HMGB1-facilitated p53 DNA binding occurs via HMG-Box/p53 transactivation domain interaction, regulated by the acidic tail

Structure

Volumn 20, Issue 12, 2012, Pages 2014-2024

  Rowell, John P ^a   Simpson, Kathryn L ^a   Stott, Katherine ^a   Watson, Matthew ^a   Thomas, Jean O ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; PROTEIN P53; SINGLE STRANDED DNA;

ARTICLE; BINDING SITE; HIGH MOBILITY GROUP BOX DOMAIN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN CROSS LINKING; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

CHROMATOGRAPHY, GEL; CROSS-LINKING REAGENTS; DIMETHYL SUBERIMIDATE; HMG-BOX DOMAINS; HMGB1 PROTEIN; HUMANS; MODELS, MOLECULAR; MOLECULAR MIMICRY; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84870565733     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.09.004     Document Type: Article

References (77)

1. A. Agresti, and M.E. Bianchi HMGB proteins and gene expression Curr. Opin. Genet. Dev. 13 2003 170 178
2. S. Aizawa, H. Nishino, K. Saito, K. Kimura, H. Shirakawa, and M. Yoshida Stimulation of transcription in cultured cells by high mobility group protein 1: essential role of the acidic carboxyl-terminal region Biochemistry 33 1994 14690 14695
3. S. Banerjee, and T.K. Kundu The acidic C-terminal domain and A-box of HMGB-1 regulates p53-mediated transcription Nucleic Acids Res. 31 2003 3236 3247
4. E. Bochkareva, L. Kaustov, A. Ayed, G.-S. Yi, Y. Lu, A. Pineda-Lucena, J.C.C. Liao, A.L. Okorokov, J. Milner, C.H. Arrowsmith, and A. Bochkarev Single-stranded DNA mimicry in the p53 transactivation domain interaction with replication protein A Proc. Natl. Acad. Sci. USA 102 2005 15412 15417
5. V. Boonyaratanakornkit, V. Melvin, P. Prendergast, M. Altmann, L. Ronfani, M.E. Bianchi, L. Taraseviciene, S.K. Nordeen, E.A. Allegretto, and D.P. Edwards High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells Mol. Cell. Biol. 18 1998 4471 4487
6. J.M. Brickman, M. Adam, and M. Ptashne Interactions between an HMG-1 protein and members of the Rel family Proc. Natl. Acad. Sci. USA 96 1999 10679 10683
7. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.-S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
8. M. Bustin, and R. Reeves High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function Prog. Nucleic Acid Res. Mol. Biol. 54 1996 35 100
9. F. Catez, H. Yang, K.J. Tracey, R. Reeves, T. Misteli, and M. Bustin Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin Mol. Cell. Biol. 24 2004 4321 4328
10. L. Cato, K. Stott, M. Watson, and J.O. Thomas The interaction of HMGB1 and linker histones occurs through their acidic and basic tails J. Mol. Biol. 384 2008 1262 1272
11. J. Cavanagh, W.J. Fairbrother, A.G. Palmer, and N.J. Skelton Protein NMR Spectroscopy: Principles and Practice 1996 Academic Press San Diego, CA, USA
12. M.S. Cheung, M.L. Maguire, T.J. Stevens, and R.W. Broadhurst DANGLE: A Bayesian inferential method for predicting protein backbone dihedral angles and secondary structure J. Magn. Reson. 202 2010 223 233
13. R. Dawson, L. Müller, A. Dehner, C. Klein, H. Kessler, and J. Buchner The N-terminal domain of p53 is natively unfolded J. Mol. Biol. 332 2003 1131 1141
14. M. Decoville, M.J. Giraud-Panis, C. Mosrin-Huaman, M. Leng, and D. Locker HMG boxes of DSP1 protein interact with the rel homology domain of transcription factors Nucleic Acids Res. 28 2000 454 462
15. P. Di Lello, L.M. Jenkins, T.N. Jones, B.D. Nguyen, T. Hara, H. Yamaguchi, J.D. Dikeakos, E. Appella, P. Legault, and J.G. Omichinski Structure of the Tfb1/p53 complex: Insights into the interaction between the p62/Tfb1 subunit of TFIIH and the activation domain of p53 Mol. Cell 22 2006 731 740
