Oxidative stress and diabetic complications

Giacco, Ferdinando; Brownlee, Michael

doi:10.1161/circresaha.110.223545

Cited by 5,461Nitric Oxide and Endothelin EffectsAdvanced Glycation End Products researchRedox biology and oxidative stress

Oxidative stress and diabetic complications

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Giacco, Ferdinando, Brownlee, Michael·2010·Circulation Research

DOI 10.1161/circresaha.110.223545PMC PMC2996922

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Abstract

Oxidative stress plays a pivotal role in the development of diabetes complications, both microvascular and cardiovascular. The metabolic abnormalities of diabetes cause mitochondrial superoxide overproduction in endothelial cells of both large and small vessels, as well as in the myocardium. This increased superoxide production causes the activation of 5 major pathways involved in the pathogenesis of complications: polyol pathway flux, increased formation of AGEs (advanced glycation end products), increased expression of the receptor for AGEs and its activating ligands, activation of protein kinase C isoforms, and overactivity of the hexosamine pathway. It also directly inactivates 2 critical antiatherosclerotic enzymes, endothelial nitric oxide synthase and prostacyclin synthase. Through these pathways, increased intracellular reactive oxygen species (ROS) cause defective angiogenesis in response to ischemia, activate a number of proinflammatory pathways, and cause long-lasting epigenetic changes that drive persistent expression of proinflammatory genes after glycemia is normalized (“hyperglycemic memory”). Atherosclerosis and cardiomyopathy in type 2 diabetes are caused in part by pathway-selective insulin resistance, which increases mitochondrial ROS production from free fatty acids and by inactivation of antiatherosclerosis enzymes by ROS. Overexpression of superoxide dismutase in transgenic diabetic mice prevents diabetic retinopathy, nephropathy, and cardiomyopathy. The aim of this review is to highlight advances in understanding the role of metabolite-generated ROS in the development of diabetic complications.

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Chronic overproduction of ROS increases oxidative stress, damages DNA, increases apoptosis, and triggers inflammation, which is a key feature in T2DM and metabolic syndrome.
“Chronic overproduction of ROS increases oxidative stress, damages DNA, increases apoptosis, and triggers inflammation, which is a key feature in T2DM and metabolic syndrome (42).”
From TFAM Enhances Fat Oxidation and Attenuates High-Fat Diet–Induced Insulin Resistance in Skeletal Muscle (2019) · cites this paper as [42]
The section on hyperglycemia-induced mitochondrial superoxide production says increased mitochondrial ROS induce DNA strand breaks, and the Abstract says increased ROS activate pro-inflammatory pathways in diabetes. The paper also links superoxide overproduction to oxidative stress, but the passages found do not establish the claimed increase in apoptosis or characterize this combination of effects as a key feature of metabolic syndrome. (LLM, conf=0.86)
Experimental — accuracy not yet measured
The data suggest significant molecular and metabolic perturbations between NHOs and PGDHOs, consistent with previous studies on PGD suggesting increased oxidative stress, cardiomyopathy, and altered lipid profiles.
“Taken together, our data suggest significant molecular and metabolic perturbations between NHOs and PGDHOs consistent with previous studies on PGD suggesting increased oxidative stress, cardiomyopathy, and altered lipid profiles48–50”
From Self-assembling human heart organoids for the modeling of cardiac development and congenital heart disease (2021) · cites this paper as [49]
Hyperglycemia and protein kinase C activation-induced reactive oxygen species production result in inflammatory changes in the vascular endothelium, including monocyte adhesion, foam cell formation, and activation of the polyol pathway and increased formation of advanced glycation end products.
“Hyperglycemia and PKC activation-induced ROS production result in inflammatory changes in the vascular endothelium including monocytes adhesion, formation of foam cells, and activation of major biochemical paths including polyol pathway flux and increased formation of advanced glycation end products, further contributing to the development of atherosclerosis.40”
From Glycemic variability and cardiovascular disease in patients with type 2 diabetes (2021) · cites this paper as [40]

