Oncogenic role of miR-155 in anaplastic large cell lymphoma lacking the t(2;5) translocation

J Pathol. 2015 Aug;236(4):445-56. doi: 10.1002/path.4539. Epub 2015 Apr 27.

Abstract

Anaplastic large cell lymphoma (ALCL) is a rare, aggressive, non-Hodgkin's lymphoma that is characterized by CD30 expression and disease onset in young patients. About half of ALCL patients bear the t(2;5)(p23;q35) translocation, which results in the formation of the nucleophosmin-anaplastic lymphoma tyrosine kinase (NPM-ALK) fusion protein (ALCL ALK(+)). However, little is known about the molecular features and tumour drivers in ALK-negative ALCL (ALCL ALK(-)), which is characterized by a worse prognosis. We found that ALCL ALK(-), in contrast to ALCL ALK(+), lymphomas display high miR-155 expression. Consistent with this, we observed an inverse correlation between miR-155 promoter methylation and miR-155 expression in ALCL. However, no direct effect of the ALK kinase on miR-155 levels was observed. Ago2 immunoprecipitation revealed miR-155 as the most abundant miRNA, and enrichment of target mRNAs C/EBPβ and SOCS1. To investigate its function, we over-expressed miR-155 in ALCL ALK(+) cell lines and demonstrated reduced levels of C/EBPβ and SOCS1. In murine engraftment models of ALCL ALK(-), we showed that anti-miR-155 mimics are able to reduce tumour growth. This goes hand-in-hand with increased levels of cleaved caspase-3 and high SOCS1 in these tumours, which leads to suppression of STAT3 signalling. Moreover, miR-155 induces IL-22 expression and suppresses the C/EBPβ target IL-8. These data suggest that miR-155 can act as a tumour driver in ALCL ALK(-) and blocking miR-155 could be therapeutically relevant. Original miRNA array data are to be found in the supplementary material (Table S1).

Keywords: ALCL; ALK kinase; IL-10; IL-21; IL-22; cytokines; miR-155.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaplastic Lymphoma Kinase
  • Animals
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • CCAAT-Enhancer-Binding Protein-beta / metabolism
  • Case-Control Studies
  • Caspase 3 / metabolism
  • Cell Line, Tumor
  • Chromosomes, Human, Pair 2*
  • Chromosomes, Human, Pair 5*
  • DNA Methylation
  • Gene Expression Regulation, Neoplastic
  • Genetic Therapy / methods
  • Humans
  • Lymphoma, Large-Cell, Anaplastic / genetics*
  • Lymphoma, Large-Cell, Anaplastic / metabolism
  • Lymphoma, Large-Cell, Anaplastic / pathology
  • Lymphoma, Large-Cell, Anaplastic / therapy
  • Mice, Inbred NOD
  • Mice, SCID
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Promoter Regions, Genetic
  • Receptor Protein-Tyrosine Kinases / deficiency
  • Receptor Protein-Tyrosine Kinases / genetics
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Suppressor of Cytokine Signaling Proteins / metabolism
  • Transfection
  • Translocation, Genetic*
  • Xenograft Model Antitumor Assays

Substances

  • AGO2 protein, human
  • Argonaute Proteins
  • CCAAT-Enhancer-Binding Protein-beta
  • CEBPB protein, human
  • MIRN155 microRNA, human
  • MicroRNAs
  • SOCS1 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins
  • ALK protein, human
  • Alk protein, mouse
  • Anaplastic Lymphoma Kinase
  • Receptor Protein-Tyrosine Kinases
  • CASP3 protein, human
  • Caspase 3