Asparagine deprivation mediated by Salmonella asparaginase causes suppression of activation-induced T cell metabolic reprogramming

J Leukoc Biol. 2016 Feb;99(2):387-98. doi: 10.1189/jlb.4A0615-252R. Epub 2015 Oct 23.

Abstract

Salmonellae are pathogenic bacteria that induce immunosuppression by mechanisms that remain largely unknown. Previously, we showed that a putative type II l-asparaginase produced by Salmonella Typhimurium inhibits T cell responses and mediates virulence in a murine model of infection. Here, we report that this putative L-asparaginase exhibits L-asparagine hydrolase activity required for Salmonella Typhimurium to inhibit T cells. We show that L-asparagine is a nutrient important for T cell activation and that L-asparagine deprivation, such as that mediated by the Salmonella Typhimurium L-asparaginase, causes suppression of activation-induced mammalian target of rapamycin signaling, autophagy, Myc expression, and L-lactate secretion. We also show that L-asparagine deprivation mediated by the Salmonella Typhimurium L-asparaginase causes suppression of cellular processes and pathways involved in protein synthesis, metabolism, and immune response. Our results advance knowledge of a mechanism used by Salmonella Typhimurium to inhibit T cell responses and mediate virulence, and provide new insights into the prerequisites of T cell activation. We propose a model in which l-asparagine deprivation inhibits T cell exit from quiescence by causing suppression of activation-induced metabolic reprogramming.

Keywords: T-lymphocyte; bacteria; host; inhibition; pathogen.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Asparaginase / genetics
  • Asparaginase / pharmacology
  • Asparaginase / physiology*
  • Asparagine / deficiency
  • Asparagine / pharmacology
  • Asparagine / physiology*
  • Autophagy / drug effects
  • Bacterial Proteins / genetics
  • Bacterial Proteins / physiology*
  • Cells, Cultured
  • Female
  • Genes, myc
  • Immune Evasion / genetics
  • Immune Evasion / physiology*
  • Interleukin-2 / biosynthesis
  • Interleukin-2 / genetics
  • Lactic Acid / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Molecular Sequence Data
  • Proto-Oncogene Proteins c-myc / biosynthesis
  • Receptors, Antigen, T-Cell, alpha-beta / biosynthesis
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Salmonella typhimurium / enzymology*
  • Salmonella typhimurium / immunology
  • Salmonella typhimurium / pathogenicity
  • T-Lymphocyte Subsets / drug effects
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism*
  • TOR Serine-Threonine Kinases / metabolism
  • Virulence

Substances

  • Bacterial Proteins
  • Interleukin-2
  • Myc protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Receptors, Antigen, T-Cell, alpha-beta
  • Lactic Acid
  • Asparagine
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases
  • Asparaginase