Abstract
The stomach is among the organs grossly affected organ by diabetic complications. The present study was aimed at investigating the protective role of zinc on stomach of streptozotocin (STZ)-induced diabetes mellitus. Female Swiss albino rats were divided in four experimental groups: Group I, control; group II, control + zinc sulfate; group III, STZ-induced diabetic animals; and group IV, STZ-diabetic + zinc sulfate. Diabetes was induced by intraperitoneal injection of STZ, at a dose of 65 mg/kg body weight. Zinc sulfate (100 mg/kg body weight) was given daily by gavage for 60 days to groups II and IV. At the end of the experiment, the rats were sacrificed, and the tissues were taken. In the diabetic group, hexose, hexosamine, fucose, and sialic acid levels, as well as tissue factor, adenosine deaminase, carbonic anhydrase, xanthine oxidase, lactate dehydrogenase, prolidase activities, advanced oxidized protein products, homocysteine, and TNF-α levels were increased in the stomach tissue homogenates. Whereas, catalase, superoxide dismutase, glutathione-S-transferase, glutathione peroxidase, glutathione reductase, paraoxonase, and aryl esterase activities were decreased in the diabetic group. The administration of zinc reversed all the deformities. These findings suggest that zinc has protective role in ameliorating several mechanisms of STZ-induced diabetic stomach injury.
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References
Yilmaz-Ozden T, Kurt-Sirin O, Tunali S, Akev N, Can A, Yanardag R (2014) Ameliorative effect of vanadium on oxidative stress in stomach tissue of diabetic rats. Bosn J Basic Med Sci 14:105–109 https://www.bjbms.org/ojs/index.php/bjbms/article/view/2273
AlFaris NA, Alshammari GM, Alsayadi MM, AlFaris MA, Yahya MA (2020) Antidiabetic and antihyperlipidemic effect of Duvalia corderoyi in rats with streptozotocin-induced diabetes. Saudi J Biol Sci 27:925–934. https://doi.org/10.1016/j.sjbs.2020.01.024
Gezginci-Oktayoglu S, Sacan O, Bolkent S, Ipci Y, Kabasakal L, Sener G, Yanardag R (2014) Chard (Beta vulgaris L. var. cicla) extract ameliorates hyperglycemia by increasing GLUT2 through Akt2 and antioxidant defense in the liver of rats. Acta Histochem 116:32–39. https://doi.org/10.1016/j.acthis.2013.04.016
Gülçin İ (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391. https://doi.org/10.1007/s00204-011-0774-2
Taslimi P, Gulçin İ (2018) Antioxidant and anticholinergic properties of olivetol. J Food Biochem 42:e12516. https://doi.org/10.1111/jfbc.12516
Gulcin İ (2020) Antioxidants and antioxidant methods-an updated overview. Arch Toxicol 94:651–715. https://doi.org/10.1007/s00204-020-02689-3
Sacan O, Turkyilmaz IB, Bayrak BB, Mutlu O, Akev N, Yanardag R (2016) Zinc supplementation ameliorates glycoprotein components and oxidative stress changes in the lung of streptozotocin diabetic rats. Biometals 29:239–248. https://doi.org/10.1007/s10534-016-9911-y
Lucchesi AN, Freitas NTD, Cassettari LL, Marques SFG, Spadella CT (2013) Diabetes mellitus triggers oxidative stress in the liver of alloxan-treated rats: a mechanism for diabetic chronic liver disease. Acta Cir Bras 28:502–508. https://doi.org/10.1590/S0102-86502013000700005
Fatmi W, Kechrid Z, Nazıroğlu M, Flores-Arce M (2013) Selenium supplementation modulates zinc levels and antioxidant values in blood and tissues of diabetic rats fed zinc-deficient diet. Biol Trace Elem Res 152:243–250. https://doi.org/10.1007/s12011-013-9613-z
Lemaire K, Chimienti F, Schuit F (2012) Zinc transporters and their role in the pancreatic β-cell. J Diabetes Invest 3:202–211. https://doi.org/10.1111/j.2040-1124.2012.00199.x
Bray TM, Betteger W (1990) The physiological role of zinc as an antioxidant. Free Radic Biol Med 8:281–291. https://doi.org/10.1016/0891-5849(90)90076-U
Junod A, Lambert AE, Stauffacher W, Renold AE (1969) Diabetogenic action of streptozotocin: relationship of dose to metabolic response. J Clin Invest 48:2129–2139 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC297467/
