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Research Paper

A model of sensitivity and resistance to histone deacetylase inhibitors in diffuse large B cell lymphoma

Role of cyclin-dependent kinase inhibitors

, , , , , , , & show all
Pages 949-961 | Received 24 Apr 2013, Accepted 29 Jul 2013, Published online: 02 Aug 2013

References

  • Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000; 403:503 - 11; http://dx.doi.org/10.1038/35000501; PMID: 10676951
  • Coiffier B, Thieblemont C, Van Den Neste E, Lepeu G, Plantier I, Castaigne S, Lefort S, Marit G, Macro M, Sebban C, et al. Long-term outcome of patients in the LNH-98.5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d’Etudes des Lymphomes de l’Adulte. Blood 2010; 116:2040 - 5; http://dx.doi.org/10.1182/blood-2010-03-276246; PMID: 20548096
  • Feugier P, Van Hoof A, Sebban C, Solal-Celigny P, Bouabdallah R, Fermé C, Christian B, Lepage E, Tilly H, Morschhauser F, et al. Long-term results of the R-CHOP study in the treatment of elderly patients with diffuse large B-cell lymphoma: a study by the Groupe d’Etude des Lymphomes de l’Adulte. J Clin Oncol 2005; 23:4117 - 26; http://dx.doi.org/10.1200/JCO.2005.09.131; PMID: 15867204
  • Rosenwald A, Wright G, Chan WC, Connors JM, Campo E, Fisher RI, Gascoyne RD, Muller-Hermelink HK, Smeland EB, Giltnane JM, et al, Lymphoma/Leukemia Molecular Profiling Project. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med 2002; 346:1937 - 47; http://dx.doi.org/10.1056/NEJMoa012914; PMID: 12075054
  • Johnson NA, Slack GW, Savage KJ, Connors JM, Ben-Neriah S, Rogic S, Scott DW, Tan KL, Steidl C, Sehn LH, et al. Concurrent expression of MYC and BCL2 in diffuse large B-cell lymphoma treated with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone. J Clin Oncol 2012; 30:3452 - 9; http://dx.doi.org/10.1200/JCO.2011.41.0985; PMID: 22851565
  • Hu S, Xu-Monette ZY, Tzankov A, Green T, Wu L, Balasubramanyam A, Liu WM, Visco C, Li Y, Miranda RN, et al. MYC/BCL2 protein coexpression contributes to the inferior survival of activated B-cell subtype of diffuse large B-cell lymphoma and demonstrates high-risk gene expression signatures: a report from The International DLBCL Rituximab-CHOP Consortium Program. Blood 2013; 121:4021 - 31, quiz 4250; http://dx.doi.org/10.1182/blood-2012-10-460063; PMID: 23449635
  • Stefancikova L, Moulis M, Fabian P, Vasova I, Zedek F, Ravcukova B, Muzik J, Kuglik P, Vranova V, Falkova I, et al. Prognostic impact of p53 aberrations for R-CHOP-treated patients with diffuse large B-cell lymphoma. Int J Oncol 2011; 39:1413 - 20; PMID: 21874232
  • Xu-Monette ZY, Wu L, Visco C, Tai YC, Tzankov A, Liu WM, Montes-Moreno S, Dybkaer K, Chiu A, Orazi A, et al. Mutational profile and prognostic significance of TP53 in diffuse large B-cell lymphoma patients treated with R-CHOP: report from an International DLBCL Rituximab-CHOP Consortium Program Study. Blood 2012; 120:3986 - 96; http://dx.doi.org/10.1182/blood-2012-05-433334; PMID: 22955915
  • Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007; 26:5541 - 52; http://dx.doi.org/10.1038/sj.onc.1210620; PMID: 17694093
  • Yamaguchi T, Cubizolles F, Zhang Y, Reichert N, Kohler H, Seiser C, Matthias P. Histone deacetylases 1 and 2 act in concert to promote the G1-to-S progression. Genes Dev 2010; 24:455 - 69; http://dx.doi.org/10.1101/gad.552310; PMID: 20194438
