Rexinoid-triggered differentiation and tumor-selective apoptosis of acute myeloid leukemia by protein kinase A-mediated desubordination of retinoid X receptor

Cancer Research

Volumn 65, Issue 19, 2005, Pages 8754-8765

  Altucci, Lucia ^a,c,d   Rossin, Aurélie ^a   Hirsch, Oliver ^a   Nebbioso, Angela ^c   Vitoux, Dominique ^b   Wilhelm, Emmanuelle ^a   Guidez, Fabien ^f,g   De Simone, Mariacarla ^e   Schiavone, Ettore Mariano ^e   Grimwade, David ^g   Zelent, Arthur ^f   De Thé, Hugues ^b   Gronemeyer, Hinrich ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b SAINT LOUIS HOSPITAL   (France)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^e CARDARELLI HOSPITAL   (Italy)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^g KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DEATH RECEPTOR 5; LIGAND; PHOSPHODIESTERASE INHIBITOR; RECEPTOR SUBUNIT; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RECEPTOR BETA; RETINOID; RETINOID X RECEPTOR; RETINOID X RECEPTOR AGONIST; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; APOPTOSIS; ARTICLE; BLAST CELL; CELL DIFFERENTIATION; CELL MATURATION; CLONOGENESIS; CLONOGENIC ASSAY; CONTROLLED STUDY; DRUG RECEPTOR BINDING; ENZYME ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GRANULOCYTE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; KARYOTYPE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA;

ACUTE DISEASE; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL DIFFERENTIATION; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DRUG SYNERGISM; HL-60 CELLS; HUMANS; LEUKEMIA, MYELOID; LEUKEMIA, PROMYELOCYTIC, ACUTE; MICE; PHOSPHODIESTERASE INHIBITORS; RECEPTOR CROSS-TALK; RECEPTORS, RETINOIC ACID; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECEPTORS, TUMOR NECROSIS FACTOR; RETINOID X RECEPTORS; U937 CELLS;

EID: 25444495618     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-3569     Document Type: Article

References (55)

