283
Views
9
CrossRef citations to date
0
Altmetric
Reviews

Emerging role of histone deacetylase inhibitors in the treatment of diffuse large B-cell lymphoma

ORCID Icon, ORCID Icon & ORCID Icon
Pages 763-775 | Received 02 Jul 2019, Accepted 04 Nov 2019, Published online: 26 Nov 2019

References

  • Al-Hamadani M, Habermann TM, Cerhan JR, et al. Non-Hodgkin lymphoma subtype distribution, geodemographic patterns, and survival in the US: a longitudinal analysis of the National Cancer Data Base from 1998 to 2011. Am J Hematol. 2015;90(9):790–795.
  • Farooq U, Maurer MJ, Thompson CA, et al. Clinical heterogeneity of diffuse large B cell lymphoma following failure of front-line immunochemotherapy. Br J Haematol. 2017;179(1):50–60.
  • Mai A, Massa S, Rotili D, et al. Histone deacetylation in epigenetics: an attractive target for anticancer therapy. Med Res Rev. 2005;25(3):261–309.
  • Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. JCO. 2009;27(32):5459–5468.
  • Gallinari P, Di Marco S, Jones P, et al. HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Res. 2007;17(3):195–211.
  • Marks PA, Miller T, Richon VM. Histone deacetylases. Curr Opin Pharmacol. 2003;3(4):344–351.
  • Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem. 2001;70(1):81–120.
  • Seto E, Yoshida M. Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb Perspect Biol. 2014;6(4):a018713.
  • Ropero S, Esteller M. The role of histone deacetylases (HDACs) in human cancer. Mol Oncol. 2007;1(1):19–25.
  • Choudhary C, Kumar C, Gnad F, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009;325(5942):834–840.
  • Morin RD, Mendez-Lago M, Mungall AJ, et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature. 2011;476(7360):298–303.
  • Pasqualucci L, Dominguez-Sola D, Chiarenza A, et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature. 2011;471(7337):189–195.
  • Gupta M, Han JJ, Stenson M, et al. Regulation of STAT3 by histone deacetylase-3 in diffuse large B-cell lymphoma: implications for therapy. Leukemia. 2012;26(6):1356–1364.
  • Gil VS, Bhagat G, Howell L, et al. Deregulated expression of HDAC9 in B cells promotes development of lymphoproliferative disease and lymphoma in mice. Dis Model Mech. 2016;9(12):1483–1495.
  • Jang KY, Hwang SH, Kwon KS, et al. SIRT1 expression is associated with poor prognosis of diffuse large B-cell lymphoma. Am J Surg Pathol. 2008;32(10):1523–1531.
  • Lee SH, Yoo C, Im S, et al. Expression of histone deacetylases in diffuse large B-cell lymphoma and its clinical significance. Int J Med Sci. 2014;11(10):994–1000.
  • Min SK, Koh YH, Park Y, et al. Expression of HAT1 and HDAC1, 2, 3 in diffuse large B-cell lymphomas, peripheral T-cell lymphomas, and NK/T-cell lymphomas. Korean J Pathol. 2012;46(2):142–150.
  • Marquard L, Poulsen CB, Gjerdrum LM, et al. Histone deacetylase 1, 2, 6 and acetylated histone H4 in B- and T-cell lymphomas. Histopathology. 2009;54(6):688–698.
  • Lin XJ, Cai LM, Qian ZJ, et al. Increased histone deacetylase 6 expression serves as a favorable prognostic factor for diffuse large B-cell lymphoma. Onco Targets Ther. 2017;10:5129–5136.
  • Seidel C, Schnekenburger M, Dicato M, et al. Histone deacetylase 6 in health and disease. Epigenomics. 2015;7(1):103–118.
  • Marquard L, Gjerdrum LM, Christensen IJ, et al. Prognostic significance of the therapeutic targets histone deacetylase 1, 2, 6 and acetylated histone H4 in cutaneous T-cell lymphoma. Histopathology. 2008;53(3):267–277.
  • Van Damme M, Crompot E, Meuleman N, et al. HDAC isoenzyme expression is deregulated in chronic lymphocytic leukemia B-cells and has a complex prognostic significance. Epigenetics. 2012;7(12):1403–1412.
  • Li Y, Seto E. HDACs and HDAC inhibitors in cancer development and therapy. Cold Spring Harb Perspect Med. 2016;6(10):a026831.
  • Cuccuini W, Briere J, Mounier N, et al. MYC + diffuse large B-cell lymphoma is not salvaged by classical R-ICE or R-DHAP followed by BEAM plus autologous stem cell transplantation. Blood. 2012;119(20):4619–4624.
