Abstract
Purpose
To evaluate thiol/disulfide homeostasis in ocular-active (OA) and ocular-inactive (OI) Behçet disease (BD) patients and compare the data with healthy subjects.
Methods
Twenty OABD patients, 20 OIBD patients and 20 healthy control subjects were included into the study. The BD ocular attack score 24 (BOS24) scoring system was used to assess the activity of disease in ocular BD patients. Systemic activity was also evaluated using BD current activity form (BDCAF). The native thiol (NT), total thiol (TT) and disulfide levels and NT/TT, disulfide/NT and disulfide/TT ratios were measured via using an innovative and automated method.
Results
BOS24 and BDCAF scores were 13.25 ± 2.32 and 4.18 ± 2.06 in OABD patients and 0.31 ± 0.47 and 2.14 ± 1.98 in OIBD patients, respectively. The NT, TT levels and NT/TT ratio were significantly reduced; in contrast, the disulfide levels, disulfide/NT and disulfide/TT ratios were significantly increased in OABD and OIBD patients compared to the healthy control subjects (p < 0.05). Moreover, while the levels of NT and TT were significantly reduced, the disulfide levels as well as disulfide/NT and disulfide/TT ratios were significantly elevated between OABD and OIBD patients (p < 0.05). However, the ratio of NT/TT did not significantly differ between OABD and OIBD patients (p = 0.449). The multiple regression model including BOS24 and BDCAF score statistically significantly predicted NT level, TT level and disulfide level (p < 0.001 for all).
Conclusion
Thiol oxidation in BD patients resulted in a change of the thiol/disulfide balance. Therefore, thiol/disulfide homeostasis in BD patients can be used an innovative oxidative stress marker.
Similar content being viewed by others
References
Mendoza-Pinto C, Garcia-Carrasco M, Jimenez-Hernandez M et al (2010) Etiopathogenesis of Behçet’s disease. Autoimmun Rev 9:241–245. https://doi.org/10.1016/j.autrev.2009.10.005
Hirohata S, Kikuchi H (2003) Behçet’s disease. Arthritis Res Ther 5:139–146. https://doi.org/10.1186/ar757
Sepici Dinçel A, Özkan Y, Yardım-Akaydın S et al (2006) The association between total antioxidant status and oxidative stress in Behçet’s disease. Rheumatol Int 26:1005–1009. https://doi.org/10.1007/s00296-006-0126-3
Harzallah O, Kerkeni A, Baati T et al (2008) Oxidative stress: correlation with Behçet’s disease duration, activity and severity. Eur J Int Med 19:541–547. https://doi.org/10.1016/j.ejim.2008.08.001
Onur E, Kabaroglu C, Inanir I et al (2011) Oxidative stress impairs endothelial nitric oxide levels in Behçet’s disease. Cutan Ocul Toxicol 30:217–220. https://doi.org/10.3109/15569527.2011.554480
Cejkova J, Stipek S, Crkovska J et al (2004) UV rays, the pro-oxidant/anti-oxidant imbalance in the cornea and oxidative eye damage. Physiol Res 53:1–10
Biswas S, Chida AS, Rahman I (2006) Redox modifications of protein-thiols: emerging roles in cell signaling. Biochem Pharmacol 71:551–564. https://doi.org/10.1016/j.bcp.10.044
Turell L, Radi R, Alvarez B (2013) The thiol pool in human plasma: the central contribution of albumin to redox processes. Free Radic Biol Med 65:244–253. https://doi.org/10.1016/j.freeradbiomed.2013.05.050
Gulpamuk B, Tekin K, Sonmez K et al (2017) The significance of thiol/disulfide homeostasis and ischemia-modified albumin levels to assess the oxidative stress in patients with different stages of diabetes mellitus. Scand J Clin Lab Invest 78:136–142. https://doi.org/10.1080/00365513.2017.1422540
Go YM, Jones DP (2011) Cysteine/cystine redox signaling in cardiovascular disease. Free Radic Biol Med 50:495–509. https://doi.org/10.1016/j.freeradbiomed.2010.11.029
Tetik S, Ahmad S, Alturfan AA et al (2010) Determination of oxidant stress in plasma of rheumatoid arthritis and primary osteoarthritis patients. Indian J Biochem Biophys 47:353–358
Altinkaynak H, Kurkcuoglu PZ, Caglayan M et al (2018) A novel marker in acute central serous chorioretinopathy: thiol/disulfide homeostasis. Int Ophthalmol 38:175–181. https://doi.org/10.1007/s10792-017-0444-3
