Intrinsic disorder explains diverse nuclear roles of chromatin remodeling proteins

Journal of Molecular Recognition

Volumn 22, Issue 1, 2009, Pages 1-8

  Sandhu, Kuljeet Singh ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Chromatin remodeling; Histone modification; Structural disorder

Indexed keywords

HISTONE; PROTEIN;

ALGORITHM; ARTICLE; CELL NUCLEUS; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; METABOLISM; PROTEIN CONFORMATION; PROTEIN DATABASE; PROTEIN FOLDING;

ALGORITHMS; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DATABASES, PROTEIN; HISTONES; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEINS;

EID: 59649087503     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.915     Document Type: Article

References (86)

1. Gangaraju VK, Bartholomew B. 2007. Mechanisms of ATP dependent chromatin remodeling. Mutat. Res. 618: 3-17.
2. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
3. van Vugt JJ, Ranes M, Campsteijn C, Logie C. 2007. The ins and outs of ATP-dependent chromatin remodeling in budding yeast: biophysical and proteomic perspectives. Biochim. Biophys. Acta. 1769: 153-171.
4. Bouazoune K, Brehm A. 2006. ATP-dependent chromatin remodeling complexes in Drosophila. Chromosome Res. 14: 433-449.
5. Mohrmann L, Verrijzer CP. 2005. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta. 1681: 59-73.
6. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. 2007. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14: 1025-1040.
7. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128(4): 693-705.
8. Neely KE, Hassan AH, Brown CE, Howe L, Workman JL. 2002. Transcription activator interactions with multiple SWI/SNF subunits. Mol. Cell Biol. 22: 1615-1625.
9. Cavellan E, Asp P, Percipalle P, Farrants AK. 2006. The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J. Biol. Chem. 281: 16264-16271.
10. Huang J, Laurent BC. 2004. A Role for the RSC chromatin remodeler in regulating cohesion of sister chromatid arms. Cell Cycle 3: 973-975.
11. Huang J, Hsu JM, Laurent BC. 2004. The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms. Mol. Cell 13: 739-750.
12. Hsu JM, Huang J, Meluh PB, Laurent BC. 2003. The yeast RSC chromatin-remodeling complex is required for kinetochore function in chromosome segregation. Mol. Cell Biol. 23: 3202-3215.
13. Sillibourne JE, Delaval B, Redick S, Sinah M, Doxsey SJ. 2007. Chromatin remodeling proteins interact with pericentrin to regulate centrosome integrity. Mol. Biol. Cell. 18: 3667-3680.
14. Ogiwara H, Enomoto T, Seki M. 2007. The INO80 chromatin remodeling complex functions in sister chromatid cohesion. Cell Cycle 6: 1090-1095.
15. Tomizawa Y, Ui A, Onoda F, Ogiwara H, Tada S, Enomoto T, Seki M. 2007. Rad50 is involved in MMS-induced recombination between homologous chromosomes in mitotic cells. Genes Genet. Syst. 82: 157-160.
16. Yu EY, Steinberg-Neifach O, Dandjinou AT, Kang F, Morrison AJ, Shen X, Lue NF. 2007. Regulation of telomere structure and functions by subunits of the INO80 chromatin remodeling complex. Mol. Cell Biol. 27: 5639-5649.
17. Pandita TK, Hunt CR, Sharma GG, Yang Q. 2007. Regulation of telomere movement by telomere chromatin structure. Cell Mol. Life Sci. 64: 131-138.
18. Bell SP, Stillman B. 1992. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357: 128-134.
19. Collins N, Poot RA, Kukimoto I, Garcia-Jimenez C, Dellaire G, Varga-Weisz PD. 2002. An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat. Genet. 32: 627-632.
20. Ehrenhofer-Murray AE. 2004. Chromatin dynamics at DNA replication, transcription and repair. Eur. J. Biochem. 271: 2335-2349.
21. Falbo KB, Shen X. 2006. Chromatin remodeling in DNA replication. J. Cell Biochem. 97: 684-689.
22. Morrison AJ, Shen X. 2006. Chromatin modifications in DNA repair. Results Probl. Cell Differ. 41: 109-125.
23. Gaillard H, Fitzgerald DJ, Smith CL, Peterson CL, Richmond TJ, Thoma F. 2003. Chromatin remodeling activities act on UV-damaged nucleosomes and modulate DNA damage accessibility to photolyase. J. Biol. Chem. 278: 17655-17663.
24. Chai B, Huang J, Cairns BR, Laurent BC. 2005. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19: 1656-1661.
25. Yu Y, Waters R. 2005. Histone acetylation, chromatin remodelling and nucleotide excision repair: hint from the study on MFA2 in Saccharomyces cerevisiae. Cell Cycle 4: 1043-1045.
