Epigenetic function of activation-induced cytidine deaminase and its link to lymphomagenesis

Frontiers in Immunology

Volumn 5, Issue DEC, 2014, Pages

  Dominguez, Pilar M ^a   Shaknovich, Rita ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Activation induced cytidine deaminase; B cells; DNA methylation; Epigenetics; Lymphomagenesis

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ACTIVATION INDUCED CYTIDINE DEAMINASE; DNA METHYLTRANSFERASE 1; METHYLOME; PROTEIN; S ADENOSYLMETHIONINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ASSAY; B CELL LYMPHOMA; B LYMPHOCYTE; CELL MATURATION; CHROMOSOMAL INSTABILITY; CHROMOSOME TRANSLOCATION; CHRONIC LYMPHATIC LEUKEMIA; DEAMINATION; DEMETHYLATION; DNA METHYLATION; DNA MICROARRAY; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; EXCISION REPAIR; FOLLICULAR LYMPHOMA; GENOMIC INSTABILITY; HUMAN; LYMPHOMA; MISMATCH REPAIR; MULTIPLE MYELOMA; NONHUMAN; NUCLEAR REPROGRAMMING; OLIGONUCLEOTIDE DEAMINATION ASSAY; POINT MUTATION; PRIMORDIAL GERM CELL; REVIEW; SOMATIC HYPERMUTATION;

EID: 84919494198     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00642     Document Type: Review

References (142)

1. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet (2003) 33(Suppl):245-54. doi:10.1038/ng1089
2. Li G, Zan H, Xu Z, Casali P. Epigenetics of the antibody response. Trends Immunol (2013) 34(9):460-70. doi:10.1016/j.it.2013.03.006
3. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science (2001) 293(5532):1068-70. doi:10.1126/science.1063852
4. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev (2002) 16(1):6-21. doi:10.1101/gad.947102
5. Robertson KD. DNA methylation and chromatin - unraveling the tangled web. Oncogene (2002) 21(35):5361-79. doi:10.1038/sj.onc.1205609
6. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature (2004) 429(6990):457-63. doi:10.1038/nature02625
7. Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, et al. Global epigenomic reconfiguration during mammalian brain development. Science (2013) 341(6146):1237905. doi:10.1126/science.1237905
8. Head JA. Patterns of DNA methylation in animals: an ecotoxicological perspective. Integr Comp Biol (2014) 54(1):77-86. doi:10.1093/icb/icu025
9. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem (2005) 74:481-514. doi:10.1146/annurev.biochem.74.010904.153721
10. He XJ, Chen T, Zhu JK. Regulation and function of DNA methylation in plants and animals. Cell Res (2011) 21(3):442-65. doi:10.1038/cr.2011.23
11. Gong Z, Zhu JK. Active DNA demethylation by oxidation and repair. Cell Res (2011) 21(12):1649-51. doi:10.1038/cr.2011.140
12. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P, et al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature (2010) 467(7313):338-42. doi:10.1038/nature09367
13. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, Uren PJ, et al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell (2011) 44(1):17-28. doi:10.1016/j.molcel.2011.08.026
14. Zilbauer M, Rayner TF, Clark C, Coffey AJ, Joyce CJ, Palta P, et al. Genome-wide methylation analyses of primary human leukocyte subsets identifies functionally important cell-type-specific hypomethylated regions. Blood (2013) 122(25):e52-60. doi:10.1182/blood-2013-05-503201
15. Shaknovich R, Cerchietti L, Tsikitas L, Kormaksson M, De S, Figueroa ME, et al. DNA methyltransferase 1 and DNA methylation patterning contribute to germinal center B-cell differentiation. Blood (2011) 118(13):3559-69. doi:10.1182/blood-2011-06-357996
