Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle

Corpeleijn, E.; Saris, W. H. M.; Blaak, E. E.

doi:10.1111/j.1467-789x.2008.00544.x

Cited by 280Metabolism, Diabetes, and CancerAdipose Tissue and MetabolismDiabetes, Cardiovascular Risks, and Lipoproteins

Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle

Corpeleijn, E., Saris, W. H. M., Blaak, E. E.·2009·Obesity Reviews

DOI 10.1111/j.1467-789x.2008.00544.x

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Abstract

Summary: Lipotoxicity in skeletal muscle plays a critical role in the aetiology of insulin resistance and type 2 diabetes mellitus by interference of lipid metabolites with insulin signalling and action. The dynamics of lipid oxidation and fine tuning with fatty acid uptake and intramyocellular triacylglycerol turnover may be very important to limit the accumulation of lipid intermediates. The use of metabolic inflexibility, defined as the impaired capacity to increase fat oxidation upon increased fatty acid availability and to switch between fat and glucose as the primary fuel source after a meal, does more justice to the complexity of changes in fuel oxidation during the day. Fatty acid availability, uptake and oxidation all play a role in metabolic flexibility and insulin resistance. During high fatty acid availability, fatty acid transporters may limit cellular and mitochondrial fatty acid uptake and thus limit fat oxidation. After a meal, when the demand for fatty acids as fuel is low, an increased fractional extraction of lipids from plasma may promote intramyocellular lipid accumulation and insulin resistance. Furthermore, defects in fuel switching cluster together with impaired mitochondrial content and/or function. Lifestyle changes in dietary fat intake, physical activity and weight loss may improve metabolic flexibility in skeletal muscle, and thereby contribute to the prevention of type 2 diabetes.

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Exercise and nutrition affect the supply and demand aspects of metabolism and have been shown to influence intramyocellular lipid levels in aging and obesity.
“they affect the supply and demand aspects of metabolism, respectively, and have been shown to influence IMCL levels in both aging and obesity [59, 97, 99, 101, 102].”
From Targeting Intramyocellular Lipids to Improve Aging Muscle Function (2025) · cites this paper as [102]
In obese, insulin resistant, and T2DM individuals, the beneficial effects of weight loss on postprandial glycemia and IR are mostly due to decreased blood levels of NEFA and to an improvement in the insulin-mediated suppression of fat oxidation.
“In the obese, insulin resistant, and T2DM individuals, the beneficial effects of weight loss on postprandial glycemia and IR are mostly due to the decreased blood levels of NEFA [110,111] and to an improvement in the insulin-mediated suppression of fat oxidation [112].”
From Effects of diet, lifestyle, Chrononutrition and alternative dietary interventions on postprandial Glycemia and insulin resistance (2022) · cites this paper as [111]
Weight loss alone is effective in improving insulin sensitivity, but it is more likely to improve fasting fat oxidation and mitochondrial function if combined with exercise training.
“It has been shown that weight loss alone is effective in improving insulin sensitivity, but it is more likely to improve fasting fat oxidation and mitochondrial function if combined with exercise training [111].”
From Effects of diet, lifestyle, Chrononutrition and alternative dietary interventions on postprandial Glycemia and insulin resistance (2022) · cites this paper as [111]
Metabolic inflexibility can already be observed in pre-diabetic individuals suffering from insulin resistance.
“Interestingly, metabolic inflexibility can already be observed in pre-diabetic individuals suffering from insulin resistance (Corpeleijn et al, 2009), limiting the ability to switch from fatty acid breakdown to fat storage after a meal and vice versa (Kelley, 2005).”
From Mitochondrial response to nutrient availability and its role in metabolic disease (2014) · cites this paper as Corpeleijn et al, 2009
Lipid accumulation in non-adipose tissues is highly associated with insulin resistance.
“but lipid accumulation in non-adipose tissues is also highly associated with insulin resistance (Canto & Auwerx, 2009; Corpeleijn et al, 2009; Schooneman et al, 2013).”
From Mitochondrial response to nutrient availability and its role in metabolic disease (2014) · cites this paper as Corpeleijn et al, 2009

