Arginase activity in pathogenic and non-pathogenic species of Leishmania parasites

PLoS Negl Trop Dis. 2017 Jul 14;11(7):e0005774. doi: 10.1371/journal.pntd.0005774. eCollection 2017 Jul.

Abstract

Proliferation of Leishmania (L.) parasites depends on polyamine availability, which can be generated by the L-arginine catabolism and the enzymatic activity of arginase (ARG) of the parasites and of the mammalian hosts. In the present study, we characterized and compared the arginase (arg) genes from pathogenic L. major and L. tropica and from non-pathogenic L. tarentolae. We quantified the level of the ARG activity in promastigotes and macrophages infected with pathogenic L. major and L. tropica and non-pathogenic L. tarentolae amastigotes. The ARG's amino acid sequences of the pathogenic and non-pathogenic Leishmania demonstrated virtually 98.6% and 88% identities with the reference L. major Friedlin ARG. Higher ARG activity was observed in all pathogenic promastigotes as compared to non-pathogenic L. tarentolae. In vitro infection of human macrophage cell line (THP1) with pathogenic and non-pathogenic Leishmania spp. resulted in increased ARG activities in the infected macrophages. The ARG activities present in vivo were assessed in susceptible BALB/c and resistant C57BL/6 mice infected with L. major, L. tropica and L. tarentolae. We demonstrated that during the development of the infection, ARG is induced in both strains of mice infected with pathogenic Leishmania. However, in L. major infected BALB/c mice, the induction of ARG and parasite load increased simultaneously according to the time course of infection, whereas in C57BL/6 mice, the enzyme is upregulated solely during the period of footpad swelling. In L. tropica infected mice, the footpads' swellings were slow to develop and demonstrated minimal cutaneous pathology and ARG activity. In contrast, ARG activity was undetectable in mice inoculated with the non-pathogenic L. tarentolae. Our data suggest that infection by Leishmania parasites can increase ARG activity of the host and provides essential polyamines for parasite salvage and its replication. Moreover, the ARG of Leishmania is vital for parasite proliferation and required for infection in mice. ARG activity can be used as one of the main marker of the disease severity.

MeSH terms

  • Animals
  • Arginase / genetics
  • Arginase / metabolism*
  • Arginine / analogs & derivatives*
  • Arginine / genetics
  • Cell Culture Techniques
  • Cell Line
  • Female
  • Humans
  • Leishmania / classification
  • Leishmania / enzymology*
  • Leishmania / genetics
  • Leishmaniasis / parasitology*
  • Lymph Nodes / parasitology
  • Macrophages / parasitology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Parasite Load
  • Phylogeny
  • Polyamines
  • Sequence Analysis, DNA

Substances

  • Polyamines
  • arginine polyamine
  • Arginine
  • Arginase

Grants and funding

AB is a PhD student who was supported by the Shahid Beheshti University of Medical Sciences, Tehran, Iran. This article has been extracted from the Ph.D. thesis written by AB in the Department of Medical Parasitology and Mycology, School of Medicine at Shahid Beheshti University of Medical Sciences (Registration No.: 26). This work was financially supported by the Pasteur Institute of Iran Grant number 730 to TT and by the Iran National Science Foundation Grant ID 94013422 and 940007 to SR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.