Restoration of miR-424 suppresses BCR-ABL activity and sensitizes CML cells to imatinib treatment

Cancer Letters

Volumn 360, Issue 2, 2015, Pages 245-256

  Hershkovitz Rokah, Oshrat ^a   Modai, Shira ^a   Pasmanik Chor, Metsada ^a   Toren, Amos ^b   Shomron, Noam ^a   Raanani, Pia ^a   Shpilberg, Ofer ^c   Granot, Galit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b Safra Children's Hospital   (Israel)

^c ASSUTA MEDICAL CENTER   (Israel)

Author keywords

Apoptosis; BCR ABL; CML; Imatinib; MiR 424

Indexed keywords

ABELSON KINASE; BCR ABL PROTEIN; CRK LIKE PROTEIN; CYCLIN E; CYCLIN E1; IMATINIB; MICRORNA; MICRORNA 424; PROTEIN P21; STAT5 PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BENZAMIDE DERIVATIVE; MIRN424 MICRORNA, HUMAN; PIPERAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE;

3' UNTRANSLATED REGION; ABL GENE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL GROWTH; CELL PROLIFERATION; CELL SIZE; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG SENSITIVITY; GENE OVEREXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IC50; MYELOID LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; HL 60 CELL LINE; K562 CELL LINE; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; METABOLISM; MULTIMODALITY CANCER THERAPY; NUCLEOTIDE SEQUENCE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BASE SEQUENCE; BENZAMIDES; CELL GROWTH PROCESSES; COMBINED MODALITY THERAPY; DOWN-REGULATION; FUSION PROTEINS, BCR-ABL; HELA CELLS; HL-60 CELLS; HUMANS; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICRORNAS; PIPERAZINES; PYRIMIDINES; TRANSFECTION;

EID: 84924858174     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.02.031     Document Type: Article

References (54)

