An ATRActive future for differentiation therapy in AML

Blood Reviews

Volumn 29, Issue 4, 2015, Pages 263-268

  Johnson, Daniel E ^a   Redner, Robert L ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

AML; ATRA; Differentiation therapy

Indexed keywords

AZACITIDINE; CYTARABINE; CYTOPLASMIC RETINOIC ACID BINDING PROTEIN; CYTOSOLIC RETINOID BINDING PROTEIN; DASATINIB; DAUNORUBICIN; ETOPOSIDE; FLUDARABINE; GLYCOGEN SYNTHASE KINASE 3; HYDROXYUREA; IDARUBICIN; MITOXANTRONE; MN1 PROTEIN; ONCOPROTEIN; PRAME PROTEIN; RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR ALPHA; RETINOID BINDING PROTEIN; SKI PROTEIN; TIOGUANINE; UNCLASSIFIED DRUG; VALPROIC ACID; ANTINEOPLASTIC AGENT;

ACUTE MONOCYTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; APOPTOSIS; CANCER CELL CULTURE; CANCER RECURRENCE; CANCER REGRESSION; CANCER SURVIVAL; CANCER THERAPY; CELL DIFFERENTIATION; CLINICAL TRIAL (TOPIC); CONSOLIDATION CHEMOTHERAPY; DIFFERENTIATION THERAPY; DOWN REGULATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME INHIBITION; EPIGENETICS; GENE INDUCTION; GENE TARGETING; HUMAN; INDUCTION CHEMOTHERAPY; INTRACELLULAR SIGNALING; MONOTHERAPY; MYELOID LEUKEMIA CELL LINE; NONHUMAN; ONCOGENE; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; UPREGULATION; LEUKEMIA, MYELOID, ACUTE; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL DIFFERENTIATION; HUMANS; LEUKEMIA, MYELOID, ACUTE; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 84937115270     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2015.01.002     Document Type: Article

References (68)

