Methylated DNA is over-represented in whole-genome bisulfite sequencing data

Frontiers in Genetics

Volumn 5, Issue SEP, 2014, Pages

  Ji, Lexiang ^a,b   Sasaki, Takahiko ^b   Sun, Xiaoxiao ^b   Ma, Ping ^b   Lewis, Zachary A ^b   Schmitz, Robert J ^a  

^a University of Georgia   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BISULFITE;

AMINO ACID SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA BASE COMPOSITION; DNA METHYLATION; GENE SEQUENCE; NEUROSPORA; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION;

EID: 84917726948     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2014.00341     Document Type: Article

References (54)

1. Aird, D., Ross, M.G., Chen, W.S., Danielsson, M., Fennell, T., Russ, C., Jaffe, D.B., Nusbaum, C., and Gnirke, A. (2011). Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries. Genome Biol 12, R18. doi: 10.1186/gb-2011-12-2-r8.
2. Arriola, E., Lambros, M.B., Jones, 1 , Dexter, T., Mackay, A., Tan, D.S., Tamber, N., Fenwick, K., Ashworth, A., Dowsett, M., and Reis-Filho, J.S. (2007). Evaluation of Phi29-based whole-genome amplification for microarray-based comparative genomic hybridisation. Lab Invest 87, 75-83. doi: 10.1038/labinvest.3700495.
3. Becker, C., Hagmann, J., Muller, J., Koenig, D., Stegle, O., Borgwardt, K., and Weigel, D. (2011). Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245-249. doi: nature10555 [pii] 10.1038/nature10555.
4. Benjamini, Y., and Speed, T.P. (2012). Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res 40, e72. doi: 10.1093/nar/gks001.
5. Bernstein, B.E., Stamatoyannopoulos, J.A., Costello, J.F., Ren, B., Milosavljevic, A., Meissner, A., Kellis, M., Marra, M.A., Beaudet, A.L., Ecker, J.R., Farnham, P.J., Hirst, M., Lander, E.S., Mikkelsen, T.S., and Thomson, J.A. (2010). The NIH Roadmap Epigenomics Mapping Consortium. Nat Biotechnol 28,1045-1048. doi: nbt1010-1045 [pii] 10.1038/nbt1010-1045.
6. Booth, M.J., Branco, M.R., Ficz, G., Oxley, D., Krueger, F., Reik, W., and Balasubramanian, S. (2012). Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336, 934- 937. doi: 10.1126/science.1220671.
7. Booth, M.J., Marsico, G., Bachman, M., and Beraldi, D. (2014). Quantitative sequencing of 5-formylcytosine in DNA at single-base resolution. Nature Chemistry. doi: 10.1038/NCHEM.1893.
8. Bredel, M., Bredel, C., Juric, D., Kim, Y., Vogel, H., Harsh, G.R., Recht, L.D., Pollack, J.R., and Sikic, B.I. (2005). Amplification of whole tumor genomes and gene-bygene mapping of genomic aberrations from limited sources of fresh-frozen and paraffin-embedded DNA. J MolDiagn 7, 171-182. doi: 10.1016/S1525-1578(10)60543-0.
9. Calarco, J.P., Borges, F., Donoghue, M.T., Van Ex, F., Jullien, P.E., Lopes, T., Gardner, R., Berger, F., Feijo, J.A., Becker, J.D., and Martienssen, R.A. (2012). Reprogramming of DNA Methylation in Pollen Guides Epigenetic Inheritance via Small RNA. Cell 151,194-205. doi: S0092-8674(12)01066-5 [pii] 10.1016/j.cell.2012.09.001.
10. Clark, S.J., Harrison, J., Paul, C.L., and Frommer, M. (1994). High sensitivity mapping of methylated cytosines. Nucleic Acids Res 22, 2990-2997.
11. Clark, S.J., Statham, A., Stirzaker, C., Molloy, P.L., and Frommer, M. (2006). DNA methylation: bisulphite modification and analysis. NatProtoc 1, 2353-2364. doi: nprot.2006.324 [pii] 10.1038/nprot.2006.324.
12. Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M., and Jacobsen, S.E. (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215-219. doi: nature06745 [pii] 10.1038/nature06745.
13. Cook, R.D., and Weisberg, S. (1982). Residuals and Influence in Regression. Chapman and Hall.
14. Creasey, K.M., Zhai, J., Borges, F., Van Ex, F., Regulski, M., Meyers, B.C., and Martienssen, R.A. (2014). miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508, 411-415. doi: 10.1038/nature13069.
15. Frommer, M., Mcdonald, L.E., Millar, D.S., Collis, C.M., Watt, F., Grigg, G.W., Molloy, P.L., and Paul, C.L. (1992). A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 89,1827-1831.
16. Gehring, M., Bubb, K.L., and Henikoff, S. (2009). Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324,1447-1451. doi: 324/5933/1447 [pii] 10.1126/science.1171609.
17. Gent, J.I., Ellis, N.A., Guo, L., Harkess, A.E., Yao, Y., Zhang, X., and Dawe, R.K. (2013). CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res 23, 628-637. doi: gr.146985.112 [pii] 10.1101/gr.146985.112.
18. Gu, H., Smith, Z.D., Bock, C., Boyle, P., Gnirke, A., and Meissner, A. (2011). Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. NatProtoc 6, 468-481. doi: nprot.2010.190 [pii] 10.1038/nprot.2010.190.
19. Hayatsu, H. (1976). Bisulfite modification of nucleic acids and their constituents. Prog Nucleic Acid Res Mol Biol 16, 75-124.
20. Hayatsu, H., Wataya, Y., Kai, K., and Iida, S. (1970). Reaction of sodium bisulfite w i th uracil, cytosine, and their derivatives. Biochemistry 9, 2858-2865.
21. Horvath, A., and Vertessy, B.G. (2010). A one-step method for quantitative determination of uracil in DNA by real-time PCR. Nucleic Acids Res 38, e196. doi: 10.1093/nar/gkq815.
22. Hsieh, T.F., Ibarra, C.A., Silva, P., Zemach, A., Eshed-Williams, L., Fischer, R.L., and Zilberman, D. (2009). Genome-wide demethylation of Arabidopsis endosperm. Science 324,1451-1454. doi: 324/5933/1451 [pii] 10.1126/science.1172417.
23. Ibarra, C.A., Feng, X., Schoft, V.K., Hsieh, T.F., Uzawa, R., Rodrigues, J.A., Zemach, A., Chumak, N., Machlicova, A., Nishimura, T., Rojas, D., Fischer, R.L., Tamaru, H., and Zilberman, D. (2012). Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337,1360-1364. doi: 10.1126/science.1224839.
24. Jiang, L., Zhang, J., Wang, J.J., Wang, L., Zhang, L., Li, G., Yang, X., Ma, X., Sun, X., Cai, J., Zhang, J., Huang, X., Yu, M., Wang, X., Liu, F., Wu, C.I., He, C., Zhang, B., Ci, W., and Liu, J. (2013). Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153, 773-784. doi: 10.1016/j.cell.2013.04.041.
25. Kobayashi, H., Sakurai, T., Miura, F., Imai, M., Mochiduki, K., Yanagisawa, E., Sakashita, A., Wakai, T., Suzuki, Y., Ito, T., Matsui, Y., and Kono, T. (2013). High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res 23, 616-627. doi: 10.1101/gr.148023.112.
26. Komori, H.K., Lamere, S.A., Torkamani, A., Hart, G.T., Kotsopoulos, S., Warner, J., Samuels, M.L., Olson, J., Head, S.R., Ordoukhanian, P., Lee, P.L., Link, D.R., and Salomon, D.R. (2011). Application of microdroplet PCR for large-scale targeted bisulfite sequencing. Genome Res 21,1738-1745. doi: 10.1101/gr.116863.110.
