Abstract
Mechanisms of interaction of DNA with nonhistone chromosomal protein HMGB1 and linker histone H1 have been studied by means of circular dichroism and absorption spectroscopy. Both proteins are located in the internucleosomal regions of chromatin. It is demonstrated that the properties of DNA-protein complexes depend on the protein content and cannot be considered as a mere summing up of the effects of individual protein components. Interaction of the HMGB1 and H1 proteins is shown with DNA to be cooperative rather than competitive. Lysine-rich histone H1 facilitates the binding of HMGB1 to DNA by screening the negatively charged groups of the sugar-phosphate backbone of DNA and dicarboxylic amino acid residues in the C-terminal domain of HMGB1. The observed joint action of HMGB1 and H1 stimulates DNA condensation with the formation of anisotropic DNA-protein complexes with typical ψ-type CD spectra. Structural organization of the complexes depends not only on DNA-protein interactions but also on interaction between the HMGB1 and H1 protein molecules bound to DNA. Manganese ions significantly modify the mode of interactions between components in the triple DNA-HMGB1-H1 complex. The binding of Mn2+ ions weakens DNA-protein interactions and strengthens protein-protein interactions, which promote DNA condensation and formation of large DNA-protein particles in solution.
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References
Reeck G.R., Isackson P.J., Teller D.C. 1982. Domain structure in high molecular weight high mobility group nonhistone chromatin proteins. Nature. 300, 76–78.
Grosschedl R. 1995. Higher-order nucleoprotein complexes in transcription: Analogies with site-specific recombination. Curr. Opin. Cell Biol. 7, 362–370.
Crothers D.M. 1993. Architectural elements in nucleoprotein complexes. Curr. Biol. 3, 675–676.
Thomas J.O., Travers A.A. 2001. HMG1 and 2, and related “architectural’ DNA-binding proteins. Trends Biochem. Sci. 26, 167–174
Thomas J.O. 1999. Histone H1: Location and role. Curr. Opin. Cell Biol. 11, 312–317.
Zlatanova J., Yaneva J. 1991. Histone H1-DNA interactions and their relation to chromatin structure and function. DNA Cell Biol. 10, 239–248.
An W., van Holde K., Zlatanova J. 1998. The non-histone chromatin protein HMG1 protects linker DNA on the side opposite to that protected by linker histones. J. Biol. Chem. 273, 26289–26291.
Silva J.J.R.F.D., Williams R.J.P. 1991. Biological Chemistry of the Elements. Oxford: Clarendon Press.
Glusker J.R. 1991. Structural aspects of metal liganding to functional groups in proteins. Adv. Protein Chem. 42, 1–76.
Metal Ions in Biological Systems: Manganese and Its Role in Biological Processes. Eds. Sigel S., Sigel H. NY: Marsel Dekker, 2000.
Noble C.G., Maxwell A. 2002.The role of GyrB in the DNA cleavage-religation reaction of DNA gyrase: A proposed two metal-ion mechanism. J. Mol. Biol. 318, 361–371.
Hays H., Berdis A. 2002. Manganese substantially alters the dynamics of translesion DNA synthesis. J. Biochem. 41, 4771–4778.
Yamagata A., Kakuta Y., Masui R., Fukuyama K. 2002. The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc. Natl. Acad. Sci. U.S.A. 99, 5908–5912.
Santagata S., Aidinis V., Spanopoulou E. 1998. The effect of Me2+ cofactors at the initial stages of V(D)J recombination. J. Biol. Chem. 273, 16325–16331.
Shockett P.E., Schatz D.G. 1999. DNA hairpin opening mediated by the RAG1 and RAG2 proteins. Mol. Cell Biol. 19, 4159–4166.
Swanson P.C. 2002. A RAG-1/RAG-2 tetramer supports 12/23-regulated synapsis, cleavage, and transposition of V(D)J recombination signals. Mol. Cell Biol. 22, 7790–7801.
Polyanichko A.M., Chikhirzhina E.V., Kostyleva E.I., Vorob’ev V.I. 2004. Structure of DNA complexes with nonhistone chromosomal protein HMGB1 in the presence of manganese ions. Mol. Biol. (Moscow). 38, 891–898.
