Influenza infection results in local expansion of memory CD8(+) T cells with antigen non-specific phenotype and function

Clin Exp Immunol. 2014 Jan;175(1):79-91. doi: 10.1111/cei.12186.

Abstract

Primary viral infections induce activation of CD8(+) T cells responsible for effective resistance. We sought to characterize the nature of the CD8(+) T cell expansion observed after primary viral infection with influenza. Infection of naive mice with different strains of influenza resulted in the rapid expansion of memory CD8(+) T cells exhibiting a unique bystander phenotype with significant up-regulation of natural killer group 2D (NKG2D), but not CD25, on the CD44(high) CD8(+) T cells, suggesting an antigen non-specific phenotype. We further confirmed the non-specificity of this phenotype on ovalbumin-specific (OT-I) CD8(+) T cells, which are not specific to influenza. These non-specific CD8(+) T cells also displayed increased lytic capabilities and were observed primarily in the lung. Thus, influenza infection was shown to induce a rapid, antigen non-specific memory T cell expansion which is restricted to the specific site of inflammation. In contrast, CD8(+) T cells of a similar phenotype could be observed in other organs following administration of systemic agonistic anti-CD40 and interleukin-2 immunotherapy, demonstrating that bystander expansion in multiple sites is possible depending on whether the nature of activation is either acute or systemic. Finally, intranasal blockade of NKG2D resulted in a significant increase in viral replication early during the course of infection, suggesting that NKG2D is a critical mediator of anti-influenza responses prior to the initiation of adaptive immunity. These results characterize further the local bystander expansion of tissue-resident, memory CD8(+) T cells which, due to their early induction, may play an important NKG2D-mediated, antigen non-specific role during the early stages of viral infection.

Keywords: NKG2D; antigen non-specific; bystander activation; memory CD8; tissue-resident.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bystander Effect / immunology*
  • CD40 Antigens / antagonists & inhibitors
  • CD40 Antigens / genetics
  • CD40 Antigens / immunology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / pathology
  • Immunologic Memory*
  • Immunotherapy / methods
  • Influenza A virus / physiology*
  • Interleukin-2 / genetics
  • Interleukin-2 / immunology
  • Interleukin-2 / pharmacology
  • Lung / immunology*
  • Lung / pathology
  • Lung / virology
  • Mice
  • Mice, Transgenic
  • NK Cell Lectin-Like Receptor Subfamily K / genetics
  • NK Cell Lectin-Like Receptor Subfamily K / immunology
  • Orthomyxoviridae Infections / genetics
  • Orthomyxoviridae Infections / immunology*
  • Orthomyxoviridae Infections / pathology
  • Orthomyxoviridae Infections / therapy
  • Virus Replication / genetics
  • Virus Replication / immunology*

Substances

  • CD40 Antigens
  • Interleukin-2
  • Klrk1 protein, mouse
  • NK Cell Lectin-Like Receptor Subfamily K