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Plasma Free Fatty Acid Uptake and Oxidation Are Already Diminished in Subjects at High Risk for Developing Type 2 Diabetes
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Beta-adrenergic stimulation of energy expenditure and forearm skeletal muscle metabolism in lean and obese men
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Insulin stimulates fatty acid transport by regulating expression of FAT/CD36 but not FABPpm
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Differential Utilization of Saturated Palmitate and Unsaturated Oleate
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Impaired skeletal muscle substrate oxidation in glucose-intolerant men improves after weight loss
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Effects of epinephrine infusion on adipose tissue: interactions between blood flow and lipid metabolism
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Is Membrane Transport of FFA Mediated by Lipid, Protein, or Both?
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Fat Oxidation before and after a High Fat Load in the Obese Insulin-Resistant State
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Training-induced alterations in fat and carbohydrate metabolism during exercise in elderly subjects
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Direct association of a promoter polymorphism in the CD36/FAT fatty acid transporter gene with Type 2 diabetes mellitus and insulin resistance
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Dietary supplementation of very long-chain n-3 fatty acids decreases whole body lipid utilization in the rat
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Elevated intramyocellular lipid concentration in obese subjects is not reduced after diet and exercise training
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Peroxisome proliferator-activated receptor-γ coactivator-1 and insulin resistance: acute effect of fatty acids
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Thiazolidinediones upregulate impaired fatty acid uptake in skeletal muscle of type 2 diabetic subjects
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Regulation of lipid metabolism in adipose tissue during early starvation
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Impaired free fatty acid uptake in skeletal muscle but not in myocardium in patients with impaired glucose tolerance: studies with PET and 14(R,S)-[18F]fluoro-6-thia-heptadecanoic acid.
Turpeinen, A., Takala, T., Nuutila, P., Axelin, T., Luotolahti, M., Haaparanta‐Solin, M., Bergman, J. R., Hämäläinen, H., Iida, H., Mäki, M. T., et al. (1999) · Diabetes · doi:10.2337/diabetes.48.6.1245 · Cited by 65 · see citing works
Substrate source utilisation in long-term diagnosed type 2 diabetes patients at rest, and during exercise and subsequent recovery
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Exercise and insulin increase muscle fatty acid uptake by recruiting putative fatty acid transporters to the sarcolemma
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Dissociation between Fat-Inducedin VivoInsulin Resistance and Proximal Insulin Signaling in Skeletal Muscle in Men at Risk for Type 2 Diabetes
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Long‐chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart‐type‐FABP null mice
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Exercise training decreases the concentration of malonyl-CoA and increases the expression and activity of malonyl-CoA decarboxylase in human muscle
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Free fatty acid transport across adipocytes is mediated by an unknown membrane protein pump
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Skeletal muscle metabolic characteristics before and after energy restriction in human obesity: fibre type, enzymatic β‐oxidative capacity and fatty acid‐binding protein content
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Weight Reduction and the Impaired Plasma-Derived Free Fatty Acid Oxidation in Type 2 Diabetic Subjects1
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Adipose tissue function in the insulin-resistance syndrome
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Lifestyle changes and lipid metabolism gene expression and protein content in skeletal muscle of subjects with impaired glucose tolerance
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Dietary fat and the etiology of type 2 diabetes: an epidemiological perspective.
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Weight Reduction and the Impaired Plasma-Derived Free Fatty Acid Oxidation in Type 2 Diabetic Subjects
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Insulin acutely upregulates protein expression of the fatty acid transporter CD36 in human skeletal muscle in vivo.
Corpeleijn, E., Pelsers, M. M. A. L., Soenen, S., Mensink, M., Bouwman, F. G., Kooi, M. E., Saris, W. H. M., Glatz, J. F. C., & Blaak, E. E. (2008) · PubMed · Cited by 35 · see citing works
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Adipose tissue, hepatic, and skeletal muscle insulin sensitivity in extremely obese subjects with acanthosis nigricans
Reeds, D. N., Stuart, C. A., Perez, O., & Klein, S. (2006) · Metabolism · doi:10.1016/j.metabol.2006.08.006 · Cited by 30 · see citing works
High carbohydrate availability increases LCFA uptake and decreases LCFA oxidation in perfused muscle
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Differences in postprandial responses to fat and carbohydrate loads in habitual high and low fat consumers (phenotypes)
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Lifestyle Intervention and Fatty Acid Metabolism in Glucose‐Intolerant Subjects
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Inflexibility of energy substrate oxidation in type 1 diabetic patients
Wohl, P., Wohl, P., Girman, P., & Pelikánová, T. (2004) · Metabolism · doi:10.1016/j.metabol.2003.12.013 · Cited by 24 · see citing works
Heterogeneity in limb fatty acid kinetics in type 2 diabetes
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Dysregulation of muscle fatty acid metabolism in type 2 diabetes is independent of malonyl-CoA
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Effects of Intrabrachial Metacholine Infusion on Muscle Capillary Recruitment and Forearm Glucose Uptake during Physiological Hyperinsulinemia in Obese, Insulin-Resistant Individuals
Murdolo, G., Sjöstrand, M., Strindberg, L., Guðbjörnsdóttir, S., Lind, L., Lönnroth, P., & Jansson, P. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2737 · Cited by 19 · see citing works

