Biomarkers of Oxidative Stress in Diabetic Microvascular Complications Review Article

Authors

DOI:

https://doi.org/10.31351/vol33iss3pp1-16

Keywords:

oxidative stress, hyperglycemia, diabetes mellitus, microvascular diseases

Abstract

Reactive oxygen species (ROS) are produced as a result of biochemical processes that are not in balance with the body's antioxidant defense mechanism. This metabolic dysfunction is referred to the oxidative stress (OS).  Metabolic dysfunction-associated diseases are affected by changes in the redox balance. It is now widely recognized that oxidative stress significantly affects diabetes mellitus (DM), particularly type 2 diabetes. The biochemical changes associated with  DM could  disturb the oxidative milieu, leading to several microvascular complications in diabetic patients. Thus, DM is a perfect disease to explore the harmful consequences of oxidative stress and how to treat it. Oxidative stress triggered by hyperglycemia is an important contributor to the effects of diabetic microvascular diseases. Uncontrolled hyperglycemia carried by deficiencies in insulin secretion or action produces a number of problems, such as peripheral vascular disorders, nephropathy, neuropathy, retinopathy, increased morbidity and/or mortality, as well as the incidence of diabetes mellitus (DM) are rising globally. The development and progression of diabetic problems are strongly correlated with reactive oxygen species and oxidative stress, according to a wide body of research. This review aims to explore various markers of oxidative stress and the role of ROS in the pathogenesis and progression of late diabetic microvascular complications.

References

Fakree NK, Ali SH. Effect of COX-2 Inhibitors Selectivity on Lipid Profile in Hyperlipidemic and Normolipidemic Type 2 Diabetics. Iraqi J. Pharm. Sci. 2009; 18:7-13.

Brar, P.C.; Tell, S.; Mehta, S.; Franklin, B. Hyperosmolar diabetic ketoacidosis– review of literature and the shifting paradigm in evaluation and management. Diabetes Metab. Syndr. 2021, 15, 102313.

Aikaeli F, Njim T, Gissing S, Moyo F, Alam U, Mfinanga SG, Okebe J, Ramaiya K, Webb EL, Jaffar S, Garrib A. Prevalence of microvascular and macrovascular complications of diabetes in newly diagnosed type 2 diabetes in low-and-middle-income countries: A systematic review and meta-analysis. PLOS global public health. 2022 Jun 15;2(6): e0000599.

Ortiz-Martínez M, González-González M, Martagón AJ, Hlavinka V, Willson RC, Rito-Palomares M. Recent developments in biomarkers for diagnosis and screening of type 2 diabetes mellitus. Current Diabetes Reports. 2022 Mar;22(3):95-115.

Bhatti JS, Sehrawat A, Mishra J, Sidhu IS, Navik U, Khullar N, Kumar S, Bhatti GK, Reddy PH. Oxidative stress in the pathophysiology of type 2 diabetes and related complications: Current therapeutics strategies and future perspectives. Free Radical Biology and Medicine. 2022 May 1;184:114-34.

Tan Y, Cheong MS, Cheang WS. Roles of Reactive Oxygen Species in Vascular Complications of Diabetes: Therapeutic Properties of Medicinal Plants and Food. Oxygen. 2022; 2(3):246-268.

Volpe CM, Villar-Delfino PH, Dos Anjos PM, NogueiraMachado JA. Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death Dis 2018; 9:119.

Jabbar TL, Kasim AA. Association of Retinol Binding Protein-4 (RBP4) with Glycemia, Dyslipidemia, Hypertension, and Obesity in Type 2 Diabetic Iraqi Patients. Iraqi Journal of Pharmaceutical Sciences (P-ISSN 1683-3597 E-ISSN 2521-3512). 2020 Dec 30;29(2):263-70.

Cole JB, Florez JC. Genetics of diabetes mellitus and diabetes complications. Nature reviews nephrology. 2020 Jul;16(7):377-90.

