NCoR1 controls Mycobacterium tuberculosis growth in myeloid cells by regulating the AMPK-mTOR-TFEB axis

PLoS Biol. 2023 Aug 17;21(8):e3002231. doi: 10.1371/journal.pbio.3002231. eCollection 2023 Aug.

Abstract

Mycobacterium tuberculosis (Mtb) defends host-mediated killing by repressing the autophagolysosome machinery. For the first time, we report NCoR1 co-repressor as a crucial host factor, controlling Mtb growth in myeloid cells by regulating both autophagosome maturation and lysosome biogenesis. We found that the dynamic expression of NCoR1 is compromised in human peripheral blood mononuclear cells (PBMCs) during active Mtb infection, which is rescued upon prolonged anti-mycobacterial therapy. In addition, a loss of function in myeloid-specific NCoR1 considerably exacerbates the growth of M. tuberculosis in vitro in THP1 differentiated macrophages, ex vivo in bone marrow-derived macrophages (BMDMs), and in vivo in NCoR1MyeKO mice. We showed that NCoR1 depletion controls the AMPK-mTOR-TFEB signalling axis by fine-tuning cellular adenosine triphosphate (ATP) homeostasis, which in turn changes the expression of proteins involved in autophagy and lysosomal biogenesis. Moreover, we also showed that the treatment of NCoR1 depleted cells by Rapamycin, Antimycin-A, or Metformin rescued the TFEB activity and LC3 levels, resulting in enhanced Mtb clearance. Similarly, expressing NCoR1 exogenously rescued the AMPK-mTOR-TFEB signalling axis and Mtb killing. Overall, our data revealed a central role of NCoR1 in Mtb pathogenesis in myeloid cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases
  • Animals
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Humans
  • Leukocytes, Mononuclear
  • Mice
  • Mycobacterium tuberculosis*
  • Myeloid Cells
  • Nuclear Receptor Co-Repressor 1* / metabolism
  • TOR Serine-Threonine Kinases

Substances

  • AMP-Activated Protein Kinases
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • TFEB protein, human
  • TOR Serine-Threonine Kinases
  • NCOR1 protein, human
  • Nuclear Receptor Co-Repressor 1

Grants and funding

This work was supported by grants from SERB (Science and Engineering Research Board)-India (grants EMR/2016/000717 to SKR) and also from DBT (Department of Biotechnology) India (grants BT/PR15908/MED/12/725/2016 to SKR). ILS (Institute of Life Sciences) provided intramural core grants and infrastructure to carry out the study to SKR. V.K.B. is supported by ILS-DBT, K.S. is supported by UGC-SRF, A.A. is supported by DBT-SRF, A.G. is supported by ICMR-SRF fellowship, R.P. is supported by DBT-RA fellowship, S.P1 is supported by UGC-SRF and S.P2 is supported by ICMR-SRF fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.