Evaluation of Oxidative Protein Damage in Patients with Type 1 and 2 Diabetes Mellitus in Bangladesh
Year 2023,
Volume: 82 Issue: 1, 23 - 30, 26.06.2023
Sanjeda Tamanna
Rocky Sheikh
Taslimul Jannat
Laila Islam
Abstract
Objective: Oxidative stress (OS) has been linked to the development and progression of diabetes mellitus (DM). Although maintaining the redox status of protein is crucial for proper cellular function, proteins are likely to be damaged by OS. Therefore, the present study aimed to evaluate oxidative protein damage (OPD) in patients with DM.
Materials and Methods: A total of 160 participants were recruited, of whom 16 were patients with type 1 DM (T1DM), 84 were patients with type 2 DM (T2DM), and 60 were healthy control subjects. The activities of NADPH oxidase (NOX) and myeloperoxidase (MPO); total oxidative stress (TOS), ferric reducing ability of plasma (FRAP), oxidative stress index (OSI); serum albumin; OPD markers-total thiols (T-SH), protein carbonyls (PCO), and advanced oxidation protein products (AOPP) were assessed.
Results: The activities of serum NOX and MPO were significantly higher in both DM groups compared to controls. Significantly higher TOS and OSI and lower FRAP values were observed in both DM groups than in controls (p<0.001, for all). In patients, the levels of albumin and T-SH were significantly lower, but PCO was significantly elevated, while AOPP was higher in T1DM and significantly elevated in T2DM compared to controls. Correlation analyses between these parameters linked hyperglycemia with enhanced NOX, MPO and AOPP, and decreased FRAP and T-SH in diabetic patients. Further, significant correlations of albumin with T-SH and AOPP suggested an association of OS with hypoalbuminemia.
Conclusion: These findings highlight that hyperglycemia induces enhanced OS and consequent protein damage in both T1DM and T2DM patients.
Supporting Institution
Bangladesh Institute of Research and Rehabilitation in Diabetes, Endocrine and Metabolic Disorders (BIRDEM) General Hospital
Thanks
The authors gratefully thank Professor Dr. M. Sawkat Hassan, Director, Laboratory Services, and Mr. Md. Nayeemul Islam Khan, Principal Scientific Officer, Clinical Biochemistry Laboratory of the BIRDEM General Hospital for their kind cooperation in collecting samples from patients. The authors wish to thank all participants of this study.
References
- Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev. 2013; 93(1):137-188. google scholar
- Maiese K. New insights for oxidative stress and diabetes mellitus. Oxid Med Cell Longev. 2015;87596. google scholar
- Yaribeygi H, Sathyapalan T, Atkin SL, Sahebkar A. Molecular mechanisms linking oxidative stress and diabetes mellitus. Oxid Med Cell Longev. 2020;8609213. google scholar
- Huang X, Sun M, Li D, et al. Augmented NADPH oxidase activity and p22phox expression in monocytes underlie oxidative stress of patients with type 2 diabetes mellitus. Diabetes Res Clin Pract. 2011;91(3):371-380. google scholar
- Ghoshal K, Das S, Aich K, Goswami S, Chowdhury S, Bhat-tacharyya M. A novel sensor to estimate the prevalence of hypochlorous (HOCl) toxicity in individuals with type 2 diabetes
and dyslipidemia. Clin Chim Acta. 2016;458:144-153. google scholar
- Lambeth JD. Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med. 2007;43(3):332-347. google scholar
- Garaa AG, Rodriguez MR, Alonso CG, Ochoa DYR, Aguilar CA. Myeloperoxidase is associated with insulin resistance and inflammation in overweight subjects with first-degree relatives with type 2 diabetes mellitus. Diabetes Metab J. 2015;39(1):59-65. google scholar
- Khan AA, Alsahli MA, Rahmani AH. Myeloperoxidase as an active disease biomarker: Recent biochemical and pathological perspectives. Med Sci (Basel). 2018;6(2):33. google scholar
- Ndrepepa G. Myeloperoxidase - A bridge linking inflammation and oxidative stress with cardiovascular disease. Clin Chim Acta. 2019;493:36-51. google scholar
- Davies MJ. Protein oxidation and peroxidation. Biochem J. 2016;473(7):805-825. google scholar
- Saha P, Banerjee P, Auddya L, et al. Simple modified colorimetric methods for assay of total oxidative stress and antioxidant defense in plasma: Study in diabetic patients. Arch Med. 2015; 7(5):1-7. google scholar
- Boyacı I, Yiğitbaşı T, Ankaralı H. Is oxidative stress a conse-quence of hyperglycemia? Or is hyperglycemia the consequence of oxidative stress? Or are both caused by insulin resistance? Int Arch Endocrinol Clin Res. 2021;7(1):023. google scholar
- Sitar ME, Aydin S, Çakatay U. Human serum albumin and its relation with oxidative stress. Clin Lab. 2013;59(9-10):945-952. google scholar
- Hu ML. Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol. 1994;233:380-385. google scholar
- Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta. 2003;329(1-2):23-38. google scholar
- Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, et al. Ad-vanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. 1996;49(5):1304-1313.
