Skip to main content

Advertisement

SpringerLink
Log in

While at Rome miRNA and TRAIL Do Whatever BCR-ABL Commands to Do

  • Review
  • Published:
Archivum Immunologiae et Therapiae Experimentalis Aims and scope

Abstract

It is a well-acclaimed fact that proteins expressed as a consequence of oncogenic fusions, mutations or amplifications can facilitate ectopic protein–protein interactions that re-wire signal dissemination pathways, in a manner that escalates malignancy. BCR-ABL-mediated signal transduction cascades in leukemic cells are assembled and modulated by a finely controlled network of protein–protein interactions, mediated by characteristic signaling domains and their respective binding motifs. BCR-ABL functions in a cell context-specific and cell type-specific manner to integrate signals that affect uncontrolled cellular proliferation. In this review, we draw attention to the recent progress made in outlining resistance against TRAIL-mediated apoptosis and diametrically opposed roles of miRNAs in BCR-ABL-positive leukemic cells. BCR-ABL governs carcinogenesis through well-organized web of antiapoptotic proteins and over-expressed oncomirs which target death receptors and pro-apoptotic genes. Set of oncomirs which inversely correlate with expression of TRAIL via suppression of SMAD is an important dimension which is gradually gaining attention of the researchers. Contrary to this, some current findings show a new role of BCR-ABL in nucleus with spotlight on apoptosis. It seems obvious that genetic heterogeneity of leukemias poses therapeutic challenges, and pharmacological agents that target components of the cancer promoting nano-machinery still need broad experimental validation to be considered competent as a component of the therapeutic arsenal for this group of diseases. Rapidly developing technologies are empowering us to explain the molecular “nature” of a patient and/or tumor and with this integration of personalized medicine, with maximized efficacy, cost effectiveness will hopefully improve survival chances of the patient.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abrahamsson AE, Geron I, Gotlib J et al (2009) Glycogen synthase kinase 3beta missplicing contributes to leukemia stem cell generation. Proc Natl Acad Sci USA 106:3925–3929

    PubMed  CAS  Google Scholar 

  • Acunzo M, Visone R, Romano G et al (2012) miR-130a targets MET and induces TRAIL-sensitivity in NSCLC by downregulating miR-221 and 222. Oncogene 31:634–642

    PubMed  CAS  Google Scholar 

  • Agirre X, Jiménez-Velasco A, San José-Enériz E et al (2008) Down-regulation of hsa-miR-10a in chronic myeloid leukemia CD34+ cells increases USF2-mediated cell growth. Mol Cancer Res 6:1830–1840

    PubMed  CAS  Google Scholar 

  • Audrito V, Vaisitti T, Rossi D et al (2011) Nicotinamide blocks proliferation and induces apoptosis of chronic lymphocytic leukemia cells through activation of the p53/miR-34a/SIRT1 tumor suppressor network. Cancer Res 71:4473–4483

    PubMed  CAS  Google Scholar 

  • Benito R, Lumbreras E, Abáigar M et al (2012) Imatinib therapy of chronic myeloid leukemia restores the expression levels of key genes for DNA damage and cell-cycle progression. Pharmacogenet Genomics 22:381–388

    PubMed  CAS  Google Scholar 

  • Bianchini L, Saâda E, Gjernes E et al (2011) Let-7 microRNA and HMGA2 levels of expression are not inversely linked in adipocytic tumors: analysis of 56 lipomas and liposarcomas with molecular cytogenetic data. Genes Chromosomes Cancer 50:442–455

    PubMed  CAS  Google Scholar 

  • Boulos N, Mulder HL, Calabrese CR et al (2011) Chemotherapeutic agents circumvent emergence of dasatinib-resistant BCR-ABL kinase mutations in a precise mouse model of Philadelphia chromosome-positive acute lymphoblastic leukemia. Blood 117:3585–3595

    PubMed  CAS  Google Scholar 

  • Bousquet M, Harris MH, Zhou B et al (2010) MicroRNA miR-125b causes leukemia. Proc Natl Acad Sci USA 107:21558–21563

    PubMed  CAS  Google Scholar 

  • Bueno MJ, Pérez de Castro I, Gómez de Cedrón M et al (2008) Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 13:496–506

