Synergistic leukemia eradication by combined treatment with retinoic acid and HIF inhibition by EZN-2208 (PEG-SN38) in preclinical models of PML-RARα and PLZF-RARα-driven leukemia

Clinical Cancer Research

Volumn 21, Issue 16, 2015, Pages 3685-3694

  Coltella, Nadia ^a   Valsecchi, Roberta ^a,b   Ponente, Manfredi ^a,c   Ponzoni, Maurilio ^a,c   Bernardi, Rosa ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FIRTECAN PEGOL; HYPOXIA INDUCIBLE FACTOR 1ALPHA; RETINOIC ACID; ARSENIC TRIOXIDE; CAMPTOTHECIN; EZN-2208; HIF1A PROTEIN, HUMAN; MACROGOL DERIVATIVE; ONCOPROTEIN; ORGANOARSENIC DERIVATIVE; OXIDE; PLZF-RARALPHA FUSION PROTEIN, HUMAN; PROMYELOCYTIC LEUKEMIA-RETINOIC ACID RECEPTOR ALPHA FUSION ONCOPROTEIN; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL RENEWAL; CLONOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENTIATION; IN VITRO STUDY; IN VIVO STUDY; MIGRATION INHIBITION; MONOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; SURVIVAL TIME; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL MOTION; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LEUKEMIA, PROMYELOCYTIC, ACUTE; MUTATION; PATHOLOGY;

ANIMALS; ARSENICALS; CAMPTOTHECIN; CELL DIFFERENTIATION; CELL MOVEMENT; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LEUKEMIA, PROMYELOCYTIC, ACUTE; MICE; MUTATION; NEOPLASM PROTEINS; ONCOGENE PROTEINS, FUSION; OXIDES; POLYETHYLENE GLYCOLS; TRETINOIN;

EID: 84942916854     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-3022     Document Type: Article

References (29)