Samsu N. Diabetic nephropathy: challenges in pathogenesis, diagnosis, and treatment. BioMed research international. 2021 Jul 8; Volume 2021, Article ID 1497449, 17 pages.

Ansari P, Tabasumma N, Snigdha NN, Siam NH, Panduru RV, Azam S, Hannan JM, Abdel-Wahab YH. Diabetic retinopathy: an overview on mechanisms, pathophysiology and pharmacotherapy. Diabetology. 2022 Feb 15;3(1):159-75.

Luna R, Manjunatha RT, Bollu B, Jhaveri S, Avanthika C, Reddy N, Saha T, Gandhi F. A comprehensive review of neuronal changes in diabetics. Cureus. 2021 Oct 30;13(10).

Diabetes Control and Complications Trial (DCCT). Update. DCCT Research Group. Diabetes Care .1990;13:427–433.

Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998;352: 837–853.

Study rationale and design of ADVANCE: Action in diabetes and vascular disease–preterax and diamicron MR controlled evaluation. Diabetologia. 2001; 44:1118–1120.

Buse, J.B.; Bigger, J.T.; Byington, R.P.; Cooper, L.S.; Cushman, W.C.; Friedewald, W.T.; Genuth, S.; Gerstein, H.C.; Ginsberg, H.N.; Goff, D.C., Jr.; et al. Action to Control Cardiovascular Risk in Diabetes (ACCORD) trial: Design and methods. Am. J. Cardiol. 2007; 99: 21i–33i.

Hur, K.Y.; Moon, M.K.; Park, J.S.; Kim, S.K.; Lee, S.H.; Yun, J.S.; Baek, J.H.; Noh, J.; Lee, B.W.; Oh, T.J.; et al. 2021 Clinical Practice Guidelines for Diabetes Mellitus of the Korean Diabetes Association. Diabetes Metab. J. 2021; 45: 461–481.

Hoffmann, A.P.; Honigberg, M.C. Glycated Hemoglobin as an Integrator of Cardiovascular Risk in Individuals Without Diabetes: Lessons from Recent Epidemiologic Studies. Curr. Atheroscler. Rep. 2022; 24:435–442.

Rigon FA, Ronsoni MF, Vianna AG, Schiavon LD, Hohl A, Sande-Lee SV. Flash glucose monitoring system in special situations. Archives of Endocrinology and Metabolism. 2022 Jun 10; 66:883-94.

Yoo, J.H.; Kim, J.H. Time in Range from Continuous Glucose Monitoring: A Novel Metric for Glycemic Control. Diabetes Metab. J. 2020;44: 828–839.

Villalpando-Rodriguez GE, Gibson SB. Reactive Oxygen Species (ROS) Regulates Different Types of Cell Death by Acting as a Rheostat. Oxid Med Cell Longev. 2021; 2021:9912436.

Cortopassi, G.A.; Shibata, D.; Soong, N.W.; Arnheim, N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl. Acad. Sci. USA 1992; 89:7370–7374.

Song, S.; Pursell, Z.F.; Copeland, W.C.; Longley, M.J.; Kunkel, T.A.; Mathews, C.K. DNA precursor asymmetries in mammalian tissue mitochondria and possible contribution to mutagenesis through reduced replication fidelity. Proc. Natl. Acad. Sci. USA 2005; 102: 4990–4995.

Hernansanz-Agustín P, Enríquez JA. Generation of reactive oxygen species by mitochondria. Antioxidants. 2021 Mar 9;10(3):415.

Kampjut, D.; Sazanov, L.A. Structure and mechanism of mitochondrial proton-translocating transhydrogenase. Nature 2019, 573, 291–295.

Pizzino G, Irrera N, Cucinotta M, Pallio G, Mannino F, Arcoraci V, Squadrito F, Altavilla D, Bitto A. Oxidative stress: harms and benefits for human health. Oxidative medicine and cellular longevity. 2017 Oct;2017.