    PubMed  CAS  Google Scholar 

  • Carayol N, Vakana E, Sassano A et al (2010) Critical roles for mTORC2- and rapamycin-insensitive mTORC1-complexes in growth and survival of BCR-ABL-expressing leukemic cells. Proc Natl Acad Sci USA 107:12469–12474

    PubMed  CAS  Google Scholar 

  • Cárdenas MG, Blank VC, Marder MN et al (2012) 2′-Nitroflavone induces apoptosis and modulates mitogen-activated protein kinase pathways in human leukaemia cells. Anticancer Drugs 23:815–826

    PubMed  Google Scholar 

  • Casnici C, Volpe G, Crotta K et al (2012) Immunologic evaluation of peptides derived from BCR/ABL-out-of-frame fusion protein in HLA A2.1 transgenic mice. J Immunother 35:321–328

    PubMed  CAS  Google Scholar 

  • Castro Alves C, Terziyska N, Grunert M et al (2012) Leukemia-initiating cells of patient-derived acute lymphoblastic leukemia xenografts are sensitive toward TRAIL. Blood 119:4224–4227

    PubMed  Google Scholar 

  • Chandra P, Luthra R, Zuo Z et al (2010) Acute myeloid leukemia with t(9;11)(p21–22;q23): common properties of dysregulated ras pathway signaling and genomic progression characterize de novo and therapy-related cases. Am J Clin Pathol 133:686–693

    PubMed  Google Scholar 

  • Chen CI, Koschmieder S, Kerstiens L et al (2012) NK cells are dysfunctional in human chronic myelogenous leukemia before and on imatinib treatment and in BCR-ABL-positive mice. Leukemia 26:465–474

    PubMed  CAS  Google Scholar 

  • Chung GE, Yoon JH, Myung SJ et al (2010) High expression of microRNA-15b predicts a low risk of tumor recurrence following curative resection of hepatocellular carcinoma. Oncol Rep 23:113–119

    PubMed  CAS  Google Scholar 

  • Cramer K, Nieborowska-Skorska M, Koptyra M et al (2008) BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate single-strand annealing, an unfaithful DNA double-strand break repair. Cancer Res 68:6884–6888

    PubMed  CAS  Google Scholar 

  • Crosby ME, Kulshreshtha R, Ivan M et al (2009) MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 69:1221–1229

    PubMed  CAS  Google Scholar 

  • D’Angelo D, Palmieri D, Mussnich P et al (2012) Altered microRNA expression profile in human pituitary GH adenomas: down-regulation of miRNA targeting HMGA1, HMGA2, and E2F1. J Clin Endocrinol Metab 97:E1128–E1138

    PubMed  Google Scholar 

  • De Carvalho DD, Binato R, Pereira WO et al (2011) BCR-ABL-mediated upregulation of PRAME is responsible for knocking down TRAIL in CML patients. Oncogene 30:223–233

    PubMed  Google Scholar 

  • De Vito C, Riggi N, Suvà ML et al (2011) Let-7a is a direct EWS-FLI-1 target implicated in Ewing’s sarcoma development. PLoS ONE 6:e23592

    PubMed  Google Scholar 

  • Dixon AS, Kakar M, Schneider KM et al (2009) Controlling subcellular localization to alter function: Sending oncogenic Bcr-Abl to the nucleus causes apoptosis. J Control Release 140:245–249

    PubMed  CAS  Google Scholar 

  • Dixon AS, Constance JE, Tanaka T et al (2011) Changing the subcellular location of the oncoprotein Bcr-Abl using rationally designed capture motifs. Pharm Res 29:1098–1109

    PubMed  Google Scholar 

  • Dixon AS, Miller GD, Bruno BJ et al (2012) Improved coiled-coil design enhances interaction with Bcr-Abl and induces apoptosis. Mol Pharm 9:187–195

    PubMed  CAS  Google Scholar 

  • Dong F, Lou D (2012) MicroRNA-34b/c suppresses uveal melanoma cell proliferation and migration through multiple targets. Mol Vis 18:537–546

    PubMed  CAS  Google Scholar 

  • Duan Z, Choy E, Harmon D et al (2011) MicroRNA-199a-3p is downregulated in human osteosarcoma and regulates cell proliferation and migration. Mol Cancer Ther 10:1337–1345

    PubMed  CAS  Google Scholar 

  • Elf S, Blevins D, Jin L et al (2011) p90RSK2 is essential for FLT3-ITD- but dispensable for BCR-ABL-induced myeloid leukemia. Blood 117:6885–6894

