Nothing Special   »   [go: up one dir, main page]
Skip to main content

Advertisement

Springer Nature Link
Log in

Oxidative stress and diabetes: antioxidative strategies

  • Review
  • Published:
Frontiers of Medicine Aims and scope Submit manuscript

Abstract

Diabetes mellitus is one of the major public health problems worldwide. Considerable recent evidence suggests that the cellular reduction-oxidation (redox) imbalance leads to oxidative stress and subsequent occurrence and development of diabetes and related complications by regulating certain signaling pathways involved in β-cell dysfunction and insulin resistance. Reactive oxide species (ROS) can also directly oxidize certain proteins (defined as redox modification) involved in the diabetes process. There are a number of potential problems in the clinical application of antioxidant therapies including poor solubility, storage instability and nonselectivity of antioxidants. Novel antioxidant delivery systems may overcome pharmacokinetic and stability problem and improve the selectivity of scavenging ROS. We have therefore focused on the role of oxidative stress and antioxidative therapies in the pathogenesis of diabetes mellitus. Precise therapeutic interventions against ROS and downstream targets are now possible and provide important new insights into the treatment of diabetes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Evans JM, Newton RW, Ruta DA, MacDonald TM, Morris AD. Socio-economic status, obesity and prevalence of type 1 and type 2 diabetes mellitus. Diabet Med 2000; 17(6): 478–480

    CAS  PubMed  Google Scholar 

  2. Bruno G, Runzo C, Cavallo-Perin P, Merletti F, Rivetti M, Pinach S, Novelli G, Trovati M, Cerutti F, Pagano G; Piedmont Study Group for Diabetes Epidemiology. Incidence of type 1 and type 2 diabetes in adults aged 30–49 years: the population-based registry in the Province of Turin, Italy. Diabetes Care 2005; 28(11): 2613–2619

    PubMed  Google Scholar 

  3. Holman N, Young B, Gadsby R. Current prevalence of type 1 and type 2 diabetes in adults and children in the UK. Diabet Med 2015; 32(9): 1119–1120

    CAS  PubMed  Google Scholar 

  4. Yang Y, Chan L. Monogenic diabetes: what it teaches us on the common forms of type 1 and type 2 diabetes. Endocr Rev 2016; 37(3): 190–222

    PubMed  PubMed Central  Google Scholar 

  5. Matkovics B, Varga SI, Szabó L, Witas H. The effect of diabetes on the activities of the peroxide metabolism enzymes. Horm Metab Res 1982; 14(2): 77–79

    CAS  PubMed  Google Scholar 

  6. Paoletti R, Bolego C, Poli A, Cignarella A. Metabolic syndrome, inflammation and atherosclerosis. Vasc Health Risk Manag 2006; 2(2): 145–152

    PubMed  PubMed Central  Google Scholar 

  7. Bukhari SA, Naqvi SA, Nagra SA, Anjum F, Javed S, Farooq M. Assessing of oxidative stress related parameters in diabetes mellitus type 2: cause excessive damaging to DNA and enhanced homocysteine in diabetic patients. Pak J Pharm Sci 2015; 28(2): 483–491

    CAS  PubMed  Google Scholar 

  8. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 2002; 23(5): 599–622

    CAS  PubMed  Google Scholar 

  9. David JA, Rifkin WJ, Rabbani PS, Ceradini DJ. The Nrf2/Keap1/ ARE pathway and oxidative stress as a therapeutic target in type II diabetes mellitus. J Diabetes Res 2017; 2017: 4826724

    PubMed  PubMed Central  Google Scholar 

  10. Okatan EN, Tuncay E, Turan B. Cardioprotective effect of selenium via modulation of cardiac ryanodine receptor calcium release channels in diabetic rat cardiomyocytes through thioredoxin system. J Nutr Biochem 2013; 24(12): 2110–2118

    CAS  PubMed  Google Scholar 

  11. Duvvuri LS, Katiyar S, Kumar A, Khan W. Delivery aspects of antioxidants in diabetes management. Expert Opin Drug Deliv 2015; 12(5): 827–844

    CAS  PubMed  Google Scholar 

  12. Maritim AC, Sanders RA, Watkins JB 3rd. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 2003; 17(1): 24–38

    CAS  PubMed  Google Scholar 

  13. Calcutt NA, Lopez VL, Bautista AD, Mizisin LM, Torres BR, Shroads AL, Mizisin AP, Stacpoole PW. Peripheral neuropathy in rats exposed to dichloroacetate. J Neuropathol Exp Neurol 2009; 68(9): 985–993

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Gray SP, Jandeleit-Dahm K. The pathobiology of diabetic vascular complications-cardiovascular and kidney disease. J Mol Med (Berl) 2014; 92(5): 441–452

    CAS  Google Scholar 

  15. Heinonen SE, Genové G, Bengtsson E, Hübschle T, Åkesson L, Hiss K, Benardeau A, Ylä-Herttuala S, Jönsson-Rylander AC, Gomez MF. Animal models of diabetic macrovascular complications: key players in the development of new therapeutic approaches. J Diabetes Res 2015; 2015: 404085

    PubMed  PubMed Central  Google Scholar 

  16. Gong Z, Neuhouser ML, Goodman PJ, Albanes D, Chi C, Hsing AW, Lippman SM, Platz EA, Pollak MN, Thompson IM, Kristal AR. Obesity, diabetes, and risk of prostate cancer: results from the prostate cancer prevention trial. Cancer Epidemiol Biomarkers Prev 2006; 15(10): 1977–1983