Arıkan Yorgun M, Toklu Y, Altınkaynak H et al (2016) A novel tool for the assessment oxidative stress in age-related macular degeneration: thiol/disulfide homeostasis revisited. Cur Eye Res 41:1584–1589. https://doi.org/10.3109/02713683.2016.1141965
Tanaka R, Murata H, Takamoto M et al (2016) Behçet’s disease ocular attack score 24 and visual outcome in patients with Behçet’s disease. Br J Ophthalmol 100:990–994. https://doi.org/10.1136/bjophthalmol-2015-307362
International Team for the revision of the International criteria for Behçet’s disease (ITR-ICBD) (2014) The International Criteria for Behçet’s disease (ICBD): a collaborative study of 27 countries on sensitivity and specificity of the new criteria. J Eur Acad Dermatol Venereol 28:338–347. https://doi.org/10.1111/jdv.12107
Lawton G, Bhakta BB, Chamberlain MA et al (2004) The Behçet’s disease activity index. Rheumatology (Oxford) 43:73–78. https://doi.org/10.1093/rheumatology/keg453
Erel O, Neselioglu S (2014) A novel and automated assay for thiol/disulphide homeostasis. Clin Biochem 47:326–332. https://doi.org/10.1016/j.clinbiochem.2014.09.026
Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog Lipid Res 43:200–227. https://doi.org/10.1016/j.plipres.2003.10.001
Therond P, Bonnefont-Rousselot D, Davit-Spraul A et al (2000) Biomarkers of oxidative stress: an analytical approach. Curr Opin Clin Nutr Metab Care 3:373–384. https://doi.org/10.1097/00075197-200009000-00009
Kokcam I, Nazıroglu M (2002) Effects of vitamin E supplementation on blood antioxidants levels in patients with Behcet’s disease. Clin Biochem 35:633–639. https://doi.org/10.1016/s0009-9120(02)00400-9
Yazici C, Kose K, Calis M et al (2004) Increased advanced oxidation protein products in Behcet’s disease: a new activity marker. Br J Dermatol 151(July):105. https://doi.org/10.1011/j.1365-2133-2004.06003.x
Bekpinar S, Kilic N, Unlucerci Y et al (2005) Evaluation of nitrosative and oxidative stress in Behcet disease. J Eur Acad Dermatol Venereol 19:167–171. https://doi.org/10.1111/j.1468-3083.2005.01075.x
Atmaca G (2004) Antioxidant effects of sulfur-containing amino acids. Yonsei Med J 45:776–788. https://doi.org/10.3349/ymj.2004.45.5.776
Halliwell B, Whiteman M (2004) Measuring RS and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142:231–255. https://doi.org/10.1038/sj.bjp.070.5776
Emmi G, Silvestri E, Squatrito D et al (2014) Behçet’s syndrome pathophysiology and potential therapeutic targets. Intern Emerg Med 9:257–265. https://doi.org/10.1007/s11739-013-1036-5
Niwa Y, Miyake S, Sakane T (1982) Autooxidative damage in Behçet’s disease- endothelial cell damage following the elevated oxygen radicals generated by stimulated neutrophils. Clin Exp Immunol 49:247–255
Chambers JC, Haskard DO, Kooner JS (2001) Vascular endothelial function and oxidative stress mechanisms in patients with Behçet’s syndrome. Am J Coll Cardiol 37:417–420. https://doi.org/10.1016/s735-1097(00)01137-2
Funding
No financial support was received for this study.
Author information
Authors and Affiliations
Contributions
MB contributed to concept, design, intellectual content and drafted the article. FU contributed to design, concept and statistical analysis. HY acquired data and interpreted data. AS contributed to data analysis and intellectual content. AD acquired data, drafted the article and interpreted data. SA contributed to data analysis.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of Fırat University Faculty of Medicine ethics committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Balbaba, M., Ulaş, F., Yıldırım, H. et al. Thiol/disulfide homeostasis in patients with ocular-active and ocular-inactive Behçet disease. Int Ophthalmol 40, 2643–2650 (2020). https://doi.org/10.1007/s10792-020-01445-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10792-020-01445-x