Eradication of acute promyelocytic leukemia-initiating cells by PML/RARA-targeting

International Journal of Hematology

Volumn 91, Issue 5, 2010, Pages 742-747

  Nasr, Rihab ^a   De Thé, Hugues ^b  

^a AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

Arsenic; Cure; Proteolysis; Retinoic acid; SUMO

Indexed keywords

ARSENIC TRIOXIDE; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEASOME; RETINOIC ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RARA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ONCOPROTEIN; ORGANOARSENIC DERIVATIVE; OXIDE; PROMYELOCYTIC LEUKEMIA-RETINOIC ACID RECEPTOR ALPHA FUSION ONCOPROTEIN;

CANCER STEM CELL; CELL DIFFERENTIATION; CELL GROWTH; HUMAN; LEUKEMIA CELL; LEUKEMIA INITIATING CELL; LEUKEMIA REMISSION; NONHUMAN; ONCOGENE; PATHOGENESIS; PROMYELOCYTE; PROMYELOCYTIC LEUKEMIA; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; REVIEW; ANIMAL; CELL TRANSFORMATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GRANULOCYTE PRECURSOR; LEUKEMIA, PROMYELOCYTIC, ACUTE; METABOLISM; MOUSE; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; ARSENICALS; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GRANULOCYTE PRECURSOR CELLS; HUMANS; LEUKEMIA, PROMYELOCYTIC, ACUTE; MICE; ONCOGENE PROTEINS, FUSION; ONCOGENES; OXIDES; TRETINOIN;

EID: 77954542260     PISSN: 09255710     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12185-010-0582-0     Document Type: Review

References (69)

