Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36

Bonen, Arend; Parolin, Michelle L.; Steinberg, Gregory R.; Calles‐Escandon, Jorge; Tandon, Narendra N.; Glatz, Jan F. C.; Luiken, Joost J. F. P.; Heigenhauser, George. J. F.; Dyck, David J.

doi:10.1096/fj.03-1065fje

Cited by 410Adipose Tissue and MetabolismMetabolism, Diabetes, and CancerLipid metabolism and biosynthesis

Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36

Bonen, Arend, Parolin, Michelle L., Steinberg, Gregory R., Calles‐Escandon, Jorge, Tandon, Narendra N., Glatz, Jan F. C., Luiken, Joost J. F. P., Heigenhauser, George. J. F. +1 more·2004·The FASEB Journal

DOI 10.1096/fj.03-1065fje

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Abstract

We examined whether, in human obesity and type 2 diabetes, long chain fatty acid (LCFA) transport into skeletal muscle is upregulated and contributes to an excess intramuscular triacylglycerol accumulation. In giant sarcolemmal vesicles prepared from human skeletal muscle, LCFA transport rates were upregulated ~4‐fold and were associated with an increased intramuscular triacylglycerol content in obese individuals and in type 2 diabetics. In these individuals, the increased sarcolemmal LCFA transport rate was not associated with an altered expression of FAT/CD36 or FABPpm. Instead, the increase in the LCFA transport rate was associated with an increase in sarcolemmal FAT/CD36 but not sarcolemmal FABPpm. Rates of fatty acid esterification were increased threefold in isolated human muscle strips obtained from obese subjects, while concomitantly rates of fatty acid oxidation were not altered. Thus, the increased rate of fatty acid transport may contribute to the increased rates of triacylglycerol accumulation in human skeletal muscle. The altered FAT/CD36 trafficking in muscle from obese subjects and type 2 diabetics juxtaposes the known alterations in GLUT4 trafficking, i.e., GLUT4 is known to be retained in its intracellular depots while FAT/CD36 is retained at the sarcolemma. This redistribution of FAT/CD36 to the sarcolemma may contribute to the etiology of insulin resistance in human muscle, and hence, FAT/CD36 provides another potential therapeutic target for the prevention and/or treatment of insulin resistance.

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Increased fatty acid uptake contributes to increased lipid accumulation in skeletal muscle, leading to lipotoxicity, which impairs muscle insulin sensitivity.
“Increased fatty acid (FA) uptake contributes to increased lipid accumulation in skeletal muscle, leading to lipotoxicity, which is known to impair muscle insulin sensitivity (2, 20).”
From Mitochondrial Fission Contributes to Mitochondrial Dysfunction and Insulin Resistance in Skeletal Muscle (2012) · cites this paper as [2]
CD36 has an important role in long-chain fatty acid uptake into skeletal muscle in rodents and humans, and its concentration and activity increase after exercise.
“There is abundant evidence which indicates that CD36 plays an important role in LCFA uptake into skeletal muscle in rodents and human and its concentration and activity are increased following exercise [89–96].”
From Pathogenesis of insulin resistance in skeletal muscle (2010) · cites this paper as [96]
Clinical studies have demonstrated that obese, insulin-resistant, and type 2 diabetic individuals do not exhibit a reduced capacity to oxidize fatty acids and have normal or even increased mitochondrial function compared with lean controls.
“Thus, clinical studies have demonstrated that obese, insulin-resistant, and type 2 diabetic individuals do not exhibit a reduced capacity to oxidize fatty acids (73,74) and have normal, or even increased, mitochondrial function, as compared with lean controls (56,75).”
From Insulin sensitivity: Modulation by nutrients and inflammation (2008) · cites this paper as [73]
Increased skeletal muscle plasmalemma CD36 content is associated with increased muscle FFA uptake and intramyocellular triglyceride accumulation in human subjects.
“The importance of CD36 in FFA transport and ectopic triglyceride accumulation has been demonstrated by observations in human subjects indicating that increased skeletal muscle plasmalemma CD36 content is associated with increased muscle FFA uptake and intramyocellular triglyceride accumulation (25).”
From Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity (2009) · cites this paper as [25]
Increased plasmalemma skeletal muscle CD36 is associated with increased FFA uptake and insulin resistance in animal models and obese and diabetic human subjects.
“The potential importance of CD36 in regulating insulin sensitivity is supported by studies conducted in animal models and in obese and diabetic human subjects that found increased plasmalemma skeletal muscle CD36 was associated with increased FFA uptake and insulin resistance (25,30,31)”
From Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity (2009) · cites this paper as [25]

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Skeletal muscle mitochondrial FAT/CD36 content and palmitate oxidation are not decreased in obese women.
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Increased levels of peroxisome proliferator-activated receptor gamma, coactivator 1 alpha (PGC-1α) improve lipid utilisation, insulin signalling and glucose transport in skeletal muscle of lean and insulin-resistant obese Zucker rats
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Intramuscular Fat and Associations With Metabolic Risk Factors in the Framingham Heart Study
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Adipokines as regulators of muscle metabolism and insulin sensitivityThis paper is one of a selection of papers published in this Special Issue, entitled 14th International Biochemistry of Exercise Conference – Muscles as Molecular and Metabolic Machines, and has undergone the Journal’s usual peer review process.
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A null mutation in skeletal muscle FAT/CD36 reveals its essential role in insulin- and AICAR-stimulated fatty acid metabolism
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The Effect of Exercise and Nutrition on Intramuscular Fat Metabolism and Insulin Sensitivity
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Sphingolipid Metabolism: New Insight into Ceramide-Induced Lipotoxicity in Muscle Cells
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Non-alcoholic fatty liver disease and insulin resistance: From bench to bedside
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In obese rat muscle transport of palmitate is increased and is channeled to triacylglycerol storage despite an increase in mitochondrial palmitate oxidation
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Obesity and Cancer Progression: Is There a Role of Fatty Acid Metabolism?
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Impaired skeletal muscle substrate oxidation in glucose-intolerant men improves after weight loss
Corpeleijn, E., Mensink, M., Kooi, M. E., Roekaerts, P. M. H. J., Saris, W. H. M., & Blaak, E. E. (2008) · Obesity · doi:10.1038/oby.2008.24 · Cited by 104 · see citing works
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“Skeletal muscle from obese humans shows increased intramuscular triglyceride content and decreased lipid oxidation [3,4].”
Background
Understanding Age-Related Changes in Skeletal Muscle Metabolism: Differences Between Females and Males
Gheller, B. J. F., Riddle, E. S., Lem, M. R., & Thalacker-Mercer, A. E. (2016) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071715-050901 · Cited by 98 · see citing works
Korean red ginseng (Panax ginseng) improves insulin sensitivity and attenuates the development of diabetes in Otsuka Long-Evans Tokushima fatty rats
Lee, H. J., Lee, Y., Park, S. K., Kang, E. S., Kim, H.-J., Lee, Y. C., Choi, C. S., Park, S. E., Ahn, C. W., Soo, B., et al. (2009) · Metabolism · doi:10.1016/j.metabol.2009.03.015 · Cited by 100 · see citing works
CD36 inhibition prevents lipid accumulation and contractile dysfunction in rat cardiomyocytes
Angın, Y., Steinbusch, L. K. M., Simons, P. J., Greulich, S., Hoebers, N., Douma, K., van Zandvoort, M. A. M. J., Coumans, W. A., Wijnen, W. J., Diamant, M., et al. (2012) · Biochemical Journal · doi:10.1042/bj20120060 · Cited by 99 · see citing works
Self-citation
Cardiac substrate uptake and metabolism in obesity and type-2 diabetes: Role of sarcolemmal substrate transporters
Coort, S. L., Bonen, A., Vusse, G. J., Glatz, J. F. C., & Luiken, J. J. F. P. (2006) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-005-9030-5 · Cited by 99 · see citing works
Self-citation
Fatty Acid Translocase (FAT/CD36) Is Localized on Insulin-Containing Granules in Human Pancreatic β-Cells and Mediates Fatty Acid Effects on Insulin Secretion
Noushmehr, H., D’Amico, E., Farilla, L., Hui, H., Wawrowsky, K., Mlynarski, W. M., Doria, A., Abumrad, N. A., & Perfetti, R. (2005) · Diabetes · doi:10.2337/diabetes.54.2.472 · Cited by 99 · see citing works
In Vivo, Fatty Acid Translocase (CD36) Critically Regulates Skeletal Muscle Fuel Selection, Exercise Performance, and Training-induced Adaptation of Fatty Acid Oxidation
McFarlan, J. T., Yoshida, Y., Jain, S. S., Han, X.-X., Snook, L. A., Lally, J., Smith, B. K., Glatz, J. F. C., Luiken, J. J. F. P., Sayer, R. A., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.315358 · Cited by 98 · see citing works
Self-citation
p38 MAPK in Glucose Metabolism of Skeletal Muscle: Beneficial or Harmful?
Bengal, E., Aviram, S., & Hayek, T. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186480 · Cited by 98 · see citing works
AMP-Activated Protein Kinase Is Not Down-Regulated in Human Skeletal Muscle of Obese Females
Steinberg, G. R., Smith, A. C., van Denderen, B. J. W., Chen, Z., Murthy, S., Campbell, D. J., Heigenhauser, G. J. F., Dyck, D. J., & Kemp, B. E. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0308 · Cited by 97 · see citing works
Self-citation
Short-chain fatty acids can improve lipid and glucose metabolism independently of the pig gut microbiota
Zhou, H. W., Yu, B., Sun, J., Liu, Z., Chen, H., Ge, L., & Chen, D. (2021) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-021-00581-3 · Cited by 96 · see citing works
Mitochondrial regulators of fatty acid metabolism reflect metabolic dysfunction in type 2 diabetes mellitus
Kulkarni, S. S., Salehzadeh, F., Fritz, T., Zierath, J. R., Krook, A., & Osler, M. E. (2011) · Metabolism · doi:10.1016/j.metabol.2011.06.014 · Cited by 94 · see citing works
Subcellular trafficking of the substrate transporters GLUT4 and CD36 in cardiomyocytes
Steinbusch, L. K. M., Schwenk, R. W., Ouwens, D. M., Diamant, M., Glatz, J. F. C., & Luiken, J. J. F. P. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0690-x · Cited by 95 · see citing works
Self-citation
Re-balancing cellular energy substrate metabolism to mend the failing heart
Glatz, J. F. C., Nabben, M., Young, M. E., Schulze, P. C., Taegtmeyer, H., & Luiken, J. J. F. P. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.165579 · Cited by 93 · see citing works
Self-citation
High fat diet induced diabetic cardiomyopathy
Dirkx, E., Schwenk, R. W., Glatz, J. F. C., Luiken, J. J. F. P., & van Eys, G. J. J. M. (2011) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2011.04.018 · Cited by 92 · see citing works
Self-citation

