A critical role in structure-specific DNA binding for the acetylatable lysine residues in HMGB1

Biochemical Journal

Volumn 411, Issue 3, 2008, Pages 553-561

  Assenberg, René ^a,b   Webb, Michelle ^a,c   Connolly, Edward ^a,d   Stott, Katherine ^a   Watson, Matthew ^a   Hobbs, Josie ^a,e   Thomas, Jean O ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d Forensic Science Laboratory Dulin Ireland   (Ireland)

^e Binding Site Group Ltd   (United Kingdom)

Author keywords

Acetylation; High mobility group (HMG) box; NMR spectroscopy; Non histone protein; Site directed mutagenesis

Indexed keywords

ACETYLATION; BINDING ENERGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SUBSTITUTION REACTIONS;

HIGH MOBILITY GROUP (HMG) BOX; NON-HISTONE PROTEIN; SITE-DIRECTED MUTAGENESIS;

DNA;

HIGH MOBILITY GROUP B1 PROTEIN; LYSINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DNA;

ACETYLATION; ARTICLE; DNA BINDING; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; STATISTICAL SIGNIFICANCE; WILD TYPE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; CONFORMATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE;

ACETYLATION; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; CREB-BINDING PROTEIN; DNA; HMGB1 PROTEIN; LYSINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 42449148710     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071613     Document Type: Article

References (38)