26. Gong F, Kwon Y, Smerdon MJ. 2005. Nucleotide excision repair in chromatin and the right of entry. DNA Repair (Amst.) 4: 884-896.
27. Gong F, Fahy D, Smerdon MJ. 2006. Rad4-Rad23 interaction with SWI/SNF links ATP-dependent chromatin remodeling with nucleotide excision repair. Nat. Struct. Mol. Biol. 13: 902-907.
28. Banine F, Bartlett C, Gunawardena R, Muchardt C, Yaniv M, Knudsen ES, Weissman BE, Sherman LS. 2005. SWI/SNF chromatin-remodeling factors induce changes in DNA methylation to promote transcriptional activation. Cancer Res. 65: 3542-3547.
29. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJ. 2004. Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14: 801-805.
30. Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke AJ. 2005. A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO. Rep. 6: 649-655.
31. Zhu H, Geiman TM, Xi S, Jiang Q, Schmidtmann A, Chen T, Li E, Muegge K. 2006. Lsh is involved in de novo methylation of DNA. EMBO. J. 25: 335-345.
32. Cairns BR. 2005. Chromatin remodeling complexes: strength in diversity, precision through specialization. Curr. Opin. Genet. Dev. 15: 185-190.
33. Liu J, Perumal NB, Oldfield CJ, Su EW, Uversky VN, Dunker AK. 2006. Intrinsic disorder in transcription factors. Biochemistry 45: 6873-6888.
34. Hansen JC, Lu X, Ross ED, Woody RW. 2006. Intrinsic protein disorder, amino acid composition, and histone terminal domains. J. Biol. Chem. 281: 1853-1856.
35. Uversky VN. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11: 739-756.
36. Uversky VN. 2002. What does it mean to be natively unfolded? Eur. J. Biochem. 269: 2-12.
37. Dyson HJ, Wright PE. 2005. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6: 197-208.
38. 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.
39. 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.
40. Singh GP, Dash D. 2007. Intrinsic disorder in yeast transcriptional regulatory network. Proteins 68: 602-605.
41. Singh GP, Ganapathi M, Dash D. 2007. Role of intrinsic disorder in transient interactions of hub proteins. Proteins 66: 761-765.
42. Kan PY, Lu X, Hansen JC, Hayes JJ. 2007. The H3 tail domain participates in multiple interactions during folding and self-association of nucleosome arrays. Mol. Cell. Biol. 27: 2084-2091.
43. Ward JJ, McGuffin LJ, Bryson K, Buxton BF, Jones DT. 2004. The DISOPRED server for the prediction of protein disorder. Bioinformatics 20: 2138-2139.
44. Dosztanyi Z, Csizmok V, Tompa P, Simon I. 2005. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433-3434.
45. Linding R, Russell RB, Neduva V, Gibson TJ. 2003. GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31: 3701-3708.
46. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman I, Sussman JL. 2005. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21: 3435-3438.
47. Shimizu K, Hirose S, Noguchi T. 2007. POODLE-S: Web application for predicting protein disorder by using physicochemical features and reduced amino acid set of a position specific scoring matrix. Bioinformatics. 23: 2337-2338.
48. Su CT, Chen CY, Hsu CM. 2007. iPDA: integrated protein disorder analyzer. Nucleic Acids Res. 35: W465-W472.
49. Hovmoller S, Zhou T. 2004. Why are both ends of the polypeptide chain on the outside of proteins? Proteins 55: 219-222.
50. Levy Y, Onuchic JN, Wolynes PG. 2007. Fly-casting in protein-DNA binding: frustration between protein folding and electrostatics facilitates target recognition. J. Am. Chem. Soc. 129: 738-739.
51. Shoemaker BA, Portman JJ, Wolynes PG. 2000. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. U S A 97: 8868-8873.
52. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK. 2001. Sequence complexity of disordered protein. Proteins 42: 38-48.
53. Tompa P. 2003. Intrinsically unstructured proteins evolve by repeat expansion. Bioessays 25: 847-855.
54. 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.
55. Durr H, Hopfner KP. 2006. Structure-function analysis of SWI2/SNF2 enzymes. Methods Enzymol. 409: 375-388.
56. Adams VH, McBryant SJ, Wade PA, Woodcock CL, Hansen JC. 2007. Intrinsic disorder and autonomous domain function in the multifunctional nuclear protein, MeCP2. J. Biol. Chem. 282(20): 15057-15064. Epub 12007 Mar 15019.
57. Szollosi E, Bokor M, Bodor A, Perczel A, Klement E, Medzihradszky KF, Tompa K, Tompa P. 2008. Intrinsic structural disorder of DF31, a drosophila protein of chromatin decondensation and remodeling activities. J. Proteome Res. 7(6): 2291-22299. Epub 2008 May 2217.
