miR-29b and miR-198 overexpression in CD8+ T cells of renal cell carcinoma patients down-modulates JAK3 and MCL-1 leading to immune dysfunction

J Transl Med. 2016 Apr 11:14:84. doi: 10.1186/s12967-016-0841-9.

Abstract

Background: Mammalian microRNAs (miR) regulate the expression of genes relevant for the development of adaptive and innate immunity against cancer. Since T cell dysfunction has previously been reported in patients with renal cell carcinoma (RCC; clear cell type), we aimed to analyze these immune cells for genetic and protein differences when compared to normal donor T cells freshly after isolation and 35 days after in vitro stimulation (IVS) with HLA-matched RCC tumor cells.

Methods: We investigated gene expression profiles of tumor-reactive CD8(+) T cells obtained from RCC patient and compared with their HLA-matched healthy sibling donors using a microarray approach. In addition, miRNAs analysis was performed in a validation cohort of peripheral blood CD8(+) T cells from 25 RCC patients compared to 15 healthy volunteers.

Results: We observed that CD8(+) T cells from RCC patients expressed reduced levels of anti-apoptotic and proliferation-associated gene products when compared with normal donor T cells both pre- and post-IVS. In particular, JAK3 and MCL-1 were down-regulated in patient CD8(+) T cells versus their normal counterparts, likely due to defective suppressor activity of miR-29b and miR-198 in RCC CD8(+) T cells. Indeed, specific inhibition of miR-29b or miR-198 in peripheral blood mononuclear cells (PBMCs) isolated from RCC patients, resulted in the up-regulation of JAK3 and MCL-1 proteins and significant improvement of cell survival in vitro.

Conclusions: Our results suggest that miR-29b and miR-198 dysregulation in RCC patient CD8(+) T cells is associated with dysfunctional immunity and foreshadow the development of miR-targeted therapeutics to correct such T cell defects in vivo.

Keywords: Apoptosis; CD8+ T cells; JAK3; MCL-1; Renal cell carcinoma; miRNA.

MeSH terms

  • Adult
  • Aged
  • Apoptosis / genetics
  • CD8-Positive T-Lymphocytes / metabolism*
  • Carcinoma, Renal Cell / genetics*
  • Carcinoma, Renal Cell / immunology*
  • Cell Separation
  • Down-Regulation / genetics*
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Janus Kinase 3 / genetics
  • Janus Kinase 3 / metabolism*
  • Kidney Neoplasms / genetics
  • Kidney Neoplasms / immunology
  • Leukocytes, Mononuclear / metabolism
  • Male
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • Myeloid Cell Leukemia Sequence 1 Protein / genetics
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism*
  • Phenotype
  • Tissue Donors
  • Transfection
  • Transplantation, Homologous
  • Tumor Cells, Cultured
  • Up-Regulation / genetics

Substances

  • MCL1 protein, human
  • MIRN198 microRNA, human
  • MIRN29a microRNA, human
  • MicroRNAs
  • Myeloid Cell Leukemia Sequence 1 Protein
  • JAK3 protein, human
  • Janus Kinase 3