1. A Melnick JD Licht 1999 Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia Blood 93 3167 3215 10233871 1:CAS:528:DyaK1MXjtVKqurg%3D
2. V Lallemand-Breitenbach J Zhu S Kogan Z Chen H de Thé 2005 Opinion: how patients have benefited from mouse models of acute promyelocytic leukaemia Nat Rev Cancer 5 821 827 10.1038/nrc1719 16175176 1:CAS:528: DC%2BD2MXhtVGjs7fO (Pubitemid 41400780)
3. R Bernardi S Grisendi PP Pandolfi 2002 Modelling haematopoietic malignancies in the mouse and therapeutical implications Oncogene 21 3445 3458 10.1038/sj.onc.1205313 12032781 1:CAS:528:DC%2BD38XksVWrsbc%3D (Pubitemid 34587715)
4. Z Chen N Brand A Chen S Chen J Tong, et al. 1993 Fusion between a novel Kruppel-like zinc finger gene and the retinoic acid receptor a locus due to a variant t(11, 17) translocation in acute promyelocytic leukemia EMBO J 12 1161 1167 8384553 1:CAS:528:DyaK3sXisFagtLc%3D
5. JD Licht 2006 Reconstructing a disease: what essential features of the retinoic acid receptor fusion oncoproteins generate acute promyelocytic leukemia? Cancer Cell 9 73 74 10.1016/j.ccr.2006.01.024 16473273 1:CAS:528:DC%2BD28XhvFynsr4%3D (Pubitemid 43202656)
6. S Minucci M Maccarana M Cioce P De Luca V Gelmetti, et al. 2000 Oligomerization of RAR and AML1 transcription factors as a novel mechanism of oncogenic activation Mol Cell 5 811 820 10.1016/S1097-2765(00)80321-4 10882117 1:CAS:528:DC%2BD3cXjsl2ku74%3D
7. R Lin R Evans 2000 Acquisition of oncogenic potential by RAR chimeras in acute promyelocytic leukemia through formation of homodimers Mol Cell 5 821 830 10.1016/S1097-2765(00)80322-6 10882118 1:CAS:528:DC%2BD3cXjsl2ku78%3D
8. Martens JH, Brinkman AB, Simmer F, Francoijs KJ, Nebbioso A, et al. PML-RARalpha/RXR alters the epigenetic landscape in acute promyelocytic leukemia. Cancer Cell. 2010;17:173-85.
9. J Zhu R Nasr L Peres F Riaucoux-Lormiere N Honore, et al. 2007 RXR is an essential component of the oncogenic PML/RARA complex in vivo Cancer Cell 12 23 35 10.1016/j.ccr.2007.06.004 17613434 1:CAS:528:DC%2BD2sXotVyqsro%3D (Pubitemid 47001786)
10. J Zhu J Zhou L Peres F Riaucoux N Honore, et al. 2005 A sumoylation site in PML/RARA is essential for leukemic transformation Cancer Cell 7 143 153 10.1016/j.ccr.2005.01.005 15710327 1:CAS:528:DC%2BD2MXitFygu7s%3D (Pubitemid 40248340)
11. DE Kamashev D Vitoux H de Thé 2004 PML/RARA-RXR oligomers mediate retinoid- and rexinoid-/cAMP in APL cell differentiation J Exp Med 199 1 13 10.1084/jem.20032226 1:CAS:528:DC%2BD2cXjtlOjtbw%3D (Pubitemid 38619912)
12. R Villa D Pasini A Gutierrez L Morey M Occhionorelli, et al. 2007 Role of the polycomb repressive complex 2 in acute promyelocytic leukemia Cancer Cell 11 513 525 10.1016/j.ccr.2007.04.009 17560333 1:CAS:528:DC%2BD2sXmvVaksrs%3D (Pubitemid 46863505)
13. BB Zeisig C Kwok A Zelent P Shankaranarayanan H Gronemeyer, et al. 2007 Recruitment of RXR by homotetrameric RARalpha fusion proteins is essential for transformation Cancer Cell 12 36 51 10.1016/j.ccr.2007.06.006 17613435 1:CAS:528:DC%2BD2sXotVyqsrs%3D (Pubitemid 47018239)
14. H Boukarabila AJ Saurin E Batsche N Mossadegh M van Lohuizen, et al. 2009 The PRC1 Polycomb group complex interacts with PLZF/RARA to mediate leukemic transformation Genes Dev 23 1195 1206 10.1101/gad.512009 19451220 1:CAS:528:DC%2BD1MXmslamtbY%3D
15. Lallemand-Breitenbach V, de Thé H. (2010) PML nuclear bodies. CSH Perspect Biol. 2010, in press.
16. K Ito R Bernardi A Morotti S Matsuoka G Saglio, et al. 2008 PML targeting eradicates quiescent leukaemia-initiating cells Nature 453 1072 1078 10.1038/nature07016 18469801 1:CAS:528:DC%2BD1cXntlGjtb0%3D (Pubitemid 351871736)
17. Bernardi R, Pandolfi PP. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol. 2007;8:1006-16.
18. MHM Koken F Puvion-Dutilleul MC Guillemin A Viron G Linares-Cruz, et al. 1994 The t(15;17) translocation alters a nuclear body in a RA-reversible fashion EMBO J 13 1073 1083 8131741 1:CAS:528:DyaK2cXksFamsb4%3D
