Unraveling the role of B cells in the pathogenesis of an oncogenic avian herpesvirus

Proc Natl Acad Sci U S A. 2018 Nov 6;115(45):11603-11607. doi: 10.1073/pnas.1813964115. Epub 2018 Oct 18.

Abstract

Marek's disease virus (MDV) is a highly oncogenic alphaherpesvirus that causes immunosuppression, paralysis, and deadly lymphomas in chickens. In infected animals, B cells are efficiently infected and are thought to amplify the virus and transfer it to T cells. MDV subsequently establishes latency in T cells and transforms CD4+ T cells, resulting in fatal lymphomas. Despite many years of research, the exact role of the different B and T cell subsets in MDV pathogenesis remains poorly understood, mostly due to the lack of reverse genetics in chickens. Recently, Ig heavy chain J gene segment knockout (JH-KO) chickens lacking mature and peripheral B cells have been generated. To determine the role of these B cells in MDV pathogenesis, we infected JH-KO chickens with the very virulent MDV RB1B strain. Surprisingly, viral load in the blood of infected animals was not altered in the absence of B cells. More importantly, disease and tumor incidence in JH-KO chickens was comparable to wild-type animals, suggesting that both mature and peripheral B cells are dispensable for MDV pathogenesis. Intriguingly, MDV efficiently replicated in the bursa of Fabricius in JH-KO animals, while spread of the virus to the spleen and thymus was delayed. In the absence of B cells, MDV readily infected CD4+ and CD8+ T cells, allowing efficient virus replication in the lymphoid organs and transformation of T cells. Taken together, our data change the dogma of the central role of B cells, and thereby provide important insights into MDV pathogenesis.

Keywords: B cells; Ig knockout chickens; Marek’s disease virus; lymphomagenesis; transgenic chickens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Animals, Newborn
  • B-Lymphocytes / immunology*
  • Bursa of Fabricius / immunology
  • Bursa of Fabricius / virology
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / virology
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / virology
  • Chick Embryo
  • Chickens
  • DNA, Viral / genetics
  • DNA, Viral / immunology
  • Genome, Viral*
  • Herpesvirus 2, Gallid / genetics
  • Herpesvirus 2, Gallid / immunology
  • Herpesvirus 2, Gallid / pathogenicity*
  • Immunoglobulin Heavy Chains / genetics
  • Lymphocyte Count
  • Lymphoma / genetics
  • Lymphoma / immunology
  • Lymphoma / pathology*
  • Lymphoma / virology
  • Marek Disease / genetics
  • Marek Disease / immunology
  • Marek Disease / pathology*
  • Marek Disease / virology
  • Oncogenic Viruses / genetics
  • Oncogenic Viruses / immunology
  • Oncogenic Viruses / pathogenicity*
  • Spleen / immunology
  • Spleen / virology
  • Thymus Gland / immunology
  • Thymus Gland / virology
  • Viral Load
  • Virulence
  • Virus Replication

Substances

  • DNA, Viral
  • Immunoglobulin Heavy Chains