Superoxide and Respiratory Coupling in Mitochondria of Insulin-Deficient Diabetic Rats
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Mitochondrial reactive oxygen species have been implicated in both diabetic complications and the progression of the underlying diabetic state. However, it is not clear whether mitochondria of diabetic origin are intrinsically altered to generate excess reactive oxygen species independent of the surrounding diabetic milieu. Mitochondria were isolated from gastrocnemius, heart, and liver of 2-wk and 2-month streptozotocin diabetic rats and controls. We rigidly quantified mitochondrial superoxide, respiration and ATP production, respiratory coupling, the expression of several proteins with antioxidant properties, and the redox state of glutathione. Both fluorescent assessment and electron paramagnetic spectroscopy revealed that superoxide production was unchanged or reduced in the 2-month diabetic mitochondria compared with controls. Kinetic analysis of the proton leak showed that diabetic heart and muscle mitochondria were actually more coupled compared with control despite an approximate 2- to 4-fold increase in uncoupling protein-3 content. Adenine nucleotide translocator type 1 expression was reduced by approximately 50% in diabetic muscle mitochondria. Catalase was significantly up-regulated in muscle and heart tissue and in heart mitochondria, whereas glutathione peroxidase expression was increased in liver mitochondria of diabetic rats. We conclude that gastrocnemius, heart, and liver mitochondria of streptozotocin diabetic rats are not irrevocably altered toward excess superoxide production either by complex I or complex III. Moreover, gastrocnemius and heart mitochondria demonstrate increased, not decreased, respiratory coupling. Mitochondria of insulin-deficient diabetic rats do show signs of adaptation to antecedent oxidative stress manifested as tissue-specific enzyme and uncoupling protein expression but remain remarkably robust with respect to superoxide production. Mitochondria of streptozotocin-diabetic rats do not generate excess superoxide, manifest decreased or unchanged respiratory coupling, and show adaptation to antecedent in vivo oxidative stress.
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The reductions in maximally uncoupled respiration in heart and gastrocnemius muscle mitochondria from STZ-diabetic rats are more pronounced at 8 weeks than at 2 weeks of diabetes.
“These findings were more pronounced in 8-week than in 2-week diabetic rats.”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [134]
Proton conductance of muscle mitochondria from STZ-diabetic rats is reduced compared with nondiabetic controls.
“Based on the kinetic relation between hydrogen transfer and membrane potential, our data indicated that the proton conductance of muscle mitochondria of the diabetic rats was reduced compared with nondiabetic controls (curve shifted down and to the right; that is, opposite to what would be expected if diabetic muscle mitochondria were uncoupled).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [134]
In liver mitochondria of insulin-deficient STZ-diabetic rats, GSH content is reduced.
“GSH content also is reduced in liver mitochondria of insulin-deficient STZ-diabetic rats, as we and others observed (21, 134).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [134]
UCP3 is upregulated under conditions of increased free fatty acid delivery to mitochondria, including fasting, insulin-deficient diabetes, and high-fat feeding.
“UCP3 is known to be upregulated under conditions of increased free fatty acid delivery to mitochondria, including fasting (44), insulin-deficient diabetes (134), and high-fat feeding (135).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [134]
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- Authors
- Herlein, J. A., Fink, B. D., O'Malley, Y., & Sivitz, W. I.
- Affiliations
- University of Iowa (US)
- University of Iowa and the Iowa City Veterans Affairs Medical Center, Iowa City, Iowa 52242
- Corresponding author
- Sivitz, William I.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2008-09-04
- Volume
- 150
- Issue
- 1
- Pages
- 46-55
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC2630897
- OpenAlex
- W2132658079
- Cited by
- 77
- References
- 59
- Citations by year
- 2024: 2 · 2022: 2 · 2021: 4 · 2020: 4 · 2018: 5 · 2017: 4 · 2016: 1 · 2015: 6 · 2014: 8 · 2013: 8 · 2012: 10
- FWCI
- 3.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Endocrinology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-25295, P30DK025295)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- mitochondrial superoxide, respiratory coupling, insulin deficiency, diabetes mellitus, streptozotocin-induced diabetes, reactive oxygen species, UCP3, catalase, glutathione peroxidase, antioxidant proteins, glutathione redox state, proton leak, oxidative stress adaptation, heart mitochondria, liver mitochondria
- MeSH terms
- Animals, Diabetes Mellitus, Experimental, Glutathione, Heart, Insulin, Liver, Malates, Male, Membrane Potentials, Mitochondria, Heart, Mitochondria, Liver, Mitochondria, Muscle, Oxygen Consumption, Rotenone, Succinates, Superoxides, Rats, Sprague-Dawley, Muscle, Skeletal, Glutamic Acid, Rats
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