Skip to main content

Advertisement

SpringerLink
Log in

Epigenetics and Lymphoma: Can We Use Epigenetics to Prime or Reset Chemoresistant Lymphoma Programs?

  • Lymphomas (PA Hamlin, Section Editor)
  • Published:
Current Oncology Reports Aims and scope Submit manuscript

Abstract

Non-Hodgkin lymphoma is a diverse group of lymphocyte-derived neoplasms. Although a heterogeneous group of malignancies, it has become apparent that epigenetic alterations, such as disturbances of DNA methylation and histone modification, are a common occurrence in both B cell and T cell lymphomas, contributing to lymphomagenesis. As a result, the use of epigenetic targeted therapy has been incorporated into various pre-clinical and clinical studies, demonstrating significant efficacy in lymphoma, with vorinostat becoming the first epigenetic therapy to receive FDA approval in any malignancy. The role of epigenetic drugs is evolving, with its potential use in combination therapy as well as a means of overcoming chemotherapy resistance. In this review, we discuss the epigenetic alterations in non-Hodgkin lymphomas as well as provide an overview of current epigenetic drugs and their role in clinical practice, and on-going clinical trials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. Waddington CH. Preliminary notes on the development of the wings in normal and mutant strains of drosophila. Proc Natl Acad Sci U S A. 1939;25(7):299–307.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Feinberg AP, Cui H, Ohlsson R. DNA methylation and genomic imprinting: insights from cancer into epigenetic mechanisms. Semin Cancer Biol. 2002;12(5):389–98.

    Article  CAS  PubMed  Google Scholar 

  3. Reik W, Lewis A. Co-evolution of X-chromosome inactivation and imprinting in mammals. Nat Rev Genet. 2005;6(5):403–10.

    Article  CAS  PubMed  Google Scholar 

  4. Bestor TH. Transposons reanimated in mice. Cell. 2005;122(3):322–5.

    Article  CAS  PubMed  Google Scholar 

  5. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell. 2012;150(1):12–27.

    Article  CAS  PubMed  Google Scholar 

  6. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med. 2003;349(21):2042–54.

    Article  CAS  PubMed  Google Scholar 

  7. Mack GS. Epigenetic cancer therapy makes headway. J Natl Cancer Inst. 2006;98(20):1443–4.

    Article  PubMed  Google Scholar 

  8. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell. 2007;128(4):669–81.

    Article  CAS  PubMed  Google Scholar 

  9. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 1997;90(4):595–606.

    Article  CAS  PubMed  Google Scholar 

  10. Rothgiesser KM, Fey M, Hottiger MO. Acetylation of p65 at lysine 314 is important for late NF-kappaB-dependent gene expression. BMC Genomics. 2010;11:22.

    Article  PubMed Central  PubMed  Google Scholar 

  11. Cerchietti LC, et al. BCL6 repression of EP300 in human diffuse large B cell lymphoma cells provides a basis for rational combinatorial therapy. J Clin Invest. 2010.

  12. Smith BC, Hallows WC, Denu JM. Mechanisms and molecular probes of sirtuins. Chem Biol. 2008;15(10):1002–13.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer. 2006;6(1):38–51.

    Article  CAS  PubMed  Google Scholar 

  14. Yang XJ, Seto E. HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene. 2007;26(37):5310–8.

    Article  CAS  PubMed  Google Scholar 

  15. Velichutina I et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood. 2010;116(24):5247–55.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Morin RD et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature. 2011;476(7360):298–303.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Morin RD et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. 2010;42(2):181–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Bodor C et al. EZH2 Y641 mutations in follicular lymphoma. Leukemia. 2011;25(4):726–9.

    Article  CAS  PubMed  Google Scholar 

  19. Bracken AP, Helin K. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer. 2009;9(11):773–84.

    Article  CAS  PubMed  Google Scholar 

  20. Su IH et al. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol. 2003;4(2):124–31.

    Article  CAS  PubMed  Google Scholar 

  21. Chi P, Allis CD, Wang GG. Covalent histone modifications—miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer. 2010;10(7):457–69.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Liu H et al. Phosphorylation of MLL by ATR is required for execution of mammalian S-phase checkpoint. Nature. 2010;467(7313):343–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Esteller M et al. A gene hypermethylation profile of human cancer. Cancer Res. 2001;61(8):3225–9.

    CAS  PubMed  Google Scholar 

  24. Martinez-Delgado B et al. Hypermethylation of a 5′ CpG island of p16 is a frequent event in non-Hodgkin’s lymphoma. Leukemia. 1997;11(3):425–8.