  • Horn H, Ziepert M, Becher C, et al. MYC status in concert with BCL2 and BCL6 expression predicts outcome in diffuse large B-cell lymphoma. Blood. 2013;121(12):2253–2263.
  • Pedersen MO, Gang AO, Poulsen TS, et al. MYC translocation partner gene determines survival of patients with large B-cell lymphoma with MYC- or double-hit MYC/BCL2 translocations. Eur J Haematol. 2014;92(1):42–48.
  • Pillonel V, Reichert N, Cao C, et al. Histone deacetylase 1 plays a predominant pro-oncogenic role in Emu-myc driven B cell lymphoma. Sci Rep. 2016;6(1):37772.
  • Zhang X, Zhao X, Fiskus W, et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell. 2012;22(4):506–523.
  • Cai Q, Tu M, Xu-Monette ZY, et al. NF-kappaB p50 activation associated with immune dysregulation confers poorer survival for diffuse large B-cell lymphoma patients with wild-type p53. Mod Pathol. 2017;30(6):854–876.
  • Zhang M, Xu-Monette ZY, Li L, et al. RelA NF-kappaB subunit activation as a therapeutic target in diffuse large B-cell lymphoma. Aging. 2016;8(12):3321–3340.
  • Bhalla S, Balasubramanian S, David K, et al. PCI-24781 induces caspase and reactive oxygen species-dependent apoptosis through NF-kappaB mechanisms and is synergistic with bortezomib in lymphoma cells. Clin Cancer Res. 2009;15(10):3354–3365.
  • Li X, He Z, Cheng B, et al. Effect of BCLAF1 on HDAC inhibitor LMK-235-mediated apoptosis of diffuse large B cell lymphoma cells and its mechanism. Cancer Biol Ther. 2018;19:825–834.
  • Deng C, Lipstein M, Rodriguez R, et al. The novel IKK2 inhibitor LY2409881 potently synergizes with histone deacetylase inhibitors in preclinical models of lymphoma through the downregulation of NF-kappaB. Clin Cancer Res. 2015;21(1):134–145.
  • Ok CY, Chen J, Xu-Monette ZY, et al. Clinical implications of phosphorylated STAT3 expression in De Novo diffuse large B-cell lymphoma. Clin Cancer Res. 2014;20(19):5113–5123.
  • Wu ZL, Song YQ, Shi YF, et al. High nuclear expression of STAT3 is associated with unfavorable prognosis in diffuse large B-cell lymphoma. J Hematol Oncol. 2011;4(1):31.
  • Hacker S, Karl S, Mader I, et al. Histone deacetylase inhibitors prime medulloblastoma cells for chemotherapy-induced apoptosis by enhancing p53-dependent Bax activation. Oncogene. 2011;30(19):2275–2281.
  • Luo J, Su F, Chen D, et al. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature. 2000;408(6810):377–381.
  • Tang Y, Zhao W, Chen Y, et al. Acetylation is indispensable for p53 activation. Cell. 2008;133(4):612–626.
  • Seo SK, Jin HO, Woo SH, et al. Histone deacetylase inhibitors sensitize human non-small cell lung cancer cells to ionizing radiation through acetyl p53-mediated c-myc down-regulation. J Thorac Oncol. 2011;6(8):1313–1319.
  • Ellis L, Bots M, Lindemann RK, et al. The histone deacetylase inhibitors LAQ824 and LBH589 do not require death receptor signaling or a functional apoptosome to mediate tumor cell death or therapeutic efficacy. Blood. 2009;114(2):380–393.
  • Insinga A, Monestiroli S, Ronzoni S, et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med. 2005;11(1):71–76.
  • Sonnemann J, Marx C, Becker S, et al. p53-dependent and p53-independent anticancer effects of different histone deacetylase inhibitors. Br J Cancer. 2014;110(3):656–667.
  • Cai Y, Cui W, Chen W, et al. The effects of a histone deacetylase inhibitor on biological behavior of diffuse large B-cell lymphoma cell lines and insights into the underlying mechanisms. Cancer Cell Int. 2013;13(1):57.
  • Amengual JE, Clark-Garvey S, Kalac M, 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):2104–2113.
  • Lindemann RK, Newbold A, Whitecross KF, et al. Analysis of the apoptotic and therapeutic activities of histone deacetylase inhibitors by using a mouse model of B cell lymphoma. Proc Natl Acad Sci USA. 2007;104(19):8071–8076.
