Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b

Rajaram, Murugesan V. S.; Ni, Bin; Morris, Jessica D.; Brooks, Michelle N.; Carlson, Tracy K.; Bakthavachalu, Baskar; Schoenberg, Daniel R.; Torrelles, Jordi B.; Schlesinger, Larry S.

doi:10.1073/pnas.1112660108

Cited by 269Tuberculosis Research and EpidemiologyImmune Response and InflammationImmune responses and vaccinations

Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b

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Rajaram, Murugesan V. S., Ni, Bin, Morris, Jessica D., Brooks, Michelle N., Carlson, Tracy K., Bakthavachalu, Baskar, Schoenberg, Daniel R., Torrelles, Jordi B. +1 more·2011·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1112660108PMC PMC3198317

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Abstract

Contact of Mycobacterium tuberculosis (M.tb) with the immune system requires interactions between microbial surface molecules and host pattern recognition receptors. Major M.tb-exposed cell envelope molecules, such as lipomannan (LM), contain subtle structural variations that affect the nature of the immune response. Here we show that LM from virulent M.tb (TB-LM), but not from avirulent Myocobacterium smegmatis (SmegLM), is a potent inhibitor of TNF biosynthesis in human macrophages. This difference in response is not because of variation in Toll-like receptor 2-dependent activation of the signaling kinase MAPK p38. Rather, TB-LM stimulation leads to destabilization of TNF mRNA transcripts and subsequent failure to produce TNF protein. In contrast, SmegLM enhances MAPK-activated protein kinase 2 phosphorylation, which is critical for maintaining TNF mRNA stability in part by contributing microRNAs (miRNAs). In this context, human miRNA miR-125b binds to the 3' UTR region of TNF mRNA and destabilizes the transcript, whereas miR-155 enhances TNF production by increasing TNF mRNA half-life and limiting expression of SHIP1, a negative regulator of the PI3K/Akt pathway. We show that macrophages incubated with TB-LM and live M.tb induce high miR-125b expression and low miR-155 expression with correspondingly low TNF production. In contrast, SmegLM and live M. smegmatis induce high miR-155 expression and low miR-125b expression with high TNF production. Thus, we identify a unique cellular mechanism underlying the ability of a major M.tb cell wall component, TB-LM, to block TNF biosynthesis in human macrophages, thereby allowing M.tb to subvert host immunity and potentially increase its virulence.

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Upon Mtb infection, miR-125b is upregulated and miR-155 is downregulated, decreasing TNF production.
“upon Mtb infection, contrary changes occur, i.e., up-regulation of miR-125b and down-regulation of miR-155 decreases TNF production [142]”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [142]
The section on infected macrophages reports that M. tuberculosis increased miR-125b, limited miR-155 relative to M. smegmatis, and yielded lower TNF production. It does not establish that miR-155 was downregulated relative to uninfected macrophages, as the citing sentence implies. (LLM, conf=0.86)
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Authors: Rajaram, M. V. S., Ni, B., Morris, J. D., Brooks, M. N., Carlson, T. K., Bakthavachalu, B., Schoenberg, D. R., Torrelles, J. B., & Schlesinger, L. S.
Affiliations: Center for Microbial Interface Biology,
Integrated Biomedical Science Graduate Program,
Center for RNA Biology and Department of Molecular and Cellular Biochemistry,
The Ohio State University (US)
ORCID: Rajaram, Murugesan V. S.
Ni, Bin
Bakthavachalu, Baskar
Schoenberg, Daniel R.
Torrelles, Jordi B.
Schlesinger, Larry S.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2011-10-03
Volume: 108
Issue: 42
Pages: 17408-17413
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1112660108
PMC: PMC3198317
OpenAlex: W2101417884
Cited by: 269
References: 43
Citations by year: 2026: 4 · 2025: 9 · 2024: 3 · 2023: 20 · 2022: 15 · 2021: 20 · 2020: 19 · 2019: 16 · 2018: 19 · 2017: 18 · 2016: 35 · 2015: 26 · 2014: 23 · 2013: 26 · 2012: 16
FWCI: 14.09
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (8k01od011077-03)
National Institute of General Medical Sciences (R01GM038277, GM038277)
National Institute of Allergy and Infectious Diseases (AI059639, R01AI059639, AI-052458, R01AI052458, R21AI059639, R21AI052458)
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Keywords: Mycobacterium tuberculosis, lipomannan, macrophages, MAPKAPK2, miR-125b, miR-155, 3' untranslated region, SHIP1, PI3K/Akt signaling, Mycobacterium smegmatis, virulence, host immune evasion
MeSH terms: Humans, Lipopolysaccharides, Macrophages, Mycobacterium tuberculosis, Phosphorylation, Promoter Regions, Genetic, Tumor Necrosis Factor-alpha, Virulence, RNA Stability, MAP Kinase Signaling System, MicroRNAs, p38 Mitogen-Activated Protein Kinases, MAP Kinase Kinase 2, Proto-Oncogene Proteins c-akt, Toll-Like Receptor 2, In Vitro Techniques

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Mycobacterium tuberculosis lipomannan blocks TNF biosynthesis by regulating macrophage MAPK-activated protein kinase 2 (MK2) and microRNA miR-125b

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