Birben, E.; Sahiner, U.M.; Sackesen, C.; Erzurum, S.; Kalayci, O. Oxidative stress and antioxidant defense. World Allergy Organ. J. 2012; 5:9–19.

Behndig, A.; Svensson, B.; Marklund, S.L.; Karlsson, K. Superoxide dismutase isoenzymes in the human eye. Investig. Ophthalmol. Vis. Sci. 1998; 39:471–475.

Deliyanti, D.; Alrashdi, S.F.; Tan, S.M.; Meyer, C.; Ward, K.W.; de Haan, J.B.; Wilkinson-Berka, J.L. Nrf2 Activation Is a Potential Therapeutic Approach to Attenuate Diabetic Retinopathy. Investig. Ophthalmol. Vis. Sci. 2018; 59:815–825.

Tonelli, C.; Chio, I.I.C.; Tuveson, D.A. Transcriptional Regulation by Nrf2. Antioxid. Redox Signal. 2017;29:1727–1745.

Shu DY, Chaudhary S, Cho KS, Lennikov A, Miller WP, Thorn DC, Yang M, McKay TB. Role of Oxidative Stress in Ocular Diseases: A Balancing Act. Metabolites. 2023 Jan 27;13(2):187.

Paz Aliaga A, Cruz Oviedo AF, Paz Matellini CM. Antioxidants: healthier life projection. Physiological Mini Reviews. 2019;12.

Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. Int J Biomed Sci. 2008; 4:89-96.

Freitas M, Gomes A, Porto G, Fernandes E. Nickel induces oxidative burst, NFκB activation and interleukin-8 production in human neutrophils. JBIC J Biol Inorg Chem. 2010; 15:1275-83.

Tauffenberger, A., Magistretti, P.J. Reactive Oxygen Species: Beyond Their Reactive Behavior. Neurochem Res .2021;46, 77–87

Singh A, Kukreti R, Saso L, Kukreti S. Mechanistic insight into oxidative stress-triggered signaling pathways and type 2 diabetes. Molecules. 2022 Jan 30;27(3):950.

Lugrin J, Rosenblatt-Velin N, Parapanov R, Liaudet L. The role of oxidative stress during inflammatory processes. Biol Chem. 2014; 395:203-30.

Wu T, Ding L, Andoh V, Zhang J, Chen L. The Mechanism of Hyperglycemia-Induced Renal Cell Injury in Diabetic Nephropathy Disease: An Update. Life (Basel). 2023;13(2):539.

Ho E, Galougahi KK, Liu CC, Bhindi R, Figtree GA. Biological markers of oxidative stress: Applications to cardiovascular research and practice. Redox Biol 2013; 1(1): 483-491.

Liguori I, Russo G, Curcio F, Bulli G, Aran L, Della-Morte D, et al. Oxidative stress, aging, and diseases. Clin Interv Aging 2018; 13: 757- 772.

Bigagli E, Lodovici M. Circulating oxidative stress biomarkers in clinical studies on type 2 diabetes and its complications. Oxidative medicine and cellular longevity. 2019 May 12;2019.

Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A. Biomarkers of oxidative damage in human disease. Clinical chemistry. 2006 Apr 1;52(4):601-23

Ito F, Sono Y, Ito T. Measurement and clinical significance of lipid peroxidation as a biomarker of oxidative stress: Oxidative stress in diabetes, atherosclerosis, and chronic inflammation. Antioxidants 2019; 8(3): 1-28.

Shabalala SC, Johnson R, Basson AK, Ziqubu K, Hlengwa N, Mthembu SXH, Mabhida SE, Mazibuko-Mbeje SE, Hanser S, Cirilli I, et al. Detrimental Effects of Lipid Peroxidation in Type 2 Diabetes: Exploring the Neutralizing Influence of Antioxidants. Antioxidants. 2022; 11(10):2071.

Spickett CM, Wiswedel I, Siems W, Zarkovic K, Zarkovic N. Advances in methods for the determination of biologically relevant lipid peroxidation products. Free Radic Res 2010; 44(10): 1172-1202.

Milkovic L., Cipak Gasparovic A., Cindric M., Mouthuy P.-A., Zarkovic N. Short overview of ROS as cell function regulators and their implications in therapy concepts. Cells. 2019;8:793.

R. L. Levine, D. Garland, C. N. Oliver et al., “Determination of carbonyl content in oxidatively modified proteins,” Methods in Enzymology.1990; 186 : 464–478.

A. Sakul, A. Cumaoglu, E. Aydın, N. Ar, N. Dilsiz, and C. Karasu, “Age-and diabetes-induced regulation of oxidative protein modification in rat brain and peripheral tissues: consequences of treatment with antioxidant pyridoindole,” Experimental Gerontology.2013; 48(5): 476–484.

D. Gradinaru, C. Borsa, C. Ionescu, and D. Margina, “Advanced oxidative and glycoxidative protein damage markers in the elderly with type 2 diabetes,” Journal of Proteomics.2013; 13: 181– 184.

Twarda-Clapa A, Olczak A, Białkowska AM, Koziołkiewicz M. Advanced glycation end-products (AGEs): Formation, chemistry, classification, receptors, and diseases related to AGEs. Cells. 2022 Apr 12;11(8):1312.

Senavirathna L, Ma C, Chen R, Pan S. Proteomic Investigation of Glyceraldehyde-Derived Intracellular AGEs and Their Potential Influence on Pancreatic Ductal Cells. Cells. 2021; 10(5):1005..

Lal MA, Brismar H, Eklöf AC, Aperia A. Role of oxidative stress in advanced glycation end product-induced mesangial cell activation. Kidney International. 2002 Jun 1;61(6):2006-14.

53.M. Kalousova, J. ´ Skrha, and T. Zima, “Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus,” Physiological Research.2002; 51(6) : 597–604.

K. B. Pandey and S. I. Rizvi, “Resveratrol may protect plasma proteins from oxidation under conditions of oxidative stress in vitro,” Journal of the Brazilian Chemical Society.2010; 21(5) : 909–913.

V. Witko-Sarsat, M. Friedlander, C. Capeillere-Blandin et al.“Advanced oxidation protein products as a novel marker of oxidative stress in uremia,” Kidney International.1996 ;49(5): 1304–1313.

Kehm R, Baldensperger T, Raupbach J, Höhn A. Protein oxidation - Formation mechanisms, detection and relevance as biomarkers in human diseases. Redox Biol. 2021;42:101901.

A. Piwowar, “Advanced oxidation protein products. Part I. Mechanism of the formation, characteristics and property,” Polski Merkuriusz Lekarski.2010; 28(164): 166–169.

A. Piwowar, M. Knapik-Kordecka, and M. Warwas, “AOPP and its relations with selected markers of oxidative/antioxidative system in type 2 diabetes mellitus,” Diabetes Research and Clinical Practice.2007;77(2): 188–192.

Khan AN, Khan RA, Ahmad M, Mushtaq N. Role of antioxidant in oxidative stress and diabetes mellitus. Journal of pharmacognosy and phytochemistry. 2015;3(6):217-20.

Chowdhury S, Ghosh S, Das AK, Sil PC. Ferulic acid protects hyperglycemia-induced kidney damage by regulating oxidative insult, inflammation and autophagy. Front Pharmacol 2019; 10(27): 1-24

Behl T, Kaur I, Kotwani A. Implication of oxidative stress in progression of diabetic retinopathy. Surv Ophthalmol 2016; 61(2): 187-196.

Kilanczyk E, Saraswat Ohri S, Whittemore SR, Hetman M. Antioxidant protection of NADPH-depleted oligodendrocyte precursor cells is dependent on supply of reduced glutathione. ASN Neuro 2016; 8(4): 1-13.

de Paula MLA, Rodrigues Villela AM, Negri MM, Kanaan S, de Carvalho Cardoso Weide L. Role of advanced glycation end products related to the onset of diabetic kidney disease complications. Clin Biomed Res 2017; 37(4): 341-348.

Ighodaro OM. Molecular pathways associated with oxidative stress in diabetes mellitus. Biomed Pharmacother 2018; 108: 656-662.

65.Yadav SK, Tripathi R, Tripathi K. Toll-like receptor in diabetic vascular endothelium dysfunction. In: Chawla R. (eds.) RSSDI diabetes update. New Delhi: Jaypee Brothers Medical Publishers; 2018, p. 11-15.

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.

Uhde K, van Tol HTA, Stout TAE, Roelen BAJ. Exposure to elevated glucose concentrations alters the metabolomic profile of bovine blastocysts. PLoS One 2018; 13(6): 1-13.

Pesta M, Cedikova M, Dvorak P, Dvorakova J, Kulda V, Srbecka K, et al. Trends in gene expression changes during adipogenesis in human adipose derived mesenchymal stem cells under dichlorodiphenyldichloroethylene exposure. Mol Cell Toxicol 2018; 14(4): 369-379.

Li WJ, Xu M, Gu M, Zheng D, Xie M, Guo J, et al. Poly (ADP-ribose) polymerase inhibition restores bladder function by suppressing bladder apoptosis in diabetic rats. Int J Clin Exp Pathol 2017; 10(4): 4451-4460.

Czapski GA, Cieślik M, Wencel PL, Wójtowicz S, Strosznajder RP, Strosznajder JB. Inhibition of poly (ADP-ribose) polymerase-1 alters expression of mitochondria-related genes in PC12 cells: Relevance to mitochondrial homeostasis in neurodegenerative disorders. Biochim Biophys Acta (BBA)- Mol Cell Res 2018; 1865(2): 281-288.

Tibaut M. Oxidative stress genes, antioxidants and coronary artery disease in type 2 diabetes mellitus. Cardiovasc Hematol Agents Med Chem (Formerly Curr Med Chem Hematol Agents) 2016; 14(1): 23-38.

Hayes, J.D.; Dinkova-Kostova, A.T. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem. Sci. 2014; 39: 199–218.

Kensler, T.W.; Wakabayashi, N.; Biswal, S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007;47: 89–116.

Yagishita, Y.; Fukutomi, T.; Sugawara, A.; Kawamura, H.; Takahashi, T.; Pi, J.; Uruno, A.; Yamamoto, M. Nrf2 protects pancreatic β-cells from oxidative and nitrosative stress in diabetic model mice. Diabetes 2014;63:605–618.

Yang, B.; Fu, J.; Zheng, H.; Xue, P.; Yarborough, K.; Woods, C.G.; Hou, Y.; Zhang, Q.; Andersen, M.E.; Pi, J. Deficiency in the nuclear factor E2-related factor 2 renders pancreatic β-cells vulnerable to arsenic-induced cell damage. Toxicol. Appl. Pharmacol. 2012;264:315–323.

Bhakkiyalakshmi, E.; Sireesh, D.; Rajaguru, P.; Paulmurugan, R.; Ramkumar, K.M. The emerging role of redox-sensitive Nrf2— Keap1 pathway in diabetes. Pharmacol. Res. 2015; 91:104–114.

Sireesh, D.; Ganesh, M.R.; Dhamodharan, U.; Sakthivadivel, M.; Sivasubramanian, S.; Gunasekaran, P.; Ramkumar, K.M. Role of pterostilbene in attenuating immune mediated devastation of pancreatic β cells via Nrf2 signaling cascade. J. Nutr. Biochem. 2017;44:11–21.

