In vivo resistance to first-line chemotherapy, including to glucocorticoids, is a strong predictor of poor outcome in children with acute lymphoblastic leukemia (ALL). Modulation of cell death regulators represents an attractive strategy for subverting such drug resistance. Here we report complete resensitization of multidrug-resistant childhood ALL cells to glucocorticoids and other cytotoxic agents with subcytotoxic concentrations of obatoclax, a putative antagonist of BCL-2 family members. The reversal of glucocorticoid resistance occurred through rapid activation of autophagy-dependent necroptosis, which bypassed the block in mitochondrial apoptosis. This effect was associated with dissociation of the autophagy inducer beclin-1 from the antiapoptotic BCL-2 family member myeloid cell leukemia sequence 1 (MCL-1) and with a marked decrease in mammalian target of rapamycin (mTOR) activity. Consistent with a protective role for mTOR in glucocorticoid resistance in childhood ALL, combination of rapamycin with the glucocorticoid dexamethasone triggered autophagy-dependent cell death, with characteristic features of necroptosis. Execution of cell death, but not induction of autophagy, was strictly dependent on expression of receptor-interacting protein (RIP-1) kinase and cylindromatosis (turban tumor syndrome) (CYLD), two key regulators of necroptosis. Accordingly, both inhibition of RIP-1 and interference with CYLD restored glucocorticoid resistance completely. Together with evidence for a chemosensitizing activity of obatoclax in vivo, our data provide a compelling rationale for clinical translation of this pharmacological approach into treatments for patients with refractory ALL.
Laura Bonapace, Beat C. Bornhauser, Maike Schmitz, Gunnar Cario, Urs Ziegler, Felix K. Niggli, Beat W. Schäfer, Martin Schrappe, Martin Stanulla, Jean-Pierre Bourquin
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Molecular and Cellular Biochemistry | 2016 |
Effects of a novel β–lapachone derivative on Trypanosoma cruzi: Parasite death involving apoptosis, autophagy and necrosis
DO Anjos, ES Alves, VT Gonçalves, SS Fontes, ML Nogueira, AM Suarez-Fontes, JB da Costa, F Rios-Santos, MA Vannier-Santos |
International Journal for Parasitology Drugs and Drug Resistance | 2016 |
Necroptosis in tumorigenesis, activation of anti-tumor immunity, and cancer therapy
MB Meng, HH Wang, YL Cui, ZQ Wu, YY Shi, NG Zaorsky, L Deng, ZY Yuan, Y Lu, P Wang |
Oncotarget | 2016 |
Wogonin induces Beclin-1/PI3K and reactive oxygen species-mediated autophagy in human pancreatic cancer cells
SJ Li, SJ Sun, J Gao, FB Sun |
Oncology Letters | 2016 |
Smac mimetic LCL161 overcomes protective ER stress induced by obatoclax, synergistically causing cell death in multiple myeloma
V Ramakrishnan, M Gomez, V Prasad, T Kimlinger, U Painuly, B Mukhopadhyay, J Haug, L Bi, SV Rajkumar, S Kumar |
Oncotarget | 2016 |
Pan-Bcl-2 inhibitor Obatoclax is a potent late stage autophagy inhibitor in colorectal cancer cells independent of canonical autophagy signaling
BC Koehler, A Jassowicz, AL Scherr, S Lorenz, P Radhakrishnan, N Kautz, C Elssner, J Weiss, D Jaeger, M Schneider, H Schulze-Bergkamen |
BMC Cancer | 2015 |
Glucocorticoid Signaling
JC Wang, C Harris |
Glucocorticoid Signaling | 2015 |
Protective Macroautophagy Is Involved in Vitamin E Succinate Effects on Human Gastric Carcinoma Cell Line SGC-7901 by Inhibiting mTOR Axis Phosphorylation
L Hou, Y Li, H Song, Z Zhang, Y Sun, X Zhang, K Wu, YJ Wang |
PloS one | 2015 |
BCL2 Inhibitor (ABT-737): A Restorer of Prednisolone Sensitivity in Early T-Cell Precursor-Acute Lymphoblastic Leukemia with High MEF2C Expression?
