New Insights on Oxidative Stress and Diabetic Complications May Lead to a “Causal” Antioxidant Therapy

Ceriello, Antonio

doi:10.2337/diacare.26.5.1589

Cited by 734Nitric Oxide and Endothelin EffectsAdvanced Glycation End Products researchAntioxidant Activity and Oxidative Stress

New Insights on Oxidative Stress and Diabetic Complications May Lead to a “Causal” Antioxidant Therapy

Ceriello, Antonio·2003·Diabetes Care

DOI 10.2337/diacare.26.5.1589

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Abstract

Evidence implicates hyperglycemia-derived oxygen free radicals as mediators of diabetic complications. However, intervention studies with classic antioxidants, such as vitamin E, failed to demonstrate any beneficial effect. Recent studies demonstrate that a single hyperglycemia-induced process of overproduction of superoxide by the mitochondrial electron-transport chain seems to be the first and key event in the activation of all other pathways involved in the pathogenesis of diabetic complications. These include increased polyol pathway flux, increased advanced glycosylation end product formation, activation of protein kinase C, and increased hexosamine pathway flux. Superoxide overproduction is accompanied by increased nitric oxide generation, due to an endothelial NOS and inducible NOS uncoupled state, a phenomenon favoring the formation of the strong oxidant peroxynitrite, which in turn damages DNA. DNA damage is an obligatory stimulus for the activation of the nuclear enzyme poly(ADP-ribose) polymerase. Poly(ADP-ribose) polymerase activation in turn depletes the intracellular concentration of its substrate NAD+, slowing the rate of glycolysis, electron transport, and ATP formation, and produces an ADP-ribosylation of the GAPDH. These processes result in acute endothelial dysfunction in diabetic blood vessels that, convincingly, also contributes to the development of diabetic complications. These new findings may explain why classic antioxidants, such as vitamin E, which work by scavenging already-formed toxic oxidation products, have failed to show beneficial effects on diabetic complications and may suggest new and attractive “causal” antioxidant therapy. New low–molecular mass compounds that act as SOD or catalase mimetics or l-propionyl-carnitine and lipoic acid, which work as intracellular superoxide scavengers, improving mitochondrial function and reducing DNA damage, may be good candidates for such a strategy, and preliminary studies support this hypothesis. This “causal” therapy would also be associated with other promising tools such as LY 333531, PJ34, and FP15, which block the protein kinase β isoform, poly(ADP-ribose) polymerase, and peroxynitrite, respectively. While waiting for these focused tools, we may have other options: thiazolinediones, statins, ACE inhibitors, and angiotensin 1 inhibitors can reduce intracellular oxidative stress generation, and it has been suggested that many of their beneficial effects, even in diabetic patients, are due to this property.

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The biological actions of statins and AT-1 receptor blockers, including their intracellular antioxidant activity, work through different mechanisms.
“Mechanisms underlying the biological effects of statins and AT-1 receptor blockers differ, even in terms of intracellular antioxidant activity.”
From Effect of Atorvastatin and Irbesartan, Alone and in Combination, on Postprandial Endothelial Dysfunction, Oxidative Stress, and Inflammation in Type 2 Diabetic Patients (2005) · cites this paper as [20]
Statins and AT-1 receptor blockers protect endothelial function and reduce inflammation in diabetic and nondiabetic subjects, an effect convincingly attributed to their intracellular antioxidant activity.
“Statins and AT-1 receptor blockers protect endothelial function and reduce inflammation in diabetic and nondiabetic subjects, and these effects are convincingly mediated through their intracellular antioxidant activity.”
From Effect of Atorvastatin and Irbesartan, Alone and in Combination, on Postprandial Endothelial Dysfunction, Oxidative Stress, and Inflammation in Type 2 Diabetic Patients (2005) · cites this paper as [20]
Considerable reactive oxygen species derives from outside mitochondria, including peroxisomal β-oxidation, NAD(P)H oxidase, xanthine oxidase, arachidonic acid metabolism, microsomal P-450 enzymes, and prooxidant heme.
“Although this review is concerned with mitochondrial ROS, it should be recognized that considerable ROS derives from outside this organelle, including oxygen radicals from peroxisomal β-oxidation of fatty acids (24), NAD(P)H oxidase (53), xanthine oxidase, arachidonic acid metabolism, microsomal P-450 enzymes (75), and the prooxidant heme molecule (226).”
From Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities (2010) · cites this paper as [53]

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Impairment of endothelium-dependent dilatation of cerebral arterioles during diabetes mellitus
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Improvement of Endothelial Function by Chronic Angiotensin-Converting Enzyme Inhibition in Heart Failure
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Diabetic endothelial dysfunction: role of reactive oxygen and nitrogen species production and poly(ADP-ribose) polymerase activation
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Endothelium-Dependent Relaxation in Aorta of BB Rat
Meraji, S., Jayakody, L., SENARATNE, M. P. J., Thomson, A. B. R., & Kappagoda, T. C. (1987) · Diabetes · doi:10.2337/diab.36.8.978 · Cited by 155 · see citing works
A hydroxyl radical–like species oxidizes cynomolgus monkey artery wall proteins in early diabetic vascular disease
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Vascular targets of redox signalling in diabetes mellitus
Spitaler, M. M., & Graier, W. F. (2002) · Diabetologia · doi:10.1007/s00125-002-0782-0 · Cited by 149 · see citing works
Topical hyperglycemia rapidly suppresses EDRF-mediated vasodilation of normal rat arterioles
Bohlen, H. G., & Lash, J. M. (1993) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1993.265.1.h219 · Cited by 145 · see citing works
Glutathione reverses systemic hemodynamic changes induced by acute hyperglycemia in healthy subjects
Marfella, R., Verrazzo, G., Acampora, R., La Marca, C., Giunta, R., Lucarelli, C., Paolisso, G., Ceriello, A., & Giugliano, D. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.6.e1167 · Cited by 129 · see citing works
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Free radical scavenging is involved in the protective effect of l-propionyl-carnitine against ischemia-reperfusion injury of the heart
Packer, L., Valenza, M., Serbinova, E. A., Starke-Reed, P. E., Frost, K., & Kagan, V. E. (1991) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(91)90231-7 · Cited by 118 · see citing works
PPARγ ligands inhibit nitrotyrosine formation and inflammatory mediator expressions in adjuvant-induced rheumatoid arthritis mice
Shiojiri, T., Wada, K., Nakajima, A., Katayama, K., Shibuya, A., Kudo, C., Kadowaki, T., Mayumi, T., Yura, Y., & Kamisaki, Y. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)01946-5 · Cited by 111 · see citing works
Effects of Insulin and Antioxidant on Plasma 8-Hydroxyguanine and Tissue 8-Hydroxydeoxyguanosine in Streptozotocin-Induced Diabetic Rats
Park, K. S., Kim, J. H., Kim, M., Kim, J. M., Kim, S. K., Choi, J. Y., Chung, M. H., Han, B., Kim, S. Y., & Lee, H. K. (2001) · Diabetes · doi:10.2337/diabetes.50.12.2837 · Cited by 108 · see citing works
Nitrotyrosine Causes Selective Vascular Endothelial Dysfunction and DNA Damage
Mihm, M. J., Liang, J., & Bauer, J. A. (2000) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-200008000-00007 · Cited by 107 · see citing works
Glucose Increases Endothelial-Dependent Superoxide Formation in Coronary Arteries by NAD(P)H Oxidase Activation
Christ, M., Bauersachs, J., Liebetrau, C., Heck, M., Günther, A., & Wehling, M. (2002) · Diabetes · doi:10.2337/diabetes.51.8.2648 · Cited by 107 · see citing works
Diabetes-induced elevations in retinal oxidative stress, protein kinase C and nitric oxide are interrelated
Kowluru, A. (2001) · Acta Diabetologica · doi:10.1007/s592-001-8076-6 · Cited by 106 · see citing works
Hyperglycemic switch from mitochondrial nitric oxide to superoxide production in endothelial cells
Brodsky, S. V., Gao, S., Li, H., & Goligorsky, M. S. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00196.2002 · Cited by 92 · see citing works
Effects of the superoxide dismutase-mimetic compound tempol on endothelial dysfunction in streptozotocin-induced diabetic rats
Nassar, T., Kadery, B., Lotan, C., Da’as, N., Kleinman, Y., & Haj-Yehia, A. I. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(01)01566-7 · Cited by 92 · see citing works
Effect of M40403 treatment of diabetic rats on endoneurial blood flow, motor nerve conduction velocity and vascular function of epineurial arterioles of the sciatic nerve
Coppey, L. J., Gellett, J. S., Davidson, E. P., Dunlap, J. A., Lund, D. D., Salvemini, D., & Yorek, M. A. (2001) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704216 · Cited by 91 · see citing works
Endothelium-dependent relaxation in aorta of BB rat
Meraji, S., Jayakody, L., SENARATNE, M. P. J., et al. (1987) · Diabetes · doi:10.2337/diabetes.36.8.978 · Cited by 77 · see citing works
Statin-stimulated nitric oxide release from endothelium.
