Hydroxymethylation of DNA influences nucleosomal conformation and stability in vitro

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 11, 2014, Pages 1323-1329

  Mendonca, Agnes ^a   Chang, En Hyung ^a   Liu, Wenjie ^a   Yuan, Chongli ^a  

^a Purdue University   (United States)

Author keywords

Chromatin; DNA hydroxymethylation; FRET; Nucleosome

Indexed keywords

CYTOSINE; DIMER; DNA; DNA FRAGMENT; HISTONE; CHROMATIN; NUCLEOSOME; PROTEIN BINDING;

5 HYDROXYMETHYLATION; ARTICLE; BINDING AFFINITY; BREAST IMPLANT; CONTROLLED STUDY; CYTOSINE METHYLATION; DNA METHYLATION; ENERGY TRANSFER; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE CONTROL; IN VITRO STUDY; METHYLATION; NUCLEOSOME; CHEMISTRY; CHROMATIN; CONFORMATION; DNA PACKAGING; HUMAN; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN STABILITY;

CHROMATIN; DNA; DNA METHYLATION; DNA PACKAGING; HISTONES; HUMANS; IN VITRO TECHNIQUES; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY;

EID: 84908679499     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.09.014     Document Type: Article

References (55)

1. Jaenisch R., Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 2003, 33:245-254. 10.1038/ng1089.
2. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16:6-21. 10.1101/gad.947102.
3. Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 2012, 13:484-492. 10.1038/nrg3230.
4. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J. 1998, 17:4905-4908. 10.1093/emboj/17.17.4905.
5. Bhutani N., Burns D.M., Blau H.M. DNA demethylation dynamics. Cell 2011, 146:866-872. 10.1016/j.cell.2011.08.042.
6. Jullien J., Pasque V., Halley-Stott R.P., Miyamoto K., Gurdon J.B. Mechanisms of nuclear reprogramming by eggs and oocytes: a deterministic process?. Nat. Rev. Mol. Cell Biol. 2011, 12:453-459. 10.1038/nrm3140.
7. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 2010, 11:607-620. 10.1038/nrm2950.
8. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935. 10.1126/science.1170116.
9. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930. 10.1126/science.1169786.
10. Guo J.U., Su Y., Zhong C., Ming G., Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011, 145:423-434. 10.1016/j.cell.2011.03.022.
11. Wossidlo M., Nakamura T., Lepikhov K., Marques C.J., Zakhartchenko V., Boiani M., et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2011, 2:241. 10.1038/ncomms1240.
12. Wu H., Zhang Y. Tet1 and 5-hydroxymethylation: a genome-wide view in mouse embryonic stem cells. Cell Cycle 2011, 10:2428-2436. 10.4161/cc.10.15.16930.
13. Yildirim O., Li R., Hung J.-H., Chen P.B., Dong X., Ee L.-S., et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 2011, 147:1498-1510. 10.1016/j.cell.2011.11.054.
14. Ficz G., Branco M.R., Seisenberger S., Santos F., Krueger F., Hore T.A., et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011, 473:398-402. 10.1038/nature10008.
15. Globisch D., Münzel M., Müller M., Michalakis S., Wagner M., Koch S., et al. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS ONE 2010, 5:e15367. 10.1371/journal.pone.0015367.
16. Wu H., D'Alessio A.C., Ito S., Wang Z., Cui K., Zhao K., et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 2011, 25:679-684. 10.1101/gad.2036011.
17. Shen L., Zhang Y. 5-Hydroxymethylcytosine: generation, fate, and genomic distribution. Curr. Opin. Cell Biol. 2013, 10.1016/j.ceb.2013.02.017.
