Intrinsically unstructured proteins and their functions

Nature Reviews Molecular Cell Biology

Volumn 6, Issue 3, 2005, Pages 197-208

  Dyson, H Jane ^a   Wright, Peter E ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HOMEODOMAIN PROTEIN; PROTEIN; PROTEIN P300; PROTEIN P53; RNA 5S; RNA BINDING PROTEIN; STEROID RECEPTOR COACTIVATOR 1; UBIQUITIN PROTEIN LIGASE E3; ZINC FINGER PROTEIN;

CIRCULAR DICHROISM; CRYSTAL STRUCTURE; DNA DAMAGE; DNA SEQUENCE; EUKARYOTE; GENE FUNCTION; GENE MAPPING; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENOME; HUMAN; MACROMOLECULE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; SPECIES DIFFERENCE; TRANSCRIPTION INITIATION; ZINC FINGER MOTIF;

CREB-BINDING PROTEIN; HUMANS; NUCLEAR PROTEINS; NUCLEIC ACIDS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEINS; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 14644435825     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1589     Document Type: Review

References (126)

1. Dunker, A. K., Brown, C. J., Lawson, J. D., Iakoucheva, L. M. & Obradovic, Z. Intrinsic disorder and protein function. Biochemistry 41, 6573-6582 (2002).
2. Uversky, V. N. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11, 739-756 (2002). Provides a comprehensive review of the field of unfolded proteins with much valuable analysis. It contains the most up-to-date table of unfolded proteins.
3. 1H nuclear-magnetic-resonance studies of the molecular conformation of monomeric glucagon in aqueous solution. Eur. J. Biochem. 91, 209-214 (1978).
4. Daniels, A. J., Williams, R. J. P. & Wright, P. E. The character of the stored molecules in chromaffin granules of the adrenal medulla: a nuclear magnetic resonance study. Neuroscience 3, 573-585 (1978).
5. Wright, P. E. & Dyson, H. J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293, 321-331 (1999).
6. Iakoucheva, L. M., Brown, C. J., Lawson, J. D., Obradovic, Z. & Dunker, A. K. Intrinsic disorder in cell-signaling and cancer-associated proteins. J. Mol. Biol. 323, 573-584 (2002).
7. Iakoucheva, L. M.et al. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32, 1037-1049 (2004).
8. Tompa, P. Intrinsically unstructured proteins. Trends Biochem. Sci. 27, 527-533 (2002).
9. Romero, P. et al. Sequence complexity of disordered protein. Proteins 42, 38-48 (2001).
10. Vucetic, S., Brown, C. J., Dunker, A. K. & Obradovic, Z. Flavors of protein disorder. Proteins 52, 573-584 (2003).
11. Mitchell, P. J. & Tjian, R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science 245, 371-378 (1989).
12. 1H NMR. Biochemistry 31, 4150-4156 (1992).
13. Longhi, S. et al. 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 (2003).
14. Romero, P., Obradovic, Z., Kissinger, C. R., Villafranca, J. E. & Dunker, A. K. Identifying disordered regions in proteins from amino acid sequences. Proc. IEEE Int. Conf. Neural Netw. 1, 90-95 (1997).
15. Uversky, V. N., Gillespie, J. R. & Fink, A. L. Why are 'natively unfolded' proteins unstructured under physiologic conditions? Proteins 41, 415-427 (2000).
16. Unding, R. et al. Protein disorder prediction: implications for structural proteomics. Structure (Camb.) 11, 1453-1459 (2003).
17. Linding, R., Russell, R. B., Neduva, V. & Gibson, T. J. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701-3708 (2003).
18. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F. & Jones, D. T. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337, 635-645 (2004).
19. Weathers, E. A., Paulaitis, M. E., Woolf, T. B. & Hoh, J. H. Reduced amino acid alphabet is sufficient to accurately recognize intrinsically disordered protein. FEBS Lett. 576, 348-352 (2004).
20. Dunker, A. K. et al. Intrinsically disordered protein. J. Mol. Graph. Model. 19, 26-59 (2001).
21. Vucetic, S. et al. DisProt: a database of protein disorder. Bioinformatics 21, 137-140 (2005).
22. Tompa, P. Intrinsically unstructured proteins evolve by repeat expansion. Bioessays 25, 847-855 (2003).
23. Dyson, H. J. & Wright, P. E. Nuclear magnetic resonance methods for elucidation of structure and dynamics of disordered states. Methods Enzymol. 339, 258-270 (2001).