Dobrucki, L. W., Kalinowski, L., Dobrucki, I. T., & Maliñski, T. (2001) · PubMed · Cited by 76 · see citing works
Hyperglycemia modulates angiotensinogen gene expression
Gabriely, I., Yang, X. M., Cases, J. A., Xiao, H., Rossetti, L., & Barzilai, N. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.3.r795 · Cited by 57 · see citing works
Effects of propionyl-l-carnitine on isolated mitochondrial function in the reperfused diabetic rat heart
Felix, C. A., Gillis, M., Driedzic, W. R., Paulson, D. J., & Broderick, T. L. (2001) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(01)00240-6 · Cited by 31 · see citing works
?-propionylcarnitine Enhancement of Substrate Oxidation and Mitochondrial Respiration in the Diabetic Rat Heart
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Possible involvement of ADP-ribosylation of particular enzymes in cell death induced by nitric oxide-donors in human neuroblastoma cells
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Effects of acetyl- and proprionyl-l-carnitine on peripheral nerve function and vascular supply in experimental diabetes
Cotter, M. A., Cameron, N. E., Keegan, A., & Dines, K. C. (1995) · Metabolism · doi:10.1016/0026-0495(95)90018-7 · Cited by 25 · see citing works
Angiotensin-Receptor Blockers, Type 2 Diabetes, and Renoprotection
(2002) · New England Journal of Medicine · doi:10.1056/nejm200202283460912 · Cited by 16 · see citing works
Self-citation
Hypertension and ascorbic acid
Ness, A., & Sterne, J. A. C. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02101-2 · Cited by 11 · see citing works
Hypertension and ascorbic acid
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Nitric Oxide and Peroxynitrite in Health and Disease
Pacher, P., Beckman, J. S., & Liaudet, L. (2007) · Physiological Reviews · doi:10.1152/physrev.00029.2006 · Cited by 6,390 · see citing works
Is Oxidative Stress the Pathogenic Mechanism Underlying Insulin Resistance, Diabetes, and Cardiovascular Disease? The Common Soil Hypothesis Revisited
Ceriello, A., & Motz, E. (2004) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000122852.22604.78 · Cited by 1,378 · see citing works
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Diabetes and mitochondrial function: Role of hyperglycemia and oxidative stress
Rolo, A. P., & Palmeira, C. M. (2006) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2006.01.003 · Cited by 1,007 · see citing works
Oxidative stress and the use of antioxidants in diabetes: Linking basic science to clinical practice
Johansen, J. S., Harris, A. K., Rychly, D. J., & Ergul, A. (2005) · Cardiovascular Diabetology · doi:10.1186/1475-2840-4-5 · Cited by 1,003 · see citing works
Postprandial Hyperglycemia and Diabetes Complications
Ceriello, A. (2005) · Diabetes · doi:10.2337/diabetes.54.1.1 · Cited by 945 · see citing works
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Mitochondrial Dysfunction in Diabetes: From Molecular Mechanisms to Functional Significance and Therapeutic Opportunities
Sivitz, W. I., & Yorek, M. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2531 · Cited by 742 · see citing works
Biomarkers of Endothelial Dysfunction and Risk of Type 2 Diabetes Mellitus
Meigs, J. B. (2004) · JAMA · doi:10.1001/jama.291.16.1978 · Cited by 643 · see citing works
The Molecular Basis for Oxidative Stress-Induced Insulin Resistance
Evans, J. L., Maddux, B. A., & Goldfine, I. D. (2005) · Antioxidants & Redox Signaling · doi:10.1089/ars.2005.7.1040 · Cited by 587 · see citing works
The Role of Oxidative Stress in Diabetic Complications
Niedowicz, D. M., & Daleke, D. L. (2005) · Cell Biochemistry and Biophysics · doi:10.1385/cbb:43:2:289 · Cited by 528 · see citing works
The Significance of Vascular and Neural Apoptosis to the Pathology of Diabetic Retinopathy
Barber, A. J., Gardner, T. W., & Abcouwer, S. F. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-6293 · Cited by 438 · see citing works
The “Metabolic Memory”: Is More Than Just Tight Glucose Control Necessary to Prevent Diabetic Complications?
