Therapeutic antagonists of microRNAs deplete leukemia-initiating cell activity

Journal of Clinical Investigation

Volumn 124, Issue 1, 2014, Pages 222-236

  Velu, Chinavenmeni S ^a   Chaubey, Aditya ^a   Phelan, James D ^a   Horman, Shane R ^a   Wunderlich, Mark ^a   Guzman, Monica L ^b   Jegga, Anil G ^a   Zeleznik Le, Nancy J ^c   Chen, Jianjun ^d   Mulloy, James C ^a   Cancelas, Jose A ^a   Jordan, Craig T ^e   Aronow, Bruce J ^a   Marcucci, Guido ^f   Bhat, Balkrishen ^g   Gebelein, Brian ^a   Leighton Grimes, H ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF COLORADO   (United States)

^f OHIO STATE UNIVERSITY   (United States)

^g REGULUS THERAPEUTICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR INDEPENDENT 1; MICRORNA; MICRORNA 196B; MICRORNA 21; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; ALLELE; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL RENEWAL; COLONY FORMATION; CONTROLLED STUDY; DNA CONTENT; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MAJOR CLINICAL STUDY; MOUSE; MYELODYSPLASTIC SYNDROME; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TARGETING; TUMOR XENOGRAFT;

EID: 84892949628     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI66005     Document Type: Article

References (46)