1. Melnick A., Licht J.D. Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 1999, 93:3167-3215.
2. de The H., Lavau C., Marchio A., Chomienne C., Degos L., Dejean A. The PML-RAR alpha fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 1991, 66:675-684.
3. Kakizuka A., Miller W.H., Umesono K., Warrell R.P., Frankel S.R., Murty V.V., et al. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR alpha with a novel putative transcription factor. PML, Cell 1991, 66:663-674.
4. Nasr R., Guillemin M.C., Ferhi O., Soilihi H., Peres L., Berthier C., et al. Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nat Med 2008, 14:1333-1342.
5. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 1988, 240:889-895.
6. Umesono K., Murakami K.K., Thompson C.C., Evans R.M. Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 1991, 65:1255-1266.
7. Nagy L., Kao H.Y., Chakravarti D., Lin R.J., Hassig C.A., Ayer D.E., et al. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 1997, 89:373-380.
8. Nagy L., Kao H.Y., Love J.D., Li C., Banayo E., Gooch J.T., et al. Mechanism of corepressor binding and release from nuclear hormone receptors. Genes Dev 1999, 13:3209-3216.
9. Balmer J.E., Blomhoff R. Gene expression regulation by retinoic acid. J Lipid Res 2002, 43:1773-1808.
10. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996, 10:940-954.
11. Breitman T.R., Selonick S.E., Collins S.J. Induction of differentiation of the human promyelocytic leukemia cell line (HL-60) by retinoic acid. Proc Natl Acad Sci U S A 1980, 77:2936-2940.
12. Giguere V., Ong E.S., Segui P., Evans R.M. Identification of a receptor for the morphogen retinoic acid. Nature 1987, 330:624-629.
13. Tsai S., Bartelmez S., Heyman R., Damm K., Evans R., Collins S.J. A mutated retinoic acid receptor-alpha exhibiting dominant-negative activity alters the lineage development of a multipotent hematopoietic cell line. Genes Dev 1992, 6:2258-2269.
14. Mendelsohn C., Lohnes D., Decimo D., Lufkin T., LeMeur M., Chambon P., et al. Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 1994, 120:2749-2771.
15. Ablain J., de The H. Revisiting the differentiation paradigm in acute promyelocytic leukemia. Blood 2011, 117:5795-5802.
16. Nasr R., de The H. Eradication of acute promyelocytic leukemia-initiating cells by PML/RARA-targeting. Int J Hematol 2010, 91:742-747.
17. de The H., Chen Z. Acute promyelocytic leukaemia: novel insights into the mechanisms of cure. Nat Rev Cancer 2010, 10:775-783.
18. Collins S.J. The role of retinoids and retinoic acid receptors in normal hematopoiesis. Leukemia 2002, 16:1896-1905.
19. Bradbury D.A., Aldington S., Zhu Y.M., Russell N.H. Down-regulation of bcl-2 in AML blasts by all-trans retinoic acid and its relationship to CD34 antigen expression. Br J Haematol 1996, 94:671-675.
20. Sakashita A., Kizaki M., Pakkala S., Schiller G., Tsuruoka N., Tomosaki R., et al. 9-cis-retinoic acid: effects on normal and leukemic hematopoiesis in vitro. Blood 1993, 81:1009-1016.
21. Lehmann S., Bengtzen S., Broberg U., Paul C. Effects of retinoids on cell toxicity and apoptosis in leukemic blast cells from patients with non-M3 AML. Leuk Res 2000, 24:19-25.
22. Ryningen A., Stapnes C., Paulsen K., Lassalle P., Gjertsen B.T., Bruserud O. In vivo biological effects of ATRA in the treatment of AML. Expert Opin Investig Drugs 2008, 17:1623-1633.
23. Griggs J.J., Henley S.E., Rowe J.M. Treatment of refractory undifferentiated acute myelogenous leukemia with all-trans-retinoic acid. Am J Hematol 1994, 45:177-180.
24. Qian S.X., Li J.Y., Hong M., Qiu H.R., Fan L., Xu W. Acute myeloid leukemia in four patients with t(8;21) treated with all-trans retinoic acid as a single agent. Leuk Lymphoma 2008, 49:998-1001.
25. Belhabri A., Thomas X., Wattel E., Chelghoum Y., Anglaret B., Vekhoff A., et al. All trans retinoic acid in combination with intermediate-dose cytarabine and idarubicin in patients with relapsed or refractory non promyelocytic acute myeloid leukemia: a phase II randomized trial. Hematol J 2002, 3:49-55.
26. Milligan D.W., Wheatley K., Littlewood T., Craig J.I., Burnett A.K. Fludarabine and cytosine are less effective than standard ADE chemotherapy in high-risk acute myeloid leukemia, and addition of G-CSF and ATRA are not beneficial: results of the MRC AML-HR randomized trial. Blood 2006, 107:4614-4622.
27. Burnett A.K., Milligan D., Prentice A.G., Goldstone A.H., McMullin M.F., Hills R.K., et al. A comparison of low-dose cytarabine and hydroxyurea with or without all-trans retinoic acid for acute myeloid leukemia and high-risk myelodysplastic syndrome in patients not considered fit for intensive treatment. Cancer 2007, 109:1114-1124.
