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Next generation sequencing reveals miR-431–3p/miR-1303 as immune-regulating microRNAs for active tuberculosis

  • Yung-Che Chen
    Correspondence
    Corresponding author at: No. 123, Ta-Pei Rd, Niao-Sung District, Kaohsiung City, Taiwan
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan

    Department of Medicine, College of Medicine, Chang Gung University, Taoyuan 33302, Taiwan
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  • Chang-Chun Hsiao
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan

    Graduate Institute of Clinical Medical Sciences, Taiwan
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  • Chao-Chien Wu
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Tung-Ying Chao
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Sum-Yee Leung
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Yu-Ping Chang
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Chia-Cheng Tseng
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Chiu-Ping Lee
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Po-Yuan Hsu
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Ting-Ya Wang
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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  • Po-Wen Wang
    Affiliations
    Institute of Bioinformatics and Systems Biology, National Yang Ming Chiao Tung University, Hsinchu 30068, Taiwan

    Department of Biological Science and Technology, National Yang Ming Chiao Tung University, Hsinchu 30068, Taiwan
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  • Ting-Wen Chen
    Correspondence
    Corresponding author at: No. 75, Boai Street, Hsinchu 300, Taiwan
    Affiliations
    Institute of Bioinformatics and Systems Biology, National Yang Ming Chiao Tung University, Hsinchu 30068, Taiwan

    Department of Biological Science and Technology, National Yang Ming Chiao Tung University, Hsinchu 30068, Taiwan
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  • Meng-Chih Lin
    Correspondence
    Corresponding author.
    Affiliations
    Division of Pulmonary and Critical Care Medicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 83301, Taiwan
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Published:August 31, 2022DOI:https://doi.org/10.1016/j.jinf.2022.08.035

      Highlights

      • Whole genome sequencing identified 55 TB-related differentially expressed microRNAs.
      • Proteoglycan, longevity, apoptosis, central carbon metabolism, and autophagy were enriched target pathways.
      • miR-431–3p down-regulation and miR-1303 up-regulation were verified in vivo & vitro.
      • miR-431–3p over-expression and miR-1303 knock-down improved macrophage functions synergistically.
      • Both microRNAs regulate autophagy, apoptosis, and phagocytosis via targeting MDR1/MMP16/RIPOR2 and ATG5.

      Abstract

      Objectives

      RNA therapeutics is an emerging field that widens the range of treatable targets and would improve disease outcome through bypassing the antibiotic bactericidal targets to kill Mycobacterium tuberculosis (M.tb).

      Methods

      We screened for microRNA with immune-regulatory functions against M.tb by next generation sequencing of peripheral blood mononuclear cells, followed by validation in an independent cohort.

      Results

      Twenty three differentially expressed microRNAs were identified between 12 active pulmonary TB patients and 4 healthy subjects, and 35 microRNAs before and after 6-month anti-TB therapy. Enriched predicted target pathways included proteoglycan, HIF-1 signaling, longevity-regulating, central carbon metabolism, and autophagy. We validated miR-431–3p down-regulation and miR-1303 up-regulation accompanied with corresponding changes in their predicted target genes in an independent validation cohort of 46 active TB patients, 30 latent TB infection subjects, and 24 non-infected healthy subjects. In vitro experiments of transfections with miR-431–3p mimic/miR-1303 short interfering RNA in THP-1 cells under ESAT-6 stimuli showed that miR-431–3p and miR-1303 were capable to augment and suppress autophagy/apoptosis/phagocytosis of macrophage via targeting MDR1/MMP16/RIPOR2 and ATG5, respectively.

      Conclusions

      This study provides a proof of concept for microRNA-based host-directed immunotherapy for active TB disease. The combined miR-431–3p over-expression and miR-1303 knock-down revealed new vulnerabilities of treatment-refractory TB disease.

      Keywords

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