S Kawashima-Goto, T Imamura, C Tomoyasu, M Yano, H Yoshida, A Fujiki, S Tamura, S Osone, H Ishida, A Morimoto, H Kuroda, H Hosoi, F Bertolini |
PloS one | 2015 |
Autophagy collaborates with ubiquitination to downregulate oncoprotein E2A/Pbx1 in B-cell acute lymphoblastic leukemia
N Yuan, L Song, W Lin, Y Cao, F Xu, S Liu, A Zhang, Z Wang, X Li, Y Fang, H Zhang, W Zhao, S Hu, J Wang, S Zhang |
Blood Cancer Journal | 2015 |
Untangling knots between autophagic targets and candidate drugs, in cancer therapy
T Xie, SJ Li, MR Guo, Y Wu, HY Wang, K Zhang, X Zhang, L Ouyang, J Liu |
Cell Proliferation | 2015 |
Cell death by autophagy: emerging molecular mechanisms and implications for cancer therapy
S Fulda, D Kögel |
Oncogene | 2015 |
Differential roles of RIPK1 and RIPK3 in TNF-induced necroptosis and chemotherapeutic agent-induced cell death
K Moriwaki, J Bertin, PJ Gough, GM Orlowski, FK Chan |
Cell Death and Disease | 2015 |
Aging and uremia: Is there cellular and molecular crossover?
WE White |
World Journal of Nephrology | 2015 |
Interferon Regulatory Factor-1 Signaling Regulates the Switch between Autophagy and Apoptosis to Determine Breast Cancer Cell Fate
JL Schwartz-Roberts, KL Cook, C Chen, AN Shajahan-Haq, M Axelrod, A Warri, RB Riggins, L Jin, BR Haddad, BV Kallakury, WT Baumann, R Clarke |
Cancer research | 2015 |
CYLD Regulates Noscapine Activity in Acute Lymphoblastic Leukemia via a Microtubule-Dependent Mechanism
Y Yang, J Ran, L Sun, X Sun, Y Luo, B Yan, Tala, M Liu, D Li, L Zhang, G Bao, J Zhou |
Theranostics | 2015 |
Cell death induction by the BH3 mimetic GX15-070 in thyroid carcinoma cells
M Broecker-Preuss, J Viehof, H Jastrow, N Becher-Boveleth, D Fuhrer, K Mann |
Journal of Experimental & Clinical Cancer Research | 2015 |
Targeting mTOR/p70S6K/glycolysis signaling pathway restores glucocorticoid sensitivity to 4E-BP1 null Burkitt Lymphoma
L Gu, L Xie, C Zuo, Z Ma, Y Zhang, Y Zhu, J Gao |
BMC Cancer | 2015 |
Genomics and drug profiling of fatal TCF3-HLF−positive acute lymphoblastic leukemia identifies recurrent mutation patterns and therapeutic options
U Fischer, M Forster, A Rinaldi, T Risch, S Sungalee, HJ Warnatz, B Bornhauser, M Gombert, C Kratsch, AM Stütz, M Sultan, J Tchinda, CL Worth, V Amstislavskiy, N Badarinarayan, A Baruchel, T Bartram, G Basso, C Canpolat, G Cario, H Cavé, D Dakaj, M Delorenzi, MP Dobay, C Eckert, E Ellinghaus, S Eugster, V Frismantas, S Ginzel, OA Haas, O Heidenreich, G Hemmrich-Stanisak, K Hezaveh, JI Höll, S Hornhardt, P Husemann, P Kachroo, CP Kratz, G Kronnie, B Marovca, F Niggli, AC McHardy, AV Moorman, R Panzer-Grümayer, BS Petersen, B Raeder, M Ralser, P Rosenstiel, D Schäfer, M Schrappe, S Schreiber, M Schütte, B Stade, R Thiele, N der Weid, A Vora, M Zaliova, L Zhang, T Zichner, M Zimmermann, H Lehrach, A Borkhardt, JP Bourquin, A Franke, JO Korbel, M Stanulla, ML Yaspo |
Nature Genetics | 2015 |