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Advanced glycation end products (AGEs) co-localize with AGE receptors in the retinal vasculature of diabetic and of AGE-infused rats.
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Demonstration that polyol accumulation is responsible for diabetic cataract by the use of transgenic mice expressing the aldose reductase gene in the lens.
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Catalase Protects Cardiomyocyte Function in Models of Type 1 and Type 2 Diabetes
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Lymphocytes From Patients With Type 1 Diabetes Display a Distinct Profile of Chromatin Histone H3 Lysine 9 Dimethylation
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Decreasing Intracellular Superoxide Corrects Defective Ischemia-induced New Vessel Formation in Diabetic Mice
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Advanced Glycation Endproducts Promote Adhesion Molecule (VCAM-1, ICAM-1) Expression and Atheroma Formation in Normal Rabbits
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High Glucose Increases Angiopoietin-2 Transcription in Microvascular Endothelial Cells through Methylglyoxal Modification of mSin3A
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Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress
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Inactivation of phosphorylated endothelial nitric oxide synthase (Ser-1177) by O -GlcNAc in diabetes-associated erectile dysfunction
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Increase in Diacylglycerol Mass in Isolated Glomeruli by Glucose From De Novo Synthesis of Glycerolipids
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Hyperglycemia Potentiates Collagen-Induced Platelet Activation Through Mitochondrial Superoxide Overproduction
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Postchallenge Hyperglycemia and Mortality in a National Sample of U.S. Adults
Saydah, S. H., Miret, M., Sung, J., Varas, C., Gause, D., & Brancati, F. L. (2001) · Diabetes Care · doi:10.2337/diacare.24.8.1397 · Cited by 221 · see citing works
High Glucose Inhibits Glucose-6-phosphate Dehydrogenase via cAMP in Aortic Endothelial Cells
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Sp1 Sites Mediate Activation of the Plasminogen Activator Inhibitor-1 Promoter by Glucose in Vascular Smooth Muscle Cells
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Activation of Protein Kinase C in Glomerular Cells in Diabetes: Mechanisms and Potential Links to the Pathogenesis of Diabetic Glomerulopathy
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AGEs induce oxidative stress and activate protein kinase C-βIIin neonatal mesangial cells
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Insulin Resistance and Atherosclerosis
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Hyperglycemia Impairs Proteasome Function by Methylglyoxal
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Activation of Nuclear Factor-κB in Cultured Endothelial Cells by Increased Glucose Concentration: Prevention by Calphostin C
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Immunohistochemical detection of imidazolone, a novel advanced glycation end product, in kidneys and aortas of diabetic patients.
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Advanced glycation endproducts inhibit prostacyclin production and induce plasminogen activator inhibitor-1 in human microvascular endothelial cells
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The Potential Role of Thiamine (Vitamin B1) in Diabetic Complications
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Overexpression of Metallothionein Reduces Diabetic Cardiomyopathy
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Glucose Metabolism to Glucosamine Is Necessary for Glucose Stimulation of Transforming Growth Factor-α Gene Transcription
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Aldose Reductase and Cardiovascular Diseases, Creating Human-Like Diabetic Complications in an Experimental Model
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Palmitate-Induced Apoptosis in Cultured Bovine Retinal Pericytes
Cacicedo, J. M., Benjachareowong, S., Chou, E. L., Ruderman, N. B., & Ido, Y. (2005) · Diabetes · doi:10.2337/diabetes.54.6.1838 · Cited by 158 · see citing works
Regulation of Intracellular Glucose and Polyol Pathway by Thiamine and Benfotiamine in Vascular Cells Cultured in High Glucose
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A Critical Role for Eukaryotic Elongation Factor 1A-1 in Lipotoxic Cell Death
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Poly(ADP-Ribose) Polymerase Inhibition Alleviates Experimental Diabetic Sensory Neuropathy
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Advanced glycation end products in vitreous: Structural and functional implications for diabetic vitreopathy.
Stitt, A. W., Moore, J. E., Sharkey, J. A., Murphy, G., Simpson, D. A. C., Bucala, R., Vlassara, H., & ARCHER, D. B. (1998) · PubMed · Cited by 137 · see citing works
Nitric Oxide Inhibition of Transforming Growth Factor-β and Collagen Synthesis in Mesangial Cells
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Poly(ADP-Ribose) Polymerase Inhibitors Ameliorate Nephropathy of Type 2 Diabetic Leprdb/dbMice
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Mechanisms of Glucose-Enhanced Extracellular Matrix Accumulation in Rat Glomerular Mesangial Cells
Pugliese, G., Pricci, F., Pugliese, F. R., Mené, P., Lenti, L., Andreani, D., Galli, G., Casini, A., Bianchi, S., Rotella, C. M., et al. (1994) · Diabetes · doi:10.2337/diab.43.3.478 · Cited by 130 · see citing works
Reactive oxygen species mediate high glucose–induced plasminogen activator inhibitor-1 up-regulation in mesangial cells and in diabetic kidney
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Benfotiamine Counteracts Glucose Toxicity Effects on Endothelial Progenitor Cell Differentiation via Akt/FoxO Signaling
Marchetti, V., Menghini, R., Rizza, S., Vivanti, A., Feccia, T., Lauro, D., Fukamizu, A., Lauro, R., & Federici, M. (2006) · Diabetes · doi:10.2337/db06-0369 · Cited by 128 · see citing works
Ceramide-induced activation of NADPH oxidase and endothelial dysfunction in small coronary arteries
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Advanced Glycation End Products Induce Expression of Vascular Endothelial Growth Factor by Retinal Müller Cells
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SOD2 protects neurons from injury in cell culture and animal models of diabetic neuropathy
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Nerve conduction and aldose reductase inhibition during 5 years of diabetes or galactosaemia in dogs
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Translocation of protein kinase C ? and ? in rat glomerular mesangial cells cultured under high glucose conditions
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Inositols prevent and reverse endothelial dysfunction in diabetic rat and rabbit vasculature metabolically and by scavenging superoxide
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Glucose-induced changes in protein kinase C and nitric oxide are prevented by vitamin E
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Catalytic effectiveness of human aldose reductase. Critical role of C-terminal domain.
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Acceleration of diabetic renal injury in the superoxide dismutase knockout mouse: effects of tempol
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Oral benfotiamine plus α-lipoic acid normalises complication-causing pathways in type 1 diabetes
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The Non-coding RNA gadd7 Is a Regulator of Lipid-induced Oxidative and Endoplasmic Reticulum Stress
Brookheart, R. T., Michel, C. I., Listenberger, L. L., Ory, D. S., & Schaffer, J. E. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m806209200 · Cited by 83 · see citing works
Dominant-negative p38α mitogen-activated protein kinase prevents cardiac apoptosis and remodeling after streptozotocin-induced diabetes mellitus
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Hyperglycemia and the O-GlcNAc Transferase in Rat Aortic Smooth Muscle Cells: Elevated Expression and Altered Patterns of O-GlcNAcylation
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α-Lipoic acid prevents lipotoxic cardiomyopathy in acyl CoA-synthase transgenic mice
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Affinity purification and glucose specificity of aldose reductase from bovine lens
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Therapeutic Approach for Diabetic Nephropathy Using Gene Delivery of Translocase of Inner Mitochondrial Membrane 44 by Reducing Mitochondrial Superoxide Production
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Replication timing and epigenetic reprogramming of gene expression: a two-way relationship?
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Immunohistochemical detection of advanced glycosylation end products within the vascular lesions and glomeruli in diabetic nephropathy
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Diabetes and Arterial Extracellular Matrix Changes in a Porcine Model of Atherosclerosis
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RAGE: A journey from the complications of diabetes to disorders of the nervous system – striking a fine balance between injury and repair
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Endothelial cell adhesion molecule and PMNL response to inflammatory stimuli and AGE-modified fibronectin
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Captopril Inhibits Glucose Accumulation in Retinal Cells in Diabetes
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Development of atherosclerosis in the diabetic BALB/c mice
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Hexosamine Pathway Is Responsible for Inhibition by Diabetes of Phenylephrine-Induced Inotropy
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Role of Protein Kinase C in Glucose- and Angiotensin II-Induced Plasminogen Activator Inhibitor Expression1
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Ribozyme Targeting of Receptor for Advanced Glycation End Products in Mouse Mesangial Cells
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Diabetic Nephropathy Is Associated With Gene Expression Levels of Oxidative Phosphorylation and Related Pathways
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Nonhuman primate models of atherosclerosis: Potential for the study of diabetes mellitus and hyperinsulinemia
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Redox state-dependent and sorbitol accumulation-independent diabetic albuminuria in mice with transgene-derived human aldose reductase and sorbitol dehydrogenase deficiency
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[113]National Diabetes Data Group Diabetes in America 1995 782 NIH Bethesda, Maryland, USA 2nd edition National Institute of Diabetes and Digestive and Kidney Diseases
[114]DECODE Study Group the European Diabetes Epidemiology Group vascular mortality: comparison of fasting and 2-hour diagnostic criteria Arch. Intern. Med 2001 161 397 405 11176766