1. Spizzo R., Nicoloso M.S., Croce C.M., Calin G.A. SnapShot: MicroRNAs in cancer. Cell 2009, 137:586-586.e1.
2. Ramkissoon S.H., Mainwaring L.A., Ogasawara Y., Keyvanfar K., McCoy J.P., Sloand E.M., et al. Hematopoietic-specific microRNA expression in human cells. Leuk. Res 2006, 30:643-647.
3. Lu J., Getz G., Miska E.A., Alvarez-Saavedra E., Lamb J., Peck D., et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
4. O'Day E., Lal A. MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res 2010, 12:201.
5. Nana-Sinkam S.P., Geraci M.W. MicroRNA in lung cancer. J. Thorac. Oncol 2006, 1:929-931.
6. Li S., Fu H., Wang Y., Tie Y., Xing R., Zhu J., et al. MicroRNA-101 regulates expression of the v-fos FBJ murine osteosarcoma viral oncogene homolog (FOS) oncogene in human hepatocellular carcinoma. Hepatology 2009, 49:1194-1202.
7. Xu C., Liu S., Fu H., Li S., Tie Y., Zhu J., et al. MicroRNA-193b regulates proliferation, migration and invasion in human hepatocellular carcinoma cells. Eur. J. Cancer 2010, 46:2828-2836.
8. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 2005, 65:6029-6033.
9. Bandres E., Cubedo E., Agirre X., Malumbres R., Zarate R., Ramirez N., et al. Identification by real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol. Cancer 2006, 5:29.
10. Garzon R., Pichiorri F., Palumbo T., Visentini M., Aqeilan R., Cimmino A., et al. MicroRNA gene expression during retinoic acid-induced differentiation of human acute promyelocytic leukemia. Oncogene 2007, 26:4148-4157.
11. Zanette D.L., Rivadavia F., Molfetta G.A., Barbuzano F.G., Proto-Siqueira R., Silva-Jr W.A., et al. miRNA expression profiles in chronic lymphocytic and acute lymphocytic leukemia. Braz. J. Med. Biol. Res 2007, 40:1435-1440.
12. Calin G.A., Ferracin M., Cimmino A., Di Leva G., Shimizu M., Wojcik S.E., et al. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med 2005, 353:1793-1801.
13. Deininger M.W., Goldman J.M., Melo J.V. The molecular biology of chronic myeloid leukemia. Blood 2000, 96:3343-3356.
14. Savage D.G., Antman K.H. Imatinib mesylate - a new oral targeted therapy. N. Engl. J. Med 2002, 346:683-693.
15. Blower P.E., Chung J.H., Verducci J.S., Lin S., Park J.K., Dai Z., et al. MicroRNAs modulate the chemosensitivity of tumor cells. Mol. Cancer Ther 2008, 7:1-9.
16. Salerno E., Scaglione B.J., Coffman F.D., Brown B.D., Baccarini A., Fernandes H., et al. Correcting miR-15a/16 genetic defect in New Zealand Black mouse model of CLL enhances drug sensitivity. Mol. Cancer Ther 2009, 8:2684-2692.
17. Zhou M., Zeng J., Wang X., Guo Q., Huang T., Shen H., et al. MiR-370 sensitizes chronic myeloid leukemia K562 cells to homoharringtonine by targeting Forkhead box M1. J. Transl. Med 2013, 11:265.
18. Rissland O.S., Hong S.J., Bartel D.P. MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol. Cell 2011, 43:993-1004.
19. Liu Q., Fu H., Sun F., Zhang H., Tie Y., Zhu J., et al. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res 2008, 36:5391-5404.
20. Forrest A.R., Kanamori-Katayama M., Tomaru Y., Lassmann T., Ninomiya N., Takahashi Y., et al. Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 2010, 24:460-466.
21. Hershkovitz-Rokah O., Modai S., Pasmanik-Chor M., Toren A., Shomron N., Raanani P., et al. MiR-30e induces apoptosis and sensitizes K562 cells to imatinib treatment via regulation of the BCR-ABL protein. Cancer Lett 2015, 356(2 Pt B):597-605.
22. Liu Y., Song Y., Ma W., Zheng W., Yin H. Decreased microRNA-30a levels are associated with enhanced ABL1 and BCR-ABL1 expression in chronic myeloid leukemia. Leuk. Res 2013, 37:349-356.
23. Li Y., Wang H., Tao K., Xiao Q., Huang Z., Zhong L., et al. miR-29b suppresses CML cell proliferation and induces apoptosis via regulation of BCR/ABL1 protein. Exp. Cell Res 2013, 319:1094-1101.
24. Xu C., Fu H., Gao L., Wang L., Wang W., Li J., et al. BCR-ABL/GATA1/miR-138 mini circuitry contributes to the leukemogenesis of chronic myeloid leukemia. Oncogene 2014, 33:44-54.
25. Agirre X., Jimenez-Velasco A., San Jose-Eneriz E., Garate L., Bandres E., Cordeu L., et al. Down-regulation of hsa-miR-10a in chronic myeloid leukemia CD34+ cells increases USF2-mediated cell growth. Mol. Cancer Res 2008, 6:1830-1840.
26. Suresh S., McCallum L., Lu W., Lazar N., Perbal B., Irvine A.E. MicroRNAs 130a/b are regulated by BCR-ABL and downregulate expression of CCN3 in CML. J. Cell. Commun. Signal 2011, 5:183-191.
27. Hussein K., Busche G., Muth M., Gohring G., Kreipe H., Bock O. Expression of myelopoiesis-associated microRNA in bone marrow cells of atypical chronic myeloid leukaemia and chronic myelomonocytic leukaemia. Ann. Hematol 2011, 90:307-313.
28. Rokah O.H., Granot G., Ovcharenko A., Modai S., Pasmanik-Chor M., Toren A., et al. Downregulation of miR-31, miR-155, and miR-564 in chronic myeloid leukemia cells. PLoS ONE 2012, 7:e35501.
29. Breccia M., Alimena G. How to treat CML patients in the tyrosine kinase inhibitors era? From imatinib standard dose to second generation drugs front-line: unmet needs, pitfalls and advantages. Cancer Lett 2012, 322:127-132.
