Abstract
The review presents modern views about the role of oxidative stress reactions in the pathogenesis of types 1 and 2 diabetes mellitus and their complications based on the analysis of experimental and clinical studies. The sources of increased ROS generation in diabetes are specified, including the main pathways of altered glucose metabolism, oxidative damage to pancreatic β-cells, and endothelial dysfunction. The relationship between oxidative stress, carbonyl stress, and inflammation is described. The significance of oxidative stress reactions associated with hyperglycemia is considered in the context of the “metabolic memory” phenomenon. The results of our studies demonstrated significant ethnic and age-related variability of the LPO—antioxidant defense system parameters in patients with diabetes mellitus, which should be considered during complex therapy of the disease. Numerous studies of the effectiveness of antioxidants in diabetes mellitus of both types convincingly proved that antioxidants should be a part of the therapeutic process. Modern therapeutic strategies in the treatment of diabetes mellitus are aimed at developing new methods of personalized antioxidant therapy, including ROS sources targeting combined with new ways of antioxidant delivery.
Key words: diabetes mellitus, oxidative stress, antioxidants, experiment, patients
Footnotes
Translated from Byulleten’ Eksperimental’noi Biologii i Meditsiny, Vol. 171, No. 2, pp. 136-149, February, 2021
References
- 1.Algorithms of Specialized Medical Care for Patients with Diabetes Mellitus. Dedov II, Shestakova MV, Maioriv AYu, eds. Moscow, 2019. Russian.
- 2.Barysheva EV. Change parameters prooxidant-antioxidant system while reducing the concentration of deuterium in laboratory animals with alloxan diabetes. Fundament. Issled. 2015;(1-3):457-461. Russian.
- 3.Belkina LM, Smirnova EA, Terekhina OL, Kruglov SV, Boichuk ES. Role of nitric oxide in the pathogenesis of alloxan diabetes. Bull. Exp. Biol. Med. 2013;154(5):602–605. doi: 10.1007/s10517-013-2009-4. [DOI] [PubMed] [Google Scholar]
- 4.Blagonravov ML, Sklifasovskaya AP, Korshunova AY, Azova MM, Kurlaeva AO. Heat Shock Protein HSP60 in Left Ventricular Cardiomyocytes of Hypertensive Rats with and without Insulin-Dependent Diabetes Mellitus. Bull. Exp. Biol. Med. 2021;170(1):10–14. doi: 10.1007/s10517-020-04994-4. [DOI] [PubMed] [Google Scholar]
- 5.Volchegorskii IA, Rassokhina LM, Miroshnichenko IY. Dynamics of lipid peroxidation-antioxidant defense system during alloxan diabetes in rats. Bull. Exp. Biol. Med. 2013;155(1):26–29. doi: 10.1007/s10517-013-2071-y. [DOI] [PubMed] [Google Scholar]
- 6.Dzugkoev SG, Kaloeva MB, Dzugkoeva FS. Effect of combination therapy with coenzyme Q10 on functional and metabolic parameters in patients with type 1 diabetes mellitus. Bull. Exp. Biol. Med. 2012;152(3):364–366. doi: 10.1007/s10517-012-1529-7. [DOI] [PubMed] [Google Scholar]
- 7.Dzugkoev SG, Metel’skaya VA, Dzugkoeva FS. Effects of endogenous regulators of endothelial NO synthase on nitric oxide homeostasis and blood serum lipoproteins during experimental diabetes mellitus. Bull. Exp. Biol. Med. 2014;156(2):205–208. doi: 10.1007/s10517-013-2311-1. [DOI] [PubMed] [Google Scholar]
- 8.Kolesnikova LI, Darenskaya MA, Kolesnikov SI. Free radical oxidation: a pathophysiologist’s view. Byull. Sib. Med. 2017;16(4):16–29. doi: 10.20538/1682-0363-2017-4-16-29. [DOI] [Google Scholar]
