EBV-miR-BHRF1-2 targets PRDM1/Blimp1: potential role in EBV lymphomagenesis

Leukemia. 2016 Mar;30(3):594-604. doi: 10.1038/leu.2015.285. Epub 2015 Nov 4.

Abstract

PRDM1/Blimp1, a master regulator of B-cell terminal differentiation, has been identified as a tumor suppressor gene in aggressive lymphomas, including diffuse large B-cell lymphoma (DLBCL). It has been shown in DLBCL and Hodgkin lymphoma that PRDM1 is downregulated by cellular microRNAs. In this study, we identify the Epstein-Barr virus (EBV) microRNA (miRNA), EBV-miR-BHRF1-2, as a viral miRNA regulator of PRDM1. EBV-miR-BHRF1-2 repressed luciferase reporter activity by specific interaction with the seed region within the PRDM1 3' untranslated region. EBV-miR-BHRF1-2 inhibition upregulated PRDM1 protein expression in lymphoblastoid cell lines (LCL), supporting a role of miR-BHRF1-2 in PRDM1 downregulation in vivo. Discordance of PRDM1 messenger RNA and protein expressions is associated with high EBV-miR-BHRF1-2 levels in LCLs and primary post-transplant EBV-positive DLBCL. Enforced expression of PRDM1-induced apoptosis and cell cycle arrest in LCL cells. Inhibition of EBV-miR-BHRF1-2 negatively regulates cell cycle and decreases expression of SCARNA20, a small nucleolar RNA that is also downregulated by PRDM1 overexpression. The interaction between EBV-miR-BHRF1-2 and PRDM1 may be one of the mechanisms by which EBV-miR-BHRF1-2 promotes EBV lymphomagenesis. Our results support the potential of EBV-miR-BHRF1-2 as a therapeutic target in EBV-associated lymphoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions
  • Base Sequence
  • Binding Sites
  • Carcinogenesis / genetics*
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Cycle Checkpoints
  • Cell Line, Tumor
  • Epstein-Barr Virus Infections / genetics*
  • Epstein-Barr Virus Infections / metabolism
  • Epstein-Barr Virus Infections / pathology
  • Gene Expression Regulation, Neoplastic*
  • Herpesvirus 4, Human / genetics
  • Herpesvirus 4, Human / pathogenicity
  • Host-Pathogen Interactions
  • Humans
  • Lymphoma, Large B-Cell, Diffuse / genetics*
  • Lymphoma, Large B-Cell, Diffuse / metabolism
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Molecular Sequence Data
  • Paraffin Embedding
  • Positive Regulatory Domain I-Binding Factor 1
  • Protein Isoforms / antagonists & inhibitors
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • RNA, Small Nucleolar / genetics
  • RNA, Small Nucleolar / metabolism
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Signal Transduction
  • Tissue Fixation
  • Viral Proteins / antagonists & inhibitors
  • Viral Proteins / genetics*
  • Viral Proteins / metabolism

Substances

  • 3' Untranslated Regions
  • BHRF1 protein, Human herpesvirus 4
  • MicroRNAs
  • Protein Isoforms
  • RNA, Small Interfering
  • RNA, Small Nucleolar
  • Repressor Proteins
  • Viral Proteins
  • PRDM1 protein, human
  • Positive Regulatory Domain I-Binding Factor 1