The Role of Epigenetic Mechanisms in B Cell Lymphoma Pathogenesis

Literature Cited

1. Afshar-Sterle S, Zotos D, Bernard NJ, Scherger AK, Rodling L et al. 2014. Fas ligand–mediated immune surveillance by T cells is essential for the control of spontaneous B cell lymphomas. Nat. Med. 20:283–90
   [Google Scholar]
2. Allis CD, Jenuwein T. 2016. The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 17:487–500
   [Google Scholar]
3. Ambrosio MR, Lo Bello G, Amato T, Lazzi S, Piccaluga PP et al. 2016. The cell of origin of Burkitt lymphoma: germinal centre or not germinal centre. ? Histopathology 69:885–86
   [Google Scholar]
4. Arpin C, Banchereau J, Liu YJ 1997. Memory B cells are biased towards terminal differentiation: a strategy that may prevent repertoire freezing. J. Exp. Med. 186:931–40
   [Google Scholar]
5. Asmar F, Punj V, Christensen J, Pedersen MT, Pedersen A et al. 2013. Genome-wide profiling identifies a DNA methylation signature that associates with TET2 mutations in diffuse large B-cell lymphoma. Haematologica 98:1912–20
   [Google Scholar]
6. Barwick BG, Gupta VA, Vertino PM, Boise LH 2019. Cell of origin and genetic alterations in the pathogenesis of multiple myeloma. Front. Immunol. 10:1121
   [Google Scholar]
7. Beguelin W, Popovic R, Teater M, Jiang Y, Bunting KL et al. 2013. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 23:677–92
   [Google Scholar]
8. Beguelin W, Rivas MA, Calvo Fernandez MT, Teater M, Purwada A et al. 2017. EZH2 enables germinal centre formation through epigenetic silencing of CDKN1A and an Rb-E2F1 feedback loop. Nat. Commun. 8:877
   [Google Scholar]
9. Beguelin W, Teater M, Gearhart MD, Calvo Fernandez MT, Goldstein RL et al. 2016. EZH2 and BCL6 cooperate to assemble CBX8-BCOR complex to repress bivalent promoters, mediate germinal center formation and lymphomagenesis. Cancer Cell 30:197–213
   [Google Scholar]
10. Beguelin W, Teater M, Meydan C, Hoehn KB, Phillip JM et al. 2020. Mutant EZH2 induces a pre-malignant lymphoma niche by reprogramming the immune response. Cancer Cell 37:655–73.e11
    [Google Scholar]
11. Bereshchenko OR, Gu W, Dalla-Favera R 2002. Acetylation inactivates the transcriptional repressor BCL6. Nat. Genet. 32:606–13
    [Google Scholar]
12. Blauth K, Owens GP, Bennett JL 2015. The ins and outs of B cells in multiple sclerosis. Front. Immunol. 6:565
    [Google Scholar]
13. Brynjolfsson SF, Persson Berg L, Olsen Ekerhult T, Rimkute I, Wick MJ et al. 2018. Long-lived plasma cells in mice and men. Front. Immunol. 9:2673
    [Google Scholar]
14. Bunting KL, Soong TD, Singh R, Jiang Y, Beguelin W et al. 2016. Multi-tiered reorganization of the genome during B cell affinity maturation anchored by a germinal center-specific locus control region. Immunity 45:497–512
    [Google Scholar]
15. Cardenas MG, Oswald E, Yu W, Xue F, MacKerell AD Jr, Melnick AM 2017. The expanding role of the BCL6 oncoprotein as a cancer therapeutic target. Clin. Cancer Res. 23:885–93
    [Google Scholar]
16. Cascione L, Rinaldi A, Bruscaggin A, Tarantelli C, Arribas AJ et al. 2019. Novel insights into the genetics and epigenetics of MALT lymphoma unveiled by next generation sequencing analyses. Haematologica 104:e558–61
    [Google Scholar]
17. Castillo JJ, Bibas M, Miranda RN 2015. The biology and treatment of plasmablastic lymphoma. Blood 125:2323–30
    [Google Scholar]