Tissue acidosis induces neuronal necroptosis via ASIC1a channel independent of its ionic conduction: ( A1 ) Electron microscopy images of neurons treated with pH 7.4 (left) or pH 6.0 solution (middle and right). Of 57 cells counted in the pH 6.0-treated samples, 47 showed morphology similar to that shown in the middle and right panels. For pH 7.4-treated samples, the majority of cells had a similar morphology to that shown in the left panel; only 3 out of the 41 cells examined showed morphology that resembled that in the middle panel. ( A2 ) Enlarged images from the white boxes in A1 showing swelling of organelles in pH 6.0- but not pH 7.4-treated neurons. ( B ) PcTX1 (10 nM) and Nec-1 (20 μM), but not BHA (100 μM), BEL (30 μM), DPI (15 μM), RTO (25 μM), CHX (100 μM), or z-VAD-fmk (10 μM), rescued cells from acid-induced neuronal death (indicated by the dashed line) (n=4–12, ***pC1) Rescue from acid-induced neuronal death by 20 μM Nec-1 (propidium iodide [PI] staining assay). ( C2 ) Summary data for C1 . At least 200 neurons were counted for each condition (***pD) Knockdown efficiency of RIP1 shRNA as determined by Western blotting (***pE) Rescue of acid-induced neuronal death by RIP1 shRNA (CTB assay, n=3, ***p
YZ Wang, JJ Wang, Y Huang, F Liu, WZ Zeng, Y Li, ZG Xiong, MX Zhu, TL Xu |
eLife | 2015 |
Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD
Kenji Mizumura, Suzanne Cloonan, Kiichi Nakahira, Abhiram R. Bhashyam, Morgan Cervo, Tohru Kitada, Kimberly Glass, Caroline Owen, Ashfaq Mahmood, George Washko, Shu Hashimoto, Stefan Ryter, Augustine M. K. Choi |
Journal of Clinical Investigation | 2014 |
A Bim-targeting strategy overcomes adaptive bortezomib resistance in myeloma through a novel link between autophagy and apoptosis
S Chen, Y Zhang, L Zhou, Y Leng, H Lin, M Kmieciak, XY Pei, R Jones, RZ Orlowski, Y Dai, S Grant |
Blood | 2014 |
Targeting SQSTM1/p62 Induces Cargo Loading Failure and Converts Autophagy to Apoptosis via NBK/Bik
S Chen, L Zhou, Y Zhang, Y Leng, XY Pei, H Lin, R Jones, RZ Orlowski, Y Dai, S Grant |
Molecular and cellular biology | 2014 |
Targeting the mitochondrial apoptotic pathway: a preferred approach in hematologic malignancies?
K Brinkmann, H Kashkar |
Cell Death and Disease | 2014 |
Human Cancer Growth and Therapy in Immunodeficient Mouse Models
LD Shultz, N Goodwin, F Ishikawa, V Hosur, BL Lyons, DL Greiner |
Cold Spring Harbor Protocols | 2014 |
Mcl-1 ubiquitination: unique regulation of an essential survival protein
B Mojsa, I Lassot, S Desagher |
Cells | 2014 |
The Impact of Autophagy on Cell Death Modalities
SW Ryter, K Mizumura, AM Choi |
International Journal of Cell Biology | 2014 |
Targeting the apoptosis pathway in hematologic malignancies
S Zaman, R Wang, V Gandhi |
Leukemia & Lymphoma | 2014 |
Taking aim at Alzheimer's disease through the mammalian target of rapamycin
K Maiese |
Annals of Medicine | 2014 |
Autosis and autophagic cell death: the dark side of autophagy
Y Liu, B Levine |
Cell Death and Differentiation | 2014 |
Autophagy in the physiology and pathology of the central nervous system
V Nikoletopoulou, ME Papandreou, N Tavernarakis |
Cell Death and Differentiation | 2014 |
Cell and Molecular Determinants of In Vivo Efficacy of the BH3 Mimetic ABT-263 against Pediatric Acute Lymphoblastic Leukemia Xenografts
S Suryani, H Carol, TN Chonghaile, V Frismantas, C Sarmah, L High, B Bornhauser, MJ Cowley, B Szymanska, K Evans, I Boehm, E Tonna, L Jones, DM Manesh, RT Kurmasheva, C Billups, W Kaplan, A Letai, JP Bourquin, PJ Houghton, MA Smith, RB Lock |
Clinical cancer research | 2014 |
Anticancer Agents Targeted to Sirtuins
T Kozako, T Suzuki, M Yoshimitsu, N Arima, S Honda, S Soeda |