16. A. Dintilhac, and J. Bernués HMGB1 interacts with many apparently unrelated proteins by recognizing short amino acid sequences J. Biol. Chem. 277 2002 7021 7028
17. W.S. el-Deiry, S.E. Kern, J.A. Pietenpol, K.W. Kinzler, and B. Vogelstein Definition of a consensus binding site for p53 Nat. Genet. 1 1992 45 49
18. J.C. Ferreon, C.W. Lee, M. Arai, M.A. Martinez-Yamout, H.J. Dyson, and P.E. Wright Cooperative regulation of p53 by modulation of ternary complex formation with CBP/p300 and HDM2 Proc. Natl. Acad. Sci. USA 106 2009 6591 6596
19. K.D. Grasser, S.H. Teo, K.B. Lee, R.W. Broadhurst, C. Rees, C.H. Hardman, and J.O. Thomas DNA-binding properties of the tandem HMG boxes of high-mobility-group protein 1 (HMG1) Eur. J. Biochem. 253 1998 787 795
20. C.H. Hardman, R.W.B. Broadhurst, A.R.C. Raine, K.D. Grasser, J.O. Thomas, and E.D. Laue Structure of the A-domain of HMG1 and its interaction with DNA as studied by heteronuclear three- and four-dimensional NMR spectroscopy Biochemistry 34 1995 16596 16607
21. T. Imamura, H. Izumi, G. Nagatani, T. Ise, M. Nomoto, Y. Iwamoto, and K. Kohno Interaction with p53 enhances binding of cisplatin-modified DNA by high mobility group 1 protein J. Biol. Chem. 276 2001 7534 7540
22. P.J. Isackson, J.L. Fishback, D.L. Bidney, and G.R. Reeck Preferential affinity of high molecular weight high mobility group non-histone chromatin proteins for single-stranded DNA J. Biol. Chem. 254 1979 5569 5572
23. L. Jayaraman, N.C. Moorthy, K.G. Murthy, J.L. Manley, M. Bustin, and C. Prives High mobility group protein-1 (HMG-1) is a unique activator of p53 Genes Dev. 12 1998 462 472
24. A.C. Joerger, and A.R. Fersht Structural biology of the tumor suppressor p53 Annu. Rev. Biochem. 77 2008 557 582
25. Y. Jung, and S.J. Lippard Nature of full-length HMGB1 binding to cisplatin-modified DNA Biochemistry 42 2003 2664 2671
26. M. Kitayner, H. Rozenberg, N. Kessler, D. Rabinovich, L. Shaulov, T.E. Haran, and Z. Shakked Structural basis of DNA recognition by p53 tetramers Mol. Cell 22 2006 741 753
27. J.D. Klemm, M.A. Rould, R. Aurora, W. Herr, and C.O. Pabo Crystal structure of the Oct-1 POU domain bound to an octamer site: DNA recognition with tethered DNA-binding modules Cell 77 1994 21 32
28. S. Knapp, S. Müller, G. Digilio, T. Bonaldi, M.E. Bianchi, and G. Musco The long acidic tail of high mobility group box 1 (HMGB1) protein forms an extended and flexible structure that interacts with specific residues within and between the HMG boxes Biochemistry 43 2004 11992 11997
29. R. Koradi, M. Billeter, and K. Wüthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55 29-32
30. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24 1991 946 950
31. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
32. H. Lee, K.H. Mok, R. Muhandiram, K.-H. Park, J.-E. Suk, D.-H. Kim, J. Chang, Y.C. Sung, K.Y. Choi, and K.-H. Han Local structural elements in the mostly unstructured transcriptional activation domain of human p53 J. Biol. Chem. 275 2000 29426 29432
33. K.-B. Lee, and J.O. Thomas The effect of the acidic tail on the DNA-binding properties of the HMG1,2 class of proteins: insights from tail switching and tail removal J. Mol. Biol. 304 2000 135 149
34. N. Lehming, A. Le Saux, J. Schüller, and M. Ptashne Chromatin components as part of a putative transcriptional repressing complex Proc. Natl. Acad. Sci. USA 95 1998 7322 7326
35. H.-H. Li, A.G. Li, H.M. Sheppard, and X. Liu Phosphorylation on Thr-55 by TAF1 mediates degradation of p53: a role for TAF1 in cell G1 progression Mol. Cell 13 2004 867 878
36. J.P. Linge, M. Habeck, W. Rieping, and M. Nilges ARIA: automated NOE assignment and NMR structure calculation Bioinformatics 19 2003 315 316