19. JA Dyck GG Maul WH Miller JD Chen A Kakizuka, et al. 1994 A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein Cell 76 333 343 10.1016/0092-8674(94)90340-9 8293467 1:CAS:528:DyaK2cXhs1Sgs7g%3D
20. ZY Wang Z Chen 2008 Acute promyelocytic leukemia: from highly fatal to highly curable Blood 111 2505 2515 10.1182/blood-2007-07-102798 18299451 1:CAS:528:DC%2BD1cXivFaktrg%3D
21. F Quignon Z Chen H de Thé 1997 Retinoic acid and arsenic: towards oncogene targeted treatments of acute promyelocytic leukaemia Biochim Biophys Acta 1333 M53 M61 9426202 1:CAS:528:DyaK2sXnsFyrsrY%3D
22. M Huang Y Ye R Chen J Chai J Lu, et al. 1988 Use of all trans retinoic acid in the treatment of acute promyelocytic leukaemia Blood 72 567 572 3165295 1:STN:280:DyaL1c3psVeisg%3D%3D
23. R Warrell H de Thé Z Wang L Degos 1993 Acute promyelocytic leukemia New Engl J Med 329 177 189 10.1056/NEJM199307153290307 8515790 1:CAS:528:DyaK3sXmt1arsL8%3D (Pubitemid 23195739)
24. L Degos ZY Wang 2001 All trans retinoic acid in acute promyelocytic leukemia Oncogene 20 7140 7145 10.1038/sj.onc.1204763 11704842 1:CAS:528:DC%2BD3MXos1Onurs%3D (Pubitemid 33107374)
25. D Douer E Estey S Santillana JM Bennett G Lopez-Bernstein, et al. 2001 Treatment of newly diagnosed and relapsed acute promyelocytic leukemia with intravenous liposomal all-trans retinoic acid Blood 97 73 80 10.1182/blood.V97.1.73 11133744 1:CAS:528:DC%2BD3MXis1eqtA%3D%3D (Pubitemid 32061244)
26. AM Tsimberidou M Tirado-Gomez M Andreeff S O'Brien H Kantarjian, et al. 2006 Single-agent liposomal all-trans retinoic acid can cure some patients with untreated acute promyelocytic leukemia: an update of The University of Texas M. D. Anderson Cancer Center Series Leuk Lymphoma 47 1062 1068 10.1080/ 10428190500463932 16840198 1:CAS:528:DC%2BD28XpvVGqsr8%3D (Pubitemid 44102970)
27. L Degos H Dombret C Chomienne MT Daniel JM Miclea, et al. 1995 All-trans retinoic acid as a differentiating agent in the treatment of acute promyelocytic leukemia Blood 85 2643 2653 7742522 1:CAS:528:DyaK2MXls1Srur0%3D
28. J Zhu V Lallemand-Breitenbach H de Thé 2001 Pathways of retinoic acid- or arsenic trioxide-induced PML/RARalpha catabolism, role of oncogene degradation in disease remission Oncogene 20 7257 7265 10.1038/sj.onc.1204852 11704854 1:CAS:528:DC%2BD3MXos1Onu7k%3D (Pubitemid 33107375)
29. C Nervi FF Ferrara M Fanelli MR Rippo B Tomassini, et al. 1998 Caspases mediate retinoic acid-induced degradation of the acute promyelocytic leukemia PML/RARalpha fusion protein Blood 92 2244 2251 9746761 1:CAS:528: DyaK1cXmsVKgu70%3D
30. J Zhu M Gianni E Kopf N Honore M Chelbi-Alix, et al. 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 10.1073/pnas.96.26.14807 10611294 1:CAS:528:DC%2BD3cXhtFagtg%3D%3D (Pubitemid 30019721)
31. 4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins Blood 88 1052 1061 8704214 1:CAS:528:DyaK28Xks1Cjur0%3D
32. V Mathews B George KM Lakshmi A Viswabandya A Bajel, et al. 2006 Single-agent arsenic trioxide in the treatment of newly diagnosed acute promyelocytic leukemia: durable remissions with minimal toxicity Blood 107 2627 2632 10.1182/blood-2005-08-3532 16352810 1:CAS:528:DC%2BD28XjtlKltbs%3D
33. A Ghavamzadeh K Alimoghaddam SH Ghaffari S Rostami M Jahani, et al. 2006 Treatment of acute promyelocytic leukemia with arsenic trioxide without ATRA and/or chemotherapy Ann Oncol 17 131 134 10.1093/annonc/mdj019 16227315 1:STN:280:DC%2BD2MnntFKiug%3D%3D (Pubitemid 43033852)
34. 3 exerts dose-dependent dual effects on APL cells Blood 89 3345 3353 9129041 1:CAS:528:DyaK2sXivVymtbg%3D
35. V Lallemand-Breitenbach M-C Guillemin A Janin M-T Daniel L Degos, et al. 1999 Retinoic acid and arsenic synergize to eradicate leukemic cells in a mouse model of acute promyelocytic leukemia J Exp Med 189 1043 1052 10.1084/jem.189.7.1043 10190895 1:CAS:528:DyaK1MXitlemtr8%3D (Pubitemid 29169821)
36. J Zhu MHM Koken F Quignon MK Chelbi-Alix L Degos, et al. 1997 Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia Proc Natl Acad Sci USA 94 3978 3983 10.1073/pnas.94.8.3978 9108090 1:CAS:528:DyaK2sXis1eht7g%3D (Pubitemid 27180484)
37. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, et al. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol. 2008;10:538-46.
38. V Lallemand-Breitenbach M Jeanne S Benhenda R Nasr M Lei, et al. 2008 Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway Nat Cell Biol 10 547 555 10.1038/ncb1717 18408733 1:CAS:528:DC%2BD1cXltl2is7o%3D (Pubitemid 351627374)
39. V Lallemand-Breitenbach J Zhu F Puvion M Koken N Honore, 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 alpha degradation J Exp Med 193 1361 1372 10.1084/jem.193.12.1361 11413191 1:CAS:528:DC%2BD3MXksFCntbc%3D (Pubitemid 32565965)
40. 3 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 10.1073/pnas.180290497 10954752 1:CAS:528: DC%2BD3cXmtlehtrk%3D
41. Y Jing L Wang L Xia G Chen Z Chen, et al. 2001 Combined effect of all-trans retinoic acid and arsenic trioxide in acute promyelocytic leukemia cells in vitro and in vivo Blood 97 264 269 10.1182/blood.V97.1.264 11133770 1:CAS:528:DC%2BD3MXis1ChsA%3D%3D (Pubitemid 32061269)
42. 3 combination yields a high quality remission and survival in newly diagnosed acute promyelocytic leukemia Proc Natl Acad Sci USA 101 5328 5335 10.1073/pnas.0400053101 15044693 1:CAS:528:DC%2BD2cXjsVagt74%3D (Pubitemid 38481160)
43. E Estey G Garcia-Manero A Ferrajoli S Faderl S Verstovsek, et al. 2006 Use of all-trans retinoic acid plus arsenic trioxide as an alternative to chemotherapy in untreated acute promyelocytic leukemia Blood 107 3469 3473 10.1182/blood-2005-10-4006 16373661 1:CAS:528:DC%2BD28Xkt1Git7c%3D
44. Hu J, Liu YF, Wu CF, Xu F, Shen ZX, et al. Long-term efficacy and safety of all-trans retinoic acid/arsenic trioxide-based therapy in newly diagnosed acute promyelocytic leukemia. Proc Natl Acad Sci USA. 2009;106:3342-7.
45. N Quenech'Du S Ruchaud N Khelef N Guiso 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 10.1038/sj.leu.2401171 9823961
46. Q Zhu JW Zhang HQ Zhu YL Shen M Flexor, 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 10.1182/blood.V99.7. 2562 11807007 1:CAS:528:DC%2BD38XhtValtrc%3D (Pubitemid 34525446)
47. MC Guillemin E Raffoux D Vitoux S Kogan H Soilihi, et al. 2002 In vivo activation of camp signaling induces growth arrest and differentiation in acute promyelocytic leukemia J Exp Med 196 1373 1380 10.1084/jem.20021129 12438428 1:CAS:528:DC%2BD38XovFOitb8%3D (Pubitemid 35375556)
48. E Duprez JR Lillehaug T Naoe M Lanotte 1996 cAMP signalling is decisive for recovery of nuclear bodies (PODs) during maturation of RA-resistant t(15;17) promyelocytic leukemia NB4 cells expressing PML-RAR alpha Oncogene 12 2451 2459 8649787 1:CAS:528:DyaK28XjvFCmtbg%3D
49. L Altucci A Rossin O Hirsch A Nebbioso D Vitoux, et al. 2005 Rexinoid-triggered differentiation and tumours selective apoptosis of AML by protein kinase-A-mediated de-subordination of RXR Cancer Res 65 8754 8765 10.1158/0008-5472.CAN-04-3569 16204045 1:CAS:528:DC%2BD2MXhtVKiu7%2FK (Pubitemid 41377364)
50. N Bruck D Vitoux C Ferry V Duong A Bauer, et al. 2009 A coordinated phosphorylation cascade initiated by p38MAPK/MSK1 directs RARalpha to target promoters EMBO J 28 34 47 10.1038/emboj.2008.256 19078967 1:CAS:528: DC%2BD1cXhsVylsbvO
51. G Bour E Gaillard N Bruck S Lalevee JL Plassat, et al. 2005 Cyclin H binding to the RARalpha activation function (AF)-2 domain directs phosphorylation of the AF-1 domain by cyclin-dependent kinase 7 Proc Natl Acad Sci USA 102 16608 16613 10.1073/pnas.0505556102 16275922 1:CAS:528: DC%2BD2MXht1KgsL7I (Pubitemid 41688824)
52. E Gaillard N Bruck Y Brelivet G Bour S Lalevee, et al. 2006 Phosphorylation by PKA potentiates retinoic acid receptor alpha activity by means of increasing interaction with and phosphorylation by cyclin H/cdk7 Proc Natl Acad Sci USA 103 9548 9553 10.1073/pnas.0509717103 16769902 1:CAS:528:DC%2BD28XmsVOns7k%3D (Pubitemid 43955862)