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Short-chain fatty acids in control of body weight and insulin sensitivity
Canfora, E. E., Jocken, J. W., & Blaak, E. E. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.128 · Cited by 2,298 · see citing works
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Gut microbial metabolites in obesity, NAFLD and T2DM
Canfora, E. E., Meex, R. C. R., Venema, K., & Blaak, E. E. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0156-z · Cited by 1,493 · see citing works
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Trends in insulin resistance: insights into mechanisms and therapeutic strategy
Li, M., Chi, X., Wang, Y., Setrerrahmane, S., Xie, W., & Xu, H. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01073-0 · Cited by 939 · see citing works
The role of the gut microbiome and its metabolites in metabolic diseases
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Dietary Strategies for Metabolic Syndrome: A Comprehensive Review
Castro‐Barquero, S., Ruiz-León, A. M., Sierra-Pérez, M., Estruch, R., & Casas, R. M. (2020) · Nutrients · doi:10.3390/nu12102983 · Cited by 514 · see citing works
Correlation between Oxidative Stress, Nutrition, and Cancer Initiation
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Colonic infusions of short-chain fatty acid mixtures promote energy metabolism in overweight/obese men: a randomized crossover trial
Canfora, E. E., van der Beek, C. M., Jocken, J. W. E., Goossens, G. H., Holst, J. J., Olde Damink, S. W. M., Lenaerts, K., Dejong, C. H. C., & Blaak, E. E. (2017) · Scientific Reports · doi:10.1038/s41598-017-02546-x · Cited by 331 · see citing works
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Do nutrient-gut-microbiota interactions play a role in human obesity, insulin resistance and type 2 diabetes?
Diamant, M., Blaak, E. E., & de Vos, W. M. (2011) · Obesity Reviews · doi:10.1111/j.1467-789x.2010.00797.x · Cited by 308 · see citing works
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MicroRNAs in skeletal muscle: Their role and regulation in development, disease and function
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Physical inactivity as the culprit of metabolic inflexibility: evidence from bed-rest studies
Bergouignan, A., Rudwill, F., Simon, C., & Blanc, S. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00698.2011 · Cited by 272 · see citing works
Maternal capital and the metabolic ghetto: An evolutionary perspective on the transgenerational basis of health inequalities
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Mechanisms of muscle insulin resistance and the cross‐talk with liver and adipose tissue
Rosa, S. C. D. S., Nayak, N., Caymo, A. M., & Gordon, J. W. (2020) · Physiological Reports · doi:10.14814/phy2.14607 · Cited by 251 · see citing works
Effects of diet, lifestyle, Chrononutrition and alternative dietary interventions on postprandial Glycemia and insulin resistance
Papakonstantinou, E., Oikonomou, C., Nychas, G., & Dimitriadis, G. D. (2022) · Nutrients · doi:10.3390/nu14040823 · Cited by 199 · see citing works
Propionate suppresses hepatic gluconeogenesis via GPR43/AMPK signaling pathway
Yoshida, H., Ishii, M., & Akagawa, M. (2019) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2019.07.022 · Cited by 201 · see citing works
Physical Fitness in Morbidly Obese Patients: Effect of Gastric Bypass Surgery and Exercise Training
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Targeting fatty acid metabolism to improve glucose metabolism
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Lower extremity muscle strength is reduced in people with type 2 diabetes, with and without polyneuropathy, and is associated with impaired mobility and reduced quality of life
IJzerman, T. H., Schaper, N. C., Melai, T., Meijer, K., Willems, P. J. B., & Savelberg, H. H. C. M. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2011.10.026 · Cited by 177 · see citing works
Source and Amount of Carbohydrate in the Diet and Inflammation in Women with Polycystic Ovary Syndrome