18. Cerutti A, Cols M, Puga I 2013. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 13:118–32
    [Google Scholar]
19. Chan TD, Gatto D, Wood K, Camidge T, Basten A, Brink R 2009. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 183:3139–49
    [Google Scholar]
20. Chapuy B, Roemer MG, Stewart C, Tan Y, Abo RP et al. 2016. Targetable genetic features of primary testicular and primary central nervous system lymphomas. Blood 127:869–81
    [Google Scholar]
21. Chapuy B, Stewart C, Dunford AJ, Kim J, Kamburov A et al. 2018. Molecular subtypes of diffuse large B cell lymphoma are associated with distinct pathogenic mechanisms and outcomes. Nat. Med. 24:679–90
    [Google Scholar]
22. Chesi M, Nardini E, Lim RS, Smith KD, Kuehl WM, Bergsagel PL 1998. The t(4;14) translocation in myeloma dysregulates both FGFR3 and a novel gene, MMSET, resulting in IgH/MMSET hybrid transcripts. Blood 92:3025–34
    [Google Scholar]
23. Chokas AL, Trivedi CM, Lu MM, Tucker PW, Li S et al. 2010. Foxp1/2/4-NuRD interactions regulate gene expression and epithelial injury response in the lung via regulation of interleukin-6. J. Biol. Chem. 285:13304–13
    [Google Scholar]
24. Clozel T, Yang S, Elstrom RL, Tam W, Martin P et al. 2013. Mechanism-based epigenetic chemosensitization therapy of diffuse large B-cell lymphoma. Cancer Discov 3:1002–19
    [Google Scholar]
25. Corn PG, Kuerbitz SJ, van Noesel MM, Esteller M, Compitello N et al. 1999. Transcriptional silencing of the p73 gene in acute lymphoblastic leukemia and Burkitt's lymphoma is associated with 5′ CpG island methylation. Cancer Res 59:3352–56
    [Google Scholar]
26. Cyster JG, Allen CDC. 2019. B cell responses: cell interaction dynamics and decisions. Cell 177:524–40
    [Google Scholar]
27. Deenick EK, Avery DT, Chan A, Berglund LJ, Ives ML et al. 2013. Naive and memory human B cells have distinct requirements for STAT3 activation to differentiate into antibody-secreting plasma cells. J. Exp. Med. 210:2739–53
    [Google Scholar]
28. Dekker JD, Park D, Shaffer AL 3rd, Kohlhammer H, Deng W et al. 2016. Subtype-specific addiction of the activated B-cell subset of diffuse large B-cell lymphoma to FOXP1. PNAS 113:E577–86
    [Google Scholar]
29. Dogan I, Bertocci B, Vilmont V, Delbos F, Megret J et al. 2009. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10:1292–99
    [Google Scholar]
30. Dominguez PM, Ghamlouch H, Rosikiewicz W, Kumar P, Beguelin W et al. 2018. TET2 deficiency causes germinal center hyperplasia, impairs plasma cell differentiation, and promotes B-cell lymphomagenesis. Cancer Discov 8:1632–53
    [Google Scholar]
31. Eberth S, Schneider B, Rosenwald A, Hartmann EM, Romani J et al. 2010. Epigenetic regulation of CD44 in Hodgkin and non-Hodgkin lymphoma. BMC Cancer 10:517
    [Google Scholar]
32. Ennishi D, Takata K, Beguelin W, Duns G, Mottok A et al. 2019. Molecular and genetic characterization of MHC deficiency identifies EZH2 as therapeutic target for enhancing immune recognition. Cancer Discov 9:546–63
    [Google Scholar]
33. Ezponda T, Dupere-Richer D, Will CM, Small EC, Varghese N et al. 2017. UTX/KDM6A loss enhances the malignant phenotype of multiple myeloma and sensitizes cells to EZH2 inhibition. Cell Rep 21:628–40
    [Google Scholar]
34. Flori M, Schmid CA, Sumrall ET, Tzankov A, Law CW et al. 2016. The hematopoietic oncoprotein FOXP1 promotes tumor cell survival in diffuse large B-cell lymphoma by repressing S1PR2 signaling. Blood 127:1438–48