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Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling
Ray, P. D., Huang, B.-W., & Tsuji, Y. (2012) · Cellular Signalling · doi:10.1016/j.cellsig.2012.01.008 · Cited by 4,373 · see citing works
Pathophysiology of type 2 diabetes mellitus
Galicia-Garcia, U., Benito-Vicente, A., Jebari, S., Larrea-Sebal, A., Siddiqi, H., Uribe, K. B., Ostolaza, H., & Martín, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176275 · Cited by 3,360 · see citing works
Type 2 diabetes mellitus
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Novruzov, E. A., Aliyeva, D. M., Mashadiyeva-Bayramova, S. A., & Bayramov, A. A. (2023) · International Journal of Science and Research Archive · doi:10.30574/ijsra.2023.9.1.0425 · Cited by 1 · see citing works
The Role of Oxidative Stress in the Pathogenesis of Type 2 Diabetes Mellitus Micro- and Macrovascular Complications: Avenues for a Mechanistic-Based Therapeutic Approach
Folli, F. B., Corradi, D., Fanti, P., Davalli, A. M., Paez, A. M., Giaccari, A., Perego, C., & Muscogiuri, G. (2011) · Current Diabetes Reviews · doi:10.2174/157339911797415585 · Cited by 376 · see citing works
Oxidative Stress and Cardiovascular Disease in Diabetes
Pop‐Busui, R., Mehta, M., & Pennathur, S. (2014) · Oxidative stress in applied basic research and clinical practice · doi:10.1007/978-1-4899-8035-9_11 · Cited by 3 · see citing works
Role of Oxidative Stress in Diabetic Cardiomyopathy
Geest, B. D., & Mishra, M. (2022) · Antioxidants · doi:10.3390/antiox11040784 · Cited by 170 · see citing works
Oxidative stress: A cause and therapeutic target of diabetic complications
Araki, E., & Nishikawa, T. (2010) · Journal of Diabetes Investigation · doi:10.1111/j.2040-1124.2010.00013.x · Cited by 139 · see citing works

