Dna methylation profiling in human b cells reveals immune regulatory elements and epigenetic plasticity at alu elements during b-cell activation

Genome Research

Volumn 23, Issue 12, 2013, Pages 2030-2041

  Lai, Anne Y ^a   Mav, Deepak ^b   Shah, Ruchir ^b   Grimm, Sara A ^a   Phadke, Dhiral ^b   Hatzi, Katerina ^c   Melnick, Ari ^c   Geigerman, Cissy ^d   Sobol, Steve E ^e   Jaye, David L ^d   Wade, Paul A ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b SRA International Inc   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d Department of Pathology and Laboratory Medicine ^*  (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B;

ALU SEQUENCE; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; BINDING SITE; DNA METHYLATION; DNA TRANSCRIPTION; EPIGENETICS; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOREGULATION; MEMORY CELL; PLASMA CELL; PLASTICITY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; SECONDARY IMMUNE RESPONSE; UPREGULATION;

ADAPTIVE IMMUNITY; ALU ELEMENTS; B-LYMPHOCYTES; BINDING SITES; CELL DIFFERENTIATION; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; PLASMA CELLS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION FACTORS;

EID: 84890450749     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.155473.113     Document Type: Article

References (62)

1. Blanco-Betancourt CE, Moncla A, Milili M, Jiang YL, Viegas-Pequignot EM, Roquelaure B, Thuret I, Schiff C. 2004. Defective B-cell-negative selection and terminal differentiation in the ICF syndrome. Blood 103: 2683-2690.
2. Bock C, Beerman I, Lien WH, Smith ZD, Gu H, Boyle P, Gnirke A, Fuchs E, Rossi DJ, Meissner A. 2012. DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol Cell 47: 633- 647.
3. Broske AM, Vockentanz L, Kharazi S, Huska MR, Mancini E, Scheller M, Kuhl C, Enns A, Prinz M, Jaenisch R, et al. 2009. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat Genet 41: 1207-1215.
4. Bultman SJ, Klebig ML, Michaud EJ, Sweet HO, Davisson MT, Woychik RP. 1994. Molecular analysis of reverse mutations from nonagouti (a) to black-and-tan (at) and white-bellied agouti (Aw) reveals alternative forms of agouti transcripts. Genes Dev 8: 481-490.
5. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci 107: 21931-21936.
6. Cuddapah S, Barski A, Zhao K. 2010. Epigenomics of T cell activation, differentiation, and memory. Curr Opin Immunol 22: 341-347.
7. Delogu A, Schebesta A, Sun Q, Aschenbrenner K, Perlot T, Busslinger M. 2006. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity 24: 269-281.
8. Ding LH, Xie Y, Park S, Xiao G, Story MD. 2008. Enhanced identification and biological validation of differential gene expression via Illumina wholegenome expression arrays through the use of the model-based background correction methodology. Nucleic Acids Res 36: e58.
9. The ENCODE Project Consortium. 2011. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 9: e1001046
10. Englander EW, Howard BH. 1995. Nucleosome positioning by human Alu elements in chromatin. J Biol Chem 270: 10091-10096.
11. Englander EW,Wolffe AP, Howard BH. 1993. Nucleosome interactions with a human Alu element. Transcriptional repression and effects of template methylation. J Biol Chem 268: 19565-19573.
12. Fujita N, Jaye DL, Geigerman C, Akyildiz A, Mooney MR, Boss JM,Wade PA. 2004. MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119: 75-86.
13. Good KL, Tangye SG. 2007. Decreased expression of Kruppel-like factors in memory B cells induces the rapid response typical of secondary antibody responses. Proc Natl Acad Sci 104: 13420-13425.
14. Hansen RS, Wijmenga C, Luo P, Stanek AM, Canfield TK, Weemaes CM, Gartler SM. 1999. The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc Natl Acad Sci 96: 14412- 14417.
15. Hellmann-Blumberg U, Hintz MF, Gatewood JM, Schmid CW. 1993. Developmental differences in methylation of human Alu repeats. Mol Cell Biol 13: 4523-4530.
16. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ, Park J, Butler J, Rafii S, McCombie WR, et al. 2011. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell 44: 17-28.
17. Jaye DL, Iqbal J, Fujita N, Geigerman CM, Li S, Karanam S, Fu K, Weisenburger DD, Chan WC, Moreno CS, et al. 2007. The BCL6- associated transcriptional co-repressor,MTA3, is selectively expressed by germinal centre B cells and lymphomas of putative germinal centre derivation. J Pathol 213: 106-115.
18. Jeong S, Liang G, Sharma S, Lin JC, Choi SH, Han H, Yoo CB, Egger G, Yang AS, Jones PA. 2009. Selective anchoring of DNA methyltransferases 3A and 3B to nucleosomes containing methylated DNA. Mol Cell Biol 29: 5366-5376.
19. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P, Lee H, Aryee MJ, Irizarry RA, Kim K, et al. 2010. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467: 338-342.
20. Johnson EW, Li C. 2007. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8: 118-127.
21. Jones PA, Liang G. 2009. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 10: 805-811.
22. Kersh EN, Fitzpatrick DR, Murali-Krishna K, Shires J, Speck SH, Boss JM, Ahmed R. 2006. Rapid demethylation of the IFN-g gene occurs in memory but not naive CD8 T cells. J Immunol 176: 4083-4093.
23. Kim K, Doi A,Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LI, et al. 2010. Epigenetic memory in induced pluripotent stem cells. Nature 467: 285-290.
24. Klein U, Tu Y, Stolovitzky GA, Keller JL, Haddad J Jr, Miljkovic V, Cattoretti G, Califano A, Dalla-Favera R. 2003. Transcriptional analysis of the B cell germinal center reaction. Proc Natl Acad Sci 100: 2639-2644.
25. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: An information aesthetic for comparative genomics. Genome Res 19: 1639-1645.
26. Lai AY, Fatemi M, Dhasarathy A, Malone C, Sobol SE, Geigerman C, Jaye DL, Mav D, Shah R, Li L, et al. 2010. DNA methylation prevents CTCFmediated silencing of the oncogene BCL6 in B cell lymphomas. J Exp Med 207: 1939-1950.
27. Lanzavecchia A, Sallusto F. 2009. Human B cell memory. Curr Opin Immunol 21: 298-304.
28. Laperriere D, Wang TT, White JH, Mader S. 2007. Widespread Alu repeatdriven expansion of consensus DR2 retinoic acid response elements during primate evolution. BMC Genomics 8: 23.
29. Leonhardt H, Page AW, Weier HU, Bestor TH. 1992. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71: 865-873.
30. Li E, Bestor TH, Jaenisch R. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915-926.
31. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315- 322.
32. Liu YJ, Barthelemy C, de Bouteiller O, Arpin C, Durand I, Banchereau J. 1995. Memory B cells from human tonsils colonize mucosal epithelium and directly present antigen to Tcells by rapid up-regulation of B7-1 and B7-2. Immunity 2: 239-248.
33. Matthias P, Rolink AG. 2005. Transcriptional networks in developing and mature B cells. Nat Rev Immunol 5: 497-508.
34. McHeyzer-Williams LJ, McHeyzer-Williams MG. 2005. Antigen-specific memory B cell development. Annu Rev Immunol 23: 487-513.
35. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, et al. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-770.
36. Messi M, Giacchetto I, Nagata K, Lanzavecchia A, Natoli G, Sallusto F. 2003. Memory and flexibility of cytokine gene expression as separable properties of human TH1 and TH2 lymphocytes. Nat Immunol 4: 78- 86.
37. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
38. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P, Bernstein BE, Jaenisch R, Lander ES, Meissner A. 2008. Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 49- 55.
39. Nabel CS, Jia H, Ye Y, Shen L, Goldschmidt HL, Stivers JT, Zhang Y, Kohli RM. 2012. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat Chem Biol 8: 751-758.
40. Okano M, Bell DW, Haber DA, Li E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
41. Pascual V, Liu YJ, Magalski A, de Bouteiller O, Banchereau J, Capra JD. 1994. Analysis of somatic mutation in five B cell subsets of human tonsil. J Exp Med 180: 329-339.
42. Ponicsan SL, Kugel JF, Goodrich JA. 2010. Genomic gems: SINE RNAs regulate mRNA production. Curr Opin Genet Dev 20: 149-155.
43. Ranuncolo SM, Polo JM, Dierov J, Singer M, Kuo T, Greally J, Green R, Carroll M, Melnick A. 2007. Bcl-6 mediates the germinal center B cell phenotype and lymphomagenesis through transcriptional repression of the DNA-damage sensor ATR. Nat Immunol 8: 705-714.
44. Rauch T, Li H, Wu X, Pfeifer GP. 2006. MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. Cancer Res 66: 7939-7947.
45. Rauch T, Wu X, Zhong X, Riggs AD, Pfeifer GP. 2009. A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci 106: 671- 678.
46. Serre D, Lee BH, Ting AH. 2010. MBD-isolated genome sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res 38: 391-399.
47. Shaknovich R, Cerchietti L, Tsikitas L, Kormaksson M, De S, Figueroa ME, Ballon G, Yang SN, Weinhold N, Reimers M, et al. 2011. DNA methyltransferase 1 and DNA methylation patterning contribute to germinal center B cell differentiation. Blood 118: 3559-3569.
48. Shapiro-Shelef M, Calame K. 2005. Regulation of plasma-cell development. Nat Rev Immunol 5: 230-242.
49. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, et al. 2011. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
50. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 102: 15545-15550.
51. Tadokoro Y, Ema H, Okano M, Li E, Nakauchi H. 2007. De novo DNA methyltransferase is essential for self-renewal, but not for differentiation, in hematopoietic stem cells. J Exp Med 204: 715-722.
52. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
53. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. 2012. The accessible chromatin landscape of the human genome. Nature 489: 75- 82.
54. Victora GD, Nussenzweig MC. 2012. Germinal centers. Annu Rev Immunol 30: 429-457.
55. Weber M, Hellman I, Stadler MB, Famos L, Paabo S, RebhanM, Schubeler D. 2007. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457- 466.
56. Weissman IL. 2000. Stem cells: Units of development, units of regeneration, and units in evolution. Cell 100: 157-168.
57. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R. 2007. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448: 318-324.
58. Wu SC, Zhang Y. 2010. Active DNA demethylation: Many roads lead to Rome. Nat Rev Mol Cell Biol 11: 607-620.
59. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE. 2010. Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329: 444-448.
60. Xie H,Wang M, de Andrade A, Bonaldo Mde F, Galat V, Arndt K, Rajaram V, Goldman S, Tomita T, Soares MB. 2011. Genome-wide quantitative assessment of variation in DNA methylation patterns. Nucleic Acids Res 39: 4099-4108.
61. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Pequignot E. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402: 187-191.
62. Yamane A, ReschW, Kuo N, Kuchen S, Li Z, Sun H-W, Robbiani DF, McBride K, Nussenzweig MC, Casellas R. 2011. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat Immunol 12: 62-69.