28. Burnett A.K., Hills R.K., Milligan D.W., Goldstone A.H., Prentice A.G., McMullin M.F., et al. Attempts to optimize induction and consolidation treatment in acute myeloid leukemia: results of the MRC AML12 trial. J Clin Oncol 2010, 28:586-595.
29. Estey E.H., Thall P.F., Pierce S., Cortes J., Beran M., Kantarjian H., et al. Randomized phase II study of fludarabine+cytosine arabinoside+idarubicin +/- all-trans retinoic acid +/- granulocyte colony-stimulating factor in poor prognosis newly diagnosed acute myeloid leukemia and myelodysplastic syndrome. Blood 1999, 93:2478-2484.
30. Schlenk R.F., Frohling S., Hartmann F., Fischer J.T., Glasmacher A., del Valle F., et al. Phase III study of all-trans retinoic acid in previously untreated patients 61years or older with acute myeloid leukemia. Leukemia 2004, 18:1798-1803.
31. Nazha A., Bueso-Ramos C., Estey E., Faderl S., O'Brien S., Fernandez M.H., et al. The Addition of All-Trans Retinoic Acid to Chemotherapy May Not Improve the Outcome of Patient with NPM1 Mutated Acute Myeloid Leukemia. Front Oncol 2013, 3:218.
32. Schlenk R.F., Dohner K., Krauter J., Giadzik V.I., Paschka P., Heuser M., et al. All-trans Retinoic Acid Improves Outcome in Younger Adult Patients with Nucleophosmin-1 Mediated Acute Myeloid Leukemia - Resutls of the AMLSG 07-04 Randomized Treatment Trial. American Society of Hematology Annual Meeting 2011, 80A.
33. Ritter M., Kattmann D., Teichler S., Hartmann O., Samuelsson M.K., Burchert A., et al. Inhibition of retinoic acid receptor signaling by Ski in acute myeloid leukemia. Leukemia 2006, 20:437-443.
34. Fazi F., Zardo G., Gelmetti V., Travaglini L., Ciolfi A., Di Croce L., et al. Heterochromatic gene repression of the retinoic acid pathway in acute myeloid leukemia. Blood 2007, 109:4432-4440.
35. Heuser M., Argiropoulos B., Kuchenbauer F., Yung E., Piper J., Fung S., et al. MN1 overexpression induces acute myeloid leukemia in mice and predicts ATRA resistance in patients with AML. Blood 2007, 110:1639-1647.
36. Bullinger L., Schlenk R.F., Gotz M., Botzenhardt U., Hofmann S., Russ A.C., et al. PRAME-induced inhibition of retinoic acid receptor signaling-mediated differentiation-a possible target for ATRA response in AML without t(15;17). Clin Cancer Res 2013, 19:2562-2571.
37. Melnick A.M. Epigenetics in AML. Best Pract Res Clin Haematol 2010, 23:463-468.
38. Figueroa M.E., Lugthart S., Li Y., Erpelinck-Verschueren C., Deng X., Christos P.J., et al. DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Cancer Cell 2010, 17:13-27.
39. Ferrara F.F., Fazi F., Bianchini A., Padula F., Gelmetti V., Minucci S., et al. Histone deacetylase-targeted treatment restores retinoic acid signaling and differentiation in acute myeloid leukemia. Cancer Res 2001, 61:2-7.
40. Trus M.R., Yang L., Suarez Saiz F., Bordeleau L., Jurisica I., Minden M.D. The histone deacetylase inhibitor valproic acid alters sensitivity towards all trans retinoic acid in acute myeloblastic leukemia cells. Leukemia 2005, 19:1161-1168.
41. Cimino G., Lo-Coco F., Fenu S., Travaglini L., Finolezzi E., Mancini M., et al. Sequential valproic acid/all-trans retinoic acid treatment reprograms differentiation in refractory and high-risk acute myeloid leukemia. Cancer Res 2006, 66:8903-8911.
42. Kuendgen A., Knipp S., Fox F., Strupp C., Hildebrandt B., Steidl C., et al. Results of a phase 2 study of valproic acid alone or in combination with all-trans retinoic acid in 75 patients with myelodysplastic syndrome and relapsed or refractory acute myeloid leukemia. Ann Hematol 2005, 84(Suppl. 1):61-66.
43. Fredly H., Ersvaer E., Kittang A.O., Tsykunova G., Gjertsen B.T., Bruserud O. The combination of valproic acid, all-trans retinoic acid and low-dose cytarabine as disease-stabilizing treatment in acute myeloid leukemia. Clin Epigen 2013, 5:13.
44. Ryningen A., Stapnes C., Lassalle P., Corbascio M., Gjertsen B.T., Bruserud O. A subset of patients with high-risk acute myelogenous leukemia shows improved peripheral blood cell counts when treated with the combination of valproic acid, theophylline and all-trans retinoic acid. Leuk Res 2009, 33:779-787.
45. Bug G., Ritter M., Wassmann B., Schoch C., Heinzel T., Schwarz K., et al. Clinical trial of valproic acid and all-trans retinoic acid in patients with poor-risk acute myeloid leukemia. Cancer 2005, 104:2717-2725.
46. Tassara M., Dohner K., Brossart P., Held G., Gotze K., Horst H.A., et al. Valproic acid in combination with all-trans retinoic acid and intensive therapy for acute myeloid leukemia in older patients. Blood 2014, 123:4027-4036.
47. Soriano A.O., Yang H., Faderl S., Estrov Z., Giles F., Ravandi F., et al. Safety and clinical activity of the combination of 5-azacytidine, valproic acid, and all-trans retinoic acid in acute myeloid leukemia and myelodysplastic syndrome. Blood 2007, 110:2302-2308.