  • Fernandez-Rodriguez C, Salar A, Navarro A, et al. Anti-tumor activity of the combination of bendamustine with vorinostat in diffuse large B-cell lymphoma cells. Leuk Lymphoma. 2016;57(3):692–699.
  • Rimsza LM, Roberts RA, Miller TP, et al. Loss of MHC class II gene and protein expression in diffuse large B-cell lymphoma is related to decreased tumor immunosurveillance and poor patient survival regardless of other prognostic factors: a follow-up study from the Leukemia and Lymphoma Molecular Profiling Project. Blood. 2004;103(11):4251–4258.
  • Veelken H, Vik DS, Schulte MJ, et al. Immunophenotype as prognostic factor for diffuse large B-cell lymphoma in patients undergoing clinical risk-adapted therapy. Ann Oncol. 2007;18(5):931–939.
  • Beresford GW, Boss JM. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nat Immunol. 2001;2(7):652–657.
  • Magner WJ, Kazim AL, Stewart C, et al. Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors. J Immunol. 2000;165(12):7017–7024.
  • Turner TB, Meza-Perez S, Londono A, et al. Epigenetic modifiers upregulate MHC II and impede ovarian cancer tumor growth. Oncotarget. 2017;8(27):44159–44170.
  • Cycon KA, Mulvaney K, Rimsza LM, et al. Histone deacetylase inhibitors activate CIITA and MHC class II antigen expression in diffuse large B-cell lymphoma. Immunology. 2013;140(2):259–272.
  • Shimizu R, Kikuchi J, Wada T, et al. HDAC inhibitors augment cytotoxic activity of rituximab by upregulating CD20 expression on lymphoma cells. Leukemia. 2010;24(10):1760–1768.
  • Sugimoto T, Tomita A, Hiraga J, et al. Escape mechanisms from antibody therapy to lymphoma cells: downregulation of CD20 mRNA by recruitment of the HDAC complex and not by DNA methylation. Biochem Biophys Res Commun. 2009;390(1):48–53.
  • Frys S, Simons Z, Hu Q, et al. Entinostat, a novel histone deacetylase inhibitor is active in B-cell lymphoma and enhances the anti-tumour activity of rituximab and chemotherapy agents. Br J Haematol. 2015;169(4):506–519.
  • Damm JK, Gordon S, Ehinger M, et al. Pharmacologically relevant doses of valproate upregulate CD20 expression in three diffuse large B-cell lymphoma patients in vivo. Exp Hematol Oncol. 2015;4(1):4.
  • Jiang Y, Ortega-Molina A, Geng H, et al. CREBBP inactivation promotes the development of HDAC3-dependent lymphomas. Cancer Discov. 2017;7(1):38–53.
  • Bhalla S, Evens AM, Prachand S, et al. Paradoxical regulation of hypoxia inducible factor-1alpha (HIF-1alpha) by histone deacetylase inhibitor in diffuse large B-cell lymphoma. PLoS One. 2013;8(11):e81333.
  • Ding H, Peterson KL, Correia C, et al. Histone deacetylase inhibitors interrupt HSP90*RASGRP1 and HSP90*CRAF interactions to upregulate BIM and circumvent drug resistance in lymphoma cells. Leukemia. 2017;31(7):1593–1602.
  • Jia YJ, Liu ZB, Wang WG, et al. HDAC6 regulates microRNA-27b that suppresses proliferation, promotes apoptosis and target MET in diffuse large B-cell lymphoma. Leukemia. 2018;32(3):703–711.
  • Lim EL, Trinh DL, Scott DW, et al. Comprehensive miRNA sequence analysis reveals survival differences in diffuse large B-cell lymphoma patients. Genome Biol. 2015;16(1):18.
  • Crump M, Coiffier B, Jacobsen ED, et al. Phase II trial of oral vorinostat (suberoylanilide hydroxamic acid) in relapsed diffuse large-B-cell lymphoma. Ann Oncol. 2008;19(5):964–969.
  • Assouline SE, Nielsen TH, Yu S, et al. Phase 2 study of panobinostat with or without rituximab in relapsed diffuse large B-cell lymphoma. Blood. 2016;128(2):185–194.
  • Zaja F, Salvi F, Rossi M, et al. Single-agent panobinostat for relapsed/refractory diffuse large B-cell lymphoma: clinical outcome and correlation with genomic data. A phase 2 study of the Fondazione Italiana Linfomi. Leuk Lymphoma. 2018;59(12):2904–2910.