- 9.Kukes VG, Parfenova OK, Romanov BK, Prokofiev AB, Parfenova EV, Sidorov NG, Gazdanova AA, Pavlova LI, Zozina VI, Andreev AD, Aleksandrova TV, Chernova SV, Ramenskaya GV. The mechanism of action of ethoxidol on oxidative stress indices in heart failure and hypotension. Sovremen. Tekhnol. Med. 2020;12(2):67-73. doi: 10.17691/stm2020.12.2.08 [DOI] [PMC free article] [PubMed]
- 10.Lankin VZ, Tikhaze AK. Free radical processes play an important role in the etiology and pathogenesis of atherosclerosis and diabetes. Kardiologiya. 2016;56(12):97–105. [PubMed] [Google Scholar]
- 11.Zhernakova YuV, Zheleznova EA, Chazova IE, Oshchepkova EV, Dolgusheva YuA, Yarovaya EB, Blinova NV, Orlovsky AA, Konosova ID, Shalnova SA, Rotar’ OP, Konradi AO, Shlyakhto EV, Boytsov SA. The prevalence of abdominal obesity and the association with socioeconomic status in Regions of the Russian Federation, the results of the epidemiological study–ESSE-RF. Ter. Arkh. 2018;90(10):46-50. doi: 10.26442/terarkh201890104-50 [DOI] [PubMed]
- 12.Mikaelian NP, Gurina AE, Terent’ev AA. Dysfunction of membrane-receptor system of blood cells and kidney tissue in experimental diabetes mellitus. Bull. Exp. Biol. Med. 2013;154(5):610–613. doi: 10.1007/s10517-013-2011-x. [DOI] [PubMed] [Google Scholar]
- 13.Mikaelyan NP, Dvornikov AS, Mikaelyan AA, Smirnova NV. Association between Disturbances in Polyunsaturated Fatty Acid Metabolism and Development of Oxidative Stress during Experimental Diabetes Mellitus. Bull. Exp. Biol. Med. 2019;167(3):343–346. doi: 10.1007/s10517-019-04523-y. [DOI] [PubMed] [Google Scholar]
- 14.Mozheyko LA. Experimental models for studying diabetes mellitus part 1. Alloxan diabetes. Zh. Grodnensk. Gos. Med. Univer. 2013;3:26–29. [Google Scholar]
- 15.Proskurnina EV, Polimova AM, Sozarukova MM, Prudnikova MA, Ametov AS, Vladimirov YA. Kinetic Chemiluminescence as a Method for Oxidative Stress Evaluation in Examinations of Patients with Type 2 Diabetes Mellitus. Bull. Exp. Biol. Med. 2016;161(1):131–133. doi: 10.1007/s10517-016-3362-x. [DOI] [PubMed] [Google Scholar]
- 16.Samotrueva MA, Sergalieva MU. Diabetes mellitus: features of experimental modelling. Astrakhan. Med. Zh. 2019;14(3):45–57. [Google Scholar]
- 17.Skliarova EI, Popova TN, Shulgin KK. Effects of N-[Imino(1-Piperidinyl)Methyl] Guanidine on the Intensity of Free Radical Processes, Aconitase Activity, and Citrate Level in the Tissues of Rats with Experimental Type 2 Diabetes Mellitus. Bull. Exp. Biol. Med. 2016;161(2):261–265. doi: 10.1007/s10517-016-3391-5. [DOI] [PubMed] [Google Scholar]
- 18.Smirnov LD, Inchina VI, Kostin JV, Kokoreva EV, Bogoljubova ZV. Possible pharmacological correction of metabolic impairments experimental diabetes mellitus by antioxidant. Biomed. Khimiya. 2004;50(5):502–508. [PubMed] [Google Scholar]
- 19.Tsakanova GV, Ayvazyan VA, Boyajyan AS, Arakelova EA, Grigoryan GS, Guevorkyan AA, Mamikonyan AA. A comparative study of antioxidant system and intensity of lipid peroxidation in type 2 diabetes mellitus and ischemic stroke aggravated and not aggravated by type 2 diabetes mellitus. Bull. Exp. Biol. Med. 2011;151(5):564–566. doi: 10.1007/s10517-011-1383-z. [DOI] [PubMed] [Google Scholar]
- 20.Chernikov AA, Severina AS, Shamhalova MS, Shestakova MV. The role of “metabolic memory” mechanisms in the development and progression of vascular complications of diabetes mellitus. Sakhar. Diabet. 2017;20(2):126–134. [Google Scholar]
- 21.Chistyakova OV, Sukhov IB, Shpakov AO. The role of oxidative stress and antioxidant enzymes in the development of diabetes mellitus. Ross. Fiziol. Zh. 2017;103(9):987-1003.Russian.
