Critical role of retinoidrexinoid signaling in mediating transformation and therapeutic response of NUP98-RARG leukemia

Leukemia

Volumn 29, Issue 5, 2015, Pages 1153-1162

  Qiu, J J ^a,b   Zeisig, B B ^c   Li, S ^a,d   Liu, W ^d   Chu, H ^a   Song, Y ^a   Giordano, A ^e,f   Schwaller, J ^g   Gronemeyer, H ^h   Dong, S ^a   So, C W E ^c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^e TEMPLE UNIVERSITY   (United States)

^f UNIVERSITY OF SIENA   (Italy)

^g UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

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

Author keywords

[No Author keywords available]

Indexed keywords

4 [2 (5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL) 1,3 DIOXOLAN 2 YL]BENZOIC ACID; BEXAROTENE; HYBRID PROTEIN; NUCLEOPORIN 98; RETINOIC ACID; RETINOIC ACID RECEPTOR GAMMA; RETINOID; NUCLEAR PORE COMPLEX PROTEIN 98; NUCLEOPORIN; PROTEIN BINDING; RETINOIC ACID RECEPTOR;

AGONIST; ANIMAL CELL; ARTICLE; BONE MARROW; CELLULAR DISTRIBUTION; DEREGULATION; DNA BINDING; DRUG TARGETING; GENE MUTATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LEUKEMIA; LIGAND BINDING; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROTEIN DOMAIN; RETROVIRIDAE; SIGNAL TRANSDUCTION; STEM CELL; TRANSFORMED CELL; TREATMENT RESPONSE; VIRAL GENE DELIVERY SYSTEM; WILD TYPE; ANIMAL; CELL NUCLEUS; CELL TRANSFORMATION; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PROTEIN ANALYSIS; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, LEUKEMIC; HEK293 CELLS; HELA CELLS; HUMANS; LEUKEMIA; MICE; MICROSCOPY, FLUORESCENCE; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, RETINOIC ACID; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 84929268991     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2014.334     Document Type: Article

References (42)