37. K.M. Livesey, R. Kang, P. Vernon, W. Buchser, P. Loughran, S.C. Watkins, L. Zhang, J.J. Manfredi, H.J. Zeh 3rd, and L. Li p53/HMGB1 complexes regulate autophagy and apoptosis Cancer Res. 72 2012 1996 2005
38. K. McKinney, and C. Prives Efficient specific DNA binding by p53 requires both its central and C-terminal domains as revealed by studies with high-mobility group 1 protein Mol. Cell. Biol. 22 2002 6797 6808
39. V.S. Melvin, C. Harrell, J.S. Adelman, W.L. Kraus, M. Churchill, and D.P. Edwards The role of the C-terminal extension (CTE) of the estrogen receptor alpha and beta DNA binding domain in DNA binding and interaction with HMGB J. Biol. Chem. 279 2004 14763 14771
40. E.A. Merritt, and D.J. Bacon Raster3D: photorealistic molecular graphics Methods Enzymol. 277 1997 505 524
41. 15N NMR assignments and global folding pattern Biochemistry 32 1993 13818 13829
42. A.K. Nagaich, E. Appella, and R.E. Harrington DNA bending is essential for the site-specific recognition of DNA response elements by the DNA binding domain of the tumor suppressor protein p53 J. Biol. Chem. 272 1997 14842 14849
43. Y. Najima, N. Yahagi, Y. Takeuchi, T. Matsuzaka, M. Sekiya, Y. Nakagawa, M. Amemiya-Kudo, H. Okazaki, S. Okazaki, and Y. Tamura High mobility group protein-B1 interacts with sterol regulatory element-binding proteins to enhance their DNA binding J. Biol. Chem. 280 2005 27523 27532
44. K. Oda, H. Arakawa, T. Tanaka, K. Matsuda, C. Tanikawa, T. Mori, H. Nishimori, K. Tamai, T. Tokino, Y. Nakamura, and Y. Taya p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53 Cell 102 2000 849 862
45. U.M. Ohndorf, M.A. Rould, Q. He, C.O. Pabo, and S.J. Lippard Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins Nature 399 1999 708 712
46. T.T. Paull, M.J. Haykinson, and R.C. Johnson The nonspecific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures Genes Dev. 7 1993 1521 1534
47. D. Payet, and A. Travers The acidic tail of the high mobility group protein HMG-D modulates the structural selectivity of DNA binding J. Mol. Biol. 266 1997 66 75
48. S. Rajagopalan, A. Andreeva, D.P. Teufel, S.M. Freund, and A.R. Fersht Interaction between the transactivation domain of p53 and PC4 exemplifies acidic activation domains as single-stranded DNA mimics J. Biol. Chem. 284 2009 21728 21737
49. S. Schwarzinger, G.J. Kroon, T.R. Foss, J. Chung, P.E. Wright, and H.J. Dyson Sequence-dependent correction of random coil NMR chemical shifts J. Am. Chem. Soc. 123 2001 2970 2978
50. L.G. Sheflin, N.W. Fucile, and S.W. Spaulding The specific interactions of HMG 1 and 2 with negatively supercoiled DNA are modulated by their acidic C-terminal domains and involve cysteine residues in their HMG 1/2 boxes Biochemistry 32 1993 3238 3248
51. K. Stott, G.S. Tang, K.B. Lee, and J.O. Thomas Structure of a complex of tandem HMG boxes and DNA J. Mol. Biol. 360 2006 90 104
52. K. Stott, M. Watson, F.S. Howe, J.G. Grossmann, and J.O. Thomas Tail-mediated collapse of HMGB1 is dynamic and occurs via differential binding of the acidic tail to the A and B domains J. Mol. Biol. 403 2010 706 722
53. M. Štros HMGB proteins: interactions with DNA and chromatin Biochim. Biophys. Acta 1799 2010 101 113
54. M. Štros, J. Stokrová, and J.O. Thomas DNA looping by the HMG-box domains of HMG1 and modulation of DNA binding by the acidic C-terminal domain Nucleic Acids Res. 22 1994 1044 1051
55. M. Štros, E. Muselíková-Polanská, Š. Pospísilová, and F. Strauss High-affinity binding of tumor-suppressor protein p53 and HMGB1 to hemicatenated DNA loops Biochemistry 43 2004 7215 7225
56. S.H. Teo, K.D. Grasser, and J.O. Thomas Differences in the DNA-binding properties of the HMG-box domains of HMG1 and the sex-determining factor SRY Eur. J. Biochem. 230 1995 943 950
57. D.P. Teufel, S.M. Freund, M. Bycroft, and A.R. Fersht Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53 Proc. Natl. Acad. Sci. USA 104 2007 7009 7014