Ceriello, A., Ihnat, M. A., & Thorpe, J. E. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1824 · Cited by 411 · see citing works
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Pathogenesis of Chronic Hyperglycemia: From Reductive Stress to Oxidative Stress
Yan, L. (2014) · Journal of Diabetes Research · doi:10.1155/2014/137919 · Cited by 403 · see citing works
Antioxidant and free radical scavenging potential of Achillea santolina extracts
Ardestani, A. D., & Yazdanparast, R. (2006) · Food Chemistry · doi:10.1016/j.foodchem.2006.10.066 · Cited by 391 · see citing works
In vivo assessment of antidiabetic and antioxidant activities of rosemary (Rosmarinus officinalis) in alloxan-diabetic rabbits
Bakırel, T., Bakırel, U., Üstüner, O., Ülgen, S., & Yardibi, H. (2007) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2007.10.039 · Cited by 390 · see citing works
Anti-oxidant effect of gold nanoparticles restrains hyperglycemic conditions in diabetic mice
BarathManiKanth, S., Kalishwaralal, K., Sriram, M. I., Pandian, S. R. K., Youn, H., Eom, S.-H., & Gurunathan, S. (2010) · Journal of Nanobiotechnology · doi:10.1186/1477-3155-8-16 · Cited by 386 · see citing works
Lipid Peroxidation in Diabetes Mellitus
Davı̀, G., Falco, A., & Patrono, C. (2004) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.256 · Cited by 377 · see citing works
Effect of Postprandial Hypertriglyceridemia and Hyperglycemia on Circulating Adhesion Molecules and Oxidative Stress Generation and the Possible Role of Simvastatin Treatment
Ceriello, A., Quagliaro, L., Piconi, L., Assaloni, R., Da Ros, R., Maier, A., Esposito, K., & Giugliano, D. (2004) · Diabetes · doi:10.2337/diabetes.53.3.701 · Cited by 362 · see citing works
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Resveratrol Improves Oxidative Stress and Protects Against Diabetic Nephropathy Through Normalization of Mn-SOD Dysfunction in AMPK/SIRT1-Independent Pathway
Kitada, M., Kume, S., Imaizumi, N., & Koya, D. (2011) · Diabetes · doi:10.2337/db10-0386 · Cited by 345 · see citing works
Evaluation of a New Measure of Blood Glucose Variability in Diabetes
Kovatchev, B. P., Otto, E., Cox, D. J., Gonder-Frederick, L. A., & Clarke, W. L. (2006) · Diabetes Care · doi:10.2337/dc06-1085 · Cited by 333 · see citing works
Mechanistic Insight into Oxidative Stress-Triggered Signaling Pathways and Type 2 Diabetes
Singh, A., Kukreti, R., Saso, L., & Kukreti, S. (2022) · Molecules · doi:10.3390/molecules27030950 · Cited by 332 · see citing works
Role of Nitrosative Stress and Peroxynitrite in the Pathogenesis of Diabetic Complications. Emerging New Therapeutical Strategies
Pacher, P., Obrosova, I. G., Mabley, J. G., & Szabó, C. (2005) · Current Medicinal Chemistry · doi:10.2174/0929867053363207 · Cited by 331 · see citing works
Constant and intermittent high glucose enhances endothelial cell apoptosis through mitochondrial superoxide overproduction
Piconi, L., Quagliaro, L., Assaloni, R., ROS, R. D., Maier, A., Zuodar, G., & Ceriello, A. (2006) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.613 · Cited by 326 · see citing works
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Oxidative stress and diabetic retinopathy: Pathophysiological mechanisms and treatment perspectives
Madsen-Bouterse, S. A., & Kowluru, R. (2008) · Reviews in Endocrine & Metabolic Disorders · doi:10.1007/s11154-008-9090-4 · Cited by 313 · see citing works
Effect of Atorvastatin and Irbesartan, Alone and in Combination, on Postprandial Endothelial Dysfunction, Oxidative Stress, and Inflammation in Type 2 Diabetic Patients
Ceriello, A., Assaloni, R., Da Ros, R., Maier, A., Piconi, L., Quagliaro, L., Esposito, K., & Giugliano, D. (2005) · Circulation · doi:10.1161/01.cir.0000165070.46111.9f · Cited by 298 · see citing works
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The molecular mechanisms of pancreatic β-cell glucotoxicity: recent findings and future research directions.