- 22.Elbekyan KS, Myraveva AB, Pazhitneva EV. Effect of melatonin on oxidative stress andindicators of the element of balance in experimental diabetes. Fundament. Issled. 2013;(9-1):178-181. Russian.
- 23.Yashanova MI, Shcherbatyuk TG, Nikolaev VYu. Validity of the models of experimental diabetes for oxidative stress studies. Zh. Med.-Biol. Issled. 2019;7(1):66-78. doi: 10.17238/issn2542-1298.2019.7.1.66
- 24.Aju BY, Rajalakshmi R, Mini S. Protective role of Moringa oleifera leaf extract on cardiac antioxidant status and lipid peroxidation in streptozotocin induced diabetic rats. Heliyon. 2019;5(12):e02935. doi: 10.1016/j.heliyon.2019.e02935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Alghazeer R, Alghazir N, Awayn N, Ahtiwesh O, Elgahmasi S. Biomarkers of oxidative stress and antioxidant defense in patients with type 1 diabetes mellitus. Ibnosina J. Med. Biomed. Sci. 2018;10(6):198. doi: 10.4103/ijmbs.ijmbs_59_18. [DOI] [Google Scholar]
- 26.Alghobashy AA, Alkholy UM, Talat MA, Abdalmonem N, Zaki A, Ahmed IA, Mohamed RH. Trace elements and oxidative stress in children with type 1 diabetes mellitus. Diabetes Metab. Syndr. Obes. 2018;11:85–92. doi: 10.2147/DMSO.S157348. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Aouacheri O, Saka S, Krim M, Messaadia A, Maidi I. The investigation of the oxidative stress-related parameters in type 2 diabetes mellitus. Can. J. Diabetes. 2015;39(1):44–49. doi: 10.1016/j.jcjd.2014.03.002. [DOI] [PubMed] [Google Scholar]
- 28.Asadipooya K, Uy EM. Advanced glycation end products (AGEs), receptor for AGEs, diabetes, and bone: review of the literature. J. Endocr. Soc. 2019;3(10):1799–1818. doi: 10.1210/js.2019-00160. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Asmat U, Abad K, Ismail K. Diabetes mellitus and oxidative stress — a concise: review. Saudi Pharm. J. 2016;24(5):547–553. doi: 10.1016/j.jsps.2015.03.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Bensellam M, Laybutt DR, Jonas JC. The molecular mechanisms of pancreatic β-cell glucotoxicity: recent findings and future research directions. Mol. Cell. Endocrinol. 2012;364(1-2):1–27. doi: 10.1016/j.mce.2012.08.003. [DOI] [PubMed] [Google Scholar]
- 31.Bigagli E, Lodovici M. Circulating oxidative stress biomarkers in clinical studies on type 2 diabetes and its complications. Oxidative Med.Cell. Longev. 2019;2019:5953685. doi: 10.1155/2019/5953685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Bulboaca AE, Boarescu PM, Porfire AS, Dogaru G, Barbalata C, Valeanu M, Munteanu C, Râjnoveanu RM, Nicula CA, Stanescu IC. The effect of nano-epigallocatechin-gallate on oxidative stress and matrix metalloproteinases in experimental diabetes mellitus. Antioxidants (Basel). 2020;9(2):172. doi: 10.3390/antiox9020172. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Burgos-Morón E, Abad-Jiménez Z, Marañón AM, Iannantuoni F, Escribano-López I, López-Domènech S, Salom C, Jover A, Mora V, Roldan I, Solá E, Rocha M, Víctor VM. Relationship between oxidative stress, ER stress, and inflammation in type 2 diabetes: the battle continues. J. Clin. Med. 2019;8(9):1385. doi: 10.3390/jcm8091385. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Ceriello A, Testa R, Genovese S. Clinical implications of oxidative stress and potential role of natural antioxidants in diabetic vascular complications. Nutr. Metab. Cardiovasc. Dis. 2016;26(4):285–292. doi: 10.1016/j.numecd.2016.01.006. [DOI] [PubMed] [Google Scholar]
- 35.Chandra K, Singh P, Dwivedi S, Jain SK. Diabetes mellitus and oxidative stress: a co-relative and therapeutic approach. J. Clin. Diagn. Res. 2019;13(5):BE07–BE12. doi: 10.7860/JCDR/2019/40628.12878. [DOI] [Google Scholar]
- 36.Daniels MC, McClain DA, Crook ED. Transcriptional regulation of transforming growth factor β1 by glucose: investigation into the role of the hexosamine biosynthesis pathway. Am. J. Med. Sci. 2020;359(2):79–83. doi: 10.1016/j.amjms.2019.12.013. [DOI] [PubMed] [Google Scholar]
- 37.Darenskaya MA, Grebenkina LA, Semenova NV, Gnusina SV, Kolesnikov SI, Kolesnikova LI. The use of integral indicator of oxidative stress in women with diabetes mellitus. Diabetes Technol. Therapeutics. 2018;20(1):143–144. [Google Scholar]
- 38.Darenskaya MA, Shemyakina NA, Namokonov EV, Semenova NV, Kolesnikov SI, Kolesnikova LI. Glyoxal, metilglyoxal and malonic dialdehyde levels in patients with diabetes mellitus and microangiopathy of the lower extremities in the course of recommended therapy with added N-acetylcysteine. Diabetes Technol. Therapeutics. 2020;22(S1):760. [Google Scholar]
- 39.Dariya B, Nagaraju GP. Advanced glycation end products in diabetes, cancer and phytochemical therapy. Drug Discov. Today. 2020;25(9):1614–1623. doi: 10.1016/j.drudis.2020.07.003. [DOI] [PubMed] [Google Scholar]
- 40.Duvvuri LS, Katiyar S, Kumar A, Khan W. Delivery aspects of antioxidants in diabetes management. Expert Opin. Drug Deliv. 2015;12(5):827–844. doi: 10.1517/17425247.2015.992413. [DOI] [PubMed] [Google Scholar]
- 41.Forrester SJ, Kikuchi DS, Hernandes MS, Xu Q, Griendling KK. Reactive oxygen species in metabolic and inflammatory signaling. Circ. Res. 2018;122(6):877–902. doi: 10.1161/CIRCRESAHA.117.311401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Gawlik K, Naskalski JW, Fedak D, Pawlica-Gosiewska D, Grudzień U, Dumnicka P, Małecki MT, Solnica B. Markers of antioxidant defense in patients with type 2 diabetes. Oxid. Med. Cell. Longev. 2016;2016:2352361. doi: 10.1155/2016/2352361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Gerber PA, Rutter GA. The role of oxidative stress and hypoxia in pancreatic beta-cell dysfunction in diabetes mellitus. Antioxidants Redox Signaling. 2017;26(10):501–518. doi: 10.1089/ars.2016.6755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Ghasemi-Dehnoo M, Amini-Khoei H, Lorigooini Z, Rafieian-Kopaei M. Oxidative stress and antioxidants in diabetes mellitus. Asian Pac. J. Trop. Med. 2020;13(10):431–438. doi: 10.4103/1995-7645.291036. [DOI] [Google Scholar]
- 45.Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ. Res. 2010;107(9):1058–1070. doi: 10.1161/CIRCRESAHA.110.223545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.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. doi: 10.1371/journal.pone.0078217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Gray SP, Jha JC, Kennedy K, van Bommel E, Chew P, Szyndralewiez C, Touyz RM, Schmidt HHHW, Cooper ME. Jandeleit- Dahm KAM. Combined NOX1/4 inhibition with GKT137831 in mice provides dosedependent reno- and atheroprotection even in established micro- and macrovascular disease. Diabetologia. 2017;60(5):927–937. doi: 10.1007/s00125-017-4215-5. [DOI] [PubMed] [Google Scholar]
- 48.Harding JL, Pavkov ME, Magliano DJ, Shaw JE, Gregg EW. Global trends in diabetes complications: a review of current evidence. Diabetologia. 2019;62(1):3–16. doi: 10.1007/s00125-018-4711-2. [DOI] [PubMed] [Google Scholar]
