Mechanisms of Sensitivity and Resistance to Histone Deacetylase Inhibitors in Diffuse Large B-Cell Lymphoma

Blood ◽  
2012 ◽  
Vol 120 (21) ◽  
pp. 1359-1359
Author(s):  
Ana A Tula-Sanchez ◽  
Aaron Havas ◽  
Peter Alonge ◽  
Mary E Klein ◽  
Taralyn Y Rogers ◽  
...  

Abstract Abstract 1359 Diffuse large B-cell lymphoma (DLBCL) is the most common type of Non-Hodgkin Lymphoma (NHL) throughout the world. DLBCL is an aggressive, heterogeneous disease with two major recognized cell-of-origin subtypes: “germinal center” (GCB) and “activated B-cell like” (ABC), the latter having the worse prognosis. Overall, DLBCL remains fatal for about 30% patients due to relapse or lack of response to initial therapy. Resistant/relapsed DLBCL patients could benefit from the addition of new promising antiproliferative drugs, such as histone deacetylase inhibitors (HDACIs), to current chemotherapy regimens. So far, Vorinostat and Romidepsin, two structurally different HDACIs, have been approved for the treatment of hematological cancers. Despite their proven antiproliferative, pro-apoptotic effects, response to these drugs against DLBCL in clinical trials have been variable, ranging from complete/partial responses to stable disease to no response. The mechanisms of action of these drugs are still poorly understood, mainly because the function of their target deacetylases are cell context-specific. Therefore, characterization of the specific anticancer mechanisms of action of HDACIs in DLBCL could potentially lead to development of novel combinatorial drug regimens effective against resistant/relapsed DLBCL patients. To define HDACI action in DLBCL, we treated DLBCL-derived cell lines with PXD101, (Belinostat); a hydroxamate HDACI, like Vorinostat. We demonstrated that PXD101 is able to produce 24h growth inhibition (IC50) at submicromolar concentrations regardless of the DLBCL subtype. The 24h IC50values were used in all the subsequent experiments. Cell cycle and apoptosis analysis by flow cytometry indicated that PXD101 produces cytotoxic effects on two of the GCB cell lines; DB and OCILY19 underwent G2/M cell cycle arrest at 24 hours followed by apoptosis at 48 and 72 hours of treatment. Immunoblotting of PARP and caspase-3 cleavage further confirmed apoptosis. More importantly, when cells were treated for only 8 hours with PXD101 and then the drug was removed for 24 hours, cells showed apoptosis rates similar to those observed with 48h of continuous treatment; suggesting that once that these cell lines are exposed to the drug they rapidly commit to cell death. Thus, we have classified the DB and OCILY19 cell lines as models for sensitivity to the apoptotic effects of HDACI. In contrast, PXD101 induced cytostatic effects on the GCB cell line SUDHL4 and ABC cell lines U2932 and SUDHL8. All three cell lines showed G1 phase cell cycle arrest with little apoptosis. The G1 arrest is reversible after 48 hours of drug removal. Because of the lack of cell death and the reversibility of cell cycle arrest, we have classified these cell lines as models of HDACI resistance. Previous studies have shown that induction of p21 is responsible for G1 arrest in cells treated with HDACIs. Western blot analysis showed that none of the cell lines, except U2932, express p21, but upon PXD101, p21 protein levels were induced at 24, 48 and 72 hours of PXD101 treatment in SUDHL4 and U2932. In contrast, p21 was induced to a lesser extent in OCILY19 and DB, but its expression was not sustained beyond 24 hours of treatment. Since we also observed a corresponding loss in Rb phosphorylation, we tested the effect of PXD101 on cyclin dependent kinase 2 (CDK2) activity. This enzyme complex is responsible for entry into S phase and is inhibited by association with p21. In all three resistant cell lines CDK2 activity was reduced after only 24 hours of treatment with PXD101. The loss in activity was correlated with increased association with p21, as determined by immunoprecipitation. These results indicate that sustained upregulation of p21 by HDACIs such as PXD101 plays a role in bringing about G1 arrest that may protect DLBCL cells from apoptosis. Combined treatment with therapeutics that prevent p21 upregulation and G1 arrest may work synergistically with HDACIs to trigger apoptosis in HDACI-resistant cell lines. To that end, we have begun analysis of the cyclin-dependent kinase inhibitor, flavopiridol, and have shown that it prevents both p21 upregulation and G1 arrest in the HDACi-resistant DLBCL cell lines. Studies to measure synergism with PXD101 in bringing about cell death are currently underway. Disclosures: No relevant conflicts of interest to declare.