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Corrected End-Tidal PCO2 Accurately Estimates PaCO2 at Rest and During Exercise in Morbidly Obese Adults
Bernhardt, V., Lorenzo, S., Babb, T. G., & Zavorsky, G. S. (2013) · CHEST Journal · doi:10.1378/chest.12-0896 · Cited by 169 · see citing works
Butyrate to combat obesity and obesity‐associated metabolic disorders: Current status and future implications for therapeutic use
van Deuren, T., Blaak, E. E., & Canfora, E. E. (2022) · Obesity Reviews · doi:10.1111/obr.13498 · Cited by 162 · see citing works
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Influence of Gender, Obesity, and Muscle Lipase Activity on Intramyocellular Lipids in Sedentary Individuals
Moro, C., Galgani, J. E., Luu, L. C. T., Pasarica, M., Mairal, A., Bajpeyi, S., Schmitz, G., Langin, D., Liebisch, G., & Smith, S. R. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0053 · Cited by 149 · see citing works
Deletion of Skeletal Muscle SOCS3 Prevents Insulin Resistance in Obesity
Jørgensen, S. B., O’Neill, H. M., Sylow, L., Honeyman, J. E., Hewitt, K. A., Palanivel, R., Fullerton, M. D., Öberg, L., Balendran, A., Galić, S., et al. (2012) · Diabetes · doi:10.2337/db12-0443 · Cited by 149 · see citing works
Mitochondrial response to nutrient availability and its role in metabolic disease
Gao, A. W., Cantó, C., & Houtkooper, R. H. (2014) · EMBO Molecular Medicine · doi:10.1002/emmm.201303782 · Cited by 148 · see citing works
High intensity interval training improves liver and adipose tissue insulin sensitivity
Marcinko, K., Sikkema, S. R., Samaan, M. C., Kemp, B. E., Fullerton, M. D., & Steinberg, G. R. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.09.006 · Cited by 141 · see citing works
Palmitate induces insulin resistance in human HepG2 hepatocytes by enhancing ubiquitination and proteasomal degradation of key insulin signaling molecules
Ishii, M., Maeda, A., Tani, S., & Akagawa, M. (2014) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2014.12.009 · Cited by 119 · see citing works
A Role of the Bile Salt Receptor FXR in Atherosclerosis
Hageman, J., Herrema, H., Groen, A. K., & Kuipers, F. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.109.197897 · Cited by 119 · see citing works
Metabolomics – the complementary field in systems biology: a review on obesity and type 2 diabetes
Bakar, M. H. A., Sarmidi, M. R., Cheng, K., Khan, A. A., Suan, C. L., Huri, H. Z., & Yaakob, H. (2015) · Molecular BioSystems · doi:10.1039/c5mb00158g · Cited by 117 · see citing works
The Role of Lipid Sensing Nuclear Receptors (PPARs and LXR) and Metabolic Lipases in Obesity, Diabetes and NAFLD
Dixon, E. D., Nardo, A. D., Claudel, T., & Trauner, M. (2021) · Genes · doi:10.3390/genes12050645 · Cited by 114 · see citing works
Changes in insulin sensitivity precede changes in body composition during 14 days of step reduction combined with overfeeding in healthy young men
Knudsen, S. H., Hansen, L. S., Pedersen, M., Dejgaard, T., Hansen, J., Hall, G. V., Thomsen, C., Solomon, T. P. J., Pedersen, B. K., & Krogh-Madsen, R. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00189.2011 · Cited by 112 · see citing works
Low-dose glucocorticoid treatment affects multiple aspects of intermediary metabolism in healthy humans: a randomised controlled trial
van Raalte, D. H., Brands, M., van der Zijl, N. J., Muskiet, M. H., Pouwels, P. J. W., Ackermans, M. T., Sauerwein, H. P., Serlie, M. J., & Diamant, M. (2011) · Diabetologia · doi:10.1007/s00125-011-2174-9 · Cited by 109 · see citing works
“As such, impaired fat oxidation in the fasted state was extensively shown in obese insulin-resistant and type 2 diabetic individuals [27].”
Background
Attenuation of Meal-Induced Inflammatory and Thrombotic Responses in Overweight Men and Women After 6-Week Daily Strawberry (Fragaria) Intake
Ellis, C. L., Edirisinghe, I., Kappagoda, T. C., & Burton‐Freeman, B. M. (2011) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.6114 · Cited by 109 · see citing works
Impaired mitochondrial fatty acid oxidation and insulin resistance in aging: novel protective role of glutathione