  • Marquard L, Poulsen CB, Gjerdrum LM, de Nully Brown P, Christensen IJ, Jensen PB, Sehested M, Johansen P, Ralfkiaer E. Histone deacetylase 1, 2, 6 and acetylated histone H4 in B- and T-cell lymphomas. Histopathology 2009; 54:688 - 98; http://dx.doi.org/10.1111/j.1365-2559.2009.03290.x; PMID: 19438744
  • Gloghini A, Buglio D, Khaskhely NM, Georgakis G, Orlowski RZ, Neelapu SS, Carbone A, Younes A. Expression of histone deacetylases in lymphoma: implication for the development of selective inhibitors. Br J Haematol 2009; 147:515 - 25; http://dx.doi.org/10.1111/j.1365-2141.2009.07887.x; PMID: 19775297
  • Kelly WK, O’Connor OA, Krug LM, Chiao JH, Heaney M, Curley T, MacGregore-Cortelli B, Tong W, Secrist JP, Schwartz L, et al. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 2005; 23:3923 - 31; http://dx.doi.org/10.1200/JCO.2005.14.167; PMID: 15897550
  • O’Connor OA, Heaney ML, Schwartz L, Richardson S, Willim R, MacGregor-Cortelli B, Curly T, Moskowitz C, Portlock C, Horwitz S, et al. Clinical experience with intravenous and oral formulations of the novel histone deacetylase inhibitor suberoylanilide hydroxamic acid in patients with advanced hematologic malignancies. J Clin Oncol 2006; 24:166 - 73; http://dx.doi.org/10.1200/JCO.2005.01.9679; PMID: 16330674
  • Crump M, Coiffier B, Jacobsen ED, Sun L, Ricker JL, Xie H, Frankel SR, Randolph SS, Cheson BD. Phase II trial of oral vorinostat (suberoylanilide hydroxamic acid) in relapsed diffuse large-B-cell lymphoma. Ann Oncol 2008; 19:964 - 9; http://dx.doi.org/10.1093/annonc/mdn031; PMID: 18296419
  • Gimsing P, Hansen M, Knudsen LM, Knoblauch P, Christensen IJ, Ooi CE, Buhl-Jensen P. A phase I clinical trial of the histone deacetylase inhibitor belinostat in patients with advanced hematological neoplasia. Eur J Haematol 2008; 81:170 - 6; http://dx.doi.org/10.1111/j.1600-0609.2008.01102.x; PMID: 18510700
  • Dasmahapatra G, Lembersky D, Kramer L, Fisher RI, Friedberg J, Dent P, Grant S. The pan-HDAC inhibitor vorinostat potentiates the activity of the proteasome inhibitor carfilzomib in human DLBCL cells in vitro and in vivo. Blood 2010; 115:4478 - 87; http://dx.doi.org/10.1182/blood-2009-12-257261; PMID: 20233973
  • Kalac M, Scotto L, Marchi E, Amengual J, Seshan VE, Bhagat G, Ulahannan N, Leshchenko VV, Temkin AM, Parekh S, et al. HDAC inhibitors and decitabine are highly synergistic and associated with unique gene-expression and epigenetic profiles in models of DLBCL. Blood 2011; 118:5506 - 16; http://dx.doi.org/10.1182/blood-2011-02-336891; PMID: 21772049
  • Polack A, Eick D, Koch E, Bornkamm GW. Truncation does not abrogate transcriptional downregulation of the c-myc gene by sodium butyrate in Burkitt’s lymphoma cells. EMBO J 1987; 6:2959 - 64; PMID: 3691477
  • Van Lint C, Emiliani S, Verdin E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr 1996; 5:245 - 53; PMID: 8723390
  • Duan H, Heckman CA, Boxer LM. Histone deacetylase inhibitors down-regulate bcl-2 expression and induce apoptosis in t(14;18) lymphomas. Mol Cell Biol 2005; 25:1608 - 19; http://dx.doi.org/10.1128/MCB.25.5.1608-1619.2005; PMID: 15713621