    PubMed  CAS  Google Scholar 

  • Faber J, Gregory RI, Armstrong SA (2008) Linking miRNA regulation to BCR-ABL expression: the next dimension. Cancer Cell 13:467–469

    PubMed  CAS  Google Scholar 

  • Falinski R, Nieborowska-Skorska M, Skorski T (2012) BCR-ABL1 kinase facilitates localization of acetylated histones 3 and 4 on DNA double-strand breaks. Leuk Res 36:241–244

    PubMed  CAS  Google Scholar 

  • Farooqi AA, Fayyaz S, Bhatti S et al (2011) Towards TRAIL to silencing of SMURF and NEDD4: FLIP is flopped. J Exp Integr Med 1:111–116

    Google Scholar 

  • Flamant S, Richie W, Guilhot J et al (2010) Micro-RNA response to imatinib mesylate in patients with chronic myeloid leukemia. Haematologica 95:1325–1333

    PubMed  CAS  Google Scholar 

  • Fornari F, Milazzo M, Chieco P et al (2010) MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 70:5184–5193

    PubMed  CAS  Google Scholar 

  • Fujishita T, Aoki K, Lane HA et al (2008) Inhibition of the mTORC1 pathway suppresses intestinal polyp formation and reduces mortality in ApcDelta716 mice. Proc Natl Acad Sci USA 105:13544–13549

    PubMed  CAS  Google Scholar 

  • Garofalo M, Quintavalle C, Di Leva G et al (2008) MicroRNA signatures of TRAIL resistance in human non-small cell lung cancer. Oncogene 27:3845–3855

    PubMed  CAS  Google Scholar 

  • Garofalo M, Di Leva G, Romano G et al (2009) miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 16:498–509

    PubMed  CAS  Google Scholar 

  • Garofalo M, Romano G, Di Leva G et al (2011) EGFR and MET receptor tyrosine kinase-altered microRNA expression induces tumorigenesis and gefitinib resistance in lung cancers. Nat Med 18:74–82

    PubMed  Google Scholar 

  • Geraldo MV, Yamashita AS, Kimura ET (2011) MicroRNA miR-146b-5p regulates signal transduction of TGF-β by repressing SMAD4 in thyroid cancer. Oncogene 31:1910–1922

    PubMed  Google Scholar 

  • Giallongo C, Tibullo D, La Cava P et al (2011) BRIT1/MCPH1 expression in chronic myeloid leukemia and its regulation of the G2/M checkpoint. Acta Haematol 126:205–210

    PubMed  CAS  Google Scholar 

  • Gniot M, Wasilewska EM, Lewandowski K (2012) K356dup—an in-frame insertion in the BCR-ABL gene in an imatinib-resistant chronic myeloid leukemia. Int J Lab Hematol. doi:10.1111/j.1751-553X.2012.01443.x

  • Gregory MA, Phang TL, Neviani P et al (2010) Wnt/Ca2+/NFAT signaling maintains survival of Ph+ leukemia cells upon inhibition of Bcr-Abl. Cancer Cell 18:74–87

    PubMed  CAS  Google Scholar 

  • Hao J, Zhang S, Zhou Y et al (2011) MicroRNA 483–3p suppresses the expression of DPC4/Smad4 in pancreatic cancer. FEBS Lett 585:207–213

    PubMed  CAS  Google Scholar 

  • Hatakeyama H, Cheng H, Wirth P et al (2010) Regulation of heparin-binding EGF-like growth factor by miR-212 and acquired cetuximab-resistance in head and neck squamous cell carcinoma. PLoS ONE 5:e12702

    PubMed  Google Scholar 

  • Holdenrieder S, Kolligs FT, Braess J et al (2012) Nature and dynamics of nucleosome release from neoplastic and non-neoplastic cells. Anticancer Res 32:2179–2183

    PubMed  CAS  Google Scholar 

  • Hu Y, Chen Y, Douglas L et al (2009) beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABL-induced chronic myeloid leukemia. Leukemia 23:109–116

    PubMed  CAS  Google Scholar 

  • Huang ZL, Gao M, Ji MS et al (2012) TAT-CC fusion protein depresses the oncogenicity of BCR-ABL in vitro and in vivo through interrupting its oligomerization. Amino Acids [Epub ahead of print]