1. Eppert K, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med. 2011;17(9):1086-1093.
2. Armstrong SA, et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet. 2002;30(1):41-47.
3. Ferrando AA, et al. Gene expression signatures in MLL-rearranged T-lineage and B-precursor acute leukemias: dominance of HOX dysregulation. Blood. 2003;102(1):262-268.
4. Grubach L, et al. Gene expression profiling of Polycomb, Hox Meis genes in patients with acute myeloid leukaemia. Eur J Haematol. 2008;81(2):112-122.
5. Wang GG, Cai L, Pasillas MP, Kamps MP. NUP98- NSD1 links H3K36 methylation to Hox-A gene activation and leukaemogenesis. Nat Cell Biol. 2007;9(7):804-812.
6. Mullighan CG, et al. Pediatric acute myeloid leukemia with NPM1 mutations is characterized by a gene expression profile with dysregulated HOX gene expression distinct from MLL-rearranged leukemias. Leukemia. 2007;21(9):2000-2009.
7. Drabkin HA, et al. Quantitative HOX expression in chromosomally defined subsets of acute myelogenous leukemia. Leukemia. 2002;16(2):186-195.
8. Golub TR, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999;286(5439):531-537.
9. Huang Y, et al. Identification and characterization of Hoxa9 binding sites in hematopoietic cells. Blood. 2012;119(2):388-398.
10. Hu YL, Passegue E, Fong S, Largman C, Lawrence HJ. Evidence that the Pim1 kinase gene is a direct target of HOXA9. Blood. 2007;109(11):4732-4738.
11. Hess JL, et al. c-Myb is an essential downstream target for homeobox-mediated transformation of hematopoietic cells. Blood. 2006;108(1):297-304.
12. Morgado E, Albouhair S, Lavau C. Flt3 is dispensable to the Hoxa9/Meis1 leukemogenic cooperation. Blood. 2007;109(9):4020-4022.
13. Wang GG, Pasillas MP, Kamps MP. Meis1 programs transcription of FLT3 and cancer stem cell character, using a mechanism that requires interaction with Pbx and a novel function of the Meis1 C-terminus. Blood. 2005;106(1):254-264.
14. Li-Kroeger D, Witt LM, Grimes HL, Cook TA, Gebelein B. Hox and senseless antagonism functions as a molecular switch to regulate EGF secretion in the Drosophila PNS. Dev Cell. 2008;15(2):298-308.
15. Horman SR, et al. Gfi1 integrates progenitor versus granulocytic transcriptional programming. Blood. 2009;113(22):5466-5475.
16. Velu CS, Baktula AM, Grimes HL. Gfi1 regulates miR-21 and miR-196b to control myelopoiesis. Blood. 2009;113(19):4720-4728.
17. Ross ME, et al. Gene expression profiling of pediatric acute myelogenous leukemia. Blood. 2004; 104(12):3679-3687.
18. Verhaak RG, et al. Prediction of molecular subtypes in acute myeloid leukemia based on gene expression profiling. Haematologica. 2009;94(1):131-134.
19. Calvo KR, Sykes DB, Pasillas MP, Kamps MP. Nup98- HoxA9 immortalizes myeloid progenitors, enforces expression of Hoxa9, Hoxa7 and Meis1, and alters cytokine-specific responses in a manner similar to that induced by retroviral co-expression of Hoxa9 and Meis1. Oncogene. 2002;21(27):4247-4256.
20. Zarebski A, et al. Mutations in growth factor independent- 1 associated with human neutropenia block murine granulopoiesis through colony stimulating factor-1. Immunity. 2008;28(3):370-380.
21. Zweidler-Mckay PA, Grimes HL, Flubacher MM, Tsichlis PN. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol Cell Biol. 1996;16(8):4024-4034.
22. Shen WF, et al. AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol Cell Biol. 1997;17(11):6448-6458.
23. Jongen-Lavrencic M, Sun SM, Dijkstra MK, Valk PJ, Lowenberg B. MicroRNA expression profiling in relation to the genetic heterogeneity of acute myeloid leukemia. Blood. 2008;111(10):5078-5085.
24. Wang Y, et al. MicroRNAs expression signatures are associated with lineage and survival in acute leukemias. Blood Cells Mol Dis. 2010;44(3):191-197.
25. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev. 2003;17(18):2298-2307.
26. Wong P, Iwasaki M, Somervaille TC, So CW, Cleary ML. Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev. 2007;21(21):2762-2774.
27. Faber J, et al. HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood. 2009;113(11):2375-2385.
28. Popovic R, et al. Regulation of mir-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood. 2009;113(14):3314-3322.
29. Krutzfeldt J, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature. 2005;438(7068):685-689.
30. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell. 2006;10(4):257-268.
31. Velu CS, Grimes HL. Utilizing antagomiR (antisense microRNA) to knock down microRNA in murine bone marrow cells. Methods Mol Biol. 2012; 928:185-195.
32. Becker H, et al. Favorable prognostic impact of NPM1 mutations in older patients with cytogenetically normal de novo acute myeloid leukemia and associated gene- And microRNA-expression signatures: a Cancer and Leukemia Group B study. J Clin Oncol. 2010;28(4):596-604.
33. Dohner H, et al. Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European LeukemiaNet. Blood. 2010;115(3):453-474.
34. Feuring-Buske M, Gerhard B, Cashman J, Humphries RK, Eaves CJ, Hogge DE. Improved engraftment of human acute myeloid leukemia progenitor cells in beta 2-microglobulin-deficient NOD/SCID mice and in NOD/SCID mice transgenic for human growth factors. Leukemia. 2003; 17(4):760-763.
35. Wunderlich M, et al. AML xenograft efficiency is significantly improved in NOD/SCID-IL2RG mice constitutively expressing human SCF, GM-CSF and IL-3. Leukemia. 2010;24(10):1785-1788.
36. Wunderlich M, et al. AML cells are differentially sensitive to chemotherapy treatment in a human xenograft model. Blood. 2013;121(12):e90-e97.
37. Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 2007;5(8):e203.
38. Morcos PA, Li Y, Jiang S. Vivo-Morpholinos: a nonpeptide transporter delivers Morpholinos into a wide array of mouse tissues. Biotechniques. 2008; 45(6):613-614.
39. Cammarata G, et al. Differential expression of specific microRNA and their targets in acute myeloid leukemia. Am J Hematol. 2010;85(5):331-339.
40. Care A, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med. 2007;13(5):613-618.
41. Ma L, et al. Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol. 2010;28(4):341-347.
42. Wolfrum C, et al. Mechanisms and optimization of in vivo delivery of lipophilic siRNAs. Nat Biotechnol. 2007;25(10):1149-1157.
43. Mulloy JC, Wunderlich M, Zheng Y, Wei J. Transforming human blood stem and progenitor cells: a new way forward in leukemia modeling. Cell Cycle. 2008;7(21):3314-3319.
44. Saito Y, et al. CD52 as a molecular target for immunotherapy to treat acute myeloid leukemia with high EVI1 expression. Leukemia. 2011;25(6):921-931.
45. Kazanjian A, et al. Growth factor independence-1 is expressed in primary human neuroendocrine lung carcinomas and mediates the differentiation of murine pulmonary neuroendocrine cells. Cancer Res. 2004;64(19):6874-6882.
46. Gebelein B, Urrutia R. Sequence-specific transcriptional repression by KS1, a multiple-zinc-finger- Kruppel-Associated box protein. Mol Cell Biol. 2001; 21(3):928-939.