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RESEARCH PAPERS

Understanding the structural and dynamic consequences of DNA epigenetic modifications: Computational insights into cytosine methylation and hydroxymethylation

, , , , &
Pages 1604-1612 | Received 16 Sep 2014, Accepted 06 Nov 2014, Published online: 27 Jan 2015

References

  • Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell 2007; 128:669-81; PMID:17320505; http://dx.doi.org/10.1016/j.cell.2007.01.033
  • Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011; 333:1300-3; PMID:21778364; http://dx.doi.org/10.1126/science.1210597
  • Robertson KD. DNA methylation and chromatin - unraveling the tangled web. Oncogene 2002; 21:5361-79; PMID:12154399; http://dx.doi.org/10.1038/sj.onc.1205609
  • Soubry A, Hoyo C, Jirtle RL, Murphy SK. A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. Bioessays 2014; 36:359-71; PMID:24431278; http://dx.doi.org/10.1002/bies.201300113
  • Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005; 6:597-610; PMID:16136652; http://dx.doi.org/10.1038/nrg1655
  • Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8:286-98; PMID:17339880; http://dx.doi.org/10.1038/nrg2005
  • Bird AP. CpG-rich islands and the function of DNA methylation. Nature 1986; 321:209-13; PMID:2423876; http://dx.doi.org/10.1038/321209a0
  • Severin PMD, Zou X, Schulten K, Gaub HE. Effects of cytosine hydroxymethylation on DNA strand separation. Biophys J 2013; 104:208-15; PMID:23332073; http://dx.doi.org/10.1016/j.bpj.2012.11.013
  • Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, An J, Lamperti ED, Koh KP, Ganetzky R, et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 2010; 468:839-43; PMID:21057493; http://dx.doi.org/10.1038/nature09586
  • Wu H, Zhang Y. Tet1 and 5-hydroxymethylation: a genome-wide view in mouse embryonic stem cells. Cell Cycle 2011; 10:2428-36; PMID:21750410; http://dx.doi.org/10.4161/cc.10.15.16930
  • Clark SJ, Harrison J, Molloy PL. Sp1 binding is inhibited by (m)Cp(m)CpG methylation. Gene 1997; 195:67-71; PMID:9300822; http://dx.doi.org/10.1016/S0378-1119(97)00164-9
  • Renciuk D, Blacque O, Vorlickova M, Spingler B. Crystal structures of B-DNA dodecamer containing the epigenetic modifications 5-hydroxymethylcytosine or 5-methylcytosine. Nucleic Acids Res 2013; 41:9891-900; PMID:23963698; http://dx.doi.org/10.1093/nar/gkt738
  • Banyay M, Gräslund A. Structural effects of cytosine methylation on DNA sugar pucker studied by FTIR. J Mol Biol 2002; 324:667-76; PMID:12460569; http://dx.doi.org/10.1016/S0022-2836(02)01104-X
  • Maehigashi T, Hsiao C, Woods KK, Moulaei T, Hud NV, Williams LD. B-DNA structure is intrinsically polymorphic: even at the level of base pair positions. Nucleic Acids Res 2012; 40:3714-22; PMID:22180536; http://dx.doi.org/10.1093/nar/gkr1168
  • Travers AA. The structural basis of DNA flexibility. Philos Trans A Math Phys Eng Sci 2004; 362:1423-38; PMID:15306459; http://dx.doi.org/10.1098/rsta.2004.1390
  • Fujii S, Kono H, Takenaka S, Go N, Sarai A. Sequence-dependent DNA deformability studied using molecular dynamics simulations. Nucleic Acids Res 2007; 35:6063-74; PMID:17766249; http://dx.doi.org/10.1093/nar/gkm627
  • Portella G, Battistini F, Orozco M. Understanding the connection between epigenetic DNA methylation and nucleosome positioning from computer simulations. PLoS Comput Biol 2013; 9:e1003354; PMID:24278005; http://dx.doi.org/10.1371/journal.pcbi.1003354
  • Yang S-Y, Yang X-L, Yao L-F, Wang H-B, Sun C-K. Effect of CpG methylation on DNA binding protein: molecular dynamics simulations of the homeodomain PITX2 bound to the methylated DNA. J Mol Graph Model 2011; 29:920-7; PMID:21498098; http://dx.doi.org/10.1016/j.jmgm.2011.03.003
  • Yusufaly TI, Li Y, Olson WK. Five-Methylation of cytosine in CG:CG base-pair steps: a physicochemical mechanism for the epigenetic control of DNA nanomechanics. J Phys Chem B 2013; 117:16436-42; PMID:24313757; http://dx.doi.org/10.1021/jp409887t