- 49.Holley CT, Duffy CM, Butterick TA, Long EK, Lindsey ME, Cabrera JA, Ward HB, McFalls EO, Kelly RF. Expression of uncoupling protein-2 remains increased within hibernating myocardium despite successful coronary artery bypass grafting at 4 wk post-revascularization. J. Surg. Res. 2015;193(1):15–21. doi: 10.1016/j.jss.2014.08.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Hoseini A, Namazi G, Farrokhian A, Reiner Ž, Aghadavod E, Bahmani F, Asemi Z. The effects of resveratrol on metabolic status in patients with type 2 diabetes mellitus and coronary heart disease. Food Function. 2019;10(9):6042–6051. doi: 10.1039/c9fo01075k. [DOI] [PubMed] [Google Scholar]
- 51.Hussein L, Gaetani S, Mousa SG, D’Evoli L, Hussein N. Dyslipidemia and other risk factors among Egyptian patients with type-2 diabetes mellitus and the impact of dietary intervention with thermally treated tomato juice. Int. J. Clin. Nutr. Diet. 2018;4. 10.15344/2456-8171/2018/128
- 52.Ighodaro OM. Molecular pathways associated with oxidative stress in diabetes mellitus. Biomed. Pharmacother. 2018;108:656–662. doi: 10.1016/j.biopha.2018.09.058. [DOI] [PubMed] [Google Scholar]
- 53.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. doi: 10.3892/mmr.2018.9637. [DOI] [PubMed] [Google Scholar]
- 54.Kang Q, Yang C. Oxidative stress and diabetic retinopathy: molecular mechanisms, pathogenetic role and therapeutic implications. Redox Biol. 2020;37:101799. doi: 10.1016/j.redox.2020.101799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Kanikarla-Marie P, Jain SK. Hyperketonemia (acetoacetate) upregulates NADPH oxidase 4 and elevates oxidative stress, ICAM-1, and monocyte adhesivity in endothelial cells. Cell. Physiol. Biochem. 2015;35(1):364–373. doi: 10.1159/000369702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Kolesnikova LI, Darenskaya MA, Grebenkina LA, Gnusina SV, Kolesnikov SI. Oxidative stress in type 1 diabetes mellitus: ethnic aspects. Free Radicals, Antioxidants and Diseases. Rizwan A, ed. Rijeka, 2018. P. 65-72. doi: 10.5772/intechopen.70075
- 57.Kolesnikova LI, Darenskaya MA, Grebenkina LA, Gnusina SV, Kolesnikov SI. Ethnic aspects of lipid peroxidation process flow in patients with type 1 diabetes mellitus. Diabetes Technol. Therapeutics. 2019;21(Suppl. 1):133. [Google Scholar]
- 58.Kolesnikova LI, Kolesnikov SI, Darenskaya MA, Grebenkina LA, Semenova NV, Osipova EV, Gnusina SV, Bardymova TA. Lipid status and predisposing genes in patients with diabetes mellitus type 1 from various ethnic groups. Bull. Exp. Biol. Med. 2015;160(2):278–280. doi: 10.1007/s10517-015-3149-5. [DOI] [PubMed] [Google Scholar]
- 59.Kolesnikova LI, Shemyakina NA, Namokonov EV, Darenskaya MA, Grebenkina LA, Kolesnikov SI. Some parameters of carbonyl and oxidative stress in patients with type 2 diabetes mellitus and macroangiopathy of the lower extremities. Diabetes Technol. Therapeutics. 2019;21(Suppl. 1):46. [Google Scholar]
- 60.Kolesnikova LI, Vlasov BY, Kolesnikov SI, Darenskaya MA, Grebenkina LA, Semenova NV, Vanteeva OA. Intensity of oxidative stress in Mongoloid and Caucasian patients with type 1 diabetes mellitus. Bull. Exp. Biol. 2016;161(6):767–769. doi: 10.1007/s10517-016-3505-0. [DOI] [PubMed] [Google Scholar]