Blood ◽  
2010 ◽  
Vol 116 (21) ◽  
pp. 4908-4908
Author(s):  
Juan Gu ◽  
Francisco J. Hernandez-Ilizaliturri ◽  
Gregory P. Kaufman ◽  
Cory Mavis ◽  
Myron S. Czuczman

Abstract Abstract 4908 Rituximab-chemotherapy relapsed/refractory B-cell lymphomas represent an emerging clinical challenge that underlies the need to develop alternative therapeutic strategies. Targeting the ubiquitin-proteasome system using bortezomib (BTZ) has resulted in significant anti-tumor activity and potentiates the effects of chemotherapy/biologic agents in multiple myeloma, and to a lesser degree, B-cell lymphoma. CFZ is as a novel proteasome inhibitor which is selective and structurally distinct from BTZ. In an attempt to characterize the biological activity of CFZ, we evaluated its anti-tumor activity in several lymphoma pre-clinical models. Rituximab-chemotherapy sensitive cell lines (RSCL), rituximab-chemotherapy resistant cell lines (RRCL), as well as primary tumor cells derived from patients with de novo or relapsed/refractory B-cell lymphoma, were exposed to escalating doses of CFZ or BTZ (1-7.5nM) alone or in combination with doxorubicin, paclitaxel, or gemcitabine for 24, 48 and 72hours. Cell viability was determined by cell titer glow luminescent assay and cell cycle was analyzed by FASCan DNA methodology. Patient-derived lymphoma cells were isolated from fresh biopsy tissue via negative selection using magnetic beads. Western blots were performed using cell lysates from CFZ, BTZ or control-treated cells to detect PARP-cleavage and/or changes in Bcl-2 family members. CFZ was more active than BTZ and exhibited dose-dependent and time-dependent cytotoxicity against RSCL, RRCL, and primary tumor cells. We found a 10-fold concentration difference between CFZ and BTZ activity. In vitro exposure of RRCL or RSCL to CFZ resulted in G2/M phase cell cycle arrest. In addition, CFZ exposure resulted in the up-regulation of Bak and Noxa levels and subsequent PARP cleavage in RRCL. Finally, CFZ demonstrated the ability to overcome resistance to chemotherapy in RRCL and potentiated the anti-tumor activity of paclitaxel and gemcitabine in B-cell lymphoma cell lines. In summary, our data strongly suggest that CFZ is a novel and potent proteasome inhibitor which is able to: overcome resistance to some conventional chemotherapeutic agents, upregulate proapoptotic proteins to enhance cell death, and induce G2/M cell cycle arrest in lymphoma cells. Our preclinical data supports future clinical evaluation of CFZ in patients with refractory B-cell lymphoma. (Supported by USPHS grant R01 CA136907-01A1 from the National Cancer Institute). Disclosures: No relevant conflicts of interest to declare.


Blood ◽  
2013 ◽  
Vol 122 (21) ◽  
pp. 1836-1836
Author(s):  
Christopher N. Ibabao ◽  
Cory Mavis ◽  
Jenny Gu ◽  
Myron S. Czuczman ◽  
Francisco Hernandez