    Article  CAS  PubMed  Google Scholar 

  25. Odejide O et al. A targeted mutational landscape of angioimmunoblastic T-cell lymphoma. Blood. 2014;123(9):1293–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Cairns RA et al. IDH2 mutations are frequent in angioimmunoblastic T-cell lymphoma. Blood. 2012;119(8):1901–3.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Lemonnier F et al. Recurrent TET2 mutations in peripheral T-cell lymphomas correlate with TFH-like features and adverse clinical parameters. Blood. 2012;120(7):1466–9.

    Article  CAS  PubMed  Google Scholar 

  28. Couronne L, Bastard C, Bernard OA. TET2 and DNMT3A mutations in human T-cell lymphoma. N Engl J Med. 2012;366(1):95–6.

    Article  CAS  PubMed  Google Scholar 

  29. Losman JA, Kaelin Jr WG. What a difference a hydroxyl makes: mutant IDH, (R)-2-hydroxyglutarate, and cancer. Genes Dev. 2013;27(8):836–52.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Losman JA et al. (R)-2-hydroxyglutarate is sufficient to promote leukemogenesis and its effects are reversible. Science. 2013;339(6127):1621–5.

    Article  CAS  PubMed  Google Scholar 

  31. Rohle D et al. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science. 2013;340(6132):626–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Davis MI et al. Biochemical, cellular, and biophysical characterization of a potent inhibitor of mutant isocitrate dehydrogenase IDH1. J Biol Chem. 2014;289(20):13717–25.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Friend C et al. Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc Natl Acad Sci U S A. 1971;68(2):378–82.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. O’Connor OA. For disease in need, a friend indeed. Blood. 2011;117(22):5787–8.

    Article  PubMed  Google Scholar 

  35. Taunton J, Hassig CA, Schreiber SL. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science. 1996;272(5260):408–11.

    Article  CAS  PubMed  Google Scholar 

  36. Duvic M et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood. 2007;109(1):31–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Olsen EA et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol. 2007;25(21):3109–15.

    Article  CAS  PubMed  Google Scholar 

  38. Piekarz RL et al. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol. 2009;27(32):5410–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Whittaker SJ et al. Final results from a multicenter, international, pivotal study of romidepsin in refractory cutaneous T-cell lymphoma. J Clin Oncol. 2010;28(29):4485–91.

    Article  CAS  PubMed  Google Scholar 

  40. Piekarz RL et al. Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood. 2011;117(22):5827–34.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Coiffier B et al. Results from a pivotal, open-label, phase II study of romidepsin in relapsed or refractory peripheral T-cell lymphoma after prior systemic therapy. J Clin Oncol. 2012;30(6):631–6.

    Article  CAS  PubMed  Google Scholar 

  42. O’Connor OA MT, Savage KJ, Pinter-Brown LC, Foss FM, Popplewell L, et al. Belinostat, a novel pan-histone deacetylase inhibitor (HDACi), in relapsed or refractory peripheral T-cell lymphoma (R/RPTCL): results from the BELIEF trial. J Clin Oncol. 2013;31 (suppl 1145; abstr 8507).

  43. Kelly WK et al. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol. 2005;23(17):3923–31.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Kelly WK et al. Phase I clinical trial of histone deacetylase inhibitor: suberoylanilide hydroxamic acid administered intravenously. Clin Cancer Res. 2003;9(10 Pt 1):3578–88.

    CAS  PubMed  Google Scholar 

  45. Bates SE et al. Laboratory correlates for a phase II trial of romidepsin in cutaneous and peripheral T-cell lymphoma. Br J Haematol. 2010;148(2):256–67.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Sandor V et al. P21-dependent g(1)arrest with downregulation of cyclin D1 and upregulation of cyclin E by the histone deacetylase inhibitor FR901228. Br J Cancer. 2000;83(6):817–25.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Zhang C et al. Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: relevance to mechanism of therapeutic action. J Invest Dermatol. 2005;125(5):1045–52.

    Article  CAS  PubMed  Google Scholar 

  48. Kirschbaum M et al. Phase II study of vorinostat for treatment of relapsed or refractory indolent non-Hodgkin’s lymphoma and mantle cell lymphoma. J Clin Oncol. 2011;29(9):1198–203.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Crump M et al. Phase II trial of oral vorinostat (suberoylanilide hydroxamic acid) in relapsed diffuse large-B-cell lymphoma. Ann Oncol. 2008;19(5):964–9.

    Article  CAS  PubMed  Google Scholar 

  50. Amengual JE et al. Sirtuin and pan-class I/II deacetylase (DAC) inhibition is synergistic in preclinical models and clinical studies of lymphoma. Blood. 2013;122(12):2104–13.

    Article  CAS  PubMed  Google Scholar 

  51. Sandor V et al. Phase I trial of the histone deacetylase inhibitor, depsipeptide (FR901228, NSC 630176), in patients with refractory neoplasms. Clin Cancer Res. 2002;8(3):718–28.

