Dicer1 imparts essential survival cues in Notch-driven T-ALL via miR-21-mediated tumor suppressor Pdcd4 repression

Blood

Volumn 126, Issue 8, 2015, Pages 993-1004

  Junker, Fabian ^a   Chabloz, Antoine ^a   Koch, Ute ^a   Radtke, Freddy ^a  

^a EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA 21; NOTCH1 RECEPTOR; APOPTOSIS REGULATORY PROTEIN; MICRORNA; MIRN21 MICRORNA, HUMAN; MIRN21 MICRORNA, MOUSE; NOTCH RECEPTOR; PDCD4 PROTEIN, HUMAN; PDCD4 PROTEIN, MOUSE; RIBONUCLEASE III; RNA BINDING PROTEIN; SMALL INTERFERING RNA;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER GROWTH; CELL CYCLE PROGRESSION; CELL SURVIVAL; CONTROLLED STUDY; DICER1 GENE; GENE; GENE FUNCTION; GENE INACTIVATION; GENE LOSS; GENE REPRESSION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PDCD4 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T CELL LEUKEMIA; T LYMPHOCYTE; T-CELL LEUKEMIA CELL LINE; TUMOR SUPPRESSOR GENE; ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICRORNAS; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTORS, NOTCH; RIBONUCLEASE III; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TRANSFECTION;

EID: 84940043946     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-12-618892     Document Type: Article

References (65)

1. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-233.
2. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19(1):92-105.
3. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol. 2010;10(2):111-122.
4. Danen-van Oorschot AA, Kuipers JE, Arentsen-Peters S, et al. Differentially expressed miRNAs in cytogenetic and molecular subtypes of pediatric acute myeloid leukemia. Pediatr Blood Cancer. 2012;58(5):715-721.
5. Guo S, Lu J, Schlanger R, et al. MicroRNA miR-125a controls hematopoietic stem cell number. Proc Natl Acad Sci USA. 2010;107(32):14229-14234.
6. Cobb BS, Nesterova TB, Thompson E, et al. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J Exp Med. 2005;201(9):1367-1373.
7. Alemdehy MF, Erkeland SJ. Stop the dicing in hematopoiesis: what have we learned? Cell Cycle. 2012;11(15):2799-2807.
8. Alemdehy MF, van Boxtel NG, de Looper HW, et al. Dicer1 deletion in myeloid-committed progenitors causes neutrophil dysplasia and blocks macrophage/dendritic cell development in mice. Blood. 2012;119(20):4723-4730.
9. Arrate MP, Vincent T, Odvody J, Kar R, Jones SN, Eischen CM. MicroRNA biogenesis is required for Myc-induced B-cell lymphoma development and survival. Cancer Res. 2010;70(14):6083-6092.
10. Mavrakis KJ, Leslie CS, Wendel HG. Cooperative control of tumor suppressor genes by a network of oncogenic microRNAs. Cell Cycle. 2011;10(17):2845-2849.
11. Li X, Sanda T, Look AT, Novina CD, von Boehmer H. Repression of tumor suppressor miR-451 is essential for NOTCH1-induced oncogenesis in T-ALL. J Exp Med. 2011;208(4):663-675.
12. Fragoso R, Mao T, Wang S, et al. Modulating the strength and threshold of NOTCH oncogenic signals by mir-181a-1/b-1. PLoS Genet. 2012;8(8):e1002855.
13. Mets E, Van der Meulen J, Van Peer G, et al. MicroRNA-193b-3p acts as a tumor suppressor by targeting the MYB oncogene in T-cell acute lymphoblastic leukemia. Leukemia. 2015;29(4):798-806.
14. Mets E, Van Peer G, Van der Meulen J, et al. MicroRNA-128-3p is a novel oncomiR targeting PHF6 in T-cell acute lymphoblastic leukemia. Haematologica. 2014;99(8):1326-1333.
15. Harfe BD, McManus MT, Mansfield JH, Hornstein E, Tabin CJ. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci USA. 2005;102(31):10898-10903.
16. Lee PP, Fitzpatrick DR, Beard C, et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity. 2001;15(5):763-774.
17. Kühn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995;269(5229):1427-1429.
18. Koch U, Fiorini E, Benedito R, et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J Exp Med. 2008;205(11):2515-2523.
19. Anderson SJ, Abraham KM, Nakayama T, Singer A, Perlmutter RM. Inhibition of T-cell receptor beta-chain gene rearrangement by overexpression of the non-receptor protein tyrosine kinase p56lck. EMBO J. 1992;11(13):4877-4886.
20. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, Rajewsky K. Aberrant T cell differentiation in the absence of Dicer. J Exp Med. 2005;202(2):261-269.
21. Kanellopoulou C, Muljo SA, Kung AL, et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 2005;19(4):489-501.
22. Mavrakis KJ, Van Der Meulen J, Wolfe AL, et al. A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL) [published correction appears in Nat Genet. 2011;43(8):815]. Nat Genet. 2011;43(7):673-678.
23. Kumar MS, Pester RE, Chen CY, et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev. 2009;23(23):2700-2704.
24. Lambertz I, Nittner D, Mestdagh P, et al. Monoallelic but not biallelic loss of Dicer1 promotes tumorigenesis in vivo. Cell Death Differ. 2010;17(4):633-641.
25. Podshivalova K, Salomon DR. MicroRNA regulation of T-lymphocyte immunity: modulation of molecular networks responsible for T-cell activation, differentiation, and development. Crit Rev Immunol. 2013;33(5):435-476.
26. Ghisi M, Corradin A, Basso K, et al. Modulation of microRNA expression in human T-cell development: targeting of NOTCH3 by miR-150. Blood. 2011;117(26):7053-7062.
27. Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol. 2009;27(34):5848-5856.
28. Palomero T, Barnes KC, Real PJ, et al. CUTLL1, a novel human T-cell lymphoma cell line with t(7;9) rearrangement, aberrant NOTCH1 activation and high sensitivity to gamma-secretase inhibitors. Leukemia. 2006;20(7):1279-1287.
29. Rao SS, O'Neil J, Liberator CD, et al. Inhibition of NOTCH signaling by gamma secretase inhibitor engages the RB pathway and elicits cell cycle exit in T-cell acute lymphoblastic leukemia cells. Cancer Res. 2009;69(7):3060-3068.
30. Wang H, Zang C, Taing L, et al. NOTCH1-RBPJ complexes drive target gene expression through dynamic interactions with superenhancers. Proc Natl Acad Sci USA. 2014;111(2):705-710.
31. Koshkin AA, Singh SK, Nielsen P, et al. LNA (locked nucleic acids): synthesis of the adenine, cytosine, guanine, 5-methylcytosine, thymine and uracil bicyclonucleoside monomers, oligomerisation, and unprecedented nucleic acid recognition. Tetrahedron. 1998;54(14):3607-3630.
32. Thum T, Chau N, Bhat B, et al. Comparison of different miR-21 inhibitor chemistries in a cardiac disease model. J Clin Invest. 2011;121(2):461-462, author reply 462-463.
33. Buscaglia LE, Li Y. Apoptosis and the target genes of microRNA-21. Chin J Cancer. 2011;30(6):371-380.