Abstract The identification of critical signaling pathways necessary for the development, maintenance and progression of specific subtypes of DLBCL are necessary in order to develop novel therapeutics against them. Increased NFkB activity and p53 deregulation contribute to either the pathogenesis of some types of DLBCL (i.e. activated B-cell [ABC] subtype) or to rituximab and/or chemotherapy resistance in B-cell lymphoma. Optimal targeting of NFkB activity is an attractive therapeutic strategy that has been evaluated in pre-clinical and clinical models for over a decade with variable degrees of success. CBL-C137 is a novel and potent member of the curaxin family, capable of modulating p53 and NFkB activity and inducing cell death in several solid tumor cancer models. It has never been previously studied in lymphoid malignancies. In order to study and define the therapeutic potential of curaxins in B-cell lymphoma, we evaluated CBL-C137 in lymphoma pre-clinical models. A panel of rituximab sensitive or resistant lymphoma cell lines representing the two most common subtypes of DLBCL (i.e. ABC-DLBCL and germinal center B-cell [GCB] DLBCL) were exposed to CBL-C137 (0.5-16mM). Changes in cell viability; cell cycle distribution; apoptosis and p53/ NFkB p65 expression were evaluated by measuring ATP content, flow cytometry, and Western blotting, respectively. Subsequently, GCB- or ABC-DLBCL cells were exposed to CBL-C137 alone or in combination with various chemotherapy agents or other available (but less selective) NFkB inhibitors (i.e. lenalidomide or Ibrutinib) for 24 or 48 hrs. Changes in cell viability were determined using the cell titer glo assay. In addition, we conducted standardized 51Cr release assays on cells previously exposed to either CBL-C137 or DMSO to investigate the effects of NFkB inhibition on rituximab (or other anti-CD20) antibody-associated complement mediated cytotoxicity (CMC) and antibody dependent cellular cytotoxicity (ADCC). CBL-C137 induced dose- and time- dependent cell death in ABC-DLBCL greater than in GCB-DLBCL cell lines. The IC50 for CBL-C137 in ABC-DLBCL (rituximab/chemotherapy sensitive or resistant cells) ranged from 1.36 to 2.77mM. In contrast rituximab/chemotherapy GCB-DLBCL cells exhibited the highest IC50 (11.91mM, 95% C.I 7.1-19.8mM). In sensitive DLBCL cells, CBL-C137 induced both apoptosis and cell cycle arrest in G1 phase. Moreover, in vitro exposure to CBL-C137 decreased p53 and p65 in sensitive cells. CBL-C137 increased Lenalidomide, but not Ibrutinib, anti-lymphoma activity in the conditions tested. Finally, CBL-C137 did not affect rituximab or other anti-CD20 antibody-associated ADCC or CMC in DLBCL cells. Our data suggest that CBL-C137 is active in DLBCL pre-clinical models, primarily in ABC-DLBCL cell lines. In sensitive cells, CBL-C137 modulates p53 and NFkB activity and promotes death and/or cell cycle arrest. Ongoing studies are aimed to further define the anti-tumor effects of CBL-C137 in combination with other small molecules inhibitors targeting directly or indirectly NFkB activity in lymphoma. (Research, in part, supported by a NIH grant R01 CA136907-01A1 awarded to Roswell Park Cancer Institute and The Eugene and Connie Corasanti Lymphoma Research Fund) Disclosures: Czuczman: Genetech, Onyx, Celgene, Astellas, Millennium, Mundipharma: Advisory Committees Other.


Blood ◽  
2008 ◽  
Vol 112 (11) ◽  
pp. 601-601 ◽  
Author(s):  
Kristopher A Sarosiek ◽  
Hovav Nechushtan ◽  
Eli Avisar ◽  
Izidore S Lossos

Abstract IL-21, a recently discovered member of the IL-2 cytokine family, has been shown to have diverse regulatory effects on B-cells including the induction of antibody secretion, differentiation, or apoptosis depending on the cellular milieu and activation status. However, the effects of IL-21 on B-cell neoplasms such as DLBCL are largely unknown. Our research has uncovered the widespread expression of the IL-21 receptor (IL-21R) in B-cell lymphomas including DLBCL. Our results confirmed reports that IL-21R stimulation results in potent phosphorylation of STAT-1 and -3 and weak activation of STAT-5. However, our findings also show that treatment of DLBCL cell lines with IL-21 induces cell cycle arrest and apoptosis. The cell death is caspase-dependent and evident in a majority of DLBCL cell lines. To further examine the potential therapeutic applicability of IL-21, we assessed the effects of IL-21 on primary DLBCL tumor cells and in vivo DLBCL mice models. In primary tumors, IL-21 induced apoptosis in five of five DLBCLs compared to two of three follicular lymphomas, and two of seven chronic lymphocytic leukemias. No apoptosis or cell death was induced in normal peripheral B-lymphocytes. In xenograft DLBCL tumors, in situ IL-21 injections induced tumor regression and dramatically extended the overall survival of mice (P<0.001). To elucidate the mechanism of IL-21-induced cell death, microarray analysis was performed on endogenously sensitive or resistant DLBCL cell lines as well as an RCK8 cell line that acquired IL-21 resistance following chronic exposure to the cytokine. The most striking difference between IL-21 sensitive and resistant cell lines was observed in the expression of c-Myc, a known target of STAT-3, which was only induced in cell lines undergoing apoptosis upon IL-21 treatment. We have shown that the cell death associated with IL-21 treatment was prevented by utilizing c-Myc specific siRNAs and shRNA. Interestingly, c-Myc upregulation and cell death was also prevented upon knockdown of STAT-3 with siRNAs. Stimulation of the STAT-3-cMYC signaling pathway led to decreases in levels of anti-apoptotic proteins Bcl-XL and Bcl-2, which are bone-fide targets of c-Myc. Our results delineate a new IL-21-induced pro-apoptotic signaling pathway involving STAT-3 and c-Myc, which are usually considered as anti-apoptotic effectors in cancer cells. Furthermore, our findings demonstrate that IL-21 is a highly potent anti-DLBCL agent in vitro and in xenograft DLBCL models and warrant initiation of clinical studies in patients.