  • Poater J, Swart M, Bickelhaupt FM, Fonseca Guerra C. B-DNA structure and stability: the role of hydrogen bonding, π-π stacking interactions, twist-angle, and solvation. Org Biomol Chem 2014; 12:4691-700; http://dx.doi.org/10.1039/c4ob00427b
  • Barone G, Fonseca Guerra C, Bickelhaupt FM. B-DNA structure and stability as function of nucleic acid composition: dispersion-corrected DFT study of dinucleoside monophosphate single and double strands. ChemistryOpen 2013; 2:186-93; PMID:24551565; http://dx.doi.org/10.1002/open.201300019
  • Garrec J, Patel C, Rothlisberger U, Dumont E. Insights into intrastrand cross-link lesions of DNA from QM/MM molecular dynamics simulations. J Am Chem Soc 2012; 134:2111-9; PMID:22200321; http://dx.doi.org/10.1021/ja2084042
  • Lavery R, Zakrzewska K, Beveridge D, Bishop TC, Case DA, Cheatham T, Dixit S, Jayaram B, Lankas F, Laughton C, et al. A systematic molecular dynamics study of nearest-neighbor effects on base pair and base pair step conformations and fluctuations in B-DNA. Nucleic Acids Res 2010; 38:299-313; PMID:19850719; http://dx.doi.org/10.1093/nar/gkp834
  • Pérez A, Luque FJ, Orozco M. Frontiers in molecular dynamics simulations of DNA. Acc Chem Res 2012; 45:196-205
  • Lankas F, Sponer J, Langowski J, Cheatham TE. DNA basepair step deformability inferred from molecular dynamics simulations. Biophys J 2003; 85:2872-83; PMID:14581192; http://dx.doi.org/10.1016/S0006-3495(03)74710-9
  • Dixit SB, Beveridge DL, Case DA, Cheatham TE, Giudice E, Lankas F, Lavery R, Maddocks JH, Osman R, Sklenar H, et al. Molecular dynamics simulations of the 136 unique tetranucleotide sequences of DNA oligonucleotides. II: sequence context effects on the dynamical structures of the 10 unique dinucleotide steps. Biophys J 2005; 89:3721-40; PMID:16169978; http://dx.doi.org/10.1529/biophysj.105.067397
  • Drew HR, Wing RM, Takano T, Broka C, Tanaka S, Itakura K, Dickerson RE. Structure of a B-DNA dodecamer: conformation and dynamics. Proc Natl Acad Sci USA 1981; 78:2179-83; http://dx.doi.org/10.1073/pnas.78.4.2179
  • Zou X, Ma W, Solov’yov IA, Chipot C, Schulten K. Recognition of methylated DNA through methyl-CpG binding domain proteins. Nucleic Acids Res. 2012; 40:2747-2758; PMID:22110028; http://dx.doi.org/10.1093/nar/gkr1057
  • Zgarbová M, Otyepka M, Sponer J, Lankas F, Jurečka P. Base pair fraying in molecular dynamics simulations of DNA and RNA. J Chem Theory Comput. 2014; 10:3177-89; http://dx.doi.org/10.1021/ct500120v
  • Gardiner EJ, Hunter CA, Packer MJ, Palmer DS, Willett P. Sequence-dependent DNA Structure: A database of octamer structural parameters. J Mol Biol 2003; 332:1025-35; PMID:14499606; http://dx.doi.org/10.1016/j.jmb.2003.08.006
  • Gorin AA, Zhurkin VB, Wilma K. B-DNA twisting correlates with base-pair morphology. J Mol Biol 1995; 247:34-48; PMID:7897660; http://dx.doi.org/10.1006/jmbi.1994.0120
  • Sandström K, Wärmländer S, Gräslund A, Leijon M. A-tract DNA disfavours triplex formation. J Mol Biol 2002; 315:737-48; PMID:11812143; http://dx.doi.org/10.1006/jmbi.2001.5249
  • Sandström K, Wärmländer S, Bergman J, Engqvist R, Leijon M, Gräslund A. The influence of intercalator binding on DNA triplex stability: correlation with effects on A-tract duplex structure. J Mol Recognit 2004; 17:277-85; PMID:15227636; http://dx.doi.org/10.1002/jmr.665
  • Wärmländer S, Sponer JE, Sponer J, Leijon M. The influence of the thymine C5 methyl group on spontaneous base pair breathing in DNA. J Biol Chem 2002; 277:28491-7; http://dx.doi.org/10.1074/jbc.M202989200
  • Wärmländer S, Sen A, Leijon M. Imino proton exchange in DNA catalyzed by ammonia and trimethylamine: evidence for a secondary long-lived open state of the base pair. Biochemistry 2000; 39:607-15; http://dx.doi.org/10.1021/bi991863b
