Biopolym. Cell. 2010; 26(5):351-359.
http://dx.doi.org/10.7124/bc.000169
Reviews
Nucleosome conformational flexibility in experiments with single chromatin fibers
1Sivolob A. V.
  1. Taras Shevchenko National University of Kyiv
    64, Volodymyrska Str., Kyiv, Ukraine, 01601

Abstract

Studies on the chromatin nucleosome organization play an ever increasing role in our comprehension of mechanisms of the gene activity regulation. This minireview describes the results on the nucleosome conformational flexibility, which were obtained using magnetic tweezers to apply torsion to oligonucleosome fibers reconstituted on single DNA molecules. Such an approach revealed a new structural form of the nucleosome, the reversome, in which DNA is wrapped in a right-handed superhelix around a distorted histone octamer. Molecular mechanisms of the nucleosome structural flexibility and its biological relevance are discussed.
Keywords: nucleosome, DNA supercoiling, chromatin fiber, conformational flexibility
Full text: (PDF, in English) (PDF, in Russian)

References

[1] Luger K., Mader A. W., Richmond R. K., Sargent D. F., Richmond T. J. Crystal structure of the nucleosome core particle at 2.8 C resolution Nature 1997 389, N 6648:251–260.
[2] Davey C. A., Sargent D. F., Luger K., Mader A. W., Richmond T. J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 C resolution J. Mol. Biol 2002 319, N 5 P. 1097–1113.
[3] Richmond T. J., Davey C. A. The structure of DNA in the nucleosome core Nature 2003 423, N 6936:145–150.
[4] Ong M. S., Richmond T. J., Davey C. A. DNA stretching and extreme kinking in the nucleosome core J. Mol. Biol 2007 368, N 4:1067–1074.
[5] Boyer L. A., Shao X., Ebright R. H., Peterson C. L. Roles of the histone H2A-H2B dimers and the (H3-H4)(2) tetramer in nucleosome remodeling by the SWI-SNF complex J. Biol. Chem 2000 275, N 16:11545–11552.
[6] Kireeva M. L., Walter W., Tchernajenko V., Bondarenko V., Kashlev M., Studitsky V. M. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription Mol. Cell 2002 9, N 3:541–552.
[7] Studitsky V. M., Walter W., Kireeva M., Kashlev M., Felsenfeld G. Chromatin remodeling by RNA polymerases Trends Biochem. Sci 2004 29, N 3:127–135.
[8] Li B., Carey M., Workman J. L. The role of chromatin during transcription Cell 2007 128, N 4:707–719.
[9] Kulaeva O. I., Gaykalova D. A., Studitsky V. M. Transcription through chromatin by RNA polymerase II: histone displacement and exchange Mutat. Res 2007 618, N 1–2 P. 116–129.
[10] Cairns B. R. Chromatin remodeling: insights and intrigue from single-molecule studies Nat. Struct. Mol. Biol 2007 14, N 11:989–996.
[11] Choudhary P., Varga-Weisz P. ATP-dependent chromatin remodelling: action and reaction Subcell. Biochem 2007 41:29–43.
[12] Cairns B. R. The logic of chromatin architecture and remodelling at promoters Nature 2009 461, N 7261:193– 198.
[13] Clapier C. R., Cairns B. R. The biology of chromatin remodeling complexes Annu. Rev. Biochem 2009 78:273– 304.
[14] Rando O. J., Chang H. Y. Genome-wide views of chromatin structure Annu. Rev. Biochem 2009 78:245–271.
[15] Marmorstein R. Protein modules that manipulate histone tails for chromatin regulation Nat. Rev. Mol. Cell Biol 2001 2, N 6:422–432.
[16] Narlikar G. J., Fan H. Y., Kingston R. E. Cooperation between complexes that regulate chromatin structure and transcription. Cell. 2002; 108, N 4:475–487.
[17] Turner B. M. Cellular memory and the histone code. Cell 2002 111, N 3:285–291.
[18] An W. Histone acetylation and methylation: combinatorial players for transcriptional regulation Subcell. Biochem 2007 41:351–369.
[19] Shahbazian M. D., Grunstein M. Functions of site-specific histone acetylation and deacetylation Annu. Rev. Biochem 2007 76:75–100.
[20] Goulet I., Zivanovic Y., Prunell A., Revet B. Chromatin reconstitution on small DNA rings J. Mol. Biol 1988 200, N 2:253–266.
