Deficiency of subsarcolemmal mitochondria in obesity and type 2 diabetes
Open accessAbstract
The current study addresses a novel hypothesis of subcellular distribution of mitochondrial dysfunction in skeletal muscle in type 2 diabetes. Vastus lateralis muscle was obtained by percutaneous biopsy from 11 volunteers with type 2 diabetes; 12 age-, sex-, and weight-matched obese sedentary nondiabetic volunteers; and 8 lean volunteers. Subsarcolemmal and intermyofibrillar mitochondrial fractions were isolated by differential centrifugation and digestion techniques. Overall electron transport chain activity was similar in type 2 diabetic and obese subjects, but subsarcolemmal mitochondria electron transport chain activity was reduced in type 2 diabetic subjects (0.017 ± 0.003 vs. 0.034 ± 0.007 units/mU creatine kinase [CK], P = 0.01) and sevenfold reduced compared with lean subjects (P < 0.01). Electron transport chain activity in intermyofibrillar mitochondria was similar in type 2 diabetic and obese subjects, though reduced compared with lean subjects. A reduction in subsarcolemmal mitochondria was confirmed by transmission electron microscopy. Although mtDNA was lower in type 2 diabetic and obese subjects, the decrement in electron transport chain activity was proportionately greater, indicating functional impairment. Because of the potential importance of subsarcolemmal mitochondria for signal transduction and substrate transport, this deficit may contribute to the pathogenesis of muscle insulin resistance in type 2 diabetes.
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Mitochondrial mass is 14-38% lower in muscle in obesity and type 2 diabetes.
“Mitochondrial mass is consistently 14–38% lower in muscle in obesity and type 2 diabetes (2–5).”
Skeletal muscle from obese humans with or without diabetes has reduced overall mitochondrial content and morphological changes similar to animal models.
“Skeletal muscle from obese humans with or without diabetes is characterized by reduced overall mitochondrial content with evidence of morphological changes similar to those in the animal models (Chomentowski et al., 2011; Kelley et al., 2002; Ritov et al., 2005).”
From Lipid-Induced Mitochondrial Stress and Insulin Action in Muscle (2012) · cites this paper as Ritov et al., 2005
Muscle insulin resistance often coexists with mitochondrial abnormalities, including altered morphology, lower NADH:O2 oxidoreductase activity, reduced in vivo ATP synthesis and TCA cycle flux, and low expression of mitochondrial biogenesis and oxidative metabolism genes.
“muscle insulin resistance often (but not always [86]) coexists with abnormalities in mitochondrial morphology, reduced NADH:O2 oxidoreductase activity, diminished in vivo rates of ATP synthesis and TCA cycle flux, as well as low expression levels of genes involved in mitochondrial biogenesis and oxidative metabolism [47,49,59,68,78].”
From Intramuscular triacylglycerol and insulin resistance: guilty as charged or wrongly accused? (2010) · cites this paper as [78]
In some studies, surrogate markers of mitochondrial content are reduced, whereas in others they are not.
“In some studies, surrogate markers of mitochondrial content are reduced (7, 9, 14), whereas in others they are not (15, 16).”
A number of studies have consistently demonstrated lower oxidative capacity in insulin-resistant subjects.
“A number of studies have consistently demonstrated lower oxidative capacity in insulin-resistant subjects (5, 7, 8, 14, 23).”
Insulin resistance was associated with less mtDNA in some studies but not in others.
“Insulin resistance was associated with less mtDNA in some studies (9, 14) but not in others (15).”
Electron microscopic studies show an approximately 40% reduction in mitochondrial density in skeletal muscle in lean normal-glucose-tolerant offspring of type 2 diabetic parents, obese non-diabetic individuals, and type 2 diabetic subjects compared with lean insulin-sensitive age-matched controls.
“Electron microscopic studies have revealed a significant reduction (~40%) in mitochondrial density in skeletal muscle in lean NGT offspring of type 2 diabetic parents, in obese nondiabetic individuals and in T2DM subjects compared to lean insulin-sensitive, age-matched controls [111, 112].”
From Pathogenesis of insulin resistance in skeletal muscle (2010) · cites this paper as [112]
Because electron transport chain activity and mitochondrial ATP synthesis rate were related to mitochondrial protein and/or citrate synthase activity, these observations indicate a basic functional defect in mitochondrial activity in skeletal muscle of obese insulin-resistant individuals.
“Since, in these studies [112, 120], ETC activity and mitochondrial ATP synthesis rate were related to the amount of mitochondrial protein and/or citrate synthase activity, these observations indicate the existence of a basic functional defect in mitochondrial activity in skeletal muscle of obese insulin-resistant individuals [115].”
From Pathogenesis of insulin resistance in skeletal muscle (2010) · cites this paper as [112]
Ex vivo measurement of electron transport chain activity and mitochondrial ATP synthesis in isolated mitochondria shows decreased electron transport chain activity and ATP synthesis in obese insulin-resistant individuals compared with lean insulin-sensitive subjects.
