MARKERS OF LIPID AND PROTEIN OXIDATION IN THE BLOOD OF WOMEN AND MEN WITH AUTOIMMUNE HASHIMOTO'S THYROIDITIS
DOI:
https://doi.org/10.58407/bht.1.24.10Keywords:
autoimmune thyroiditis, oxidative stress, subclinical hypothyroidism, 2-thiobarbituric acid reactive substances (TBARS), carbonyl derivatives of protein oxidative modification (OMP), total antioxidant capacity (TAC)Abstract
Purpose: The aim of this study was to analyze changes in markers of oxidative stress (lipid peroxidation and oxidative modification of proteins) and the total antioxidant activity in the blood of women and men with autoimmune Hashimoto's thyroiditis (HT).
Methodology. This study was carried out in a group of 153 individuals. The group of women participating in the study consisted of 109 individuals (71.24%), while the group of men consisted of 44 individuals (28.76%). All persons were divided into two groups: 1) euthyroidism (n = 64; men – n = 18, and women – n = 46); and 2) Hashimoto's autoimmune thyroiditis with subclinical hypothyroidism (n = 89; men – n = 26, and women – n = 63). The functioning of the thyroid gland was additionally verified by measuring the concentration of thyrotropin (TSH), free triiodothyronine (fT3), free tetraiodothyronine (thyroxine, fT4), and antibodies against thyroid peroxidase (anti-TPO). The concentration of thyrotropin, triiodothyronine, free thyroxine and the concentration of antibodies against thyroperoxidase in human serum were determined using the electrochemiluminescence method "ECLIA" on the immunological analyzer Elecsys Cobas e 411 (Hitachi, Japan). In each group of women and men with euthyroidism and Hashimoto's autoimmune thyroiditis with subclinical hypothyroidism, the 2-thiobarbituric acid reactive substances (TBARS), carbonyl derivatives of protein oxidative modification (OMP), and total antioxidant capacity (TAC) were determined.
Scientific novelty. Statistically significant changes in levels of oxidative stress markers were not observed. In women with HT, elevated TBARS levels with simultaneously increased TAC levels in the plasma and erythrocytes were observed. Additionally, levels of aldehydic and ketonic derivatives of oxidative modification of proteins in the blood of women with HT were lower compared to the women with the euthyroid state. In men with HT, levels of markers of oxidative stress (except TAC levels in the plasma) were lower compared to those obtained in men with the euthyroid state.
Conclusions. Hashimoto's thyroiditis with subclinical hypothyroidism does not have a direct influence on levels of biomarkers of lipid and protein oxidation. The results obtained in the current study highlight the need for future investigations of biomarkers of lipid and protein oxidation, especially depending on the duration of this disease.
Downloads
References
Antonelli, A., Ferrari, S. M., Corrado, A., Di Domenicantonio, A., & Fallahi, P. (2015). Autoimmune thyroid disorders. Autoimmunity reviews, 14(2), 174–180. https://doi.org/10.1016/j.autrev.2014.10.016
Ates, I., Arikan, M. F., Altay, M., Yilmaz, F. M., Yilmaz, N., Berker, D., & Guler, S. (2018). The effect of oxidative stress on the progression of Hashimoto's thyroiditis. Archives of physiology and biochemistry, 124(4), 351–356. https://doi.org/10.1080/13813455.2017.1408660