- 61.Kowluru RA. Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression. Curr. Med. Chem. 2013;20(26):3226–3233. doi: 10.2174/09298673113209990029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Krog S, Ludvigsen TP, Nielsen OL, Kirk RK, Lykkegaard K, Wulff EM, Møller JE, Pedersen HD, Olsen LH. Myocardial changes in diabetic and nondiabetic nonhuman primates. Vet. Pathol. 2020;57(2):332–343. doi: 10.1177/0300985820901332. [DOI] [PubMed] [Google Scholar]
- 63.Langlais P, Yi Z, Finlayson J, Luo M, Mapes R, De Filippis E, Meyer C, Plummer E, Tongchinsub P, Mattern M, Mandarino LJ. Global IRS-1 phosphorylation analysis in insulin resistance. Diabetologia. 2011;54(11):2878–2889. doi: 10.1007/s00125-011-2271-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Lei XG, Zhu JH, Cheng WH, Bao Y, Ho YS, Reddi AR, Holmgren A, Arnér ES. Paradoxical roles of antioxidant enzymes: Basic mechanisms and health implications. Physiol. Rev. 2016;96(1):307–364. doi: 10.1152/physrev.00010.2014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Liu J, Li X, Cai R, Ren Z, Zhang A, Deng F, Chen D. Simultaneous study of anti-ferroptosis and antioxidant mechanisms of butein and (S)-butin. Molecules. 2020;25(3):674. doi: 10.3390/molecules25030674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Lotfy M, Adeghate J, Kalasz H, Singh J, Adeghate E. Chronic complications of diabetes mellitus: a mini review. Curr. Diabetes Rev. 2017;13(1):3–10. doi: 10.2174/1573399812666151016101622. [DOI] [PubMed] [Google Scholar]
- 67.Maleki V, Foroumandi E, Hajizadeh-Sharafabad F, Kheirouri S, Alizadeh M. The effect of resveratrol on advanced glycation end products in diabetes mellitus: a systematic review. Arch. Physiol. Biochem. 2020;3:1–8. doi: 10.1080/13813455.2019.1673434. [DOI] [PubMed] [Google Scholar]
- 68.Mason SA, Della Gatta PA, Snow RJ, Russell AP, Wad- ley GD. Ascorbic acid supplementation improves skeletal muscle oxidative stress and insulin sensitivity in people with type 2 diabetes: Findings of a randomized controlled study. Free Radic. Biol. Med. 2016;93:227-238. doi: 10.1016/j.freeradbiomed.2016.01.006 [DOI] [PubMed]
- 69.Mehta MM, Weinberg SE, Chandel NS. Mitochondrial control of immunity: beyond ATP. Nat. Rev. Immunol. 2017;17(10):608–620. doi: 10.1038/nri.2017.66. [DOI] [PubMed] [Google Scholar]
- 70.Mirończuk-Chodakowska I, Witkowska AM, Zujko ME. Endogenous non-enzymatic antioxidants in the human body. Adv. Med. Sci. 2018;63(1):68–78. doi: 10.1016/j.advms.2017.05.005. [DOI] [PubMed] [Google Scholar]
- 71.Mistry KN, Dabhi BK, Joshi BB. Evaluation of oxidative stress biomarkers and inflammation in pathogenesis of diabetes and diabetic nephropathy. Indian J. Biochem. Biophys. (IJBB). 2020;57(1):45-50.
- 72.Mukhtar MH, El-Emshaty HM, Alamodi HS, Nasif WA. The activity of serum 8-iso-prostaglandin F2α as oxidative stress marker in patients with diabetes mellitus type 2 and associated dyslipidemic hyperglycemia. J. Diabetes Mellitus. 2016;6(4):318–332. doi: 10.4236/jdm.2016.64033. [DOI] [Google Scholar]
- 73.Nasri H, Shirzad H, Baradaran A, Rafieian-Kopaei M. Antioxidant plants and diabetes mellitus. J. Res. Med. Sci. 2015;20(5):491-502. doi: 10.4103/1735-1995.163977 [DOI] [PMC free article] [PubMed]
- 74.Oguntibeju OO. Type 2 diabetes mellitus, oxidative stress and inflammation: examining the links. Int. J. Physiol. Pathophysiol. Pharmacol. 2019;11(3):45–63. [PMC free article] [PubMed] [Google Scholar]
- 75.Oxidative Stress. Eustress and Distress. Sies H, ed. Academic Press, 2020.
