Differential Targeting of c-Maf, Bach-1, and Elmo-1 by microRNA-143 and microRNA-365 Promotes the Intracellular Growth of Mycobacterium tuberculosis in Alternatively IL-4/IL-13 Activated Macrophages Article Swipe
Ousman Tamgue
,
Lorna Gcanga
,
Mumin Ozturk
,
Lauren Whitehead
,
Shandre Pillay
,
Raygaana Jacobs
,
Sugata Roy
,
Sebastian Schmeier
,
Malika Davids
,
Yulia A. Medvedeva
,
Keertan Dheda
,
Harukazu Suzuki
,
Frank Brombacher
,
Reto Guler
·
YOU?
·
· 2019
· Open Access
·
· DOI: https://doi.org/10.3389/fimmu.2019.00421
YOU?
·
· 2019
· Open Access
·
· DOI: https://doi.org/10.3389/fimmu.2019.00421
Mycobacterium tuberculosis (Mtb) can subvert the host defense by skewing macrophage activation toward a less microbicidal alternative activated state to avoid classical effector killing functions. Investigating the molecular basis of this evasion mechanism could uncover potential candidates for host directed therapy against tuberculosis (TB). A limited number of miRNAs have recently been shown to regulate host-mycobacterial interactions. Here, we performed time course kinetics experiments on bone marrow-derived macrophages (BMDMs) and human monocyte-derived macrophages (MDMs) alternatively activated with IL-4, IL-13, or a combination of IL-4/IL-13, followed by infection with Mtb clinical Beijing strain HN878. MiR-143 and miR-365 were highly induced in Mtb-infected M(IL-4/IL-13) BMDMs and MDMs. Knockdown of miR-143 and miR-365 using antagomiRs decreased the intracellular growth of Mtb HN878, reduced the production of IL-6 and CCL5 and promoted the apoptotic death of Mtb HN878-infected M(IL-4/IL-13) BMDMs. Computational target prediction identified c-Maf, Bach-1 and Elmo-1 as potential targets for both miR-143 and miR-365. Functional validation using luciferase assay, RNA-pulldown assay and Western blotting revealed that c-Maf and Bach-1 are directly targeted by miR-143 while c-Maf, Bach-1, and Elmo-1 are direct targets of miR-365. Knockdown of c-Maf using GapmeRs promoted intracellular Mtb growth when compared to control treated M(IL-4/IL-13) macrophages. Meanwhile, the blocking of Bach-1 had no effect and blocking Elmo-1 resulted in decreased Mtb growth. Combination treatment of M(IL-4/IL-13) macrophages with miR-143 mimics or miR-365 mimics and c-Maf, Bach-1, or Elmo-1 gene-specific GapmeRs restored Mtb growth in miR-143 mimic-treated groups and enhanced Mtb growth in miR-365 mimics-treated groups, thus suggesting the Mtb growth-promoting activities of miR-143 and miR-365 are mediated at least partially through interaction with c-Maf, Bach-1, and Elmo-1. We further show that knockdown of miR-143 and miR-365 in M(IL-4/IL-13) BMDMs decreased the expression of HO-1 and IL-10 which are known targets of Bach-1 and c-Maf, respectively, with Mtb growth-promoting activities in macrophages. Altogether, our work reports a host detrimental role of miR-143 and miR-365 during Mtb infection and highlights for the first time the role and miRNA-mediated regulation of c-Maf, Bach-1, and Elmo-1 in Mtb-infected M(IL-4/IL-13) macrophages.
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- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.3389/fimmu.2019.00421
- https://www.frontiersin.org/articles/10.3389/fimmu.2019.00421/pdf
- OA Status
- gold
- Cited By
- 39
- References
- 55
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W2924454231
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
-
https://openalex.org/W2924454231Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.3389/fimmu.2019.00421Digital Object Identifier
- Title
-
Differential Targeting of c-Maf, Bach-1, and Elmo-1 by microRNA-143 and microRNA-365 Promotes the Intracellular Growth of Mycobacterium tuberculosis in Alternatively IL-4/IL-13 Activated MacrophagesWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2019Year of publication
- Publication date
-
2019-03-19Full publication date if available
- Authors
-
Ousman Tamgue, Lorna Gcanga, Mumin Ozturk, Lauren Whitehead, Shandre Pillay, Raygaana Jacobs, Sugata Roy, Sebastian Schmeier, Malika Davids, Yulia A. Medvedeva, Keertan Dheda, Harukazu Suzuki, Frank Brombacher, Reto GulerList of authors in order
- Landing page
-
https://doi.org/10.3389/fimmu.2019.00421Publisher landing page
- PDF URL
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https://www.frontiersin.org/articles/10.3389/fimmu.2019.00421/pdfDirect link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
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https://www.frontiersin.org/articles/10.3389/fimmu.2019.00421/pdfDirect OA link when available
- Concepts
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Gene knockdown, Mycobacterium tuberculosis, microRNA, Intracellular, Molecular biology, Biology, Apoptosis, Chemistry, Tuberculosis, Cell biology, Medicine, Gene, Biochemistry, PathologyTop concepts (fields/topics) attached by OpenAlex
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39Total citation count in OpenAlex
- Citations by year (recent)
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2025: 2, 2024: 3, 2023: 4, 2022: 7, 2021: 13Per-year citation counts (last 5 years)
- References (count)
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55Number of works referenced by this work
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10Other works algorithmically related by OpenAlex
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| referenced_works | https://openalex.org/W2274570194, https://openalex.org/W2048692951, https://openalex.org/W2109484445, https://openalex.org/W2238742400, https://openalex.org/W2026016063, https://openalex.org/W144423133, https://openalex.org/W2116665225, https://openalex.org/W2085276736, https://openalex.org/W2065230752, https://openalex.org/W2060827500, https://openalex.org/W2080595107, https://openalex.org/W4313333717, https://openalex.org/W2088557228, https://openalex.org/W2133418861, https://openalex.org/W1537903189, https://openalex.org/W2037432461, https://openalex.org/W2129038286, https://openalex.org/W2588058521, https://openalex.org/W2038180405, https://openalex.org/W2168552645, https://openalex.org/W2607232908, https://openalex.org/W2793723628, https://openalex.org/W2408063023, https://openalex.org/W2949880186, https://openalex.org/W2094468530, https://openalex.org/W2066512300, https://openalex.org/W2811271319, https://openalex.org/W1498517665, https://openalex.org/W2806918138, https://openalex.org/W1966978281, https://openalex.org/W2027768860, https://openalex.org/W1999792045, https://openalex.org/W2019255399, https://openalex.org/W1966113758, https://openalex.org/W6714029009, https://openalex.org/W2025016149, https://openalex.org/W1996600340, https://openalex.org/W2065232902, https://openalex.org/W2018387247, https://openalex.org/W1985123329, https://openalex.org/W2134167837, https://openalex.org/W2072347527, https://openalex.org/W2022429639, https://openalex.org/W1992071574, https://openalex.org/W2598517284, https://openalex.org/W2620139340, https://openalex.org/W2003408748, https://openalex.org/W2095592851, https://openalex.org/W2120293851, https://openalex.org/W2118938986, https://openalex.org/W2150109976, https://openalex.org/W2063263528, https://openalex.org/W2071481601, https://openalex.org/W2302313082, https://openalex.org/W2762375963 |
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| abstract_inverted_index.IL-4, | 77 |
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| abstract_inverted_index.IL-13, | 78 |
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