    PubMed  Google Scholar 

  17. Lu FP, Lin KP, Kuo HK. Diabetes and the risk of multi-system aging phenotypes: a systematic review and meta-analysis. PLoS One 2009; 4(1): e4144

    Google Scholar 

  18. Wong E, Backholer K, Gearon E, Harding J, Freak-Poli R, Stevenson C, Peeters A. Diabetes and risk of physical disability in adults: a systematic review and meta-analysis. Lancet Diabetes Endocrinol 2013; 1(2): 106–114

    PubMed  Google Scholar 

  19. Jeon CY, Murray MB. Diabetes mellitus increases the risk of active tuberculosis: a systematic review of 13 observational studies. PLoS Med 2008; 5(7): e152

    PubMed  PubMed Central  Google Scholar 

  20. Riza AL, Pearson F, Ugarte-Gil C, Alisjahbana B, van de Vijver S, Panduru NM, Hill PC, Ruslami R, Moore D, Aarnoutse R, Critchley JA, van Crevel R. Clinical management of concurrent diabetes and tuberculosis and the implications for patient services. Lancet Diabetes Endocrinol 2014; 2(9): 740–753

    PubMed  PubMed Central  Google Scholar 

  21. Roy T, Lloyd CE. Epidemiology of depression and diabetes: a systematic review. J Affect Disord 2012; 142(Suppl): S8–S21

    Google Scholar 

  22. You WP, Henneberg M. Type 1 diabetes prevalence increasing globally and regionally: the role of natural selection and life expectancy at birth. BMJ Open Diabetes Res Care 2016; 4(1): e000161

    PubMed  PubMed Central  Google Scholar 

  23. Bluestone JA, Herold K, Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 2010; 464(7293): 1293–1300

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Katsarou A, Gudbjörnsdottir S, Rawshani A, Dabelea D, Bonifacio E, Anderson BJ, Jacobsen LM, Schatz DA, Lernmark Å. Type 1 diabetes mellitus. Nat Rev Dis Primers 2017; 3(1): 17016

    PubMed  Google Scholar 

  25. Barnett R. Type 1 diabetes. Lancet 2018; 391(10117): 195

    PubMed  Google Scholar 

  26. Sakurai T, Tsuchiya S. Superoxide production from nonenzymatically glycated protein. FEBS Lett 1988; 236(2): 406–410

    CAS  PubMed  Google Scholar 

  27. Rochette L, Zeller M, Cottin Y, Vergely C. Diabetes, oxidative stress and therapeutic strategies. Biochim Biophys Acta 2014; 1840(9): 2709–2729

    CAS  PubMed  Google Scholar 

  28. Zeller M, Steg PG, Ravisy J, Lorgis L, Laurent Y, Sicard P, Janin- Manificat L, Beer JC, Makki H, Lagrost AC, Rochette L, Cottin Y; RICO Survey Working Group. Relation between body mass index, waist circumference, and death after acute myocardial infarction. Circulation 2008; 118(5): 482–490

    PubMed  Google Scholar 

  29. Olsson AH, Rönn T, Elgzyri T, Hansson O, Eriksson KF, Groop L, Vaag A, Poulsen P, Ling C. The expression of myosin heavy chain (MHC) genes in human skeletal muscle is related to metabolic characteristics involved in the pathogenesis of type 2 diabetes. Mol Genet Metab 2011; 103(3): 275–281

    CAS  PubMed  Google Scholar 

  30. Kahn CR. Banting Lecture. Insulin action, diabetogenes, and the cause of type II diabetes. Diabetes 1994; 43(8): 1066–1084

    CAS  PubMed  Google Scholar 

  31. Ayepola OR, Brooks NL, Oguntibeju O. Oxidative stress and diabetic complications: the role of antioxidant vitamins and flavonoids. In: Oguntibeju O. Antioxidant-Antidiabetic Agents and Human Health. IntechOpen, 2014

    Google Scholar 

  32. Fetita LS, Sobngwi E, Serradas P, Calvo F, Gautier JF. Consequences of fetal exposure to maternal diabetes in offspring. J Clin Endocrinol Metab 2006; 91(10): 3718–3724

    CAS  PubMed  Google Scholar 

  33. Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and metaanalysis. Lancet 2009; 373(9677): 1773–1779

    CAS  PubMed  Google Scholar 

  34. Catalano PM, McIntyre HD, Cruickshank JK, McCance DR, Dyer AR, Metzger BE, Lowe LP, Trimble ER, Coustan DR, Hadden DR, Persson B, Hod M, Oats JJ; HAPO Study Cooperative Research Group. The hyperglycemia and adverse pregnancy outcome study: associations of GDM and obesity with pregnancy outcomes. Diabetes Care 2012; 35(4): 780–786

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Kelstrup L, Damm P, Mathiesen ER, Hansen T, Vaag AA, Pedersen O, Clausen TD. Insulin resistance and impaired pancreatic β-cell function in adult offspring of women with diabetes in pregnancy. J Clin Endocrinol Metab 2013; 98(9): 3793–3801

    CAS  PubMed  PubMed Central  Google Scholar 

  36. World Health Organization. WHO Guidelines Approved by the Guidelines Review Committee. In: Diagnostic Criteria and Classification of Hyperglycaemia First Detected in Pregnancy. Geneva: World Health Organization, 2013

    Google Scholar 

  37. Radaelli T, Varastehpour A, Catalano P, Hauguel-de Mouzon S. Gestational diabetes induces placental genes for chronic stress and inflammatory pathways. Diabetes 2003; 52(12): 2951–2958