1. Kouzarides, T. (2000) Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 19, 1176-1179
2. Glozak, M. A., Sengupta, N., Zhang, X and Seto, E. (2005) Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23
3. Imhof, A., Yang, X. J., Ogryzko, W., Nakatani, Y., Wolffe, A. P. and Ge, H. (1997) Acetylation of general transcription factors by histone acetyltransferases. Curr. Biol. 7, 689-692
4. Sterner, R., Vidali, G. and Allfrey, V. G. (1979) Studies of acetylation and deacetylation in high mobility group proteins: identification of the sites of acetylation in HMG-1. J. Biol. Chem. 254, 11577-11583
5. Bustin, M. (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19, 5237-5246
6. Agresti, A. and Bianchi, M. (2003) HMG proteins and gene expression. Curr. Op. Gen. Dev. 13, 170-178
7. Thomas, J. O. and Travers, A. A. (2001) HMGB1 and 2 and related "architectural" DNA-binding proteins. Trends Biochem. Sci. 26, 167-174
8. Travers, A. A. and Thomas, J. O. (2004) Chromatin structure and dynamics: state-of-the-art. In New Comprehensive Biochemistry (Zlatanova, J. and Leuba, S.H., eds), pp. 103-134, Elsevier Science, Amsterdam
9. Pauli, T. T., Haykinson, M. J. and Johnson, R. C. (1993) The non-specific DNA-binding and -bending proteins HMG1 and HMG2 promote the assembly of complex nucieoprotein structures. Genes Dev. 7, 1521-1534
10. Teo, S. H., Grasser, K. D. and Thomas, J. O. (1995) Differences in the DNA-binding properties of the HMG-box domains of HMGB1 and the sex-determining factor SRY. Eur. J. Biochem. 230, 943-950
11. Webb, M. and Thomas, J. O. (1999) Structure-specific-binding of the HMGB1 di-domain to four-way junction DNA is mediated by the A domain. J. Mol. Biol. 294, 373-387
12. Hardman, C. H., Broadhurst, R. W., Raine, A. R. C., Grasser, K. D., Thomas, J. O. and Laue, E. D. (1995) Structure of the A domain of HMGB1 and its interaction with DNA as studied by heteronuclear three- and four-dimensional NMR spectroscopy. Biochemistry 34, 16596-16607
13. Love, J. J., Li, X. A., Case, D. A., Giese, K., Grosschedl, R. and Wright, P. E. (1995) Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 376, 791-795
14. Masse, J. E., Wong, B., Yen, Y.-M., Allain, F. H.-T., Johnson, R. C. and Feigon, J. (2002) The S. cerevisiae architectural HMGB protein NHP6A complexed with DNA: DNA and protein conformational changes upon binding. J. Mol. Biol. 323, 263-284
15. Murphy, IV, F. V., Sweet, R. M. and Churchill, M. E. (1999) The structure of a chromosomal high mobility group protein-DNA complex reveals sequence-neutral mechanisms important for non-sequence-specific DNA recognition. EMBO J. 18, 6610-6618
16. Murphy, E. C., Zhurkin, V. B., Louis, J. M., Cornilescu, G. and Clore, G. M. (2001) Structural basis for SRY-dependent 46-X,Y sex reversal: modulation of DNA bending by a naturally occurring point mutation. J. Mol. Biol. 312, 481-499
17. Stott, K., Tang, G., Lee, K.-B. and Thomas, J. O. (2006) Structure of a complex of tandem HMG boxes bound to DNA. J. Mol. Biol. 360, 92-106
18. Ohndorf, U.-M., Rould, M. A., He, Q., Pabo, C. O. and Lippard, S. J. (1999) Basis of cisplatin-modified DNA binding by high-mobility group proteins. Nature 399, 708-712
19. 15N NMR spectroscopy. Biochemistry 34, 16608-16617
20. Kraulis, P. J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950
21. Grasser, K. D., Teo, S.-H., Lee, K. B., Broadhurst, R. W., Rees, C., Hardman, C. H. and Thomas, J. O. (1998) DNA-binding properties of the tandem HMG boxes of high-mobility-group protein 1 (HMGB1). Eur. J. Biochem. 253, 787-795
22. Lee, K. B. and Thomas, J. O. (2000) The effect of the acidic tail on the DNA-binding properties of the HMGB1,2 class of proteins: insights from tail switching and tail removal. J. Mol. Biol. 304, 135-149
23. Webb, M., Payet, D., Lee, K. B., Travers, A. A. and Thomas, J. O. (2001) Structural requirements for cooperative binding of HMGB1 to DNA minicircles. J. Mol. Biol. 309, 79-88
24. Pasheva, E., Sarov, M., Bidjekov, K., Ugrinova, I., Sarg, B., Lindner, H. and Pashev, I. G. (2004) In vitro acetylation of HMGB-1 and -2 proteins by CBP: the role of the acidic tail. Biochemistry 43, 2935-2940
25. Lee, K.-B., Brooks, D. J. and Thomas, J. O. (1998) Selection of a cDNA clone for chicken high-mobility-group 1 (HMG1) protein through its unusually conserved 3′-untranslated region, and improved expression of recombinant HMG1 in Escherichia coli. Gene 225, 97-105
26. Bannister, A. J. and Kouzarides, T (1996) The CBP co-activator is a histone acetyltransferase. Nature 384, 641-643
27. Thomas, J. O. and Kornberg, R. D. (1978) The study of histone-histone associations by chemical cross-linking. Methods Cell Biol. 18, 429-440
28. Watson, M., Stott, K. and Thomas, J. O. (2007) Mapping intramolecular interactions between domains in HMGB1 using a tail-truncation approach. J. Mol. Biol. 374, 1286-1297
29. Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A. and Bianchi, M. E. (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551-5560
30. Ramstein, J., Locker, D., Bianchi, M. E. and Leng, M. (1999) Domain-domain interactions in high mobility group 1 protein (HMG1). Eur. J. Biochem. 260, 692-700
31. Knapp, S., Muller, S., Digilio, G., Bonaldi, T., Bianchi, M. E. and Musco, G. (2004) 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, 11992-11997
32. Jung, Y. and Lippard, S. J. (2003) Nature of full-length HMGB1 binding to cisplatin-modified DNA. Biochemistry 42, 2664-2671
33. Wang, Q., Zeng, M., Wang, W. and Tang, J. (2007) The HMGB1 acidic tail regulates HMGB1 DNA binding specificity by a unique mechanism. Biochem. Biophys. Res. Commun. 360, 14-19
34. Štros, M., Bernuès, J. and Quérol, E. (1990) Calcium modulates the binding of high-mobility-group protein 1 to DNA. Biochem. Int. 21, 891-899
35. Štros, M. and Kolíbalovà, A. (1987) Interaction of nonhistone proteins HMG1 and HMG2 with core histones in nucleosomes and core particles revealed by chemical cross-linking, Eur. J. Biochem. 162, 111-118
36. Ueda, T., Chou, H., Kawase, T., Shirakawa, H. and Yoshida, M. (2004) Acidic C-tail of HMGB1 is required for its target binding to nucleosome linker DNA and transcription stimulation. Biochemistry 43, 9901-9908
37. Ugrinova, I., Pasheva, E. A., Armengaud, J. and Pashev, I. G. (2001) In vivo acetylation of HMGB1 protein enhances its binding affinity to distorted DNA. Biochemistry 40, 14655-14660
38. Ugrinova, I., Mitkova, E., Moskalenko, C., Pashev, I. and Pasheva, E. (2007) DNA bending versus DNA end joining activity of HMGB1 protein is modulated in vitro by acetylation. Biochemistry 46, 2111-2117