mTORC2 deficiency alters the metabolic profile of conventional dendritic cells
Open accessAbstract
In myeloid dendritic cells (DC), deletion of the mechanistic target of rapamycin complex 2 (TORC2) results in an augmented pro-inflammatory phenotype and T cell stimulatory activity; however, the underlying mechanism has not been resolved. Here, we demonstrate that mouse bone marrow-derived TORC2-deficient myeloid DC (TORC2-/- DC) utilize an altered metabolic program, characterized by enhanced baseline glycolytic function compared to wild-type WT control (Ctrl) DC, increased dependence on glycolytic ATP production, elevated lipid content and higher viability following stimulation with LPS. In addition, TORC2-/- DC display an increased spare respiratory capacity (SRC) compared to WT Ctrl DC; this metabolic phenotype corresponds with increased mitochondrial mass and mean mitochondrial DNA copy number, and failure of TORC2-/- DC mitochondria to depolarize following LPS stimulation. Our data suggest that the enhanced metabolic activity of TORC2-/- DC may be due to compensatory TORC1 pathway activity, namely increased expression of multiple genes upstream of Akt/TORC1 activity, including the integrin alpha IIb, protein tyrosine kinase 2/focal adhesion kinase, IL-7R and Janus kinase 1(JAK1), and the activation of downstream targets of TORC1, including p70S6K, eukaryotic translation initiation factor 4E binding protein 1 (4EBP1) and CD36 (fatty acid translocase). These enhanced TORC1 pathway activities may culminate in increased expression of the nuclear receptor peroxisome proliferator-activated receptor γ (Pparγ) that regulates fatty acid storage, and the transcription factor sterol regulatory element-binding transcription factor 1 (Srebf1). Taken together, our data suggest that TORC2 may function to restrain TORC1-driven metabolic activity and mitochondrial regulation in myeloid DC.
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Data suggest that mTORC2 stimulates mitochondrial biogenesis in liver and myeloid dendritic cells, although equivocal data exist in macrophages from Rictor-knockout mice.
“Interestingly, data suggest that mTORC2 stimulates mitochondrial biogenesis in liver (Betz et al., 2013) and myeloid dendritic cells (Watson et al., 2019), although equivocal data exist in macrophages from Rictor-knockout mice (Oh et al., 2017).”
From Skeletal Muscle Ribosome and Mitochondrial Biogenesis in Response to Different Exercise Training Modalities (2021) · cites this paper as Watson et al., 2019
The cited paper reports the opposite direction for myeloid dendritic cells: TORC2-deficient cells had increased mitochondrial biomass and mean mitochondrial DNA copy number (Results, page not provided). The Discussion suggests that TORC2 may restrain, rather than stimulate, mitochondrial regulation in these cells. The liver and macrophage clauses cite other papers and are not attributed to Watson et al. (LLM, conf=0.88)
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- Authors
- Watson, A. R., Dai, H., Zheng, Y., Nakano, R., Giannou, A. D., Menk, A. V., Stolz, D. B., Delgoffe, G. M., & Thomson, A. W.
- Affiliations
- University of Pittsburgh (US)
- University Medical Center Hamburg-Eppendorf (DE)
- Corresponding author
- Thomson, Angus W.
- ORCID
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2019-07-02
- Volume
- 10
- Pages
- 1451-1451
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC6626913
- OpenAlex
- W2954300524
- Cited by
- 15
- References
- 58
- Citations by year
- 2025: 2 · 2024: 1 · 2022: 3 · 2021: 6 · 2020: 3
- FWCI
- 1.20
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (R01 AI118777, R01 AI67541)
- National Natural Science Foundation of China (81800664)
- Natural Science Foundation of Hunan Province (2019JJ50842)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- mTORC2, myeloid dendritic cells, dendritic cell metabolism, glycolysis, spare respiratory capacity, mitochondrial function, TORC1, PPARγ, SREBF1, fatty acid storage, lipopolysaccharide stimulation, T cell activation, pro-inflammatory phenotype, CD36, p70S6K, 4E-BP1
- MeSH terms
- Mechanistic Target of Rapamycin Complex 1, Mechanistic Target of Rapamycin Complex 2, Animals, Dendritic Cells, DNA, Mitochondrial, Glycolysis, Golgi Apparatus, Lipopolysaccharides, Mice, Inbred C57BL, Mice, Transgenic, Mitochondria, Phenotype, Signal Transduction, NF-kappa B, Cell Respiration, Sirolimus, Ribosomal Protein S6 Kinases, 70-kDa, Mice, Transcriptome, Lipid Droplets
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