    [Google Scholar]
35. Gearhart MD, Corcoran CM, Wamstad JA, Bardwell VJ 2006. Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol. Cell. Biol. 26:6880–89
    [Google Scholar]
36. Ghetu AF, Corcoran CM, Cerchietti L, Bardwell VJ, Melnick A, Prive GG 2008. Structure of a BCOR corepressor peptide in complex with the BCL6 BTB domain dimer. Mol. Cell 29:384–91
    [Google Scholar]
37. Good-Jacobson KL, Chen Y, Voss AK, Smyth GK, Thomas T, Tarlinton D 2014. Regulation of germinal center responses and B-cell memory by the chromatin modifier MOZ. PNAS 111:9585–90
    [Google Scholar]
38. Grande BM, Gerhard DS, Jiang A, Griner NB, Abramson JS et al. 2019. Genome-wide discovery of somatic coding and noncoding mutations in pediatric endemic and sporadic Burkitt lymphoma. Blood 133:1313–24
    [Google Scholar]
39. Green MR, Kihira S, Liu CL, Nair RV, Salari R et al. 2015. Mutations in early follicular lymphoma progenitors are associated with suppressed antigen presentation. PNAS 112:E1116–25
    [Google Scholar]
40. Guenther MG, Barak O, Lazar MA 2001. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol. Cell. Biol. 21:6091–101
    [Google Scholar]
41. Gulati N, Beguelin W, Giulino-Roth L 2018. Enhancer of zeste homolog 2 (EZH2) inhibitors. Leuk. Lymphoma 59:1574–85
    [Google Scholar]
42. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646–74
    [Google Scholar]
43. Haralambieva E, Adam P, Ventura R, Katzenberger T, Kalla J et al. 2006. Genetic rearrangement of FOXP1 is predominantly detected in a subset of diffuse large B-cell lymphomas with extranodal presentation. Leukemia 20:1300–3
    [Google Scholar]
44. Hashwah H, Schmid CA, Kasser S, Bertram K, Stelling A et al. 2017. Inactivation of CREBBP expands the germinal center B cell compartment, down-regulates MHCII expression and promotes DLBCL growth. PNAS 114:9701–6
    [Google Scholar]
45. Hatzi K, Geng H, Doane AS, Meydan C, LaRiviere R et al. 2019. Histone demethylase LSD1 is required for germinal center formation and BCL6-driven lymphomagenesis. Nat. Immunol. 20:86–96
    [Google Scholar]
46. Hatzi K, Jiang Y, Huang C, Garrett-Bakelman F, Gearhart MD et al. 2013. A hybrid mechanism of action for BCL6 in B cells defined by formation of functionally distinct complexes at enhancers and promoters. Cell Rep 4:578–88
    [Google Scholar]
47. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39:311–18
    [Google Scholar]
48. Ho AW, Hatjiharissi E, Ciccarelli BT, Branagan AR, Hunter ZR et al. 2008. CD27-CD70 interactions in the pathogenesis of Waldenström macroglobulinemia. Blood 112:4683–89
    [Google Scholar]
49. Hobeika E, Maity PC, Jumaa H 2016. Control of B cell responsiveness by isotype and structural elements of the antigen receptor. Trends Immunol 37:310–20
    [Google Scholar]
50. Huang C, Geng H, Boss I, Wang L, Melnick A 2014a. Cooperative transcriptional repression by BCL6 and BACH2 in germinal center B-cell differentiation. Blood 123:1012–20
    [Google Scholar]
51. Huang C, Gonzalez DG, Cote CM, Jiang Y, Hatzi K et al. 2014b. The BCL6 RD2 domain governs commitment of activated B cells to form germinal centers. Cell Rep 8:1497–508
    [Google Scholar]
52. Hunter ZR, Xu L, Tsakmaklis N, Demos MG, Kofides A et al. 2018. Insights into the genomic landscape of MYD88 wild-type Waldenström macroglobulinemia. Blood Adv 2:2937–46
    [Google Scholar]