google scholar
- Höhn A, Jung T, Grune T. Pathophysiological importance of ag-gregated damaged proteins. Free Radic Biol Med. 2014;71:70-89. google scholar
- American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of medical care in diabetes-2021. Diabetes Care. 2021;44(Suppl 1):15-33. google scholar
- Reusch VM Jr, Burger MM. Distribution of marker enzymes between mesosomal and protoplast membranes. J Biol Chem. 1974;249(16):5337-5345. google scholar
- Ferdausi N, Anik MEK, Binti NN, Islam LN. Oxidase enzyme ac-tivities and their correlations with antioxidative stress biomarkers in patients with acute coronary syndrome in
Bangladesh. World J Cardiovasc Dis. 2020;10(4): 163-177. google scholar
- Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measure-ment of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol. 1982;78(3):206-209. google scholar
- Choudhury TZ, Kamruzzaman M, Islam LN. Investigation of the cellular and soluble markers of inflammation for the assessment of cardiovascular risk in patients with acute coronary syndrome in Bangladesh. Int J Electron Healthc. 2019;11(1): 67-80. google scholar
- Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem. 1996;239(1):70-76. google scholar
- Haque R, Hafiz FB, Habib MA, Radeen KR, Islam LN. Role of complete blood count, antioxidants, and total antioxidant capacity in the pathophysiology of acute coronary syndrome.
Afr J Bio Sci. 2022;4(1):37-47. google scholar
- Rodkey FL. Direct spectrophotometric determination of albumin in human serum. Clin Chem. 1965;11(4):478-487. google scholar
- Binti NN, Ferdausi N, Anik MEK, Islam LN. Associa-tion of albumin, fibrinogen, and modified proteins with acute coronary syndrome. PLOS One. 2022;17(7):e0271882.
doi:10.1371/journal.pone.0271882 google scholar
- Levine RL, Garland D, Oliver CN, et al. Determination of car-bonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-478. google scholar
- Geetha A, Gopalakrishnan S, Umadevi R. Study on the impact of family history of diabetes among type 2 diabetes mellitus patients in an urban area of Kancheepuram district,
Tamil Nadu. Int J Community Med Public Health. 2017;4(11):4151-4156. google scholar
- Savu O, Serafinceanu C, Grajdeanu IV, Iosif L, Gaman L, Stoian I. Paraoxonase lactonase activity, inflammation and antioxidant status in plasma of patients with type 1 diabetes
mellitus. J Int Med Res. 2014;42(2):523-529. google scholar
- Marra G, Cotroneo P, Pitocco D, et al. Early increase of oxidative stress and reduced antioxidant defenses in patients with uncom-plicated type 1 diabetes: a case for gender
difference. Diabetes Care. 2002;25(2):370-375. google scholar
- Fatima N, Faisal SM, Zubair S, et al. Role of pro-inflammatory cytokines and biochemical markers in the pathogenesis of type 1 diabetes: Correlation with age and glycemic condition in diabetic human subjects. PLOS One. 2016;11(8):e0161548. doi:10.1371/journal.pone.0161548 google scholar
- Siddique MAH, Tamannaa Z, Kamaluddin SM, et al. Total an-tioxidant status in newly-diagnosed type II diabetes patients in Bangladeshi population. JMol Pathophysiol. 2014;5(1):5-9. google scholar
- Al-Deen ZMM, Ajeena IA. Study of total antioxidant capacity in patients with diabetic peripheral neuropathy. Med J Babylon. 2015;12(1):192-201. google scholar
- Rehman A, Zamir S, Bhatti A, Jan SS, Ali S, Wazir F. Evalua-tion of albuminuria, total plasma proteins, and serum albumin in diabetics. Gomal J Med Sci. 2012;10(2):198-200. google scholar
- Cheng PC, Hsu SR, Cheng YC. Association between serum al-bumin concentration and ketosis risk in hospitalized individuals with type 2 diabetes mellitus. J Diabetes Res.
