CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients

Eur J Immunol. 2012 Feb;42(2):447-57. doi: 10.1002/eji.201141826. Epub 2011 Dec 16.

Abstract

Natural killer (NK) cells are affected by infection with human cytomegalovirus (HCMV) manifested by increased expression of the HLA-E binding activating receptor NKG2C. We here show that HCMV seropositivity was associated with a profound expansion of NKG2C(+) CD56(dim) NK cells in patients with chronic hepatitis B virus (HBV) or hepatitis C virus (HCV) infection. Multi-color flow cytometry revealed that the expanded NKG2C(+) CD56(dim) NK cells displayed a highly differentiated phenotype, expressed high amounts of granzyme B and exhibited polyfunctional responses (CD107a, IFN-γ, and TNF-α) to stimulation with antibody-coated as well as HLA-E expressing target cells but not when stimulated with IL-12/IL-18. More importantly, NKG2C(+) CD56(dim) NK cells had a clonal expression pattern of inhibitory killer cell immunoglobulin-like receptors (KIRs) specific for self-HLA class I molecules, with predominant usage of KIR2DL2/3. KIR engagement dampened NKG2C-mediated activation suggesting that such biased expression of self-specific KIRs may preserve self-tolerance and limit immune-pathology during viral infection. Together, these findings shed new light on how the human NK-cell compartment adjusts to HCMV infection resulting in clonal expansion and differentiation of educated and polyfunctional NK cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Antibodies, Viral / blood
  • Autoantigens / immunology
  • CD56 Antigen / metabolism
  • Cell Differentiation
  • Cell Growth Processes
  • Cells, Cultured
  • Clonal Selection, Antigen-Mediated*
  • Cytokines / metabolism
  • Cytomegalovirus / immunology*
  • Cytomegalovirus / pathogenicity
  • Female
  • Gene Expression Regulation / immunology
  • HLA-E Antigens
  • Hepatitis, Chronic / blood
  • Hepatitis, Chronic / immunology*
  • Hepatitis, Chronic / virology
  • Histocompatibility Antigens Class I / metabolism*
  • Humans
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / metabolism*
  • Killer Cells, Natural / pathology
  • Killer Cells, Natural / virology
  • Lymphocyte Subsets / immunology
  • Lymphocyte Subsets / metabolism*
  • Lymphocyte Subsets / pathology
  • Lymphocyte Subsets / virology
  • Male
  • Middle Aged
  • NK Cell Lectin-Like Receptor Subfamily C / metabolism
  • Receptors, KIR2DL2 / immunology
  • Receptors, KIR2DL2 / metabolism

Substances

  • Antibodies, Viral
  • Autoantigens
  • CD56 Antigen
  • Cytokines
  • Histocompatibility Antigens Class I
  • KIR2DL2 protein, human
  • KLRC2 protein, human
  • NK Cell Lectin-Like Receptor Subfamily C
  • Receptors, KIR2DL2