Mutation of a diacidic motif in SIV-PBj Nef impairs T-cell activation and enteropathic disease

Retrovirology. 2011 Mar 2:8:14. doi: 10.1186/1742-4690-8-14.

Abstract

Background: The non-pathogenic course of SIV infection in its natural host is characterized by robust viral replication in the absence of chronic immune activation and T cell proliferation. In contrast, acutely lethal enteropathic SIVsmm strain PBj induces a strong immune activation and causes a severe acute and lethal disease in pig-tailed macaques after cross-species transmission. One important pathogenicity factor of the PBj virus is the PBj-Nef protein, which contains a conserved diacidic motif and, unusually, an immunoreceptor tyrosine-based activation motif (ITAM).

Results: Mutation of the diacidic motif in the Nef protein of the SIVsmmPBj abolishes the acute phenotype of this virus. In vitro, wild-type and mutant PBj (PBj-Nef202/203GG) viruses replicated to similar levels in macaque PBMCs, but PBj-Nef202/203GG no longer triggers ERK mitogen-activated protein (MAP) kinase pathway including an alteration of a Nef-associated Raf-1/ERK-2 multiprotein signaling complex. Moreover, stimulation of IL-2 and down-modulation of CD4 and CD28 were impaired in the mutant virus. Pig-tailed macaques infected with PBj-Nef202/203GG did not show enteropathic complications and lethality as observed with wild-type PBj virus, despite efficient replication of both viruses in vivo. Furthermore, PBj-Nef202/203GG infected animals revealed reduced T-cell activation in periphery lymphoid organs and no detectable induction of IL-2 and IL-6.

Conclusions: In sum, we report here that mutation of the diacidic motif in the PBj-Nef protein abolishes disease progression in pig-tailed macaques despite efficient replication. These data suggest that alterations in the ability of a lentivirus to promote T cell activation and proliferation can have a dramatic impact on its pathogenic potential.

MeSH terms

  • Amino Acid Motifs
  • Animals
  • Cells, Cultured
  • Colon / pathology*
  • Colon / virology
  • Gene Products, nef / chemistry*
  • Gene Products, nef / genetics
  • Gene Products, nef / metabolism
  • Humans
  • Lymphocyte Activation*
  • Lymphopenia / virology
  • Macaca nemestrina
  • Monkey Diseases / immunology
  • Monkey Diseases / pathology
  • Monkey Diseases / virology
  • Mutation*
  • Phenotype
  • Simian Acquired Immunodeficiency Syndrome / immunology
  • Simian Acquired Immunodeficiency Syndrome / physiopathology
  • Simian Acquired Immunodeficiency Syndrome / virology
  • Simian Immunodeficiency Virus / genetics
  • Simian Immunodeficiency Virus / immunology
  • Simian Immunodeficiency Virus / metabolism
  • Simian Immunodeficiency Virus / pathogenicity*
  • T-Lymphocytes / immunology*
  • Viremia / virology
  • Virus Replication

Substances

  • Gene Products, nef