24. Dyson, H. J. & Wright, P. E. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104, 3607-3622 (2004).
25. Rose, G. D. in Advances in Protein Chemistry Vol. 62, (eds Richards, F. M., Eisenberg, D. S. & Kuriyan, J.) (Academic Press, San Diego, 2002). This book provides an excellent introduction to the biophysical techniques that can be used to identify and characterize unfolded proteins and protein domains.
26. Dyson, H. J. & Wright, P. E. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv. Protein Chem. 62, 311-340 (2002).
27. Rucker, A. L., Pager, C. T., Campbell, M. N., Quails, J. E. & Creamer, T. P. Host-guest scale of left-handed polyproline II helix formation. Proteins 53, 68-75 (2003).
28. Shi, Z., Olson, C. A., Rose, G. D., Babwin, R. L. & Kallenbach, N. R. Polyproline II structure in a sequence of seven alanine residues. Proc. Natl Acad. Sci. USA 99, 9190-9195 (2002).
29. Dunker, A. K., Obradovic, Z., Romero, P., Garner, E. C. & Brown, C. J. Intrinsic protein disorder in complete genomes. Genome Inform. Ser. Workshop Genome Inform. 11, 161-171 (2000).
30. Wootton, J. C. & Drummond, M. H. The Q-linker: a class of interdomain sequences found in bacterial multidomain regulatory proteins. Protein Eng. Des. Sci. 2, 535-543 (1989).
31. Zhou, H. X. Quantitative account of the enhanced affinity of two linked scFvs specific for different epitopes on the same antigen. J. Mol. Biol. 329, 1-8 (2003).
32. 2 zinc fingers. J. Mol. Biol. 295, 719-727 (2000).
33. Young, M. A., Gonfloni, S., Superti-Furga, G., Roux, B. & Kuriyan, J. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell 105, 115-126 (2001).
34. Laity, J. H., Dyson, H. J. & Wright, P. E. Molecular basis for modulation of biological function by alternate splicing of the Wilms' tumor suppressor protein. Proc. Natl Acad. Sci. USA 97, 11932-11935 (2000).
35. Namba, K. Roles of partly unfolded conformations in macromolecular self-assembly. Genes Cells 6, 1-12 (2001).
36. Tompa, P. & Csermely, P. The role of structural disorder in the function of RNA and protein chaperones. FASEB J. 18, 1169-1175 (2004).
37. Dyson, H. J. & Wright, P. E. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 12, 54-60 (2002). Provides a comprehensive survey of protein folding and binding events.
38. Demchenko, A. P. Recognition between flexible protein molecules: induced and assisted folding. J. Mol. Recognit. 14, 42-61 (2001).
39. 133-phosphorylated and non-phosphorylated forms of the kinase inducible transactivation domain of CREB. FEBS Lett. 430, 317-322 (1998).
40. Richards, J. P., Bächinger, H. P., Goodman, R. H. & Brennan, R. G. Analysis of the structural properties of cAMP-responsive element-binding protein (CREB) and phosphorylated CREB. J. Biol. Chem. 271, 13716-13723 (1996).
41. Radhakrishnan, I. et al. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator: coactivator interactions. Cell 91, 741-752 (1997).
42. Zhou, P., Lugovskoy, A. A., McCarty, J. S., Li, P. & Wagner, G. Solution structure of DFF40 and DFF45 N-terminal domain complex and mutual chaperone activity of DFF40 and DFF45. Proc. Natl Acad. Sci. USA 98, 6051-6055 (2001).
43. Giordano, A. & Avantaggiati, M. L. p300 and CBP: partners for life and death. J. Cell. Physiol. 181, 218-230 (1999).
44. Blobel, G. A. CREB-binding protein and p300: molecular integrators of hematopoietic transcription. Blood 95, 745-755 (2000).
45. Goodman, R. H. & Smolik, S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 14, 1553-1577 (2000).
46. Ponting, C. P., Blake, D. J., Davies, K. E., Kendrick-Jones, J. & Winder, S. J. ZZ and TAZ: new putative zinc fingers in dystrophin and other proteins. Trends Biochem. Sci. 21, 11-13 (1996).
47. De Guzman, R. N., Liu, H. Y., Martinez-Yamout, M., Dyson, H. J. & Wright, P. E. Solution structure of the TAZ2 (CH3) domain of the transcriptional adaptor protein CBP. J. Mol. Biol. 303, 243-253 (2000).