  • Lindemann RK, Newbold A, Whitecross KF, Cluse LA, Frew AJ, Ellis L, Williams S, Wiegmans AP, Dear AE, Scott CL, 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 U S A 2007; 104:8071 - 6; http://dx.doi.org/10.1073/pnas.0702294104; PMID: 17470784
  • Deng X, Gao F, Flagg T, May WS Jr.. Mono- and multisite phosphorylation enhances Bcl2’s antiapoptotic function and inhibition of cell cycle entry functions. Proc Natl Acad Sci U S A 2004; 101:153 - 8; http://dx.doi.org/10.1073/pnas.2533920100; PMID: 14660795
  • Pasqualucci L, Trifonov V, Fabbri G, Ma J, Rossi D, Chiarenza A, Wells VA, Grunn A, Messina M, Elliot O, et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet 2011; 43:830 - 7; http://dx.doi.org/10.1038/ng.892; PMID: 21804550
  • Schuetz JM, Johnson NA, Morin RD, Scott DW, Tan K, Ben-Nierah S, Boyle M, Slack GW, Marra MA, Connors JM, et al. BCL2 mutations in diffuse large B-cell lymphoma. Leukemia 2012; 26:1383 - 90; http://dx.doi.org/10.1038/leu.2011.378; PMID: 22189900
  • Vervoorts J, Lüscher-Firzlaff JM, Rottmann S, Lilischkis R, Walsemann G, Dohmann K, Austen M, Lüscher B. Stimulation of c-MYC transcriptional activity and acetylation by recruitment of the cofactor CBP. EMBO Rep 2003; 4:484 - 90; http://dx.doi.org/10.1038/sj.embor.embor821; PMID: 12776737
  • Patel JH, Du Y, Ard PG, Phillips C, Carella B, Chen CJ, Rakowski C, Chatterjee C, Lieberman PM, Lane WS, et al. The c-MYC oncoprotein is a substrate of the acetyltransferases hGCN5/PCAF and TIP60. Mol Cell Biol 2004; 24:10826 - 34; http://dx.doi.org/10.1128/MCB.24.24.10826-10834.2004; PMID: 15572685
  • Faiola F, Liu X, Lo S, Pan S, Zhang K, Lymar E, Farina A, Martinez E. Dual regulation of c-Myc by p300 via acetylation-dependent control of Myc protein turnover and coactivation of Myc-induced transcription. Mol Cell Biol 2005; 25:10220 - 34; http://dx.doi.org/10.1128/MCB.25.23.10220-10234.2005; PMID: 16287840
  • Mitsiades N, Mitsiades CS, Richardson PG, McMullan C, Poulaki V, Fanourakis G, Schlossman R, Chauhan D, Munshi NC, Hideshima T, et al. Molecular sequelae of histone deacetylase inhibition in human malignant B cells. Blood 2003; 101:4055 - 62; http://dx.doi.org/10.1182/blood-2002-11-3514; PMID: 12531799
  • Vaziri C, Stice L, Faller DV. Butyrate-induced G1 arrest results from p21-independent disruption of retinoblastoma protein-mediated signals. Cell Growth Differ 1998; 9:465 - 74; PMID: 9663465
  • Sandor V, Senderowicz A, Mertins S, Sackett D, Sausville E, Blagosklonny MV, Bates SE. 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; 83:817 - 25; http://dx.doi.org/10.1054/bjoc.2000.1327; PMID: 10952788
  • Rosato RR, Almenara JA, Grant S. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1 1. Cancer Res 2003; 63:3637 - 45; PMID: 12839953
  • Zarkowska T, Mittnacht S. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J Biol Chem 1997; 272:12738 - 46; http://dx.doi.org/10.1074/jbc.272.19.12738; PMID: 9139732
  • Kitagawa M, Higashi H, Jung HK, Suzuki-Takahashi I, Ikeda M, Tamai K, Kato J, Segawa K, Yoshida E, Nishimura S, et al. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J 1996; 15:7060 - 9; PMID: 9003781
  • Seo JS, Cho NY, Kim HR, Tsurumi T, Jang YS, Lee WK, Lee SK. Cell cycle arrest and lytic induction of EBV-transformed B lymphoblastoid cells by a histone deacetylase inhibitor, Trichostatin A. Oncol Rep 2008; 19:93 - 8; PMID: 18097580