  • Imam JS, Buddavarapu K, Lee-Chang JS et al (2010) MicroRNA-185 suppresses tumor growth and progression by targeting the Six1 oncogene in human cancers. Oncogene 29:4971–4979

    PubMed  CAS  Google Scholar 

  • Incoronato M, Garofalo M, Urso L et al (2010) miR-212 increases tumor necrosis factor-related apoptosis-inducing ligand sensitivity in non-small cell lung cancer by targeting the antiapoptotic protein PED. Cancer Res 70:3638–3646

    PubMed  CAS  Google Scholar 

  • Inoki K, Ouyang H, Zhu T et al (2006) TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126:955–568

    Google Scholar 

  • Joha S, Nugues AL, Hétuin D et al (2012) GILZ inhibits the mTORC2/AKT pathway in BCR-ABL(+) cells. Oncogene 31:1419–1430

    PubMed  CAS  Google Scholar 

  • Johnson SM, Grosshans H, Shingara J et al (2005) RAS is regulated by the let-7 microRNA family. Cell 120:635–647

    PubMed  CAS  Google Scholar 

  • Khamaisie H, Sussan S, Tal M et al (2011) Oleic acid is the active component in the mushroom Daedalea gibbosa inhibiting Bcr-Abl kinase autophosphorylation activity. Anticancer Res 31:177–183

    PubMed  CAS  Google Scholar 

  • Kim S, Lee UJ, Kim MN et al (2008) MicroRNA miR-199a* regulates the MET proto-oncogene and the downstream extracellular signal-regulated kinase 2 (ERK2). J Biol Chem 283:18158–18166

    PubMed  CAS  Google Scholar 

  • Kim HB, Kim MJ, Lee SH et al (2012) a novel SIRT1 inhibitor, sensitizes TRAIL-resistant human leukemic K562 cells to TRAIL-induced apoptosis. Biochem Pharmacol 84:402–410

    PubMed  CAS  Google Scholar 

  • Koptyra M, Stoklosa T, Hoser G et al (2011) Monoubiquitinated Fanconi anemia D2 (FANCD2-Ub) is required for BCR-ABL1 kinase-induced leukemogenesis. Leukemia 25:1259–1267

    PubMed  CAS  Google Scholar 

  • Kuroda I, Inukai T, Zhang X et al (2012) BCR-ABL regulates death receptor expression for TNF-related apoptosis-inducing ligand (TRAIL) in Philadelphia chromosome-positive leukemia. Oncogene. doi:10.1038/onc.2012.186

  • Liu P, Wilson MJ (2012) miR-520c and miR-373 upregulate MMP9 expression by targeting mTOR and SIRT1, and activate the Ras/Raf/MEK/Erk signaling pathway and NF-κB factor in human fibrosarcoma cells. J Cell Physiol 227:867–876

    PubMed  CAS  Google Scholar 

  • Liu Z, Lu CL, Cui LP et al (2012) MicroRNA-146a modulates TGF-β1-induced phenotypic differentiation in human dermal fibroblasts by targeting SMAD4. Arch Dermatol Res 304:195–202

    PubMed  CAS  Google Scholar 

  • Lopotová T, Záčková M, Klamová H et al (2011) MicroRNA-451 in chronic myeloid leukemia: miR-451-BCR-ABL regulatory loop? Leuk Res 35:974–977

    PubMed  Google Scholar 

  • Lu Q, Lu C, Zhou GP et al (2010) MicroRNA-221 silencing predisposed human bladder cancer cells to undergo apoptosis induced by TRAIL. Urol Oncol 28:635–641

    PubMed  CAS  Google Scholar 

  • Machová Poláková K, Lopotová T et al (2011) Expression patterns of microRNAs associated with CML phases and their disease related targets. Mol Cancer 10:41

    PubMed  Google Scholar 

  • Majsterek I, Sliwinski T, Poplawski T et al (2006) Imatinib mesylate (STI571) abrogates the resistance to doxorubicin in human K562 chronic myeloid leukemia cells by inhibition of BCR/ABL kinase-mediated DNA repair. Mutat Res 603:74–82

    PubMed  CAS  Google Scholar 

  • Mancini M, Petta S, Martinelli G et al (2010) RAD 001 (everolimus) prevents mTOR and Akt late re-activation in response to imatinib in chronic myeloid leukemia. J Cell Biochem 109:320–328