Oncogene ◽  
2013 ◽  
Vol 33 (47) ◽  
pp. 5415-5423 ◽  
Author(s):  
A Newbold ◽  
J M Salmon ◽  
B P Martin ◽  
K Stanley ◽  
R W Johnstone

Blood ◽  
2004 ◽  
Vol 104 (11) ◽  
pp. 4620-4620
Author(s):  
Kathrin Wanner ◽  
Susanne Hipp ◽  
Christian Peschel ◽  
Thomas Decker

Abstract Purpose: DLBCL is a common lymphoma entity. Although a significant amount of patients can be cured with modern chemotherapeutic regimen, a substantial proportion of patients die due to progressive disease. Therefore, new therapeutic strategies are clearly needed. Inhibitors of MTOR (mammalian target of rapamycin) represent a new class of antiproliferative drugs with applications as immunosuppressive and anticancer agents. Extensive safety data exist on RAD001 which is already approved as an immunosuppressant in organ transplant recipients. Methods: We have analyzed the effects of MTOR inhibition in three DLBCL cell lines: SUDHL-4, DB, DOOH-2. Propidium Iodide staining, MTT- and Annexin-V assays were performed to test the effects on viability, cell cycle distribution and apoptosis. Expression of cell cycle regulatory and phosphorylation of p70 s6 kinase and 4-EBP-1 molecules was revealed in western blot experiments Results: Rapamycin and RAD001 inhibited cell cycle progression in DLBCL cells by inducing a G1 arrest without inducing apoptosis. Phosphorylation of the main targets of MTOR, p70s6 kinase and 4-EBP-1 was reduced in cells cultured in the presence of RAD001.Cell cycle arrest was accompanied by reduced phosphorylation of the Retinoblastoma protein (RB) as well as reduced expression of cyclin D3, E and A in all cell lines. Although the effect of chemotherapeutic agents like Vincristin or Doxorubicin was not enhance by Rad001, Rituximab induced cytotoxicity was augemted in both Rituximab sensitive cell lines. Conclusion: MTOR Inhibition is a promising therapeutic strategy in DLBCL of the germinal center like subtype by inducing a G1 arrest and augments Rituximab induced cytotoxicity. Therefore, combination of these drugs might be an interesting new therapeutic approach in DLBCL patients.


Oncotarget ◽  
2016 ◽  
Vol 8 (8) ◽  
pp. 12741-12753 ◽  
Author(s):  
Juan J. Gu ◽  
Gregory P. Kaufman ◽  
Cory Mavis ◽  
Myron S Czuczman ◽  
Francisco J. Hernandez-Ilizaliturri

Immunology ◽  
2009 ◽  
Vol 128 (3) ◽  
pp. 360-368 ◽  
Author(s):  
Ga Bin Park ◽  
Hyunkeun Song ◽  
Yeong-Seok Kim ◽  
Minjung Sung ◽  
Jeoung W. Ryu ◽  
...  

Molecules ◽  
2020 ◽  
Vol 25 (11) ◽  
pp. 2687
Author(s):  
Mateus L. Nogueira ◽  
Emilly J. S. P. de Lima ◽  
Asenate A. X. Adrião ◽  
Sheila S. Fontes ◽  
Valdenizia R. Silva ◽  
...  

