Cited by 407Mitochondrial Function and PathologyLiver Disease Diagnosis and TreatmentMetabolism, Diabetes, and Cancer

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Elevated TCA cycle function in the pathology of diet-induced hepatic insulin resistance and fatty liver

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Satapati, Santhosh, Sunny, Nishanth E., Kucejova, Blanka, Fu, Xiaorong, He, Tian Teng, Méndez-Lucas, Andrés, Shelton, John M., Perales, Jose C., Browning, Jeffrey D., Burgess, Shawn C.·2012·Journal of Lipid Research

DOI 10.1194/jlr.m023382PMC PMC3351815

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Abstract

The manner in which insulin resistance impinges on hepatic mitochondrial function is complex. Although liver insulin resistance is associated with respiratory dysfunction, the effect on fat oxidation remains controversial, and biosynthetic pathways that traverse mitochondria are actually increased. The tricarboxylic acid (TCA) cycle is the site of terminal fat oxidation, chief source of electrons for respiration, and a metabolic progenitor of gluconeogenesis. Therefore, we tested whether insulin resistance promotes hepatic TCA cycle flux in mice progressing to insulin resistance and fatty liver on a high-fat diet (HFD) for 32 weeks using standard biomolecular and in vivo (2)H/(13)C tracer methods. Relative mitochondrial content increased, but respiratory efficiency declined by 32 weeks of HFD. Fasting ketogenesis became unresponsive to feeding or insulin clamp, indicating blunted but constitutively active mitochondrial β-oxidation. Impaired insulin signaling was marked by elevated in vivo gluconeogenesis and anaplerotic and oxidative TCA cycle flux. The induction of TCA cycle function corresponded to the development of mitochondrial respiratory dysfunction, hepatic oxidative stress, and inflammation. Thus, the hepatic TCA cycle appears to enable mitochondrial dysfunction during insulin resistance by increasing electron deposition into an inefficient respiratory chain prone to reactive oxygen species production and by providing mitochondria-derived substrate for elevated gluconeogenesis.

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BackgroundMethodInfluential
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Self-citation
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Background
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“Moreover, rather than detecting oxidation metabolism through in vivo 2H/13C tracer methods (Satapati et al, 2015; Satapati et al, 2012), we used HRR to obtain the maximal mitochondrial OXPHOS capacity with excess substrates and ADP in isolated hepatic mitochondria.”
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Method
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MethodInfluential
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Background
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Method
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Background
In Vivo Estimation of Ketogenesis Using Metabolic Flux Analysis—Technical Aspects and Model Interpretation
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“91 μmol/hr, respectively) similar to previous studies [28,29,54].”
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“Finally, MSDC-0602K was tested in a phase 2b clinical trial for patients with NASH and, although it failed to achieve its primary endpoint (histologic improvements in NASH), MSDC-0602K reduced hepatic steatosis and lowered circulating levels of transaminases and other NASH biomarkers [39].”
BackgroundInfluential
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“Impaired ketogenesis induced by an obesogenic diet or/and by genetic manipulation is linked to an increase in TCA flux, gluconeogenesis, oxidative stress, and severe inflammation in both mice and humans [49,50,53].”
Background
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“Mitochondrial oxidative networks in the liver, which include β-oxidation, ketogenesis, tricarboxylic acid (TCA) cycle and electron transport chain, adapt and remodel in response to different nutrient and hormonal cues under normal physiological states and during stages of insulin resistance (Satapati et al., 2012; Kol…”
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“The citrate cycle is the main source of energy for cells, and an elevated citrate cycle can be found in the diabetic mouse liver due to insulin resistance (Satapati et al., 2012).”
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Identification of multiple dysregulated metabolic pathways by GC-MS-based profiling of liver tissue in mice with OVA-induced asthma exposed to PM2.5
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[13C]bicarbonate labelled from hyperpolarized [1-13C]pyruvate is an in vivo marker of hepatic gluconeogenesis in fasted state.
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“Moreover, oxidative stress is considered to be an important stage in the development of steatohepatitis, being the consequence of mitochondrial dysfunction that generates ROS species and favors the dysfunction of DNA, lipid, and protein membranes [50,51].”
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Proteomic study of gamma-oryzanol preventive effect on a diet-induced non-alcoholic fatty liver disease model
Siqueira, J. S., Garcia, J. L., Ferron, A. J. T., Moreto, F., Sormani, L. E., Costa, M. R., Palacio, T. L. N., Nai, G. A., Aldini, G., Francisqueti‐Ferron, F. V., et al. (2024) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2024.109607 · Cited by 10
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Stress du réticulum endoplasmique et stéatopathies métaboliques
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“Cependant, au cours de l’obésité, la b-oxydation des acides gras et l’activité du cycle de Krebs peuvent être temporairement augmentées dans les foiesdes souris et depatientsobèses (Satapati et al., 2012).”
Background
Investigation of Obesity-Alleviation Effect of Eurycoma longifolia on Mice Fed with a High-Fat Diet through Metabolomics Revealed Enhanced Decomposition and Inhibition of Accumulation of Lipids
Zhang, D., Zheng, W. L., Li, X., Ge, L., Ye, N., Liu, Y., Li, A., Liu, X., Zhang, R., Cheng, J., et al. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.1c00015 · Cited by 10
Dietary Macronutrient Composition Differentially Modulates the Remodeling of Mitochondrial Oxidative Metabolism during NAFLD
Kattapuram, N., Zhang, C., Muyyarikkandy, M. S., Surugihalli, C., Muralidaran, V., Gregory, T., & Sunny, N. E. (2021) · Metabolites · doi:10.3390/metabo11050272 · Cited by 10
“Chronic exposure to diets rich in fat/lipid calories or refined carbohydrate calories (usually from fructose) are common strategies to induce insulin resistance and NAFLD in rodent models [4,17,18].”
BackgroundMethodInfluentialSelf-citation
[13C]bicarbonate labelled from hyperpolarized [1-13C]pyruvate is an in vivo marker of hepatic gluconeogenesis in fasted state
Can, E., Bastiaansen, J., Couturier, D., Gruetter, R., Yoshihara, H. A. I., & Comment, A. (2022) · Communications Biology · doi:10.1038/s42003-021-02978-2 · Cited by 10
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“Pathways including “Fructose and mannose metabolism”, “Starch and sucrose metabolism”, “Pentose phosphate pathway”, “Citrate cycle (TCA cycle)”, “Fatty acid biosynthesis”, and “Biosynthesis of unsaturated fatty acids”, contribute to glycolysis, resulting in production of ATPs, which helps to improve various metabolism…”
Background
Analysis of the metabolic switch induced by the spirulina peptide SP6 in high fat diet ApoE-/- mice model: A direct infusion FT-ICR-MS based approach
Sommella, E., Carrizzo, A., Merciai, F., Sarno, V. D., Carbone, D., Lucia, M. D., Musella, S., Vecchione, C., & Campiglia, P. (2020) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2020.113865 · Cited by 10
Insulin Resistance, but Not Obstructive Sleep Apnea Is Associated with Hepatic Steatosis in Chinese Patients with Severe Obesity
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Loss of ovarian function prevents exercise-induced activation of hepatic mitophagic flux
Franczak, E., Kugler, B. A., Salathe, S. F., Allen, J., Sardiu, M. E., McCoin, C. S., Hevener, A. L., Morris, E. M., & Thyfault, J. P. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00107.2025 · Cited by 9
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Feeding medium-chain fatty acid-rich formula causes liver steatosis and alters hepatic metabolism in neonatal pigs
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A high-protein diet is anti-steatotic and has no pro-inflammatory side effects in dyslipidaemic APOE2 knock-in mice
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“The subsequent loss of insulin sensitivity then allows an increased rate of gluconeogenesis and mitochondrial TCA cycle metabolism((6)).”
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Machine Learning-Based Plasma Metabolomics in Liraglutide-Treated Type 2 Diabetes Mellitus Patients and Diet-Induced Obese Mice
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“During insulin resistance, impaired mitochondrial respiration increases the metabolic fluxes of gluconeogenesis and the citric acid cycle, which subsequently leads to oxidative stress and recruitment of pro-inflammatory cytokines, such as tumor necrosis factor-α (TNF-α ) and interleukin 6 [39].”
Background
A comparative genomic study across 396 liver biopsies provides deep insight into FGF21 mode of action as a therapeutic agent in metabolic dysfunction‐associated steatotic liver disease
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“As the activity of these enzymes is regulated by insulin (Feldhoff et al., 1993; Satapati et al., 2012), it is suggested that central insulin resistance plays a role in this disease.”
Using liquid chromatography mass spectrometry (LC-MS) to assess the effect of age, high-fat diet, and rat strain on the liver metabolome
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“In obese persons with fatty livers, the rate of ketogenesis is reduced by an increase in hepatic TG loading, and a decreased turnover rate is shown with severe insulin resistance, presumably contributing to hypoketonemia, when compared to lean controls in animal models [65,66].”
Background
Metagenomic signatures reveal the key role of phloretin in amelioration of gut dysbiosis attributed to metabolic dysfunction-associated fatty liver disease by time-dependent modulation of gut microbiome
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“Diet-induced hepatic insulin resistance and fatty liver have been attributed to an elevated TCA cycle (Satapati et al., 2012).”
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Metabolomics reveals altered metabolites in cirrhotic patients with severe portal hypertension in Tibetan population
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Deciphering Blood Flow Restriction Training to Aid Lipid Lowering in Obese College Students through Untargeted Metabolomics
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“The whole chemical process is capable of generating two-thirds of the food energy source; thus, in combination with the above analyses, as well as the results of the present study, it is clear that the TCA cycle is an extremely important metabolic pathway in organisms [53,54].”
Result
Accumulation of succinate in the blood is a potential early indicator of metabolic dysfunction-associated steatotic liver disease (MASLD)
Chalifoux, O., Dagostino, C., Li, M., Trezza, S., Grayson, C., Russo, M. D. S. T., Avizonis, D. Z., Michalak, M., Agellon, L. B., & Mailloux, R. J. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.09.029 · Cited by 9
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Background
Estimated glucose disposal rate mediates the association between Life’s Crucial 9 and congestive heart failure: a population-based study
Wang, L., Xu, Y., Chen, L., & Zhang, H. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1540794 · Cited by 6

Authors: Satapati, S., Sunny, N. E., Kucejova, B., Fu, X., He, T. T., Méndez-Lucas, A., Shelton, J. M., Perales, J. C., Browning, J. D., & Burgess, S. C.
Affiliations: The University of Texas Southwestern Medical Center (US)
Universitat de Barcelona (ES)
Corresponding author: Burgess, Shawn C.
ORCID: Satapati, Santhosh
Sunny, Nishanth E.
Fu, Xiaorong
Shelton, John M.
Perales, Jose C.
Burgess, Shawn C.
Venue: Journal of Lipid Research
Publisher: Elsevier BV
Published: 2012-06
Volume: 53
Issue: 6
Pages: 1080-1092
ISSN: 0022-2275 (ISSN-L)
DOI: 10.1194/jlr.m023382
PMC: PMC3351815
OpenAlex: W2036097574
Cited by: 407
References: 70
Citations by year: 2026: 19 · 2025: 33 · 2024: 23 · 2023: 41 · 2022: 35 · 2021: 30 · 2020: 44 · 2019: 36 · 2018: 25 · 2017: 24 · 2016: 31 · 2015: 23 · 2014: 22 · 2013: 17 · 2012: 2
FWCI: 8.22
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 3004 d)
Locations: Journal of Lipid Research (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (P01DK058398, R01DK087977, R01DK078184)
National Institute of Dental and Craniofacial Research (UL1DE019584)
National Center for Research Resources (P41RR002584, RR‐02584)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Keywords: TCA cycle, hepatic insulin resistance, high-fat diet, mitochondrial dysfunction, mitochondrial respiration, fat oxidation, ketogenesis, gluconeogenesis, oxidative stress, inflammation, insulin signaling, reactive oxygen species, mitochondrial beta-oxidation
MeSH terms: Animals, Citric Acid Cycle, Fatty Liver, Gluconeogenesis, Hyperglycemia, Insulin Resistance, Ketone Bodies, Liver, Male, Mice, Inbred C57BL, Mitochondria, Obesity, Time Factors, Oxidative Stress, Cell Respiration, Mice, Diet, High-Fat

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Elevated TCA cycle function in the pathology of diet-induced hepatic insulin resistance and fatty liver

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