    CAS  PubMed  Google Scholar 

  52. San-Miguel JF et al. Panobinostat plus bortezomib and dexamethasone versus placebo plus bortezomib and dexamethasone in patients with relapsed or relapsed and refractory multiple myeloma: a multicentre, randomised, double-blind phase 3 trial. Lancet Oncol. 2014;15(11):1195–206.

    Article  CAS  PubMed  Google Scholar 

  53. Lee TT, Karon MR. Inhibition of protein synthesis in 5-azacytidine-treated HeLa cells. Biochem Pharmacol. 1976;25(15):1737–42.

    Article  CAS  PubMed  Google Scholar 

  54. Santi DV, Garrett CE, Barr PJ. On the mechanism of inhibition of DNA-cytosine methyltransferases by cytosine analogs. Cell. 1983;33(1):9–10.

    Article  CAS  PubMed  Google Scholar 

  55. Fenaux P et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol. 2009;10(3):223–32.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Lubbert M et al. Low-dose decitabine versus best supportive care in elderly patients with intermediate- or high-risk myelodysplastic syndrome (MDS) ineligible for intensive chemotherapy: final results of the randomized phase III study of the European Organisation for Research and Treatment of Cancer Leukemia Group and the German MDS Study Group. J Clin Oncol. 2011;29(15):1987–96.

    Article  PubMed  Google Scholar 

  57. Blum KA et al. Phase I trial of low dose decitabine targeting DNA hypermethylation in patients with chronic lymphocytic leukaemia and non-Hodgkin lymphoma: dose-limiting myelosuppression without evidence of DNA hypomethylation. Br J Haematol. 2010;150(2):189–95.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Stewart DJ et al. Decitabine effect on tumor global DNA methylation and other parameters in a phase I trial in refractory solid tumors and lymphomas. Clin Cancer Res. 2009;15(11):3881–8.

    Article  CAS  PubMed  Google Scholar 

  59. Cameron EE et al. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat Genet. 1999;21(1):103–7.

    Article  CAS  PubMed  Google Scholar 

  60. Kikuchi T et al. Inactivation of p57KIP2 by regional promoter hypermethylation and histone deacetylation in human tumors. Oncogene. 2002;21(17):2741–9.

    Article  CAS  PubMed  Google Scholar 

  61. Yang H et al. Antileukemia activity of the combination of 5-aza-2′-deoxycytidine with valproic acid. Leuk Res. 2005;29(7):739–48.

    Article  CAS  PubMed  Google Scholar 

  62. Stathis A et al. Phase I study of decitabine in combination with vorinostat in patients with advanced solid tumors and non-Hodgkin’s lymphomas. Clin Cancer Res. 2011;17(6):1582–90.

    Article  CAS  PubMed  Google Scholar 

  63. Garcia-Manero G et al. Phase 1/2 study of the combination of 5-aza-2′-deoxycytidine with valproic acid in patients with leukemia. Blood. 2006;108(10):3271–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Braiteh F et al. Phase I study of epigenetic modulation with 5-azacytidine and valproic acid in patients with advanced cancers. Clin Cancer Res. 2008;14(19):6296–301.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. Gore SD et al. Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer Res. 2006;66(12):6361–9.

    Article  CAS  PubMed  Google Scholar 

  66. Kalac M et al. HDAC inhibitors and decitabine are highly synergistic and associated with unique gene-expression and epigenetic profiles in models of DLBCL. Blood. 2011;118(20):5506–16. Compared to single agent activity, the use of hypomethylating agents in combination with HDAC inhibitors in DLBCL models demonstrated significant tumor growth inhibition and apoptosis with a unique gene expression after treatment. This data suggests a potential role of combinational epigenetic therapy in DLBCL.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. O’Connor OA et al. The combination of hypomethylating agents and histone deacetylase inhibitors (HDACi) are synergistically cytotoxic and reverse the malignant phenotype in preclinical models of T-Cell lymphoma. Clin Adv Hematol Oncol. 2013;122:646.

    Google Scholar 

  68. Love C et al. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet. 2012;44(12):1321–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Nikoloski G et al. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat Genet. 2010;42(8):665–7.

    Article  CAS  PubMed  Google Scholar 

  70. Visser HP et al. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol. 2001;112(4):950–8.

    Article  CAS  PubMed  Google Scholar 

  71. Eckerle S et al. Gene expression profiling of isolated tumour cells from anaplastic large cell lymphomas: insights into its cellular origin, pathogenesis and relation to Hodgkin lymphoma. Leukemia. 2009;23(11):2129–38.