Cyperus articulatus L. (Cyperaceae), popularly known in Brazil as “priprioca” or “piriprioca”, is a tropical and subtropical plant used in popular medical practices to treat many diseases, including cancer. In this study, C. articulatus rhizome essential oil (EO), collected from the Brazilian Amazon rainforest, was addressed in relation to its chemical composition, induction of cell death in vitro and inhibition of tumor development in vivo, using human hepatocellular carcinoma HepG2 cells as a cell model. EO was obtained by hydrodistillation using a Clevenger-type apparatus and characterized qualitatively and quantitatively by gas chromatography coupled to mass spectrometry (GC-MS) and gas chromatography with flame ionization detection (GC-FID), respectively. The cytotoxic activity of EO was examined against five cancer cell lines (HepG2, HCT116, MCF-7, HL-60 and B16-F10) and one non-cancerous one (MRC-5) using the Alamar blue assay. Cell cycle distribution and cell death were investigated using flow cytometry in HepG2 cells treated with EO after 24, 48 and 72 h of incubation. The cells were also stained with May–Grunwald–Giemsa to analyze the morphological changes. The anti-liver-cancer activity of EO in vivo was evaluated in C.B-17 severe combined immunodeficient (SCID) mice with HepG2 cell xenografts. The main representative substances of this EO sample were muskatone (11.6%), cyclocolorenone (10.3%), α-pinene (8.26%), pogostol (6.36%), α-copaene (4.83%) and caryophyllene oxide (4.82%). EO showed IC50 values for cancer cell lines ranging from 28.5 µg/mL for HepG2 to >50 µg/mL for HCT116, and an IC50 value for non-cancerous of 46.0 µg/mL (MRC-5), showing selectivity indices below 2-fold for all cancer cells tested. HepG2 cells treated with EO showed cell cycle arrest at G2/M along with internucleosomal DNA fragmentation. The morphological alterations included cell shrinkage and chromatin condensation. Treatment with EO also increased the percentage of apoptotic-like cells. The in vivo tumor mass inhibition rates of EO were 46.5–50.0%. The results obtained indicate the anti-liver-cancer potential of C. articulatus rhizome EO.


Molecules ◽  
2020 ◽  
Vol 25 (21) ◽  
pp. 5016
Author(s):  
Aveen N. Adham ◽  
Mohamed Elamir F. Hegazy ◽  
Alaadin M. Naqishbandi ◽  
Thomas Efferth

Thymus vulgaris and Arctium lappa have been used as a folk remedy in the Iraqi Kurdistan region to deal with different health problems. The aim of the current study is to investigate the cytotoxicity of T. vulgaris and A. lappa in leukemia and multiple myeloma (MM) cell lines and determine the mode of cell death triggered by the most potent cytotoxic fractions of both plants in MM. Resazurin assay was used to evaluate cytotoxic and ferroptosis activity, apoptosis, and modulation in the cell cycle phase were investigated via Annexin V-FITC/PI dual stain and cell-cycle arrest assays. Furthermore, we used western blotting assay for the determination of autophagy cell death. n-Hexane, chloroform, ethyl acetate, and butanol fractions of T. vulgaris and A. lappa exhibited cytotoxicity in CCRF-CEM and CEM/ADR 5000 cell lines at concentration range 0.001–100 μg/mL with potential activity revealed by chloroform and ethyl acetate fractions. NCI-H929 displayed pronounced sensitivity towards T. vulgaris (TCF) and A. lappa (ACF) chloroform fractions with IC50 values of 6.49 ± 1.48 and 21.9 ± 0.69 μg/mL, respectively. TCF induced apoptosis in NCI-H929 cells with a higher ratio (71%), compared to ACF (50%) at 4 × IC50. ACF demonstrated more potent autophagy activity than TCF. TCF and ACF induced cell cycle arrest and ferroptosis. Apigenin and nobiletin were identified in TCF, while nobiletin, ursolic acid, and lupeol were the main compounds identified in ACF. T. vulgaris and A. lappa could be considered as potential herbal drug candidates, which arrest cancer cell proliferation by induction of apoptosis, autophagic, and ferroptosis.


Sign in / Sign up

Export Citation Format

Share Document