DNA ligand designed to antagonize EBNA1 represses Epstein-Barr virus-induced immortalization

Cancer Sci. 2011 Dec;102(12):2221-30. doi: 10.1111/j.1349-7006.2011.02098.x. Epub 2011 Sep 30.

Abstract

Epstein-Barr virus (EBV) transforms human B lymphocytes into immortalized cells in vitro and is associated with various malignancies in vivo. EBNA1, which is expressed in the majority of EBV-infected cells, recognizes specific DNA sequences at the cis-acting latent origin of plasmid replication (oriP) element of the EBV genome. EBNA1 plays a critical role in the viral episome maintenance and transactivates viral transforming genes in latently infected cells. Therefore, DNA-targeting agents that can disrupt the EBNA1-oriP interaction will offer novel functional inhibitors of EBNA1. Pyrrole-imidazole polyamides, sequence-specific DNA ligands, can be designed to interfere with the binding of various transcriptional factors. Here, we synthesized pyrrole-imidazole polyamides targeting EBNA1-bound DNA sequences and developed an inhibitor for the EBNA1-oriP interaction. A pyrrole-imidazole polyamide, designated as DSE-3, bound adjacent to the EBNA1 recognition sequences located in the dyad symmetry element of oriP, and selectively inhibited EBNA1-oriP binding both in vitro and in vivo. DSE-3 also inhibited the proliferation of established lymphoblastoid cell lines by eradicating EBV episomes from the cells. In addition, DSE-3 repressed the expression of viral transforming genes after infecting human peripheral blood mononuclear cells with EBV and, as a consequence, inhibited EBV-mediated B-cell immortalization. These results suggest that EBNA1 functions will be an attractive pharmacological target for EBV-associated diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / physiology
  • B-Lymphocytes / virology*
  • Base Sequence
  • Binding Sites
  • Callithrix
  • Cell Line
  • Cell Transformation, Viral / drug effects*
  • DNA Replication
  • DNA, Viral / genetics
  • DNA, Viral / metabolism*
  • Epstein-Barr Virus Nuclear Antigens / metabolism*
  • Herpesvirus 4, Human / genetics
  • Herpesvirus 4, Human / metabolism*
  • Humans
  • Imidazoles / chemical synthesis
  • Imidazoles / metabolism
  • Imidazoles / pharmacology*
  • Leukocytes, Mononuclear / physiology
  • Leukocytes, Mononuclear / virology
  • Nylons / chemical synthesis
  • Nylons / metabolism
  • Nylons / pharmacology*
  • Pyrroles / chemical synthesis
  • Pyrroles / metabolism
  • Pyrroles / pharmacology*
  • Replication Origin / drug effects
  • Virus Replication

Substances

  • DNA, Viral
  • DSE-3 compound
  • Epstein-Barr Virus Nuclear Antigens
  • Imidazoles
  • Nylons
  • Pyrroles
  • EBV-encoded nuclear antigen 1