16. Lai AY, Mav D, Shah R, Grimm SA, Phadke D, Hatzi K, et al. DNA methylation profiling in human B cells reveals immune regulatory elements and epigenetic plasticity at Alu elements during B-cell activation. Genome Res (2013) 23(12):2030-41. doi:10.1101/gr.155473.113
17. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell (2000) 102(5):553-63. doi:10.1016/S0092-8674(00)00078-7
18. Conticello SG. The AID/APOBEC family of nucleic acid mutators. Genome Biol (2008) 9(6):229. doi:10.1186/gb-2008-9-6-229
19. Zan H, Casali P. Regulation of Aicda expression and AID activity. Autoimmunity (2013) 46(2):83-101. doi:10.3109/08916934.2012.749244
20. Storb U, Stavnezer J. Immunoglobulin genes: generating diversity with AID and UNG. Curr Biol (2002) 12(21):R725-7. doi:10.1016/S0960-9822(02)01247-2
21. Teng G, Papavasiliou FN. Immunoglobulin somatic hypermutation. Annu Rev Genet (2007) 41:107-20. doi:10.1146/annurev.genet.41.110306.130340
22. Chaudhuri J, Alt FW. Class-switch recombination: interplay of transcription, DNA deamination and DNA repair. Nat Rev Immunol (2004) 4(7):541-52. doi:10.1038/nri1425
23. Stavnezer J, Guikema JE, Schrader CE. Mechanism and regulation of class switch recombination. Annu Rev Immunol (2008) 26:261-92. doi:10.1146/annurev.immunol.26.021607.090248
24. Xu Z, Zan H, Pone EJ, Mai T, Casali P. Immunoglobulin class-switch DNA recombination: induction, targeting and beyond. Nat Rev Immunol (2012) 12(7):517-31. doi:10.1038/nri3216
25. Honjo T, Nagaoka H, Shinkura R, Muramatsu M. AID to overcome the limitations of genomic information. Nat Immunol (2005) 6(7):655-61. doi:10.1038/ni1218
26. Peled JU, Kuang FL, Iglesias-Ussel MD, Roa S, Kalis SL, Goodman MF, et al. The biochemistry of somatic hypermutation. Annu Rev Immunol (2008) 26:481-511. doi:10.1146/annurev.immunol.26.021607.090236
27. Morgan HD, Dean W, Coker HA, Reik W, Petersen-Mahrt SK. Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J Biol Chem (2004) 279(50):52353-60. doi:10.1074/jbc.M407695200
28. Cattoretti G, Buettner M, Shaknovich R, Kremmer E, Alobeid B, Niedobitek G. Nuclear and cytoplasmic AID in extrafollicular and germinal center B cells. Blood (2006) 107(10):3967-75. doi:10.1182/blood-2005-10-4170
29. Pone EJ, Zan H, Zhang J, Al-Qahtani A, Xu Z, Casali P. Toll-like receptors and B-cell receptors synergize to induce immunoglobulin class-switch DNA recombination: relevance to microbial antibody responses. Crit Rev Immunol (2010) 30(1):1-29. doi:10.1615/CritRevImmunol.v30.i1.10
30. Shaffer AL, Lin KI, Kuo TC, Yu X, Hurt EM, Rosenwald A, et al. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity (2002) 17(1):51-62. doi:10.1016/S1074-7613(02)00335-7
31. Crouch EE, Li Z, Takizawa M, Fichtner-Feigl S, Gourzi P, Montano C, et al. Regulation of AID expression in the immune response. J Exp Med (2007) 204(5):1145-56. doi:10.1084/jem.20061952
32. Gourzi P, Leonova T, Papavasiliou FN. Viral induction of AID is independent of the interferon and the toll-like receptor signaling pathways but requires NF-kappaB. J Exp Med (2007) 204(2):259-65. doi:10.1084/jem.20061801
33. Machida K, Cheng KT, Sung VM, Shimodaira S, Lindsay KL, Levine AM, et al. Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc Natl Acad Sci U S A (2004) 101(12):4262-7. doi:10.1073/pnas.0303971101
34. Tobollik S, Meyer L, Buettner M, Klemmer S, Kempkes B, Kremmer E, et al. Epstein-Barr virus nuclear antigen 2 inhibits AID expression during EBV-driven B-cell growth. Blood (2006) 108(12):3859-64. doi:10.1182/blood-2006-05-021303