    PubMed  CAS  Google Scholar 

  • Mancini M, Leo E, Aluigi M et al (2012a) Gadd45a transcriptional induction elicited by the Aurora kinase inhibitor MK-0457 in Bcr-Abl-expressing cells is driven by Oct-1 transcription factor. Leuk Res 36:1028–1034

    PubMed  CAS  Google Scholar 

  • Mancini M, Veljkovic N, Leo E et al (2012b) Cytoplasmatic compartmentalization by BCR-ABL promotes TET2 loss-of-function in chronic myeloid leukemia. J Cell Biochem 113:2765–2774

    PubMed  CAS  Google Scholar 

  • Martin SE, Sausen M, Joseph A et al (2012) Identification of a HMGA2-EFCAB6 gene rearrangement following next-generation sequencing in a patient with a t(12;22)(q14.3;q13.2) and JAK2V617F-positive myeloproliferative neoplasm. Cancer Genet 205:295–303

    PubMed  CAS  Google Scholar 

  • Mineo M, Garfield SH, Taverna S et al (2012) Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis 15:33–45

    PubMed  CAS  Google Scholar 

  • Mott JL, Kurita S, Cazanave SC et al (2010) Transcriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NF-kappaB. J Cell Biochem 110:1155–1164

    PubMed  CAS  Google Scholar 

  • Nagao R, Ashihara E, Kimura S et al (2011) Growth inhibition of imatinib-resistant CML cells with the T315I mutation and hypoxia-adaptation by AV65–a novel Wnt/β-catenin signaling inhibitor. Cancer Lett 312:91–100

    PubMed  CAS  Google Scholar 

  • Nguyen T, Dai Y, Attkisson E et al (2011) HDAC inhibitors potentiate the activity of the BCR/ABL kinase inhibitor KW-2449 in imatinib-sensitive or -resistant BCR/ABL+ leukemia cells in vitro and in vivo. Clin Cancer Res 17:3219–3232

    PubMed  CAS  Google Scholar 

  • Nieborowska-Skorska M, Stoklosa T, Datta M et al (2006) ATR-Chk1 axis protects BCR/ABL leukemia cells from the lethal effect of DNA double-strand breaks. Cell Cycle 5:994–1000

    PubMed  CAS  Google Scholar 

  • Nimmanapalli R, Porosnicu M, Nguyen D et al (2001) Cotreatment with STI-571 enhances tumor necrosis factor alpha-related apoptosis-inducing ligand (TRAIL or apo-2L)-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Clin Cancer Res 7:350–357

    PubMed  CAS  Google Scholar 

  • Nobusawa S, Yokoo H, Hirato J et al (2012) Analysis of chromosome 19q13.42 amplification in embryonal brain tumors with ependymoblastic multilayered rosettes. Brain Pathol 22:689–697

    PubMed  CAS  Google Scholar 

  • Okabe S, Tauchi T, Tanaka Y et al (2012) Effects of the hedgehog inhibitor GDC-0449, alone or in combination with dasatinib, on BCR-ABL-positive leukemia cells. Stem Cells Dev 21:2939–2948

    PubMed  CAS  Google Scholar 

  • Oneyama C, Ikeda J, Okuzaki D et al (2011) MicroRNA-mediated downregulation of mTOR/FGFR3 controls tumor growth induced by Src-related oncogenic pathways. Oncogene 30:3489–3501

    PubMed  CAS  Google Scholar 

  • Ovcharenko D, Kelnar K, Johnson C et al (2007) Genome-scale microRNA and small interfering RNA screens identify small RNA modulators of TRAIL-induced apoptosis pathway. Cancer Res 67:10782–10788

    PubMed  CAS  Google Scholar 

  • Park SJ, Kim MJ, Kim HB et al (2009a) Sensitization of imatinib-resistant CML cells to TRAIL-induced apoptosis is mediated through down-regulation of Bcr-Abl as well as c-FLIP. Biochem J 420:73–81

    PubMed  CAS  Google Scholar 

  • Park SJ, Kim MJ, Kim HB et al (2009b) Cotreatment with apicidin overcomes TRAIL resistance via inhibition of Bcr-Abl signaling pathway in K562 leukemia cells. Exp Cell Res 315:1809–1918

    PubMed  CAS  Google Scholar 

  • Peng Z, Yuan Y, Li YJ et al (2012) Targeting BCR tyrosine177 site with novel SH2-DED causes selective leukemia cell death in vitro and in vivo. Int J Biochem Cell Biol 44:861–868

