Mycobacterium tuberculosis effector PPE36 attenuates host cytokine storm damage via inhibiting macrophage M1 polarization

J Cell Physiol. 2021 Nov;236(11):7405-7420. doi: 10.1002/jcp.30411. Epub 2021 May 7.

Abstract

Tuberculosis caused by Mycobacterium tuberculosis remains a serious global public health threat. Macrophage polarization is crucial for the innate immunity against M. tuberculosis. However, how M. tuberculosis interferes with macrophage polarization is elusive. We demonstrated here that M. tuberculosis PPE36 (Rv2108) blocked macrophage M1 polarization, preventing the cytokine storm, and alleviating inflammatory damage to mouse immune organs. PPE36 inhibited the polarization of THP-1 cell differentiation to M1 macrophages, reduced mitochondrial dehydrogenase activity, inhibited the expression of CD16, and repressed the expression of pro-inflammatory cytokines IL-6 and TNF-α, as well as chemokines CXCL9, CXCL10, CCL3, and CCL5. Intriguingly, in the mouse infection model, PPE36 significantly alleviated the inflammatory damage of immune organs caused by a cytokine storm. Furthermore, we found that PPE36 inhibited the polarization of macrophages into mature M1 macrophages by suppressing the ERK signaling. The study provided novel insights into the function and mechanism of action of M. tuberculosis effector PPE36 both at the cellular and animal level.

Keywords: ERK; Mycobacterium tuberculosis; cytokine storm; inflammatory; macrophage polarization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Bacterial / genetics
  • Antigens, Bacterial / immunology
  • Antigens, Bacterial / metabolism*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / immunology
  • Bacterial Proteins / metabolism*
  • Cytokine Release Syndrome / immunology
  • Cytokine Release Syndrome / metabolism
  • Cytokine Release Syndrome / microbiology
  • Cytokine Release Syndrome / prevention & control*
  • Cytokines / metabolism*
  • Disease Models, Animal
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • Host-Pathogen Interactions
  • Humans
  • Inflammation Mediators / metabolism*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / microbiology*
  • Mice
  • Mice, Inbred C57BL
  • Mycobacterium Infections, Nontuberculous / immunology
  • Mycobacterium Infections, Nontuberculous / metabolism
  • Mycobacterium Infections, Nontuberculous / microbiology*
  • Mycobacterium smegmatis / genetics
  • Mycobacterium smegmatis / immunology
  • Mycobacterium smegmatis / metabolism*
  • Phenotype
  • Signal Transduction
  • THP-1 Cells

Substances

  • Antigens, Bacterial
  • Bacterial Proteins
  • Cytokines
  • Inflammation Mediators
  • PPE36 protein, Mycobacterium tuberculosis
  • Extracellular Signal-Regulated MAP Kinases