Polyanichko A.M., Chikhirzhina E.V., Andrushchenko V.V., Kostyleva E.I., Wieser H., Vorob’ev V.I. 2004. The effect of Ca2+ ions on DNA compaction in the complex with HMGB1 nonhistone chromosomal protein. Mol. Biol. (Moscow). 38, 590–599.
Chikhirzhina E.V., Polyanichko A.M., Skvortsov A.N., Kostyleva E.I., Houssier C., Vorob’ev V.I. 2002. HMG1 domains: The victims of the circumstance. Mol. Biol. (Moscow). 36, 412–418.
Johns E.W. 1982. The HMG Chromosomal Proteins. London: Academic Press.
Kohlstaedt L.A, Cole R.D. 1994. Specific interaction between H1 histone and high mobility protein HMG1. Biochemistry. 33, 570–575.
Polyanichko A., Andrushchenko V., Chikhirzhina E., Vorob’ev V., Wieser H. 2004. The effect of manganese(II) on DNA structure: Electronic and vibrational circular dichroism studies. Nucleic Acids Res. 32, 989–996.
Polyanichko A.M., Chikhirzhina E.V., Andrushchenko V.V., Wieser H., Vorob’ev V.I. 2005. Spectroscopic investigations of the structure of DNA complexes with Mn2+ in UV and IR regions. Biophysics. 50, 710–715.
Ramakrishnan V., Fich J.T., Graziano V., Lee P.L., Sweet R.M. 1993.Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature. 362, 219–223.
Travers A., Thomas J.O. 2004. Chromosomal HMG-box proteins. In: Chromatin Structure and Dynamics: State-of-the-Art. Eds. Zlatanova J., Leuba S.H. NY: Elsevier, pp. 103–126.
Lerman L.S. 1971. A transition to a compact form of DNA in polymer solutions. Proc. Natl. Acad. Sci. U.S.A. 68, 1886–1890
Jordan C.F, Lerman L.S, Venable J.H. 1972. Structure and circular dichroism of DNA in concentrated polymer solutions. Nature New Biol. 236, 67–70.
Chikhirzhina E.V., Vorob’ev V.I. 2002. Linker histones: Conformational changes and the role in the structural organization of chromatin. Tsitologiya. 44, 721–736.
Chikhirzhina E.V., Kostyleva E.I., Ramm E.I., Vorob’ev V.I. 1998. Chromatin compactification using a model system of DNA-protein complexes. Tsitologiya. 40, 883–888.
Fasman G.D., Valenzuela M.S., Adler A.L. 1971. Complexes of deoxyribonucleic acid with fragments of lysine-rich histone (f-1). Circular dichroism studies. Biochemistry. 10, 3795–3801.
Maniatis T., Venable J.H.Jr., Lerman L.S. 1974. The structure of psi DNA. J. Mol. Biol. 84, 37–64.
Jerzmanowski A. 2004. The linker histones. In: Chromatin Structure and Dynamics: State-of-the-Art. Eds. Zlatanova J., Leuba S.H. NY: Elsevier, pp. 75–102.
Polyanichko A.M., Chikhirzhina E.V., Skvortsov A.N., Kostyleva E.I., Colson P., Houssier C., Vorob’ev V.I. 2002. The HMG1 ta(i)le. J. Biomol. Struct. Dyn. 19, 1053–1062.
Hadden J.M., Declais A.-C., Phillips S.E.V., Lilley M.J. 2002. Metal ions bound at the active site of the junction resolving enzyme T7 endonuclease. EMBO J. 21, 3505–3515.
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Original Russian Text © E.V. Chikhirzhina, A.M. Polyanichko, E.I. Kostyleva, V.I. Vorobyev, 2011, published in Molekulyarnaya Biologiya, 2011, Vol. 45, No. 2, pp. 356–365.
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Chikhirzhina, E.V., Polyanichko, A.M., Kostyleva, E.I. et al. Structure of DNA complexes with chromosomal protein HMGB1 and histone H1 in the presence of manganese ions: 1. Circular dichroism spectroscopy. Mol Biol 45, 318–326 (2011). https://doi.org/10.1134/S002689331102004X
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DOI: https://doi.org/10.1134/S002689331102004X