27. Kozarewa, I., Ning, Z., Quail, M.A., Sanders, M.J., Berriman, M., and Turner, D.J. (2009). Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat Methods 6, 291-295. doi: 10.1038/nmeth.1311.
28. Lister, R., O'malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H., and Ecker, J.R. (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523-536. doi: S0092-8674(08)00448-0 [pii] 10.1016/j.cell.2008.03.029.
29. Lister, R., Pelizzola, M., Dowen, R.H., Hawkins, R.D., Hon, G., Tonti-Filippini, J., Nery, J.R., Lee, L., Ye, Z., Ngo, Q.M., Edsall, L., Antosiewicz-Bourget, J., Stewart, R., Ruotti, V., Millar, A.H., Thomson, J.A., Ren, B., and Ecker, J.R. (2009). Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322. doi: 10.1038/nature08514.
30. Lister, R., Pelizzola, M., Kida, Y.S., Hawkins, R.D., Nery, J.R., Hon, G., Antosiewicz- Bourget, J., O'malley, R., Castanon, R., Klugman, S., Downes, M., Yu, R., Stewart, R., Ren, B., Thomson, J.A., Evans, R.M., and Ecker, J.R. (2011). Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68-73. doi: 10.1038/nature09798.
31. Mccluskey, K., Wiest, A., and Plamann, M. (2010). The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci 35,119-126.
32. Meissner, A., Gnirke, A., Bell, G.W., Ramsahoye, B., Lander, E.S., and Jaenisch, R. (2005). Reduced representation bisulfite sequencing for comparative highresolution DNA methylation analysis. Nucleic Acids Res. 33, 5868-5877. doi: 10.1093/nar/gki901.
33. Moskalev, E.A., Zavgorodnij, M.G., Majorova, S.P., Vorobjev, I.A., Jandaghi, P., Bure, I.V., and Hoheisel, J.D. (2011). Correction of PCR-bias in quantitative DNA methylation studies by means of cubic polynomial regression. Nucleic Acids Res 39, e77. doi: 10.1093/nar/gkr213.
34. Orozco, L.D., Rubbi, L., Martin, L.J., Fang, F., Hormozdiari, F., Che, N., Smith, A.D., Lusis, A.J., and Pellegrini, M. (2014). Intergenerational genomic DNA methylation patterns in mouse hybrid strains. Genome Biol 15, R68. doi: 10.1186/gb-2014-15-5-r68.
35. Ossowski, S., Schneeberger, K., Lucas-Lledo, J.I., Warthmann, N., Clark, R.M., Shaw, R.G., Weigel, D., and Lynch, M. (2010). The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92-94. doi: 327/5961/92 [pii] 10.1126/science.1180677.
36. Oyola, S.O., Otto, T.D., Gu, Y., Maslen, G., Manske, M., Campino, S., Turner, D.J., Macinnis, B., Kwiatkowski, D.P., Swerdlow, H.P., and Quail, M.A. (2012). Optimizing Illumina next-generation sequencing library preparation for extremely AT-biased genomes. BMC Genomics 13,1. doi: 10.1186/1471- 2164-13-1.
37. Sasaki, T., Lynch, K.L., Mueller, C.V., Friedman, S., Freitag, M., and Lewis, Z.A. (2014). Heterochromatin controls gammaH2A localization in Neurospora crassa. Eukaryot Cell. doi: 10.1128/EC.00117-14.
38. Schmitz, R.J., He, Y., Valdes-Lopez, O., Khan, S.M., Joshi, T., Urich, M.A., Nery, J.R., Diers, B., Xu, D., Stacey, G., and Ecker, J.R. (2013a). Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. doi: gr.152538.112 [pii] 10.1101/gr.152538.112.
39. Schmitz, R.J., Schultz, M.D., Lewsey, M.G., O'malley, R.C., Urich, M.A., Libiger, O., Schork, N.J., and Ecker, J.R. (2011). Transgenerational epigenetic instability i a source of novel methylation variants. Science 334, 369-373. doi: science.1212959 [pii] 10.1126/science.1212959.