  • Besson A, Dowdy SF, Roberts JM. CDK inhibitors: cell cycle regulators and beyond. Dev Cell 2008; 14:159 - 69; http://dx.doi.org/10.1016/j.devcel.2008.01.013; PMID: 18267085
  • Shin JY, Kim HS, Park J, Park JB, Lee JY. Mechanism for inactivation of the KIP family cyclin-dependent kinase inhibitor genes in gastric cancer cells. Cancer Res 2000; 60:262 - 5; PMID: 10667572
  • Huang L, Sowa Y, Sakai T, Pardee AB. Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites. Oncogene 2000; 19:5712 - 9; http://dx.doi.org/10.1038/sj.onc.1203963; PMID: 11126357
  • Nakano K, Mizuno T, Sowa Y, Orita T, Yoshino T, Okuyama Y, Fujita T, Ohtani-Fujita N, Matsukawa Y, Tokino T, et al. Butyrate activates the WAF1/Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line. J Biol Chem 1997; 272:22199 - 206; http://dx.doi.org/10.1074/jbc.272.35.22199; PMID: 9268365
  • Wang H, Zhou W, Zheng Z, Zhang P, Tu B, He Q, Zhu WG. The HDAC inhibitor depsipeptide transactivates the p53/p21 pathway by inducing DNA damage. DNA Repair (Amst) 2012; 11:146 - 56; http://dx.doi.org/10.1016/j.dnarep.2011.10.014; PMID: 22112863
  • Eot-Houllier G, Fulcrand G, Magnaghi-Jaulin L, Jaulin C. Histone deacetylase inhibitors and genomic instability. Cancer Lett 2009; 274:169 - 76; http://dx.doi.org/10.1016/j.canlet.2008.06.005; PMID: 18635312
  • Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004; 303:844 - 8; http://dx.doi.org/10.1126/science.1092472; PMID: 14704432
  • Jenkins LM, Durell SR, Mazur SJ, Appella E. p53 N-terminal phosphorylation: a defining layer of complex regulation. Carcinogenesis 2012; 33:1441 - 9; http://dx.doi.org/10.1093/carcin/bgs145; PMID: 22505655
  • Bots M, Johnstone RW. Rational combinations using HDAC inhibitors. Clin Cancer Res 2009; 15:3970 - 7; http://dx.doi.org/10.1158/1078-0432.CCR-08-2786; PMID: 19509171
  • Gupta M, Ansell SM, Novak AJ, Kumar S, Kaufmann SH, Witzig TE. Inhibition of histone deacetylase overcomes rapamycin-mediated resistance in diffuse large B-cell lymphoma by inhibiting Akt signaling through mTORC2. Blood 2009; 114:2926 - 35; http://dx.doi.org/10.1182/blood-2009-05-220889; PMID: 19641186
  • Bodo J, Sedlak J, Maciejewski JP, Almasan A, Hsi ED. HDAC inhibitors potentiate the apoptotic effect of enzastaurin in lymphoma cells. Apoptosis 2011; 16:914 - 23; http://dx.doi.org/10.1007/s10495-011-0617-x; PMID: 21667043
  • Cerchietti LC, Hatzi K, Caldas-Lopes E, Yang SN, Figueroa ME, Morin RD, Hirst M, Mendez L, Shaknovich R, Cole PA, 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; 120:4569 - 82; http://dx.doi.org/10.1172/JCI42869; PMID: 21041953
  • Robey RW, Chakraborty AR, Basseville A, Luchenko V, Bahr J, Zhan Z, Bates SE. Histone deacetylase inhibitors: emerging mechanisms of resistance. Mol Pharm 2011; 8:2021 - 31; http://dx.doi.org/10.1021/mp200329f; PMID: 21899343
  • Zupkovitz G, Grausenburger R, Brunmeir R, Senese S, Tischler J, Jurkin J, Rembold M, Meunier D, Egger G, Lagger S, et al. The cyclin-dependent kinase inhibitor p21 is a crucial target for histone deacetylase 1 as a regulator of cellular proliferation. Mol Cell Biol 2010; 30:1171 - 81; http://dx.doi.org/10.1128/MCB.01500-09; PMID: 20028735
