Effect of Single-Strand DNA Breaks on Transcription of Nucleosomes
Tóm tắt
Previous studies have revealed the inhibitory effect of single-strand breaks in a non-template DNA strand (NT-SSB) on RNA polymerase (RNAP) transcription through the nucleosome. The observed effect was explained within the model of chromatin transcription mechanism with the formation of intranucleosomal DNA loops (i-loops), intermediates, in which the enzyme is locked in the DNA loop on the histone octamer. According to the model, NT-SSBs reduce the tension in the DNA structure caused by transcription, thus stabilizing DNA-histone interactions and inhibiting RNAP. In this work, the boundaries of such i-loops have been determined. It has been found that the formation of contacts between DNA and histones behind RNAP occurs at a distance of more than 17 base pairs from the active center of the enzyme.
Tài liệu tham khảo
Tubbs, A. and Nussenzweig, A., Endogenous DNA damage as a source of genomic instability in cancer, Cell, 2017, vol. 168, no. 4, pp. 644‒656.
Caldecott, K.W., DNA single-strand break repair and human genetic disease, Trends Cell Biol., 2022, vol. 32, no. 9, pp. 733‒745.
McKinnon, P.J. and Caldecott, K.W., DNA strand break repair and human genetic disease, Annu. Rev. Genomics Hum. Genet., 2007, vol. 8, pp. 37‒55.
Zhou, W. and Doetsch, P.W., Effects of abasic sites and DNA single-strand breaks on prokaryotic RNA polymerases, Proc. Natl. Acad. Sci. U. S. A., 1993, vol. 90, no. 14, pp. 6601‒6605.
Kathe, S.D., Shen, G.P., and Wallace, S.S., Single-stranded breaks in DNA but not oxidative DNA base damages block transcriptional elongation by RNA polymerase II in HeLa cell nuclear extracts, J. Biol. Chem., 2004, vol. 279, no. 18, pp. 18511‒18520.
Neil, A.J., Belotserkovskii, B.P., and Hanawalt, P.C., Transcription blockage by bulky end termini at single-strand breaks in the DNA template: differential effects of 5' and 3' adducts, Biochemistry, 2012, vol. 51, no. 44, pp. 8964‒8970.
Li, S. and Smerdon, M.J., Dissecting transcription-coupled and global genomic repair in the chromatin of yeast GAL1-10 genes, J. Biol. Chem., 2004, vol. 279, no. 14, pp. 14418‒14426.
Pestov, N.A., Gerasimova, N.S., Kulaeva, O.I., and Studitsky, V.M., Structure of transcribed chromatin is a sensor of DNA damage, Sci. Adv., 2015, vol. 1, no. 6, p. e1500021.
Luger, K., Mäder, A.W., Richmond, R.K., Sar-gent, D.F., and Richmond, T.J., Crystal structure of the nucleosome core particle at 2.8 Å resolution, Nature, 1997, vol. 389, no. 6648, pp. 251‒260.
Hartzog, G.A., Speer, J.L., and Lindstrom, D.L., Transcript elongation on a nucleoprotein template, Biochim. Biophys. Acta, 2002, vol. 1577, no. 2, pp. 276‒286.
Gerasimova, N.S., Pestov, N.A., Kulaeva, O.I., Clark, D.J., and Studitsky, V.M., Transcription-induced DNA supercoiling: New roles of intranucleosomal DNA loops in DNA repair and transcription, Transcription, 2016, vol. 7, no. 3, pp. 91‒95.
Lowary, P.T. and Widom, J., New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning, J. Mol. Biol., 1998, vol. 276, no. 1, pp. 19‒42.
Artsimovitch, I., Svetlov, V., Murakami, K.S., and Landick, R., Co-overexpression of Escherichia coli RNA polymerase subunits allows isolation and analysis of mutant enzymes lacking lineage-specific sequence insertions, J. Biol. Chem., 2003, vol. 278, no. 14, pp. 12344‒12355.
Thastrom, A., Lowary, P.T., Widlund, H.R., Cao, H., Kubista, M., and Widom, J., Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences, J. Mol. Biol., 1999, vol. 288, no. 2, pp. 213‒229.
Bondarenko, V.A., Steele, L.M., Ujvari, A., Gaykalova, D.A., Kulaeva, O.I., Polikanov, Y.S., Luse, D.S., and Studitsky, V.M., Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II, Mol. Cell, 2006, vol. 24, no. 3, pp. 469‒479.
Chang, H.W., Kulaeva, O.I., Shaytan, A.K., Kiba-nov, M., Kuznedelov, K., Severinov, K.V., Kirpichnikov, M.P., Clark, D.J., and Studitsky, V.M., Analysis of the mechanism of nucleosome survival during transcription, Nucleic Acids Res., 2014, vol. 42, no. 3, pp. 1619‒1627.
Kulaeva, O.I., Gaykalova, D.A., Pestov, N.A., Golovastov, V.V., Vassylyev, D.G., Artsimovitch, I., and Studitsky, V.M., Mechanism of chromatin remodeling and recovery during passage of RNA polymerase II, Nat. Struct. Mol. Biol., 2009, vol. 16, no. 12, pp. 1272‒1278.
Walter, W., Kireeva, M.L., Studitsky, V.M., and Kashlev, M., Bacterial polymerase and yeast polymerase II use similar mechanisms for transcription through nucleosomes, J. Biol. Chem., 2003, vol. 278, no. 38, pp. 36148‒36156.
Ausio, J., Seger, D., and Eisenberg, H., Nucleosome core particle stability and conformational change: Effect of temperature, particle and NaCl concentrations, and crosslinking of histone H3 sulfhydryl groups, J. Mol. Biol., 1984, vol. 176, no. 1, pp. 77‒104.
Bancaud, A., Wagner, G., Conde, E.S.N., Lavelle, C., Wong, H., Mozziconacci, J., Barbi, M., Sivolob, A., Le Cam, E., Mouawad, L., Viovy, J.L., Victor, J.M., and Prunell, A., Nucleosome chiral transition under positive torsional stress in single chromatin fibers, Mol. Cell, 2007, vol. 27, no. 1, pp. 135‒147.
Lilley, D.M., DNA opens up—supercoiling and heavy breathing, Trends Genet., 1988, vol. 4, no. 4, pp. 111‒114.