Biopolym. Cell. 2010; 26(5):351-359.
http://dx.doi.org/10.7124/bc.000169
Огляди
Конформаційна рухливість нуклеосом в експериментах з індивідуальними хроматиновими фібрилами
1Сиволоб А. В.
  1. Київський національний університет імені Тараса Шевченка
    вул. Володимирська 64, Київ, Україна, 01601

Abstract

Дослідження нуклеосомної організації хроматину відіграє все більшу роль у розумінні механізмів регуляції генетичної активності. У представленому огляді описано результати вивчення конформаційної рухливості нуклеосом, отримані в експериментах з магнітним пінцетом – приладом, за допомогою якого можна індукувати торсійні деформації в олігонуклеосомних фібрилах, реконструйованих на індивідуальних молекулах ДНК. Такий підхід дозволяє виявити нову структурну форму нуклеосоми – реверсому, у складі якої ДНК формує праву суперспіраль на поверхні перебудованого октамеру гістонів. Обговорюються молекулярні механізми та біологічне значення структурної рухливості нуклеосом.
Keywords: нуклеосома, надспіралізація ДНК, хроматинова фібрила, конформаційна рухливість
Повний текст: (PDF, російською) (PDF, англійською)

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.