INFLUENCE OF SODIUM AND POTASSIUM IONS ON CONFORMATION OF LINKER PARTS OF NUCLEOSOMES
Abstract
The structure of chromatin and DNA accessibility to proteins depend on the structure of DNA “linkers” entering and exiting the nucleosome. Since DNA is negatively charged, conformation of the DNA linkers, in turn, is likely affected by ionic microenvironment. Here method of fluorescence microscopy of single complexes was used to study the effect of Na+ and K+ ions on the structure of the DNA linkers. It was revealed that nucleosomes adopt one of two conformational states, and occupancy of these states is considerably changed after substitution of K+ ions by Na+. These changes are likely caused by different interaction of Na+ and K+ ions with DNA in the regions of entry and exit of DNA from the nucleosome. Cation- dependent changes in conformation of the DNA linkers can affect topological barriers in nucleosomes, structure of polynucleosome chromatin and interactions of DNA with different protein factors.
Keywords
About the Authors
A. V. LyubitelevRussian Federation
Bioengineering Department, School of Biology
Leninskiye Gory 1–12, Moscow, 119234, Russia
V. M. Studitsky
Russian Federation
Bioengineering Department, School of Biology
Leninskiye Gory 1–12, Moscow, 119234, Russia
333 Cottman avenue, Philadelphia, Pennsylvania 19111, USA
A. V. Feofanov
Russian Federation
Bioengineering Department, School of Biology
Leninskiye Gory 1–12, Moscow, 119234, Russia
M. P. Kirpichnikov
Russian Federation
Bioengineering Department, School of Biology
Leninskiye Gory 1–12, Moscow, 119234, Russia
Miklukho-Maklaya ul. 16/10, 117997, Moscow, Russia
References
1. Ngo T.T., Zhang Q., Zhou R., Yodh J.G., Ha T. Asymmetric unwrapping of nucleosomes under tension directed by DNA local flexibility // Cell. 2015. Vol. 160 N 6. P. 1135–1144.
2. Li G., Levitus M., Bustamante C., Widom J. Rapid spontaneous accessibility of nucleosomal DNA // Nat. Struct. Mol. Biol. 2005. Vol. 12. N 1. P. 46–53.
3. Gansen A., Toth K., Schwarz N.,Langowski J. Structural variability of nucleosomes detected by single-pair Forster resonance energy transfer: histone acetylation, sequence variation, and salt effects // J. Phys. Chem. B. 2009. Vol. 113. N 9. P. 2604–2613.
4. Gansen A., Valeri A., Hauger F., Felekyan S., Kalinin S., Toth K., Langowski J., Seidel C.A. Nucleosome disassembly intermediates characterized by single-molecule FRET // Proc. Natl. Acad. Sci. U.S.A. 2009. Vol. 106. N 36. P. 15308–15313.
5. Zinchenko A.A., Yoshikawa K. Na+ shows a markedly higher potential than K+ in DNA compaction in a crowded environment // Biophys. J. 2005. Vol. 88. N 6. P. 4118–4123.
6. Savelyev A., Papoian G.A. Electrostatic, steric, and hydration interactions favor Na(+) condensation around DNA compared with K(+) // J. Am. Chem. Soc. 2006. Vol. 128. N 45. P. 14506–14518.
7. Materese C.K., Savelyev A., Papoian G.A. Counterion atmosphere and hydration patterns near a nucleosome core particle // J. Am. Chem. Soc. 2009. Vol. 131. N 41. P. 15005– 15013.
8. Gaykalova D.A., Kulaeva O.I., Bondarenko V.A., Studitsky V.M. Preparation and analysis of uniquely positioned mononucleosomes // Chromatin Protocols. Methods Mol. Biol. Vol. 523 / Ed. S.P. Chellappan. Humana Press, 2009. P. 109–123.
9. Kudryashova K.S., Chertkov O.V., Nikitin D.V., Pestov N.A., Kulaeva O.I., Efremenko A.V., Solonin A.S., Kirpichnikov M.P., Studitsky V.M., Feofanov A.V. Preparation of mononucleosomal templates for analysis of transcription with RNA polymerase using spFRET // Chromatin Protocols. Methods Mol. Biol. Vol. 1288 / Ed. S.P. Chellappan. N.Y.: Springer, 2015. P. 395–412.
10. Lyubitelev A.V., Kudryashova K.S., Mikhaylova M.S., Malyuchenko N.V., Chertkov O.V., Studitsky V.M., Feofanov A.V., Kirpichnikov M.P. Change in conformation of linker DNA upon binding of histone H1.5 to nucleosome: fluorescent microscopy of single complexes // Moscow Univ. Biol. Sci. Bull. 2016. Vol. 71. N 2. P. 108–113.
11. Manning G.S. The persistence length of DNA is reached from the persistence length of its null isomer through an internal electrostatic stretching force // Biophys. J. 2006. Vol. 91. N 10. P. 3607–3616.
12. Valieva M.E., Armeev G.A., Kudryashova K.S., Gerasimova N.S., Shaytan A.K., Kulaeva O.I., McCullough L.L., Formosa T., Georgiev P.G., Kirpichnikov M.P., Studitsky V.M., Feofanov A.V. Large-scale ATP-independent nucleosome unfolding by a histone chaperone // Nat. Struct. Mol. Biol. 2016. Vol. 23. N 12. P. 1111–1116.
13. Sultanov D., Gerasimova N., Kudryashova K., Maluchenko N., Kotova E., Langelier M.F., Pascal J., Kirpichnikov M., Feofanov A., Studitsky V. Unfolding of core nucleosomes by PARP- 1 revealed by spFRET microscopy // AIMS Genetics. 2017. Vol. 4. N 1. P. 21–31.
14. Choy J.S., Lee T.H. Structural dynamics of nucleosomes at single-molecule resolution // Trends Biochem. Sci. 2012. Vol. 37. N 10. P. 425–435.
15. Wei S., Falk S.J., Black B.E., Lee T.H. A novel hybrid single molecule approach reveals spontaneous DNA motion in the nucleosome // Nucleic Acids Res. 2015. Vol. 43. N 17. e111.
16. Koopmans W.J., Brehm A., Logie C., Schmidt T., van Noort J. Single-pair FRET microscopy reveals mononucleosome dynamics // J. Fluoresc. 2007. Vol. 17. N 6. P. 785–795.
17. Kenzaki H., Takada S. Partial unwrapping and histone tail dynamics in nucleosome revealed by coarse-grained molecular simulations // PLoS Comput. Biol. 2015. Vol. 11. N 8. e1004443.
18. Li Z., Kono H. Distinct roles of histone H3 and H2A tails in nucleosome stability // Sci. Rep. 2016. Vol. 6. 31437.
19. Forties R.A., North J.A., Javaid S., Tabbaa O.P., Fishel R., Poirier M.G., Bundschuh R. A quantitative model of nucleosome dynamics // Nucleic Acids Res. 2011. Vol. 39. N 19. P. 8306–8313.
Review
For citations:
Lyubitelev A.V., Studitsky V.M., Feofanov A.V., Kirpichnikov M.P. INFLUENCE OF SODIUM AND POTASSIUM IONS ON CONFORMATION OF LINKER PARTS OF NUCLEOSOMES. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2017;72(3):169-173. (In Russ.)