53. Jepsen K, Gleiberman AS, Shi C, Simon DI, Rosenfeld MG 2008. Cooperative regulation in development by SMRT and FOXP1. Genes Dev 22:740–45
    [Google Scholar]
54. Jiang Y, Ortega-Molina A, Geng H, Ying HY, Hatzi K et al. 2017. CREBBP inactivation promotes the development of HDAC3-dependent lymphomas. Cancer Discov 7:38–53
    [Google Scholar]
55. Kania A, Scharer CD, Price MJ, Haines RR, Alexander-George L-E, Boss J 2019. H3K27me3-specific demethylases modulate B cell development and differentiation. J. Immunol. 202:188.15
    [Google Scholar]
56. Kiel MJ, Velusamy T, Betz BL, Zhao L, Weigelin HG et al. 2012. Whole-genome sequencing identifies recurrent somatic NOTCH2 mutations in splenic marginal zone lymphoma. J. Exp. Med. 209:1553–65
    [Google Scholar]
57. Korfi K, Ali S, Heward JA, Fitzgibbon J 2017. Follicular lymphoma, a B cell malignancy addicted to epigenetic mutations. Epigenetics 12:370–77
    [Google Scholar]
58. Kulis M, Merkel A, Heath S, Queiros AC, Schuyler RP et al. 2015. Whole-genome fingerprint of the DNA methylome during human B cell differentiation. Nat. Genet. 47:746–56
    [Google Scholar]
59. Lai AY, Mav D, Shah R, Grimm SA, Phadke D et al. 2013. DNA methylation profiling in human B cells reveals immune regulatory elements and epigenetic plasticity at Alu elements during B-cell activation. Genome Res 23:2030–41
    [Google Scholar]
60. Laidlaw BJ, Duan L, Xu Y, Vazquez SE, Cyster JG 2020. The transcription factor Hhex cooperates with the corepressor Tle3 to promote memory B cell development. Nat. Immunol. 21:1082–93
    [Google Scholar]
61. Li X, Zhang Y, Zheng L, Liu M, Chen CD, Jiang H 2018. UTX is an escape from X-inactivation tumor-suppressor in B cell lymphoma. Nat. Commun. 9:2720
    [Google Scholar]
62. Limpens J, Stad R, Vos C, de Vlaam C, de Jong D et al. 1995. Lymphoma-associated translocation t(14;18) in blood B cells of normal individuals. Blood 85:2528–36
    [Google Scholar]
63. Liu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC et al. 2008. Two levels of protection for the B cell genome during somatic hypermutation. Nature 451:841–45
    [Google Scholar]
64. Love C, Sun Z, Jima D, Li G, Zhang J et al. 2012. The genetic landscape of mutations in Burkitt lymphoma. Nat. Genet. 44:1321–25
    [Google Scholar]
65. Maitre E, Bertrand P, Maingonnat C, Viailly PJ, Wiber M et al. 2018. New generation sequencing of targeted genes in the classical and the variant form of hairy cell leukemia highlights mutations in epigenetic regulation genes. Oncotarget 9:28866–76
    [Google Scholar]
66. Mansouri L, Wierzbinska JA, Plass C, Rosenquist R 2018. Epigenetic deregulation in chronic lymphocytic leukemia: clinical and biological impact. Semin. Cancer Biol. 51:1–11
    [Google Scholar]
67. Mesin L, Ersching J, Victora GD 2016. Germinal center B cell dynamics. Immunity 45:471–82
    [Google Scholar]
68. Mesin L, Schiepers A, Ersching J, Barbulescu A, Cavazzoni CB et al. 2020. Restricted clonality and limited germinal center reentry characterize memory B cell reactivation by boosting. Cell 180:92–106.e11
    [Google Scholar]
69. Meyer SN, Scuoppo C, Vlasevska S, Bal E, Holmes AB et al. 2019. Unique and shared epigenetic programs of the CREBBP and EP300 acetyltransferases in germinal center B cells reveal targetable dependencies in lymphoma. Immunity 51:535–47.e9
    [Google Scholar]
70. Mlynarczyk C, Fontan L, Melnick A 2019. Germinal center-derived lymphomas: the darkest side of humoral immunity. Immunol. Rev. 288:214–39