    Article  CAS  PubMed  Google Scholar 

  72. Sasaki D et al. Overexpression of enhancer of zeste homolog 2 with trimethylation of lysine 27 on histone H3 in adult T-cell leukemia/lymphoma as a target for epigenetic therapy. Haematologica. 2011;96(5):712–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Fiskus W et al. Combined epigenetic therapy with the histone methyltransferase EZH2 inhibitor 3-deazaneplanocin A and the histone deacetylase inhibitor panobinostat against human AML cells. Blood. 2009;114(13):2733–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. McCabe MT et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. 2012;492(7427):108–12.

    Article  CAS  PubMed  Google Scholar 

  75. Fojo T. Multiple paths to a drug resistance phenotype: mutations, translocations, deletions and amplification of coding genes or promoter regions, epigenetic changes and microRNAs. Drug Resist Updat. 2007;10(1-2):59–67.

    Article  CAS  PubMed  Google Scholar 

  76. Glasspool RM, Teodoridis JM, Brown R. Epigenetics as a mechanism driving polygenic clinical drug resistance. Br J Cancer. 2006;94(8):1087–92.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Herman JG et al. Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci U S A. 1994;91(21):9700–4.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Merlo A et al. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat Med. 1995;1(7):686–92.

    Article  CAS  PubMed  Google Scholar 

  79. Herman JG et al. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res. 1995;55(20):4525–30.

    CAS  PubMed  Google Scholar 

  80. Gonzalez-Zulueta M et al. Methylation of the 5′ CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res. 1995;55(20):4531–5.

    CAS  PubMed  Google Scholar 

  81. Kucuk C, et al. Global promoter methylation analysis reveals novel candidate tumor suppressor genes in natural killer cell lymphoma. Clin Cancer Res. 2015.

  82. Hayslip J, Montero A. Tumor suppressor gene methylation in follicular lymphoma: a comprehensive review. Mol Cancer. 2006;5:44.

    Article  PubMed Central  PubMed  Google Scholar 

  83. Soengas MS et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature. 2001;409(6817):207–11.

    Article  CAS  PubMed  Google Scholar 

  84. Furukawa Y et al. Methylation silencing of the Apaf-1 gene in acute leukemia. Mol Cancer Res. 2005;3(6):325–34.

    Article  CAS  PubMed  Google Scholar 

  85. Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol. 2003;15(2):172–83.

    Article  CAS  PubMed  Google Scholar 

  86. Clozel T et al. Mechanism-based epigenetic chemosensitization therapy of diffuse large B-cell lymphoma. Cancer Discov. 2013;3(9):1002–19. DNA hypermethylation of SMAD1 contributes to doxorubicin resistance in DLBCL cell lines. This resistance can be reversed with pre-treatment using decitabine prior to standard R-CHOP therapy.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  87. Jain S, et al. Preclinical pharmacologic evaluation of pralatrexate and romidepsin confirms potent synergy of the combination in a murine model of human t-cell lymphoma. Clin Cancer Res. 2015. Treatment of T-cell lymphoma mouse models with pralatrexate and romidepsin led to complete responses in all models tested. This drug combination is currently under investigation in a Phase I/II clinical trial.

  88. Zullo K et al. The aurora a kinase inhibitor, alisertib, has broad activity in nonclinical models Of T-Cell lymphoma and is highly synergistic with romidepsin, but not with pralatrexate or the proteasome inhibitor, ixazomib. Blood. 2013;122:5141.

    Google Scholar 

  89. Sharma SV et al. Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer. 2007;7(3):169–81.

    Article  CAS  PubMed  Google Scholar 

  90. Gray JE et al. A phase I, pharmacokinetic, and pharmacodynamic study of panobinostat, an HDAC inhibitor, combined with erlotinib in patients with advanced aerodigestive tract tumors. Clin Cancer Res. 2014;20(6):1644–55.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Compliance with Ethics Guidelines

ᅟ

Conflict of Interest

Jennifer K. Lue declares that she has no conflict of interest. Jennifer E. Amengual declares that she has no conflict of interest. Owen A. O’Connor has received research support through grants from Celgene and Spectrum Pharmaceuticals.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Author information

Authors and Affiliations

  1. Center for Lymphoid Malignancies, Herbert Irving Comprehensive Cancer Center, Columbia University Medical Center, Columbia University, New York, NY, USA

    Jennifer K. Lue, Jennifer E. Amengual & Owen A. O’Connor

Authors
  1. Jennifer K. Lue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer E. Amengual
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Owen A. O’Connor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Owen A. O’Connor.

Additional information

This article is part of the Topical Collection on Lymphomas

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lue, J.K., Amengual, J.E. & O’Connor, O.A. Epigenetics and Lymphoma: Can We Use Epigenetics to Prime or Reset Chemoresistant Lymphoma Programs?. Curr Oncol Rep 17, 40 (2015). https://doi.org/10.1007/s11912-015-0464-y

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11912-015-0464-y

Keywords

Search

Navigation