MicroRNA-155 Is Required for Mycobacterium bovis BCG-Mediated Apoptosis of Macrophages

Ghorpade, Devram Sampat; Leyland, Rebecca; Kurowska-Stolarska, Mariola; Patil, Shripad A.; Balaji, Kithiganahalli Narayanaswamy

doi:10.1128/mcb.06597-11

Cited by 142Tuberculosis Research and EpidemiologyMicroRNA in disease regulationImmune Response and Inflammation

MicroRNA-155 Is Required for Mycobacterium bovis BCG-Mediated Apoptosis of Macrophages

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Ghorpade, Devram Sampat, Leyland, Rebecca, Kurowska-Stolarska, Mariola, Patil, Shripad A., Balaji, Kithiganahalli Narayanaswamy·2012·Molecular and Cellular Biology

DOI 10.1128/mcb.06597-11PMC PMC3372268

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Abstract

Pathogenic mycobacteria, including Mycobacterium tuberculosis and Mycobacterium bovis, cause significant morbidity and mortality worldwide. However, the vaccine strain Mycobacterium bovis BCG, unlike virulent strains, triggers extensive apoptosis of infected macrophages, a step necessary for the elicitation of robust protective immunity. We here demonstrate that M. bovis BCG triggers Toll-like receptor 2 (TLR2)-dependent microRNA-155 (miR-155) expression, which involves signaling cross talk among phosphatidylinositol 3-kinase (PI3K), protein kinase Cδ (PKCδ), and mitogen-activated protein kinases (MAPKs) and recruitment of NF-κB and c-ETS to miR-155 promoter. Genetic and signaling perturbations presented the evidence that miR-155 regulates PKA signaling by directly targeting a negative regulator of PKA, protein kinase inhibitor alpha (PKI-α). Enhanced activation of PKA signaling resulted in the generation of PKA C-α; phosphorylation of MSK1, cyclic AMP response element binding protein (CREB), and histone H3; and recruitment of phospho-CREB to the apoptotic gene promoters. The miR-155-triggered activation of caspase-3, BAK1, and cytochrome c translocation involved signaling integration of MAPKs and epigenetic or posttranslational modification of histones or CREB. Importantly, M. bovis BCG infection-induced apoptosis was severely compromised in macrophages derived from miR-155 knockout mice. Gain-of-function and loss-of-function studies validated the requirement of miR-155 for M. bovis BCG's ability to trigger apoptosis. Overall, M. bovis BCG-driven miR-155 dictates cell fate decisions of infected macrophages, strongly implicating a novel role for miR-155 in orchestrating cellular reprogramming during immune responses to mycobacterial infection.

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Mycobacterium bovis BCG stimulates the TLR2-PI3K-PKCδ-MAPK pathway, overexpresses miR-155, indirectly upregulates PUMA, NOXA, BID, BIM, BAK1, and SMAC, leading to apoptosis and immunity.
“Mycobacterium bovis BCG, a strain used in vaccines, stimulates the TLR2-PI3K-PKCδ-MAPK pathway with subsequent overexpression of miR-155, further resulting in indirect (i.e., miR-155 targets PKI-α, a negative regulator of PKA), upregulation of PUMA, NOXA, BID, BIM, BAK1, and SMAC, and eventually to apoptosis, which results in acquiring immunity [209].”
From MicroRNAs as Regulators of Phagocytosis (2022) · cites this paper as [209]

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MicroRNA-155 induction by Mycobacterium bovis BCG enhances ROS production through targeting SHIP1
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Small Non-Coding RNAs: New Insights in Modulation of Host Immune Response by Intracellular Bacterial Pathogens
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MiR‐140 modulates the inflammatory responses of Mycobacterium tuberculosis‐infected macrophages by targeting TRAF6
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Authors: Ghorpade, D. S., Leyland, R., Kurowska-Stolarska, M., Patil, S. A., & Balaji, K. N.
Affiliations: Indian Institute of Science Bangalore (IN)
Babraham Institute (GB)
Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow, United Kingdom
National Institute of Mental Health and Neurosciences (IN)
ORCID: Ghorpade, Devram Sampat
Leyland, Rebecca
Patil, Shripad A.
Balaji, Kithiganahalli Narayanaswamy
Venue: Molecular and Cellular Biology
Publisher: Informa UK Limited
Published: 2012-06-01
Volume: 32
Issue: 12
Pages: 2239-2253
ISSN: 0270-7306 (ISSN-L)
1098-5549
DOI: 10.1128/mcb.06597-11
PMC: PMC3372268
OpenAlex: W2133418861
Cited by: 142
References: 73
Citations by year: 2026: 3 · 2025: 3 · 2024: 3 · 2023: 8 · 2022: 14 · 2021: 14 · 2020: 9 · 2019: 12 · 2018: 14 · 2017: 8 · 2016: 11 · 2015: 10 · 2014: 14 · 2013: 14 · 2012: 4
FWCI: 9.32
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Molecular and Cellular Biology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
NOT FOUND REPOSITORY (Indian Institute of Science Bangalore) (acceptedVersion)
ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
Funders: Indian Institute of Science
National Institute of Mental Health and Neurosciences
Department of Biotechnology, Ministry of Science and Technology, India
Indian Council of Medical Research
Versus Arthritis (19213)
National Institutes of Health
Center for Advanced Study, University of Illinois at Urbana-Champaign
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: miR-155, Mycobacterium bovis BCG, macrophage apoptosis, TLR2, PI3K signaling, protein kinase C delta, MAPK signaling, NF-κB, PKA signaling, CREB, histone H3 phosphorylation, MSK1, caspase-3, BAK1, cytochrome c translocation, mycobacterial infection, BCG vaccine, macrophage reprogramming
MeSH terms: Animals, Bacterial Vaccines, Cells, Cultured, Macrophages, Mycobacterium bovis, Phosphorylation, Signal Transduction, Apoptosis, Phosphatidylinositol 3-Kinases, MicroRNAs, Toll-Like Receptor 2, Mice, Transcription Factor RelA

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MicroRNA-155 Is Required for Mycobacterium bovis BCG-Mediated Apoptosis of Macrophages

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