Changes in hepatic thiol contents and regulation of glutathione S-transferase by high-fructose diet: Effects of kefir and some probiotic bacteria
Abstract views: 198
/ 
PDF downloads: 185
DOI:
https://doi.org/10.26900/hsq.1942Keywords:
Kefir, Lactobacillus plantarum, Lactobacillus helveticus, glutathione S-transferase, thiol/disulfide balance, fructoseAbstract
In this study, thiol/disulfide homeostasis in the liver tissues of high-fructose-fed rats was investigated in conjunction with the changes in the main hepatic detoxification enzyme, glutathione S-transferase (GST). Additionally, the effects of well-known probiotics namely Kefir, Lactobacillus helveticus, and Lactobacillus plantarum supplementation on the thiol/disulfate contents and GST activity and gene expression levels were analyzed. Fructose, administered as a 20% solution in drinking water for 15 weeks, developed an animal model of metabolic syndrome in male Wistar rats. Kefir, L. helveticus, and L. plantarum supplementations were given by gastric gavage once a day during the final 6-weeks. The changes in hepatic GST were determined with kinetic-optimized spectrophotometric enzyme assays and qRT-PCR. Total thiol, native thiol, and disulfide levels were analyzed using (5,5-dithio-bis-(2-nitrobenzoic acid) as a chromogenic agent. High-fructose consumption reduced total and native thiol contents while increasing disulfide levels in the liver tissues of rats. Kefir and L. plantarum normalized the thiol levels and all probiotics reduced disulfide contents. High fructose augmented total GST activity but reduced the GST-Mu isoform. L. helveticus and L. plantarum normalized the total and GST-Mu activity, respectively. These results demonstrated a shift toward disulfide formation in the hepatic tissues of rats fed with high fructose. A possible reason would be the increase in total GST activity that uses the free glutathione, the main native thiol source in cells, as a substrate. Besides, probiotics such as Kefir, L. helveticus, and L. plantarum have an improving effect on thiol/disulfide homeostasis as well as main detoxification enzymes.
Downloads
References
Johnson RJ, Segal MS, Sautin Y, Nakagawa T, Feig DI, Kang D-H, et al. Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am J Clin Nutr. 2007;86(4):899-906. doi: 10.1093/ajcn/86.4.899.
Miller A, Adeli K. Dietary fructose and the metabolic syndrome. Curr Opin Gastroenterol. 2008;24(2):204-9. doi: 10.1097/MOG.0b013e3282f3f4c4.
Zhang DM, Jiao RQ, Kong LD. High dietary fructose: Direct or indirect dangerous factors disturbing tissue and organ functions. Nutrients. 2017;9(4):335. doi: 10.3390/nu9040335.
Roberts CK, Sindhu KK. Oxidative stress and metabolic syndrome. Life Sci. 2009;84(21-22):705-12. doi: 10.1016/j.lfs.2009.02.026.
Kelley GL, Allan G, Azhar S. High dietary fructose induces a hepatic stress response resulting in cholesterol and lipid dysregulation. Endocrinology. 2004;145(2):548-55. doi: 10.1210/en.2003-1167.
Vona R, Gambardella L, Cittadini C, Straface E, Pietraforte D. Biomarkers of oxidative stress in metabolic syndrome and associated diseases. Oxidative Medicine and Cellular Longevity. 2019.p.1-19. doi: 10.1155/2019/8267234.
Spahis S, Borys JM, Levy E. Metabolic syndrome as a multifaceted risk factor for oxidative stress. Antioxidants Redox Signal. 2017;26(9):445-61. doi: 10.1089/ars.2016.6756.
Grandl G, Wolfrum C. Hemostasis, endothelial stress, inflammation, and the metabolic syndrome. Seminars in Immunopathology. 2018;40:215-224.doi: 10.1007/s00281-017-0666-5.
Mungli P, Shetty MS, Tilak P, Anwar N. Total thiols: Biomedical importance and their alteration in various disorders. Online J Heal Allied Sci. 2009;8(2):1-9. url: http://www.ojhas.org/issue30/2009-2-2.htm.
Lohning AE, Salinas AE. Glutathione S-transferases--a review. Curr Med Chem. 1999;6:279-309. doi:10.2174/0929867306666220208213032.
