Kaposi's sarcoma-associated herpesvirus vIRF2 protein utilizes an IFN-dependent pathway to regulate viral early gene expression

PLoS Pathog. 2019 May 6;15(5):e1007743. doi: 10.1371/journal.ppat.1007743. eCollection 2019 May.

Abstract

Kaposi's sarcoma-associated herpesvirus (KSHV; human herpesvirus 8) belongs to the subfamily of Gammaherpesvirinae and is the etiological agent of Kaposi's sarcoma as well as of two lymphoproliferative diseases: primary effusion lymphoma and multicentric Castleman disease. The KSHV life cycle is divided into a latent and a lytic phase and is highly regulated by viral immunomodulatory proteins which control the host antiviral immune response. Among them is a group of proteins with homology to cellular interferon regulatory factors, the viral interferon regulatory factors 1-4. The KSHV vIRFs are known as inhibitors of cellular interferon signaling and are involved in different oncogenic pathways. Here we characterized the role of the second vIRF protein, vIRF2, during the KSHV life cycle. We found the vIRF2 protein to be expressed in different KSHV positive cells with early lytic kinetics. Importantly, we observed that vIRF2 suppresses the expression of viral early lytic genes in both newly infected and reactivated persistently infected endothelial cells. This vIRF2-dependent regulation of the KSHV life cycle might involve the increased expression of cellular interferon-induced genes such as the IFIT proteins 1, 2 and 3, which antagonize the expression of early KSHV lytic proteins. Our findings suggest a model in which the viral protein vIRF2 allows KSHV to harness an IFN-dependent pathway to regulate KSHV early gene expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / pathology
  • Endothelium, Vascular / virology*
  • Gene Expression Regulation, Viral*
  • Herpesvirus 8, Human / physiology*
  • Humans
  • Immediate-Early Proteins / genetics
  • Immediate-Early Proteins / metabolism*
  • Interferon Regulatory Factors / genetics
  • Interferon Regulatory Factors / metabolism*
  • Interferons / genetics
  • Interferons / metabolism*
  • Sarcoma, Kaposi / genetics
  • Sarcoma, Kaposi / metabolism
  • Sarcoma, Kaposi / virology*
  • Viral Proteins / genetics
  • Viral Proteins / metabolism*
  • Virus Activation*
  • Virus Latency

Substances

  • Immediate-Early Proteins
  • Interferon Regulatory Factors
  • Viral Proteins
  • viral interferon regulatory factors
  • Interferons

Grants and funding

This study was supported by the Collaborative Research Centre 900 ‘Chronic Infections’ of the Deutsche Forschungsgemeinschaft (project C1 to TFS) and a personal doctoral fellowship of the German Academic Exchange Service (DAAD) to MD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.