Mycobacterium tuberculosis Sulfolipid-1 Activates Nociceptive Neurons and Induces Cough

Cell. 2020 Apr 16;181(2):293-305.e11. doi: 10.1016/j.cell.2020.02.026. Epub 2020 Mar 5.

Abstract

Pulmonary tuberculosis, a disease caused by Mycobacterium tuberculosis (Mtb), manifests with a persistent cough as both a primary symptom and mechanism of transmission. The cough reflex can be triggered by nociceptive neurons innervating the lungs, and some bacteria produce neuron-targeting molecules. However, how pulmonary Mtb infection causes cough remains undefined, and whether Mtb produces a neuron-activating, cough-inducing molecule is unknown. Here, we show that an Mtb organic extract activates nociceptive neurons in vitro and identify the Mtb glycolipid sulfolipid-1 (SL-1) as the nociceptive molecule. Mtb organic extracts from mutants lacking SL-1 synthesis cannot activate neurons in vitro or induce cough in a guinea pig model. Finally, Mtb-infected guinea pigs cough in a manner dependent on SL-1 synthesis. Thus, we demonstrate a heretofore unknown molecular mechanism for cough induction by a virulent human pathogen via its production of a complex lipid.

Keywords: cough; glycolipid; host-pathogen; mucosal immunology; mycobacteria; neuro-immune; nociceptor; sulfolipid; tuberculosis.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Cell Line
  • Cough / etiology
  • Cough / microbiology
  • Cough / physiopathology*
  • Female
  • Glycolipids / metabolism*
  • Glycolipids / physiology
  • Guinea Pigs
  • Host-Pathogen Interactions
  • Humans
  • Lipids / physiology
  • Lung / microbiology
  • Macrophages / microbiology
  • Male
  • Mice
  • Mycobacterium tuberculosis / metabolism
  • Mycobacterium tuberculosis / pathogenicity
  • Nociceptors / physiology*
  • Primary Cell Culture
  • Tuberculosis / microbiology
  • Tuberculosis, Pulmonary / microbiology
  • Tuberculosis, Pulmonary / physiopathology
  • Virulence Factors / metabolism*
  • Virulence Factors / physiology

Substances

  • Glycolipids
  • Lipids
  • Virulence Factors
  • sulfolipids
  • sulfolipid I