Differential Requirements for L-Citrulline and L-Arginine during Antimycobacterial Macrophage Activity

J Immunol. 2015 Oct 1;195(7):3293-300. doi: 10.4049/jimmunol.1500800. Epub 2015 Aug 26.

Abstract

Microbicidal NO production is reliant on inducible NO synthase-mediated L-arginine metabolism in macrophages (MΦs). However, L-arginine supply can be restricted by arginase activity, resulting in inefficient NO output and inhibition of antimicrobial MΦ function. MΦs circumvent this by converting L-citrulline to L-arginine, thereby resupplying substrate for NO production. In this article, we define the metabolic signature of mycobacteria-infected murine MΦs supplied L-arginine, L-citrulline, or both amino acids. Using liquid chromatography-tandem mass spectrometry, we determined that L-arginine synthesized from L-citrulline was less effective as a substrate for arginase-mediated L-ornithine production compared with L-arginine directly imported from the extracellular milieu. Following Mycobacterium bovis bacillus Calmette-Guérin infection and costimulation with IFN-γ, we observed that MΦ arginase activity did not inhibit production of NO derived from L-citrulline, contrary to NO inhibition witnessed when MΦs were cultured in L-arginine. Furthermore, we found that arginase-expressing MΦs preferred L-citrulline over L-arginine for the promotion of antimycobacterial activity. We expect that defining the consequences of L-citrulline metabolism in MΦs will provide novel approaches for enhancing immunity, especially in the context of mycobacterial disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / metabolism
  • Arginine / biosynthesis
  • Arginine / metabolism*
  • Cells, Cultured
  • Citrulline / metabolism*
  • Interferon-gamma / pharmacology
  • Macrophage Activation / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mycobacterium bovis / immunology
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase Type II / metabolism
  • Tuberculosis / immunology*
  • Tuberculosis / microbiology

Substances

  • Citrulline
  • Nitric Oxide
  • Interferon-gamma
  • Arginine
  • Nitric Oxide Synthase Type II
  • Arginase