- 76.Ozougwu JC. The role of reactive oxygen species and antioxidants in oxidative stress. Int. J. Res. Pharm. Biosci. 2016;3(6):1–8. [Google Scholar]
- 77.Pavithra D, Praveen D, Chowdary PR, Aanandhi MV. A review on role of vitamin E supplementation in type 2 diabetes mellitus. Drug Invent. Today. 2018;10(2):236–240. [Google Scholar]
- 78.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. doi: 10.1016/j.ejphar.2019.04.038. [DOI] [PubMed] [Google Scholar]
- 79.Pickering RJ, Rosado CJ, Sharma A, Buksh S, Tate M, de Haan JB. Recent novel approaches to limit oxidative stress and inflammation in diabetic complications. Clin. Transl. Immunology. 2018;7(4):e1016. doi: 10.1002/cti2.1016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80.Pivari F, Mingione A, Brasacchio C, Soldati L. Curcumin and type 2 diabetes mellitus: prevention and treatment. Nutrients. 2019;11(8):1837. doi: 10.3390/nu11081837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81.Rahimi-Madiseh M, Malekpour-Tehrani A, Bahmani M, Rafieian-Kopaei M. The research and development on the antioxidants in prevention of diabetic complications. Asian Pac. J. Trop. Med. 2016;9(9):825–831. doi: 10.1016/j.apjtm.2016.07.001. [DOI] [PubMed] [Google Scholar]
- 82.Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J. Biol. Chem. 2004;279(41):42351–42354. doi: 10.1074/jbc.R400019200. [DOI] [PubMed] [Google Scholar]
- 83.Robson R, Kundur AR, Singh I. Oxidative stress biomarkers in type 2 diabetes mellitus for assessment of cardiovascular disease risk. Diabetes Metab. Syndr. 2018;12(3):455–462. doi: 10.1016/j.dsx.2017.12.029. [DOI] [PubMed] [Google Scholar]
- 84.Rochette L, Zeller M, Cottin Y, Vergely C. Diabetes, oxidative stress and therapeutic strategies. Biochim. Biophys. Acta. 2014;1840(9):2709–2729. doi: 10.1016/j.bbagen.2014.05.017. [DOI] [PubMed] [Google Scholar]
- 85.Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol. 2006;212(2):167–178. doi: 10.1016/j.taap.2006.01.003. [DOI] [PubMed] [Google Scholar]
- 86.Roohbakhsh A, Karimi G, Iranshahi M. Carotenoids in the treatment of diabetes mellitus and its complications. Biomed. Pharmacother. 2017;91:31–42. doi: 10.1016/j.biopha.2017.04.057. [DOI] [PubMed] [Google Scholar]
- 87.Rosta V, Trentini A, Passaro A, Zuliani G, Sanz JM, Bosi C, Bonaccorsi G, Bellini T, Cervellati C. Sex difference impacts on the relationship between paraoxonase-1 (PON1) and type 2 diabetes. Antioxidants. 2020;9(8):683. doi: 10.3390/antiox9080683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 88.Saeedi Borujeni MJ, Esfandiary E, Baradaran A, Valiani A, Ghanadian M, Codoñer-Franch P, Basirat R, Alonso-Iglesias E, Mirzaei H, Yazdani A. Molecular aspects of pancreatic β-cell dysfunction: oxidative stress, microRNA, and long noncoding RNA. J. Cell. Physiol. 2019;234(6):8411–8425. doi: 10.1002/jcp.27755. [DOI] [PubMed] [Google Scholar]
- 89.Schrammel A, Mussbacher M, Winkler S, Haemmerle G, Stessel H, Wölkart G, Zechner R, Mayer B. Cardiac oxidative stress in a mouse model of neutral lipid storage disease. Biochim. Biophys. Acta. 2013;1831(11):1600–1608. doi: 10.1016/j.bbalip.2013.07.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 90.Selvin E, Juraschek SP. Diabetes epidemiology in the COVID-19 pandemic. Diabetes Care. 2020;43(8):1690–1694. doi: 10.2337/dc20-1295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 91.Serhiyenko V, Hotsko M, Serhiyenko A, Snitynska O, Serhiyenko L, Segin V. The impact of alpha-lipoic acid on insulin resistance and inflammatory parameters in patients with type 2 diabetes mellitus and cardiac autonomic neuropathy. Am. J. Int. Med. 2020;8(5):197-203. doi: 10.11648/j.ajim.20200805.11
- 92.Sies H. Oxidative stress: concept and some practical aspects. Antioxidants (Basel). 2020;9(9):852. doi: 10.3390/antiox9090852. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93.Sies H, Jones DP. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 2020;21(7):363–383. doi: 10.1038/s41580-020-0230-3. [DOI] [PubMed] [Google Scholar]
- 94.Sifuentes-Franco S, Pacheco-Moisés FP, Rodríguez-Carrizalez AD, Miranda-Díaz AG. The role of oxidative stress, mitochondrial function, and autophagy in diabetic polyneuropathy. J. Diabetes Res. 2017;2017:1673081. doi: 10.1155/2017/1673081. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 95.Sifuentes-Franco S, Padilla-Tejeda DE, Carrillo-Ibarra S, Miranda-Díaz AG. Oxidative stress, apoptosis, and mitochondrial function in diabetic nephropathy. Int. J. Endocrinol. 2018;2018. ID 1875870. doi: 10.1155/2018/1875870 [DOI] [PMC free article] [PubMed]
- 96.Tavakoli M, Gogas Yavuz D, Tahrani A.A, Selvarajah D, Bowling F.L, Fadavi H. Diabetic neuropathy: current status and future prospects. J. Diabetes Res. 2017;2017:5825971. doi: 10.1155/2017/5825971 [DOI] [PMC free article] [PubMed]
- 97.Testa R, Bonfigli AR, Prattichizzo F, La Sala L, De Nigris V, Ceriello A. The “metabolic memory” theory and the early treatment of hyperglycemia in prevention of diabetic complications. Nutrients. 2017;9(5):437. doi: 10.3390/nu9050437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 98.Wang J, Wang H. Oxidative stress in pancreatic beta cell regeneration. Oxid. Med. Cell. Longev. 2017;2017:1930261. doi: 10.1155/2017/1930261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 99.Wang X, Tao L, Hai CX. Redox-regulating role of insulin: the essence of insulin effect. Mol. Cell. Endocrinol. 2012;349(2):111–127. doi: 10.1016/j.mce.2011.08.019. [DOI] [PubMed] [Google Scholar]
- 100.Xiao L, Xu X, Zhang F, Wang M, Xu Y, Tang D, Wang J, Qin Y, Liu Y, Tang C, He L, Greka A, Zhou Z, Liu F, Dong Z, Sun L. The mitochondria-targeted antioxidant MitoQ ameliorated tubular injury mediated by mitophagy in diabetic kidney disease via Nrf2/PINK1. Redox Biol. 2017;11:297–311. doi: 10.1016/j.redox.2016.12.022. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 101.Yin Y, Zheng Z, Jiang Z. Effects of lycopene on metabolism of glycolipid in type 2 diabetic rats. Biomed. Pharmacother. 2019;109:2070–2077. doi: 10.1016/j.biopha.2018.07.100. [DOI] [PubMed] [Google Scholar]
- 102.Zhang P, Li T, Wu X, Nice EC, Huang C, Zhang Y. Oxidative stress and diabetes: antioxidative strategies. Front. Med. 2020;14(5):583–600. doi: 10.1007/s11684-019-0729-1. [DOI] [PubMed] [Google Scholar]
- 103.Zhang YJ, Gan RY, Li S, Zhou Y, Li AN, Xu DP, Li HB. Antioxidant phytochemicals for the prevention and treatment of chronic diseases. Molecules. 2015;20(12):21138–21156. doi: 10.3390/molecules201219753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 104.Zheng Z, Yin Y, Lu R, Jiang Z. Lycopene ameliorated oxidative stress and inflammation in type 2 diabetic rats. J. Food Sci. 2019;84(5):1194–1200. doi: 10.1111/1750-3841.14505. [DOI] [PubMed] [Google Scholar]