Ates, I., Yilmaz, F. M., Altay, M., Yilmaz, N., Berker, D., & Güler, S. (2015). The relationship between oxidative stress and autoimmunity in Hashimoto's thyroiditis. European journal of endocrinology, 173(6), 791–799. https://doi.org/10.1530/EJE-15-0617
Barreiro Arcos, M. L., Gorelik, G., Klecha, A., Genaro, A. M., & Cremaschi, G. A. (2006). Thyroid hormo¬nes increase inducible nitric oxide synthase gene expression downstream from PKC-zeta in murine tumor T lymphocytes. American journal of physiology. Cell physiology, 291(2), C. 327–336. https:// doi.org/10.1152/ajpcell.00316.2005
Burton, G. J., & Jauniaux, E. (2011). Oxidative stress. Best practice & research. Clinical obstetrics & gynaecology, 25(3), 287–299. https://doi.org/10.1016/j.bpobgyn.2010.10.016
Carvalho, D. P., & Dupuy, C. (2013). Role of the NADPH Oxidases DUOX and NOX4 in Thyroid Oxidative Stress. European thyroid journal, 2(3), 160–167. https://doi.org/10.1159/000354745
Chakrabarti, S. K., Ghosh, S., Banerjee, S., Mukherjee, S., & Chowdhury, S. (2016). Oxidative stress in hypothyroid patients and the role of antioxidant supplementation. Indian journal of endocrinology and metabolism, 20(5), 674–678. https://doi.org/10.4103/2230-8210.190555
Cheserek, M. J., Wu, G. R., Ntazinda, A., Shi, Y. H., Shen, L. Y., & Le, G. W. (2015). Association Between Thyroid Hormones, Lipids and Oxidative Stress Markers in Subclinical Hypothyroidism. Journal of medical biochemistry, 34(3), 323–331. https://doi.org/10.2478/jomb-2014-0044
Dissmeyer, N., Rivas, S., & Graciet, E. (2018). Life and death of proteins after protease cleavage: protein degradation by the N-end rule pathway. The New phytologist, 218(3), 929–935. https:// doi.org/ 10.1111/nph.14619
Dubinina, E. E., Burmistrov, S. O., Khodov, D. A., & Porotov, I. G. (1995). Oxidative modification of human serum proteins. A method of determining it. Voprosy meditsinskoi khimii, 41(1), 24–26. (in Russian)
Дубинина Е. Е., Бурмистров С. О., Ходов Д. А., Поротов И.Г. Окислительная модификация белков сыво¬ротки крови человека, метод ее определения. Вопросы медицинской химии. 1995. Т. 41, № 1. С. 24-26.
Erdamar, H., Cimen, B., Gülcemal, H., Saraymen, R., Yerer, B., & Demirci, H. (2010). Increased lipid peroxidation and impaired enzymatic antioxidant defense mechanism in thyroid tissue with multinodular goiter and papillary carcinoma. Clinical biochemistry, 43(7-8), 650–654. https://doi.org/ 10.1016/j.clinbiochem.2010.02.005
Franco, J.-S., Amaya-Amaya, J., & Anaya J.-M. (2013). Thyroid disease and autoimmune diseases. In Anaya J.M., Shoenfeld Y., Rojas-Villarraga A. et al. (Eds), Autoimmunity: From Bench to Bedside (Chapter 30). El Rosario University Press. Available from: https://www.ncbi.nlm.nih.gov/books/ NBK459466/
Galaktionova, L.P., Molchanov, A.V., Elchaninova, S.A., & Varshavsky, B.Ya. (1998). Lipid peroxidation in patients with gastric and duodenal peptic ulcers. Klinicheskaia laboratornaia diagnostika, (6), 10–14. (in Russian)
Галактионова Л.П., Молчанов А.В., Ельчанинова С.А., Варшавский Б.Я. Состояние перекисного окисле¬ния у больных язвенной болезнью желудка и двенадцатиперстной кишки. Клиническая лабораторная диагностика. 1998. № 6. С. 10-14.
Grimsrud, P. A., Xie, H., Griffin, T. J., & Bernlohr, D. A. (2008). Oxidative stress and covalent modification of protein with bioactive aldehydes. The Journal of biological chemistry, 283(32), 21837–21841. https://doi.org/10.1074/jbc.R700019200
Haribabu, A., Reddy, V. S., Pallavi, C.h, Bitla, A. R., Sachan, A., Pullaiah, P., Suresh, V., Rao, P. V., & Suchitra, M. M. (2013). Evaluation of protein oxidation and its association with lipid peroxidation and thyrotropin levels in overt and subclinical hypothyroidism. Endocrine, 44(1), 152–157. https:// doi.org/10.1007/s12020-012-9849-y
Hollowell, J. G., Staehling, N. W., Flanders, W. D., Hannon, W. H., Gunter, E. W., Spencer, C. A., & Braverman, L. E. (2002). Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). The Journal of clinical endocrinology and metabolism, 87(2), 489–499. https://doi.org/10.1210/jcem.87.2.8182
Huh, K., Kwon, T. H., Kim, J. S., & Park, J. M. (1998). Role of the hepatic xanthine oxidase in thyroid dysfunction: effect of thyroid hormones in oxidative stress in rat liver. Archives of pharmacal research, 21(3), 236–240. https://doi.org/10.1007/BF02975281
Kamel, A., & Hamouli-Said, Z. (2018). Neonatal exposure to T3 disrupts male reproductive functions by altering redox homeostasis in immature testis of rats. Andrologia, 50(9), e13082. https://doi.org/ 10.1111/and.13082
Kamyshnikov, V. S. (2004). A reference book on clinical and biochemical research and laboratory diagnostics (2nd ed.). MEDpress-inform. (in Russian)
Камышников В.С. Справочник по клинико-биохимическим исследованиям и лабораторной диагностике. Москва: Изд. «МЕДпресс-информ», 2004. 920 с.
Khan, F. A., Al-Jameil, N., Khan, M. F., Al-Rashid, M., & Tabassum, H. (2015). Thyroid dysfunction: an autoimmune aspect. International journal of clinical and experimental medicine, 8(5), 6677–6681.
Kochman, J., Jakubczyk, K., Bargiel, P., & Janda-Milczarek, K. (2021). The Influence of Oxidative Stress on Thyroid Diseases. Antioxidants (Basel, Switzerland), 10(9), 1442. https://doi.org/10.3390/ antiox10091442
Kristensen, B. (2016). Regulatory B and T cell responses in patients with autoimmune thyroid disease and healthy controls. Danish medical journal, 63(2), B5177.
Lanni, A., Moreno, M., Lombardi, A., & Goglia, F. (2003). Thyroid hormone and uncoupling proteins. FEBS letters, 543(1-3), 5–10. https://doi.org/10.1016/s0014-5793(03)00320-x
Levine, R. L., Garland, D., Oliver, C. N., Amici, A., Climent, I., Lenz, A. G., Ahn, B. W., Shaltiel, S., & Stadtman, E. R. (1990). Determination of carbonyl content in oxidatively modified proteins. Methods in enzymology, 186, 464–478. https://doi.org/10.1016/0076-6879(90)86141-h
Lobo, V., Patil, A., Phatak, A., & Chandra, N. (2010). Free radicals, antioxidants and functional foods: Impact on human health. Pharmacognosy reviews, 4(8), 118–126. https://doi.org/10.4103/0973-7847.70902
Mancini, A., Di Segni, C., Raimondo, S., Olivieri, G., Silvestrini, A., Meucci, E., & Currò, D. (2016). Thyroid Hormones, Oxidative Stress, and Inflammation. Mediators of inflammation, 2016, 6757154. https://doi.org/10.1155/2016/6757154
Marrocco, I., Altieri, F., & Peluso, I. (2017). Measurement and Clinical Significance of Biomarkers of Oxidative Stress in Humans. Oxidative medicine and cellular longevity, 2017, 6501046. https:// doi.org/10.1155/2017/6501046
Mikoś, H., Mikoś, M., Obara-Moszyńska, M., & Niedziela, M. (2014). The role of the immune system and cytokines involved in the pathogenesis of autoimmune thyroid disease (AITD). Endokrynologia Polska, 65(2), 150–155. https://doi.org/10.5603/EP.2014.0021
Mikulska, A. A., Karaźniewicz-Łada, M., Filipowicz, D., Ruchała, M., & Główka, F. K. (2022). Metabolic Characteristics of Hashimoto's Thyroiditis Patients and the Role of Microelements and Diet in the Disease Management – An Overview. International journal of molecular sciences, 23(12), 6580. https://doi.org/10.3390/ijms23126580
Morawska, K., Maciejczyk, M., Popławski, Ł., Popławska-Kita, A., Kretowski, A., & Zalewska, A. (2020). Enhanced Salivary and General Oxidative Stress in Hashimoto's Thyroiditis Women in Euthyreosis. Journal of clinical medicine, 9(7), 2102. https://doi.org/10.3390/jcm9072102
Nekrasova, T. A., Shcherbatyuk, T. G., Davydenko, D. V., Ledentsova, O. V., & Strongin, L. G. (2011). Peculiarities of lipid and protein peroxidation in autoimmune thyroiditis with and without mild thyroid dysfunction. Clinical and experimental thyroidology, 7(4):38-43. (in Russian)
Некрасова Т. А., Щербатюк Т. Г., Давыденко Д. В., Леденцова О. В., Стронгин Л. Г. Особенности перекисного окисления липидов и белков при аутоиммунном тиреоидите с легкой степенью нарушения функции щитовидной железы и без нее. Клиническая и экспериментальная тиреоидология. 2011. Вып.7, №4. С. 38-43.