Bensellam, M., Laybutt, D., & Jonas, J. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.08.003 · Cited by 282 · see citing works
Diabetes and the Impairment of Reproductive Function: Possible Role of Mitochondria and Reactive Oxygen Species
Ramalho-Santos, J., Amaral, S., & Oliveira, P. (2008) · Current Diabetes Reviews · doi:10.2174/157339908783502398 · Cited by 359 · see citing works
Oxidative Stress in Diabetes
Piconi, L., Quagliaro, L., & Ceriello, A. (2003) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2003.177 · Cited by 255 · see citing works
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Advanced glycation endproducts (AGEs): pharmacological inhibition in diabetes
Peyroux, J., & Sternberg, M. (2006) · Pathologie Biologie · doi:10.1016/j.patbio.2006.07.006 · Cited by 247 · see citing works
Curcumin-induced inhibition of cellular reactive oxygen species generation: Novel therapeutic implications
Balasubramanyam, M., Koteswari, A., Kumar, R. S., Monickaraj, S. F., Maheswari, J., & Mohan, V. (2003) · Journal of Biosciences · doi:10.1007/bf02708432 · Cited by 268 · see citing works
Insulin resistance: an additional risk factor in the pathogenesis of cardiovascular disease in type 2 diabetes
Patel, T. P., Rawal, K., Bagchi, A. K., Akolkar, G., Bernardes, N., Dias, D. D. S., Gupta, S. S., & Singal, P. K. (2015) · Heart Failure Reviews · doi:10.1007/s10741-015-9515-6 · Cited by 240 · see citing works
Nitrosative stress and pharmacological modulation of heart failure
Pacher, P., Schulz, R., Liaudet, L., & Szabó, C. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.04.003 · Cited by 237 · see citing works
Coffee consumption and reduced risk of developing type 2 diabetes: a systematic review with meta-analysis
Carlström, M., & Larsson, S. C. (2018) · Nutrition Reviews · doi:10.1093/nutrit/nuy014 · Cited by 242 · see citing works
Diabetic nephropathy: Is there a role for oxidative stress?
Sagoo, M. K., & Gnudi, L. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.12.040 · Cited by 233 · see citing works
The Keap1-Nrf2 system and diabetes mellitus
Uruno, A., Yagishita, Y., & Yamamoto, M. (2015) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2014.12.012 · Cited by 231 · see citing works
Possible role of oxidative stress in the pathogenesis of hypertension
Ceriello, A. (2008) · Diabetes Care · doi:10.2337/dc08-s245 · Cited by 215 · see citing works
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Therapeutic Applications of Rose Hips from Different Rosa Species
Mármol, I., Sánchez‐de‐Diego, C., Jiménez‐Moreno, N., Ancín‐Azpilicueta, C., & Rodriguez‐Yoldi, M. J. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18061137 · Cited by 213 · see citing works
Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2‐deficient mice
Yoh, K., Hirayama, A., Ishizaki, K., Yamada, A., Takeuchi, M., Yamagishi, S., Morito, N., Nakano, T., Ojima, M., Shimohata, H., et al. (2008) · Genes to Cells · doi:10.1111/j.1365-2443.2008.01234.x · Cited by 207 · see citing works
Activation of Nrf2 signaling by natural products-can it alleviate diabetes?