48. Dames, S. A., Martinez-Yamout, M., De Guzman, R. N., Dyson, H. J. & Wright, P. E. Structural basis for Hif-1α/CBP recognition in the cellular hypoxic response. Proc. Natl Acad. Sci. USA 99, 5271 -5276 (2002).
49. Eckner, R. et al. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev. 8, 869-884 (1994).
50. Avantaggiati, M. et al. Recruitment of p300/CBP in p53-dependent signal pathways. Cell 89, 1175-1184 (1997).
51. Lill, N. L., Grossman, S. R., Ginsberg, D., DeCaprio, J. & Livingston, D. M. Binding and modulation of p53 by p300/CBP coactivators. Nature 387, 823-827 (1997).
52. Gu, W., Shi, X. L. & Roeder, R. G. Synergistic activation of transcription by CBP and p53. Nature 387, 819-823 (1997).
53. Arany, Z. et al. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl Acad. Sci. USA 93, 12969-12973 (1996).
54. Freedman, S. J. et al. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1α. Proc. Natl Acad. Sci. USA 99, 5367-5372 (2002).
55. Gunasekaran, K., Tsai, C. J., Kumar, S., Zanuy, D. & Nussinov, R. Extended disordered proteins: targeting function with less scaffold. Trends Biochem. Sci. 28, 81-85 (2003). Points out that the extensive interfaces observed when unfolded proteins bind their targets would only be possible for fully structured proteins if they were much larger. However, increased protein size would result in greater macromolecular crowding or would require cells to be larger.
56. Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382, 325-331 (1996).
57. Huber, A. H. & Weis, W. I. The structure of the β-catenin/ E-cadherin complex and the molecular basis of diverse ligand recognition by β-catenin. Cell 105, 391-402 (2001).
58. 28/FlgM reveals an intact σ factor in an inactive conformation. Mol. Cell 14, 127-138 (2004).
59. Bhattacharya, S. et al. Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev. 13, 64-75 (1999).
60. Freedman, S. J. et al. Structural basis for negative regulation of hypoxia-inducible factor-1α by CITED2. Nature Struct. Biol. 10, 504-512 (2003).
61. De Guzman, R. N., Martinez-Yamout, M., Dyson, H. J. & Wright, P. E. Interaction of the TAZ1 domain of CREB-binding protein with the activation domain of CITED2: regulation by competition between intrinsically unstructured ligands for non-identical binding sites. J. Biol. Chem. 279, 3042-3049 (2004).
62. 2-regulated prolyl hydroxylation. Science 292, 468-472 (2001).
63. 2 sensing. Science 292, 464-468 (2001).
64. Yu, F., White, S. B., Zhao, Q. & Lee, F. S. HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl Acad Sci. USA 98, 9630-9635 (2001).
65. Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J. & Whitelaw, M. L. Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295, 858-861 (2002).
66. Elkins, J. M. et al. Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1α. J. Biol. Chem. 278, 1802-1806 (2003).
67. Dann, C. E. III, Bruick, R. K. & Deisenhofer, J. Structure of factor-inhibiting hypoxia-inducible factor 1: an asparaginyl hydroxylase involved in the hypoxic response pathway. Proc. Natl Acad. Sci. USA 99, 15351-15356 (2002).
68. Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc. Natl Acad. Sci. USA 93, 11504-11509 (1996).
69. Hon, W. et al. Structural basis for the recognition of hydroxyproline in HIF-1α by pVHL. Nature 417, 975-978 (2002).
70. Min, J. H. et al. Structure of an HIF-1α-pVHL complex: hydroxyproline recognition in signaling. Science 296, 1886-1889 (2002).
71. Chrivia, J. C. et al. Phosphorylated CREB binds specifically to nuclear protein CBP. Nature 365, 855-859 (1993).
72. Zor, T., Mayr, B. M., Dyson, H. J., Montminy, M. R. & Wright, P. E. Roles of phosphorylation and helix propensity in the binding of the KIX domain of CREB-binding protein by constitutive (c-Myb) and inducible (CREB) activators. J. Biol. Chem. 277, 42241-42248 (2002).
73. Knighton, D. R. et al. Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 414-420 (1991).
74. Goto, N. K., Zor, T., Martinez-Yamout, M., Dyson, H. J. & Wright, P. E. Cooperativity in transcription factor binding to the coactivator CREB-binding protein (CBP). The mixed lineage leukemia protein (MLL) activation domain binds to an allosteric site on the Kix domain. J. Biol. Chem. 277, 43168-43174 (2002).