Ohye, H., & Sugawara, M. (2010). Dual oxidase, hydrogen peroxide and thyroid diseases. Experimental biology and medicine (Maywood, N.J.), 235(4), 424–433. https://doi.org/10.1258/ebm.2009.009241
Öztürk, Ü., Vural, P., Özderya, A., Karadağ, B., Doğru-Abbasoğlu, S., & Uysal, M. (2012). Oxidative stress parameters in serum and low density lipoproteins of Hashimoto's thyroiditis patients with subclinical and overt hypothyroidism. International immunopharmacology, 14(4), 349–352. https://doi.org/10.1016/j.intimp.2012.08.010
Papadopoulou, A. M., Bakogiannis, N., Skrapari, I., Moris, D., & Bakoyiannis, C. (2020). Thyroid Dysfunction and Atherosclerosis: A Systematic Review. In vivo (Athens, Greece), 34(6), 3127–3136. https://doi.org/10.21873/invivo.12147
Phaniendra, A., Jestadi, D. B., & Periyasamy, L. (2015). Free radicals: properties, sources, targets, and their implication in various diseases. Indian journal of clinical biochemistry: IJCB, 30(1), 11–26. https://doi.org/10.1007/s12291-014-0446-0
Ralli, M., Angeletti, D., Fiore, M., D'Aguanno, V., Lambiase, A., Artico, M., de Vincentiis, M., & Greco, A. (2020). Hashimoto's thyroiditis: An update on pathogenic mechanisms, diagnostic protocols, therapeutic strategies, and potential malignant transformation. Autoimmunity reviews, 19(10), 102649. https://doi.org/10.1016/j.autrev.2020.102649
Rocchi, R., Rose, N.R., & Caturegli, P. (2008). Hashimoto Thyroiditis. In: Shoenfeld Y., Cervera R., & Gershwin M.E. (Eds.), Diagnostic Criteria in Autoimmune Diseases (pp. 217–220). Humana Press.
Rovcanin, B. R., Gopcevic, K. R., Kekic, D. L.j, Zivaljevic, V. R., Diklic, A. D.j, & Paunovic, I. R. (2016). Papillary Thyroid Carcinoma: A Malignant Tumor with Increased Antioxidant Defense Capacity. The Tohoku journal of experimental medicine, 240(2), 101–111. https://doi.org/10.1620/tjem.240.101
Ruggeri, R. M., Giovinazzo, S., Barbalace, M. C., Cristani, M., Alibrandi, A., Vicchio, T. M., Giuffrida, G., Aguennouz, M. H., Malaguti, M., Angeloni, C., Trimarchi, F., Hrelia, S., Campennì, A., & Cannavò, S. (2021). Influence of Dietary Habits on Oxidative Stress Markers in Hashimoto's Thyroiditis. Thyroid: official journal of the American Thyroid Association, 31(1), 96–105. https://doi.org/10.1089/thy. 2020.0299
Rybakova, A. A., Platonova, N. M., & Troshina, E. A. (2020). Oxidative stress and its role in the deve-lopment of autoimmune thyroid diseases. Problems of Endocrinology, 65(6), 451–457. https://doi.org/ 10.14341/probl11827 (in Russian)
Рыбакова А.А., Платонова Н.М., Трошина Е.А. Оксидативный стресс и его роль в развитии ауто-иммунных заболеваний щитовидной железы. Проблемы эндокринологии. 2020. Вып. 65, №6. С. 451-457.