18. Yu M., Hon G.C., Szulwach K.E., Song C.-X., Zhang L., Kim A., et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 2012, 149:1368-1380. 10.1016/j.cell.2012.04.027.
19. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389:251-260.
20. Choy J.S., Wei S., Lee J.Y., Tan S., Chu S., Lee T.-H. DNA methylation increases nucleosome compaction and rigidity. J. Am. Chem. Soc. 2010, 132:1782-1783. 10.1021/ja910264z.
21. Collings C.K., Waddell P.J., Anderson J.N. Effects of DNA methylation on nucleosome stability. Nucleic Acids Res. 2013, 41:2918-2931. 10.1093/nar/gks893.
22. Jimenez-Useche I., Ke J., Tian Y., Shim D., Howell S.C., Qiu X., et al. DNA methylation regulated nucleosome dynamics. Sci. Rep. 2013, 3. 10.1038/srep02121.
23. Wyrick J.J., Kyriss M.N.M., Davis W.B. Ascending the nucleosome face: recognition and function of structured domains in the histone H2A-H2B dimer. Biochim. Biophys. Acta Gene Regul. Mech. 2012, 1819:892-901. 10.1016/j.bbagrm.2012.04.001.
24. Zentner G.E., Henikoff S. Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 2013, 20:259-266. 10.1038/nsmb.2470.
25. Bettecken T., Frenkel Z.M., Trifonov E.N. Human nucleosomes: special role of CG dinucleotides and Alu-nucleosomes. BMC Genomics 2011, 12:273. 10.1186/1471-2164-12-273.
26. Chodavarapu R.K., Feng S., Bernatavichute Y.V., Chen P.-Y., Stroud H., Yu Y., et al. Relationship between nucleosome positioning and DNA methylation. Nature 2010, 466:388-392. 10.1038/nature09147.
27. McClelland M., Ivarie R. Asymmetrical distribution of CpG in an "average" mammalian gene. Nucleic Acids Res. 1982, 10:7865-7877. 10.1093/nar/10.23.7865.
28. Lowary P.T., Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 1998, 276:19-42. 10.1006/jmbi.1997.1494.
29. Thåström A., Lowary P.T., Widlund H.R., Cao H., Kubista M., Widom J. Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol. 1999, 288:213-229. 10.1006/jmbi.1999.2686.
30. Richmond T.J., Davey C.A. The structure of DNA in the nucleosome core. Nature 2003, 423:145-150. 10.1038/nature01595.
31. Jimenez-Useche I., Yuan C. The effect of DNA CpG methylation on the dynamic conformation of a nucleosome. Biophys. J. 2012, 103:2502-2512. 10.1016/j.bpj.2012.11.012.
32. North J.A., Shimko J.C., Javaid S., Mooney A.M., Shoffner M.A., Rose S.D., et al. Regulation of the nucleosome unwrapping rate controls DNA accessibility. Nucleic Acids Res. 2012, 40:10215-10227. 10.1093/nar/gks747.
33. Thåström A., Lowary P., Widom J. Measurement of histone-DNA interaction free energy in nucleosomes. Methods 2004, 33:33-44. 10.1016/j.ymeth.2003.10.018.
34. Henikoff S. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 2008, 9:15-26. 10.1038/nrg2206.
35. Pérez A., Castellazzi C.L., Battistini F., Collinet K., Flores O., Deniz O., et al. Impact of methylation on the physical properties of DNA. Biophys. J. 2012, 102:2140-2148. 10.1016/j.bpj.2012.03.056.
36. Kaur P., Plochberger B., Costa P., Cope S.M., Vaiana S.M., Lindsay S. Hydrophobicity of methylated DNA as a possible mechanism for gene silencing. Phys. Biol. 2012, 9:065001. 10.1088/1478-3975/9/6/065001.
37. Böhm V., Hieb A.R., Andrews A.J., Gansen A., Rocker A., Tóth K., et al. Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res. 2011, 39:3093-3102. 10.1093/nar/gkq1279.
