A novel dominant-negative mutant form of Epstein-Barr virus latent membrane protein-1 (LMP1) selectively and differentially impairs LMP1 and TNF signaling pathways

Oncogene. 2004 Apr 8;23(15):2681-93. doi: 10.1038/sj.onc.1207432.

Abstract

The latent membrane protein-1 (LMP1) is an integral membrane molecule expressed by Epstein-Barr virus (EBV) during viral latency and displays properties of a constitutively activated member of the TNF receptor family. LMP1 is required for B-cell or monocyte immortalization induced by EBV and is sufficient to transform rodent fibroblasts. Transforming potential of LMP1 is mediated by its cytoplasmic C-terminal domain, which activates various cellular signaling pathways including NFkappaB and JNK. In this report, we constructed mutants of LMP1 with preserved membrane spanning domain but mutated in the C-terminal domain and a second truncated C-terminal LMP1 fused to the enhanced green fluorescent protein. This latter mutant, termed LMP1-CT, impairs signaling by ectopic LMP1 as well as endogenous EBV-expressed wild-type (wt) LMP1. In contrast to dominant-negative mutants of LMP1 with preserved membrane spanning domains, LMP1-CT was unable to bind wt LMP1 to form an inactive complex. Its dominant-negative effects were due to binding and sequestration of LMP1 adapters TRAF2 and TRADD as assessed by coimmunoprecipitation experiments and confocal analysis. The effect was selective since LMP1-CT did not inhibit IL-1beta-induced signaling, whereas it impaired TNF-triggered NFkappaB and JNK signals without affecting TNF-induced apoptosis. In addition and in contrast to LMP1 constructs with membrane localization, LMP-CT did not display cytostatic properties in noninfected cells. Importantly, LMP1-CT inhibited survival induced by LMP1 in an EBV-transformed T-cell line expressing the type II viral latency commonly found in the majority of EBV-associated human tumors. These data demonstrate that LMP1-CT is a new tool to explore the differences between LMP1 and TNF signaling and may facilitate the design of molecules with potential therapeutic roles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Blotting, Western
  • Cell Division
  • Cell Line
  • Cell Line, Transformed
  • Cell Membrane / metabolism
  • Cell Survival
  • Dose-Response Relationship, Drug
  • Down-Regulation
  • Genes, Dominant
  • Genetic Vectors
  • Herpesvirus 4, Human / metabolism*
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • JNK Mitogen-Activated Protein Kinases*
  • Luciferases / metabolism
  • MAP Kinase Kinase 4
  • Microscopy, Confocal
  • Microscopy, Fluorescence
  • Mitogen-Activated Protein Kinase Kinases / metabolism
  • Models, Biological
  • Monocytes / metabolism
  • Mutation*
  • NF-kappa B / metabolism
  • Precipitin Tests
  • Protein Structure, Tertiary
  • Proteins / metabolism
  • Rats
  • Signal Transduction*
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / virology
  • TNF Receptor-Associated Factor 2
  • Transfection
  • Tumor Necrosis Factor-alpha / metabolism*
  • Viral Matrix Proteins / genetics*
  • Viral Matrix Proteins / metabolism*

Substances

  • EBV-associated membrane antigen, Epstein-Barr virus
  • NF-kappa B
  • Proteins
  • TNF Receptor-Associated Factor 2
  • Tumor Necrosis Factor-alpha
  • Viral Matrix Proteins
  • Intercellular Adhesion Molecule-1
  • Luciferases
  • JNK Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase 4
  • Mitogen-Activated Protein Kinase Kinases