Paradoxical effect of mitochondrial respiratory chain impairment on insulin signaling and glucose transport in adipose cells.
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Adipocyte function is crucial for the control of whole body energy homeostasis. Pathway analysis of differentiating 3T3-L1 adipocytes reveals that major metabolic pathways induced during differentiation involve mitochondrial function. However, it is not clear why differentiated white adipocytes require enhanced respiratory chain activity relative to pre-adipocytes. To address this question, we used small interference RNA to interfere with the induction of the transcription factor Tfam, which is highly induced between days 2 and 4 of differentiation and is crucial for replication of mitochondrial DNA. Interference with Tfam resulted in cells with decreased respiratory chain capacity, reflected by decreased basal oxygen consumption, and decreased mitochondrial ATP synthesis, but no difference in many other adipocyte functions or expression levels of adipose-specific genes. However, insulin-stimulated GLUT4 translocation to the cell surface and subsequent glucose transport are impaired in Tfam knockdown cells. Paradoxically, insulin-stimulated Akt phosphorylation is significantly enhanced in these cells. These studies reveal independent links between mitochondrial function, insulin signaling, and glucose transport, in which impaired respiratory chain activity enhances insulin signaling to Akt phosphorylation, but impairs GLUT4 translocation. These results indicate that mitochondrial respiratory chain dysfunction in adipocytes can cause impaired insulin responsiveness of GLUT4 translocation by a mechanism downstream of the Akt protein kinase.
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Among the mitochondrial functions that may be relevant for white adipose tissue function are the anaplerotic generation of metabolic intermediates for fatty acid synthesis and esterification, the maintenance of a robust pathway for the folding and secretion of high abundance circulating proteins such as adiponectin, and interactions between mitochondrial function and components of the insulin-sign
“Among the mitochondrial functions that may be relevant for white adipose tissue function are the anaplerotic generation of metabolic intermediates for fatty acid synthesis and esterification (159), the maintenance of a robust pathway for the folding and secretion of high abundance circulating proteins such as adiponectin (160), and interactions between mitochondrial function and components of the”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [161]
Decreased mitochondrial capacity in adipocytes may also alter adipocyte insulin sensitivity and/or function due to the high energetic requirements for fatty acid storage, adipokine secretion, insulin signaling, and glucose uptake.
“In addition to effects on fuel utilization, decreased mitochondrial capacity in adipocytes may also alter adipocyte insulin sensitivity and/or function due to the high energetic requirements for fatty acid storage, adipokine secretion (160), insulin signaling (161), and glucose uptake.”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [161]
In cultured adipocytes, impairment of respiratory chain function through depletion of Tfam during adipocyte differentiation results in impaired insulin-stimulated glucose transport.
“Interestingly, in cultured adipocytes, impairment of respiratory chain function through depletion of Tfam during adipocyte differentiation results in impaired insulinstimulated glucose transport (161); data in animal models are necessary to determine the physiological relevance of this finding.”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [161]
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- Authors
- Shi, X., Burkart, A., Nicoloro, S. M., Czech, M. P., Straubhaar, J., & Corvera, S.
- Affiliations
- University of Massachusetts Chan Medical School (US)
- Corresponding author
- Corvera, Silvia
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2008-11
- Volume
- 283
- Issue
- 45
- Pages
- 30658-30667
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC2576555
- OpenAlex
- W2066447432
- Cited by
- 70
- References
- 48
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 1 · 2023: 2 · 2022: 5 · 2021: 1 · 2020: 2 · 2019: 9 · 2018: 2 · 2017: 2 · 2016: 4 · 2015: 7 · 2014: 1 · 2013: 6 · 2012: 5
- FWCI
- 3.78
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 32520, DK-60837, P30DK032520, R01DK060837)
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- mitochondrial respiratory chain, adipocytes, insulin signaling, glucose transport, GLUT4 translocation, Akt phosphorylation, TFAM, 3T3-L1 adipocyte differentiation, mitochondrial function, insulin resistance, white adipose tissue
- MeSH terms
- Adenosine Triphosphate, Animals, Biological Transport, Cell Differentiation, DNA-Binding Proteins, Electron Transport, Glucose, High Mobility Group Proteins, Hypoglycemic Agents, Insulin, Mitochondria, Oxygen Consumption, Phosphorylation, Time Factors, Signal Transduction, Adipocytes, RNA, Small Interfering, 3T3-L1 Cells, Proto-Oncogene Proteins c-akt, Glucose Transporter Type 4, Mice
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