A calcium-redox feedback loop controls human monocyte immune responses: The role of ORAI Ca2+ channels

Sci Signal. 2016 Mar 8;9(418):ra26. doi: 10.1126/scisignal.aaf1639.

Abstract

In phagocytes, pathogen recognition is followed by Ca(2+) mobilization and NADPH oxidase 2 (NOX2)-mediated "oxidative burst," which involves the rapid production of large amounts of reactive oxygen species (ROS). We showed that ORAI Ca(2+) channels control store-operated Ca(2+) entry, ROS production, and bacterial killing in primary human monocytes. ROS inactivate ORAI channels that lack an ORAI3 subunit. Staphylococcal infection of mice reduced the expression of the gene encoding the redox-sensitive Orai1 and increased the expression of the gene encoding the redox-insensitive Orai3 in the lungs or in bronchoalveolar lavages. A similar switch from ORAI1 to ORAI3 occurred in primary human monocytes exposed to bacterial peptides in culture. These alterations in ORAI1 and ORAI3 abundance shifted the channel assembly toward a more redox-insensitive configuration. Accordingly, silencing ORAI3 increased the redox sensitivity of the channel and enhanced oxidation-induced inhibition of NOX2. We generated a mathematical model that predicted additional features of the Ca(2+)-redox interplay. Our results identified the ORAI-NOX2 feedback loop as a determinant of monocyte immune responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / immunology*
  • Calcium / metabolism
  • Calcium Release Activated Calcium Channels / genetics
  • Calcium Release Activated Calcium Channels / immunology*
  • Calcium Release Activated Calcium Channels / metabolism
  • Female
  • Humans
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology
  • Membrane Glycoproteins / metabolism
  • Mice
  • Models, Biological*
  • Monocytes / immunology*
  • Monocytes / metabolism
  • Monocytes / pathology
  • NADPH Oxidase 2
  • NADPH Oxidases / genetics
  • NADPH Oxidases / immunology
  • NADPH Oxidases / metabolism
  • Oxidation-Reduction
  • Pneumonia, Staphylococcal / genetics
  • Pneumonia, Staphylococcal / immunology*
  • Pneumonia, Staphylococcal / metabolism
  • Pneumonia, Staphylococcal / pathology
  • Reactive Oxygen Species / immunology*
  • Reactive Oxygen Species / metabolism
  • Staphylococcus aureus / immunology*
  • Staphylococcus aureus / metabolism

Substances

  • Calcium Release Activated Calcium Channels
  • Membrane Glycoproteins
  • Reactive Oxygen Species
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases
  • Calcium