Epstein-Barr virus nuclear antigen 3A partially coincides with EBNA3C genome-wide and is tethered to DNA through BATF complexes

Proc Natl Acad Sci U S A. 2015 Jan 13;112(2):554-9. doi: 10.1073/pnas.1422580112. Epub 2014 Dec 24.

Abstract

Epstein-Barr Virus (EBV) conversion of B-lymphocytes to Lymphoblastoid Cell Lines (LCLs) requires four EBV nuclear antigen (EBNA) oncoproteins: EBNA2, EBNALP, EBNA3A, and EBNA3C. EBNA2 and EBNALP associate with EBV and cell enhancers, up-regulate the EBNA promoter, MYC, and EBV Latent infection Membrane Proteins (LMPs), which up-regulate BCL2 to protect EBV-infected B-cells from MYC proliferation-induced cell death. LCL proliferation induces p16(INK4A) and p14(ARF)-mediated cell senescence. EBNA3A and EBNA3C jointly suppress p16(INK4A) and p14(ARF), enabling continuous cell proliferation. Analyses of the EBNA3A human genome-wide ChIP-seq landscape revealed 37% of 10,000 EBNA3A sites to be at strong enhancers; 28% to be at weak enhancers; 4.4% to be at active promoters; and 6.9% to be at weak and poised promoters. EBNA3A colocalized with BATF-IRF4, ETS-IRF4, RUNX3, and other B-cell Transcription Factors (TFs). EBNA3A sites clustered into seven unique groups, with differing B-cell TFs and epigenetic marks. EBNA3A coincidence with BATF-IRF4 or RUNX3 was associated with stronger EBNA3A ChIP-Seq signals. EBNA3A was at MYC, CDKN2A/B, CCND2, CXCL9/10, and BCL2, together with RUNX3, BATF, IRF4, and SPI1. ChIP-re-ChIP revealed complexes of EBNA3A on DNA with BATF. These data strongly support a model in which EBNA3A is tethered to DNA through a BATF-containing protein complexes to enable continuous cell proliferation.

Keywords: BATF; CDKN2A; EBNA3A; IRF4; RUNX3.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • B-Lymphocytes / metabolism
  • B-Lymphocytes / virology
  • Basic-Leucine Zipper Transcription Factors / metabolism*
  • Binding Sites / genetics
  • Cell Line
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL9 / genetics
  • Core Binding Factor Alpha 3 Subunit / metabolism
  • Cyclin D2 / genetics
  • DNA / genetics*
  • DNA / metabolism*
  • Enhancer Elements, Genetic
  • Epstein-Barr Virus Nuclear Antigens / genetics*
  • Epstein-Barr Virus Nuclear Antigens / metabolism
  • Genes, bcl-2
  • Genes, myc
  • Genes, p16
  • Genome, Human
  • Genome, Viral*
  • Herpesvirus 4, Human / genetics*
  • Herpesvirus 4, Human / pathogenicity*
  • Herpesvirus 4, Human / physiology
  • Host-Pathogen Interactions / genetics
  • Humans
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / metabolism
  • Interferon Regulatory Factors / metabolism
  • Promoter Regions, Genetic
  • Viral Proteins / genetics
  • Viral Proteins / metabolism

Substances

  • BATF protein, human
  • Basic-Leucine Zipper Transcription Factors
  • CCND2 protein, human
  • CXCL10 protein, human
  • CXCL9 protein, human
  • Chemokine CXCL10
  • Chemokine CXCL9
  • Core Binding Factor Alpha 3 Subunit
  • Cyclin D2
  • EBNA-2 protein, Human herpesvirus 4
  • EBNA-3A antigen
  • EBNA-3C, epstein-barr virus
  • EBNA-LP protein, Human herpesvirus 4
  • Epstein-Barr Virus Nuclear Antigens
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein
  • Interferon Regulatory Factors
  • RBPJ protein, human
  • Runx3 protein, human
  • Viral Proteins
  • interferon regulatory factor-4
  • DNA

Associated data

  • GEO/GSE59181