043 1059
105. V. Vacic, C.J. Oldfield, A. Mohan, P. Radivojac, M.S. Cortese, V.N. Uversky, and A.K. Dunker Characterization of molecular recognition features, MoRFs, and their binding partners J. Proteome Res. 6 2007 2351 2366
106. E. Garner, P. Romero, A.K. Dunker, C. Brown, and Z. Obradovic Predicting binding regions within disordered proteins Genome Inform. Ser. Workshop Genome Inform. 10 1999 41 50
107. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
108. S. Kumar, M. Nei, J. Dudley, and K. Tamura MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences Brief. Bioinform. 9 2008 299 306
109. G.E. Crooks, G. Hon, J.M. Chandonia, and S.E. Brenner WebLogo: a sequence logo generator Genome Res. 14 2004 1188 1190
110. T.D. Schneider, and R.M. Stephens Sequence logos: a new way to display consensus sequences Nucleic Acids Res. 18 1990 6097 6100
111. G.M. Popowicz, A. Czarna, and T.A. Holak Structure of the human Mdmx protein bound to the p53 tumor suppressor transactivation domain Cell Cycle 7 2008 2441 2443
112. P.R. Mittl, P. Chene, and M.G. Grutter Crystallization and structure solution of p53 (residues 326-356) by molecular replacement using an NMR model as template Acta Crystallogr. D Biol. Crystallogr. 54 1998 86 89
113. J.L. Avalos, I. Celic, S. Muhammad, M.S. Cosgrove, J.D. Boeke, and C. Wolberger Structure of a Sir2 enzyme bound to an acetylated p53 peptide Mol. Cell 10 2002 523 535
114. C.H. Arrowsmith Structure and function in the p53 family Cell Death Differ. 6 1999 1169 1173
115. M.L. Connolly The molecular surface package J. Mol. Graph. 11 1993 139 141
116. F. Eisenhaber, P. Lijnzaad, P. Argos, C. Sander, and M. Scharf The double cubic lattice method - efficient approaches to numerical-integration of surface-area and volume and to dot surface contouring of molecular assemblies J. Comput. Chem. 16 1995 273 284
117. S. Jones, and J.M. Thornton Prediction of protein-protein interaction sites using patch analysis J. Mol. Biol. 272 1997 133 143
118. S. Jones, and J.M. Thornton Analysis of protein-protein interaction sites using surface patches J. Mol. Biol. 272 1997 121 132
119. C.J. Oldfield, J. Meng, J.Y. Yang, M.Q. Yang, V.N. Uversky, and A.K. Dunker Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners BMC Genomics 9 Suppl. 1 2008 S1
120. E.D. Lowe, I. Tews, K.Y. Cheng, N.R. Brown, S. Gul, M.E. Noble, S.J. Gamblin, and L.N. Johnson Specificity determinants of recruitment peptides bound to phospho-CDK2/cyclin A Biochemistry 41 2002 15625 15634
121. S. Mujtaba, Y. He, L. Zeng, S. Yan, O. Plotnikova, Sachchidanand, R. Sanchez, N.J. Zeleznik-Le, Z. Ronai, and M.M. Zhou Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation Mol. Cell 13 2004 251 263
122. H. Wu, M.W. Maciejewski, A. Marintchev, S.E. Benashski, G.P. Mullen, and S.M. King Solution structure of a dynein motor domain associated light chain Nat. Struct. Biol. 7 2000 575 579
123. B.C. McNulty, G.B. Young, and G.J. Pielak Macromolecular crowding in the Escherichia coli periplasm maintains alpha-synuclein disorder J. Mol. Biol. 355 2006 893 897
124. C. Li, L.M. Charlton, A. Lakkavaram, C. Seagle, G. Wang, G.B. Young, J.M. Macdonald, and G.J. Pielak Differential dynamical effects of macromolecular crowding on an intrinsically disordered protein and a globular protein: implications for in-cell NMR spectroscopy J. Am. Chem. Soc. 130 2008 6310 6311
125. C. Li, G.F. Wang, Y. Wang, R. Creager-Allen, E.A. Lutz, H. Scronce, K.M. Slade, R.A. Ruf, R.A. Mehl, and G.J. Pielak Protein (19)F NMR in Escherichia coli J. Am. Chem. Soc. 132 2010 321 327
126. A.P. Schlesinger, Y. Wang, X. Tadeo, O. Millet, and G.J. Pielak Macromolecular crowding fails to fold a globular protein in cells J. Am. Chem. Soc. 133 2011 8082 8085