  • Puvvada SD, Li H, Rimsza LM, et al. A phase II study of belinostat (PXD101) in relapsed and refractory aggressive B-cell lymphomas: SWOG S0520. Leuk Lymphoma. 2016;57(10):2359–2369.
  • Ribrag V, Kim WS, Bouabdallah R, et al. Safety and efficacy of abexinostat, a pan-histone deacetylase inhibitor, in non-Hodgkin lymphoma and chronic lymphocytic leukemia: results of a phase II study. Haematologica. 2017;102(5):903–909.
  • Batlevi CL, Crump M, Andreadis C, et al. A phase 2 study of mocetinostat, a histone deacetylase inhibitor, in relapsed or refractory lymphoma. Br J Haematol. 2017;178(3):434–441.
  • Hofmeister CC, Williams N, Geyer S, et al. A phase 1 study of vorinostat maintenance after autologous transplant in high-risk lymphoma. Leuk Lymphoma. 2015;56(4):1043–1049.
  • Gimsing P, Hansen M, Knudsen LM, et al. A phase I clinical trial of the histone deacetylase inhibitor belinostat in patients with advanced hematological neoplasia. Eur J Haematol. 2008;81(3):170–176.
  • Morschhauser F, Terriou L, Coiffier B, et al. Phase 1 study of the oral histone deacetylase inhibitor abexinostat in patients with Hodgkin lymphoma, non-Hodgkin lymphoma, or chronic lymphocytic leukaemia. Invest New Drugs. 2015;33(2):423–431.
  • Barnes JA, Redd R, Fisher DC, et al. Panobinostat in combination with rituximab in heavily pretreated diffuse large B-cell lymphoma: results of a phase II study. Hematol Oncol. 2018;36(4):633–637.
  • Persky DO, Li H, Rimsza LM, et al. A phase I/II trial of vorinostat (SAHA) in combination with rituximab-CHOP in patients with newly diagnosed advanced stage diffuse large B-cell lymphoma (DLBCL): SWOG S0806. Am J Hematol. 2018;93(4):486–493.
  • Drott K, Hagberg H, Papworth K, et al. Valproate in combination with rituximab and CHOP as first-line therapy in diffuse large B-cell lymphoma (VALFRID). Blood Adv. 2018;2(12):1386–1392.
  • Oki Y, Kelly KR, Flinn I, et al. CUDC-907 in relapsed/refractory diffuse large B-cell lymphoma, including patients with MYC-alterations: results from an expanded phase I trial. Haematologica. 2017;102(11):1923–1930.
  • Pera B, Tang T, Marullo R, et al. Combinatorial epigenetic therapy in diffuse large B cell lymphoma pre-clinical models and patients. Clin Epigenet. 2016;8(1):79.
  • Yazbeck V, Shafer D, Perkins EB, et al. A phase II trial of bortezomib and vorinostat in mantle cell lymphoma and diffuse large b-cell lymphoma. Clin Lymphoma Myeloma Leuk. 2018;18(9):569–575.e1.
  • Zhao WL, Wang L, Liu YH, et al. Combined effects of histone deacetylase inhibitor and rituximab on non-Hodgkin’s B-lymphoma cells apoptosis. Exp Hematol. 2007;35(12):1801–1811.
  • Ageberg M, Rydstrom K, Relander T, et al. The histone deacetylase inhibitor valproic acid sensitizes diffuse large B-cell lymphoma cell lines to CHOP-induced cell death. Am J Transl Res. 2013;5(2):170–183.
  • Rahmani M, Aust MM, Benson EC, et al. PI3K/mTOR inhibition markedly potentiates HDAC inhibitor activity in NHL cells through BIM- and MCL-1-dependent mechanisms in vitro and in vivo. Clin Cancer Res. 2014;20(18):4849–4860.
  • Gupta M, Ansell SM, Novak AJ, et al. Inhibition of histone deacetylase overcomes rapamycin-mediated resistance in diffuse large B-cell lymphoma by inhibiting Akt signaling through mTORC2. Blood. 2009;114(14):2926–2935.
  • Oki Y, Buglio D, Fanale M, et al. Phase I study of panobinostat plus everolimus in patients with relapsed or refractory lymphoma. Clin Cancer Res. 2013;19(24):6882–6890.
  • Sun K, Atoyan R, Borek MA, et al. Dual HDAC and PI3K Inhibitor CUDC-907 downregulates MYC and suppresses growth of MYC-dependent cancers. 2017;16(2):285–299.