  • Lankas F, Cheatham TE, Spackova N, Hobza P, Langowski J, Sponer J. Critical effect of the N2 amino group on structure, dynamics, and elasticity of DNA polypurine tracts. Biophys J 2002; 82:2592-609; PMID:11964246; http://dx.doi.org/10.1016/S0006-3495(02)75601-4
  • Hashimoto H, Horton JR, Zhang X, Cheng X. UHRF1, a modular multi-domain protein, regulates replication-coupled crosstalk between DNA methylation and histone modifications. Epigenetics 2009; 4:8-14; PMID:19077538; http://dx.doi.org/10.4161/epi.4.1.7370
  • Rechkoblit O, Delaney JC, Essigmann JM, Patel DJ. Implications for damage recognition during Dpo4-mediated mutagenic bypass of m1G and m3C lesions. Structure 2011; 19:821-32; PMID:21645853; http://dx.doi.org/10.1016/j.str.2011.03.020
  • Wojciechowski M, Czapinska H, Bochtler M. CpG underrepresentation and the bacterial CpG-specific DNA methyltransferase M.MpeI. Proc Natl Acad Sci USA 2013; 110:105-10; http://dx.doi.org/10.1073/pnas.1207986110
  • Rohs R, Jin X, West SM, Joshi R, Honig B, Mann RS. Origins of specificity in protein-DNA recognition. Annu Rev Biochem 2010; 79:233-69; PMID:20334529; http://dx.doi.org/10.1146/annurev-biochem-060408-091030
  • Parker SCJ, Hansen L, Abaan HO, Tullius TD, Margulies EH. Local DNA topography correlates with functional noncoding regions of the human genome. Science 2009; 324:389-92; PMID:19286520; http://dx.doi.org/10.1126/science.1169050
  • Ooi SKT, O’Donnell AH, Bestor TH. Mammalian cytosine methylation at a glance. J Cell Sci 2009; 122:2787-91; PMID:19657014; http://dx.doi.org/10.1242/jcs.015123
  • Araúzo-Bravo MJ, Fujii S, Kono H, Ahmad S, Sarai A. Sequence-dependent conformational energy of DNA derived from molecular dynamics simulations: toward understanding the indirect readout mechanism in protein-DNA recognition. J Am Chem Soc 2005; 127:16074-89; PMID:16287294; http://dx.doi.org/10.1021/ja053241l
  • Cheatham TE, Kollman PA. Molecular dynamics simulations highlight the structural differences among DNA:DNA, RNA:RNA, and DNA:RNA hybrid duplexes. J Am Chem Soc 1997; 119:4805-25; http://dx.doi.org/10.1021/ja963641w
  • Xiao S, Zhu H, Wang L, Liang H. DNA conformational flexibility study using phosphate backbone neutralization model. Soft Matter 2014; 10;1045-55; PMID:24983118; http://dx.doi.org/10.1039/c3sm52345d
  • Olson WK, Gorin AA, Lu XJ, Hock LM, Zhurkin VB. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc Natl Acad Sci USA 1998; 95:11163-8; http://dx.doi.org/10.1073/pnas.95.19.11163
  • Severin PMD, Zou X, Gaub HE, Schulten K. Cytosine methylation alters DNA mechanical properties. Nucleic Acids Res 2011; 39:8740-51; PMID:21775342; http://dx.doi.org/10.1093/nar/gkr578
  • Temiz NA, Donohue DE, Bacolla A, Luke BT, Collins JR. The role of methylation in the intrinsic dynamics of B- and Z-DNA. PLoS ONE 2012; 7:e35558; PMID:22530050; http://dx.doi.org/10.1371/journal.pone.0035558
  • Lankas F, Sponer J, Langowski J, Cheatham TE. DNA deformability at the base pair level. J Am Chem Soc 2004; 126:4124-5; PMID:15053599; http://dx.doi.org/10.1021/ja0390449
  • Araúzo-Bravo MJ, Fujii S, Kono H, Ahmad S, Sarai A. Sequence-dependent conformational energy of DNA derived from molecular dynamics simulations: toward understanding the indirect readout mechanism in protein-DNA recognition. J Am Chem Soc 2005; 127:16074-89; PMID:16287294; http://dx.doi.org/10.1021/ja053241l
  • Zheng G, Lu X-J, Olson WK. Web 3DNA-a web server for the analysis, reconstruction, and visualization of three-dimensional nucleic-acid structures. Nucleic Acids Res 2009; 37:W240-6; PMID:19474339; http://dx.doi.org/10.1093/nar/gkp358
  • Lu X-J, Olson WK. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res 2003; 31:5108-21; PMID:12930962; http://dx.doi.org/10.1093/nar/gkg680
  • Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, et al. Gaussian 09, Revision D.01. Gaussian, Inc., Wallingford CT, 2009.
