Distinct Trends of DNA Methylation Patterning in the Innate and Adaptive Immune Systems

Cell Reports

Volumn 17, Issue 8, 2016, Pages 2101-2111

  Schuyler, Ronald P ^a,b   Merkel, Angelika ^a,b   Raineri, Emanuele ^a,b   Altucci, Lucia ^c   Vellenga, Edo ^d   Martens, Joost H A ^e   Pourfarzad, Farzin ^f   Kuijpers, Taco W ^f   Burden, Frances ^g,h   Farrow, Samantha ^g,h   Downes, Kate ^g,h   Ouwehand, Willem H ^g,h,i   Clarke, Laura ^j   Datta, Avik ^j   Lowy, Ernesto ^j   Flicek, Paul ^j   Frontini, Mattia ^g,h   Stunnenberg, Hendrik G ^e   Martín Subero, José I ^k   Gut, Ivo ^a,b   Heath, Simon ^a,b   more..

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h NHS BLOOD AND TRANSPLANT   (United Kingdom)

ⁱ WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^j EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^k UNIVERSITY OF BARCELONA   (Spain)

more..

Author keywords

BLUEPRINT; CTCF; DNA methylation; epigenetics; hematopoiesis; nucleosomes; whole genome bisulfite sequencing

Indexed keywords

TRANSCRIPTION FACTOR CTCF; CYTIDYLYL-3'-5'-GUANOSINE; DINUCLEOSIDE PHOSPHATE;

ADAPTIVE IMMUNITY; ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL ACTIVATION; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; DNA METHYLATION; EFFECTOR CELL; EPIGENETICS; HUMAN; HUMAN CELL; INNATE IMMUNITY; LYMPHOCYTE; MACROPHAGE; MONOCYTE; NEUTROPHIL; NUCLEOSOME; POLARIZATION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; T LYMPHOCYTE; BONE MARROW CELL; EXON; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE;

ADAPTIVE IMMUNITY; B-LYMPHOCYTES; BASE SEQUENCE; BINDING SITES; CCCTC-BINDING FACTOR; DINUCLEOSIDE PHOSPHATES; DNA METHYLATION; EXONS; HUMANS; IMMUNITY, INNATE; LYMPHOCYTES; MYELOID CELLS; NUCLEOSOMES;

EID: 85003874995     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.10.054     Document Type: Article

References (73)