    CAS  PubMed  Google Scholar 

  38. Mrizak I, Grissa O, Henault B, Fekih M, Bouslema A, Boumaiza I, Zaouali M, Tabka Z, Khan NA. Placental infiltration of inflammatory markers in gestational diabetic women. Gen Physiol Biophys 2014; 33(2): 169–176

    CAS  PubMed  Google Scholar 

  39. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 2004; 24(5): 816–823

    CAS  PubMed  Google Scholar 

  40. Mohsen L, Akmal DM, Ghonaim EKE, Riad NM. Role of mean platelet volume and ischemia modified albumin in evaluation of oxidative stress and its association with postnatal complications in infants of diabetic mothers. J Matern Fetal Neonatal Med 2018; 31(14): 1819–1823

    CAS  PubMed  Google Scholar 

  41. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 2008; 57(6): 1446–1454

    CAS  PubMed  Google Scholar 

  42. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39(1): 44–84

    CAS  PubMed  Google Scholar 

  43. Abhary S, Kasmeridis N, Burdon KP, Kuot A, Whiting MJ, Yew WP, Petrovsky N, Craig JE. Diabetic retinopathy is associated with elevated serum asymmetric and symmetric dimethylarginines. Diabetes Care 2009; 32(11): 2084–2086

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Cassuto J, Dou H, Czikora I, Szabo A, Patel VS, Kamath V, Belin de Chantemele E, Feher A, Romero MJ, Bagi Z. Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow-mediated dilation in coronary arterioles of diabetic patients. Diabetes 2014; 63(4): 1381–1393

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Franco MC, Ye Y, Refakis CA, Feldman JL, Stokes AL, Basso M, Melero Fernández de Mera RM, Sparrow NA, Calingasan NY, Kiaei M, Rhoads TW, Ma TC, Grumet M, Barnes S, Beal MF, Beckman JS, Mehl R, Estévez AG. Nitration of Hsp90 induces cell death. Proc Natl Acad Sci USA 2013; 110(12): E1102–E1111

    CAS  PubMed  Google Scholar 

  46. Shadel GS, Horvath TL. Mitochondrial ROS signaling in organismal homeostasis. Cell 2015; 163(3): 560–569

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Ekstedt B. Substrate specificity of the different forms of monoamine oxidase in rat liver mitochondria. Biochem Pharmacol 1976; 25(10): 1133–1138

    CAS  PubMed  Google Scholar 

  48. Orsini F, Migliaccio E, Moroni M, Contursi C, Raker VA, Piccini D, Martin-Padura I, Pelliccia G, Trinei M, Bono M, Puri C, Tacchetti C, Ferrini M, Mannucci R, Nicoletti I, Lanfrancone L, Giorgio M, Pelicci PG. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates trans-membrane potential. J Biol Chem 2004; 279(24): 25689–25695

    CAS  PubMed  Google Scholar 

  49. Mrácek T, Pecinová A, Vrbacký M, Drahota Z, Houstek J. High efficiency of ROS production by glycerophosphate dehydrogenase in mammalian mitochondria. Arch Biochem Biophys 2009; 481(1): 30–36

    PubMed  Google Scholar 

  50. Boveris A, Oshino N, Chance B. The cellular production of hydrogen peroxide. Biochem J 1972; 128(3): 617–630

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Gardner PR, Fridovich I. Inactivation-reactivation of aconitase in Escherichia coli. a sensitive measure of superoxide radical. J Biol Chem 1992; 267(13): 8757–8763

    CAS  PubMed  Google Scholar 

  52. Rivera J, Sobey CG, Walduck AK, Drummond GR. Nox isoforms in vascular pathophysiology: insights from transgenic and knockout mouse models. Redox Rep 2010; 15(2): 50–63

    CAS  PubMed  Google Scholar 

  53. Kayama Y, Raaz U, Jagger A, Adam M, Schellinger IN, Sakamoto M, Suzuki H, Toyama K, Spin JM, Tsao PS. Diabetic cardiovascular disease induced by oxidative stress. Int J Mol Sci 2015; 16(10): 25234–25263

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Kietzmann T, Petry A, Shvetsova A, Gerhold JM, Görlach A. The epigenetic landscape related to reactive oxygen species formation in the cardiovascular system. Br J Pharmacol 2017; 174(12): 1533–1554

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Butler R, Morris AD, Belch JJ, Hill A, Struthers AD. Allopurinol normalizes endothelial dysfunction in type 2 diabetics with mild hypertension. Hypertension 2000; 35(3): 746–751

    CAS  PubMed  Google Scholar 

  56. Brandes RP, Weissmann N, Schröder K. Redox-mediated signal transduction by cardiovascular Nox NADPH oxidases. J Mol Cell Cardiol 2014; 73: 70–79

    CAS  PubMed  Google Scholar 

  57. Baum C, Johannsen SS, Zeller T, Atzler D, Ojeda FM, Wild PS, Sinning CR, Lackner KJ, Gori T, Schwedhelm E, Böger RH, Blankenberg S, Münzel T, Schnabel RB; Gutenberg Health Study investigators. ADMA and arginine derivatives in relation to noninvasive vascular function in the general population. Atherosclerosis 2016; 244: 149–156

    Google Scholar 

  58. Drummond GR, Selemidis S, Griendling KK, Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov 2011; 10(6): 453–471

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000; 86(5): 494–501

    CAS  PubMed  Google Scholar 

  60. Gray SP, Di Marco E, Okabe J, Szyndralewiez C, Heitz F, Montezano AC, de Haan JB, Koulis C, El-Osta A, Andrews KL, Chin-Dusting JP, Touyz RM, Wingler K, Cooper ME, Schmidt HH, Jandeleit-Dahm KA. NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 2013; 127(18): 1888–1902

