Influenza viruses differ in ability to infect macrophages and to induce a local inflammatory response following intraperitoneal injection of mice

Immunol Cell Biol. 2010 Aug;88(6):641-50. doi: 10.1038/icb.2010.11. Epub 2010 Feb 9.

Abstract

Strains of influenza A virus show marked differences in their ability to infect murine macrophages (MPhi) such that strain A/PR/8/34 (PR8; H1N1) infects MPhi poorly while strain BJx109 (H3N2) infects MPhi to high levels. Given the central role of MPhi in initiating and regulating inflammatory responses, we hypothesized that virus strains that infect MPhi poorly may also be poor at initiating inflammatory responses. Studies to compare the inflammatory response of mice after intranasal inoculation with either BJx109 or PR8 were confounded by the rapid growth of the PR8 virus in lung tissues. Consequently, we have characterized the cellular inflammatory response following inoculation into the peritoneal cavity, as influenza viruses do not replicate at this site. Herein, we report marked differences in the local inflammatory response to BJx109 or PR8 in the peritoneal cavity with strain PR8 being particularly poor in its ability to recruit and activate peritoneal leukocytes, including NK cells and MPhi. In vitro BJx109, but not PR8, stimulated release of high levels of type I IFNs and TNF-alpha from PEC MPhi, and treatment of mice with neutralizing antibodies to either cytokine inhibited the ability of BJx109 to recruit and activate NK cells and MPhis in the peritoneal cavity. Together, these data suggest that the ability of influenza virus strains to infect MPhi and stimulate cytokine release is an important factor governing the nature of the acute inflammatory response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Blocking / administration & dosage
  • Cell Line
  • Cell Movement / drug effects
  • Cell Movement / immunology
  • Influenza A Virus, H1N1 Subtype / immunology*
  • Influenza A Virus, H1N1 Subtype / pathogenicity
  • Influenza A Virus, H3N2 Subtype / immunology*
  • Influenza A Virus, H3N2 Subtype / pathogenicity
  • Injections, Intraperitoneal
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / genetics
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism*
  • Macrophages, Peritoneal / pathology
  • Macrophages, Peritoneal / virology
  • Male
  • Mice
  • Mice, Inbred Strains
  • Mice, Knockout
  • Mice, SCID
  • Orthomyxoviridae Infections / immunology*
  • Orthomyxoviridae Infections / pathology
  • Orthomyxoviridae Infections / virology*
  • Species Specificity
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Necrosis Factor-alpha / genetics
  • Virulence

Substances

  • Antibodies, Blocking
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma