BNIP3L/Nix-induced mitochondrial fission, mitophagy, and impaired myocyte glucose uptake are abrogated by PRKA/PKA phosphorylation
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Abstract
Abstract Lipotoxicity is a form of cellular stress caused by the accumulation of lipids resulting in mitochondrial dysfunction and insulin resistance in muscle. Previously, we demonstrated that the mitophagy receptor Nix is responsive to lipotoxicity and accumulates in response to diacylglycerols induced by high-fat (HF) feeding. In addition, previous studies have implicated autophagy and mitophagy in muscle insulin sensitivity. To provide a better understanding of these observations, we undertook gene expression array and shot-gun metabolomics studies in soleus muscle from rodents on an HF diet. Interestingly, we observed a modest reduction in several autophagy-related genes including Beclin-1, ATG3, and -5. Moreover, we observed alterations in the fatty acyl composition of cardiolipins and phosphatidic acids. Given the previously reported roles of these phospholipids and Nix in mitochondrial dynamics, we investigated aberrant mitochondrial fission and turn-over as a mechanism of myocyte insulin resistance. In a series of gain-of-function and loss-of-function experiments in rodent and human myotubes, we demonstrate that Nix accumulation triggers mitochondrial depolarization, fragmentation, calcium-dependent activation of DRP1, and mitophagy. In addition, Nix-induced mitochondrial fission leads to myotube insulin resistance through activation of mTOR-p70S6 kinase inhibition of IRS1, which is contingent on phosphatidic acids and Rheb. Finally, we demonstrate that Nix-induced mitophagy and insulin resistance can be reversed by direct phosphorylation of Nix by PKA, leading to the translocation of Nix from the mitochondria and sarcoplasmic reticulum to the cytosol. These findings provide insight into the role of Nix-induced mitophagy and myocyte insulin resistance during an overfed state when overall autophagy-related gene expression is reduced. Furthermore, our data suggests a mechanism by which exercise or pharmacological activation of PKA may overcome myocyte insulin resistance. Graphical Abstract
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Mitochondrial dysfunction and impaired cell death pathways downstream contribute to insulin resistance in the muscle tissue of gestational diabetes mellitus-exposed offspring.
“Consequently, mitochondrial dysfunction and impaired cell death pathways downstream contribute to insulin resistance in the muscle tissue of GDM-exposed offspring [105,106].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [105]
The Introduction and Discussion (page unavailable) link mitochondrial dysfunction, mitophagy, and impaired insulin signaling in muscle under lipotoxic or high-fat conditions. They do not establish this pathway in GDM-exposed offspring or show that impaired cell-death pathways downstream contribute to their insulin resistance. The Methods describe high-fat-fed rats, not a GDM-exposed offspring model. (LLM, conf=0.88)
Experimental — accuracy not yet measuredOffspring exposed to gestational diabetes mellitus exhibited skeletal muscle lipotoxicity and insulin resistance.
“Subsequent studies using this approach have demonstrated that offspring exposed to GDM exhibited skeletal muscle lipotoxicity and insulin resistance [105,106] (Figure 1).”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [105]
The Results (Metabolomics and gene expression screen) report elevated lipids in the soleus muscle of high-fat-fed rats, and the Discussion describes a lipotoxicity-related pathway that impairs insulin signaling. The paper does not report these findings in offspring exposed to gestational diabetes: its Materials and methods describe rats assigned to low- or high-fat diets after weaning. The References mention gestational-diabetes-exposed offspring only in the title of a study about hepatic steatosis. (LLM, conf=0.85)
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- Authors
- da Silva Rosa, S. C., Martens, M. D., Field, J. T., Nguyen, L., Kereliuk, S. M., Hai, Y., Chapman, D., Diehl-Jones, W., Aliani, M., West, A. R., Thliveris, J., Ghavami, S., Rampitsch, C., Dolinsky, V. W., & Gordon, J. W.
- Affiliations
- Departments of Human Anatomy and Cell Science, University of Manitoba, Winnipeg, Canada
- Children's Hospital Research Institute of Manitoba (CA)
- Children’s Hospital Research Institute of Manitoba, University of Manitoba, Winnipeg, Canada
- Human Nutritional Science
- University of Manitoba (CA)
- Agriculture and Agri-Food Canada (CA)
- Corresponding author
- Gordon, Joseph W.
- ORCID
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2020-10-12
- Volume
- 17
- Issue
- 9
- Pages
- 2257-2272
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC8496715
- OpenAlex
- W3092101056
- Cited by
- 117
- References
- 69
- Citations by year
- 2026: 13 · 2025: 20 · 2024: 28 · 2023: 19 · 2022: 16 · 2021: 19 · 2020: 2
- FWCI
- 10.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Autophagy (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- Mspace (University of Manitoba) (submittedVersion)
- Figshare (cc-by)
- Funders
- Canadian Institutes of Health Research (N/A)
- Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (N/A)
- Children’s Hospital Research Institute of Manitoba (N/A)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- BNIP3L/NIX, lipotoxicity, mitochondrial fission, mitophagy, glucose uptake, Drp1, mitochondrial depolarization, cardiolipin, phosphatidic acid, Rheb, mTOR signaling, IRS-1, high-fat diet, soleus muscle
- MeSH terms
- Animals, Autophagy, Cells, Cultured, Glucose, Humans, Membrane Proteins, Phosphorylation, Proto-Oncogene Proteins, Mitochondrial Proteins, Tumor Suppressor Proteins, Muscle Cells, Mitochondrial Dynamics, Mitophagy
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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