    CAS  PubMed  Google Scholar 

  61. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995; 377(6546): 239- 242

    Google Scholar 

  62. Tejero J, Shiva S, Gladwin MT. Sources of vascular nitric oxide and reactive oxygen species and their regulation. Physiol Rev 2019; 99(1): 311–379

    CAS  PubMed  Google Scholar 

  63. Engineer A, Saiyin T, Greco ER, Feng Q. Say NO to ROS: their roles in embryonic heart development and pathogenesis of congenital heart defects in maternal diabetes. Antioxidants 2019; 8(10): E436

    Google Scholar 

  64. Rozoy E, Simard S, Liu Y, Kitts D, Lessard J, Bazinet L. The use of cyclic voltammetry to study the oxidation of l-5-methyltetrahydrofolate and its preservation by ascorbic acid. Food Chem 2012; 132(3): 1429–1435

    CAS  PubMed  Google Scholar 

  65. Bazinet L, Doyen A. Antioxidants, mechanisms, and recovery by membrane processes. Crit Rev Food Sci Nutr 2017; 57(4): 677–700

    CAS  PubMed  Google Scholar 

  66. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003; 52(1): 102–110

    CAS  PubMed  Google Scholar 

  67. Marrazzo G, Barbagallo I, Galvano F, Malaguarnera M, Gazzolo D, Frigiola A, D'Orazio N, Li Volti G. Role of dietary and endogenous antioxidants in diabetes. Crit Rev Food Sci Nutr 2014; 54(12): 1599–1616

    CAS  PubMed  Google Scholar 

  68. Banerjee M, Vats P. Reactive metabolites and antioxidant gene polymorphisms in type 2 diabetes mellitus. Redox Biol 2014; 2: 170–177

    CAS  PubMed  Google Scholar 

  69. Lykkesfeldt J, Michels AJ, Frei B. Vitamin C. Adv Nutr 2014; 5(1): 16–18

    PubMed  PubMed Central  Google Scholar 

  70. López-Burillo S, Tan DX, Mayo JC, Sainz RM, Manchester LC, Reiter RJ. Melatonin, xanthurenic acid, resveratrol, EGCG, vitamin C and a-lipoic acid differentially reduce oxidative DNA damage induced by Fenton reagents: a study of their individual and synergistic actions. J Pineal Res 2003; 34(4): 269–277

    PubMed  Google Scholar 

  71. Jiang Q. Natural forms of vitamin E: metabolism, antioxidant, and anti-inflammatory activities and their role in disease prevention and therapy. Free Radic Biol Med 2014; 72: 76–90

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Farhangi MA, Mesgari-Abbasi M, Hajiluian G, Nameni G, Shahabi P. Adipose tissue inflammation and oxidative stress: the ameliorative effects of vitamin D. Inflammation 2017; 40(5): 1688–1697

    CAS  PubMed  Google Scholar 

  73. Gerber PA, Rutter GA. The role of oxidative stress and hypoxia in pancreatic β-cell dysfunction in diabetes mellitus. Antioxid Redox Signal 2017; 26(10): 501–518

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Drews G, Krippeit-Drews P, Düfer M. Oxidative stress and β-cell dysfunction. Pflugers Arch 2010; 460(4): 703–718

    CAS  PubMed  Google Scholar 

  75. Maechler P, Jornot L, Wollheim CB. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic β cells. J Biol Chem 1999; 274(39): 27905–27913

    CAS  PubMed  Google Scholar 

  76. Robertson RP, Harmon J, Tran PO, Poitout V. β-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 2004; 53(Suppl 1): S119–S124

    CAS  PubMed  Google Scholar 

  77. Lameloise N, Muzzin P, Prentki M, Assimacopoulos-Jeannet F. Uncoupling protein 2: a possible link between fatty acid excess and impaired glucose-induced insulin secretion? Diabetes 2001; 50(4): 803–809

    CAS  PubMed  Google Scholar 

  78. Kaneto H, Xu G, Fujii N, Kim S, Bonner-Weir S, Weir GC. Involvement of c-Jun N-terminal kinase in oxidative stressmediated suppression of insulin gene expression. J Biol Chem 2002; 277(33): 30010–30018

    CAS  PubMed  Google Scholar 

  79. Kawamori D, Kajimoto Y, Kaneto H, Umayahara Y, Fujitani Y, Miyatsuka T, Watada H, Leibiger IB, Yamasaki Y, Hori M. Oxidative stress induces nucleo-cytoplasmic translocation of pancreatic transcription factor PDX-1 through activation of c-Jun NH(2)-terminal kinase. Diabetes 2003; 52(12): 2896–2904

    CAS  PubMed  Google Scholar 

  80. Kawamori D, Kaneto H, Nakatani Y, Matsuoka TA, Matsuhisa M, Hori M, Yamasaki Y. The forkhead transcription factor Foxo1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J Biol Chem 2006; 281(2): 1091–1098

    CAS  PubMed  Google Scholar 

  81. Matsuoka TA, Artner I, Henderson E, Means A, Sander M, Stein R. The MafA transcription factor appears to be responsible for tissue-specific expression of insulin. Proc Natl Acad Sci USA 2004; 101(9): 2930–2933

    CAS  PubMed  Google Scholar 

  82. El Khattabi I, Sharma A. Preventing p38 MAPK-mediated MafA degradation ameliorates β-cell dysfunction under oxidative stress. Mol Endocrinol 2013; 27(7): 1078–1090

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Kondo T, El Khattabi I, Nishimura W, Laybutt DR, Geraldes P, Shah S, King G, Bonner-Weir S, Weir G, Sharma A. p38 MAPK is a major regulator of MafA protein stability under oxidative stress. Mol Endocrinol 2009; 23(8): 1281–1290

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Gurzov EN, Eizirik DL. Bcl-2 proteins in diabetes: mitochondrial pathways of β-cell death and dysfunction. Trends Cell Biol 2011; 21(7): 424–431

    CAS  PubMed  Google Scholar 

  85. Heimberg H, Heremans Y, Jobin C, Leemans R, Cardozo AK, Darville M, Eizirik DL. Inhibition of cytokine-induced NF-?B activation by adenovirus-mediated expression of a NF-?B superrepressor prevents β-cell apoptosis. Diabetes 2001; 50(10): 2219–2224

    CAS  PubMed  Google Scholar 

  86. Henriksen EJ, Diamond-Stanic MK, Marchionne EM. Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic Biol Med 2011; 51(5): 993–999

    CAS  PubMed  Google Scholar 

  87. Mahadev K, Motoshima H, Wu X, Ruddy JM, Arnold RS, Cheng G, Lambeth JD, Goldstein BJ. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol 2004; 24(5): 1844–1854

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Archuleta TL, Lemieux AM, Saengsirisuwan V, Teachey MK, Lindborg KA, Kim JS, Henriksen EJ. Oxidant stress-induced loss of IRS-1 and IRS-2 proteins in rat skeletal muscle: role of p38 MAPK. Free Radic Biol Med 2009; 47(10): 1486–1493

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Stuart CA, Howell ME, Cartwright BM, McCurry MP, Lee ML, Ramsey MW, Stone MH. Insulin resistance and muscle insulin receptor substrate-1 serine hyperphosphorylation. Physiol Rep 2014; 2(12): e12236

    PubMed  PubMed Central  Google Scholar 

  90. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spiegelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-a- and obesity-induced insulin resistance. Science 1996; 271(5249): 665–668

    CAS  PubMed  Google Scholar 

  91. Hirosumi J, Tuncman G, Chang L, Görgün CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 2002; 420(6913): 333–336

    CAS  PubMed  Google Scholar 

  92. Yuan M, Konstantopoulos N, Lee J, Hansen L, Li ZW, Karin M, Shoelson SE. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of IKKβ. Science 2001; 293(5535): 1673–1677

    CAS  PubMed  Google Scholar 

  93. Diamond-Stanic MK, Henriksen EJ. Direct inhibition by angiotensin II of insulin-dependent glucose transport activity in mammalian skeletal muscle involves a ROS-dependent mechanism. Arch Physiol Biochem 2010; 116(2): 88–95

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Hurrle S, Hsu WH. The etiology of oxidative stress in insulin resistance. Biomed J 2017; 40(5): 257–262

    PubMed  PubMed Central  Google Scholar 

  95. Rurali E, Noris M, Chianca A, Donadelli R, Banterla F, Galbusera M, Gherardi G, Gastoldi S, Parvanova A, Iliev I, Bossi A, Haefliger C, Trevisan R, Remuzzi G, Ruggenenti P; BENEDICT Study Group. ADAMTS13 predicts renal and cardiovascular events in type 2 diabetic patients and response to therapy. Diabetes 2013; 62(10): 3599–3609

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Kaiser N, Sasson S, Feener EP, Boukobza-Vardi N, Higashi S, Moller DE, Davidheiser S, Przybylski RJ, King GL. Differential regulation of glucose transport and transporters by glucose in vascular endothelial and smooth muscle cells. Diabetes 1993; 42(1): 80–89

    CAS  PubMed  Google Scholar 

  97. Nascimento NR, Lessa LM, Kerntopf MR, Sousa CM, Alves RS, Queiroz MG, Price J, Heimark DB, Larner J, Du X, Brownlee M, Gow A, Davis C, Fonteles MC. Inositols prevent and reverse endothelial dysfunction in diabetic rat and rabbit vasculature metabolically and by scavenging superoxide. Proc Natl Acad Sci USA 2006; 103(1): 218–223

    CAS  PubMed  Google Scholar 

  98. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010; 107(9): 1058–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Wautier JL, Schmidt AM. Protein glycation: a firm link to endothelial cell dysfunction. Circ Res 2004; 95(3): 233–238

    CAS  PubMed  Google Scholar 

  100. White PJ, Arita M, Taguchi R, Kang JX, Marette A. Transgenic restoration of long-chain n-3 fatty acids in insulin target tissues improves resolution capacity and alleviates obesity-linked inflammation and insulin resistance in high-fat-fed mice. Diabetes 2010; 59(12): 3066–3073

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Giannini C, Mohn A, Chiarelli F, Kelnar CJ. Macrovascular angiopathy in children and adolescents with type 1 diabetes. Diabetes Metab Res Rev 2011; 27(5): 436–460

    PubMed  Google Scholar 

  102. Gimbrone MA Jr, García-Cardeña G. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ Res 2016; 118(4): 620–636

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Engerman RL, Kern TS, Larson ME. Nerve conduction and aldose reductase inhibition during 5 years of diabetes or galactosaemia in dogs. Diabetologia 1994; 37(2): 141–144

