The complex of MCMV proteins and MHC class I evades NK cell control and drives the evolution of virus-specific activating Ly49 receptors

J Exp Med. 2019 Aug 5;216(8):1809-1827. doi: 10.1084/jem.20182213. Epub 2019 May 29.

Abstract

CMVs efficiently target MHC I molecules to avoid recognition by cytotoxic T cells. However, the lack of MHC I on the cell surface renders the infected cell susceptible to NK cell killing upon missing self recognition. To counter this, mouse CMV (MCMV) rescues some MHC I molecules to engage inhibitory Ly49 receptors. Here we identify a new viral protein, MATp1, that is essential for MHC I surface rescue. Rescued altered-self MHC I molecules show increased affinity to inhibitory Ly49 receptors, resulting in inhibition of NK cells despite substantially reduced MHC I surface levels. This enables the virus to evade recognition by licensed NK cells. During evolution, this novel viral immune evasion mechanism could have prompted the development of activating NK cell receptors that are specific for MATp1-modified altered-self MHC I molecules. Our study solves a long-standing conundrum of how MCMV avoids recognition by NK cells, unravels a fundamental new viral immune evasion mechanism, and demonstrates how this forced the evolution of virus-specific activating MHC I-restricted Ly49 receptors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Ly / genetics
  • Cytotoxicity, Immunologic
  • Disease Models, Animal
  • Female
  • Fibroblasts / metabolism
  • Herpesviridae Infections / immunology*
  • Herpesviridae Infections / virology
  • Histocompatibility Antigens Class I / immunology
  • Histocompatibility Antigens Class I / metabolism*
  • Immune Evasion / immunology*
  • Killer Cells, Natural / immunology*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Muromegalovirus / metabolism*
  • NK Cell Lectin-Like Receptor Subfamily A / metabolism*
  • Natural Cytotoxicity Triggering Receptor 1 / genetics
  • Viral Proteins / metabolism*

Substances

  • Antigens, Ly
  • Histocompatibility Antigens Class I
  • NK Cell Lectin-Like Receptor Subfamily A
  • Natural Cytotoxicity Triggering Receptor 1
  • Ncr1 protein, mouse
  • Viral Proteins

Associated data

  • GENBANK/AM886412
  • GENBANK/EU579859
  • GENBANK/HE610453
  • GENBANK/HE610456
  • GENBANK/EU579860
  • GENBANK/GU305914.1