38. Tóth K., Böhm V., Sellmann C., Danner M., Hanne J., Berg M., et al. Histone- and DNA sequence-dependent stability of nucleosomes studied by single-pair FRET. Cytometry A 2013, 83:839-846. 10.1002/cyto.a.22320.
39. Gansen A., Tóth K., Schwarz N., Langowski J. Structural variability of nucleosomes detected by single-pair Förster resonance energy transfer: histone acetylation, sequence variation, and salt effects. J. Phys. Chem. B 2009, 113:2604-2613. 10.1021/jp7114737.
40. Alexandrov B.S., Fukuyo Y., Lange M., Horikoshi N., Gelev V., Rasmussen K.Ø., et al. DNA breathing dynamics distinguish binding from nonbinding consensus sites for transcription factor YY1 in cells. Nucleic Acids Res. 2012, 40:10116-10123. 10.1093/nar/gks758.
41. Choi C.H., Kalosakas G., Rasmussen K.Ø., Hiromura M., Bishop A.R., Usheva A. DNA dynamically directs its own transcription initiation. Nucleic Acids Res. 2004, 32:1584-1590. 10.1093/nar/gkh335.
42. Li G., Widom J. Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. 2004, 11:763-769. 10.1038/nsmb801.
43. Li G., Levitus M., Bustamante C., Widom J. Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 2005, 12:46-53. 10.1038/nsmb869.
44. Koopmans W.J.A., Brehm A., Logie C., Schmidt T., van Noort J. Single-pair FRET microscopy reveals mononucleosome dynamics. J. Fluoresc. 2007, 17:785-795. 10.1007/s10895-007-0218-9.
45. van der Heijden T., van Vugt J.J.F.A., Logie C., van Noort J. Sequence-based prediction of single nucleosome positioning and genome-wide nucleosome occupancy. Proc. Natl. Acad. Sci. 2012, 109:E2514-E2522. 10.1073/pnas.1205659109.
46. Prinsen P., Schiessel H. Nucleosome stability and accessibility of its DNA to proteins. Biochimie 2010, 92:1722-1728. 10.1016/j.biochi.2010.08.008.
47. Lee J.Y., Lee T.-H. Effects of DNA methylation on the structure of nucleosomes. J. Am. Chem. Soc. 2012, 134:173-175. 10.1021/ja210273w.
48. Kelbauskas L., Chan N., Bash R., DeBartolo P., Sun J., Woodbury N., et al. Sequence-dependent variations associated with H2A/H2B depletion of nucleosomes. Biophys. J. 2008, 94:147-158. 10.1529/biophysj.107.111906.
49. Anderson J.D., Widom J. Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 2000, 296:979-987. 10.1006/jmbi.2000.3531.
50. Jimenez-Useche I., Shim D., Yu J., Yuan C. Unmethylated and methylated CpG dinucleotides distinctively regulate the physical properties of DNA. Biopolymers 2013, 10.1002/bip.22411.
51. Nathan D., Crothers D.M. Bending and flexibility of methylated and unmethylated EcoRI DNA. J. Mol. Biol. 2002, 316:7-17. 10.1006/jmbi.2001.5247.
52. Wanunu M., Cohen-Karni D., Johnson R.R., Fields L., Benner J., Peterman N., et al. Discrimination of methylcytosine from hydroxymethylcytosine in DNA molecules. J. Am. Chem. Soc. 2011, 133:486-492. 10.1021/ja107836t.
53. Derreumaux S., Chaoui M., Tevanian G., Fermandjian S. Impact of CpG methylation on structure, dynamics and solvation of cAMP DNA responsive element. Nucleic Acids Res. 2001, 29:2314-2326. 10.1093/nar/29.11.2314.
54. Andrews A.J., Chen X., Zevin A., Stargell L.A., Luger K. The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell 2010, 37:834-842. 10.1016/j.molcel.2010.01.037.
55. Pastor W.A., Pape U.J., Huang Y., Henderson H.R., Lister R., Ko M., et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011, 473:394-397. 10.1038/nature10102.