Interactions between N- and C-terminal domains of the Saccharomyces cerevisiae high-mobility group protein HMO1 are required for DNA bending

Biochemistry

Volumn 45, Issue 11, 2006, Pages 3635-3645

  Bauerle, Kevin T ^a,b   Kamau, Edwin ^a,c   Grove, Anne ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ELECTROPHORESIS; MELT SPINNING; SPECTROSCOPIC ANALYSIS; SUBSTRATES; THERMODYNAMIC STABILITY;

CIRCULAR DICHROISM; DESTABILIZATION; DNA BENDING; MELTING TEMPERATURES; MELTING TRANSITION;

PROTEINS;

CURVED DNA; FUNGAL PROTEIN; HIGH MOBILITY GROUP PROTEIN; LYSINE; PROTEIN HMO1; PROTEIN HMO1 BOX A; PROTEIN HMO1 BOX B; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; DNA BINDING; DNA CONFORMATION; GEL MOBILITY SHIFT ASSAY; MELTING POINT; NONHUMAN; PHASE TRANSITION; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; TEMPERATURE DEPENDENCE; THERMOSTABILITY;

AMINO ACID SEQUENCE; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HIGH MOBILITY GROUP PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TEMPERATURE;

SACCHAROMYCES CEREVISIAE;

EID: 33645242130     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0522798     Document Type: Article

References (39)