2016;1269706. google scholar
- Bansal S, Chawla D, Siddarth M, Banerjee BD, Madhu SV, Tri-pathi AK. A study on serum advanced glycation end products and its association with oxidative stress and paraoxonase activ-ity in type 2 diabetic patients with vascular complications. Clin Biochem. 2013;46(1-2):109-114. google scholar
- Kalousova M, Fialova L, Skrha J, et al. Oxidative stress, inflam-mation and autoimmune reaction in type 1 and type 2 diabetes mellitus. PragueMedRep. 2004;105(1):21-28. google scholar
- Ates I, Kaplan M, Yuksel M, et al. Determination of thiol/disulphide homeostasis in type 1 diabetes mellitus and the factors associated with thiol oxidation. Endocrine. 2016;51(1):47-51. google scholar
- Michelis R, Kristal B, Snitkovsky T, Sela S. Oxidative mod-ifications impair albumin quantification. Biochem Biophys Res Commun. 2010;401(1):137-142. google scholar
- Witko-Sarsat V, Gausson V, Nguyen AT, et al. AOPP-induced acti-vation of human neutrophil and monocyte oxidative metabolism: a potential target for N-acetylcysteine
treatment in dialysis patients. Kidney Int. 2003;64(1):82-91. google scholar
- Yuan F, Liu SX, Tian JW. Advanced oxidation protein products induce reactive oxygen species production in endothelial cells. Di Yi Jun Yi Da Xue Xue Bao. 2004;24(12):1350-1352. google scholar
Year 2023,
Volume: 82 Issue: 1, 23 - 30, 26.06.2023
Sanjeda Tamanna
Rocky Sheikh
Taslimul Jannat
Laila Islam
References
- Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev. 2013; 93(1):137-188. google scholar
- Maiese K. New insights for oxidative stress and diabetes mellitus. Oxid Med Cell Longev. 2015;87596. google scholar
- Yaribeygi H, Sathyapalan T, Atkin SL, Sahebkar A. Molecular mechanisms linking oxidative stress and diabetes mellitus. Oxid Med Cell Longev. 2020;8609213. google scholar
- Huang X, Sun M, Li D, et al. Augmented NADPH oxidase activity and p22phox expression in monocytes underlie oxidative stress of patients with type 2 diabetes mellitus. Diabetes Res Clin Pract. 2011;91(3):371-380. google scholar
- Ghoshal K, Das S, Aich K, Goswami S, Chowdhury S, Bhat-tacharyya M. A novel sensor to estimate the prevalence of hypochlorous (HOCl) toxicity in individuals with type 2 diabetes
and dyslipidemia. Clin Chim Acta. 2016;458:144-153. google scholar
- Lambeth JD. Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med. 2007;43(3):332-347. google scholar
- Garaa AG, Rodriguez MR, Alonso CG, Ochoa DYR, Aguilar CA. Myeloperoxidase is associated with insulin resistance and inflammation in overweight subjects with first-degree relatives with type 2 diabetes mellitus. Diabetes Metab J. 2015;39(1):59-65. google scholar
- Khan AA, Alsahli MA, Rahmani AH. Myeloperoxidase as an active disease biomarker: Recent biochemical and pathological perspectives. Med Sci (Basel). 2018;6(2):33. google scholar
- Ndrepepa G. Myeloperoxidase - A bridge linking inflammation and oxidative stress with cardiovascular disease. Clin Chim Acta. 2019;493:36-51. google scholar
- Davies MJ. Protein oxidation and peroxidation. Biochem J. 2016;473(7):805-825. google scholar
- Saha P, Banerjee P, Auddya L, et al. Simple modified colorimetric methods for assay of total oxidative stress and antioxidant defense in plasma: Study in diabetic patients. Arch Med. 2015; 7(5):1-7. google scholar
- Boyacı I, Yiğitbaşı T, Ankaralı H. Is oxidative stress a conse-quence of hyperglycemia? Or is hyperglycemia the consequence of oxidative stress? Or are both caused by insulin resistance? Int Arch Endocrinol Clin Res. 2021;7(1):023. google scholar
- Sitar ME, Aydin S, Çakatay U. Human serum albumin and its relation with oxidative stress. Clin Lab. 2013;59(9-10):945-952. google scholar
- Hu ML. Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol. 1994;233:380-385. google scholar
- Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta. 2003;329(1-2):23-38. google scholar
- Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, et al. Ad-vanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int. 1996;49(5):1304-1313.
google scholar
- Höhn A, Jung T, Grune T. Pathophysiological importance of ag-gregated damaged proteins. Free Radic Biol Med. 2014;71:70-89. google scholar
- American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of medical care in diabetes-2021. Diabetes Care. 2021;44(Suppl 1):15-33. google scholar
- Reusch VM Jr, Burger MM. Distribution of marker enzymes between mesosomal and protoplast membranes. J Biol Chem. 1974;249(16):5337-5345. google scholar
- Ferdausi N, Anik MEK, Binti NN, Islam LN. Oxidase enzyme ac-tivities and their correlations with antioxidative stress biomarkers in patients with acute coronary syndrome in
Bangladesh. World J Cardiovasc Dis. 2020;10(4): 163-177. google scholar
- Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measure-ment of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol. 1982;78(3):206-209. google scholar
- Choudhury TZ, Kamruzzaman M, Islam LN. Investigation of the cellular and soluble markers of inflammation for the assessment of cardiovascular risk in patients with acute coronary syndrome in Bangladesh. Int J Electron Healthc. 2019;11(1): 67-80. google scholar
- Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem. 1996;239(1):70-76. google scholar
- Haque R, Hafiz FB, Habib MA, Radeen KR, Islam LN. Role of complete blood count, antioxidants, and total antioxidant capacity in the pathophysiology of acute coronary syndrome.