[21] Toth K., Brun N., Langowski J. Chromatin compaction at the mononucleosome level Biochemistry 2006 45, N 6 P. 1591–1598.
[22] Mihardja S., Spakowitz A. J., Zhang Y., Bustamante C. Effect of force on mononucleosomal dynamics Proc. Nat. Acad. Sci. USA 2006 103, N 43:15871–15876.
[23] Hall M. A., Shundrovsky A., Bai L., Fulbright R. M., Lis J. T., Wang M. D. High-resolution dynamic mapping of histoneDNA interactions in a nucleosome Nat. Struct. Mol. Biol 2009 16, N 2 P.124–129.
[24] Polach K. J., Widom J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation J. Mol. Biol 1995 254, N 2 P. 130–149.
[25] Anderson J. D., Thastrom A., Widom J. Spontaneous access of proteins to buried nucleosomal DNA target sites occurs via a mechanism that is distinct from nucleosome translocation Mol. Cell. Biol 2002 22, N 20:7147–7157.
[26] Li G., Levitus M., Bustamante C., Widom J. Rapid spontaneous accessibility of nucleosomal DNA Nat. Struct. Mol. Biol 2005 12, N 1:46–53.
[27] Hodges C., Bintu L., Lubkowska L., Kashlev M., Bustamante C. Nucleosomal fluctuations govern the transcription dynamics of RNA polymerase II Science 2009 325, N 5940 P. 626–628.
[28] Muthurajan U. M., Park Y. J., Edayathumangalam R. S., Suto R. K., Chakravarthy S., Dyer P. N., Luger K. Structure and dynamics of nucleosomal DNA Biopolymers 2003 68, N 4:547–556.
[29] Li G., Widom J. Nucleosomes facilitate their own invasion Nat. Struct. Mol. Biol 2004 11, N 8:763–769.
[30] Tomschik M., Zheng H., van Holde K., Zlatanova J., Leuba S. H. Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer Proc. Nat. Acad. Sci. USA 2005 102, N 9:3278–3283.
[31] Cook P. R., Brazell I. A. Conformational constraints in nuclear DNA. J. Cell Sci. 1976; 22, N 2:287–302.
[32] Benyajati C., Worcel A. Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster Cell 1976 9, N 3:393–407.
[33] Lebkowski J. S., Laemmli U. K. Nonhistone proteins and long range organization of HeLa interphase DNA J. Mol. Biol 1982 156, N 2:325–344.
[34] Hamiche A., Carot V., Alilat M., De Lucia F., O'Donohue M. F., Revet B., Prunell A. Interaction of the histone (H3–H4)2 tetramer of the nucleosome with positively supercoiled DNA minicircles: Potential flipping of the protein from a leftto a right-handed superhelical form Proc. Natl Acad. Sci. USA 1996 93, N 15:7588–7593.
[35] Sivolob A., De Lucia F., Revet B., Prunell A. Nucleosome dynamics II. High flexibility of nucleosome entering and exiting DNAs to positive crossing J. Mol. Biol 1999 285, N 3 P. 1081–1099.
[36] De Lucia F., Alilat M., Sivolob A., Prunell A. Nucleosome dynamics III. Histone tail-dependent fluctuation of nucleosomes between open and closed DNA conformations J. Mol. Biol 1999 285, N 3:1101–1119.
[37] Alilat M., Sivolob A., Revet B., Prunell A. Nucleosome dynamics IV. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA particle J. Mol. Biol 1999 291, N 4:815– 841.
[38] Sivolob A., Prunell A. Nucleosome dynamics V. Ethidium bromide versus histone tails in modulating ethidium bromide-driven tetrasome chiral transition J. Mol. Biol 2000 295, N 1:41–53.
[39] Sivolob A., De Lucia F., Alilat M., Prunell A. Nucleosome dynamics. VI. Histone tail regulation of tetrasome chiral transition. A relaxation study of tetrasomes on DNA minicircles J. Mol. Biol 2000 295, N 1:55–69.
[40] Sivolob A., Lavelle C., Prunell A. Sequence-dependent nucleosome structural and dynamic polymorphism. Potential involvement of histone H2B N-terminal tail proximal domain J. Mol. Biol 2003 326, N 1:49–63.
[41] Sivolob A., Prunell A. Linker histone-dependent organization and dynamics of nucleosome entry/exit DNAs J. Mol. Biol 2003 331, N 5:1025–1040.
[42] Conde e Silva N., Black B. E., Sivolob A., Filipski J., Cleveland D. W., Prunell A. CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization J. Mol. Biol 2007 370, N 3:555–573.