  • Munro J, Barr NI, Ireland H, Morrison V, Parkinson EK. Histone deacetylase inhibitors induce a senescence-like state in human cells by a p16-dependent mechanism that is independent of a mitotic clock. Exp Cell Res 2004; 295:525 - 38; http://dx.doi.org/10.1016/j.yexcr.2004.01.017; PMID: 15093749
  • Alao JP, Stavropoulou AV, Lam EW, Coombes RC, Vigushin DM. Histone deacetylase inhibitor, trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells. Mol Cancer 2006; 5:8; http://dx.doi.org/10.1186/1476-4598-5-8; PMID: 16504004
  • Hu J, Colburn NH. Histone deacetylase inhibition down-regulates cyclin D1 transcription by inhibiting nuclear factor-kappaB/p65 DNA binding. Mol Cancer Res 2005; 3:100 - 9; http://dx.doi.org/10.1158/1541-7786.MCR-04-0070; PMID: 15755876
  • Wilting RH, Yanover E, Heideman MR, Jacobs H, Horner J, van der Torre J, DePinho RA, Dannenberg JH. Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis. EMBO J 2010; 29:2586 - 97; http://dx.doi.org/10.1038/emboj.2010.136; PMID: 20571512
  • Ogryzko VV, Hirai TH, Russanova VR, Barbie DA, Howard BH. Human fibroblast commitment to a senescence-like state in response to histone deacetylase inhibitors is cell cycle dependent. Mol Cell Biol 1996; 16:5210 - 8; PMID: 8756678
  • Chan HM, Krstic-Demonacos M, Smith L, Demonacos C, La Thangue NB. Acetylation control of the retinoblastoma tumour-suppressor protein. Nat Cell Biol 2001; 3:667 - 74; http://dx.doi.org/10.1038/35083062; PMID: 11433299
  • Nguyen DX, Baglia LA, Huang SM, Baker CM, McCance DJ. Acetylation regulates the differentiation-specific functions of the retinoblastoma protein. EMBO J 2004; 23:1609 - 18; http://dx.doi.org/10.1038/sj.emboj.7600176; PMID: 15044952
  • Pickard A, Wong PP, McCance DJ. Acetylation of Rb by PCAF is required for nuclear localization and keratinocyte differentiation. J Cell Sci 2010; 123:3718 - 26; http://dx.doi.org/10.1242/jcs.068924; PMID: 20940255
  • Markham D, Munro S, Soloway J, O’Connor DP, La Thangue NB. DNA-damage-responsive acetylation of pRb regulates binding to E2F-1. EMBO Rep 2006; 7:192 - 8; http://dx.doi.org/10.1038/sj.embor.7400591; PMID: 16374512
  • Chau BN, Wang JY. Coordinated regulation of life and death by RB. Nat Rev Cancer 2003; 3:130 - 8; http://dx.doi.org/10.1038/nrc993; PMID: 12563312
  • Dou QP, An B, Will PL. Induction of a retinoblastoma phosphatase activity by anticancer drugs accompanies p53-independent G1 arrest and apoptosis. Proc Natl Acad Sci U S A 1995; 92:9019 - 23; http://dx.doi.org/10.1073/pnas.92.20.9019; PMID: 7568064
  • Wang RH, Liu CW, Avramis VI, Berndt N. Protein phosphatase 1alpha-mediated stimulation of apoptosis is associated with dephosphorylation of the retinoblastoma protein. Oncogene 2001; 20:6111 - 22; http://dx.doi.org/10.1038/sj.onc.1204829; PMID: 11593419
  • Schrump DS. Cytotoxicity mediated by histone deacetylase inhibitors in cancer cells: mechanisms and potential clinical implications. Clin Cancer Res 2009; 15:3947 - 57; http://dx.doi.org/10.1158/1078-0432.CCR-08-2787; PMID: 19509170
  • LaBaer J, Garrett MD, Stevenson LF, Slingerland JM, Sandhu C, Chou HS, Fattaey A, Harlow E. New functional activities for the p21 family of CDK inhibitors. Genes Dev 1997; 11:847 - 62; http://dx.doi.org/10.1101/gad.11.7.847; PMID: 9106657