1. Cheung N, So CW. Transcriptional and epigenetic networks in haematological malignancy. FEBS Lett 2011; 585: 2100-2111.
2. Such E, Cervera J, Valencia A, Barragan E, Ibanez M, Luna I et al. A novel NUP98/RARG gene fusion in acute myeloid leukemia resembling acute promyelocytic leukemia. Blood 2011; 117: 242-245.
3. Qiu JJ, Lu X, Zeisig BB, Ma Z, Cai X, Chen S et al. Leukemic transformation by the APL fusion protein PRKAR1A-RAR{alpha} critically depends on recruitment of RXR {alpha}. Blood 2010; 115: 643-652.
4. de The H, Chen Z. Acute promyelocytic leukaemia: novel insights into the mechanisms of cure. Nat Rev Cancer 2010; 10: 775-783.
5. Hollink IH, van den Heuvel-Eibrink MM, Arentsen-Peters ST, Pratcorona M, Abbas S, Kuipers JE et al. NUP98/NSD1 characterizes a novel poor prognostic group in acute myeloid leukemia with a distinct HOX gene expression pattern. Blood 2011; 118: 3645-3656.
6. Borrow J, Shearman AM, Stanton VP Jr., Becher R, Collins T, Williams AJ et al. The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat Genet 1996; 12: 159-167.
7. Nakamura T, Largaespada DA, Lee MP, Johnson LA, Ohyashiki K, Toyama K et al. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15;p15) in human myeloid leukaemia. Nat Genet 1996; 12: 154-158.
8. Gough SM, Slape CI, Aplan PD. NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood 2011; 118: 6247-6257.
9. Kasper LH, Brindle PK, Schnabel CA, Pritchard CE, Cleary ML, van Deursen JM et al. CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol Cell Biol 1999; 19: 764-776.
10. Chambon P. The molecular and genetic dissection of the retinoid signaling pathway. Recent Prog Horm Res 1995; 50: 317-332.
11. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996; 10: 940-954.
12. Qiu JJ, Chu H, Lu X, Jiang X, Dong S. The reduced and altered activities of PAX5 are linked to the protein-protein interaction motif (coiled-coil domain) of the PAX5-PML fusion protein in t(9;15)-associated acute lymphocytic leukemia. Oncogene 2011; 30: 967-977.
13. Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H et al. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 2009; 459: 847-851.
14. Kwok C, Zeisig BB, Dong S, So CW. Forced homo-oligomerization of RARalpha leads to transformation of primary hematopoietic cells. Cancer Cell 2006; 9: 95-108.
15. Cheung N, Chan LC, Thompson A, Cleary ML, So CW. Protein arginine-methyl-transferase-dependent oncogenesis. Nat Cell Biol 2007; 9: 1208-1215.
16. Zeisig BB, Kwok C, Zelent A, Shankaranarayanan P, Gronemeyer H, Dong S et al. Recruitment of RXR by homotetrameric RARalpha fusion proteins is essential for transformation. Cancer Cell 2007; 12: 36-51.
17. Qiu J, Huang Y, Chen G, Chen Z, Tweardy DJ, Dong S et al. Aberrant chromatin remodeling by retinoic acid receptor alpha fusion proteins assessed at the single-cell level. Mol Biol Cell 2007; 18: 3941-3951.
18. de Lera AR, Bourguet W, Altucci L, Gronemeyer H. Design of selective nuclear receptor modulators: RAR and RXR as a case study. Nat Rev Drug Discov 2007; 6: 811-820.
19. Arteaga MF, Mikesch JH, Qiu JH, Christensen J, Helin K, Kogan SC et al. The histone demethylase PHF8 governs retinoic acid response in acute promyelocyctic leukemia. Cancer Cell 2013; 23: 376-389.
20. So CW, Cleary ML. Common mechanism for oncogenic activation of MLL by forkhead family proteins. Blood 2003; 101: 633-639.
21. So CW, Cleary ML. MLL-AFX requires the transcriptional effector domains of AFX to transform myeloid progenitors and transdominantly interfere with forkhead protein function. Mol Cell Biol 2002; 22: 6542-6552.
22. Dong S, Tweardy DJ. Interactions of STAT5b-RARalpha, a novel acute promyelocytic leukemia fusion protein, with retinoic acid receptor and STAT3 signaling pathways. Blood 2002; 99: 2637-2646.
23. Oka M, Asally M, Yasuda Y, Ogawa Y, Tachibana T, Yoneda Y et al. . The mobile FG nucleoporin Nup98 is a cofactor for Crm1-dependent protein export. Mol Biol Cell 2010; 21: 1885-1896.
24. Zhu J, Nasr R, Peres L, Riaucoux-Lormiere F, Honore N, Berthier C et al. RXR Is an Essential Component of the Oncogenic PML/RARA Complex In Vivo. Cancer Cell 2007; 12: 23-35.
25. Kwok C, Zeisig BB, Qiu J, Dong S, So CW. Transforming activity of AML1-ETO is independent of CBFbeta and ETO interaction but requires formation of homo-oligomeric complexes. Proc Natl Acad Sci USA 2009; 106: 2853-2858.
26. So CW, Cleary ML. Dimerization: a versatile switch for oncogenesis. Blood 2004; 104: 919-922.
27. 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.
28. Sternsdorf T, Phan VT, Maunakea ML, Ocampo CB, Sohal J, Silletto A et al. Forced retinoic acid receptor alpha homodimers prime mice for APL-like leukemia. Cancer Cell 2006; 9: 81-94.
29. Pitha-Rowe I, Petty WJ, Kitareewan S, Dmitrovsky E. Retinoid target genes in acute promyelocytic leukemia. Leukemia 2003; 17: 1723-1730.
30. Zeisig BB, So CW. Retroviral/Lentiviral transduction and transformation assay. Methods Mol Biol 2009; 538: 207-229.
31. Zhou J, Peres L, Honore N, Nasr R, Zhu J, de The H et al. Dimerization-induced corepressor binding and relaxed DNA-binding specificity are critical for PML/RARA-induced immortalization. Proc Natl Acad Sci USA 2006; 103: 9238-9243.
32. So CW, Lin M, Ayton PM, Chen EH, Cleary ML. Dimerization contributes to oncogenic activation of MLL chimeras in acute leukemias. Cancer Cell 2003; 4: 99-110.
33. Martin ME, Milne TA, Bloyer S, Galoian K, Shen W, Gibbs D et al. Dimerization of MLL fusion proteins immortalizes hematopoietic cells. Cancer Cell 2003; 4: 197-207.
34. Liu Y, Cheney MD, Gaudet JJ, Chruszcz M, Lukasik SM, Sugiyama D et al. The tetramer structure of the Nervy homology two domain, NHR2, is critical for AML1/ETO's activity. Cancer Cell 2006; 9: 249-260.
35. Such E, Cordon L, Sempere A, Villamon E, Ibanez M, Luna I et al. In vitro all-trans retinoic acid sensitivity of acute myeloid leukemia blasts with NUP98/RARG fusion gene. Ann Hematol 2014; 93: 1931-1933.
36. Altucci L, Leibowitz MD, Ogilvie KM, de Lera AR, Gronemeyer H. RAR and RXR modulation in cancer and metabolic disease. Nat Rev Drug Discov 2007; 6: 793-810.
37. Fung TK, So CW. Overcoming treatment resistance in acute promyelocytic leukemia and beyond. Oncotarget 2013; 4: 1128-1129.
38. Schenk T, Chen WC, Gollner S, Howell L, Jin L, Hebestreit K et al. Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-trans-retinoic acid differentiation pathway in acute myeloid leukemia. Nat Med 2012; 18: 605-611.
39. Huang S, Laoukili J, Epping MT, Koster J, Holzel M, Westerman BA et al. ZNF423 is critically required for retinoic acid-induced differentiation and is a marker of neuroblastoma outcome. Cancer Cell 2009; 15: 328-340.
40. Epping MT, Wang L, Edel MJ, Carlee L, Hernandez M, Bernards R et al. The human tumor antigen PRAME is a dominant repressor of retinoic acid receptor signaling. Cell 2005; 122: 835-847.
41. Marinelli A, Bossi D, Pelicci PG, Minucci S. A redundant oncogenic potential of the retinoic receptor (RAR) alpha, beta and gamma isoforms in acute promyelocytic leukemia. Leukemia 2007; 21: 647-650.
42. Shankaranarayanan P, Rossin A, Khanwalkar H, Alvarez S, Alvarez R, Jacobson A et al. Growth factor-antagonized rexinoid apoptosis involves permissive PPARgamma/RXR heterodimers to activate the intrinsic death pathway by NO. Cancer Cell 2009; 16: 220-231.