75. Vendel, A. C. & Lumb, K. J. NMR mapping of the HIV-1 Tat interaction surface of the KIX domain of the human coactivator CBP. Biochemistry 43, 904-908 (2004).
76. Campbell, K. M. & Lumb, K. J. Structurally distinct modes of recognition of the KIX domain of CBP by Jun and CREB. Biochemistry 41, 13956-13964 (2002).
77. Vendel, A. C., McBryant, S. J. & Lumb, K. J. KIX-mediated assembly of the CBP-CREB-HTLV-1 tax coactivator-activator complex. Biochemistry 42, 12481-12487 (2003).
78. Xu, W. et al. A transcriptional switch mediated by cofactor methylation. Science 294, 2507-2511 (2001).
79. Radhakrishnan, I. et al. Structural analyses of CREB-CBP transcriptional activator-coactivator complexes by NMR spectroscopy: implications for mapping the boundaries of structural domains. J. Mol. Biol. 287, 859-865 (1999).
80. Wei, Y., Horng, J. C., Vendel, A. C., Raleigh, D. P. & Lumb, K. J. Contribution to stability and folding of a buried polar residue at the CARM1 methylation site of the KIX domain of CBP. Biochemistry 42, 7044-7049 (2003).
81. Shapiro, L. β-catenin and its multiple partners: promiscuity explained. Nature Struct. Biol. 8, 484-487 (2001).
82. Daniels, D. L., Eklof, S. K. & Weis, W. I. β-catenin: molecular plasticity and drug design. Trends Biochem. Sci. 26, 672-678 (2001).
83. Huber, A. H., Stewart, D. B., Laurents, D. V., Nelson, W. J. & Weis, W. I. The cadherin cytoplasmic domain is unstructured in the absence of β-catenin. A possible-mechanism for regulating cadherin turnover. J. Biol. Chem. 276, 12301-12309 (2001).
84. Graham, T. A., Weaver, C., Mao, F., Kimelman, D. & Xu, W. Crystal structure of a β-catenin/Tcf complex. Cell 103, 885-896 (2000).
85. Graham, T. A., Ferkey, D. M., Mao, F., Kimelman, D. & Xu, W. Tcf4 can specifically recognize β-catenin using alternative conformations. Nature Struct. Biol. 8, 1048-1052 (2001).
86. Eklof Spink, K., Fridman, S. G. & Weis, W. I. Molecular mechanisms of β-catenin recognition by adenomatous polyposis coli revealed by the structure of an APC-β-catenin complex. EMBO J. 20, 6203-6212 (2001).
87. Graham, T. A., Clements, W. K., Kimelman, D. & Xu, W. The crystal structure of the β-catenin/ICAT complex reveals the inhibitory mechanism of ICAT. Mol. Cell 10, 563-571 (2002).
88. Daniels, D. L. & Weis, W. I. ICAT inhibits β-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol. Cell 10, 573-584 (2002).
89. Lin, C. H. et al. A small domain of cbp/p300 binds diverse proteins. Solution structure and functional studies. Mol. Cell 8, 581-590 (2001).
90. Demarest, S. J., Deechongkit, S., Dyson, H. J., Evans, R. M. & Wright, P. E. Packing, specificity, and mutability at the binding interface between the p160 coactivator and CREB-binding protein. Protein Sci. 13, 203-210 (2004).
91. Demarest, S. J. et al. Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415, 549-553 (2002). Presents the first example of two domains that are largely, if not completely, unfolded when free in solution, but that fold together when they interact to produce a complex of exceptionally high specificity and with a large surface area of binding.
92. Grossman, S. R. p300/CBP/p53 interaction and regulation of the p53 response. Eur. J. Biochem. 268, 2773-2778 (2001).
93. Bell, S., Klein, C., Muller, L., Hansen, S. & Buchner, J. p53 contains large unstructured regions in its native state. J. Mol. Biol. 322, 917-927 (2002).
94. Ayed, A. et al. Latent and active p53 are identical in conformation. Nature Struct. Biol. 8, 756-760 (2001). Provides important information on the N- and C-terminal domains of p53, which are unstructured in the context of the full-length protein, as well as isolated in solution.
95. Dawson, R. et al. The N-terminal domain of p53 is natively unfolded. J. Mol. Biol. 332, 1131-1141 (2003).
96. Prives, C. & Hall, P. A. The p53 pathway. J. Pathol. 187, 112-126 (1999).
97. Alarcon-Vargas, D. & Ronai, Z. p53-Mdm2 - the affair that never ends. Carcinogenesis 23, 541-547 (2002).
98. Mujtaba, S. et al. Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol. Cell 13, 251-263 (2004).
99. Kamei, Y. et al. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85, 403-414 (1996).
100. Heery, D. M., Kalkhoven, E., Hoare, S. & Parker, M. G. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387, 733-736 (1997).