    [Google Scholar]
71. Mondello P, Tadros S, Teater M, Fontan L, Chang AY et al. 2020. Selective inhibition of HDAC3 targets synthetic vulnerabilities and activates immune surveillance in lymphoma. Cancer Discov 10:440–59
    [Google Scholar]
72. Montes-Moreno S, Martinez-Magunacelaya N, Zecchini-Barrese T, Villambrosia SG, Linares E et al. 2017. Plasmablastic lymphoma phenotype is determined by genetic alterations in MYC and PRDM1.Mod. . Pathol 30:85–94
    [Google Scholar]
73. Morschhauser F, Tilly H, Chaidos A, Phillips TJ, Ribrag V et al. 2019. Phase 2 multicenter study of tazemetostat, an EZH2 inhibitor, in patients with relapsed or refractory follicular lymphoma. Blood 134:123
    [Google Scholar]
74. Muppidi JR, Schmitz R, Green JA, Xiao W, Larsen AB et al. 2014. Loss of signalling via Gα13 in germinal centre B-cell-derived lymphoma. Nature 516:254–58
    [Google Scholar]
75. Nemajerova A, Petrenko O, Trumper L, Palacios G, Moll UM 2010. Loss of p73 promotes dissemination of Myc-induced B cell lymphomas in mice. J. Clin. Investig. 120:2070–80
    [Google Scholar]
76. Ortega-Molina A, Boss IW, Canela A, Pan H, Jiang Y et al. 2015. The histone lysine methyltransferase KMT2D sustains a gene expression program that represses B cell lymphoma development. Nat. Med. 21:1199–208
    [Google Scholar]
77. Paik JH, Nam SJ, Kim TM, Heo DS, Kim CW, Jeon YK 2014. Overexpression of sphingosine-1-phosphate receptor 1 and phospho-signal transducer and activator of transcription 3 is associated with poor prognosis in rituximab-treated diffuse large B-cell lymphomas. BMC Cancer 14:911
    [Google Scholar]
78. Pals ST, de Gorter DJ, Spaargaren M 2007. Lymphoma dissemination: the other face of lymphocyte homing. Blood 110:3102–11
    [Google Scholar]
79. Papa I, Vinuesa CG. 2018. Synaptic interactions in germinal centers. Front. Immunol. 9:1858
    [Google Scholar]
80. Parry M, Rose-Zerilli MJ, Ljungstrom V, Gibson J, Wang J et al. 2015. Genetics and prognostication in splenic marginal zone lymphoma: revelations from deep sequencing. Clin. Cancer Res. 21:4174–83
    [Google Scholar]
81. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A et al. 2011. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 471:189–95
    [Google Scholar]
82. Pawlyn C, Kaiser MF, Heuck C, Melchor L, Wardell CP et al. 2016. The spectrum and clinical impact of epigenetic modifier mutations in myeloma. Clin. Cancer Res. 22:5783–94
    [Google Scholar]
83. Pei JH, Luo SQ, Zhong Y, Chen JH, Xiao HW, Hu WX 2011. The association between non-Hodgkin lymphoma and methylation of p73. Tumour Biol 32:1133–38
    [Google Scholar]
84. Polo JM, Ci W, Licht JD, Melnick A 2008. Reversible disruption of BCL6 repression complexes by CD40 signaling in normal and malignant B cells. Blood 112:644–51
    [Google Scholar]
85. Popovic R, Martinez-Garcia E, Giannopoulou EG, Zhang Q, Zhang Q et al. 2014. Histone methyltransferase MMSET/NSD2 alters EZH2 binding and reprograms the myeloma epigenome through global and focal changes in H3K36 and H3K27 methylation. PLOS Genet 10:e1004566
    [Google Scholar]
86. Price MJ, Scharer CD, Kania AK, Mi T, Hicks SL et al. 2019. Epigenetic priming underpins enhanced memory B cell differentiation. J. Immunol. 202:123.8
    [Google Scholar]
