Potent obatoclax cytotoxicity and activation of triple death mode killing across infant acute lymphoblastic leukemia

Blood

Volumn 121, Issue 14, 2013, Pages 2689-2703

  Urtishak, Karen A ^a   Edwards, Alena Y Z ^a   Wang, Li San ^b   Hudome, Amanda ^a   Robinson, Blaine W ^a   Barrett, Jeffrey S ^a,b   Cao, Kajia ^b   Cory, Lori ^a   Moore, Jonni S ^b   Bantly, Andrew D ^b   Yu, Qian Chun ^b   Chen, I Ming L ^c   Atlas, Susan R ^c   Willman, Cheryl L ^c   Kundu, Mondira ^d   Carroll, Andrew J ^e   Heerema, Nyla A ^f   Devidas, Meenakshi ^g   Hilden, Joanne M ^h   Dreyer, ZoAnn E ⁱ   Hunger, Stephen P ^h   Reaman, Gregory H ^j   Felix, Carolyn A ^a,b   more..

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF NEW MEXICO   (United States)

^d Division of Virology Department of Infectious Diseases St Jude Children's Hospital   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f OHIO STATE UNIVERSITY   (United States)

^g Children's Oncology Group   (United States)

^h UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

ⁱ BAYLOR COLLEGE OF MEDICINE   (United States)

^j CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MIXED LINEAGE LEUKEMIA PROTEIN; OBATOCLAX; PROTEIN BCL 2; ANTINEOPLASTIC AGENT; MLL AF4 FUSION PROTEIN, HUMAN; MLL ENL ONCOPROTEIN, HUMAN; MLL PROTEIN, HUMAN; MLL-AF4 FUSION PROTEIN, HUMAN; MLL-ENL ONCOPROTEIN, HUMAN; ONCOPROTEIN; PYRROLE DERIVATIVE;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER PROGNOSIS; CONTROLLED STUDY; EC50; ELECTRON MICROSCOPY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFANT; MAXIMUM PLASMA CONCENTRATION; MICROARRAY ANALYSIS; MTT ASSAY; NECROPTOSIS; PRIORITY JOURNAL; WESTERN BLOTTING; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; NECROSIS; NEWBORN; PATHOLOGY; PHASE 1 CLINICAL TRIAL; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; INFANT; INFANT, NEWBORN; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NECROSIS; ONCOGENE PROTEINS, FUSION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRROLES;

MLCS; MLOWN;

EID: 84878254063     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-04-425033     Document Type: Article

References (41)