48. van der Helm L.H., Scheepers E.R., Veeger N.J., Daenen S.M., Mulder A.B., van den Berg E., et al. Azacitidine might be beneficial in a subgroup of older AML patients compared to intensive chemotherapy: a single centre retrospective study of 227 consecutive patients. J Hematol Oncol 2013, 6:29.
49. Schenk T., Chen W.C., 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.
50. Gianni M., Peviani M., Bruck N., Rambaldi A., Borleri G., Terao M., et al. p38alphaMAPK interacts with and inhibits RARalpha: suppression of the kinase enhances the therapeutic activity of retinoids in acute myeloid leukemia cells. Leukemia 2012, 26:1850-1861.
51. Srinivas H., Juroske D.M., Kalyankrishna S., Cody D.D., Price R.E., Xu X.C., et al. c-Jun N-terminal kinase contributes to aberrant retinoid signaling in lung cancer cells by phosphorylating and inducing proteasomal degradation of retinoic acid receptor alpha. Mol Cell Biol 2005, 25:1054-1069.
52. Srinivas H., Xia D., Moore N.L., Uray I.P., Kim H., Ma L., et al. Akt phosphorylates and suppresses the transactivation of retinoic acid receptor alpha. Biochem J 2006, 395:653-662.
53. Delmotte M.H., Tahayato A., Formstecher P., Lefebvre P. Serine 157, a retinoic acid receptor alpha residue phosphorylated by protein kinase C in vitro, is involved in RXR.RARalpha heterodimerization and transcriptional activity. J Biol Chem 1999, 274:38225-38231.
54. Hoshikawa Y., Kanki K., Ashla A.A., Arakaki Y., Azumi J., Yasui T., et al. c-Jun N-terminal kinase activation by oxidative stress suppresses retinoid signaling through proteasomal degradation of retinoic acid receptor alpha protein in hepatic cells. Cancer Sci 2011, 102:934-941.
55. Si J., Mueller L., Collins S.J. GSK3 inhibitors enhance retinoic acid receptor activity and induce the differentiation of retinoic acid-sensitive myeloid leukemia cells. Leukemia 2011, 25:1914-1918.
56. Gupta K., Gulen F., Sun L., Aguilera R., Chakrabarti A., Kiselar J., et al. GSK3 is a regulator of RAR-mediated differentiation. Leukemia 2012, 26:1277-1285.
57. Kropf P.L., Wang L., Zang Y., Redner R.L., Johnson D.E. Dasatinib promotes ATRA-induced differentiation of AML cells. Leukemia 2010, 24:663-665.
58. Miranda M.B., Redner R.L., Johnson D.E. Inhibition of Src family kinases enhances retinoic acid induced gene expression and myeloid differentiation. Mol Cancer Ther 2007, 6:3081-3090.
59. Bastien J., Rochette-Egly C. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 2004, 328:1-16.
60. Boudjelal M., Voorhees J.J., Fisher G.J. Retinoid signaling is attenuated by proteasome-mediated degradation of retinoid receptors in human keratinocyte HaCaT cells. Exp Cell Res 2002, 274:130-137.
61. Tanaka T. Rodriguez de la Concepcion ML, De Luca LM. Involvement of all-trans-retinoic acid in the breakdown of retinoic acid receptors alpha and gamma through proteasomes in MCF-7 human breast cancer cells. Biochem Pharmacol 2001, 61:1347-1355.
62. Luo P., Lin M., Li L., Yang B., He Q. The proteasome inhibitor bortezomib enhances ATRA-induced differentiation of neuroblastoma cells via the JNK mitogen-activated protein kinase pathway. PLoS One 2011, 6:e27298.
63. Ying M., Zhou X., Zhong L., Lin N., Jing H., Luo P., et al. Bortezomib sensitizes human acute myeloid leukemia cells to all-trans-retinoic acid-induced differentiation by modifying the RARalpha/STAT1 axis. Mol Cancer Ther 2013, 12:195-206.
64. Desmond J.C., Mountford J.C., Drayson M.T., Walker E.A., Hewison M., Ride J.P., et al. The aldo-keto reductase AKR1C3 is a novel suppressor of cell differentiation that provides a plausible target for the non-cyclooxygenase-dependent antineoplastic actions of nonsteroidal anti-inflammatory drugs. Cancer Res 2003, 63:505-512.
65. Khanim F.L., Hayden R.E., Birtwistle J., Lodi A., Tiziani S., Davies N.J., et al. Combined bezafibrate and medroxyprogesterone acetate: potential novel therapy for acute myeloid leukaemia. PLoS One 2009, 4:e8147.
66. Brown G., Hughes P. Retinoid differentiation therapy for common types of acute myeloid leukemia. Leuk Res Treatment 2012, 2012:939021.
67. Meli M., Tolomeo M., Grifantini M., Franchetti P., Cappellacci L., Simoni D., et al. The synergistic apoptotic effects of thiophenfurin, an inosine monophosphate dehydrogenase inhibitor, in combination with retinoids in HL60 cells. Oncol Rep 2007, 17:185-192.
68. Moosavi M.A., Yazdanparast R., Lotfi A. 3-Hydrogenkwadaphnin induces monocytic differentiation and enhances retinoic acid-mediated granulocytic differentiation in NB4 cell line. J Biochem Mol Biol 2006, 39:722-729.