1. Lowenberg B, Downing JR, Burnett A. Acute myeloid leukemia. N Engl J Med 1999;341:1051-62.
2. Bennett JM, Catovsky D, Daniel MT, et al. Proposed revised criteria for the classification of acute myeloid leukemia. A report of the French-American-British Cooperative Group. Ann Intern Med 1985;103:620-5.
3. Tenen DG. Disruption of differentiation in human cancer: AML shows the way. Nat Rev Cancer 2003;3:89-101.
4. Wang Z, Sun G, Shen Z, Chen S, Chen Z. Differentiation therapy for acute promyelocytic leukemia with all-trans retinoic acid: 10-year experience of its clinical application. Chin Med J (Engl) 1999;112:963-7.
5. Fenaux P, Chomienne C, Degos L. Treatment of acute promyelocytic leukaemia. Best Pract Res Clin Haematol 2001;14:153-74.
6. Altucci L, Gronemeyer H. The promise of retinoids to fight against cancer. Nat Rev Cancer 2001;1:181-93.
7. Piazza F, Gurrieri C, Pandolfi PP. The theory of APL. Oncogene 2001;20:7216-22.
8. Degos L, Wang ZY. All trans retinoic acid in acute promyelocytic leukemia. Oncogene 2001;20:7140-5.
9. Minucci S, Nervi C, Lo Coco F, Pelicci PG. Histone deacetylases: a common molecular target for differentiation treatment of acute myeloid leukemias? Oncogene 2001;20:3110-5.
10. de The H, Chelbi-Alix MK. APL, a model disease for cancer therapies? Oncogene 2001;20:7136-9.
11. Lin RJ, Sternsdorf T, Tini M, Evans RM. Transcriptional regulation in acute promyelocytic leukemia. Oncogene 2001;20:7204-15.
12. Lin HK, Bergmann S, Pandolfi PP. Cytoplasmic PML function in TGF-β signalling. Nature 2004;431:205-11.
13. Alcalay M, Meani N, Gelmetti V, et al. Acute myeloid leukemia fusion proteins deregulate genes involved in stem cell maintenance and DNA repair. J Clin Invest 2003;112:1751-61.
14. Minucci S, Cioce M, Maccarana M, Pelicci PG. The APL-associated fusion proteins. Haematologica 1999;84:70-1.
15. de Stanchina E, Querido E, Narita M, et al. PML is a direct p53 target that modulates p53 effector functions. Mol Cell 2004;13:523-35.
16. Bernardi R, Scaglioni PP, Bergmann S, Horn HF, Vousden KH, Pandolfi PP. PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat Cell Biol 2004;6:665-72.
17. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003;22:8628-33.
18. Altucci L, Rossin A, Raffelsberger W, Reitmair A, Chomienne C, Gronemeyer H. Retinoic acid-induced apoptosis in leukemia cells is mediated by paracrine action of tumor-selective death ligand TRAIL. Nat Med 2001;7:680-6.
19. Clarke N, Jimenez-Lara AM, Voltz E, Gronemeyer H. Tumor suppressor IRF-1 mediates retinoid and interferon anticancer signaling to death ligand TRAIL. EMBO J 2004;23:3051-60.
20. Grimwade D, Biondi A, Mozziconacci MJ, et al. Characterization of acute promyelocytic leukemia cases lacking the classic t(15;17): results of the European Working Party. Blood 2000;96:1297-308.
21. Zhou DC, Kim SH, Ding W, Schultz C, Warrell RP, Jr., Gallagher RE. Frequent mutations in the ligand-binding domain of PML-RAR α 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.
22. Landet V, Gronemeyer H. The nuclear receptor facts book, San Diego: Academic Press; 2002.
23. Gronemeyer H, Gustafsson JA, Laudet V. Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Design 2004;3:950-64.
24. Chen JY, Clifford J, Zusi C, et al. Two distinct actions of retinoid-receptor ligands. Nature 1996;382:819-22.
25. Germain P, Iyer J, Zechel C, Gronemeyer H. Coregulator recruitment and the mechanism of retinoic acid receptor synergy. Nature 2002;415:187-92.
26. Zusi FC, Lorenzi MV, Vivat-Hannah V. Selective retinoids and rexinoids in cancer therapy and chemoprevention. Drug Discov Today 2002;7:1165-74.
27. Sun SY, Lotan R. Retinoids and their receptors in cancer development and chemoprevention. Crit Rev Oncol Hematol 2002;41:41-55.
28. Altucci L, Wilhelm E, Gronemeyer H. Leukemia: beneficial actions of retinoids and rexinoids. Int J Biochem Cell Biol 2004;36:178-82.
29. Gottardis MM, Bischoff ED, Shirley MA, Wagoner MA, Lamph WW, Heyman RA. Chemoprevention of mammary carcinoma by LGD1069 (Targretin): an RXR-selective ligand. Cancer Res 1996;56:5566-70.
30. Sporn MB. Suh N. Opinion: chemoprevention: an essential approach to controlling cancer. Nat Rev Cancer 2002;2:537-43.
31. Benoit G, Altucci L, Flexor M, et al. RAR-independent RXR signaling induces t(15;17) leukemia cell maturation. EMBO J 1999;18:7011-8.
32. Pogenberg V, Guichou JF, Vivat-Hannah V, et al. Characterization of the interaction between retinoic acid receptor/retinoid X receptor (RAR/RXR) heterodimers and transcriptional coactivators through structural and fluorescence anisotropy studies. J Biol Chem 2005;280:1625-33.
33. Lanotte M, Martin-Thouvenin V, Najman S, Balerini P, Valensi F, Berger R. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood 1991;77:1080-6.
34. Chomienne C, Ballerini P, Balitrand N, et al. All-trans retinoic acid in acute promyelocytic leukemias. II. In vitro studies: structure-function relationship. Blood 1990;76:1710-7.
35. Chapellier B, Mark M, Garnier JM, Dierich A, Chambon P, Ghyselinck NB. A conditional floxed (loxP-flanked) allele for the retinoic acid receptor γ (RARγ) gene. Genesis 2002;32:95-8.
36. Chapellier B, Mark M, Bastien J, et al. A conditional floxed (loxP-flanked) allele for the retinoic acid receptor β (RARβ) gene. Genesis 2002;32:91-4.
37. Chapellier B, Mark M, Garnier JM, LeMeur M, Chambon P, Ghyselinck NB. A conditional floxed (loxP-flanked) allele for the retinoic acid receptor α (RARα) gene. Genesis 2002;32:87-90.
38. Benoit GR, Flexor M, Besancon F, et al. Autonomous rexinoid death signaling is suppressed by converging signaling pathways in immature leukemia cells. Mol Endocrinol 2001;15:1154-69.
39. Sainty D, Liso V, Cantu-Rajnoldi A, et al. A new morphologic classification system for acute promyelocytic leukemia distinguishes cases with underlying PLZF/RARA gene rearrangements. Blood 2000;96:1287-96.
40. Sprick MR, Rieser E, Stahl H, Grosse-Wilde A, Weigand MA, Walczak H. Caspase-10 is recruited to and activated at the native TRAIL and CD95 death-inducing signalling complexes in a FADD-dependent manner but can not functionally substitute caspase-8. EMBO J 2002;21:4520-30.
41. Bodmer JL, Holler N, Reynard S, et al. TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat Cell Biol 2000;2:241-3.
42. Zhao Q, Tao J, Zhu Q, et al. Rapid induction of cAMP/PKA pathway during retinoic acid-induced acute promyelocytic leukemia cell differentiation. Leukemia 2004;18:285-92.
43. Kamashev D, Vitoux D, De The H. PML-RARA-RXR oligomers mediate retinoid and rexinoid/cAMP crosstalk in acute promyelocytic leukemia cell differentiation, J Exp Med 2004;199:1163-74.
44. Waxman S. Differentiation therapy in acute myelogenous leukemia (non-APL). Leukemia 2000;14:491-6.
45. Parrella E, Gianni M, Cecconi V, et al. Phosphodiesterase IV inhibition by piclamilast potentiates the cytodifferentiating action of retinoids in myeloid leukemia cells. Cross-talk between the cAMP and the retinoic acid signaling pathways. J Biol Chem 2004;279:42026-40.
46. Guillemin MC, Raffoux E, Vitoux D, et al. In vivo Activation of cAMP signaling induces growth arrest and differentiation in acute promyelocytic leukemia. J Exp Med 2002;196:1373-80.
47. Rochette-Egly C, Oulad-Abdelghani M, Staub A, et al. Phosphorylation of the retinoic acid receptor-α by protein kinase A. Mol Endocrinol 1995;9:860-71.
48. Sheridan JP, Marsters SA, Pitti RM, et al. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997;277:818-21.
49. Ichikawa K, Liu W, Zhao L, et al. Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat Med 2001;7:954-60.
50. Manganiello VC, Murata T, Taira M, Belfrage P, Degerman E. Diversity in cyclic nucleotide phosphodiesterase isoenzyme families. Arch Biochem Biophys 1995;322:1-13.
51. Kim DH, Lerner A. Type 4 cyclic adenosine monophosphate phosphodiesterase as a therapeutic target in chronic lymphocytic leukemia. Blood 1998;92:2484-94.
52. Ogawa R, Streiff MB, Bugayenko A, Kato GJ. Inhibition of PDE4 phosphodiesterase activity induces growth suppression, apoptosis, glucocorticoid sensitivity, p53, and p21(WAF1/CIP1) proteins in human acute lymphoblastic leukemia cells. Blood 2002;99:3390-7.
53. Boehm MF, Zhang L, Zhi L, et al. Design and synthesis of potent retinoid X receptor selective ligands that induce apoptosis in leukemia cells. J Med Chem 1995;38:3146-55.
54. Nebbioso A, Clarke N, Voltz E, et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat Med 2005;11:77-84.
55. Insinga A, Monestiroli S, Ronzoni S, et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med 2005;11:71-6.