Markowiak P, Ślizewska K. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients; 2017;9(9):1021. doi: 10.3390/nu9091021.
Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, et al. Antioxidant properties of probiotic bacteria. Nutrients. 2017;9(5):521. doi: 10.3390/nu9050521.
Yakovlieva M, Tacheva T, Mihaylova S, Tropcheva R, Trifonova K, Toleкova A, et al. Influence of Lactobacillus brevis 15 and Lactobacillus plantarum 13 on blood glucose and body weight in rats after high-fructose diet. Benef Microbes. 2015;6(4):505-12. doi: 10.3920/BM2014.0012.
Sumlu E, Bostancı A, Sadi G, A ME, Akar F. Lactobacillus plantarum improves lipogenesis and IRS-1/AKT/eNOS signalling pathway in the liver of high-fructose-fed rats. Arch Physiol Biochem. 2022;128(3):786-94. doi: 10.1080/13813455.2020.1727527.
Korkmaz OA, Sumlu E, Koca HB, Pektas MB, Kocabas A, Sadi G, et al. Effects of Lactobacillus plantarum and Lactobacillus helveticus on renal insulin signaling, inflammatory markers, and glucose transporters in high-fructosefed rats. Med. 2019;55(5):207. doi: 10.3390/medicina55050207.
Ahn HY, Kim M, Chae JS, Ahn YT, Sim JH, Choi ID, et al. Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduces fasting triglycerides and enhances apolipoprotein A-V levels in nondiabetic subjects with hypertriglyceridemia. Atherosclerosis. 2015;241(2):649-56. doi: 10.1016/j.atherosclerosis.2015.06.030.
Korkmaz ÖA, Sadi G, Kocabaş A, Yildirim OG, Sumlu E, Koca HB, et al. Lactobacillus helveticus and Lactobacillus plantarum modulate renal antioxidant status in a rat model of fructoseinduced metabolic syndrome. Arch Biol Sci. 2019;71(2):265–73. doi: 10.2298/abs190123008k.
Kim DH, Jeong D, Kim H, Seo KH. Modern perspectives on the health benefits of kefir in next generation sequencing era: Improvement of the host gut microbiota. Critical Reviews in Food Science and Nutrition. 2018;59(11):1782-93. doi: 10.1080/10408398.2018.1428168.
Rosa DD, Grześkowiak LM, Ferreira CLLF, Fonseca ACM, Reis SA, Dias MM, et al. Kefir reduces insulin resistance and inflammatory cytokine expression in an animal model of metabolic syndrome. Food Funct. 2016;7(8):3390-401. doi: 10.1039/C6FO00339G.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem.1951;193(1):265-75. doi: 10.1016/S0021-9258(19)52451-6.
Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974;249(22):7130-9. doi: 10.1016/S0021-9258(19)42083-8.
Kütük A, Sadi G. Inhibitory effects of Armillaria mellea (Vahl) P. Kumm. on liver glutathione S-transferase activity. Anatol J Bot. 2020;4(1):1-7. doi: 10.30616/ajb.690005.
Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82(1):70-77. doi: 10.1016/0003-9861(59)90090-6.
Ellman G, Lysko H. A precise method for the determination of whole blood and plasma sulfhydryl groups. Anal Biochem. 1979;93:98-102. doi: 10.1016/S0003-2697(79)80122-0.
Hu ML. Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol. 1994;233:380-5. doi: 10.1016/S0076-6879(94)33044-1.
Alışık M. A colorimetric method to measure oxidized, reduced and total glutathione levels in erythrocytes. J Lab Med. 2019;43(5):269-277. doi: 10.1515/labmed-2019-0098.
Erel O, Neselioglu S. A novel and automated assay for thiol/disulphide homeostasis. Clin Biochem. 2014;47(18):326-32. doi: 10.1016/j.clinbiochem.2014.09.026.
Bostancı A, Sencan EN, Kütük A, Sadi G. Differential regulation of antioxidant enzymes by resveratrol in healthy and cancerous hepatocytes. Anatol J Bot. 2022;6(2):62-8. doi: 10.30616/ajb.1103463.