Bhakkiyalakshmi, E.; Shalini, D.; Sekar, T.V.; Rajaguru, P.; Paulmurugan, R.; Ramkumar, K.M. Therapeutic potential of pterostilbene against pancreatic β-cell apoptosis mediated through Nrf2. Br. J. Pharmacol. 2014;171: 1747–1757.

Bhakkiyalakshmi, E.; Dineshkumar, K.; Karthik, S.; Sireesh, D.; Hopper, W.; Paulmurugan, R.; Ramkumar, K.M. Pterostilbenemediated Nrf2 activation: Mechanistic insights on Keap1:Nrf2 interface. Bioorganic Med. Chem. 2016;24:3378–3386.

Ramkumar, K.M.; Sekar, T.V.; Foygel, K.; Elango, B.; Paulmurugan, R. Reporter protein complementation imaging assay to screen and study Nrf2 activators in cells and living animals. Anal. Chem. 2013;85:7542–7549.

Wang, B.; Sun, J.; Li, X.; Zhou, Q.; Bai, J.; Shi, Y.; Le, G. Resveratrol prevents suppression of regulatory T-cell production, oxidative stress, and inflammation of mice prone or resistant to high-fat diet-induced obesity. Nutr. Res. 2013;33:971–981.

Song, M.Y.; Kim, E.K.; Moon, W.S.; Park, J.W.; Kim, H.J.; So, H.S.; Park, R.; Kwon, K.B.; Park, B.H. Sulforaphane protects against cytokine- and streptozotocin-induced β-cell damage by suppressing the NF kappaB pathway. Toxicol. Appl. Pharmacol. 2009;235:57–67.

Rashid, K.; Sil, P.C. Curcumin enhances recovery of pancreatic islets from cellular stress induced inflammation and apoptosis in diabetic rats. Toxicol. Appl. Pharmacol. 2015;282:297–310.

Coskun, O.; Kanter, M.; Korkmaz, A.; Oter, S. Quercetin, a flavonoid antioxidant, prevents and protects streptozotocin-induced oxidative stress and β-cell damage in rat pancreas. Pharmacol. Res. 2005;51:117–123.

Li, W.; Wu, W.; Song, H.; Wang, F.; Li, H.; Chen, L.; Lai, Y.; Janicki, J.S.; Ward, K.W.; Meyer, C.J.; et al. Targeting Nrf2 by dihydro-CDDO-trifluoroethyl amide enhances autophagic clearance and viability of β-cells in a setting of oxidative stress. FEBS Lett. 2014; 588:2115–2124.

Li, W.; Kong, A.N. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinog. 2009;48:91–104.

Salih BH, Ali SH, Allehibi KI. Serum Aldosterone Levels in Patients With Diabetic Nephropathy in Relation to Vascular Calcification. Iraqi Journal of Pharmaceutical Sciences (P-ISSN 1683-3597 E-ISSN 2521-3512). 2019 Jun 11;28(1):53-63.

Filippatos G, Anker SD, Agarwal R, et al. Finerenone and cardiovascular outcomes in patients with chronic kidney disease and type 2 diabetes. Circulation. 2021;143(6):540–552.

Lassén E, Daehn IS. Molecular Mechanisms in Early Diabetic Kidney Disease: Glomerular Endothelial Cell Dysfunction. Int J Mol Sci. 2020 Dec 11;21(24):9456

Kao MP, Ang DS, Pall AA, Struthers AD. Oxidative stress in renal dysfunction: mechanisms, clinical sequelae and therapeutic options. Journal of human hypertension. 2010 Jan;24(1):1-8.

Wen C, Ying Y, Zhao H, et al. Resistance exercise affects catheter-related thrombosis in rats through miR-92a-3p, oxidative stress and the MAPK/NF-jB pathway. BMC Cardiovasc Disord. 2021;21(1):440.

Zoccali C, Mallamaci F. Nonproteinuric progressive diabetic kidney disease. Curr Opin Nephrol Hypertens. 2019;28(3):227–232.

