Nucleolin is important for Epstein-Barr virus nuclear antigen 1-mediated episome binding, maintenance, and transcription

Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):243-8. doi: 10.1073/pnas.1321800111. Epub 2013 Dec 16.

Abstract

Epstein-Barr virus (EBV) nuclear antigen 1 (EBNA1) is essential for EBV episome maintenance, replication, and transcription. These effects are mediated by EBNA1 binding to cognate oriP DNA, which comprise 20 imperfect copies of a 30-bp dyad symmetry enhancer and an origin for DNA replication. To identify cell proteins essential for these EBNA1 functions, EBNA1 associated cell proteins were immune precipitated and analyzed by liquid chromatography-tandem mass spectrometry. Nucleolin (NCL) was identified to be EBNA1 associated. EBNA1's N-terminal 100 aa and NCL's RNA-binding domains were critical for EBNA1/NCL interaction. Lentivirus shRNA-mediated NCL depletion substantially reduced EBNA1 recruitment to oriP DNA, EBNA1-dependent transcription of an EBV oriP luciferase reporter, and EBV genome maintenance in lymphoblastoid cell lines. NCL RNA-binding domain K429 was critical for ATP and EBNA1 binding. NCL overexpression increased EBNA1 binding to oriP and transcription, whereas NCL K429A was deficient. Moreover, NCL silencing impaired lymphoblastoid cell line growth. These experiments reveal a surprisingly critical role for NCL K429 in EBNA1 episome maintenance and transcription, which may be a target for therapeutic intervention.

Keywords: chromatin; lymphoma; nasopharyngeal carcinoma; oncogenic herpesvirus.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / chemistry
  • Binding Sites
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Chromatography, Liquid
  • DNA Replication
  • Epitopes / chemistry
  • Epstein-Barr Virus Nuclear Antigens / chemistry*
  • Epstein-Barr Virus Nuclear Antigens / physiology*
  • Gene Expression Regulation
  • Gene Silencing
  • Genome
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Immunoprecipitation
  • Luciferases / metabolism
  • Mass Spectrometry
  • Microscopy, Confocal
  • Nucleolin
  • Phosphoproteins / chemistry*
  • Phosphoproteins / physiology*
  • Plasmids / metabolism*
  • Protein Binding
  • Protein Structure, Tertiary
  • RNA-Binding Proteins / chemistry*
  • RNA-Binding Proteins / physiology*
  • Replication Origin
  • Transcription, Genetic*
  • Virus Replication

Substances

  • Epitopes
  • Epstein-Barr Virus Nuclear Antigens
  • Phosphoproteins
  • RNA-Binding Proteins
  • Green Fluorescent Proteins
  • Adenosine Triphosphate
  • Luciferases
  • EBV-encoded nuclear antigen 1