1. Ablain J, de The H. Revisiting the differentiation paradigm in acute promyelocytic leukemia. Blood 2011;117:5795-802
2. Du C, Redner RL, Cooke MP, Lavau C. Overexpression of wild-type retinoic acid receptor alpha (RARalpha) recapitulates retinoic acid-sensitive transformation of primary myeloid progenitors by acute promyelocytic leukemia RARalpha-fusion genes. Blood 1999;94:793-802.
3. Wang ZY, Chen Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood 2008;111:2505-15.
4. Lo-Coco F, Avvisati G, Vignetti M, Thiede C, Orlando SM, Iacobelli S, et al. Retinoic acid and arsenic trioxide for acute promyelocytic leukemia. N Engl J Med 2013;369:111-21.
5. Zhou DC, Kim SH, Ding W, Schultz C, Warrell RP Jr, Gallagher RE. Frequent mutations in the ligand-binding domain of PML-RARalpha after multiple relapses of acute promyelocytic leukemia: analysis for functional relationship to response to all-trans retinoic acid and histone deacetylase inhibitors in vitro and in vivo. Blood 2002;99:1356-63.
6. Goto E, Tomita A, Hayakawa F, Atsumi A, Kiyoi H, Naoe T. Missense mutations in PML-RARA critical for the lack of responsiveness to arsenic trioxide treatment. Blood 2011;118:1600-9
7. Zhu HH, Qin YZ, Huang XJ. Resistance to arsenic therapy in acute promyelocytic leukemia. N Engl J Med 2014;370:1864-6.
8. Licht JD, Chomienne C, Goy A, Chen A, Scott AA, Head DR, et al. Clinical and molecular characterization of a rare syndrome of acute promyelocytic leukemia associated with translocation (11;17). Blood 1995;85:1083-94.
9. Koken MH, Daniel MT, Gianni M, Zelent A, Licht J, Buzyn A, et al. Retinoic acid, but not arsenic trioxide, degrades the PLZF/RARalpha fusion protein, without inducing terminal differentiation or apoptosis, in a RA-therapy resistant t (11;17) (q23;q21) APL patient. Oncogene 1999;18:1113-8.
10. Nasr R, Guillemin MC, Ferhi O, Soilihi H, Peres L, Berthier C, et al. Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat Med 2008;14:1333-42.
11. Lee KE, Simon MC. From stem cellstocancer stem cells: HIF takes the stage. Curr Opin Cell Biol 2012;24:232-5.
12. Coltella N, Percio S, Valsecchi R, Cuttano R, Guarnerio J, Ponzoni M, et al. HIF factors cooperate with PML-RARalphatopromote acute promyelocytic leukemia progression and relapse. EMBO Mol Med 2014;6:640-50.
13. Percio S, Coltella N, Grisanti S, Bernardi R, Pattini L. A HIF-1 network reveals characteristics of epithelial-mesenchymal transition in acute pro-myelocytic leukemia. Genome Med 2014;6:84.
14. Zheng X, Seshire A, Ruster B, Bug G, Beissert T, Puccetti E, et al. Arsenic but not all-trans retinoic acid overcomes the aberrant stem cell capacityof PML/RARalpha-positive leukemic stem cells. Haematologica 2007;92:323-31.
15. Rapisarda A, Uranchimeg B, Sordet O, Pommier Y, Shoemaker RH, Melillo G. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications. Cancer Res 2004;64:1475-82.
16. Xia Y, Choi HK, Lee K. Recent advances in hypoxia-inducible factor (HIF)-1 inhibitors. Eur J Med Chem 2012;49:24-40.
17. Sapra P, Zhao H, Mehlig M, Malaby J, Kraft P, Longley C, et al. Novel delivery of SN38 markedly inhibits tumor growth in xenografts, including a camptothecin-11-refractory model. Clin Cancer Res 2008;14:1888-96.
18. Sapra P, Kraft P, Pastorino F, Ribatti D, Dumble M, Mehlig M, et al. Potent and sustained inhibition of HIF-1alpha and downstream genes by a polyethyleneglycol-SN38 conjugate, EZN-2208, results in anti-angiogenic effects. Angiogenesis 2011;14:245-53.
19. Pastorino F, Loi M, Sapra P, Becherini P, Cilli M, Emionite L, et al. Tumor regression and curability of preclinical neuroblastoma models by PEGy-lated SN38 (EZN-2208), a novel topoisomerase I inhibitor. Clin Cancer Res 2010;16:4809-21.
20. Grignani F, De Matteis S, Nervi C, Tomassoni L, Gelmetti V, Cioce M, et al. Fusion proteins of the retinoic acid receptor-alpha recruit histone deace-tylase in promyelocytic leukaemia. Nature 1998;391:815-8.
21. He LZ, Bhaumik M, Tribioli C, Rego EM, Ivins S, Zelent A, et al. Two critical hits for promyelocytic leukemia. Mol Cell 2000;6:1131-41.
22. Guarnerio J, Coltella N, Ala U, Tonon G, Pandolfi PP, Bernardi R. Bone marrow endosteal mesenchymal progenitors depend on HIF factors for maintenance and regulation of hematopoiesis. Stem Cell Reports 2014;2:794-809.
23. Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006;6:789-802.
24. Minucci S, Monestiroli S, Giavara S, Ronzoni S, Marchesi F, Insinga A, et al. PML-RAR induces promyelocytic leukemias with high efficiency following retroviral gene transfer into purified murine hematopoietic progenitors. Blood 2002;100:2989-95.
25. Guibal FC, Alberich-Jorda M, Hirai H, Ebralidze A, Levantini E, Di Ruscio A, et al. Identification of a myeloid committed progenitor as the cancer-initiating cell in acute promyelocytic leukemia. Blood 2009;114:5415-25.
26. Wojiski S, Guibal FC, Kindler T, Lee BH, Jesneck JL, Fabian A, et al. PML-RARalpha initiates leukemia by conferring properties of self-renewal to committed promyelocytic progenitors. Leukemia 2009;23:1462-71.
27. Sapra P, Kraft P, Mehlig M, Malaby J, Zhao H, Greenberger LM, et al. Marked therapeutic efficacy of a novel polyethylene glycol-SN38 conjugate, EZN-2208, in xenograft models of B-cell non-Hodgkin's lymphoma. Haema-tologica 2009;94:1456-9.
28. Ablain J, Rice K, Soilihi H, de Reynies A, Minucci S, de The H. Activation of a promyelocytic leukemia-tumor protein 53 axis underlies acute promyelo-cytic leukemia cure. Nat Med 2014;20:167-74.
29. Park JH, Tallman MS. Treatment of acute promyelocytic leukemia without cytotoxic chemotherapy. Oncology 2011;25:733-41.