1. Benjamini, Y., Yekutieli, D., The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29 (2001), 1165–1188.
2. Bock, C., Beerman, I., Lien, W.H., Smith, Z.D., Gu, H., Boyle, P., Gnirke, A., Fuchs, E., Rossi, D.J., Meissner, A., DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol. Cell 47 (2012), 633–647.
3. Booth, M.J., Branco, M.R., Ficz, G., Oxley, D., Krueger, F., Reik, W., Balasubramanian, S., Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336 (2012), 934–937.
4. Bröske, A.M., Vockentanz, L., Kharazi, S., Huska, M.R., Mancini, E., Scheller, M., Kuhl, C., Enns, A., Prinz, M., Jaenisch, R., et al. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat. Genet. 41 (2009), 1207–1215.
5. Cedar, H., Bergman, Y., Epigenetics of haematopoietic cell development. Nat. Rev. Immunol. 11 (2011), 478–488.
6. Chen, H., Tian, Y., Shu, W., Bo, X., Wang, S., Comprehensive identification and annotation of cell type-specific and ubiquitous CTCF-binding sites in the human genome. PLoS ONE, 7, 2012, e41374.
7. Chodavarapu, R.K., Feng, S., Bernatavichute, Y.V., Chen, P.Y., Stroud, H., Yu, Y., Hetzel, J.A., Kuo, F., Kim, J., Cokus, S.J., et al. Relationship between nucleosome positioning and DNA methylation. Nature 466 (2010), 388–392.
8. Cruickshanks, H.A., McBryan, T., Nelson, D.M., Vanderkraats, N.D., Shah, P.P., van Tuyn, J., Singh Rai, T., Brock, C., Donahue, G., Dunican, D.S., et al. Senescent cells harbour features of the cancer epigenome. Nat. Cell Biol. 15 (2013), 1495–1506.
9. Du, J., Johnson, L.M., Jacobsen, S.E., Patel, D.J., DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16 (2015), 519–532.
10. Farh, K.K., Marson, A., Zhu, J., Kleinewietfeld, M., Housley, W.J., Beik, S., Shoresh, N., Whitton, H., Ryan, R.J.H., Shishkin, A.A., et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 518 (2015), 337–343.
11. Felle, M., Hoffmeister, H., Rothammer, J., Fuchs, A., Exler, J.H., Längst, G., Nucleosomes protect DNA from DNA methylation in vivo and in vitro. Nucleic Acids Res. 39 (2011), 6956–6969.
12. Flavahan, W.A., Drier, Y., Liau, B.B., Gillespie, S.M., Venteicher, A.S., Stemmer-Rachamimov, A.O., Suvà, M.L., Bernstein, B.E., Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature 529 (2016), 110–114.
13. Fu, Y., Sinha, M., Peterson, C.L., Weng, Z., The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet., 4, 2008, e1000138.
14. Gaffney, D.J., McVicker, G., Pai, A.A., Fondufe-Mittendorf, Y.N., Lewellen, N., Michelini, K., Widom, J., Gilad, Y., Pritchard, J.K., Controls of nucleosome positioning in the human genome. PLoS Genet., 8, 2012, e1003036.
15. Guo, X., Wang, L., Li, J., Ding, Z., Xiao, J., Yin, X., He, S., Shi, P., Dong, L., Li, G., et al. Structural insight into autoinhibition and histone H3-induced activation of DNMT3A. Nature 517 (2015), 640–644.
16. Hansen, K.D., Sabunciyan, S., Langmead, B., Nagy, N., Curley, R., Klein, G., Klein, E., Salamon, D., Feinberg, A.P., Large-scale hypomethylated blocks associated with Epstein-Barr virus-induced B-cell immortalization. Genome Res. 24 (2014), 177–184.
17. He, Y., Ecker, J.R., Non-CG methylation in the human genome. Annu. Rev. Genomics Hum. Genet. 16 (2015), 55–77.
18. Heyn, H., Moran, S., Esteller, M., Aberrant DNA methylation profiles in the premature aging disorders Hutchinson-Gilford Progeria and Werner syndrome. Epigenetics 8 (2013), 28–33.
19. Hodges, E., Molaro, A., Dos Santos, C.O., Thekkat, P., Song, Q., Uren, P.J., Park, J., Butler, J., Rafii, S., McCombie, W.R., et al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol. Cell 44 (2011), 17–28.
20. Huff, J.T., Zilberman, D., Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes. Cell 156 (2014), 1286–1297.
21. Ichiyanagi, T., Ichiyanagi, K., Miyake, M., Sasaki, H., Accumulation and loss of asymmetric non-CpG methylation during male germ-cell development. Nucleic Acids Res. 41 (2013), 738–745.
22. Ito, Y., Nativio, R., Murrell, A., Induced DNA demethylation can reshape chromatin topology at the IGF2-H19 locus. Nucleic Acids Res. 41 (2013), 5290–5302.
23. Jasielec, J., Saloura, V., Godley, L.A., The mechanistic role of DNA methylation in myeloid leukemogenesis. Leukemia 28 (2014), 1765–1773.
24. Ji, H., Ehrlich, L.I., Seita, J., Murakami, P., Doi, A., Lindau, P., Lee, H., Aryee, M.J., Irizarry, R.A., Kim, K., et al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467 (2010), 338–342.
25. Jia, D., Jurkowska, R.Z., Zhang, X., Jeltsch, A., Cheng, X., Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449 (2007), 248–251.
26. Jimenez-Useche, I., Ke, J., Tian, Y., Shim, D., Howell, S.C., Qiu, X., Yuan, C., DNA methylation regulated nucleosome dynamics. Sci. Rep., 3, 2013, 2121.