[43] Ito T., Ikehara T., Nakagawa T., Kraus W.L., Muramatsu M. p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone Genes Develop 2000 14, N 15:1899–1907.
[44] Reinberg D., Sims R. J. de FACTo nucleosome dynamics J. Biol. Chem 2006 281, N 33:23297–23301.
[45] Prunell A., Sivolob A. Paradox lost: nucleosome structure and dynamics by the DNA minicircle approach Chromatin structure and dynamics: state-of-the-art. New Comprehensive Biochemistry. Eds J. Zlatanova, S. H. Leuba Amsterdam: Elsevier, 2004 Vol. 39:45–73.
[46] Sivolob A., Prunell A. Nucleosome conformational flexibility and implications for chromatin dynamics Phil. Trans. Roy. Soc. Lond. A 2004 362, N 1820:1519–1547.
[47] Sivolob A., Lavelle C., Prunell A. Flexibility of nucleosomes on topologically constrained DNA IMA Volumes in Mathematics and its Applications / Eds C. J. Benham, S. Harvey, W. Olson, D. W. Sumners, D. Swigon New York: Springer, 2009 Vol. 150:251–291.
[48] Strick T. R., Allemand J.-F., Bensimon D., Bensimon A., Croquette V. The elasticity of a single supercoiled DNA molecule Science 1996 271, N 5257:1835–1837.
[49] Strick T. R., Allemand J.-F., Bensimon D., Croquette V. Behavior of supercoiled DNA Biophys. J 1998 74, N 4 P. 2016–2028.
[50] Strick T. R., Allemand J.-F., Bensimon D., Croquette V. Stress-induced structural transitions in DNA and proteins Annu. Rev. Biophys. Biomol. Struct 2000 29:523– 543.
[51] Strick T. R., Croquette V., Bensimon D. Homologous pairing in stretched supercoiled DNA Proc. Nat. Acad. Sci. USA 1998 95, N 18:10579–10583.
[52] Bancaud A., Conde e Silva N., Barbi M., Wagner G., Allemand J. F., Mozziconacci J., Lavelle C., Croquette V., Victor J.-M., Prunell A., Viovy J.-L. Structural plasticity of single chromatin fibers revealed by torsional manipulation Nat. Struct. Mol. Biol 2006 13, N 5:444–450.
[53] Bancaud A., Wagner G., Conde e Silva N., Lavelle C., Wong H., Mozziconacci J., Barbi M., Sivolob A., Le Cam E., Mouawad L., Viovy J.-L., Victor J.-M., Prunell A. Nucleosome chiral transition under positive torsional stress in single chromatin fibers Mol. Cell 2007 27, N 1:135–147.
[54] Benedict R. C., Moudrianakis E. N., Ackers G. K. Interactions of the nucleosomal core histones: a calorimetric study of octamer assembly. Biochemistry. 1984 23, N 6:1214–1218.
[55] Liu L. F., Wang J. C. Supercoiling of the DNA template during transcription Proc. Nat. Acad. Sci. USA 1987 84, N 20:7024–7027.
[56] Tsao Y.-P., Wu H.-Y., Liu L. F. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies Cell 1989 56, N 1:111–118.
[57] Rahmouni A. R., Wells R. D. Direct evidence for the effect of transcription on local DNA supercoiling in vivo J. Mol. Biol 1992 223, N 1:131–144.
[58] Kramer P. R., Sinden R. R. Measurement of unrestrained negative supercoiling and topological domain size in living human cells Biochemistry 1997 36, N 11:3151–3158.
[59] Wang Z., Droge P. Long-range effects in a supercoiled DNA domain generated by transcription in vitro J. Mol. Biol 1997 271, N 4:499–510.
[60] Kouzine F., Sanford S., Elisha-Feil Z., Levens D. The functional response of upstream DNA to dynamic supercoiling in vivo Nat. Struct. Mol. Biol 2008 15, N 2:146–154.
[61] Wang J. C. Cellular roles of DNA topoisomerases: a molecular perspective Nat. Rev. Mol. Cell Biol 2002 3, N 6 P. 430–440.
[62] Salceda J., Fernandez X., Roca J. Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA EMBO J 2006 25, N 11:2575–2583.
[63] Harada Y., Ohara O., Takatsuki A., Itoh H., Shimamoto N., Kinosita K. Direct observation of DNA rotation during transcription by Escherichia coli RNA polymerase Nature 2001 409, N 6816:113–115.