Nguyen, D. J. M., Samson, S. L., Reddy, V. T., GONZALEZ, E. V., & Sekhar, R. V. (2013) · Aging Cell · doi:10.1111/acel.12073 · Cited by 99 · see citing works
The role of low-grade inflammation and metabolic flexibility in aging and nutritional modulation thereof: a systems biology approach
Calçada, D., Vianello, D., Giampieri, E., Sala, C., Castellani, G., de Graaf, A., Kremer, B., van Ommen, B., Feskens, E., Santoro, A., et al. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2014.01.004 · Cited by 97 · see citing works
Electric Pulse Stimulation of Cultured Murine Muscle Cells Reproduces Gene Expression Changes of Trained Mouse Muscle
Burch, N., Arnold, A., Item, F., Summermatter, S., Santos, G., Christe, M., Boutellier, U., Toigo, M., & Handschin, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010970 · Cited by 94 · see citing works
Impairment of fat oxidation under high- vs. low-glycemic index diet occurs before the development of an obese phenotype
Isken, F., Klaus, S., Petzke, K. J., Loddenkemper, C., Pfeiffer, A. F. H., & Weickert, M. O. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00515.2009 · Cited by 95 · see citing works
Systems biology of personalized nutrition
van Ommen, B., van den Broek, T., de Hoogh, I. M., van Erk, M., van Someren, E. P., Rankouhi, T. R., Anthony, J. C., Hogenelst, K., Pasman, W. J., Boorsma, A., et al. (2017) · Nutrition Reviews · doi:10.1093/nutrit/nux029 · Cited by 95 · see citing works
Effect of Increasing Glutathione With Cysteine and Glycine Supplementation on Mitochondrial Fuel Oxidation, Insulin Sensitivity, and Body Composition in Older HIV-Infected Patients
Nguyen, D. J. M., Jean, W. H., Jahoor, F., & Rajagopal, V. S. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2376 · Cited by 93 · see citing works
Variations in the Prevalence of Obesity Among European Countries, and a Consideration of Possible Causes
Blundell, J. E., Baker, J. L., Boyland, E. J., Blaak, E. E., Charzewska, J., Henauw, S. D., Frühbeck, G., González‐Gross, M., Hebebrand, J., Holm, L., et al. (2017) · Obesity Facts · doi:10.1159/000455952 · Cited by 1,980 · see citing works
Self-citation
Mitochondrial dysfunction as a central event for mechanisms underlying insulin resistance: The roles of long chain fatty acids
Hafizi Abu Bakar, M., Kian Kai, C., Wan Hassan, W. N., Sarmidi, M. R., Yaakob, H., & Zaman Huri, H. (2015) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2601 · Cited by 91 · see citing works
From Obesity-Induced Low-Grade Inflammation to Lipotoxicity and Mitochondrial Dysfunction: Altered Multi-Crosstalk between Adipose Tissue and Metabolically Active Organs
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Authors: Corpeleijn, E., Saris, W. H. M., & Blaak, E. E.
Affiliations: Maastricht University (NL)
Corresponding author: Corpeleijn, E.
ORCID: Corpeleijn, E.
Saris, W. H. M.
Blaak, E. E.
Venue: Obesity Reviews
Publisher: Wiley
Published: 2009-02-23
Volume: 10
Issue: 2
Pages: 178-193
ISSN: 1467-7881 (ISSN-L)
1467-789X
DOI: 10.1111/j.1467-789x.2008.00544.x
OpenAlex: W2016142529
Cited by: 280
References: 112
Citations by year: 2026: 10 · 2025: 12 · 2024: 11 · 2023: 12 · 2022: 16 · 2021: 17 · 2020: 15 · 2019: 13 · 2018: 10 · 2017: 22 · 2016: 21 · 2015: 18 · 2014: 19 · 2013: 21 · 2012: 16
FWCI: 1.58
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Obesity Reviews (publishedVersion)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
Research Publications (Maastricht University) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Keywords: metabolic flexibility, insulin resistance, type 2 diabetes, lipotoxicity, skeletal muscle, fatty acid oxidation, fat oxidation, fatty acid uptake, fatty acid transporters, mitochondrial function, fuel switching, dietary fat intake, physical activity, weight loss, lifestyle intervention
MeSH terms: Animals, Diabetes Mellitus, Type 2, Diet, Energy Metabolism, Fatty Acids, Humans, Insulin Resistance, Life Style, Oxidation-Reduction, Weight Loss, Exercise, Muscle, Skeletal

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Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle

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