    CAS  PubMed  Google Scholar 

  104. Geraldes P, King GL. Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res 2010; 106(8): 1319–1331

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Isakov N. Protein kinase C (PKC) isoforms in cancer, tumor promotion and tumor suppression. Semin Cancer Biol 2018; 48: 36–52

    CAS  PubMed  Google Scholar 

  106. Land M, Rubin CS. A calcium- and diacylglycerol-stimulated protein kinase C (PKC), Caenorhabditis elegans PKC-2, links thermal signals to learned behavior by acting in sensory neurons and intestinal cells. Mol Cell Biol 2017; 37(19): e00192–17

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001; 414(6865): 813–820

    CAS  PubMed  Google Scholar 

  108. Brinkmann C, Schwinger RH, Brixius K. Physical activity and endothelial dysfunction in type 2 diabetic patients: the role of nitric oxide and oxidative stress. Wien Med Wochenschr 2011; 161(11-12): 305–314 (in German)

    PubMed  Google Scholar 

  109. Kong L, Shen X, Lin L, Leitges M, Rosario R, Zou YS, Yan SF. PKCβ promotes vascular inflammation and acceleration of atherosclerosis in diabetic ApoE null mice. Arterioscler Thromb Vasc Biol 2013; 33(8): 1779–1787

    CAS  PubMed  Google Scholar 

  110. Pieper GM, Riaz-ul-Haq. Activation of nuclear factor-?B in cultured endothelial cells by increased glucose concentration: prevention by calphostin C. J Cardiovasc Pharmacol 1997; 30(4): 528–532

    CAS  PubMed  Google Scholar 

  111. Ganz MB, Seftel A. Glucose-induced changes in protein kinase C and nitric oxide are prevented by vitamin E. Am J Physiol Endocrinol Metab 2000; 278(1): E146–E152

    CAS  PubMed  Google Scholar 

  112. Kuboki K, Jiang ZY, Takahara N, Ha SW, Igarashi M, Yamauchi T, Feener EP, Herbert TP, Rhodes CJ, King GL. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: a specific vascular action of insulin. Circulation 2000; 101(6): 676–681

    CAS  PubMed  Google Scholar 

  113. Federici M, Menghini R, Mauriello A, Hribal ML, Ferrelli F, Lauro D, Sbraccia P, Spagnoli LG, Sesti G, Lauro R. Insulin-dependent activation of endothelial nitric oxide synthase is impaired by Olinked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation 2002; 106(4): 466–472

    CAS  PubMed  Google Scholar 

  114. Martínez-Ruiz A, Cadenas S, Lamas S. Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med 2011; 51(1): 17–29

    PubMed  Google Scholar 

  115. Wang K, Zhang T, Dong Q, Nice EC, Huang C, Wei Y. Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis 2013; 4(3): e537

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24(5): 981–990

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Thamsen M, Jakob U. The redoxome: proteomic analysis of cellular redox networks. Curr Opin Chem Biol 2011; 15(1): 113–119

    CAS  PubMed  Google Scholar 

  118. Reddie KG, Carroll KS. Expanding the functional diversity of proteins through cysteine oxidation. Curr Opin Chem Biol 2008; 12(6): 746–754

    CAS  PubMed  Google Scholar 

  119. May MJ, Ghosh S. Signal transduction through NF-?B. Immunol Today 1998; 19(2): 80–88

    CAS  PubMed  Google Scholar 

  120. Korn SH, Wouters EF, Vos N, Janssen-Heininger YM. Cytokineinduced activation of nuclear factor-?B is inhibited by hydrogen peroxide through oxidative inactivation of I?B kinase. J Biol Chem 2001; 276(38): 35693–35700

    CAS  PubMed  Google Scholar 

  121. Jaspers I, Zhang W, Fraser A, Samet JM, Reed W. Hydrogen peroxide has opposing effects on IKK activity and I?Ba breakdown in airway epithelial cells. Am J Respir Cell Mol Biol 2001; 24(6):769–777

    CAS  PubMed  Google Scholar 

  122. Kapahi P, Takahashi T, Natoli G, Adams SR, Chen Y, Tsien RY, Karin M. Inhibition of NF-?B activation by arsenite through reaction with a critical cysteine in the activation loop of I?B kinase. J Biol Chem 2000; 275(46): 36062–36066

    CAS  PubMed  Google Scholar 

  123. Thallas-Bonke V, Jha JC, Gray SP, Barit D, Haller H, Schmidt HH, Coughlan MT, Cooper ME, Forbes JM, Jandeleit-Dahm KA. Nox- 4 deletion reduces oxidative stress and injury by PKC-a-associated mechanisms in diabetic nephropathy. Physiol Rep 2014; 2(11): e12192

    PubMed  PubMed Central  Google Scholar 

  124. Gopalakrishna R, Jaken S. Protein kinase C signaling and oxidative stress. Free Radic Biol Med 2000; 28(9): 1349–1361

    CAS  PubMed  Google Scholar 

  125. Stäuble B, Boscoboinik D, Tasinato A, Azzi A. Modulation of activator protein-1 (AP-1) transcription factor and protein kinase C by hydrogen peroxide and D-a-tocopherol in vascular smooth muscle cells. Eur J Biochem 1994; 226(2): 393–402

    PubMed  Google Scholar 

  126. Cuadrado A, Rojo AI, Wells G, Hayes JD, Cousin SP, Rumsey WL, Attucks OC, Franklin S, Levonen AL, Kensler TW, Dinkova- Kostova AT. Therapeutic targeting of the NRF2 and KEAP1 partnership in chronic diseases. Nat Rev Drug Discov 2019; 18(4): 295–317