Afr J Bio Sci. 2022;4(1):37-47. google scholar
- Rodkey FL. Direct spectrophotometric determination of albumin in human serum. Clin Chem. 1965;11(4):478-487. google scholar
- Binti NN, Ferdausi N, Anik MEK, Islam LN. Associa-tion of albumin, fibrinogen, and modified proteins with acute coronary syndrome. PLOS One. 2022;17(7):e0271882.
doi:10.1371/journal.pone.0271882 google scholar
- Levine RL, Garland D, Oliver CN, et al. Determination of car-bonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-478. google scholar
- Geetha A, Gopalakrishnan S, Umadevi R. Study on the impact of family history of diabetes among type 2 diabetes mellitus patients in an urban area of Kancheepuram district,
Tamil Nadu. Int J Community Med Public Health. 2017;4(11):4151-4156. google scholar
- Savu O, Serafinceanu C, Grajdeanu IV, Iosif L, Gaman L, Stoian I. Paraoxonase lactonase activity, inflammation and antioxidant status in plasma of patients with type 1 diabetes
mellitus. J Int Med Res. 2014;42(2):523-529. google scholar
- Marra G, Cotroneo P, Pitocco D, et al. Early increase of oxidative stress and reduced antioxidant defenses in patients with uncom-plicated type 1 diabetes: a case for gender
difference. Diabetes Care. 2002;25(2):370-375. google scholar
- Fatima N, Faisal SM, Zubair S, et al. Role of pro-inflammatory cytokines and biochemical markers in the pathogenesis of type 1 diabetes: Correlation with age and glycemic condition in diabetic human subjects. PLOS One. 2016;11(8):e0161548. doi:10.1371/journal.pone.0161548 google scholar
- Siddique MAH, Tamannaa Z, Kamaluddin SM, et al. Total an-tioxidant status in newly-diagnosed type II diabetes patients in Bangladeshi population. JMol Pathophysiol. 2014;5(1):5-9. google scholar
- Al-Deen ZMM, Ajeena IA. Study of total antioxidant capacity in patients with diabetic peripheral neuropathy. Med J Babylon. 2015;12(1):192-201. google scholar
- Rehman A, Zamir S, Bhatti A, Jan SS, Ali S, Wazir F. Evalua-tion of albuminuria, total plasma proteins, and serum albumin in diabetics. Gomal J Med Sci. 2012;10(2):198-200. google scholar
- Cheng PC, Hsu SR, Cheng YC. Association between serum al-bumin concentration and ketosis risk in hospitalized individuals with type 2 diabetes mellitus. J Diabetes Res.
2016;1269706. google scholar
- Bansal S, Chawla D, Siddarth M, Banerjee BD, Madhu SV, Tri-pathi AK. A study on serum advanced glycation end products and its association with oxidative stress and paraoxonase activ-ity in type 2 diabetic patients with vascular complications. Clin Biochem. 2013;46(1-2):109-114. google scholar
- Kalousova M, Fialova L, Skrha J, et al. Oxidative stress, inflam-mation and autoimmune reaction in type 1 and type 2 diabetes mellitus. PragueMedRep. 2004;105(1):21-28. google scholar
- Ates I, Kaplan M, Yuksel M, et al. Determination of thiol/disulphide homeostasis in type 1 diabetes mellitus and the factors associated with thiol oxidation. Endocrine. 2016;51(1):47-51. google scholar
- Michelis R, Kristal B, Snitkovsky T, Sela S. Oxidative mod-ifications impair albumin quantification. Biochem Biophys Res Commun. 2010;401(1):137-142. google scholar
- Witko-Sarsat V, Gausson V, Nguyen AT, et al. AOPP-induced acti-vation of human neutrophil and monocyte oxidative metabolism: a potential target for N-acetylcysteine
treatment in dialysis patients. Kidney Int. 2003;64(1):82-91. google scholar
- Yuan F, Liu SX, Tian JW. Advanced oxidation protein products induce reactive oxygen species production in endothelial cells. Di Yi Jun Yi Da Xue Xue Bao. 2004;24(12):1350-1352. google scholar