Hofmann MA, Schiekofer S, Isermann B, et al. Peripheral blood mononuclear cells isolated from patients with diabetic nephropathy show increased activation of the oxidative-stress sensitive transcription factor NF-kappaB. Diabetologia. 1999;42(2): 222–232.

Viswanath, K.; McGavin, D.D. Diabetic retinopathy: Clinical findings and management. Community Eye Health 2003; 16:21–24.

Frank, R.N. Diabetic Retinopathy. N. Engl. J. Med. 2004; 350:48–58.

Kowluru, R.A.; Kowluru, A.; Mishra, M.; Kumar, B. Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy. Prog. Retin. Eye Res. 2015;48: 40–61.

Kowluru, R.A.; Mohammad, G. Epigenetic modifications in diabetes. Metabolism 2021; 126:154920.

Sharifi-Rad M, Anil Kumar NV, Zucca P, Varoni EM, Dini L, Panzarini E, Rajkovic J, Tsouh Fokou PV, Azzini E, Peluso I, Prakash Mishra A. Lifestyle, oxidative stress, and antioxidants: Back and forth in the pathophysiology of chronic diseases. Frontiers in physiology. 2020 Jul 2;11:694.

Poljsak B, Šuput D, Milisav I. Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxidative medicine and cellular longevity. 2013 Oct;2013.

Kang Q, Yang C. Oxidative stress and diabetic retinopathy: Molecular mechanisms, pathogenetic role and therapeutic implications. Redox Biol. 2020;37:101799.

Kowluru RA. Cross Talks between Oxidative Stress, Inflammation and Epigenetics in Diabetic Retinopathy. Cells. 2023;12(2):300

Kowluru RA. Diabetic Retinopathy: Mitochondria Caught in a Muddle of Homocysteine. Journal of Clinical Medicine. 2020; 9(9):3019.

Kowluru, R.A.; Mishra, M. Regulation of matrix metalloproteinase in the pathogenesis of diabetic retinopathy. Prog. Mol. Biol. Transl. Sci. 2017;148:67–85.

Murphy, M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009;417: 1–13.

Kowluru, R.A.; Kowluru, A.; Veluthakal, R.; Mohammad, G.; Syed, I.; Santos, J.M.; Mishra, M. TIAM1-RAC1 signalling axismediated activation of NADPH oxidase-2 initiates mitochondrial damage in the development of diabetic retinopathy. Diabetologia 2014;57: 1047–1056.

Kowluru, R.A. Diabetic retinopathy, oxidative stress and antioxidants. Curr. Top. Nutraceutical Res. 2005;3:209–218

Feldman EL, Callaghan BC, Pop-Busui R, Zochodne DW, Wright DE, Bennett DL, Bril V, Russell JW, Viswanathan V. Diabetic neuropathy. Nature reviews Disease primers. 2019 Jun 13;5(1):41.

G. Sloan, P. Shillo, D. Selvarajah et al., “A new look at painful diabetic neuropathy,” Diabetes Research and Clinical Practice.2018; 144: 177–191.

Liu H, Bian W, Yang D, Yang M, Luo H. Inhibiting the Piezo1 channel protects microglia from acute hyperglycaemia damage through the JNK1 and mTOR signalling pathways. Life Sci. 2021;264: 118667.

Vargas-Soria M, García-Alloza M, Corraliza-Gómez M. Effects of diabetes on microglial physiology: a systematic review of in vitro, preclinical and clinical studies. Journal of Neuroinflammation. 2023 Dec;20(1):1-30.

Chhetri DR. Myo-Inositol and Its Derivatives: Their Emerging Role in the Treatment of Human Diseases. Front Pharmacol. 2019;10:1172.

H. E. Poulsen, E. Specht, K. Broedbaek et al., “RNA modifications by oxidation: a novel disease mechanism?” Free Radical Biology & Medicine.2012; 52(8): 1353–1361.

