Marek's disease viral interleukin-8 promotes lymphoma formation through targeted recruitment of B cells and CD4+ CD25+ T cells

J Virol. 2012 Aug;86(16):8536-45. doi: 10.1128/JVI.00556-12. Epub 2012 May 30.

Abstract

Marek's disease virus (MDV) is a cell-associated and highly oncogenic alphaherpesvirus that infects chickens. During lytic and latent MDV infection, a CXC chemokine termed viral interleukin-8 (vIL-8) is expressed. Deletion of the entire vIL-8 open reading frame (ORF) was shown to severely impair disease progression and tumor development; however, it was unclear whether this phenotype was due to loss of secreted vIL-8 or of splice variants that fuse exons II and III of vIL-8 to certain upstream open reading frames, including the viral oncoprotein Meq. To specifically examine the role of secreted vIL-8 in MDV pathogenesis, we constructed a recombinant virus, vΔMetvIL-8, in which we deleted the native start codon from the signal peptide encoding exon I. This mutant lacked secreted vIL-8 but did not affect Meq-vIL-8 splice variants. Loss of secreted vIL-8 resulted in highly reduced disease and tumor incidence in animals infected with vΔMetvIL-8 by the intra-abdominal route. Although vΔMetvIL-8 was still able to spread to naïve animals by the natural route, infection and lymphomagenesis in contact animals were severely impaired. In vitro assays showed that purified recombinant vIL-8 efficiently binds to and induces chemotaxis of B cells, which are the main target for lytic MDV replication, and also interacts with CD4(+) CD25(+) T cells, known targets of MDV transformation. Our data provide evidence that vIL-8 attracts B and CD4(+) CD25(+) T cells to recruit targets for both lytic and latent infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / physiology*
  • CD4-Positive T-Lymphocytes / chemistry
  • CD4-Positive T-Lymphocytes / physiology*
  • Chemotaxis*
  • Chickens
  • Interleukin-2 Receptor alpha Subunit / analysis
  • Lymphoma / pathology*
  • Lymphoma / virology
  • Mardivirus / pathogenicity*
  • Marek Disease / immunology
  • Marek Disease / pathology
  • Marek Disease / virology
  • Oncogene Proteins, Viral / genetics
  • Oncogene Proteins, Viral / metabolism*
  • Protein Sorting Signals / genetics
  • Sequence Deletion
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*

Substances

  • Interleukin-2 Receptor alpha Subunit
  • Oncogene Proteins, Viral
  • Protein Sorting Signals
  • Virulence Factors
  • vIL-8 protein, Marek's disease virus