40. Schmitz, R.J., Schultz, M.D., Urich, M.A., Nery, J.R., Pelizzola, M., Libiger, O., Alix, A., Mccosh, R.B., Chen, H., Schork, N.J., and Ecker, J.R. (2013b). Patterns of population epigenomic diversity. Nature 495,193-198. doi: nature11968 [pii] 10.1038/nature11968.
41. Schultz, M.D., Schmitz, R.J., and Ecker, J.R. (2012). "Leveling" the playing field for analyses of single-base resolution DNA methylomes. Trends Genet.
42. Seisenberger, S., Andrews, S., Krueger, F., Arand, J., Walter, J., Santos, F., Popp, C., Thienpont, B., Dean, W., and Reik, W. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48, 849-862. doi: 10.1016/j.molcel.2012.11.001.
43. Shapiro, R., Braverman, B., Louis, J.B., and Servis, R.E. (1973). Nucleic acid reactivity and conformation. II. Reaction of cytosine and uracil with sodium bisulfite. J Biol Chem 248, 4060-4064.
44. Shapiro, R., Difate, V., and Welcher, M. (1974). Deamination of cytosine derivatives by bisulfite. Mechanism of the reaction. J Am Chem Soc 96, 906-912.
45. Shaw, R.G., Byers, D.L., and Darmo, E. (2000). Spontaneous mutational effects on reproductive traits of arabidopsis thaliana. Genetics 155, 369-378.
46. Shirane, K., Toh, H., Kobayashi, H., Miura, F., Chiba, H., Ito, T., Kono, T., and Sasaki, H. (2013). Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoSGenet 9, e1003439. doi: 10.1371/journal.pgen.1003439.
47. Slotkin, R.K., Vaughn, M., Borges, F., Tanurdzic, M., Becker, J.D., Feijo, J.A., and Martienssen, R.A. (2009). Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461-472. doi: S0092- 8674(08)01644-9 [pii] 10.1016/j.cell.2008.12.038.
48. Stadler, M.B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Scholer, A., Van Nimwegen, E., Wirbelauer, C., Oakeley, E.J., Gaidatzis, D., Tiwari, V.K., and Schubeler, D. (2011). DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495. doi: 10.1038/nature10716.
49. Trapnell, C., Hendrickson, D.G., Sauvageau, M., Goff, L., Rinn, J.L., and Pachter, L. (2013). Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31, 46-53. doi: nbt.2450 [pii] 10.1038/nbt.2450.
50. Urich, M.A., Nery, J.R., Lister, R., Schmitz, R.J., and Ecker, J.R. (2014). MethylC-seq: Base resolution whole genome bisulfite sequencing library preparation. Nature Protocols in press.
51. Warnecke, P.M., Stirzaker, C., Melki, J.R., Millar, D.S., Paul, C.L., and Clark, S.J. (1997). Detection and measurement of PCR bias in quantitative methylation analysis of bisulphite-treated DNA. Nucleic Acids Res 25, 4422-4426.
52. Xie, W., Barr, C.L., Kim, A., Yue, F., Lee, A.Y., Eubanks, J., Dempster, E.L., and Ren, B. (2012). Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 148, 816-831. doi: 10.1016/j.cell.2011.12.035.
53. Yu, M., Hon, G.C., Szulwach, K.E., Song, C.X., Zhang, L., Kim, A., Li, X., Dai, Q., Shen, Y., Park, B., Min, J.H., Jin, P., Ren, B., and He, C. (2012). Base-resolution analysis 5-hydroxymethylcytosine in the mammalian genome. Cell 149,1368-1380. doi: 10.1016/j.cell.2012.04.027.
54. Zemach, A., Kim, M.Y., Silva, P., Rodrigues, J.A., Dotson, B., Brooks, M.D., and Zilberman, D. (2010). Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA 107,18729-18734. doi: 1009695107 [pii]