“Ex vivo measurement of electron transport chain activity (ETC) [112] and mitochondrial ATP synthesis in isolated mitochondria [120, 121] have demonstrated a decrease in ETC activity and ATP synthesis in obese insulin-resistant individuals compared to lean insulin-sensitive subjects.”
From Pathogenesis of insulin resistance in skeletal muscle (2010) · cites this paper as [112]
It has generally been assumed that a reduction in muscle mitochondrial function will result in reductions in whole-body fat oxidative capacity.
“it has generally been assumed that a reduction in muscle mitochondrial function will result in reductions in whole-body fat oxidative capacity (3–5,42,43).”
From Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance (2010) · cites this paper as [43]
In vivo and ex vivo ATP production capacity has been reported lower in skeletal muscle of type 2 diabetes patients than in age- and BMI-matched controls in some studies but not all.
“Similarly, in vivo and ex vivo measurements of ATP production capacity have been reported to be reduced in skeletal muscle of T2DM patients compared with ageand body mass index (BMI)-matched controls in some (6, 7) but not in all studies (4, 8).”
From Physical activity is the key determinant of skeletal muscle mitochondrial function in type 2 diabetes (2012) · cites this paper as [7]
Aging and obesity/diabetes share physiological aspects including accumulation of ectopic lipids and lipotoxicity in liver, skeletal muscle and heart, as well as decreased mitochondrial number and activity.
“A number of physiological aspects of aging are also found in obesity and diabetes (Fig. 2) including accumulation of ectopic lipids and lipotoxicity in metabolic organs such as liver, skeletal muscle and heart, as well as decreased mitochondrial number and activity [144–147].”
From Targeting Intramyocellular Lipids to Improve Aging Muscle Function (2025) · cites this paper as [147]
Type 2 diabetes and obese subjects have reduced numbers of SLM in skeletal muscle associated with reduced electron-transport activity per unit mitochondrial DNA.
“Studies with transmission electron microscopy revealed reduced numbers of SLM in skeletal muscle of type 2 diabetes and obese subjects associated with reduced electron-transport activity per unit mitochondrial DNA, suggesting functional impairment as well (268).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [268]
Mitochondrial dysfunction and/or a reduction in mitochondrial content, as characterised by a fall in oxidative capacity, has been reported in skeletal muscle and adipose tissue from obese and diabetic subjects.
“Indeed, mitochondrial dysfunction and/or a reduction in mitochondrial content, as characterised by a fall in oxidative capacity, has been reported in skeletal muscle and adipose tissue from obese and diabetic subjects [8, 9].”
From Proinflammatory NFkB signalling promotes mitochondrial dysfunction in skeletal muscle in response to cellular fuel overloading (2019) · cites this paper as [9]
Electron microscopy demonstrates diminished mitochondrial size in obesity and diabetes, particularly in subsarcolemmal fractions.
“This possibility is consistent with electron microscopy demonstrating diminished mitochondrial size in obesity and diabetes (116), particularly in subsarcolemmal fractions (114).”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [114]
The enzymatic activity of OXPHOS complex I is reduced by about 40% in skeletal muscle biopsy samples from individuals with type 2 DM and by 20% in obese individuals.
“Ritov et al. (114) demonstrated that the enzymatic activity of OXPHOS complex I, as assessed by the activity of rotenone-sensitive NADH:O 2 oxidoreductase, was reduced by about 40% in skeletal muscle biopsy samples from individuals with type 2 DM and by 20% in obese individuals.”
From The role of mitochondria in the pathogenesis of type 2 diabetes (2010) · cites this paper as [114]
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- Authors
- Ritov, V. B., Menshikova, E. V., He, J., Ferrell, R. E., Goodpaster, B. H., & Kelley, D. E.
- Affiliations
- University of Pittsburgh (US)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2005-01-01
- Volume
- 54
- Issue
- 1
- Pages
- 8-14
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2165096496
- Cited by
- 887
- References
- 48
- Citations by year
- 2026: 20 · 2025: 20 · 2024: 24 · 2023: 36 · 2022: 44 · 2021: 32 · 2020: 46 · 2019: 33 · 2018: 43 · 2017: 44 · 2016: 47 · 2015: 28 · 2014: 43 · 2013: 48 · 2012: 63
- FWCI
- 19.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Pittsburgh (M01RR00056)
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (P30-DK-462, DK-49200, R01DK049200)
- National Center for Research Resources (M01RR000056, 5 M01 RR00056)
- Topics
- 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
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- subsarcolemmal mitochondria, interfibrillar mitochondria, mitochondrial dysfunction, skeletal muscle, type 2 diabetes, obesity, mitochondrial DNA, muscle insulin resistance, vastus lateralis
- MeSH terms
- Adult, Base Sequence, Blood Glucose, Diabetes Mellitus, Type 2, DNA, Mitochondrial, Female, Glycated Hemoglobin, Humans, Insulin Resistance, Male, Middle Aged, Mitochondria, Obesity, Reference Values, Sarcolemma, Glucose Clamp Technique, Body Mass Index, DNA Primers, Muscle, Skeletal, Diabetes Complications
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