34. Haferlach T, Kohlmann A, Wieczorek L, et al. Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukemia: report from the International Microarray Innovations in Leukemia Study Group. J Clin Oncol. 2010;28(15):2529-2537.
35. Durinck K, Wallaert A, Van de Walle I, et al. The Notch driven long non-coding RNA repertoire in T-cell acute lymphoblastic leukemia. Haematologica. 2014;99(12):1808-1816.
36. Shibahara K, Asano M, Ishida Y, Aoki T, Koike T, Honjo T. Isolation of a novel mouse gene MA-3 that is induced upon programmed cell death. Gene. 1995;166(2):297-301.
37. Zhang H, Ozaki I, Mizuta T, et al. Involvement of programmed cell death 4 in transforming growth factor-beta1-induced apoptosis in human hepatocellular carcinoma. Oncogene. 2006;25(45):6101-6112.
38. Wang X, Patenode C, Roizman B. US3 protein kinase of HSV-1 cycles between the cytoplasm and nucleus and interacts with programmed cell death protein 4 (PDCD4) to block apoptosis. Proc Natl Acad Sci USA. 2011;108(35):14632-14636.
39. Liwak U, Jordan LE, Von-Holt SD, et al. Loss of PDCD4 contributes to enhanced chemoresistance in Glioblastoma multiforme through de-repression of Bcl-xL translation. Oncotarget. 2013;4(9):1365-1372.
40. Hebestreit K, Gröttrup S, Emden D, et al. Leukemia gene atlas - a public platform for integrative exploration of genome-wide molecular data. PLoS ONE. 2012;7(6):e39148.
41. Loh PG, Yang HS, Walsh MA, et al. Structural basis for translational inhibition by the tumour suppressor Pdcd4. EMBO J. 2009;28(3):274-285.
42. Liwak U, Thakor N, Jordan LE, et al. Tumor suppressor PDCD4 represses internal ribosome entry site-mediated translation of antiapoptotic proteins and is regulated by S6 kinase 2. Mol Cell Biol. 2012;32(10):1818-1829.
43. Chonghaile TN, Roderick JE, Glenfield C, et al. Maturation stage of T-cell acute lymphoblastic leukemia determines BCL-2 versus BCL-XL dependence and sensitivity to ABT-199. Cancer Discov. 2014;4(9):1074-1087.
44. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834-838.
45. Gaur A, Jewell DA, Liang Y, et al. Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Res. 2007;67(6):2456-2468.
46. Arcangeli ML, Lancrin C, Lambolez F, et al. Extrathymic hemopoietic progenitors committed to T cell differentiation in the adult mouse. J Immunol. 2005;174(4):1980-1988.
47. Ravi A, Gurtan AM, Kumar MS, et al. Proliferation and tumorigenesis of a murine sarcoma cell line in the absence of DICER1. Cancer Cell. 2012;21(6):848-855.
48. Davalos V, Esteller M. Rolling the dice to discover the role of DICER in tumorigenesis. Cancer Cell. 2012;21(6):717-719.
49. Chivukula RR, Mendell JT. Circular reasoning: microRNAs and cell-cycle control. Trends Biochem Sci. 2008;33(10):474-481.
50. Subramanian S, Steer CJ. MicroRNAs as gatekeepers of apoptosis. J Cell Physiol. 2010;223(2):289-298.
51. Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005;65(14):6029-6033.
52. Rask L, Balslev E, Jørgensen S, et al. High expression of miR-21 in tumor stroma correlates with increased cancer cell proliferation in human breast cancer. APMIS. 2011;119(10):663-673.
53. Dillhoff M, Liu J, Frankel W, Croce C, Bloomston M. MicroRNA-21 is overexpressed in pancreatic cancer and a potential predictor of survival. J Gastrointest Surg. 2008;12(12):2171-2176.
54. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology. 2007;133(2):647-658.
55. Meng F, Henson R, Lang M, et al. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology. 2006;130(7):2113-2129.
56. Gaur AB, Holbeck SL, Colburn NH, Israel MA. Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro-oncol. 2011;13(6):580-590.
57. Yang HS, Jansen AP, Nair R, et al. A novel transformation suppressor, Pdcd4, inhibits AP-1 transactivation but not NF-kappaB or ODC transactivation. Oncogene. 2001;20(6):669-676.
58. Hilliard A, Hilliard B, Zheng SJ, et al. Translational regulation of autoimmune inflammation and lymphoma genesis by programmed cell death 4. J Immunol. 2006;177(11):8095-8102.
59. Schmid T, Jansen AP, Baker AR, Hegamyer G, Hagan JP, Colburn NH. Translation inhibitor Pdcd4 is targeted for degradation during tumor promotion. Cancer Res. 2008;68(5):1254-1260.
60. Lankat-Buttgereit B, Lenschen B, Schmidt H, Göke R. The action of Pdcd4 may be cell type specific: evidence that reduction of dUTPase levels might contribute to its tumor suppressor activity in Bon-1 cells. Apoptosis. 2008;13(1):157-164.
61. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH. Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem. 2008;283(2):1026-1033.
62. Lu Z, Liu M, Stribinskis V, et al. MicroRNA-21 promotes cell transformation by targeting the programmed cell death 4 gene. Oncogene. 2008;27(31):4373-4379.
63. Asangani IA, Rasheed SA, Nikolova DA, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 2008;27(15):2128-2136.
64. Yao Q, Xu H, Zhang QQ, Zhou H, Qu LH. MicroRNA-21 promotes cell proliferation and down-regulates the expression of programmed cell death 4 (PDCD4) in HeLa cervical carcinoma cells. Biochem Biophys Res Commun. 2009;388(3):539-542.
65. Waters LC, Strong SL, Ferlemann E, et al. Structure of the tandem MA-3 region of Pdcd4 protein and characterization of its interactions with eIF4A and eIF4G: molecular mechanisms of a tumor suppressor. J Biol Chem. 2011;286(19):17270-17280.