35. Berek C, Milstein C. Mutation drift and repertoire shift in the maturation of the immune response. Immunol Rev (1987) 96:23-41. doi:10.1111/j.1600-065X.1987.tb00507.x
36. Rajewsky K, Forster I, Cumano A. Evolutionary and somatic selection of the antibody repertoire in the mouse. Science (1987) 238(4830):1088-94. doi:10.1126/science.3317826
37. Shen HM, Peters A, Baron B, Zhu X, Storb U. Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science (1998) 280(5370):1750-2. doi:10.1126/science.280.5370.1750
38. Pasqualucci L, Migliazza A, Fracchiolla N, William C, Neri A, Baldini L, et al. BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc Natl Acad Sci U S A (1998) 95(20):11816-21. doi:10.1073/pnas.95.20.11816
39. Gordon MS, Kanegai CM, Doerr JR, Wall R. Somatic hypermutation of the B cell receptor genes B29 (Igbeta, CD79b) and mb1 (Igalpha, CD79a). Proc Natl Acad Sci U S A (2003) 100(7):4126-31. doi:10.1073/pnas.0735266100
40. Muschen M, Re D, Jungnickel B, Diehl V, Rajewsky K, Kuppers R. Somatic mutation of the CD95 gene in human B cells as a side-effect of the germinal center reaction. J Exp Med (2000) 192(12):1833-40. doi:10.1084/jem.192.12.1833
41. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, Kleinstein SH, et al. Two levels of protection for the B cell genome during somatic hypermutation. Nature (2008) 451(7180):841-5. doi:10.1038/nature06547
42. Yamane A, Resch W, Kuo N, Kuchen S, Li Z, Sun HW, et al. Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat Immunol (2011) 12(1):62-9. doi:10.1038/ni.1964
43. Kumar R, DiMenna LJ, Chaudhuri J, Evans T. Biological function of activation-induced cytidine deaminase (AID). Biomed J (2014) 37(5):269-83. doi:10.4103/2319-4170.128734
44. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature (2010) 463(7284):1042-7. doi:10.1038/nature08752
45. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell (2008) 135(7):1201-12. doi:10.1016/j.cell.2008.11.042
46. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature (2010) 463(7284):1101-5. doi:10.1038/nature08829
47. Nabel CS, Jia H, Ye Y, Shen L, Goldschmidt HL, Stivers JT, et al. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat Chem Biol (2012) 8(9):751-8. doi:10.1038/nchembio.1042
48. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev (2002) 117(1-2):15-23. doi:10.1016/S0925-4773(02)00181-8
49. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet (2008) 9(2):129-40. doi:10.1038/nrg2295
50. Hay ED. An overview of epithelio-mesenchymal transformation. Acta Anat (1995) 154(1):8-20. doi:10.1159/000147748
51. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest (2009) 119(6):1420-8. doi:10.1172/JCI39104
52. Komori J, Marusawa H, Machimoto T, Endo Y, Kinoshita K, Kou T, et al. Activation-induced cytidine deaminase links bile duct inflammation to human cholangiocarcinoma. Hepatology (2008) 47(3):888-96. doi:10.1002/hep.22125
53. Endo Y, Marusawa H, Kou T, Nakase H, Fujii S, Fujimori T, et al. Activation-induced cytidine deaminase links between inflammation and the development of colitis-associated colorectal cancers. Gastroenterology (2008) 135(3):e1-3. doi:10.1053/j.gastro.2008.06.091
54. Matsumoto Y, Marusawa H, Kinoshita K, Endo Y, Kou T, Morisawa T, et al. Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium. Nat Med (2007) 13(4):470-6. doi:10.1038/nm1566
55. Munoz DP, Lee EL, Takayama S, Coppe JP, Heo SJ, Boffelli D, et al. Activation-induced cytidine deaminase (AID) is necessary for the epithelial-mesenchymal transition in mammary epithelial cells. Proc Natl Acad Sci U S A (2013) 110(32):E2977-86. doi:10.1073/pnas.1301021110