Matzinger, M., Fischhuber, K., & Heiß, E. H. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.12.015 · Cited by 205 · see citing works
Chronic Kidney Disease Influences Multiple Systems: Describing the Relationship between Oxidative Stress, Inflammation, Kidney Damage, and Concomitant Disease
Tucker, P. S., Scanlan, A. T., & Dalbo, V. J. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/806358 · Cited by 203 · see citing works
Inhibition of Superoxide Generation and Associated Nitrosative Damage Is Involved in Metallothionein Prevention of Diabetic Cardiomyopathy
Cai, L., Wang, J., Li, Y., Sun, X., Wang, L., Zhou, Z., & Kang, Y. J. (2005) · Diabetes · doi:10.2337/diabetes.54.6.1829 · Cited by 199 · see citing works
Catalase delivery for inhibiting ROS-mediated tissue injury and tumor metastasis
Nishikawa, M., Hashida, M., & Takakura, Y. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.01.001 · Cited by 199 · see citing works
Intervention against the Maillard reaction in vivo
Monnier, V. M. (2003) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2003.08.014 · Cited by 196 · see citing works
Diabetic nephropathy and antioxidants
Tavafi, M. (2013) · Journal of Nephropathology · doi:10.5812/nephropathol.9093 · Cited by 195 · see citing works
Antioxidant Anti-Inflammatory Treatment in Type 2 Diabetes
Ceriello, A., & Testa, R. (2009) · Diabetes Care · doi:10.2337/dc09-s316 · Cited by 199 · see citing works
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Effect of NCB-02, Atorvastatin and Placebo on Endothelial Function, Oxidative Stress and Inflammatory Markers in Patients with Type 2 Diabetes Mellitus
Usharani, P., Mateen, A., Naidu, M. U. R., Raju, Y. S. N., & Chandra, N. (2008) · Drugs in R&D · doi:10.2165/00126839-200809040-00004 · Cited by 195 · see citing works
Mitochondria, Synaptic Plasticity, And Schizophrenia
Ben‐Shachar, D., & Laifenfeld, D. (2004) · International review of neurobiology · doi:10.1016/s0074-7742(04)59011-6 · Cited by 194 · see citing works
Dietary Advanced Glycation End Products and Risk Factors for Chronic Disease: A Systematic Review of Randomised Controlled Trials
Clarke, R., Dordevic, A. L., Tan, S. M., Ryan, L., & Coughlan, M. T. (2016) · Nutrients · doi:10.3390/nu8030125 · Cited by 186 · see citing works
Role of Poly(ADP-Ribose) Polymerase-1 Activation in the Pathogenesis of Diabetic Complications: Endothelial Dysfunction, as a Common Underlying Theme
Pacher, P., & Szabó, C. (2005) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.1568 · Cited by 180 · see citing works
Postprandial hyperglycemia as an etiological factor in vascular failure
Node, K., & Inoue, T. (2009) · Cardiovascular Diabetology · doi:10.1186/1475-2840-8-23 · Cited by 182 · see citing works
The Role of Oxidative Stress, Mitochondrial Function, and Autophagy in Diabetic Polyneuropathy
Sifuentes-Franco, S., Pacheco-Moisés, F. P., Rodríguez-Carrizález, A. D., & Miranda‐Díaz, A. G. (2017) · Journal of Diabetes Research · doi:10.1155/2017/1673081 · Cited by 180 · see citing works
Sulforaphane: Its “Coming of Age” as a Clinically Relevant Nutraceutical in the Prevention and Treatment of Chronic Disease
Houghton, C. A. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/2716870 · Cited by 183 · see citing works
Mild hypoglycemia is independently associated with increased mortality in the critically ill
Krinsley, J. S., Schultz, M. J., Spronk, P. E., Harmsen, R. E., Houckgeest, F. V. B., van der Sluijs, J. P., Mélot, C., & Preiser, J. (2011) · Critical Care · doi:10.1186/cc10322 · Cited by 179 · see citing works
Role of peroxynitrite in the pathogenesis of cardiovascular complications of diabetes
Pacher, P., & Szabó, C. (2006) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2006.01.001 · Cited by 173 · see citing works
The emerging challenge in diabetes: The “metabolic memory”
Ceriello, A. (2012) · Vascular Pharmacology · doi:10.1016/j.vph.2012.05.005 · Cited by 174 · see citing works
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Oxidative stress in diabetes: A mechanistic overview of its effects on atherogenesis and myocardial dysfunction
Mehta, J. L., Rasouli, N., Sinha, A. K., & Molavi, B. (2006) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.12.008 · Cited by 169 · see citing works
Hypothesis: the ‘metabolic memory’, the new challenge of diabetes
Ihnat, M. A., Thorpe, J. E., & Ceriello, A. (2007) · Diabetic Medicine · doi:10.1111/j.1464-5491.2007.02138.x · Cited by 167 · see citing works