Molecules (Basel, Switzerland) | 2014 |
Assessment of the effect of sphingosine kinase inhibitors on apoptosis,unfolded protein response and autophagy of T-cell acute lymphoblastic leukemia cells; indications for novel therapeutics
Evangelisti C, Evangelisti C, Teti G, Chiarini F, Falconi M, Melchionda F, Pession A, Bertaina A, Locatelli F, McCubrey JA, Beak DJ, Bittman R, Pyne S, Pyne NJ, Martelli AM |
Oncotarget | 2014 |
WISP1: Clinical Insights for a Proliferative and Restorative Member of the CCN Family
Maiese K |
Current neurovascular research | 2014 |
RFX1–dependent activation of SHP-1 induces autophagy by a novel obatoclax derivative in hepatocellular carcinoma cells
Su JC, Tseng PH, Hsu CY, Tai WT, Huang JW, Ko CH, Lin MW, Liu CY, Chen KF, Shiau CW |
Oncotarget | 2014 |
Image-based RNA interference screening reveals an individual dependence of acute lymphoblastic leukemia on stromal cysteine support
Boutter J, Huang Y, Marovca B, Vonderheit A, Grotzer MA, Eckert C, Cario G, Wollscheid B, Horvath P, Bornhauser BC, Bourquin JP |
Oncotarget | 2014 |
Cutting through the complexities of mTOR for the treatment of stroke.
Maiese K |
Current neurovascular research | 2014 |
Inhibiting autophagy potentiates the anticancer activity of IFN1@/IFNα in chronic myeloid leukemia cells
S Zhu, L Cao, Y Yu, L Yang, M Yang, K Liu, J Huang, R Kang, KM Livesey, D Tang |
Autophagy | 2013 |
MicroRNAs and Glucocorticoid-Induced Apoptosis in Lymphoid Malignancies
RV Sionov |
ISRN Hematology | 2013 |
Photoreceptor cell death and rescue in retinal detachment and degenerations
Y Murakami, S Notomi, T Hisatomi, T Nakazawa, T Ishibashi, JW Miller, DG Vavvas |
Progress in Retinal and Eye Research | 2013 |
Glucocorticoids and Osteocyte Autophagy
W Yao, W Dai, JX Jiang, NE Lane |
Bone | 2013 |
An evidence-based review of obatoclax mesylate in the treatment of hematological malignancies
CA Goard, AD Schimmer |
Core evidence | 2013 |
A JNK-mediated autophagy pathway that triggers c-IAP degradation and necroptosis for anticancer chemotherapy
W He, Q Wang, B Srinivasan, J Xu, MT Padilla, Z Li, X Wang, Y Liu, X Gou, HM Shen, C Xing, Y Lin |
Oncogene | 2013 |
Obatoclax (GX15-070) triggers necroptosis by promoting the assembly of the necrosome on autophagosomal membranes
F Basit, S Cristofanon, S Fulda |
Cell Death and Differentiation | 2013 |
Placental autophagy regulation by the BOK-MCL1 rheostat
M Kalkat, J Garcia, J Ebrahimi, M Melland-Smith, T Todros, M Post, I Caniggia |
Autophagy | 2013 |
BECN1 and BIM interactions with MCL-1 determine fludarabine resistance in leukemic B cells
A Sharma, K Singh, S Mazumder, BT Hill, M Kalaycio, A Almasan |
Cell Death and Disease | 2013 |
The mechanism of necroptosis in normal and cancer cells
S Fulda |
Cancer biology & therapy | 2013 |
Potent obatoclax cytotoxicity and activation of triple death mode killing across infant acute lymphoblastic leukemia
KA Urtishak, AY Edwards, LS Wang, A Hudome, BW Robinson, JS Barrett, K Cao, L Cory, JS Moore, AD Bantly, QC Yu, IM Chen, SR Atlas, CL Willman, M Kundu, AJ Carroll, NA Heerema, M Devidas, JM Hilden, ZE Dreyer, SP Hunger, GH Reaman, CA Felix |
Blood | 2013 |
Identification of novel predictor classifiers for inflammatory bowel disease by gene expression profiling
T Montero-Meléndez, X Llor, E García-Planella, M Perretti, A Suárez |
PloS one | 2013 |
The synergism of MCL1 and glycolysis on pediatric acute lymphoblastic leukemia cell survival and prednisolone resistance
IM Ariës, BR Hansen, T Koch, R Dungen, WE Evans, R Pieters, ML Boer |
Haematologica | 2013 |
Shikonin kills glioma cells through necroptosis mediated by RIP-1
C Huang, Y Luo, J Zhao, F Yang, H Zhao, W Fan, P Ge |
PloS one | 2013 |
Potent antitumor activity of oncolytic adenovirus expressing Beclin-1 via induction of autophagic cell death in leukemia
Tong Y, You L, Liu H, Li L, Meng H, Qian Q, Qian W |
Oncotarget | 2013 |
Sphingosine analogue drug FTY720 targets I2PP2A/SET and mediates lung tumour suppression via activation of PP2A-RIPK1-dependent necroptosis
SA Saddoughi, S Gencer, YK Peterson, KE Ward, A Mukhopadhyay, J Oaks, J Bielawski, ZM Szulc, RJ Thomas, SP Selvam, CE Senkal, E Garrett-Mayer, RM de Palma, D Fedarovich, A Liu, AA Habib, RV Stahelin, D Perrotti, B Ogretmen |
EMBO Molecular Medicine | 2012 |
Staurosporine Induces Necroptotic Cell Death under Caspase-Compromised Conditions in U937 Cells
ZA Dunai, G Imre, G Barna, T Korcsmaros, I Petak, PI Bauer, R Mihalik |
PloS one | 2012 |
Efficacy of the investigational mTOR kinase inhibitor MLN0128 / INK128 in models of B-cell acute lymphoblastic leukemia
MR Janes, C Vu, S Mallya, M Shieh, JJ Limon, LS Li, KA Jessen, MB Martin, P Ren, MB Lilly, L Sender, Y Liu, C Rommel, DA Fruman |
Leukemia | 2012 |
The Role of mTOR Inhibitors for the Treatment of B-Cell Lymphomas
P Argyriou, P Economopoulou, S Papageorgiou |
Advances in Hematology | 2012 |
Inhibition of Bcl-2 antiapoptotic members by obatoclax potently enhances sorafenib-induced apoptosis in human myeloid leukemia cells through a Bim-dependent process
M Rahmani, MM Aust, E Attkisson, DC Williams, A Ferreira-Gonzalez, S Grant |
Blood | 2012 |
Relapsed or Refractory Pediatric Acute Lymphoblastic Leukemia: Current and Emerging Treatments
A Martin, E Morgan, N Hijiya |
Pediatric Drugs | 2012 |
Attenuation of TNFSF10/TRAIL-induced apoptosis by an autophagic survival pathway involving TRAF2- and RIPK1/RIP1-mediated MAPK8/JNK activation
W He, Q Wang, J Xu, X Xu, MT Padilla, G Ren, X Gou, Y Lin |
Autophagy | 2012 |
Copy number aberrations of BCL2 and CDKN2A/B identified by array-CGH in thymic epithelial tumors
I Petrini, PS Meltzer, PA Zucali, J Luo, C Lee, A Santoro, HS Lee, KJ Killian, Y Wang, M Tsokos, M Roncalli, SM Steinberg, Y Wang, G Giaccone |
Cell Death and Disease | 2012 |
Two hits are better than one: targeting both phosphatidylinositol 3-kinase and mammalian target of rapamycin as a therapeutic strategy for acute leukemia treatment
Martelli AM, Chiarini F, Evangelisti C, Cappellini A, Buontempo F, Bressanin D, Fini M, McCubrey JA |
Oncotarget | 2012 |
Glucocorticoid dose determines osteocyte cell fate
J Jia, W Yao, M Guan, W Dai, M Shahnazari, R Kar, L Bonewald, JX Jiang, NE Lane |
The FASEB Journal | 2011 |
Autophagy: for better or for worse
E Wirawan, TV Berghe, S Lippens, P Agostinis, P Vandenabeele |
Cell Research | 2011 |
Inhibitors of the anti-apoptotic Bcl-2 proteins: a patent review
N Bajwa, C Liao, Z Nikolovska-Coleska |
Expert Opinion on Therapeutic Patents | 2011 |
Autophagy and apoptosis- what’s the connection?