Akar F, Sumlu E, Alçığır ME, Bostancı A, Sadi G. Potential mechanistic pathways underlying intestinal and hepatic effects of kefir in highfructose-fed rats. Food Res Int. 2021;143:110287. doi: 10.1016/j.foodres.2021.110287.
Croom E. Metabolism of xenobiotics of human environments. Prog Mol Biol Transl Sci. 2012;112:31-88. doi: 10.1016/B978-0-12-415813-9.00003-9.
Tappy L, Lê KA. Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev. 2010;90(1):23-46. doi: 10.1152/physrev.00019.2009.
Castro MC, Massa ML, Arbeláez LG, Schinella G, Gagliardino JJ, Francini F. Fructose-induced inflammation, insulin resistance and oxidative stress: A liver pathological triad effectively disrupted by lipoic acid. Life Sci. 2015;137:1-6. doi: 10.1016/j.lfs.2015.07.010.
Baba SP, Bhatnagar A. Role of thiols in oxidative stress. Curr Opin Toxicol. 2018(7):133-139. doi: 10.1016/j.cotox.2018.03.005.
Meyer AJ. The integration of glutathione homeostasis and redox signaling. J Plant Physiol. 2008;165(13):1390-1403. doi: 10.1016/j.jplph.2007.10.015.
Sadi G, Kartal DI, Güray T. Regulation of glutathione S-transferase mu with type 1 diabetes and its regulation with antioxidants. Turkish J Biochem. 2013;38(1):106-14. doi: 10.5505/tjb.2013.96720.
Marí M, Cederbaum AI. Induction of catalase, alpha, and microsomal glutathione S-transferase in CYP2E1 overexpressing HepG2 cells and protection against short-term oxidative stress. Hepatology. 2001;33(3):652-61. doi: 10.1053/jhep.2001.22521.
Yang Y, Cheng JZ, Singhal SS, Saini M, Pandya U, Awasthi S, et al. Role of glutathione S-transferases in protection against lipid peroxidation. Overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation. J Biol Chem. 2001;276(22):19220-30. doi: 10.1074/jbc.M100551200.
Vargas-Blanco DA, Shell SS. Regulation of mRNA stability during bacterial stress responses. Frontiers in Microbiology.Frontiers Media SA;2020(11):2111. doi: 10.3389/fmicb.2020.02111.
Vieira CP, Rosario AILS, Lelis CA, Rekowsky BSS, Carvalho APA, Rosário DKA, et al. Bioactive compounds from kefir and their potential benefits on health: A systematic review and metaanalysis. Oxid Med Cell Longev. 2021:1-34. doi: 10.1155/2021/9081738.
Lutgendorff F, Trulsson LM, Van Minnen LP, Rijkers GT, Timmerman HM, Franzén LE, et al. Probiotics enhance pancreatic glutathione biosynthesis and reduce oxidative stress in experimental acute pancreatitis. Am J Physiol - Gastrointest Liver Physiol. 2008; 295(5):1111-21. doi: 10.1152/ajpgi.00603.2007.
Lutgendorff F, Nijmeijer RM, Sandström PA, Trulsson LM, Magnusson KE, Timmerman HM, et al. Probiotics prevent intestinal barrier
dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis. PLoS One. 2009;4(2):e4512. doi: 10.1371/journal.pone.0004512.
Peran L, Camuesco D, Comalada M, Bailon E, Henriksson A, Xaus J, et al. A comparative study of the preventative effects exerted by three probiotics, Bifidobacterium lactis, Lactobacillus casei and Lactobacillus acidophilus, in the TNBS model of rat colitis. J Appl Microbiol. 2007;103(4):836-44. doi: 10.1017/S0007114507257770
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Holistence Publications
This work is licensed under a Creative Commons Attribution 4.0 International License.
When the article is accepted for publication in the HSQ authors transfer all copyright in the article to the Holistence Academy Ar-Ge Yazılım Yayıncılık Eğitim Danışmanlık ve Organizasyon Ticaret Ltd. Şti.The authors reserve all proprietary right other than copyright, such as patent rights.
Everyone who is listed as an author in this article should have made a substantial, direct, intellectual contribution to the work and should take public responsibility for it.
This paper contains works that have not previously published or not under consideration for publication in other journals.