Authors: Giacco, F., & Brownlee, M.
Affiliations: Albert Einstein College of Medicine (US)
Corresponding author: Brownlee, Michael
Venue: Circulation Research
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2010-10-29
Volume: 107
Issue: 9
Pages: 1058-1070
ISSN: 0009-7330 (ISSN-L)
1524-4571
DOI: 10.1161/circresaha.110.223545
PMC: PMC2996922
OpenAlex: W2105731956
Cited by: 5,461
References: 152
Citations by year: 2026: 305 · 2025: 331 · 2024: 416 · 2023: 448 · 2022: 478 · 2021: 435 · 2020: 411 · 2019: 349 · 2018: 370 · 2017: 367 · 2016: 338 · 2015: 318 · 2014: 327 · 2013: 260 · 2012: 203
FWCI: 17.36
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Circulation Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (R01DK074153, R01-DK07453, P60DK020541)
Topics: Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Keywords: oxidative stress, diabetes complications, superoxide, reactive oxygen species, mitochondrial dysfunction, polyol pathway, advanced glycation end products, AGE receptor, protein kinase C, hexosamine biosynthetic pathway, endothelial nitric oxide synthase, prostacyclin synthase, angiogenesis, inflammation, epigenetic modifications, atherosclerosis, diabetic cardiomyopathy, type 2 diabetes, insulin resistance, superoxide dismutase, diabetic retinopathy, diabetic nephropathy
MeSH terms: Animals, Humans, Hyperglycemia, Cardiomyopathies, Signal Transduction, Reactive Oxygen Species, Oxidative Stress, Diabetes Complications, Atherosclerosis, Microvessels

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