  • Ditchfield R, Hehre WJ, Pople JA. Self-consistent molecular-orbital methods. IX. An extended Gaussian-type basis for molecular-orbital studies of organic molecules. J Chem Phys 1971; 54:724-8; http://dx.doi.org/10.1063/1.1674902
  • Hariharan PC, Pople JA. The influence of polarization functions on molecular orbital hydrogenation energies. Theoret Chim Acta 1973; 28:213-22; http://dx.doi.org/10.1007/BF00533485
  • Clark T, Chandrasekhar J, Spitznagel GNW, Schleyer PVR. Efficient diffuse function-augmented basis sets for anion calculations. III. The 3-21+G basis set for first-row elements, Li-F. J Comput Chem 1983; 4:294-301; http://dx.doi.org/10.1002/jcc.540040303
  • Cieplak P, Cornell WD, Bayly C, Kollman PA. Application of the multimolecule and multiconformational RESP methodology to biopolymers: Charge derivation for DNA, RNA, and proteins. J Comput Chem 1995; 16:1357-77; http://dx.doi.org/10.1002/jcc.540161106
  • Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, Shirts MR, Smith JC, Kasson PM, van der Spoel D, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 2013; 29:845-54; PMID:23407358; http://dx.doi.org/10.1093/bioinformatics/btt055
  • Pérez A, Marchán I, Svozil D, Sponer J, Cheatham TE, Laughton CA, Orozco M. Refinement of the AMBER force field for nucleic acids: improving the description of α/gamma conformers. Biophys J 2007; 92:3817-29; http://dx.doi.org/10.1529/biophysj.106.097782
  • Wang J, Cieplak P, Kollman PA. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Comput Chem 2000; 21:1049-74; http://dx.doi.org/10.1002/1096-987X(200009)21:12%3c1049::AID-JCC3%3e3.0.CO;2-F
  • Sponer J, Banáš P, Jurečka P, Zgarbová M, Kührová P, Havrila M, Krepl M, Stadlbauer P, Otyepka M. Molecular dynamics simulations of nucleic acids. From tetranucleotides to the ribosome. J Phys Chem Lett 2014; 5:1771-82;
  • Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983; 79:926; http://dx.doi.org/10.1063/1.445869
  • Essmann U, Perera L, Berkowitz ML. A smooth particle mesh Ewald method. J Chem Phys 1995; 103:8577; http://dx.doi.org/10.1063/1.470117
  • Bussi G, Donadio D, Parrinello M. Canonical sampling through velocity rescaling. J Chem Phys 2007; 126:014101; PMID:17212484; http://dx.doi.org/10.1063/1.2408420
  • Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984; 81:3684; http://dx.doi.org/10.1063/1.448118
  • Parrinello M. Polymorphic transitions in single crystals: A new molecular dynamics method. J Appl Phys 1981; 52:7182; http://dx.doi.org/10.1063/1.328693
  • Pérez A, Luque FJ, Orozco M. Dynamics of B-DNA on the microsecond time scale. J Am Chem Soc 2007; 129:14739-45; http://dx.doi.org/10.1021/ja0753546