58. J.O. Thomas, and R.D. Kornberg An octamer of histones in chromatin and free in solution Proc. Natl. Acad. Sci. USA 72 1975 2626 2630
59. J.O. Thomas, and A.A. Travers HMG1 and 2, and related 'architectural' DNA-binding proteins Trends Biochem. Sci. 26 2001 167 174
60. J.O. Thomas, and K. Stott H1 and HMGB1: modulators of chromatin structure Biochem. Soc. Trans. 40 2012 341 346
61. A.A. Travers, and J.O. Thomas Chromosomal HMG-box proteins J. Zlatanova, S.H. Leuba, Chromatin Structure and Dynamics: State-of-the-Art 2004 Elsevier Amsterdam 103 134
62. T. Ueda, H. Chou, T. Kawase, H. Shirakawa, and M. Yoshida Acidic C-tail of HMGB1 is required for its target binding to nucleosome linker DNA and transcription stimulation Biochemistry 43 2004 9901 9908
63. J. van Dieck, D.P. Teufel, A.M. Jaulent, M.R. Fernandez-Fernandez, T.J. Rutherford, A. Wyslouch-Cieszynska, and A.R. Fersht Posttranslational modifications affect the interaction of S100 proteins with tumor suppressor p53 J. Mol. Biol. 394 2009 922 930
64. C.P. Verrijzer, J.A. van Oosterhout, W.W. van Weperen, and P.C. van der Vliet POU proteins bend DNA via the POU-specific domain EMBO J. 10 1991 3007 3014
65. P.D. Vise, B. Baral, A.J. Latos, and G.W. Daughdrill NMR chemical shift and relaxation measurements provide evidence for the coupled folding and binding of the p53 transactivation domain Nucleic Acids Res. 33 2005 2061 2077
66. W.F. Vranken, W. Boucher, T.J. Stevens, R.H. Fogh, A. Pajon, M. Llinas, E.L. Ulrich, J.L. Markley, J. Ionides, and E.D. Laue The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59 2005 687 696
67. M. Watson, K. Stott, and J.O. Thomas Mapping intramolecular interactions between domains in HMGB1 using a tail-truncation approach J. Mol. Biol. 374 2007 1286 1297
68. M. Webb, and J.O. Thomas Structure-specific binding of the two tandem HMG boxes of HMG1 to four-way junction DNA is mediated by the A domain J. Mol. Biol. 294 1999 373 387
69. H.M. Weir, P.J. Kraulis, C.S. Hill, A.R.C. Raine, E.D. Laue, and J.O. Thomas Structure of the HMG box motif in the B-domain of HMG1 EMBO J. 12 1993 1311 1319
70. M. Wells, H. Tidow, T.J. Rutherford, P. Markwick, M.R. Jensen, E. Mylonas, D.I. Svergun, M. Blackledge, and A.R. Fersht Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain Proc. Natl. Acad. Sci. USA 105 2008 5762 5767
71. T.S. Wong, S. Rajagopalan, S.M. Freund, T.J. Rutherford, A. Andreeva, F.M. Townsley, M. Petrovich, and A.R. Fersht Biophysical characterizations of human mitochondrial transcription factor A and its binding to tumor suppressor p53 Nucleic Acids Res. 37 2009 6765 6783
72. T.S. Wong, S. Rajagopalan, F.M. Townsley, S.M. Freund, M. Petrovich, D. Loakes, and A.R. Fersht Physical and functional interactions between human mitochondrial single-stranded DNA-binding protein and tumour suppressor p53 Nucleic Acids Res. 37 2009 568 581
73. Y. Xu Regulation of p53 responses by post-translational modifications Cell Death Differ. 10 2003 400 403
74. V. Zappavigna, L. Falciola, M. Helmer-Citterich, F. Mavilio, and M.E. Bianchi HMG1 interacts with HOX proteins and enhances their DNA binding and transcriptional activation EMBO J. 15 1996 4981 4991
75. E.R. Zuiderweg Mapping protein-protein interactions in solution by NMR spectroscopy Biochemistry 41 2002 1 7
76. C. Zwahlen, P. Legault, S.J.F. Vincent, J. Greenblatt, R. Konrat, and L.E. Kay Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage λ N-peptide/boxB RNA complex J. Am. Chem. Soc. 119 1997 6711 6721
77. S. Zwilling, H. König, and T. Wirth High mobility group protein 2 functionally interacts with the POU domains of octamer transcription factors EMBO J. 14 1995 1198 1208