58. Tompa P, Csermely P. 2004. The role of structural disorder in the function of RNA and protein chaperones. Faseb. J. 18(11): 1169-1175.
59. Sanchez-Puig N, Veprintsev DB, Fersht AR. 2005. Human full-length Securin is a natively unfolded protein. Protein Sci. 14(6): 1410-1418.
60. Marmorstein R. 2004. Structure and chemistry of the Sir2 family of NAD+-dependent histone/protein deactylases. Biochem Soc. Trans. 32(Pt 6): 904-909.
61. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. 2007. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449(7159): 248-251. Epub 2007 Aug 2022.
62. Banerjee A, Santos WL, Verdine GL. 2006. Structure of a DNA glycosylase searching for lesions. Science 311(5764): 1153-1157.
63. Ariza A, Richard DJ, White MF, Bond CS. 2005. Conformational flexibility revealed by the crystal structure of a crenarchaeal RadA. Nucleic Acids Res. 33: 1465-1473.
64. Leschziner AE, Saha A, Wittmeyer J, Zhang Y, Bustamante C, Cairns BR, Nogales E. 2007. Conformational flexibility in the chromatin remodeler RSC observed by electron microscopy and the orthogonal tilt reconstruction method. Proc. Natl. Acad. Sci. U S A 104: 4913-4918.
65. Skiniotis G, Moazed D, Walz T. 2007. Acetylated histone tail peptides induce structural rearrangements in the rsc chromatin remodeling complex. J. Biol. Chem. 282: 20804-20808.
66. Li B, Gogol M, Carey M, Lee D, Seidel C, Workman JL. 2007. Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316: 1050-1054.
67. Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F, Khorasanizadeh S. 2005. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181-1185.
68. Hilser VJ, Thompson EB. 2007. Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc. Natl. Acad. Sci. U S A 104: 8311-8315.
69. Dunn KL, Davie JR. 2003. The many roles of the transcriptional regulator CTCF. Biochem. Cell Biol. 81(3): 161-167.
70. Williams A, Flavell RA. 2008. The role of CTCF in regulating nuclear organization. J. Exp. Med. 205(4): 747-750. Epub 2008 Mar 2017.
71. Filippova GN, Fagerlie S, Klenova EM, Myers C, Dehner Y, Goodwin G, Neiman PE, Collins SJ, Lobanenkov VV. 1996. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell Biol. 16(6): 2802-2813.
72. Traut W, Endl E, Garagna S, Scholzen T, Schwinger E, Gerdes J, Winking H. 2002. Chromatin preferences of the perichromosomal layer constituent pKi-67. Chromosome Res. 10(8): 685-694.
73. Scholzen T, Endl E, Wohlenberg C, van der Sar S, Cowell IG, Gerdes J, Singh PB. 2002. The Ki-67 protein interacts with members of the heterochromatin protein 1 (HP1) family: a potential role in the regulation of higher-order chromatin structure. J. Pathol. 196(2): 135-144.
74. Foster KSJ, McCrary WJ, Ross JS, Wright CF, 2006. Members of the hSWI/SNF chromatin remodeling complex associate with and are phosphorylated by protein kinase B/Akt. Oncogene 25: 4605-4612.
75. 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.
76. Hansen JC, Lu X, Ross ED, Woody RW. 2006. Intrinsic protein disorder, amino acid composition, and histone terminal domains. J. Biol. Chem. 281: 1853-1856.
77. Khorasanizadeh S. 2004. The nucleosome: from genomic organization to genomic regulation. Cell 116: 259-272.
78. Sandhu KS, Dash D. 2006. Conformational flexibility may explain multiple cellular roles of PEST motifs. Proteins 63(4): 727-732.
79. El-Kady A, Klenova E. 2005. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS. Lett. 579(6): 1424-1434.
80. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, Docquier F, Farrar D, Tavoosidana G, Mukhopadhyay R, Kanduri C, Oshimura M, Feinberg AP, Lobanenkov V, Klenova E, Ohlsson R. 2004. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 36(10): 1105-1110. Epub 2004 Sep 1107.
81. Radivojac P, Obradovic Z, Smith DK, Zhu G, Vucetic S, Brown CJ, Lawson JD, Dunker AK. 2004. Protein flexibility and intrinsic disorder. Protein Sci. 13(1): 71-80.
82. Sugase K, Dyson HJ, Wright PE. 2007. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447: 1021-1025.
83. Sandhu KS, Dash D. 2007. Dynamic alpha-helices: conformations that do not conform. Proteins 68: 109-122.
84. Gunasekaran K, Tsai CJ, Nussinov R. 2004. Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers. J. Mol. Biol. 341(5): 1327-1341.
85. 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(5): 1043-1059. Epub 2006 Au 1044.
86. 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 14-3-3with their partners. BMC Genomics 9 (Suppl 1): S1.