56. Liu Y, Mukhopadhyay P, Pisano MM, Lu X, Huang L, Lu Q, et al. Repression of Zeb1 and hypoxia cause sequential mesenchymal-to-epithelial transition and induction of aid, Oct4, and Dnmt1, leading to immortalization and multipotential reprogramming of fibroblasts in spheres. Stem Cells (2013) 31(7):1350-62. doi:10.1002/stem.1382
57. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell (2006) 126(4):663-76. doi:10.1016/j.cell.2006.07.024
58. Bhutani N, Decker MN, Brady JJ, Bussat RT, Burns DM, Corbel SY, et al. A critical role for AID in the initiation of reprogramming to induced pluripotent stem cells. FASEB J (2013) 27(3):1107-13. doi:10.1096/fj.12-222125
59. Kumar R, DiMenna L, Schrode N, Liu TC, Franck P, Munoz-Descalzo S, et al. AID stabilizes stem-cell phenotype by removing epigenetic memory of pluripotency genes. Nature (2013) 500(7460):89-92. doi:10.1038/nature12299
60. Habib O, Habib G, Do JT, Moon SH, Chung HM. Activation-induced deaminase-coupled DNA demethylation is not crucial for the generation of induced pluripotent stem cells. Stem Cells Dev (2014) 23(3):209-18. doi:10.1089/scd.2013.0337
61. Shimamoto R, Amano N, Ichisaka T, Watanabe A, Yamanaka S, Okita K. Generation and characterization of induced pluripotent stem cells from Aid-deficient mice. PLoS One (2014) 9(4):e94735. doi:10.1371/journal.pone.0094735
62. Polo JM, Anderssen E, Walsh RM, Schwarz BA, Nefzger CM, Lim SM, et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell (2012) 151(7):1617-32. doi:10.1016/j.cell.2012.11.039
63. Fritz EL, Rosenberg BR, Lay K, Mihailovic A, Tuschl T, Papavasiliou FN. A comprehensive analysis of the effects of the deaminase AID on the transcriptome and methylome of activated B cells. Nat Immunol (2013) 14(7):749-55. doi:10.1038/ni.2616
64. Jolly CJ, Neuberger MS. Somatic hypermutation of immunoglobulin kappa transgenes: association of mutability with demethylation. Immunol Cell Biol (2001) 79(1):18-22. doi:10.1046/j.1440-1711.2001.00968.x
65. Larijani M, Frieder D, Sonbuchner TM, Bransteitter R, Goodman MF, Bouhassira EE, et al. Methylation protects cytidines from AID-mediated deamination. Mol Immunol (2005) 42(5):599-604. doi:10.1016/j.molimm.2004.09.007
66. Fraenkel S, Mostoslavsky R, Novobrantseva TI, Pelanda R, Chaudhuri J, Esposito G, et al. Allelic 'choice' governs somatic hypermutation in vivo at the immunoglobulin kappa-chain locus. Nat Immunol (2007) 8(7):715-22. doi:10.1038/ni1476
67. Mather EL, Perry RP. Methylation status and DNase I sensitivity of immunoglobulin genes: changes associated with rearrangement. Proc Natl Acad Sci U S A (1983) 80(15):4689-93. doi:10.1073/pnas.80.15.4689
68. Storb U, Arp B. Methylation patterns of immunoglobulin genes in lymphoid cells: correlation of expression and differentiation with undermethylation. Proc Natl Acad Sci U S A (1983) 80(21):6642-6. doi:10.1073/pnas.80.21.6642
69. Ha K, Lee GE, Palii SS, Brown KD, Takeda Y, Liu K, et al. Rapid and transient recruitment of DNMT1 to DNA double-strand breaks is mediated by its interaction with multiple components of the DNA damage response machinery. Hum Mol Genet (2011) 20(1):126-40. doi:10.1093/hmg/ddq451
70. Hervouet E, Nadaradjane A, Gueguen M, Vallette FM, Cartron PF. Kinetics of DNA methylation inheritance by the Dnmt1-including complexes during the cell cycle. Cell Div (2012) 7:5. doi:10.1186/1747-1028-7-5
71. Hervouet E, Vallette FM, Cartron PF. Dnmt1/transcription factor interactions: an alternative mechanism of DNA methylation inheritance. Genes Cancer (2010) 1(5):434-43. doi:10.1177/1947601910373794
72. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res (1965) 37:614-36. doi:10.1016/0014-4827(65)90211-9
73. Kim MJ, Kim MH, Kim SA, Chang JS. Age-related deterioration of hematopoietic stem cells. Int J Stem Cells (2008) 1(1):55-63. doi:10.15283/ijsc.2008.1.1.55
74. Martin A, Bardwell PD, Woo CJ, Fan M, Shulman MJ, Scharff MD. Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas. Nature (2002) 415(6873):802-6. doi:10.1038/nature714
75. McKean D, Huppi K, Bell M, Staudt L, Gerhard W, Weigert M. Generation of antibody diversity in the immune response of BALB/c mice to influenza virus hemagglutinin. Proc Natl Acad Sci U S A (1984) 81(10):3180-4. doi:10.1073/pnas.81.10.3180
76. Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y, Difilippantonio S, et al. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell (2008) 135(6):1028-38. doi:10.1016/j.cell.2008.09.062
77. Hogenbirk MA, Heideman MR, Velds A, van den Berk PC, Kerkhoven RM, van Steensel B, et al. Differential programming of B cells in AID deficient mice. PLoS One (2013) 8(7):e69815. doi:10.1371/journal.pone.0069815
78. Muto T, Okazaki IM, Yamada S, Tanaka Y, Kinoshita K, Muramatsu M, et al. Negative regulation of activation-induced cytidine deaminase in B cells. Proc Natl Acad Sci U S A (2006) 103(8):2752-7. doi:10.1073/pnas.0510970103
79. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, et al. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell (2002) 110(1):33-42. doi:10.1016/S0092-8674(02)00807-3
80. Gong Z, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, David L, Zhu JK. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell (2002) 111(6):803-14. doi:10.1016/S0092-8674(02)01133-9
81. Jullien PE, Kinoshita T, Ohad N, Berger F. Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell (2006) 18(6):1360-72. doi:10.1105/tpc.106.041178
82. Kim YJ, Wilson DM III. Overview of base excision repair biochemistry. Curr Mol Pharmacol (2012) 5(1):3-13. doi:10.2174/1874467211205010003
83. Gehring M, Reik W, Henikoff S. DNA demethylation by DNA repair. Trends Genet (2009) 25(2):82-90. doi:10.1016/j.tig.2008.12.001
84. Zhu JK. Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet (2009) 43:143-66. doi:10.1146/annurev-genet-102108-134205
85. Zharkova DO, Mechetina GV, Nevinskya GA. Uracil-DNA glycosylase: Structural, thermodynamic and kinetic aspects of lesion search and recognition. Mutat Res (2010) 685(1-2):11-20. doi:10.1016/j.mrfmmm.2009.10.017
86. Cortellino S, Xu J, Sannai M, Moore R, Caretti E, Cigliano A, et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell (2011) 146(1):67-79. doi:10.1016/j.cell.2011.06.020
87. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science (2009) 324(5929):929-30. doi:10.1126/science.1169786
88. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science (2009) 324(5929):930-5. doi:10.1126/science.1170116
89. Wu SC, Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol (2010) 11(9):607-20. doi:10.1038/nrm2950
90. Guo JU, Su Y, Zhong C, Ming GL, Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell (2011) 145(3):423-34. doi:10.1016/j.cell.2011.03.022
91. Rangam G, Schmitz KM, Cobb AJ, Petersen-Mahrt SK. AID enzymatic activity is inversely proportional to the size of cytosine C5 orbital cloud. PLoS One (2012) 7(8):e43279. doi:10.1371/journal.pone.0043279
92. Franchini DM, Chan CF, Morgan H, Incorvaia E, Rangam G, Dean W, et al. Processive DNA demethylation via DNA deaminase-induced lesion resolution. PLoS One (2014) 9(7):e97754. doi:10.1371/journal.pone.0097754