    CAS  PubMed  Google Scholar 

  127. McMahon M, Lamont DJ, Beattie KA, Hayes JD. Keap1 perceives stress via three sensors for the endogenous signaling molecules nitric oxide, zinc, and alkenals. Proc Natl Acad Sci USA 2010; 107(44): 18838–18843

    CAS  PubMed  Google Scholar 

  128. Takaya K, Suzuki T, Motohashi H, Onodera K, Satomi S, Kensler TW, Yamamoto M. Validation of the multiple sensor mechanism of the Keap1-Nrf2 system. Free Radic Biol Med 2012; 53(4): 817–827

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Saito R, Suzuki T, Hiramoto K, Asami S, Naganuma E, Suda H, Iso T, Yamamoto H, Morita M, Baird L, Furusawa Y, Negishi T, Ichinose M, Yamamoto M. Characterizations of three major cysteine sensors of Keap1 in stress response. Mol Cell Biol 2015; 36(2): 271–284

    PubMed  Google Scholar 

  130. Uruno A, Furusawa Y, Yagishita Y, Fukutomi T, Muramatsu H, Negishi T, Sugawara A, Kensler TW, Yamamoto M. The Keap1- Nrf2 system prevents onset of diabetes mellitus. Mol Cell Biol 2013; 33(15): 2996–3010

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Zheng H, Whitman SA, Wu W, Wondrak GT, Wong PK, Fang D, Zhang DD. Therapeutic potential of Nrf2 activators in streptozotocin- induced diabetic nephropathy. Diabetes 2011; 60(11): 3055–3066

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Chuengsamarn S, Rattanamongkolgul S, Luechapudiporn R, Phisalaphong C, Jirawatnotai S. Curcumin extract for prevention of type 2 diabetes. Diabetes Care 2012; 35(11): 2121–2127

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Golbidi S, Ebadi SA, Laher I. Antioxidants in the treatment of diabetes. Curr Diabetes Rev 2011; 7(2): 106–125

    CAS  PubMed  Google Scholar 

  134. Belch J, MacCuish A, Campbell I, Cobbe S, Taylor R, Prescott R, Lee R, Bancroft J, MacEwan S, Shepherd J, Macfarlane P, Morris A, Jung R, Kelly C, Connacher A, Peden N, Jamieson A, Matthews D, Leese G, McKnight J, O'Brien I, Semple C, Petrie J, Gordon D, Pringle S, MacWalter R; Prevention of Progression of Arterial Disease and Diabetes Study Group; Diabetes Registry Group; Royal College of Physicians Edinburgh. The prevention of progression of arterial disease and diabetes (POPADAD) trial: factorial randomised placebo controlled trial of aspirin and antioxidants in patients with diabetes and asymptomatic peripheral arterial disease. BMJ 2008; 337: a1840

    PubMed  PubMed Central  Google Scholar 

  135. Bhagavan HN, Chopra RK. Coenzyme Q10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic Res 2006; 40(5): 445–453

    CAS  PubMed  Google Scholar 

  136. Armstrong JS. Mitochondrial medicine: pharmacological targeting of mitochondria in disease. Br J Pharmacol 2007; 151(8): 1154–1165

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Umpierre D, Ribeiro PA, Kramer CK, Leitão CB, Zucatti AT, Azevedo MJ, Gross JL, Ribeiro JP, Schaan BD. Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: a systematic review and metaanalysis. JAMA 2011; 305(17): 1790–1799

    CAS  PubMed  Google Scholar 

  138. Church TS, Blair SN, Cocreham S, Johannsen N, Johnson W, Kramer K, Mikus CR, Myers V, Nauta M, Rodarte RQ, Sparks L, Thompson A, Earnest CP. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA 2010; 304(20): 2253–2262

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Sigal RJ, Kenny GP, Boulé NG,Wells GA, Prud'homme D, Fortier M, Reid RD, Tulloch H, Coyle D, Phillips P, Jennings A, Jaffey J. Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial. Ann Intern Med 2007; 147(6): 357–369

    PubMed  Google Scholar 

  140. Moe B, Eilertsen E, Nilsen TI. The combined effect of leisure-time physical activity and diabetes on cardiovascular mortality: the Nord-Trondelag Health (HUNT) cohort study, Norway. Diabetes Care 2013; 36(3): 690–695

    PubMed  PubMed Central  Google Scholar 

  141. Yamashita N, Hoshida S, Otsu K, Asahi M, Kuzuya T, Hori M. Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation. J Exp Med 1999; 189(11): 1699–1706

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Haffner SM; American Diabetes Association. Management of dyslipidemia in adults with diabetes. Diabetes Care 2003; 26(Suppl 1): S83–S86

    PubMed  Google Scholar 

  143. Lee S, Yang SC, Heffernan MJ, Taylor WR, Murthy N. Polyketal microparticles: a new delivery vehicle for superoxide dismutase. Bioconjug Chem 2007; 18(1): 4–7

    CAS  PubMed  Google Scholar 

  144. Grama CN, Suryanarayana P, Patil MA, Raghu G, Balakrishna N, Kumar MN, Reddy GB. Efficacy of biodegradable curcumin nanoparticles in delaying cataract in diabetic rat model. PLoS One 2013; 8(10): e78217

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Takahashi M, Uechi S, Takara K, Asikin Y,Wada K. Evaluation of an oral carrier system in rats: bioavailability and antioxidant properties of liposome-encapsulated curcumin. J Agric Food Chem 2009; 57(19): 9141–9146