    PubMed  CAS  Google Scholar 

  • Pizzatti L, Binato R, Cofre J et al (2010) SUZ12 is a candidate target of the non-canonical WNT pathway in the progression of chronic myeloid leukemia. Genes Chromosomes Cancer 49:107–118

    PubMed  CAS  Google Scholar 

  • Poplawski T, Blasiak J (2010) BCR/ABL downregulates DNA-PK(CS)-dependent and upregulates backup non-homologous end joining in leukemic cells. Mol Biol Rep 37:2309–2315

    PubMed  CAS  Google Scholar 

  • Prabhu S, Saadat D, Zhang M et al (2007) A novel mechanism for Bcr-Abl action: Bcr-Abl-mediated induction of the eIF4F translation initiation complex and mRNA translation. Oncogene 26:1188–1200

    PubMed  CAS  Google Scholar 

  • Preyer M, Vigneri P, Wang JY (2011) Interplay between kinase domain autophosphorylation and F-actin binding domain in regulating imatinib sensitivity and nuclear import of BCR-ABL. PLoS ONE 6:e17020

    PubMed  CAS  Google Scholar 

  • Razumilava N, Bronk SF, Smoot RL et al (2012) miR-25 targets TNF-related apoptosis inducing ligand (TRAIL) death receptor-4 and promotes apoptosis resistance in cholangiocarcinoma. Hepatology 55:465–475

    PubMed  CAS  Google Scholar 

  • Reins J, Mossner M, Neumann M et al (2010) Transcriptional down-regulation of the Wnt antagonist SFRP1 in haematopoietic cells of patients with different risk types of MDS. Leuk Res 34:1610–1616

    PubMed  CAS  Google Scholar 

  • Riggi N, Suvà ML, De Vito C et al (2010) EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes Dev 24:916–932

    PubMed  CAS  Google Scholar 

  • Rink L, Slupianek A, Stoklosa T et al (2007) Enhanced phosphorylation of Nbs1, a member of DNA repair/checkpoint complex Mre11-RAD50-Nbs1, can be targeted to increase the efficacy of imatinib mesylate against BCR/ABL-positive leukemia cells. Blood 110:651–660

    PubMed  CAS  Google Scholar 

  • Rippe V, Dittberner L, Lorenz VN et al (2010) The two stem cell microRNA gene clusters C19MC and miR-371-3 are activated by specific chromosomal rearrangements in a subgroup of thyroid adenomas. PLoS ONE 5:e9485

    PubMed  Google Scholar 

  • Salles D, Mencalha AL, Ireno IC et al (2011) BCR-ABL stimulates mutagenic homologous DNA double-strand break repair via the DNA-end-processing factor CtIP. Carcinogenesis 32:27–34

    PubMed  CAS  Google Scholar 

  • Sallmyr A, Tomkinson AE, Rassool FV (2008) Up-regulation of WRN and DNA ligase IIIalpha in chronic myeloid leukemia: consequences for the repair of DNA double-strand breaks. Blood 112:1413–1423

    PubMed  CAS  Google Scholar 

  • Schemionek M, Spieker T, Kerstiens L et al (2012) Leukemic spleen cells are more potent than bone marrow-derived cells in a transgenic mouse model of CML. Leukemia 26:1030–1037

    PubMed  CAS  Google Scholar 

  • Scholl V, Hassan R, Zalcberg IR (2012) miRNA-451: a putative predictor marker of Imatinib therapy response in chronic myeloid leukemia. Leuk Res 36:119–121

    PubMed  CAS  Google Scholar 

  • Schotte D, Lange-Turenhout EA, Stumpel DJ et al (2010) Expression of miR-196b is not exclusively MLL-driven but is especially linked to activation of HOXA genes in pediatric acute lymphoblastic leukemia. Haematologica 95:1675–1682

    PubMed  CAS  Google Scholar 

  • Schürch C, Riether C, Matter MS et al (2012) CD27 signaling on chronic myelogenous leukemia stem cells activates Wnt target genes and promotes disease progression. J Clin Invest 122:624–638

    PubMed  Google Scholar 

  • Sercan HO, Pehlivan M, Simsek O et al (2007) Induction of apoptosis increases expression of non-canonical WNT genes in myeloid leukemia cell lines. Oncol Rep 18:1563–1569