53. C Rochette-Egly S Adam M Rossignol J-M Egly P Chambon 1997 Stimulation of RAR alpha activation function AF-1 through binding to the general transcription factor TFIIH and phosphorylation by CDK7 Cell 90 97 107 10.1016/S0092-8674(00) 80317-7 9230306 1:CAS:528:DyaK2sXkslShu7k%3D (Pubitemid 28009422)
54. JC Wang JE Dick 2005 Cancer stem cells: lessons from leukemia Trends Cell Biol 15 494 501 10.1016/j.tcb.2005.07.004 16084092 1:CAS:528: DC%2BD2MXpvFenu7c%3D (Pubitemid 41253469)
55. Guibal FC, Alberich-Jorda M, Hirai H, Ebralidze A, Levantini E, et al. Identification of a myeloid committed progenitor as the cancer initiating cell in acute promyelocytic leukemia. Blood. 2009;114:5415-25.
56. S Wojiski FC Guibal T Kindler BH Lee JL Jesneck, et al. 2009 PML-RARalpha initiates leukemia by conferring properties of self-renewal to committed promyelocytic progenitors Leukemia 23 1462 1471 10.1038/leu.2009.63 19322209 1:CAS:528:DC%2BD1MXpvF2ktbg%3D
57. C Du RL Redner MP Cooke C Lavau 1999 Overexpression of wild-type retinoic acid receptor alpha (RAR alpha) recapitulates retinoic acid-sensitive transformation of primary myeloid progenitors by acute promyelocytic leukemia RAR alpha-fusion genes Blood 94 793 802 10397747 1:CAS:528:DyaK1MXksVemu70%3D
58. R Nasr MC Guillemin O Ferhi H Soilihi L Peres, et al. 2008 Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation Nat Med 14 1333 1342 10.1038/nm.1891 19029980 1:CAS:528:DC%2BD1cXhsVWhu7jN
59. JD Licht 2009 Acute promyelocytic leukemia-weapons of mass differentiation N Engl J Med 360 928 930 10.1056/NEJMcibr0810371 19246367 1:CAS:528:DC%2BD1MXis1Cntrs%3D
60. SC Kogan 2009 Curing APL: differentiation or destruction? Cancer Cell 15 7 8 10.1016/j.ccr.2008.12.012 19111876 1:CAS:528:DC%2BD1MXptVGqtw%3D%3D
61. X Zheng A Seshire B Ruster G Bug T Beissert, et al. 2007 Arsenic but not all-trans retinoic acid overcomes the aberrant stem cell capacity of PML/RARalpha-positive leukemic stem cells Haematologica 92 323 331 10.3324/haematol.10541 17339181 1:CAS:528:DC%2BD2sXhtFGqu77I (Pubitemid 350143541)
62. JD Licht C Chomienne A Goy A Chen AA Scott, et al. 1995 Clinical and molecular characterization of a rare syndrome of acute promyelocytic leukemia associated with translocation (11;17) Blood 85 1083 1094 7849296 1:CAS:528:DyaK2MXjs1OjtbY%3D
63. RJ Lin L Nagy S Inoue WL Shao WH Miller, et al. 1998 Role of the histone deacetylase complex in acute promyelocytic leukaemia Nature 391 811 814 10.1038/35895 9486654 1:CAS:528:DyaK1cXhtlCisr4%3D (Pubitemid 28099682)
64. L-Z He F Guidez C Tribioli D Peruzzi M Ruthardt, et al. 1998 Distinct interactions of PML-RARalpha and PLZF-RARalpha with co-repressors determine differential responses to RA in APL Nat Genet 18 126 135 10.1038/ng0298-126 9462740 1:CAS:528:DyaK1cXosFOrsw%3D%3D (Pubitemid 28082458)
65. F Grignani S de Matteis C Nervi L Tomassoni V Gelmetti, et al. 1998 Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia Nature 391 815 818 10.1038/35901 9486655 1:CAS:528:DyaK1cXhtlCisrs%3D (Pubitemid 28099683)
66. Rice KL, Hormaeche I, Doulatov S, Flatow JM, Grimwade D, et al. Comprehensive genomic screens identify a role for PLZF-RAR{alpha} as a positive regulator of cell proliferation via direct regulation of c-MYC. Blood. 2009;114:5499-511.
67. B Cassinat I Guillemot C Molucon-Chabrot F Zassadowski P Fenaux, et al. 2006 Favourable outcome in an APL patient with PLZF/RARalpha fusion gene: quantitative real-time RT-PCR confirms molecular response Haematologica 91 ECR58 17194664
68. W Shao M Fanelli FF Ferrara R Riccioni A Rosenauer, et al. 1998 Arsenic trioxide as an inducer of apoptosis and loss of PML/RARalpha protein in acute promyelocytic leukemia cells J Natl Cancer Inst 90 124 133 10.1093/jnci/90.2.124 9450572 1:CAS:528:DyaK1cXosleltw%3D%3D
69. R Nasr V Lallemand-Breitenbach J Zhu MC Guillemin H de Thé 2009 Therapy-induced PML/RARA proteolysis and acute promyelocytic leukemia cure Clin Cancer Res 15 6321 6326 10.1158/1078-0432.CCR-09-0209 19808868 1:CAS:528:DC%2BD1MXhtlyqsLfI