27. Jin, B., Ernst, J., Tiedemann, R.L., Xu, H., Sureshchandra, S., Kellis, M., Dalton, S., Liu, C., Choi, J.-H., Robertson, K.D., Linking DNA methyltransferases to epigenetic marks and nucleosome structure genome-wide in human tumor cells. Cell Rep. 2 (2012), 1411–1424.
28. Jose, L., Ramachandran, R., Bhagavat, R., Gomez, R.L., Chandran, A., Raghunandanan, S., Omkumar, R.V., Chandra, N., Mundayoor, S., Kumar, R.A., Hypothetical protein Rv3423.1 of Mycobacterium tuberculosis is a histone acetyltransferase. FEBS J. 283 (2016), 265–281.
29. Jurkowska, R.Z., Jurkowski, T.P., Jeltsch, A., Structure and function of mammalian DNA methyltransferases. ChemBioChem 12 (2011), 206–222.
30. Kelly, T.K., Liu, Y., Lay, F.D., Liang, G., Berman, B.P., Jones, P.A., Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules. Genome Res. 22 (2012), 2497–2506.
31. Khare, T., Pai, S., Koncevicius, K., Pal, M., Kriukiene, E., Liutkeviciute, Z., Irimia, M., Jia, P., Ptak, C., Xia, M., et al. 5-hmC in the brain is abundant in synaptic genes and shows differences at the exon-intron boundary. Nat. Struct. Mol. Biol. 19 (2012), 1037–1043.
32. Kondilis-Mangum, H.D., Wade, P.A., Epigenetics and the adaptive immune response. Mol. Aspects Med. 34 (2013), 813–825.
33. Kulis, M., Heath, S., Bibikova, M., Queirós, A.C., Navarro, A., Clot, G., Martínez-Trillos, A., Castellano, G., Brun-Heath, I., Pinyol, M., et al. Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat. Genet. 44 (2012), 1236–1242.
34. Kulis, M., Merkel, A., Heath, S., Queirós, A.C., Schuyler, R.P., Castellano, G., Beekman, R., Raineri, E., Esteve, A., Clot, G., et al. Whole-genome fingerprint of the DNA methylome during human B cell differentiation. Nat. Genet. 47 (2015), 746–756.
35. Li, Y., Huang, W., Niu, L., Umbach, D.M., Covo, S., Li, L., Characterization of constitutive CTCF/cohesin loci: a possible role in establishing topological domains in mammalian genomes. BMC Genomics, 14, 2013, 553.
36. 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., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462 (2009), 315–322.
37. Lister, R., Mukamel, E.A., Nery, J.R., Urich, M., Puddifoot, C.A., Johnson, N.D., Lucero, J., Huang, Y., Dwork, A.J., Schultz, M.D., et al. Global epigenomic reconfiguration during mammalian brain development. Science, 341, 2013, 1237905.
38. Luperchio, T.R., Wong, X., Reddy, K.L., Genome regulation at the peripheral zone: lamina associated domains in development and disease. Curr. Opin. Genet. Dev. 25 (2014), 50–61.
39. Mammana, A., Vingron, M., Chung, H.-R., Inferring nucleosome positions with their histone mark annotation from ChIP data. Bioinformatics 29 (2013), 2547–2554.
40. Marco-Sola, S., Sammeth, M., Guigó, R., Ribeca, P., The GEM mapper: fast, accurate and versatile alignment by filtration. Nat. Methods 9 (2012), 1185–1188.
41. Mueller-Planitz, F., Klinker, H., Becker, P.B., Nucleosome sliding mechanisms: new twists in a looped history. Nat. Struct. Mol. Biol. 20 (2013), 1026–1032.
42. Ong, C.-T., Corces, V.G., CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 15 (2014), 234–246.
43. Pacis, A., Tailleux, L., Morin, A.M., Lambourne, J., MacIsaac, J.L., Yotova, V., Dumaine, A., Danckaert, A., Luca, F., Grenier, J.-C., et al. Bacterial infection remodels the DNA methylation landscape of human dendritic cells. Genome Res. 25 (2015), 1801–1811.
44. Percival, D.B., Walden, A.T., Wavelet Methods for Time Series Analysis. 2006, Cambridge University Press.
45. Pérez, A., Castellazzi, C.L., Battistini, F., Collinet, K., Flores, O., Deniz, O., Ruiz, M.L., Torrents, D., Eritja, R., Soler-López, M., Orozco, M., Impact of methylation on the physical properties of DNA. Biophys. J. 102 (2012), 2140–2148.
46. Peric-Hupkes, D., Meuleman, W., Pagie, L., Bruggeman, S.W.M., Solovei, I., Brugman, W., Gräf, S., Flicek, P., Kerkhoven, R.M., van Lohuizen, M., et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38 (2010), 603–613.
47. Portela, A., Liz, J., Nogales, V., Setién, F., Villanueva, A., Esteller, M., DNA methylation determines nucleosome occupancy in the 5′-CpG islands of tumor suppressor genes. Oncogene 32 (2013), 5421–5428.
48. R Development Core Team. R: A Language and Environment for Statistical Computing. 2014, the R Foundation for Statistical Computing, Vienna, Austria.
49. Rajavelu, A., Jurkowska, R.Z., Fritz, J., Jeltsch, A., Function and disruption of DNA methyltransferase 3a cooperative DNA binding and nucleoprotein filament formation. Nucleic Acids Res. 40 (2012), 569–580.