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Postprandial glucose regulation: New data andnew implications
Leiter, L. A., Ceriello, A., Davidson, J. A., Hanefeld, M., Monnier, L., Owens, D. R., Tajima, N., & Tuomilehto, J. O. (2005) · Clinical Therapeutics · doi:10.1016/j.clinthera.2005.11.020 · Cited by 159 · see citing works
Self-citation
α-lipoic acid induces apoptosis in human colon cancer cells by increasing mitochondrial respiration with a concomitant O2−.-generation
Wenzel, U., Nickel, A. G., & Daniel, H. (2005) · APOPTOSIS · doi:10.1007/s10495-005-0810-x · Cited by 159 · see citing works
Attenuation of Angiotensin II Signaling Recouples eNOS and Inhibits Nonendothelial NOX Activity in Diabetic Mice
Oak, J., & Cai, H. “. (2006) · Diabetes · doi:10.2337/db06-0288 · Cited by 157 · see citing works
Postprandial hyperglycaemia and cardiovascular complications of diabetes: An update
Ceriello, A., Davidson, J., Markolf Hanefeld, E., Leiter, L. A., Monnier, L., Owens, D. R., Tajima, N., & Tuomilehto, J. O. (2006) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2006.05.006 · Cited by 149 · see citing works
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Evaluation of oxidative stress markers in pathogenesis of diabetic neuropathy
Kasznicki, J., Kosmalski, M., Śliwińska, A., Mrowicka, M., Stańczyk, M. B., Majsterek, I., & Drzewoski, J. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1722-9 · Cited by 146 · see citing works
The research and development on the antioxidants in prevention of diabetic complications
Rahimi‐Madiseh, M., Malekpour-Tehrani, A., Bahmani, M., & Rafieian‐Kopaei, M. (2016) · Asian Pacific Journal of Tropical Medicine · doi:10.1016/j.apjtm.2016.07.001 · Cited by 145 · see citing works
Erythritol is a sweet antioxidant
den Hartog, G. J. M., Boots, A. W., Adam‐Perrot, A., Brouns, F. J. P. H., Verkooijen, I., Weseler, A. R., Haenen, G. R. M. M., & Bast, A. (2009) · Nutrition · doi:10.1016/j.nut.2009.05.004 · Cited by 140 · see citing works
Hypoglycemic and antioxidant effects of leaf essential oil of Pelargonium graveolens L’Hér. in alloxan induced diabetic rats
Boukhris, M., Bouaziz, M. A., Feki, I., Jemai, H., Feki, A. E., & Sayadi, S. (2012) · Lipids in Health and Disease · doi:10.1186/1476-511x-11-81 · Cited by 138 · see citing works
Regular Physical Exercise as a Strategy to Improve Antioxidant and Anti-Inflammatory Status: Benefits in Type 2 Diabetes Mellitus
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New insights on oxidative stress and diabetic complications may lead to a “causal” antioxidant therapy. Diabetes Care May 2003
Md, A. C. (2016)
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Authors: Ceriello, A.
Affiliations: University of Udine (IT)
Corresponding author: Ceriello, Antonio
ORCID: Ceriello, Antonio
Venue: Diabetes Care
Publisher: American Diabetes Association
Published: 2003-05-01
Volume: 26
Issue: 5
Pages: 1589-1596
ISSN: 0149-5992 (ISSN-L)
1935-5548
DOI: 10.2337/diacare.26.5.1589
OpenAlex: W2058550328
Cited by: 734
References: 102
Citations by year: 2026: 9 · 2025: 8 · 2024: 16 · 2023: 15 · 2022: 16 · 2021: 24 · 2020: 13 · 2019: 27 · 2018: 34 · 2017: 41 · 2016: 33 · 2015: 34 · 2014: 46 · 2013: 49 · 2012: 50
FWCI: 4.48
Type: journal article
Language: en
Open access: closed
Locations: Diabetes Care (publishedVersion)
PubMed (publishedVersion)
Institutional Research Information System (University of Udine) (submittedVersion)
Topics: Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
Keywords: oxidative stress, diabetes complications, superoxide, mitochondrial electron transport chain, hyperglycemia, polyol pathway, advanced glycation end products, protein kinase C, hexosamine biosynthetic pathway, nitric oxide, peroxynitrite, DNA damage, poly(ADP-ribose) polymerase, NAD+ depletion, endothelial dysfunction, antioxidant therapy, superoxide dismutase mimetic, catalase mimetics, alpha-lipoic acid, PJ34, thiazolidinediones, statins, ACE inhibitors, angiotensin receptor blockers
MeSH terms: Antioxidants, Diabetes Mellitus, DNA Damage, Endothelium, Vascular, Humans, Hyperglycemia, Models, Biological, Oxidative Stress, Peroxynitrous Acid, Diabetes Complications

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New Insights on Oxidative Stress and Diabetic Complications May Lead to a “Causal” Antioxidant Therapy

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