Oyenihi AB, Ayeleso AO, Mukwevho E, Masola B. Antioxidant strategies in the management of diabetic neuropathy. Biomed Res Int. 2015 Oct;2015(515042):515042.

Yang C, Zhao X, An X, Zhang Y, Sun W, Zhang Y, Duan Y, Kang X, Sun Y, Jiang L, Lian F. Axonal transport deficits in the pathogenesis of diabetic peripheral neuropathy. Frontiers in Endocrinology. 2023 Mar 28;14:1136796.

Rahimi-Madiseh M, Malekpour-Tehrani A, Bahmani M, Rafeian-Kopaei M. The research and development on the antioxidants in prevention of diabetic complications. Asian Pac. J. Trop. Med. 2016;9(9):825-831.

Serhiyenko V, Hotsko M, Serhiyenko A, Snitynska O, Serhiyenko L, Segin V. The impact of alpha-lipoic acid on insulin resistance and infammatory parameters in patients with type 2 diabetes mellitus and cardiac autonomic neuropathy. Am. J. Int. Med. 2020;8(5):197-203.

Asbaghi, O., Nazarian, B., Yousefi, M. et al. Effect of vitamin E intake on glycemic control and insulin resistance in diabetic patients: an updated systematic review and meta-analysis of randomized controlled trials. Nutr J.2023; 22:10

Shaun A. Mason, Michelle A. Keske, Glenn D. Wadley; Effects of Vitamin C Supplementation on Glycemic Control and Cardiovascular Risk Factors in People With Type 2 Diabetes: A GRADE-Assessed Systematic Review and Meta-analysis of Randomized Controlled Trials. Diabetes Care 1 February 2021; 44 (2): 618–630.

Jin Y, Arroo R. The protective effects of flavonoids and carotenoids against diabetic complications—A review of in vivo evidence. Frontiers in Nutrition. 2023 Mar 24;10:1020950.

Leh HE, Lee LK. Lycopene: A potent antioxidant for the amelioration of type II diabetes mellitus. Molecules. 2022 Apr 4;27(7):2335.

Yedjou CG, Grigsby J, Mbemi A, Nelson D, Mildort B, Latinwo L, Tchounwou PB. The Management of Diabetes Mellitus Using Medicinal Plants and Vitamins. International Journal of Molecular Sciences. 2023; 24(10):9085.

Pivari F, Mingione A, Brasacchio C, Soldati L. Curcumin and type 2 diabetes mellitus: prevention and treatment. Nutrients. 2019;11(8):1837.

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.

Hoseini A, Namazi G, Farrokhian A, Reiner Ž, Aghadavod E, Bahmani F, Asemi Z. The efects of resveratrol on metabolic status in patients with type 2 diabetes mellitus and coronary heart disease. Food Function. 2019;10(9):6042-6051.

Darenskaya MA, Kolesnikova LI, Kolesnikov SI. Oxidative stress: pathogenetic role in diabetes mellitus and its complications and therapeutic approaches to correction. Bulletin of experimental biology and medicine. 2021 May;171(2):179-89.

Dzugkoev SG, Kaloeva MB, Dzugkoeva FS. Efect 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.

Skliarova EI, Popova TN, Shulgin KK. Efects 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.

Sun C, Liu Y, Zhan L, Rayat GR, Xiao J, Jiang H, Li X, Chen K. Anti-diabetic effects of natural antioxidants from fruits. Trends in Food Science & Technology. 2021 Nov 1;117:3-14

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2024-09-15

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Sarah Hashim Mhaibes, Shatha H. Ali. Biomarkers of Oxidative Stress in Diabetic Microvascular Complications Review Article. IJPS [Internet]. 2024 Sep. 15 [cited 2024 Oct. 9];33(3):1-16. Available from: https://bijps.uobaghdad.edu.iq/index.php/bijps/article/view/2743