93. Robertson AB, Klungland A, Rognes T, Leiros I. DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci (2009) 66(6):981-93. doi:10.1007/s00018-009-8736-z
94. Li GM. Mechanisms and functions of DNA mismatch repair. Cell Res (2008) 18(1):85-98. doi:10.1038/cr.2007.115
95. Jiricny J. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol (2006) 7(5):335-46. doi:10.1038/nrm1907
96. Fritz EL, Papavasiliou FN. Cytidine deaminases: AIDing DNA demethylation? Genes Dev (2010) 24(19):2107-14. doi:10.1101/gad.1963010
97. Bransteitter R, Pham P, Scharff MD, Goodman MF. Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc Natl Acad Sci U S A (2003) 100(7):4102-7. doi:10.1073/pnas.0730835100
98. Pavri R, Gazumyan A, Jankovic M, Di Virgilio M, Klein I, Ansarah-Sobrinho C, et al. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell (2010) 143(1):122-33. doi:10.1016/j.cell.2010.09.017
99. Storck S, Aoufouchi S, Weill JC, Reynaud CA. AID and partners: for better and (not) for worse. Curr Opin Immunol (2011) 23(3):337-44. doi:10.1016/j.coi.2011.02.002
100. Duke JL, Liu M, Yaari G, Khalil AM, Tomayko MM, Shlomchik MJ, et al. Multiple transcription factor binding sites predict AID targeting in non-Ig genes. J Immunol (2013) 190(8):3878-88. doi:10.4049/jimmunol.1202547
101. Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature (2013) 502(7472):472-9. doi:10.1038/nature12750
102. Huang Y, Rao A. Connections between TET proteins and aberrant DNA modification in cancer. Trends Genet (2014) 30(10):464-74. doi:10.1016/j.tig.2014.07.005
103. Pfaffeneder T, Spada F, Wagner M, Brandmayr C, Laube SK, Eisen D, et al. Tet oxidizes thymine to 5-hydroxymethyluracil in mouse embryonic stem cell DNA. Nat Chem Biol (2014) 10(7):574-81. doi:10.1038/nchembio.1532
104. Wahlfors J, Hiltunen H, Heinonen K, Hamalainen E, Alhonen L, Janne J. Genomic hypomethylation in human chronic lymphocytic leukemia. Blood (1992) 80(8):2074-80.
105. Kulis M, Heath S, Bibikova M, Queiros AC, Navarro A, Clot G, et al. Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat Genet (2012) 44(11):1236-42. doi:10.1038/ng.2443
106. Fabris S, Scarciolla O, Morabito F, Cifarelli RA, Dininno C, Cutrona G, et al. Multiplex ligation-dependent probe amplification and fluorescence in situ hybridization to detect chromosomal abnormalities in chronic lymphocytic leukemia: a comparative study. Genes Chromosomes Cancer (2011) 50(9):726-34. doi:10.1002/gcc.20894
107. Chambwe N, Kormaksson M, Geng H, De S, Michor F, Johnson NA, et al. Variability in DNA methylation defines novel epigenetic subgroups of DLBCL associated with different clinical outcomes. Blood (2014) 123(11):1699-708. doi:10.1182/blood-2013-07-509885
108. Choi JH, Li Y, Guo J, Pei L, Rauch TA, Kramer RS, et al. Genome-wide DNA methylation maps in follicular lymphoma cells determined by methylation-enriched bisulfite sequencing. PLoS One (2010) 5(9). doi:10.1371/journal.pone.0013020
109. Shaknovich R, De S, Michor F. Epigenetic diversity in hematopoietic neoplasms. Biochim Biophys Acta (2014) 1846(2):477-84. doi:10.1016/j.bbcan.2014.09.003
110. Oshima M, Iwama A. Epigenetics of hematopoietic stem cell aging and disease. Int J Hematol (2014) 100(4):326-34. doi:10.1007/s12185-014-1647-2
111. Dykstra B, de Haan G. Hematopoietic stem cell aging and self-renewal. Cell Tissue Res (2008) 331(1):91-101. doi:10.1007/s00441-007-0529-9
112. Potter JD. Methyl supply, methyl metabolizing enzymes and colorectal neoplasia. J Nutr (2002) 132(8 Suppl):2410S-2S.
113. Wilson MJ, Shivapurkar N, Poirier LA. Hypomethylation of hepatic nuclear DNA in rats fed with a carcinogenic methyl-deficient diet. Biochem J (1984) 218(3):987-90.
114. Soares J, Pinto AE, Cunha CV, Andre S, Barao I, Sousa JM, et al. Global DNA hypomethylation in breast carcinoma: correlation with prognostic factors and tumor progression. Cancer (1999) 85(1):112-8. doi:10.1002/(SICI)1097-0142(19990101)85:1<112::AID-CNCR16>3.0.CO;2-T
115. Kim YI, Giuliano A, Hatch KD, Schneider A, Nour MA, Dallal GE, et al. Global DNA hypomethylation increases progressively in cervical dysplasia and carcinoma. Cancer (1994) 74(3):893-9. doi:10.1002/1097-0142(19940801)74:3<893::AID-CNCR2820740316>3.0.CO;2-B
116. Shen L, Fang J, Qiu D, Zhang T, Yang J, Chen S, et al. Correlation between DNA methylation and pathological changes in human hepatocellular carcinoma. Hepatogastroenterology (1998) 45(23):1753-9.
117. Ramchandani S, Bhattacharya SK, Cervoni N, Szyf M. DNA methylation is a reversible biological signal. Proc Natl Acad Sci U S A (1999) 96(11):6107-12. doi:10.1073/pnas.96.11.6107
118. Cervoni N, Bhattacharya S, Szyf M. DNA demethylase is a processive enzyme. J Biol Chem (1999) 274(13):8363-6. doi:10.1074/jbc.274.13.8363
119. Hamm S, Just G, Lacoste N, Moitessier N, Szyf M, Mamer O. On the mechanism of demethylation of 5-methylcytosine in DNA. Bioorg Med Chem Lett (2008) 18(3):1046-9. doi:10.1016/j.bmcl.2007.12.027
120. Bhattacharya SK, Ramchandani S, Cervoni N, Szyf M. A mammalian protein with specific demethylase activity for mCpG DNA. Nature (1999) 397(6720):579-83. doi:10.1038/17533
121. Robbiani DF, Bunting S, Feldhahn N, Bothmer A, Camps J, Deroubaix S, et al. AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol Cell (2009) 36(4):631-41. doi:10.1016/j.molcel.2009.11.007
122. Esteller M. Epigenetics in cancer. N Engl J Med (2008) 358(11):1148-59. doi:10.1056/NEJMra072067
123. Hoffmann MJ, Schulz WA. Causes and consequences of DNA hypomethylation in human cancer. Biochem Cell Biol (2005) 83(3):296-321. doi:10.1139/o05-036
124. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, et al. Induction of tumors in mice by genomic hypomethylation. Science (2003) 300(5618):489-92. doi:10.1126/science.1083558
125. Hervouet E, Lalier L, Debien E, Cheray M, Geairon A, Rogniaux H, et al. Disruption of Dnmt1/PCNA/UHRF1 interactions promotes tumorigenesis from human and mice glial cells. PLoS One (2010) 5(6):e11333. doi:10.1371/journal.pone.0011333
126. Smit LA, Bende RJ, Aten J, Guikema JE, Aarts WM, van Noesel CJ. Expression of activation-induced cytidine deaminase is confined to B-cell non-Hodgkin's lymphomas of germinal-center phenotype. Cancer Res (2003) 63(14):3894-8.
127. Greeve J, Philipsen A, Krause K, Klapper W, Heidorn K, Castle BE, et al. Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas. Blood (2003) 101(9):3574-80. doi:10.1182/blood-2002-08-2424
128. Gu X, Shivarov V, Strout MP. The role of activation-induced cytidine deaminase in lymphomagenesis. Curr Opin Hematol (2012) 19(4):292-8. doi:10.1097/MOH.0b013e328353da3a
129. Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti RS, Kuppers R, et al. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature (2001) 412(6844):341-6. doi:10.1038/35085588
130. Bergsagel PL, Kuehl WM. Chromosome translocations in multiple myeloma. Oncogene (2001) 20(40):5611-22. doi:10.1038/sj.onc.1204641
131. Kuppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat Rev Cancer (2005) 5(4):251-62. doi:10.1038/nrc1589
132. Ramiro AR, Jankovic M, Eisenreich T, Difilippantonio S, Chen-Kiang S, Muramatsu M, et al. AID is required for c-myc/IgH chromosome translocations in vivo. Cell (2004) 118(4):431-8. doi:10.1016/j.cell.2004.08.006
133. Kovalchuk AL, duBois W, Mushinski E, McNeil NE, Hirt C, Qi CF, et al. AID-deficient Bcl-xL transgenic mice develop delayed atypical plasma cell tumors with unusual Ig/Myc chromosomal rearrangements. J Exp Med (2007) 204(12):2989-3001. doi:10.1084/jem.20070882
134. Lohr JG, Stojanov P, Lawrence MS, Auclair D, Chapuy B, Sougnez C, et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc Natl Acad Sci U S A (2012) 109(10):3879-84. doi:10.1073/pnas.1121343109
135. Cattoretti G, Pasqualucci L, Ballon G, Tam W, Nandula SV, Shen Q, et al. Deregulated BCL6 expression recapitulates the pathogenesis of human diffuse large B cell lymphomas in mice. Cancer Cell (2005) 7(5):445-55. doi:10.1016/j.ccr.2005.03.037
136. Pasqualucci L, Bhagat G, Jankovic M, Compagno M, Smith P, Muramatsu M, et al. AID is required for germinal center-derived lymphomagenesis. Nat Genet (2008) 40(1):108-12. doi:10.1038/ng.2007.35
137. Takizawa M, Tolarova H, Li Z, Dubois W, Lim S, Callen E, et al. AID expression levels determine the extent of cMyc oncogenic translocations and the incidence of B cell tumor development. J Exp Med (2008) 205(9):1949-57. doi:10.1084/jem.20081007
138. Chesi M, Robbiani DF, Sebag M, Chng WJ, Affer M, Tiedemann R, et al. AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies. Cancer Cell (2008) 13(2):167-80. doi:10.1016/j.ccr.2008.01.007
139. Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, Kinoshita K, et al. Constitutive expression of AID leads to tumorigenesis. J Exp Med (2003) 197(9):1173-81. doi:10.1084/jem.20030275
140. Komeno Y, Kitaura J, Watanabe-Okochi N, Kato N, Oki T, Nakahara F, et al. AID-induced T-lymphoma or B-leukemia/lymphoma in a mouse BMT model. Leukemia (2010) 24(5):1018-24. doi:10.1038/leu.2010.40
141. De S, Shaknovich R, Riester M, Elemento O, Geng H, Kormaksson M, et al. Aberration in DNA methylation in B-cell lymphomas has a complex origin and increases with disease severity. PLoS Genet (2013) 9(1):e1003137. doi:10.1371/journal.pgen.1003137
142. TNHLCP. A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin's lymphoma. The non-Hodgkin's lymphoma classification project. Blood (1997) 89(11):3909-18.