30. Gorre M.E., Mohammed M., Ellwood K., Hsu N., Paquette R., Rao P.N., et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001, 293:876-880.
31. Wilda M., Fuchs U., Wossmann W., Borkhardt A. Killing of leukemic cells with a BCR/ABL fusion gene by RNA interference (RNAi). Oncogene 2002, 21:5716-5724.
32. Wohlbold L., van der Kuip H., Miething C., Vornlocher H.P., Knabbe C., Duyster J., et al. Inhibition of bcr-abl gene expression by small interfering RNA sensitizes for imatinib mesylate (STI571). Blood 2003, 102:2236-2239.
33. Koldehoff M., Kordelas L., Beelen D.W., Elmaagacli A.H. Small interfering RNA against BCR-ABL transcripts sensitize mutated T315I cells to nilotinib. Haematologica 2010, 95:388-397.
34. Lee Y.S., Dutta A. MicroRNAs: small but potent oncogenes or tumor suppressors. Curr. Opin. Investig. Drugs 2006, 7:560-564.
35. Wang V., Wu W. MicroRNA-based therapeutics for cancer. Biodrugs 2009, 23:15-23.
36. Yu L., Ding G.F., He C., Sun L., Jiang Y., Zhu L. MicroRNA-424 is down-regulated in hepatocellular carcinoma and suppresses cell migration and invasion through c-Myb. PLoS ONE 2014, 9:e91661.
37. Oneyama C., Kito Y., Asai R., Ikeda J., Yoshida T., Okuzaki D., et al. MiR-424/503-mediated Rictor upregulation promotes tumor progression. PLoS ONE 2013, 8:e80300.
38. Chen B., Duan L., Yin G., Tan J., Jiang X. Simultaneously expressed miR-424 and miR-381 synergistically suppress the proliferation and survival of renal cancer cells - Cdc2 activity is up-regulated by targeting WEE1. Clinics (Sao Paulo) 2013, 68:825-833.
39. Long X.H., Mao J.H., Peng A.F., Zhou Y., Huang S.H., Liu Z.L. Tumor suppressive microRNA-424 inhibits osteosarcoma cell migration and invasion via targeting fatty acid synthase. Exp. Ther. Med 2013, 5:1048-1052.
40. Wu K., Hu G., He X., Zhou P., Li J., He B., et al. MicroRNA-424-5p suppresses the expression of SOCS6 in pancreatic cancer. Pathol. Oncol. Res 2013, 19:739-748.
41. Cheung T.H., Man K.N., Yu M.Y., Yim S.F., Siu N.S., Lo K.W., et al. Dysregulated microRNAs in the pathogenesis and progression of cervical neoplasm. Cell Cycle 2012, 11:2876-2884.
42. Ghosh G., Subramanian I.V., Adhikari N., Zhang X., Joshi H.P., Basi D., et al. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis. J. Clin. Invest 2010, 120:4141-4154.
43. Donnem T., Fenton C.G., Lonvik K., Berg T., Eklo K., Andersen S., et al. MicroRNA signatures in tumor tissue related to angiogenesis in non-small cell lung cancer. PLoS ONE 2012, 7:e29671.
44. Chamorro-Jorganes A., Araldi E., Penalva L.O., Sandhu D., Fernandez-Hernando C., Suarez Y. MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler. Thromb. Vasc. Biol 2011, 31:2595-2606.
45. Zhou R., Gong A.Y., Chen D., Miller R.E., Eischeid A.N., Chen X.M. Histone deacetylases and NF-kB signaling coordinate expression of CX3CL1 in epithelial cells in response to microbial challenge by suppressing miR-424 and miR-503. PLoS ONE 2013, 8:e65153.
46. Pallasch C.P., Patz M., Park Y.J., Hagist S., Eggle D., Claus R., et al. miRNA deregulation by epigenetic silencing disrupts suppression of the oncogene PLAG1 in chronic lymphocytic leukemia. Blood 2009, 114:3255-3264.
47. Faraoni I., Laterza S., Ardiri D., Ciardi C., Fazi F., Lo-Coco F. MiR-424 and miR-155 deregulated expression in cytogenetically normal acute myeloid leukaemia: correlation with NPM1 and FLT3 mutation status. J. Hematol. Oncol 2012, 5:26.
48. Linsley P.S., Schelter J., Burchard J., Kibukawa M., Martin M.M., Bartz S.R., et al. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol. Cell. Biol 2007, 27:2240-2252.
49. Seminario M.C., Precht P., Wersto R.P., Gorospe M., Wange R.L. PTEN expression in PTEN-null leukaemic T cell lines leads to reduced proliferation via slowed cell cycle progression. Oncogene 2003, 22:8195-8204.
50. Baccarani M., Deininger M.W., Rosti G., Hochhaus A., Soverini S., Apperley J.F., et al. European LeukemiaNet recommendations for the management of chronic myeloid leukemia: 2013. Blood 2013, 122:872-884.
51. Breccia M., Alimena G. Occurrence and current management of side effects in chronic myeloid leukemia patients treated frontline with tyrosine kinase inhibitors. Leuk. Res 2013, 37:713-720.
52. Cortes J.E., Baccarani M., Guilhot F., Druker B.J., Branford S., Kim D.W., et al. Phase III, randomized, open-label study of daily imatinib mesylate 400 mg versus 800 mg in patients with newly diagnosed, previously untreated chronic myeloid leukemia in chronic phase using molecular end points: tyrosine kinase inhibitor optimization and selectivity study. J. Clin. Oncol 2010, 28:424-430.
53. Gafter-Gvili A., Leader A., Gurion R., Vidal L., Ram R., Shacham-Abulafia A., et al. High-dose imatinib for newly diagnosed chronic phase chronic myeloid leukemia patients-systematic review and meta-analysis. Am. J. Hematol 2011, 86:657-662.
54. Johnson-Ansah H., Guilhot J., Rousselot P., Rea D., Legros L., Rigal-Huguet F., et al. Tolerability and efficacy of pegylated interferon-alpha-2a in combination with imatinib for patients with chronic-phase chronic myeloid leukemia. Cancer 2013, 119:4284-4289.