127. B. Fauvet, M.B. Fares, F. Samuel, I. Dikiy, A. Tandon, D. Eliezer, and H.A. Lashuel Characterization of semisynthetic and naturally nalpha-acetylated alpha-synuclein in vitro and in intact cells: implications for aggregation and cellular properties of alpha-synuclein J. Biol. Chem. 287 2012 28243 28262
128. A. Binolfi, F.X. Theillet, and P. Selenko Bacterial in-cell NMR of human alpha-synuclein: a disordered monomer by nature? Biochem. Soc. Trans. 40 2012 950 954
129. R. Thongwichian, and P. Selenko In-cell NMR in Xenopus laevis oocytes Methods Mol. Biol. 895 2012 33 41
130. B. Bekei, H.M. Rose, M. Herzig, A. Dose, D. Schwarzer, and P. Selenko In-cell NMR in mammalian cells: part 1 Methods Mol. Biol. 895 2012 43 54
131. B. Bekei, H.M. Rose, M. Herzig, and P. Selenko In-cell NMR in mammalian cells: part 2 Methods Mol. Biol. 895 2012 55 66
132. B. Bekei, H.M. Rose, M. Herzig, H. Stephanowitz, E. Krause, and P. Selenko In-cell NMR in mammalian cells: part 3 Methods Mol. Biol. 895 2012 67 83
133. Y. Ito, T. Mikawa, and B.O. Smith In-cell NMR of intrinsically disordered proteins in prokaryotic cells Methods Mol. Biol. 895 2012 19 31
134. J. Janin, and M.J.E. Sternberg Protein flexibility, not disorder, is intrinsic to molecular recognition F1000 Biol. Rep. 5 2013
135. V.M. Parmar, and M. Schroder Sensing endoplasmic reticulum stress Adv. Exp. Med. Biol. 738 2012 153 168
136. A.K. Dunker, and V.N. Uversky The case for intrinsically disordered proteins playing contributory roles in molecular recognition without a stable 3D structure, F1000 Biol Rep. 5 2013 1
137. C.E. Shamu, and P. Walter Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus EMBO J. 15 1996 3028 3039
138. A.A. Welihinda, and R.J. Kaufman The unfolded protein response pathway in Saccharomyces cerevisiae. Oligomerization and trans-phosphorylation of Ire1p (Ern1p) are required for kinase activation J. Biol. Chem. 271 1996 18181 18187
139. J.S. Cox, and P. Walter A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response Cell 87 1996 391 404
140. T. Kawahara, H. Yanagi, T. Yura, and K. Mori Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response Mol. Biol. Cell 8 1997 1845 1862
141. C. Sidrauski, and P. Walter The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response Cell 90 1997 1031 1039
142. T.N. Gonzalez, C. Sidrauski, S. Dorfler, and P. Walter Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway EMBO J. 18 1999 3119 3132
143. K.J. Travers, C.K. Patil, L. Wodicka, D.J. Lockhart, J.S. Weissman, and P. Walter Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation Cell 101 2000 249 258
144. A. Todd-Corlett, E. Jones, C. Seghers, and M.J. Gething Lobe IB of the ATPase domain of Kar2p/BiP interacts with Ire1p to negatively regulate the unfolded protein response in Saccharomyces cerevisiae J. Mol. Biol. 367 2007 770 787
145. J.J. Credle, J.S. Finer-Moore, F.R. Papa, R.M. Stroud, and P. Walter On the mechanism of sensing unfolded protein in the endoplasmic reticulum Proc. Natl. Acad. Sci. U.S.A. 102 2005 18773 18784
146. M.J. Gething Role and regulation of the ER chaperone BiP Semin. Cell Dev. Biol. 10 1999 465 472
147. B. Kleizen, and I. Braakman Protein folding and quality control in the endoplasmic reticulum Curr. Opin. Cell Biol. 16 2004 343 349
148. Y. Ma, and L.M. Hendershot ER chaperone functions during normal and stress conditions J. Chem. Neuroanat. 28 2004 51 65
149. L.M. Hendershot The ER function BiP is a master regulator of ER function Mt. Sinai J. Med. 71 2004 289 297
150. S. Blond-Elguindi, S.E. Cwirla, W.J. Dower, R.J. Lipshutz, S.R. Sprang, J.F. Sambrook, and M.J. Gething Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP Cell 75 1993 717 728
151. P.J. Bjorkman, and P. Parham Structure, function, and diversity of class I major histocompatibility complex molecules Annu. Rev. Biochem. 59 1990 253 288
152. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 27 28