    CAS  PubMed  Google Scholar 

  146. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 2010; 107(1): 106–116

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Graham D, Huynh NN, Hamilton CA, Beattie E, Smith RA, Cochemé HM, Murphy MP, Dominiczak AF. Mitochondriatargeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension 2009; 54(2): 322–328

    CAS  PubMed  Google Scholar 

  148. Jiao W, Ji J, Li F, Guo J, Zheng Y, Li S, Xu W. Activation of the NotchNox4 reactive oxygen species signaling pathway induces cell death in high glucosetreated human retinal endothelial cells. Mol Med Rep 2019; 19(1): 667–677

    CAS  PubMed  Google Scholar 

  149. Peng JJ, Xiong SQ, Ding LX, Peng J, Xia XB. Diabetic retinopathy: focus on NADPH oxidase and its potential as therapeutic target. Eur J Pharmacol 2019; 853: 381–387

    CAS  PubMed  Google Scholar 

  150. Pergola PE, Raskin P, Toto RD, Meyer CJ, Huff JW, Grossman EB, Krauth M, Ruiz S, Audhya P, Christ-Schmidt H, Wittes J, Warnock DG; BEAM Study Investigators. Bardoxolone methyl and kidney function in CKD with type 2 diabetes. N Engl J Med 2011; 365(4): 327–336

    CAS  PubMed  Google Scholar 

  151. Zhong Q, Mishra M, Kowluru RA. Transcription factor Nrf2- mediated antioxidant defense system in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci 2013; 54(6): 3941–3948

    CAS  PubMed  PubMed Central  Google Scholar 

  152. Gopalakrishna R, Jaken S. Protein kinase C signaling and oxidative stress. Free Radic Biol Med 2000; 28(9): 1349–1361

    CAS  PubMed  Google Scholar 

  153. Gopalakrishna R, Gundimeda U. Protein kinase C as a molecular target for cancer prevention by selenocompounds. Nutr Cancer 2001; 40(1): 55–63

    CAS  PubMed  Google Scholar 

  154. Gopalakrishna R, Chen ZH, Gundimeda U. Selenocompounds induce a redox modulation of protein kinase C in the cell, compartmentally independent from cytosolic glutathione: its role in inhibition of tumor promotion. Arch Biochem Biophys 1997; 348(1): 37–48

    CAS  PubMed  Google Scholar 

  155. Alam F, Islam MA, Gan SH, Mohamed M, Sasongko TH. DNA methylation: an epigenetic insight into type 2 diabetes mellitus. Curr Pharm Des 2016; 22(28): 4398–4419

    CAS  PubMed  Google Scholar 

  156. Lei XW, Li Q, Zhang JZ, Zhang YM, Liu Y, Yang KH. The protective roles of folic acid in preventing diabetic retinopathy are potentially associated with suppressions on angiogenesis, inflammation, and oxidative stress. Ophthalmic Res 2019; 62(2): 80–92

    CAS  PubMed  Google Scholar 

  157. Beard KM, Shangari N, Wu B, O'Brien PJ. Metabolism, not autoxidation, plays a role in a-oxoaldehyde- and reducing sugarinduced erythrocyte GSH depletion: relevance for diabetes mellitus. Mol Cell Biochem 2003; 252(1-2): 331–338

    CAS  PubMed  Google Scholar 

  158. Shukla S, Dubey KK. CoQ10 a super-vitamin: review on application and biosynthesis. 3 Biotech 2018; 8(5):249

    PubMed  PubMed Central  Google Scholar 

  159. Lasram MM, Dhouib IB, Annabi A, El Fazaa S, Gharbi N. A review on the possible molecular mechanism of action of Nacetylcysteine against insulin resistance and type-2 diabetes development. Clin Biochem 2015; 48(16-17): 1200–1208

    CAS  PubMed  Google Scholar 

  160. Kamenova P. Improvement of insulin sensitivity in patients with type 2 diabetes mellitus after oral administration of a-lipoic acid. Hormones (Athens) 2006; 5(4): 251–258

    Google Scholar 

  161. Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 2006; 86(1): 205–243

    CAS  PubMed  Google Scholar 

  162. Tauskela JS. MitoQ-a mitochondria-targeted antioxidant. IDrugs 2007; 10(6): 399–412

    CAS  PubMed  Google Scholar 

  163. Wilcox CS. Effects of tempol and redox-cycling nitroxides in models of oxidative stress. Pharmacol Ther 2010; 126(2): 119–145

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (Nos. 81770580, 81430071, 81821002, and 81790251) and Sichuan Science and Technology Program (No. 2018RZ0133).

Author information

Authors and Affiliations

  1. Department of Pharmacology, West China School of Basic Medical Sciences & Forensic Medicine, Sichuan University, Chengdu, 610041, China

    Pengju Zhang, Tao Li, Xingyun Wu, Canhua Huang & Yuanyuan Zhang

  2. Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, Australia

    Edouard C. Nice

Authors
  1. Pengju Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xingyun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edouard C. Nice
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Canhua Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuanyuan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Canhua Huang or Yuanyuan Zhang.

Ethics declarations

Pengju Zhang, Tao Li, Xingyun Wu, Edouard C. Nice, Canhua Huang, and Yuanyuan Zhang declare no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, P., Li, T., Wu, X. et al. Oxidative stress and diabetes: antioxidative strategies. Front. Med. 14, 583–600 (2020). https://doi.org/10.1007/s11684-019-0729-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-019-0729-1

Keywords

Search

Navigation