STAT5 induces miR-21 expression in cutaneous T cell lymphoma

Oncotarget. 2016 Jul 19;7(29):45730-45744. doi: 10.18632/oncotarget.10160.

Abstract

In cutaneous T cell lymphomas (CTCL), miR-21 is aberrantly expressed in skin and peripheral blood and displays anti-apoptotic properties in malignant T cells. It is, however, unclear exactly which cells express miR-21 and what mechanisms regulate miR-21. Here, we demonstrate miR-21 expression in situ in both malignant and reactive lymphocytes as well as stromal cells. qRT-PCR analysis of 47 patients with mycosis fungoides (MF) and Sezary Syndrome (SS) confirmed an increased miR-21 expression that correlated with progressive disease. In cultured malignant T cells miR-21 expression was inhibited by Tofacitinib (CP-690550), a clinical-grade JAK3 inhibitor. Chromatin immunoprecipitation (ChIP) analysis showed direct binding of STAT5 to the miR-21 promoter. Cytokine starvation ex vivo triggered a decrease in miR-21 expression, whereas IL-2 induced an increased miR-21 expression in primary SS T cells and cultured cytokine-dependent SS cells (SeAx). siRNA-mediated depletion of STAT5 inhibited constitutive- and IL-2-induced miR-21 expression in cytokine-independent and dependent T cell lines, respectively. IL-15 and IL-2 were more potent than IL-21 in inducing miR-21 expression in the cytokine-dependent T cells. In conclusion, we provide first evidence that miR-21 is expressed in situ in CTCL skin lesions, induced by IL-2 and IL-15 cytokines, and is regulated by STAT5 in malignant T cells. Thus, our data provide novel evidence for a pathological role of IL-2Rg cytokines in promoting expression of the oncogenic miR-21 in CTCL.

Keywords: IL-2; STAT5; cutaneous T-cell lymphoma (CTCL); in situ; miR-21.

MeSH terms

  • Female
  • Gene Expression Regulation, Neoplastic / physiology*
  • Humans
  • Lymphoma, T-Cell, Cutaneous / genetics
  • Lymphoma, T-Cell, Cutaneous / metabolism*
  • Male
  • MicroRNAs / biosynthesis*
  • MicroRNAs / genetics
  • STAT5 Transcription Factor / genetics
  • STAT5 Transcription Factor / metabolism*
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism*

Substances

  • MIRN21 microRNA, human
  • MicroRNAs
  • STAT5 Transcription Factor