Santi, A., Duarte, M. M., de Menezes, C. C., & Loro, V. L. (2012). Association of lipids with oxidative stress biomarkers in subclinical hypothyroidism. International journal of endocrinology, 2012, 856359. https://doi.org/10.1155/2012/856359
Szanto, I., Pusztaszeri, M., & Mavromati, M. (2019). H2O2 Metabolism in Normal Thyroid Cells and in Thyroid Tumorigenesis: Focus on NADPH Oxidases. Antioxidants (Basel, Switzerland), 8(5), 126. https://doi.org/10.3390/antiox8050126
Tapia, G., Fernández, V., Varela, P., Cornejo, P., Guerrero, J., & Videla, L. A. (2003). Thyroid hormone-induced oxidative stress triggers nuclear factor-kappaB activation and cytokine gene expression in rat liver. Free radical biology & medicine, 35(3), 257–265. https://doi.org/10.1016/s0891-5849(03) 00209-0
Torun, A. N., Kulaksizoglu, S., Kulaksizoglu, M., Pamuk, B. O., Isbilen, E., & Tutuncu, N. B. (2009). Serum total antioxidant status and lipid peroxidation marker malondialdehyde levels in overt and subclinical hypothyroidism. Clinical endocrinology, 70(3), 469–474. https://doi.org/10.1111/j.1365-2265.2008.03348.x
Venditti, P., Balestrieri, M., Di Meo, S., & De Leo, T. (1997). Effect of thyroid state on lipid peroxidation, antioxidant defences, and susceptibility to oxidative stress in rat tissues. The Journal of endocrinology, 155(1), 151–157. https://doi.org/10.1677/joe.0.1550151
Venditti, P., Daniele, M. C., Masullo, P., & Di Meo, S. (1999). Antioxidant-sensitive triiodothyronine effects on characteristics of rat liver mitochondrial population. Cellular physiology and biochemistry: international journal of experimental cellular physiology, biochemistry, and pharmacology, 9(1), 38–52. https://doi.org/10.1159/000016301
Villanueva, I., Alva-Sánchez, C., & Pacheco-Rosado, J. (2013). The role of thyroid hormones as inductors of oxidative stress and neurodegeneration. Oxidative medicine and cellular longevity, 2013, 218145. https://doi.org/10.1155/2013/218145
Zamoner, A., Barreto, K. P., Filho, D. W., Sell, F., Woehl, V. M., Guma, F. C., Silva, F. R., & Pessoa-Pureur, R. (2007). Hyperthyroidism in the developing rat testis is associated with oxidative stress and hyperphosphorylated vimentin accumulation. Molecular and cellular endocrinology, 267(1-2), 116–126. https://doi.org/10.1016/j.mce.2007.01.005
Zaninovich, A. A. (2005). Role of uncoupling proteins UCP1, UCP2 and UCP3 in energy balance, type 2 diabetes and obesity. Synergism with the thyroid. Medicine, 65(2), 163–169.
Занинович А. А. Роль разобщающих белков UCP1, UCP2 и UCP3 в энергетическом балансе, диабете 2 типа и ожирении. Синергизм с щитовидной железой. Медицина. 2005. Вып. 65, №2. С. 163-169.
Zar, J.H. (1999). Biostatistic Analysis. 4th ed. Prentice Hall Inc.
Zimmermann, M. B., & Boelaert, K. (2015). Iodine deficiency and thyroid disorders. The lancet. Diabetes & endocrinology, 3(4), 286–295. https://doi.org/10.1016/S2213-8587(14)70225-6
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Галина Ткаченко, Уршуля Осмульська, Наталія Кургалюк
This work is licensed under a Creative Commons Attribution 4.0 International License.