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
Self-citation
The Exocyst Is Required For CD36 Fatty Acid Translocase Trafficking And Free Fatty Acid Uptake In Skeletal And Cardiac Muscle Cells
Nakamura, N. (2023) · ScholarSpace (University of Hawaii at Manoa)
Exercise and insulin increase muscle fatty acid uptake by recruiting putative fatty acid transporters to the sarcolemma
Glatz, J. F. C., Bonen, A., & Luiken, J. J. F. P. (2002) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200207000-00003 · Cited by 56 · see citing works
Self-citation
Cardiac and skeletal muscle fatty acid transport and transporters and triacylglycerol and fatty acid oxidation in lean and Zucker diabetic fatty rats
Bonen, A., Holloway, G. P., Tandon, N. N., Han, X.-X., McFarlan, J. T., Glatz, J. F. C., & Luiken, J. J. F. P. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90820.2008 · Cited by 60 · see citing works
Self-citation
Plasmalemmal fatty acid transport is regulated in heart and skeletal muscle by contraction, insulin and leptin, and in obesity and diabetes
Bonen, A., Benton, C. R., Campbell, S. E., Chabowski, A., Clarke, D. C., Han, X. ‐., Glatz, J. F. C., & Luiken, J. J. F. P. (2003) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2003.01157.x · Cited by 64 · see citing works
Self-citation

Authors: Bonen, A., Parolin, M. L., Steinberg, G. R., Calles‐Escandon, J., Tandon, N. N., Glatz, J. F. C., Luiken, J. J. F. P., Heigenhauser, G. J. F., & Dyck, D. J.
Affiliations: University of Guelph (CA)
University of Waterloo (CA)
Section of Endocrinology and Metabolism Wake Forest University School of Medicine & Baptist Medical Center Winston‐Salem North Carolina 27157
Otsuka (United States) (US)
Maastricht University (NL)
McMaster University (CA)
ORCID: Steinberg, Gregory R.
Glatz, Jan F. C.
Luiken, Joost J. F. P.
Dyck, David J.
Venue: The FASEB Journal
Publisher: Wiley
Published: 2004-05-07
Volume: 18
Issue: 10
Pages: 1144-1146
ISSN: 0892-6638 (ISSN-L)
1530-6860
DOI: 10.1096/fj.03-1065fje
OpenAlex: W2122852774
Cited by: 410
References: 63
Citations by year: 2026: 7 · 2025: 13 · 2024: 9 · 2023: 9 · 2022: 10 · 2021: 15 · 2020: 13 · 2019: 19 · 2018: 5 · 2017: 9 · 2016: 21 · 2015: 10 · 2014: 22 · 2013: 21 · 2012: 33
FWCI: 14.20
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
doi.wiley.com/10.1002/tdm_license_1.1 (tdm)
Locations: The FASEB Journal (publishedVersion)
PubMed (publishedVersion)
Funders: Canadian Institutes of Health Research
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 › Biochemistry › Lipid metabolism and biosynthesis
Keywords: triglyceride accumulation, skeletal muscle, obesity, type 2 diabetes, fatty acid uptake, FAT/CD36, FABPpm, fatty acid esterification, fatty acid oxidation, insulin resistance, GLUT4 trafficking, long-chain fatty acids
MeSH terms: Aged, Biological Transport, Carrier Proteins, Diabetes Mellitus, Type 2, Fatty Acids, Female, Humans, Insulin Resistance, Male, Middle Aged, Obesity, Sarcolemma, Triglycerides, Body Mass Index, Muscle, Skeletal, CD36 Antigens, Palmitic Acid, Fatty Acid-Binding Proteins

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Triacylglycerol accumulation in human obesity and type 2 diabetes is associated with increased rates of skeletal muscle fatty acid transport and increased sarcolemmal FAT/CD36

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