  • Younes A, Berdeja JG, Patel MR, et al. Safety, tolerability, and preliminary activity of CUDC-907, a first-in-class, oral, dual inhibitor of HDAC and PI3K, in patients with relapsed or refractory lymphoma or multiple myeloma: an open-label, dose-escalation, phase 1 trial. Lancet Oncol. 2016;17(5):622–631.
  • Kalac M, Scotto L, Marchi E, 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):5506–5516.
  • Witzig TE, Hu G, Offer SM, et al. Epigenetic mechanisms of protein tyrosine phosphatase 6 suppression in diffuse large B-cell lymphoma: implications for epigenetic therapy. Leukemia. 2014;28(1):147–154.
  • Han Y, Amin HM, Frantz C, et al. Restoration of shp1 expression by 5-AZA-2’-deoxycytidine is associated with downregulation of JAK3/STAT3 signaling in ALK-positive anaplastic large cell lymphoma. Leukemia. 2006;20(9):1602–1609.
  • Chim CS, Wong KY, Loong F, et al. SOCS1 and SHP1 hypermethylation in mantle cell lymphoma and follicular lymphoma: implications for epigenetic activation of the Jak/STAT pathway. Leukemia. 2004;18(2):356–358.
  • Honigberg LA, Smith AM, Sirisawad M, et al. The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci USA. 2010;107(29):13075–13080.
  • Mondello P, Brea EJ, De Stanchina E, et al. Panobinostat acts synergistically with ibrutinib in diffuse large B cell lymphoma cells with MyD88 L265 mutations. JCI Insight. 2017;2(6):e90196.
  • Ngo VN, Young RM, Schmitz R, et al. Oncogenically active MYD88 mutations in human lymphoma. Nature. 2011;470(7332):115–119.
  • Wilson WH, Young RM, Schmitz R, et al. Targeting B cell receptor signaling with ibrutinib in diffuse large B cell lymphoma. Nat Med. 2015;21(8):922–926.
  • Phelan JD, Young RM, Webster DE, et al. A multiprotein supercomplex controlling oncogenic signalling in lymphoma. Nature. 2018;560(7718):387–391.
  • Amengual JE, Prabhu SA, Lombardo M, et al. Mechanisms of acquired drug resistance to the HDAC6 selective inhibitor ricolinostat reveals rational drug-drug combination with ibrutinib. Clin Cancer Res. 2017;23(12):3084–3096.
  • Holkova B, Kmieciak M, Bose P, et al. Phase 1 trial of carfilzomib (PR-171) in combination with vorinostat (SAHA) in patients with relapsed or refractory B-cell lymphomas. Leuk Lymphoma. 2016;57(3):635–643.
  • Amengual JE, Johannet P, Lombardo M, et al. Dual targeting of protein degradation pathways with the selective HDAC6 inhibitor ACY-1215 and bortezomib is synergistic in lymphoma. Clin Cancer Res. 2015;21(20):4663–4675.
  • Cerchietti LC, Hatzi K, Caldas-Lopes E, 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;120(12):4569–4582.
  • Cosenza M, Civallero M, Marcheselli L, et al. Ricolinostat, a selective HDAC6 inhibitor, shows anti-lymphoma cell activity alone and in combination with bendamustine. Apoptosis. 2017;22(6):827–840.
  • Havas AP, Rodrigues KB, Bhakta A, et al. Belinostat and vincristine demonstrate mutually synergistic cytotoxicity associated with mitotic arrest and inhibition of polyploidy in a preclinical model of aggressive diffuse large B cell lymphoma. Cancer Biol Ther. 2016;17(12):1240–1252.
  • Nieto Y, Valdez BC, Thall PF, et al. Vorinostat combined with high-dose gemcitabine, busulfan, and melphalan with autologous stem cell transplantation in patients with refractory lymphomas. Biol Blood Marrow Transplant. 2015;21(11):1914–1920.
  • Joosten M, Ginzel S, Blex C, et al. A novel approach to detect resistance mechanisms reveals FGR as a factor mediating HDAC inhibitor SAHA resistance in B-cell lymphoma. Mol Oncol. 2016;10(8):1232–1244.
  • Tula-Sanchez AA, Havas AP, Alonge PJ, et al. A model of sensitivity and resistance to histone deacetylase inhibitors in diffuse large B cell lymphoma: role of cyclin-dependent kinase inhibitors. Cancer Biol Ther. 2013;14(10):949–961.
  • Geeleher P, Loboda A, Lenkala D, et al. Predicting response to histone deacetylase inhibitors using high-throughput genomics. JNCIJ. 2015;107(11):djv247.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.