1. Bustin, M., and Reeves, R. (1996) High-mobility-group chromosomal proteins: Architectural components that facilitate chromatin function, Prog. Nucleic Acid Res. Mol. Biol. 54, 35-100.
2. 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.
3. Love, J. L., Li, X., 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.
4. Hardman, C. H., Broadhurst, R. W., Raine, A. R., Grasser, K. D., Thomas, J. O., and Laue, E. D. (1995) Structure of the A-domain of HMG1 and its interaction with DNA as studied by heteronuclear three- and four-dimensional NMR spectroscopy, Biochemistry 34, 16596-16607.
5. Weir, H. M., Kraulis, P. J., Hill, C. S., Raine, A. R. C., Laue, E. D., and Thomas, J. O. (1993) Structure of the HMG box motif in the B-domain of HMG1, EMBO J. 12, 1311-1319.
6. He, Q., Ohndorf, U. M., and Lippard, S. J. (2000) Intercalating residues determine the mode of HMG1 domains A and B binding to cisplatin-modified DNA, Biochemistry 39, 14426-14435.
7. Jones, D. N. M., Searles, M. A., Shaw, G. L., Churchill, M. E. A., Ner, S. S., Keeler, J., Travers, A. A., and Neuhaus, D. (1994) The solution structure and dynamics of the DNA-binding domain of HMG-D from Drosophila melanogaster, Structure 2, 609-627.
8. Allain, F. H. T., Yen, Y. M., Masse, J. E., Schultze, P., Dieckmann, T., Johnson, R. C., and Feigon, J. (1999) Solution structure of the HMG protein NHP6A and its interaction with DNA reveals the structural determinants for non-sequence-specific binding, EMBO J. 18, 2563-2579.
9. Werner, M. H., Huth, J. R., Gronenborn, A. M., and Clore, G. M. (1995) Molecular basis of human 46X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex, Cell 81, 705-714.
10. Ohndorf, U. M., Rould, M. A., He, Q., Pabo, C. O., and Lippard, S. J. (1999) Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins, Nature 399, 708-712.
11. Jamieson, E. R., and Lippard, S. J. (1999) Structure, Recognition, and Processing of Cisplatin-DNA Adducts, Chem. Rev. 99, 2469-2498.
12. Thomas, J. O. (2001) HMG1 and 2: Architectural DNA-binding proteins, Biochem. Soc. Trans. 29, 395-401.
13. Lee, K. B., and Thomas, J. O. (2000) 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, 135-149.
14. 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.
15. Taudte, S., Xin, H., Bell, A. J., Jr., and Kallenbach, N. R. (2001) Interactions between HMG boxes, Protein Eng. 14, 1015-1023.
16. 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.
17. Yen, Y., Wong, B., and Johnson, C. R. (1998) Determinants of DNA binding and bending by the Saccharomyces cerevisiae high mobility group protein NHP6A that are important for its biological activities. Role of the unique N terminus and putative intercalating methionine, J. Biol. Chem. 273, 4430-4435.
18. Dow, L. K., Jones, D. N., Wolfe, S. A., Verdine, G. L., and Churchill, M. E. (2000) Structural studies of the high mobility group globular domain and basic tail of HMG-D bound to disulfide cross-linked DNA, Biochemistry 39, 9725-9736.
19. Thomsen, M. S., Franssen, L., Launholt, D., Fojan, P., and Grasser, K. D. (2004) Interactions of the basic N-terminal and the acidic C-terminal domains of the maize chromosomal HMGB1 protein, Biochemistry 43, 8029-8037.
20. Lu, J., Kobayashi, R., and Brill, J. S. (1996) Characterization of a high mobility group 1/2 homolog in yeast, J. Biol. Chem. 271, 33678-33685.
21. Dolinski, J. K., and Heitmain, J. (1999) Hmo1p, a high mobility group 1/2 homolog, genetically and physically interacts with the yeast FKBP12 prolyl isomerase, Genetics 151, 935-944.
22. Gadal, O., Labarre, S., Boschiero, C., and Thuriaux, P. (2002) Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system, EMBO J. 21, 5498-5507.
23. Alekseev, Y. S., Kovaltsova, V. S., Fedorova, V. I., Gracheva, M. L., Evstukhina, A. T., Peshekhonov, T. V., and Korolev, G. V. (2002) HSM2 (HMO1) gene participates in mutagenesis control in yeast Saccharomyces cerevisiae, DNA Repair 1, 287-297.
24. Kamau, E., Bauerle, K. T., and Grove, A. (2004) The Saccharomyces cerevisiae high mobility group box protein HMO1 contains two functional DNA-binding domains, J. Biol. Chem. 279, 55234-55240.
25. Ramsay, G. D., and Eftink, M. R. (1994) Analysis of multidimensional spectroscopic data to monitor unfolding of proteins, Methods Enzymol. 240, 615-645.
26. Grove, A., and Lim, L. (2001) High affinity DNA binding of HU protein from the hyperthermophile Thermotoga maritima, J. Mol. Biol. 311, 491-502.
27. Klimczak, L. J., and Cashmore, A. R. (1994) Microheterogeneous Cytosolic High-Mobility Group Proteins from Broccoli Co-Purify with and Are Phosphorylated by Casein Kinase II, Plant Physiol. 105, 911-919.
28. Wisniewski, J. R., Szewczuk, Z., Petry, I., Schwanbeck, R., and Renner, U. (1999) Constitutive phosphorylation of the acidic tails of the high mobility group 1 proteins by casein kinase II alters their conformation, stability, and DNA binding specificity, J. Biol. Chem. 274, 20116-20122.
29. Stemmer, C., Schwander, A., Bauw, G., Fojan, P., and Grasser, K. D. (2002) Protein kinase CK2 differentially phosphorylates maize chromosomal high mobility group B (HMGB) proteins modulating their stability and DNA interactions, J. Biol. Chem. 277, 1092-1098.
30. Songyang, Z., Blechner, S., Hoagland, N., Hoekstra, M. F., Piwnica-Worms, H., and Cantley, L. C. (1994) Use of an oriented peptide library to determine the optimal substrates of protein kinases, Curr. Biol. 4, 973-982.
31. Obenauer, J. C., Cantley, L. C., and Yaffe, M. B. (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs, Nucleic Acids Res. 31, 3635-3641.
32. 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 (HMG1), Eur. J. Biochem. 253, 787-795.
33. Crane-Robinson, C., Read, C. M., Cary, P. D., Driscoll, P. C., Dragan, A. I., and Privalov, P. L. (1998) The energetics of HMG box interactions with DNA, Thermodynamic description of the box from mouse Sox-5, J. Mol. Biol. 281, 705-717.
34. Taudte, S., Xin, H., and Kallenbach, N. R. (2000) Alanine mutagenesis of high-mobility-group-protein-1 box B (HMG1-B), Biochem. J. 347, 807-814.
35. Wong, B., Masse, E. J., Yen, Y., Giannikoupolous, P., Feigon, J., and Johnson, C. R. (2002) Binding to cisplatin-modified DNA by the Saccharomyces cerevisiae HMGB protein Nhp6A, Biochemistry 41, 5404-5414.
36. Pöhler, J. R., Norman, D. G., Bramham, J., Bianchi, M. E., and Lilley, D. M. J. (1998) HMG box proteins bind to four-way DNA junctions in their open conformation, EMBO J. 17, 817-826.
37. Chow, C. S., Whitehead, J. P., and Lippard, S. J. (1994) HMG domain proteins induce sharp bends in cisplatin-modified DNA, Biochemistry 33, 15124-15130.
38. He, Q., Ohndorf, U. M., and Lippard, S. J. (2000) Intercalating residues determine the mode of HMG1 domains A and B binding to cisplatin-modified DNA, Biochemistry 39, 14426-14435.
39. Jung, Y., and Lippard S. J. (2003) Nature of full-length HMGB1 binding to cisplatin-modified DNA, Biochemistry 42, 2664-2671.