Bolkent S, Yanardag R, Bolkent S, Mutlu O, Yildirim S, Kangawa K, Minegishi Y, Suzuki H (2006) The effect of zinc supplementation on ghrelin-immunoreactive cells and lipid parameters in gastrointestinal tissue of streptozotocin-induced female diabetic rats. Mol Cell Biochem 286:77–85. https://doi.org/10.1007/s11010-005-9095-1
Winzler RJ (1955) Determination of serum glycoproteins. Methods Biochem Anal 2:279. https://doi.org/10.1002/9780470110188.ch10
Dische Z, Shettles LB (1948) A specific color reaction of methylpentoses and a spectrophotometric micromethod for their determination. J Biol Chem 175:595–603 https://pubmed.ncbi.nlm.nih.gov/18880756/
Lorentz K, Weiss T, Kraas E (1986) Sialic acid in human serum and cerebrospinal fluid. Comparison of methods and reference values. J Clin Chem Clin Biochem 24:189–198. https://doi.org/10.1515/cclm.1986.24.3.189
Ingram GI, Hills M (1976) Reference method for the one-stage prothrombin time test on human blood. Thromb Haemost 36:237–238 https://pubmed.ncbi.nlm.nih.gov/1036814/
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Mylroie AA, Colins H, Umbles C, Kyle J (1986) Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 82:512–520. https://doi.org/10.1016/0041-008X(86)90286-3
Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405. https://doi.org/10.1016/S0076-6879(81)77053-8
Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169 https://pubmed.ncbi.nlm.nih.gov/6066618/
Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333. https://doi.org/10.1016/S0076-6879(81)77046-0
Beutler E (1971) Red cell metabolism, a manual of biochemical methods, vol 12. Academic Press, London, pp 68–70
Furlong CE, Richter RJ, Seidel SL, Motulsky AG (1988) Role of genetic polymorphism of human plasma paraoxonase/arylesterase in hydrolysis of the insecticide metabolites chlorpyrifos oxon and paraoxon. Am J Hum Genet 43:230–238 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1715392/
Gan KN, Smolen A, Eckerson HW, La Du BN (1991) Purification of human serum paraoxonase/arylesterase. Evidence for one esterase catalyzing both activities. Drug Metab Dispos 19:100–106 https://pubmed.ncbi.nlm.nih.gov/1673382/
Karker H (1964) Method for estimation of serum adenosine deaminase. Scand J Clin Lab Invest 16:570–574. https://doi.org/10.3109/00365516409060557
Verpoorte JA, Mehta S, Edsall JT (1967) Esterase activities of human carbonic anhydrases B and C. J Biol Chem 242:4221–4229 https://pubmed.ncbi.nlm.nih.gov/4964830/
Corte ED, Stirpe F (1968) Regulation of xanthine oxidase in rat liver: modifications of the enzyme activity of rat liver supernatant on storage at 20 degrees. Biochem J 108:349–351. https://doi.org/10.1042/bj1080349
Wroblewski F (1957) Clinical significance of serum enzyme alterations associated with myocardial infarction. Am Heart J 54:219–224. https://doi.org/10.1016/0002-8703(57)90149-7
Chinard FP (1952) Photometric estimation of proline and ornithine. J Biol Chem 199:91–95 https://www.jbc.org/content/199/1/91.full.pdf
Witko-Sarsat V, Friedlander M, Capeillère-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, Jungers P, Descamps-Latscha B (1996) Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 49:1304–1313. https://doi.org/10.1038/ki.1996.186
Lowry OH, Rosebrough HJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275 https://pubmed.ncbi.nlm.nih.gov/14907713/
Norouzi S, Adulcikas J, Singh Sohal S, Myers S (2018) Zinc stimulates glucose oxidation and glycemic control by modulating the insulin signaling pathway in human and mouse skeletal muscle cell lines. PLoS One 13:e0191727. https://doi.org/10.1371/journal.pone.0191727.g001
Duraisamy G, Ganesan R, Manokaran K, Kanakasabapathi D, Chandrasekar U (2013) Protective effect of the whole plant extract of Evolvulus alsinoides on glycoprotein alterations in streptozotocin induced diabetic rats. J Acute Dis 2:148–150. https://doi.org/10.1016/S2221-6189(13)60116-X
Sambola A, Osende J, Hathcock J, Degen M, Nemerson Y, Fuster V, Crandall J, Badimon JJ (2003) Role of risk factors in the modulation of tissue factor activity and blood thrombogenicity. Circulation 107:973–977. https://doi.org/10.1161/01.CIR.0000050621.67499.7D
