Preclinical and Clinical Evidence of Mycobacterium tuberculosis Persistence in the Hypoxic Niche of Bone Marrow Mesenchymal Stem Cells after Therapy

Am J Pathol. 2015 Jul;185(7):1924-34. doi: 10.1016/j.ajpath.2015.03.028. Epub 2015 Jun 8.

Abstract

Mycobacterium tuberculosis (MTB), the causative agent of pulmonary tuberculosis, is difficult to eliminate by antibiotic therapy. We recently identified CD271(+) bone marrow-mesenchymal stem cells (BM-MSCs) as a potential site of MTB persistence after therapy. Herein, we have characterized the potential hypoxic localization of the post-therapy MTB-infected CD271(+) BM-MSCs in both mice and human subjects. We first demonstrate that in a Cornell model of MTB persistence in mice, green fluorescent protein-labeled virulent MTB-strain H37Rv was localized to pimonidazole (an in vivo hypoxia marker) positive CD271(+) BM-MSCs after 90 days of isoniazid and pyrazinamide therapy that rendered animal's lung noninfectious. The recovered CD271(+) BM-MSCs from post-therapy mice, when injected into healthy mice, caused active tuberculosis infection in the animal's lung. Moreover, MTB infection significantly increased the hypoxic phenotype of CD271(+) BM-MSCs. Next, in human subjects, previously treated for pulmonary tuberculosis, the MTB-containing CD271(+) BM-MSCs exhibited high expression of hypoxia-inducible factor 1α and low expression of CD146, a hypoxia down-regulated cell surface marker of human BM-MSCs. These data collectively demonstrate the potential localization of MTB harboring CD271(+) BM-MSCs in the hypoxic niche, a critical microenvironmental factor that is well known to induce the MTB dormancy phenotype.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adapalene / immunology*
  • Animals
  • Antitubercular Agents / therapeutic use
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / microbiology*
  • Cell Hypoxia
  • Down-Regulation
  • Female
  • Green Fluorescent Proteins
  • Humans
  • Isoniazid / therapeutic use
  • Lung / microbiology
  • Lung / pathology
  • Mesenchymal Stem Cells / immunology
  • Mesenchymal Stem Cells / microbiology*
  • Mice
  • Mice, Inbred BALB C
  • Mycobacterium tuberculosis / pathogenicity
  • Mycobacterium tuberculosis / physiology*
  • Nitroimidazoles
  • Radiation-Sensitizing Agents
  • Specific Pathogen-Free Organisms
  • Tuberculosis, Pulmonary / drug therapy
  • Tuberculosis, Pulmonary / microbiology*
  • Tuberculosis, Pulmonary / pathology
  • Up-Regulation

Substances

  • Antitubercular Agents
  • Nitroimidazoles
  • Radiation-Sensitizing Agents
  • Green Fluorescent Proteins
  • Adapalene
  • pimonidazole
  • Isoniazid