50. Ramsahoye, B.H., Biniszkiewicz, D., Lyko, F., Clark, V., Bird, A.P., Jaenisch, R., Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl. Acad. Sci. USA 97 (2000), 5237–5242.
51. Raynal, N.J.-M., Si, J., Taby, R.F., Gharibyan, V., Ahmed, S., Jelinek, J., Estécio, M.R.H., Issa, J.-P.J., DNA methylation does not stably lock gene expression but instead serves as a molecular mark for gene silencing memory. Cancer Res. 72 (2012), 1170–1181.
52. Reddy, K.L., Feinberg, A.P., Higher order chromatin organization in cancer. Semin. Cancer Biol. 23 (2013), 109–115.
53. Russ, B.E., Prier, J.E., Rao, S., Turner, S.J., T cell immunity as a tool for studying epigenetic regulation of cellular differentiation. Front. Genet., 4, 2013, 218.
54. Schultz, M.D., He, Y., Whitaker, J.W., Hariharan, M., Mukamel, E.A., Leung, D., Rajagopal, N., Nery, J.R., Urich, M.A., Chen, H., et al. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature 523 (2015), 212–216.
55. Sellars, M., Huh, J.R., Day, K., Issuree, P.D., Galan, C., Gobeil, S., Absher, D., Green, M.R., Littman, D.R., Regulation of DNA methylation dictates Cd4 expression during the development of helper and cytotoxic T cell lineages. Nat. Immunol. 16 (2015), 746–754.
56. Sharma, S., De Carvalho, D.D., Jeong, S., Jones, P.A., Liang, G., Nucleosomes containing methylated DNA stabilize DNA methyltransferases 3A/3B and ensure faithful epigenetic inheritance. PLoS Genet., 7, 2011, e1001286.
57. Sharma, G., Upadhyay, S., Srilalitha, M., Nandicoori, V.K., Khosla, S., The interaction of mycobacterial protein Rv2966c with host chromatin is mediated through non-CpG methylation and histone H3/H4 binding. Nucleic Acids Res. 43 (2015), 3922–3937.
58. Shen, H., Laird, P.W., Interplay between the cancer genome and epigenome. Cell 153 (2013), 38–55.
59. Shih, A.H., Abdel-Wahab, O., Patel, J.P., Levine, R.L., The role of mutations in epigenetic regulators in myeloid malignancies. Nat. Rev. Cancer 12 (2012), 599–612.
60. Sinclair, D.A., Oberdoerffer, P., The ageing epigenome: damaged beyond repair?. Ageing Res. Rev. 8 (2009), 189–198.
61. Smith, Z.D., Meissner, A., DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14 (2013), 204–220.
62. Takeshima, H., Suetake, I., Tajima, S., Mouse Dnmt3a preferentially methylates linker DNA and is inhibited by histone H1. J. Mol. Biol. 383 (2008), 810–821.
63. Teif, V.B., Beshnova, D.A., Vainshtein, Y., Marth, C., Mallm, J.-P., Höfer, T., Rippe, K., Nucleosome repositioning links DNA (de)methylation and differential CTCF binding during stem cell development. Genome Res. 24 (2014), 1285–1295.
64. Tiedemann, R.L., Putiri, E.L., Lee, J.H., Hlady, R.A., Kashiwagi, K., Ordog, T., Zhang, Z., Liu, C., Choi, J.H., Robertson, K.D., Acute depletion redefines the division of labor among DNA methyltransferases in methylating the human genome. Cell Rep. 9 (2014), 1554–1566.
65. Tsagaratou, A., Äijö, T., Lio, C.-W.J., Yue, X., Huang, Y., Jacobsen, S.E., Lähdesmäki, H., Rao, A., Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proc. Natl. Acad. Sci. USA 111 (2014), E3306–E3315.
66. Valouev, A., Johnson, S.M., Boyd, S.D., Smith, C.L., Fire, A.Z., Sidow, A., Determinants of nucleosome organization in primary human cells. Nature 474 (2011), 516–520.
67. Varley, K.E., Gertz, J., Bowling, K.M., Parker, S.L., Reddy, T.E., Pauli-Behn, F., Cross, M.K., Williams, B.A., Stamatoyannopoulos, J.A., Crawford, G.E., et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res. 23 (2013), 555–567.
68. Vlachogiannis, G., Niederhuth, C.E., Tuna, S., Stathopoulou, A., Viiri, K., de Rooij, D.G., Jenner, R.G., Schmitz, R.J., Ooi, S.K.T., The Dnmt3L ADD domain controls cytosine methylation establishment during spermatogenesis. Cell Rep. 10 (2015), 944–956.
69. Wang, H., Maurano, M.T., Qu, H., Varley, K.E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22 (2012), 1680–1688.
70. Yu, M., Hon, G.C., Szulwach, K.E., Song, C.X., Zhang, L., Kim, A., Li, X., Dai, Q., Shen, Y., Park, B., et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149 (2012), 1368–1380.
71. Zemach, A., McDaniel, I.E., Silva, P., Zilberman, D., Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328 (2010), 916–919.
72. Zhang, Y., Jurkowska, R., Soeroes, S., Rajavelu, A., Dhayalan, A., Bock, I., Rathert, P., Brandt, O., Reinhardt, R., Fischle, W., Jeltsch, A., Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res. 38 (2010), 4246–4253.
73. Ziller, M.J., Müller, F., Liao, J., Zhang, Y., Gu, H., Bock, C., Boyle, P., Epstein, C.B., Bernstein, B.E., Lengauer, T., et al. Genomic distribution and inter-sample variation of non-CpG methylation across human cell types. PLoS Genet., 7, 2011, e1002389.