87. Roccaro AM, Sacco A, Jia X, Azab AK, Maiso P et al. 2010. microRNA-dependent modulation of histone acetylation in Waldenström macroglobulinemia. Blood 116:1506–14
    [Google Scholar]
88. Roco JA, Mesin L, Binder SC, Nefzger C, Gonzalez-Figueroa P et al. 2019. Class-switch recombination occurs infrequently in germinal centers. Immunity 51:337–50.e7
    [Google Scholar]
89. Rosikiewicz W, Chen X, Dominguez PM, Ghamlouch H, Aoufouchi S et al. 2020. TET2 deficiency reprograms the germinal center B cell epigenome and silences genes linked to lymphomagenesis. Sci. Adv. 6:eaay5872
    [Google Scholar]
90. Sagardoy A, Martinez-Ferrandis JI, Roa S, Bunting KL, Aznar MA et al. 2013. Downregulation of FOXP1 is required during germinal center B-cell function. Blood 121:4311–20
    [Google Scholar]
91. Sahasrabuddhe AA, Chen X, Chung F, Velusamy T, Lim MS, Elenitoba-Johnson KS 2015. Oncogenic Y641 mutations in EZH2 prevent Jak2/β-TrCP-mediated degradation. Oncogene 34:445–54
    [Google Scholar]
92. Sahota SS, Babbage G, Weston-Bell NJ 2009. CD27 in defining memory B-cell origins in Waldenström's macroglobulinemia. Clin. Lymphoma Myeloma 9:33–35
    [Google Scholar]
93. Scharer CD, Barwick BG, Guo M, Bally APR, Boss JM 2018. Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs. Nat. Commun. 9:1698
    [Google Scholar]
94. Schmitz R, Wright GW, Huang DW, Johnson CA, Phelan JD et al. 2018. Genetics and pathogenesis of diffuse large B-cell lymphoma. N. Engl. J. Med. 378:1396–407
    [Google Scholar]
95. Schroeder HW Jr, Cavacini L. 2010. Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125:S41–52
    [Google Scholar]
96. Seifert M, Przekopowitz M, Taudien S, Lollies A, Ronge V et al. 2015. Functional capacities of human IgM memory B cells in early inflammatory responses and secondary germinal center reactions. PNAS 112:E546–55
    [Google Scholar]
97. Sermer D, Pasqualucci L, Wendel HG, Melnick A, Younes A 2019. Emerging epigenetic-modulating therapies in lymphoma. Nat. Rev. Clin. Oncol. 16:494–507
    [Google Scholar]
98. Shinnakasu R, Inoue T, Kometani K, Moriyama S, Adachi Y et al. 2016. Regulated selection of germinal-center cells into the memory B cell compartment. Nat. Immunol. 17:861–69
    [Google Scholar]
99. Sneeringer CJ, Scott MP, Kuntz KW, Knutson SK, Pollock RM et al. 2010. Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. PNAS 107:20980–85
    [Google Scholar]
100. Spina V, Khiabanian H, Messina M, Monti S, Cascione L et al. 2016. The genetics of nodal marginal zone lymphoma. Blood 128:1362–73
     [Google Scholar]
101. Stathis A, Bertoni F. 2018. BET proteins as targets for anticancer treatment. Cancer Discov 8:24–36
     [Google Scholar]
102. Stelling A, Wu CT, Bertram K, Hashwah H, Theocharides APA et al. 2019. Pharmacological DNA demethylation restores SMAD1 expression and tumor suppressive signaling in diffuse large B-cell lymphoma. Blood Adv 3:3020–32
     [Google Scholar]
103. Stengel KR, Bhaskara S, Wang J, Liu Q, Ellis JD et al. 2019. Histone deacetylase 3 controls a transcriptional network required for B cell maturation. Nucleic Acids Res 47:10612–27
     [Google Scholar]
104. Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature 403:41–45
     [Google Scholar]
105. Sungalee S, Mamessier E, Morgado E, Gregoire E, Brohawn PZ et al. 2014. Germinal center reentries of BCL2-overexpressing B cells drive follicular lymphoma progression. J. Clin. Investig. 124:5337–51
     [Google Scholar]
