Mouse model for acute Epstein-Barr virus infection

Proc Natl Acad Sci U S A. 2016 Nov 29;113(48):13821-13826. doi: 10.1073/pnas.1616574113. Epub 2016 Nov 16.

Abstract

Epstein-Barr Virus (EBV) infects human B cells and drives them into continuous proliferation. Two key viral factors in this process are the latent membrane proteins LMP1 and LMP2A, which mimic constitutively activated CD40 receptor and B-cell receptor signaling, respectively. EBV-infected B cells elicit a powerful T-cell response that clears the infected B cells and leads to life-long immunity. Insufficient immune surveillance of EBV-infected B cells causes life-threatening lymphoproliferative disorders, including mostly germinal center (GC)-derived B-cell lymphomas. We have modeled acute EBV infection of naive and GC B cells in mice through timed expression of LMP1 and LMP2A. Although lethal when induced in all B cells, induction of LMP1 and LMP2A in just a small fraction of naive B cells initiated a phase of rapid B-cell expansion followed by a proliferative T-cell response, clearing the LMP-expressing B cells. Interfering with T-cell activity prevented clearance of LMP-expressing B cells. This was also true for perforin deficiency, which in the human causes a life-threatening EBV-related immunoproliferative syndrome. LMP expression in GC B cells impeded the GC reaction but, upon loss of T-cell surveillance, led to fatal B-cell expansion. Thus, timed expression of LMP1 together with LMP2A in subsets of mouse B cells allows one to study major clinically relevant features of human EBV infection in vivo, opening the way to new therapeutic approaches.

Keywords: Epstein–Barr virus; LMP1; LMP2A; familial hemophagocytic lymphohistiocytosis; post-transplant lymphoproliferative disorder.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology
  • B-Lymphocytes / virology*
  • CD40 Antigens / genetics
  • Cell Proliferation / genetics
  • Disease Models, Animal
  • Epstein-Barr Virus Infections / genetics*
  • Epstein-Barr Virus Infections / immunology
  • Epstein-Barr Virus Infections / pathology
  • Epstein-Barr Virus Infections / virology
  • Gene Expression Regulation, Viral
  • Germinal Center / immunology
  • Germinal Center / metabolism
  • Herpesvirus 4, Human / genetics*
  • Herpesvirus 4, Human / pathogenicity
  • Humans
  • Mice
  • Perforin / deficiency
  • Perforin / genetics
  • T-Lymphocytes / immunology
  • T-Lymphocytes / pathology
  • T-Lymphocytes / virology
  • Viral Matrix Proteins / biosynthesis
  • Viral Matrix Proteins / genetics*

Substances

  • CD40 Antigens
  • EBV-associated membrane antigen, Epstein-Barr virus
  • Viral Matrix Proteins
  • Perforin