Limitation of TCA Cycle Intermediates Represents an Oxygen-Independent Nutritional Antibacterial Effector Mechanism of Macrophages

Cell Rep. 2019 Mar 26;26(13):3502-3510.e6. doi: 10.1016/j.celrep.2019.02.103.

Abstract

In hypoxic and inflamed tissues, oxygen (O2)-dependent antimicrobial defenses are impaired due to a shortage of O2. To gain insight into the mechanisms that control bacterial infection under hypoxic conditions, we infected macrophages with the obligate intracellular pathogen Coxiella burnetii, the causative agent of Q fever. Our experiments revealed that hypoxia impeded C. burnetii replication in a hypoxia-inducible factor (HIF) 1α-dependent manner. Mechanistically, under hypoxia, HIF1α impaired the activity of STAT3, which in turn reduced the intracellular level of TCA cycle intermediates, including citrate, and impeded C. burnetii replication in macrophages. However, bacterial viability was maintained, allowing the persistence of C. burnetii, which is a prerequisite for the development of chronic Q fever. This knowledge will open future research avenues on the pathogenesis of chronic Q fever. In addition, the regulation of TCA cycle metabolites by HIF1α represents a previously unappreciated mechanism of host defense against intracellular pathogens.

Keywords: Coxiella burnetii; HIF1α; STAT3; citrate; macrophage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Cell Hypoxia
  • Cells, Cultured
  • Citric Acid Cycle*
  • Coxiella burnetii / immunology*
  • Female
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology
  • Macrophages / immunology*
  • Macrophages / microbiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Oxygen / metabolism
  • Q Fever / immunology
  • STAT3 Transcription Factor / physiology

Substances

  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Oxygen