JM Gump, A Thorburn |
Trends in Cell Biology | 2011 |
Novel type II anti-CD20 monoclonal antibody (GA101) evokes homotypic adhesion and actin-dependent, lysosome-mediated cell death in B-cell malignancies
W Alduaij, A Ivanov, J Honeychurch, EJ Cheadle, S Potluri, SH Lim, K Shimada, CH Chan, A Tutt, SA Beers, MJ Glennie, MS Cragg, TM Illidge |
Blood | 2011 |
Necroptosis: Biochemical, Physiological and Pathological Aspects
Z Dunai, PI Bauer, R Mihalik |
Pathology & Oncology Research | 2011 |
Autophagic activity in cortical neurons under acute oxidative stress directly contributes to cell death
GC Higgins, RJ Devenish, PM Beart, P Nagley |
Cellular and Molecular Life Sciences | 2011 |
Necroptosis, necrostatins and tissue injury
CC Smith, DM Yellon |
Journal of Cellular and Molecular Medicine | 2011 |
Noninvasive bioluminescent imaging of primary patient acute lymphoblastic leukemia: a strategy for preclinical modeling
DM Barrett, AE Seif, C Carpenito, DT Teachey, JD Fish, CH June, SA Grupp, GS Reid |
Blood | 2011 |
A comprehensive glossary of autophagy-related molecules and processes (2 nd edition)
DJ Klionsky, EH Baehrecke, JH Brumell, CT Chu, P Codogno, AM Cuervo, J Debnath, V Deretic, Z Elazar, EL Eskelinen, S Finkbeiner, J Fueyo-Margareto, DA Gewirtz, M Jäättelä, G Kroemer, B Levine, TJ Melia, N Mizushima, DC Rubinsztein, A Simonsen, A Thorburn, M Thumm, SA Tooze |
Autophagy | 2011 |
zVAD-induced autophagic cell death requires c-Src-dependent ERK and JNK activation and reactive oxygen species generation
SY Chen, LY Chiu, MC Ma, JS Wang, CL Chien, WW Lin |
Autophagy | 2011 |
Optimization of Circulating Biomarkers of Obatoclax-Induced Cell Death in Patients with Small Cell Lung Cancer
Dean EJ, Cummings J, Roulston A, Berger M, Ranson M, Blackhall F, Dive C |
Neoplasia (New York, N.Y.) | 2011 |
Smac Mimetic Bypasses Apoptosis Resistance in FADD- or Caspase-8-Deficient Cells by Priming for Tumor Necrosis Factor α-Induced Necroptosis
Laukens B, Jennewein C, Schenk B, Vanlangenakker N, Schier A, Cristofanon S, Zobel K, Deshayes K, Vucic D, Jeremias I, Bertrand MJ, Vandenabeele P, Fulda S |
Neoplasia (New York, N.Y.) | 2011 |
Obatoclax induces Atg7-dependent autophagy independent of beclin-1 and BAX/BAK
F McCoy, J Hurwitz, N McTavish, I Paul, C Barnes, B O'Hagan, K Odrzywol, J Murray, D Longley, G McKerr, DA Fennell |
Cell Death and Disease | 2010 |
GX15-070 (obatoclax) overcomes glucocorticoid resistance in acute lymphoblastic leukemia through induction of apoptosis and autophagy
N Heidari, MA Hicks, H Harada |
Cell Death and Disease | 2010 |
The mammalian target of rapamycin inhibitor RAD001 (everolimus) synergizes with chemotherapeutic agents, ionizing radiation and proteasome inhibitors in pre-B acute lymphocytic leukemia
P Saunders, A Cisterne, J Weiss, KF Bradstock, LJ Bendall |
Haematologica | 2010 |
Novel Approaches to Prevent Leukemia Relapse Following Allogeneic Hematopoietic Cell Transplantation
MR Verneris, MJ Burke |
Current Hematologic Malignancy Reports | 2010 |
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |