PML-RARA-RXR Oligomers Mediate Retinoid and Rexinoid/cAMP Cross-Talk in Acute Promyelocytic Leukemia Cell Differentiation

Journal of Experimental Medicine

Volumn 199, Issue 8, 2004, Pages 1163-1174

  Kamashev, Dmitrii ^a   Vitoux, Dominique ^a   De Thé, Hugues ^a  

^a SAINT LOUIS HOSPITAL   (France)

Author keywords

Leukemia; Oncogene; Selex; Therapy; Transcription

Indexed keywords

CYCLIC AMP; OLIGOMER; PROMYELOCYTIC LEUKEMIA PROTEIN; RETINOIC ACID RECEPTOR ALPHA; RETINOID; RETINOID X RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN COS7; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA BINDING; DNA RESPONSIVE ELEMENT; GEL MOBILITY SHIFT ASSAY; GENE TARGETING; NONHUMAN; ONCOGENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN PROTEIN INTERACTION; REPORTER GENE; TRANSACTIVATION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELL LINE; COS CELLS; CYCLIC AMP; DNA, NEOPLASM; HUMANS; LEUKEMIA, PROMYELOCYTIC, ACUTE; NEOPLASM PROTEINS; NUCLEAR PROTEINS; RECEPTOR CROSS-TALK; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; RETINOIDS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; U937 CELLS;

EID: 2442478144     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20032226     Document Type: Article

References (48)

1. Castelein, H., A. Janssen, P.E. Declercq, and M. Baes. 1996. Sequence requirements for high affinity retinoid X receptor-alpha homodimer binding. Mol. Cell. Endocrinol. 119:11-20.
2. Forman, B.M., K. Umesono, J. Chen, and R.M. Evans. 1995. Unique response pathways are established by allosteric interactions among nuclear hormone receptors. Cell. 81:541-550.
3. Germain, P., J. Iyer, C. Zechel, and H. Gronemeyer. 2002. Co-regulator recruitment and the mechanism of retinoic acid receptor synergy. Nature. 415:187-192.
4. Minucci, S., C. Nervi, F. Lo Coco, and P.G. Pelicci. 2001. Histone deacetylases: a common molecular target for differentiation treatment of acute myeloid leukemias? Oncogene. 20:3110-3115.
5. Jansen, J.H., A. Mahfoudi, S. Rambaud, C. Lavau, W. Wahli, and A. Dejean. 1995. Multimeric complexes of the PML-retinoic acid receptor alpha fusion protein in acute promyelocytic leukemia cells and interference with retinoid and peroxisome-proliferator signaling pathways. Proc. Natl. Acad. Sci. USA. 92:7401-7405.
6. Perez, A., P. Kastner, S. Sethi, Y. Lutz, C. Reibel, and P. Chambon. 1993. PML/RAR homodimers: distinct binding properties and heteromeric interactions with RXR. EMBO J. 12:3171-3182.
7. He, L.-Z., F. Guidez, C. Tribioli, D. Peruzzi, M. Ruthardt, A. Zelent, and P.P. Pandolfi. 1998. Distinct interactions of PML-RARalpha and PLZF-RAR-alpha with co-repressors determine differential responses to RA in APL. Nat. Genet. 18:126-135.
8. Grignani, F., S. de Matteis, C. Nervi, L. Tomassoni, V. Gelmetti, M. Cioce, M. Fanelli, M. Ruthardt, F.F. Ferrara, I. Zamir, et al. 1998. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature. 391:815-818.
9. Lin, R.J., L. Nagy, S. Inoue, W.L. Shao, W.H. Miller, and R.M. Evans. 1998. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature. 391:811-814.
10. Lin, R., and R. Evans. 2000. Acquisition of oncogenic potential by RAR chimeras in acute promyelocytic leukemia through formation of homodimers. Mol. Cell. 5:821-830.
11. Minucci, S., M. Maccarana, M. Cioce, P. De Luca, V. Gelmetti, S. Segalla, L. Di Croce, S. Giavara, C. Matteucci, A. Gobbi, et al. 2000. Oligomerization of RAR and AML1 transcription factors as a novel mechanism of oncogenic activation. Mol. Cell. 5:811-820.
12. Degos, L., and Z.Y. Wang. 2001. All trans retinoic acid in acute promyelocytic leukemia. Oncogene. 20:7140-7145.
13. Zhu, J., Z. Chen, V. Lallemand-Breitenbach, and H. de Thé. 2002. How acute promyelocytic leukemia revived arsenic. Nat. Rev. Cancer. 2:705-713.
14. Zhu, J., M.H.M. Koken, F. Quignon, M.K. Chelbi-Alix, L. Degos, Z.Y. Wang, Z. Chen, and H. de Thé. 1997. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc. Natl. Acad. Sci. USA. 94:3978-3983.
15. Zhu, J., M. Gianni, E. Kopf, N. Honore, M. Chelbi-Alix, M. Koken, F. Quignon, C. Rochette-Egly, and H. de Thé. 1999. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RAR alpha) and oncogenic RAR alpha fusion proteins. Proc. Natl. Acad. Sci. USA. 96:14807-14812.
16. Benoit, G., M. Roussel, F. Pendino, E. Segal-Bendirdjian, and M. Lanotte. 2001. Orchestration of multiple arrays of signal cross-talk and combinatorial interactions for maturation and cell death: another vision of t(15;17) preleukemic blast and APL-cell maturation. Oncogene. 20:7161-7177.
17. Guillemin, M.C., E. Raffoux, D. Vitoux, S. Kogan, H. Soilihi, V. Lallemand-Breitenbach, J. Zhu, A. Janin, M.T. Daniel, B. Gourmel, et al. 2002. In vivo activation of cAMP signaling induces growth arrest and differentiation in acute promyelocytic leukemia. J. Exp. Med. 196:1373-1380.
18. Taneja, R., C. Rochette-Egly, J.-L. Plassat, L. Penna, M.-P. Gaub, and P. Chambon. 1997. Phosphorylation of activation functions AF-1 and AF-2 of RAR alpha and RAR gamma is indispensable for differentiation of F9 cells upon retinoic acid and cAMP treatment. EMBO J. 16:6452-6465.
19. Benoit, G., L. Altucci, M. Flexor, S. Ruchaud, J. Lillehaug, W. Raffelsberger, H. Gronemeyer, and M. Lanotte. 1999. RAR-independent RXR signaling induces t(15;17) leukemia cell maturation. EMBO J. 18:7011-7018.
20. Benoit, G.R., M. Flexor, F. Besancon, L. Altucci, A. Rossin, J. Hillion, Z. Balajthy, L. Legres, E. Segal-Bendirdjian, H. Gronemeyer, et al. 2001. Autonomous rexinoid death signaling is suppressed by converging signaling pathways in immature leukemia cells. Mol. Endocrinol. 15:1154-1169.
21. Altucci, L., and H. Gronemeyer. 2001. The promise of retinoids to fight against cancer. Nat. Rev. Cancer. 1:181-193.
22. Subauste, J.S., and R.J. Koenig. 1998. Characterization of the DNA-binding and dominant negative activity of V-erbA homodimers. Mol. Endocrinol. 12:1380-1392.
23. de Thé, H., M.d.M. Vivanco-Ruiz, P. Tiollais, H. Stunnenberg, and A. Dejean. 1990. Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature. 343:177-180.
24. Roussel, M.J., and M. Lanotte. 2001. Maturation sensitive and resistant t(15;17) NB4 cell lines as tools for APL physiopathology: nomenclature of cells and repertory of their known genetic alterations and phenotypes. Oncogene. 20: 7287-7291.
25. Gianni, M., M.H.M. Koken, M.K. Chelbi-Alix, G. Benoit, M. Lanotte, Z. Chen, and H. de Thé. 1998. Combined arsenic and retinoic acid treatment enhances differentiation and apoptosis in arsenic-resistant NB4 cells. Blood. 91:4300-4310.
26. Hauksdottir, H., and M.L. Privalsky. 2001. DNA recognition by the aberrant retinoic acid receptors implicated in human acute promyelocytic leukemia. Cell Growth Differ. 12:85-98.
27. Jamieson, A.C., J.C. Miller, and C.O. Pabo. 2003. Drug discovery with engineered zinc-finger proteins. Nat. Rev. Drug Discov. 2:361-368.
28. Kamashev, D.E., A.V. Balandina, and V.L. Karpov. 2000. Tramtrack protein-DNA interactions. A cross-linking study. J. Biol. Chem. 275:36056-36061.
29. Lallemand-Breitenbach, V., J. Zhu, F. Puvion, M. Koken, N. Honore, A. Doubeikovsky, E. Duprez, P.P. Pandolfi, E. Puvion, P. Freemont, et al. 2001. Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As(2)O(3)-induced PML or PML/retinoic acid receptor α degradation. J. Exp. Med. 193: 1361-1372.
30. Quenech'Du, N., S. Ruchaud, N. Khelef, N. Guiso, and M. Lanotte. 1998. A sustained increase in the endogenous level of cAMP reduces the retinoid concentration required for APL cell maturation to near physiological levels. Leukemia 12: 1829-1833.
31. Zhu, Q., J.W. Zhang, H.Q. Zhu, Y.L. Shen, M. Flexor, P.M. Jia, Y. Yu, X. Cai, S. Waxman, M. Lanotte, et al. 2002. Synergic effects of arsenic trioxide and cAMP during acute promyelocytic leukemia cell maturation subtends a novel signaling cross-talk. Blood. 99:1014-1022.
32. Ruchaud, S., E. Duprez, M.C. Gendron, G. Houge, H.G. Genieser, B. Jastorff, S.O. Doskeland, and M. Lanotte. 1994. Two distinctly regulated events, priming and triggering, during retinoid-induced maturation and resistance of NB4 promyelocytic leukemia cell line. Proc. Natl. Acad. Sci. USA. 91: 8428-8432.
33. Duprez, E., G. Benoit, M. Flexor, J.R. Lillehaug, and M. Lanotte. 2000. A mutated PML/RARA found in the retinoid maturation resistant NB4 subclone, NB4-R2, blocks RARA and wild-type PML/RARA transcriptional activities. Leukemia. 14:255-261.
34. Shao, W., L. Benedetti, W.W. Lamph, C. Nervi, and W.H.J. Miller. 1997. A retinoid-resistant acute promyelocytic leukemia subclone expresses a dominant negative PML-RAR alpha mutation. Blood. 89:4282-4289.
35. Kogan, S.C., S.H. Hong, D.B. Shultz, M.L. Privalsky, and J.M. Bishop. 2000. Leukemia initiated by PMLRARalpha: the PML domain plays a critical role while retinoic acid-mediated transactivation is dispensable. Blood. 95:1541-1550.
36. Kurokawa, R., M. Söderström, A. Hörlein, S. Halachmi, M. Brown, M.G. Rosenfeld, and C.K. Glass. 1995. Polarity-specific activities of retinoic acid receptors determined by a corepressor. Nature. 377:451-454.
37. Gianni, M., A. Bauer, E. Garratini, P. Chambon, and C. Rochette-Egly. 2002. Phosphorylation by p38MAPK and recruitment of SUG-1 are required for RA-induced RAR gamma degradation and transactivation. EMBOJ. 15:3760-3769.
38. Grignani, F., P. Ferrucci, U. Testa, G. Talamo, M. Fagioli, M. Alcalay, A. Mencarelli, F. Grignani, C. Peschle, I. Nicoletti, et al. 1993. The acute promyelocytic leukemia specific PML/RARα fusion protein inhibits differentiation and promotes survival of myeloid precursor cells. Cell. 74:423-431.
39. Kastner, P., A. Perez, Y. Lutz, C. Rochette-Egly, M.-P. Gaub, B. Durand, M. Lanotte, R. Berger, and P. Chambon. 1992. Structure, localization and transcriptional properties of two classes of retinoic acid receptor alpha fusion proteins in acute promyelocytic leukemia (APL): structural similarities with a new family of oncoproteins. EMBO J. 11:629-642.
40. Pandolfi, P.P., F. Grignani, M. Alcalay, A. Mencarelli, A. Biondi, F. LoCoco, F. Grignani, and P.G. Pelicci. 1991. Structure and origin of the acute promyelocytic leukemia myl/RARα cDNA and characterization of its retinol-binding and transactivation properties. Oncogene. 6:1285-1292.
41. de Thé, H., C. Lavau, A. Marchio, C. Chomienne, L. Degos, and A. Dejean. 1991. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell. 66:675-684.
42. Segalla, S., L. Rinaldi, C. Kilstrup-Nielsen, G. Badaracco, S. Minucci, P.G. Pelicci, and N. Landsberger. 2003. Retinoic acid receptor alpha fusion to PML affects its transcriptional and chromatin-remodeling properties. Mol. Cell. Biol. 23: 8795-8808.
43. Chen, J.-Y., J. Clifford, C. Zusi, J. Starrett, D. Tortolani, J. Ostrowski, P.R. Reczek, P. Chambon, and H. Gronemeyer. 1996. Two distinct actions of retinoid-receptor ligands. Nature. 382:819-822.
44. Herzig, S., F. Long, U.S. Jhala, S. Hedrick, R. Quinn, A. Bauer, D. Rudolph, G. Schutz, C. Yoon, P. Puigserver, et al. 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature. 413:179-183.
45. Yoon, J.C., P. Puigserver, G. Chen, J. Donovan, Z. Wu, J. Rhee, G. Adelmant, J. Stafford, C.R. Kahn, D.K. Granner, et al. 2001. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature. 413:131-138.
46. Sohn, Y.C., S.W. Kim, S. Lee, Y.Y. Kong, D.S. Na, S.K. Lee, and J.W. Lee. 2003. Dynamic inhibition of nuclear receptor activation by corepressor binding. Mol. Endocrinol. 17: 366-372.
47. Lallemand-Breitenbach, V., M.-C. Guillemin, A. Janin, M.-T. Daniel, L. Degos, S.C. Kogan, J.M. Bishop, and H. de Thé. 1999. Retinoic acid and arsenic synergize to eradicate leukemic cells in a mouse model of acute promyelocytic leukemia. J. Exp. Med. 189:1043-1052.
48. Rego, E.M., L.Z. He, R.P. Warrell, Jr., Z.G. Wang, and P.P. Pandolfi. 2000. Retinoic acid (RA) and As2O3 treatment in transgenic models of acute promyelocytic leukemia (APL) unravel the distinct nature of the leukemogenic process induced by the PML-RARalpha and PLZF-RARalpha oncoproteins. Proc. Natl. Acad. Sci. USA. 97:10173-10178.