Turkyilmaz IB, Coskun ZM, Bolkent S, Yanardag R (2019) The effects of antioxidant combination on indomethacin-induced gastric mucosal injury in rats. Cell Mol Biol 65:76–83. https://doi.org/10.14715/cmb/2019.65.3.11
Fujimaki S, Kuwabara T (2017) Diabetes-induced dysfunction of mitochondria and stem cells in skeletal muscle and the nervous system. Int J Mol Sci 18:2147. https://doi.org/10.3390/ijms18102147
Coskun ZM, Sacan O, Karatug A, Yanardag R, Bolkent S, Bolkent S (2013) Regulation of oxidative stress and somatostatin, cholecystokinin, apelin gene expressions by ghrelin in stomach of newborn diabetic rats. Acta Histochem 115:740–747. https://doi.org/10.1016/j.acthis.2013.03.001
Kotur-Stevuljević J, Vekić J, Stefanović A, Zeljković A, Ninić A, Ivanišević J, Miljković M, Sopić M, Munjas J, Mihajlović M, Spasić S, Jelić-Ivanović Z, Spasojević-Kalimanovska V (2020) Paraoxonase 1 and atherosclerosis-related diseases. Biofactors 46:193–205. https://doi.org/10.1002/biof.1549
Larijani B, Heshmat R, Ebrahimi-Rad M, Khatami S, Valadbeigi S, Saghiri R (2016) Diagnostic value of adenosine deaminase and its isoforms in type II diabetes mellitus. Enzyme Res 2016:1–6. https://doi.org/10.1155/2016/9526593
Kılınç N, İşgör MM, Şengül B, Beydemir Ş (2015) Influence of pesticide exposure on carbonic anhydrase II from sheep stomach. Toxicol Ind Health 31:823–830. https://doi.org/10.1177/0748233713475508
Koyuturk M, Tunali S, Bolkent S, Yanardag R (2005) Effects of vanadyl sulfate on liver of streptozotocin-induced diabetic rats. Biol Trace Elem Res 104:233–247. https://doi.org/10.1385/BTER:104:3:233
Jin DQ, Li G, Kim JS, Yong CS, Kim JA, Huh K (2004) Preventive effects of laminaria japonica aqueous extract on the oxidative stress and xanthine oxidase activity in streptozotocin-induced diabetic rat liver. Biol Pharm Bull 27:1037–1040 https://pubmed.ncbi.nlm.nih.gov/15256736/
Altinoz E, Oner Z, Elbe H, Cigremis Y, Turkoz Y (2014) Protective effects of saffron (its active constituent, crocin) on nephropathy in streptozotocin-induced diabetic rats. Hum Exp Toxicol 34:127–134. https://doi.org/10.1177/0960327114538989
Althunibat OY, Al Hroob AM, Abukhalil MH, Germoush MO, Bin-Jumah M, Mahmoud AM (2019) Fisetin ameliorates oxidative stress, inflammation and apoptosis in diabetic cardiomyopathy. Life Sci 221:83–92. https://doi.org/10.1016/j.lfs.2019.02.017
Sayın R, Aslan M, Kucukoglu ME, Luleci A, Atmaca M, Esen R, Demir H (2014) Serum prolidase enzyme activity and oxidative stress levels in patients with diabetic neuropathy. Endocrine 47:146–151. https://doi.org/10.1007/s12020-013-0136-3
Kalousova M, Skrha J, Zima T (2002) Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus. Physiol Res 51:597–604 https://pubmed.ncbi.nlm.nih.gov/12511184/
Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17. https://doi.org/10.1007/s00726-009-0269-0
Heidari TF, Rabizadeh S, Mansournia MA, Mirmiranpoor H, Salehi SS, Akhavan S, Esteghamati A, Nakhjavani M (2019) Inflammatory, oxidative stress and anti-oxidative markers in patients with endometrial carcinoma and diabetes. Cytokine 120:186–190. https://doi.org/10.1016/j.cyto.2019.05.007
Prasad AS, Bao B, Beck FW, Kucuk O, Sarkar FH (2004) Antioxidant effect of zinc in humans. Free Radic Biol Med 37:1182–1190. https://doi.org/10.1016/j.freeradbiomed.2004.07.007
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This work was supported by Scientific Research Projects Coordination Unit of Istanbul University and Istanbul University-Cerrahpaşa. Project number: BEK-2016-22420 and FYO-2019-32112.
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Turkyilmaz, I.B., Bayrak, B.B., Sacan, O. et al. Zinc Supplementation Restores Altered Biochemical Parameters in Stomach Tissue of STZ Diabetic Rats. Biol Trace Elem Res 199, 2259–2265 (2021). https://doi.org/10.1007/s12011-020-02352-z
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DOI: https://doi.org/10.1007/s12011-020-02352-z