    PubMed  CAS  Google Scholar 

  • Sliwinski T, Czechowska A, Szemraj J et al (2008) STI571 reduces NER activity in BCR/ABL-expressing cells. Mutat Res 654:162–167

    PubMed  CAS  Google Scholar 

  • Slupianek A, Dasgupta Y, Ren SY et al (2011a) Targeting RAD51 phosphotyrosine-315 to prevent unfaithful recombination repair in BCR-ABL1 leukemia. Blood 118:1062–1068

    PubMed  CAS  Google Scholar 

  • Slupianek A, Poplawski T, Jozwiakowski SK et al (2011b) BCR/ABL stimulates WRN to promote survival and genomic instability. Cancer Res 71:842–851

    PubMed  CAS  Google Scholar 

  • Stumpel DJ, Schotte D, Lange-Turenhout EA et al (2011) Hypermethylation of specific microRNA genes in MLL-rearranged infant acute lymphoblastic leukemia: major matters at a micro scale. Leukemia 25:429–439

    PubMed  CAS  Google Scholar 

  • Sudbery I, Enright AJ, Fraser AG et al (2010) Systematic analysis of off-target effects in an RNAi screen reveals microRNAs affecting sensitivity to TRAIL-induced apoptosis. BMC Genomics 11:175

    PubMed  Google Scholar 

  • Sun J, McKallip RJ et al (2011) Plumbagin treatment leads to apoptosis in human K562 leukemia cells through increased ROS and elevated TRAIL receptor expression. Leuk Res 35:1402–1408

    PubMed  CAS  Google Scholar 

  • Suresh S, McCallum L, Lu W et al (2011) MicroRNAs 130a/b are regulated by BCR-ABL and downregulate expression of CCN3 in CML. J Cell Commun Signal 5:183–191

    PubMed  Google Scholar 

  • Tan S, Li R, Ding K et al (2011) miR-198 inhibits migration and invasion of hepatocellular carcinoma cells by targeting the HGF/c-MET pathway. FEBS Lett 585:2229–2234

    PubMed  CAS  Google Scholar 

  • ten Cate B, Bremer E, de Bruyn M et al (2009) A novel AML-selective TRAIL fusion protein that is superior to Gemtuzumab Ozogamicin in terms of in vitro selectivity, activity and stability. Leukemia 23:1389–1397

    PubMed  Google Scholar 

  • Tobin LA, Robert C, Rapoport AP et al (2012) Targeting abnormal DNA double-strand break repair in tyrosine kinase inhibitor-resistant chronic myeloid leukemias. Oncogene. doi:10.1038/onc.2012.203

  • Turrini E, Haenisch S, Laechelt S et al (2012) MicroRNA profiling in K-562 cells under imatinib treatment: influence of miR-212 and miR-328 on ABCG2 expression. Pharmacogenet Genomics 22:198–205

    PubMed  CAS  Google Scholar 

  • Uesugi A, Kozaki K, Tsuruta T et al (2011) The tumor suppressive microRNA miR-218 targets the mTOR component Rictor and inhibits AKT phosphorylation in oral cancer. Cancer Res 71:5765–5778

    PubMed  CAS  Google Scholar 

  • Uno K, Inukai T, Kayagaki N et al (2003) TNF-related apoptosis-inducing ligand (TRAIL) frequently induces apoptosis in Philadelphia chromosome-positive leukemia cells. Blood 101:3658–3667

    PubMed  CAS  Google Scholar 

  • Vakana E, Sassano A, Platanias LC (2010) Induction of autophagy by dual mTORC1-mTORC2 inhibition in BCR-ABL-expressing leukemic cells. Autophagy 6:966–967

    PubMed  Google Scholar 

  • Valeri A, Alonso-Ferrero ME, Río P et al (2010) Bcr/Abl interferes with the Fanconi anemia/BRCA pathway: implications in the chromosomal instability of chronic myeloid leukemia cells. PLoS ONE 5:e15525

    PubMed  CAS  Google Scholar 

  • Venturini L, Battmer K, Castoldi M et al (2007) Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34 + cells. Blood 109:4399–4405

    PubMed  CAS  Google Scholar 

  • Vigneri P, Wang JY (2001) Induction of apoptosis in chronic myelogenous leukemia cells through nuclear entrapment of BCR-ABL tyrosine kinase. Nat Med 7:228–234