  • Zhang H, Hannon GJ, Beach D. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev 1994; 8:1750 - 8; http://dx.doi.org/10.1101/gad.8.15.1750; PMID: 7958854
  • Ray A, James MK, Larochelle S, Fisher RP, Blain SW. p27Kip1 inhibits cyclin D-cyclin-dependent kinase 4 by two independent modes. Mol Cell Biol 2009; 29:986 - 99; http://dx.doi.org/10.1128/MCB.00898-08; PMID: 19075005
  • Ocker M, Schneider-Stock R. Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int J Biochem Cell Biol 2007; 39:1367 - 74; http://dx.doi.org/10.1016/j.biocel.2007.03.001; PMID: 17412634
  • Gabrielli B, Chia K, Warrener R. Finally, how histone deacetylase inhibitors disrupt mitosis!. Cell Cycle 2011; 10:2658 - 61; http://dx.doi.org/10.4161/cc.10.16.16953; PMID: 21811095
  • Wahl AF, Donaldson KL, Fairchild C, Lee FY, Foster SA, Demers GW, Galloway DA. Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis. Nat Med 1996; 2:72 - 9; http://dx.doi.org/10.1038/nm0196-72; PMID: 8564846
  • Morin RD, Mendez-Lago M, Mungall AJ, Goya R, Mungall KL, Corbett RD, Johnson NA, Severson TM, Chiu R, Field M, et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 2011; 476:298 - 303; http://dx.doi.org/10.1038/nature10351; PMID: 21796119
  • Khan O, Fotheringham S, Wood V, Stimson L, Zhang C, Pezzella F, Duvic M, Kerr DJ, La Thangue NB. HR23B is a biomarker for tumor sensitivity to HDAC inhibitor-based therapy. Proc Natl Acad Sci U S A 2010; 107:6532 - 7; http://dx.doi.org/10.1073/pnas.0913912107; PMID: 20308564
  • Visco C, Tzankov A, Xu-Monette ZY, Miranda RN, Tai YC, Li Y, Liu WM, d’Amore ES, Li Y, Montes-Moreno S, et al. Patients with diffuse large B-cell lymphoma of germinal center origin with BCL2 translocations have poor outcome, irrespective of MYC status: a report from an International DLBCL rituximab-CHOP Consortium Program Study. Haematologica 2013; 98:255 - 63; http://dx.doi.org/10.3324/haematol.2012.066209; PMID: 22929980
  • Dasmahapatra G, Almenara JA, Grant S. Flavopiridol and histone deacetylase inhibitors promote mitochondrial injury and cell death in human leukemia cells that overexpress Bcl-2. Mol Pharmacol 2006; 69:288 - 98; PMID: 16219908
  • Farrugia MM, Duan LJ, Reis MD, Ngan BY, Berinstein NL. Alterations of the p53 tumor suppressor gene in diffuse large cell lymphomas with translocations of the c-MYC and BCL-2 proto-oncogenes. Blood 1994; 83:191 - 8; PMID: 8274734
  • Hasegawa H, Yamada Y, Iha H, Tsukasaki K, Nagai K, Atogami S, Sugahara K, Tsuruda K, Ishizaki A, Kamihira S. Activation of p53 by Nutlin-3a, an antagonist of MDM2, induces apoptosis and cellular senescence in adult T-cell leukemia cells. Leukemia 2009; 23:2090 - 101; http://dx.doi.org/10.1038/leu.2009.171; PMID: 19710698
  • Li CC, O’Connell CD, Beckwith M, Longo DL. Detection of p53 mutations in B cell non-Hodgkin’s lymphoma cell lines. Leukemia 1995; 9:650 - 5; PMID: 7723400
  • Amini RM, Berglund M, Rosenquist R, Von Heideman A, Lagercrantz S, Thunberg U, Bergh J, Sundström C, Glimelius B, Enblad G. A novel B-cell line (U-2932) established from a patient with diffuse large B-cell lymphoma following Hodgkin lymphoma. Leuk Lymphoma 2002; 43:2179 - 89; http://dx.doi.org/10.1080/1042819021000032917; PMID: 12533045