101. Darimont, B. D. et al. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 12, 3343-3356 (1998).
102. WAF1/CIP1 induction of p300 transactivation. Mol. Cell. Biol. 20, 2676-2686 (2000).
103. Girdwood, D. et al. p300 transcriptional repression is mediated by SUMO modification. Mol. Cell, 1043-1054 (2003).
104. Thompson, P. R. et al. Regulation of the p300 HAT domain via a novel activation loop. Nature Struct. Mol. Biol. 11, 308-315 (2004).
105. Gerber, H. P. et al. Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 263, 808-811 (1994).
106. Shoemaker, B. A., Portman, J. J. & Wolynes, P. G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl Acad. Sci. USA 97, 8868-8873 (2000). Describes a possible rationale for the presence of unstructured linker regions in multidomain proteins: a conformational ensemble for part of an interaction domain ensures that the volume of the surrounding solution is sampled extensively, which increases the likelihood of encountering the binding partner.
107. Smith, J. L. et al. Kinetic profiles of p300 occupancy in vivo predict common features of promoter structure and coactivator recruitment. Proc. Natl Acad. Sci. USA 101, 11554-11559 (2004).
108. Spolar, R. S. & Record, M. T. Coupling of local folding to site-specific binding of proteins to DNA. Science 263, 777-784 (1994).
109. Patel, L., Abate, C. & Curran, T. Altered protein conformation on DNA binding by Fos and Jun. Nature 347, 572-574 (1990).
110. DiNitto, J. P. & Huber, P. W. Mutual induced fit binding of Xenopus ribosomal protein L5 to 5S rRNA. J. Mol. Biol. 330, 979-992 (2003).
111. Salghetti, S. E., Caudy, A. A., Chenoweth, J. G. & Tansey, W. P. Regulation of transcriptional activation domain function by ubiquitin. Science 293, 1651-1653 (2001).
112. Venkatraman, P., Wetzel, R., Tanaka, M., Nukina, N. & Goldberg, A. L. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol. Cell 14, 95-104 (2004).
113. Yang, X. J. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 32, 959-976 (2004).
114. McCampbell, A. & Fischbeck, K. H. Polyglutamine and CBP: fatal attraction? Nature Med. 7, 528-530 (2001).
115. Nucifora, F. C. et al. Interference by Huntingtin and atrophin-1 with CBP-mediated transcription leading to cellular toxicity. Science 291, 2423-2428 (2001).
116. Karlin, S., Brocchieri, L., Bergman, A., Mrazek, J. & Gentles, A. J. Amino acid runs in eukaryotic proteomes and disease associations. Proc. Natl Acad. Sci. USA 99, 333-338 (2002).
117. Rost, B. & Liu, J. The Predict Protein server. Nucleic Acids Res. 31, 3300-3304 (2003).
118. Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074-1080 (2001).
119. Berger, S. L. Histone modifications in transcriptional regulation. Cur. Opin. Genet. Dev. 12, 142-143 (2002).
120. Hartman, P. G., Chapman, G. E., Moss, T. & Bradbury, E. M. Studies on the role and mode of operation of the very-lysine-rich histone H1 in eukaryote chromatin. The three structural regions of the histone H1 molecule. Eur. J. Biochem. 77, 45-51 (1977).
121. Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (1997).
122. Brüschweiler, R., Liao, X. & Wright, P. E. Long-range motional restrictions in a multidomain zinc-finger protein from anisotropic tumbling. Science 268, 886-889 (1995).
123. Gross, J. D. et al. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 115, 739-750 (2003).
124. Wuttke, D. S., Foster, M. P., Case, D. A., Gottesfeld, J. M. & Wright, P. E. Solution structure of the first three zinc fingers of TFIIIA bound to the cognate DNA sequence: determinants of affinity and sequence specificity. J. Mol. Biol. 273, 183-206 (1997).
125. Koradi, R., Billeter, M. Wüthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55 (1996).
126. Lee, C., Kim, S. J., Jeong, D. G., Lee, S. M. & Ryu, S. E. Structure of human FIH-1 reveals a unique active site pocket and interaction sites for HIF-1 and von Hippel-Lindau. J. Biol. Chem. 278, 7558-7563 (2003).