    PubMed  CAS  Google Scholar 

  • Wang X, Hulshizer RL, Erickson-Johnson MR et al (2009) Identification of novel HMGA2 fusion sequences in lipoma: evidence that deletion of let-7 miRNA consensus binding site 1 in the HMGA2 3′ UTR is not critical for HMGA2 transcriptional upregulation. Genes Chromosomes Cancer 48:673–678

    PubMed  CAS  Google Scholar 

  • Wang Z, Yuan H, Roth M et al (2012) SIRT1 deacetylase promotes acquisition of genetic mutations for drug resistance in CML cells. Oncogene. doi:10.1038/onc.2012.83

  • Wu ZS, Wu Q, Wang CQ et al (2011) miR-340 inhibition of breast cancer cell migration and invasion through targeting of oncoprotein c-Met. Cancer 117:2842–2852

    PubMed  CAS  Google Scholar 

  • Wu Y, Chen C, Sun X et al (2012) Cyclin-dependent kinase 7/9 inhibitor SNS-032 abrogates FIP1-like-1 platelet-derived growth factor receptor α and bcr-abl oncogene addiction in malignant hematologic cells. Clin Cancer Res 18:1966–1978

    PubMed  CAS  Google Scholar 

  • Xiao B, Zhu ED, Li N et al (2012) Increased miR-146a in gastric cancer directly targets SMAD4 and is involved in modulating cell proliferation and apoptosis. Oncol Rep 27:559–566

    PubMed  CAS  Google Scholar 

  • Zhang C, Wang G, Kang C et al (2009) Up-regulation of p27(kip1) by miR-221/222 antisense oligonucleotides enhances the radiosensitivity of U251 glioblastoma. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 26:634–638

    PubMed  CAS  Google Scholar 

  • Zhang J, Huang S, Zhang H et al (2010) Targeted knockdown of Bcl2 in tumor cells using a synthetic TRAIL 3′-UTR microRNA. Int J Cancer 126:2229–2239

    PubMed  CAS  Google Scholar 

  • Zhang J, Yang WH, Yang XD et al (2012a) Establishment and identification of cml model via injection of k562 cells into the murine caudal vein. Zhongguo Shi Yan Xue Ye Xue Za Zhi 20:773–776

    PubMed  CAS  Google Scholar 

  • Zhang X, Inukai T, Hirose Ket al (2012b) Oncogenic fusion E2A-HLF sensitizes t(17;19)-positive acute lymphoblastic leukemia to TRAIL-mediated apoptosis by upregulating the expression of death receptors. Leukemia. doi:10.1038/leu.2012.139

  • Zhong H, Wang HR, Yang S et al (2010) Targeting Smad4 links microRNA-146a to the TGF-beta pathway during retinoid acid induction in acute promyelocytic leukemia cell line. Int J Hematol 92:129–135

    PubMed  CAS  Google Scholar 

  • Zhou AD, Diao LT, Xu H et al (2012) β-Catenin/LEF1 transactivates the microRNA-371-373 cluster that modulates the Wnt/β-catenin-signaling pathway. Oncogene 31:2968–2978

    PubMed  CAS  Google Scholar 

  • Zhu YF, Wang YZ, Meng FY (2012) TEC Promoter Mediates P210(bcr/abl) gene expression in BaF3 cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 20:769–772

    PubMed  CAS  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Laboratory for Translational Oncology and Personalized Medicine, Rashid Latif Medical College (RLMC), 35 km Ferozepur Road, Lahore, Pakistan

    Ammad Ahmad Farooqi

  2. IMBB, The University of Lahore, Lahore, Pakistan

    Ali Nawaz, Zeeshan Javed & Shahzad Bhatti

  3. Institute of Biomedical and Genetic Engineering, Islamabad, Pakistan

    Muhammad Ismail

Authors
  1. Ammad Ahmad Farooqi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Nawaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zeeshan Javed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shahzad Bhatti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Ismail
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ammad Ahmad Farooqi.

About this article

Cite this article

Farooqi, A.A., Nawaz, A., Javed, Z. et al. While at Rome miRNA and TRAIL Do Whatever BCR-ABL Commands to Do. Arch. Immunol. Ther. Exp. 61, 59–74 (2013). https://doi.org/10.1007/s00005-012-0204-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00005-012-0204-z

Keywords

Search

Navigation