1. Hilden JM, Dinndorf PA, Meerbaum SO, et al; Children’s Oncology Group. Analysis of prognostic factors of acute lymphoblastic leukemia in infants: report on CCG 1953 from the Children’s Oncology Group. Blood. 2006;108(2): 441-451.
2. Pieters R, Schrappe M, De Lorenzo P, et al. A treatment protocol for infants younger than 1 year with acute lymphoblastic leukaemia (Interfant-99): an observational study and a multicentre randomised trial. Lancet. 2007; 370(9583):240-250.
3. Salzer WL, Jones TL, Devidas M, et al. Modifications to induction therapy decrease risk of early death in infants with acute lymphoblastic leukemia treated on Children’s Oncology Group P9407. Pediatr Blood Cancer. 2012;59(5): 834-839.
4. Kersey JH, Wang D, Oberto M. Resistance of t(4;11) (MLL-AF4 fusion gene) leukemias to stress-induced cell death: possible mechanism for extensive extramedullary accumulation of cells and poor prognosis. Leukemia. 1998; 12(10):1561-1564.
5. Robinson BW, Behling KC, Gupta M, et al. Abundant anti-apoptotic BCL-2 is a molecular target in leukaemias with t(4;11) translocation. Br J Haematol. 2008;141(6):827-839.
6. Nguyen M, Marcellus RC, Roulston A, et al. Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc Natl Acad Sci USA. 2007;104(49):19512-19517.
7. Stam RW, Den Boer ML, Schneider P, et al. Association of high-level MCL-1 expression with in vitro and in vivo prednisone resistance in MLL-rearranged infant acute lymphoblastic leukemia. Blood. 2010;115(5): 1018-1025.
8. Thomas M, Gessner A, Vornlocher HP, et al. Targeting MLL-AF4 with short interfering RNAs inhibits clonogenicity and engraftment of t(4;11)positive human leukemic cells. Blood. 2005; 106(10):3559-3566.
9. Fennell DA, Corbo MV, Dean NM, et al. In vivo suppression of Bcl-XL expression facilitates chemotherapy-induced leukaemia cell death in a SCID/NOD-Hu model. Br J Haematol. 2001; 112(3):706-713.
10. Brown PA, Felix CA. Molecularly Targeted Therapy for Infant ALL. In: Houghton PJ, Arceci RJ, eds. Molecularly Targeted Therapy for Childhood Cancer. New York: Springer Science; 2010:31-58.
11. Schimmer AD, O’Brien S, Kantarjian H, et al. A phase I study of the pan bcl-2 family inhibitor obatoclax mesylate in patients with advanced hematologic malignancies. Clin Cancer Res. 2008;14(24):8295-8301.
12. Pérez-Galán P, Roué G, Villamor N, et al. The BH3-mimetic GX15-070 synergizes with bortezomib in mantle cell lymphoma by enhancing Noxa-mediated activation of Bak. Blood. 2007; 109(10):4441-4449.
13. Vogler M, Weber K, Dinsdale D, et al. Different forms of cell death induced by putative BCL2 inhibitors. Cell Death Differ. 2009;16(7): 1030-1039.
14. Huang S, Okumura K, Sinicrope FA. BH3 mimetic obatoclax enhances TRAIL-mediated apoptosis in human pancreatic cancer cells. Clin Cancer Res. 2009;15(1):150-159.
15. Bonapace L, Bornhauser BC, Schmitz M, et al. Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J Clin Invest. 2010;120(4): 1310-1323.
16. Robinson BW, Devidas M, Carroll AJ, et al. Specific MLL partner genes in infant acute lymphoblastic leukemia (ALL) associated with outcome are linked to age and white blood cell count (WBC) at diagnosis: a report on the Children’s Oncology Group (COG) P9407 trial [abstract]. Blood. 2009;114(22):907. Abstract 907.
17. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2008.
18. Kang H, Chen IM, Wilson CS, et al. Gene expression classifiers for relapse-free survival and minimal residual disease improve risk classification and outcome prediction in pediatric B-precursor acute lymphoblastic leukemia. Blood. 2010;115(7):1394-1405.
19. Vandenabeele P, Galluzzi L, Vanden Berghe T, et al. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol. 2010;11(10):700-714.
20. Wang D, Yu QC, Schröer J, et al. Human cytomegalovirus uses two distinct pathways to enter retinal pigmented epithelial cells. Proc Natl Acad Sci USA. 2007;104(50): 20037-20042.
21. O’Brien SM, Claxton DF, Crump M, et al. Phase I study of obatoclax mesylate (GX15-070), a small molecule pan-Bcl-2 family antagonist, in patients with advanced chronic lymphocytic leukemia. Blood. 2009;113(2):299-305.
22. Patel T, Gores GJ, Kaufmann SH. The role of proteases during apoptosis. FASEB J. 1996; 10(5):587-597.
23. Kroemer G, Galluzzi L, Vandenabeele P, et al; Nomenclature Committee on Cell Death 2009. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009; 16(1):3-11.
24. Klionsky DJ, Abeliovich H, Agostinis P, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4(2):151-175.
25. Degterev A, Hitomi J, Germscheid M, et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol. 2008;4(5): 313-321.
26. Sinha S, Levine B. The autophagy effector Beclin 1: a novel BH3-only protein. Oncogene. 2008; 27(Suppl 1):S137-S148.
27. Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122(6):927-939.
28. Shimizu S, Kanaseki T, Mizushima N, et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol. 2004;6(12):1221-1228.
29. Vandenabeele P, Declercq W, Van Herreweghe F, et al. The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Sci Signal. 2010; 3(115):re4.
30. Degterev A, Huang Z, Boyce M, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005;1(2):112-119.
31. Reed JC. Bcl-2-family proteins and hematologic malignancies: history and future prospects. Blood. 2008;111(7):3322-3330.
32. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010; 221(1):3-12.
33. Campàs C, Cosialls AM, Barragán M, et al. Bcl-2 inhibitors induce apoptosis in chronic lymphocytic leukemia cells. Exp Hematol. 2006;34(12): 1663-1669.
34. Hochhauser D. Modulation of chemosensitivity through altered expression of cell cycle regulatory genes in cancer. Anticancer Drugs. 1997;8(10): 903-910.
35. Konopleva M, Watt J, Contractor R, et al. Mechanisms of antileukemic activity of the novel Bcl-2 homology domain-3 mimetic GX15-070 (obatoclax). Cancer Res. 2008;68(9): 3413-3420.
36. Wlodkowic D, Telford W, Skommer J, et al. Apoptosis and beyond: cytometry in studies of programmed cell death. Methods Cell Biol. 2011; 103:55-98.
37. Douglas RS, Tarshis AD, Pletcher CH Jr, et al. A simplified method for the coordinate examination of apoptosis and surface phenotype of murine lymphocytes. J Immunol Methods. 1995;188(2): 219-228.
38. Hu X, Xuan Y. Bypassing cancer drug resistance by activating multiple death pathways—a proposal from the study of circumventing cancer drug resistance by induction of necroptosis. Cancer Lett. 2008;259(2): 127-137.
39. Wei Y, Kadia T, Tong W, et al. The combination of a histone deacetylase inhibitor with the Bcl-2 homology domain-3 mimetic GX15-070 has synergistic antileukemia activity by activating both apoptosis and autophagy. Clin Cancer Res. 2010; 16(15):3923-3932.
40. Heidari N, Hicks MA, Harada H. GX15-070 (obatoclax) overcomes glucocorticoid resistance in acute lymphoblastic leukemia through induction of apoptosis and autophagy. Cell Death Dis. 2010;1:e76.
41. Liedtke M, Cleary ML. Therapeutic targeting of MLL. Blood. 2009;113(24):6061-6068.