106. Tian L, Chavez M, Wartman LD 2018. The complex role of KDM6A in B-cell development and function. Blood 132:513
     [Google Scholar]
107. Venturutti L, Teater M, Zhai A, Chadburn A, Babiker L et al. 2020. TBL1XR1 mutations drive extranodal lymphoma by introducing a protumorigenic memory fate. Cell 182:297–316.e27
     [Google Scholar]
108. Vikova V, Jourdan M, Robert N, Requirand G, Boireau S et al. 2019. Comprehensive characterization of the mutational landscape in multiple myeloma cell lines reveals potential drivers and pathways associated with tumor progression and drug resistance. Theranostics 9:540–53
     [Google Scholar]
109. Vinuesa CG, Linterman MA, Goodnow CC, Randall KL 2010. T cells and follicular dendritic cells in germinal center B-cell formation and selection. Immunol. Rev. 237:72–89
     [Google Scholar]
110. Weisel FJ, Shlomchik M. 2017. Memory B cells of mice and humans. Annu. Rev. Immunol. 35:255–84
     [Google Scholar]
111. Weisel FJ, Zuccarino-Catania GV, Chikina M, Shlomchik MJ 2016. A temporal switch in the germinal center determines differential output of memory B and plasma cells. Immunity 44:116–30
     [Google Scholar]
112. Wright GW, Huang DW, Phelan JD, Coulibaly ZA, Roulland S et al. 2020. A probabilistic classification tool for genetic subtypes of diffuse large B cell lymphoma with therapeutic implications. Cancer Cell 37:551–68.e14
     [Google Scholar]
113. Wright GW, Tan B, Rosenwald A, Hurt EH, Wiestner A, Staudt LM 2003. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. PNAS 100:9991–96
     [Google Scholar]
114. Wu X, Zhang Y. 2017. TET-mediated active DNA demethylation: mechanism, function and beyond. Nat. Rev. Genet. 18:517–34
     [Google Scholar]
115. Xu L, Ciccarelli B, Hatjiharissi E, Yang G, Zhou Y et al. 2009. Aberrant DNA methylation and transcriptional silencing of DLC-1 in Waldenstrom's macroglobulinemia. Blood 114:2954–54
     [Google Scholar]
116. Yu X, Li W, Deng Q, Li L, Hsi ED et al. 2018. MYD88 L265P mutation in lymphoid malignancies. Cancer Res 78:2457–62
     [Google Scholar]
117. Zhang J, Dominguez-Sola D, Hussein S, Lee JE, Holmes AB et al. 2015. Disruption of KMT2D perturbs germinal center B cell development and promotes lymphomagenesis. Nat. Med. 21:1190–98
     [Google Scholar]
118. Zhang J, Jima D, Moffitt AB, Liu Q, Czader M et al. 2014. The genomic landscape of mantle cell lymphoma is related to the epigenetically determined chromatin state of normal B cells. Blood 123:2988–96
     [Google Scholar]
119. Zhang J, Kalkum M, Chait BT, Roeder RG 2002. The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol. Cell 9:611–23
     [Google Scholar]
120. Zhang J, Vlasevska S, Wells VA, Nataraj S, Holmes AB et al. 2017. The CREBBP acetyltransferase is a haploinsufficient tumor suppressor in B-cell lymphoma. Cancer Discov 7:322–37
     [Google Scholar]
121. Zhang YW, Wang Z, Xie W, Cai Y, Xia L et al. 2017. Acetylation enhances TET2 function in protecting against abnormal DNA methylation during oxidative stress. Mol. Cell 65:323–35
     [Google Scholar]
122. Zhao S, Zhu W, Xue S, Han D 2014. Testicular defense systems: immune privilege and innate immunity. Cell Mol. Immunol. 11:428–37
     [Google Scholar]
123. Zhou Y, Liu W, Xu Z, Zhu H, Xiao D et al. 2018. Analysis of genomic alteration in primary central nervous system lymphoma and the expression of some related genes. Neoplasia 20:1059–69
     [Google Scholar]