Centaurium erythraea extract reduces redox imbalance and improves insulin expression and secretion in pancreatic β-cells exposed to oxidative and nitrosative stress

Authors

  • Miloš Đorđević Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0001-9951-1932
  • Nevena Grdović Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0003-1504-4578
  • Mirjana Mihailović Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0002-8097-1186
  • Jelena Arambašić Jovanović Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0002-8810-0668
  • Aleksandra Uskoković Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0002-9616-1102
  • Jovana Rajić Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0002-2808-8484
  • Marija Đorđević Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0001-9051-9583
  • Anja Tolić Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0003-4703-6214
  • Danijela Mišić Department of Plant Physiology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0002-5419-0773
  • Branislav Šiler Department of Plant Physiology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0001-5831-6612
  • Goran Poznanović Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0003-0839-7017
  • Melita Vidaković Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0001-8410-6264
  • Svetlana Dinić Department of Molecular Biology, Institute for Biological Research “Siniša Stanković”, National Institute of Republic of Serbia, University of Belgrade, Bulevar despota Stefana 142, 11060, Belgrade http://orcid.org/0000-0002-7612-3117

Keywords:

oxidative stress, nitrosative stress, β-cells, Centaurium erythraea, antioxidant, cytoprotective

Abstract

Paper description:

  • Oxidative stress underlies b-cell damage and a diminished capacity for insulin secretion in diabetes.
  • Previously we have shown that the Centaurium erythraea extract (CEe) exhibits a significant redox potential both in vitroand in an animal model of diabetes.
  • Herein we examined the antioxidant effects of CEe in H2O2-and sodium nitroprusside (SNP)-treated Rin-5F b-cells.
  • CEe attenuated the H2O2- and SNP-induced redox imbalance, contributing to a decrease in DNA, lipid and protein damage and to an increase in cell-viability and insulin expression and secretion.


Abstract: Oxidative stress is one of the major mechanisms that underlies the damage of pancreatic b-cells and defects in insulin secretion in diabetes. As herbal preparations can alleviate oxidative stress through their redox-active secondary metabolites, in this study we investigated the cytoprotective effects of Centaurium erythraea extract (CEe) against H2O2- and SNP-induced oxidative/nitrosative stress in Rin-5F b-cells. The antioxidant activity of CEe and its effect on cell survival and insulin expression/secretion were evaluated. The CEe increased cell viability and ameliorated the disturbance of redox homeostasis in H2O2- and SNP-treated cells by decreasing DNA damage, lipid peroxidation and protein S-glutathionylation. The CEe restored GSH homeostasis in H2O2-treated b-cells and attenuated the SNP-induced disturbance of the GSH/GSSG ratio. The H2O2- and SNP-induced disruption of CAT, GPx, GR, MnSOD and CuZnSOD activities was adjusted by the CEe towards control values, as well as mRNA and protein levels of GPx, MnSOD and CAT. The CEe increased insulin expression/secretion particularly in H2O2-treated b-cells, which was in accordance with the more pronounced antioxidant effect of the CEe observed in H2O2-treated b-cells as compared to SNP-treated cells. These findings support the beneficial effect of the CEe in preventing or slowing down b-cell damage and dysfunction caused by oxidative/nitrosative stress during diabetes development.

https://doi.org/10.2298/ABS200127005D

Received: January 27, 2020; Revised: January 31, 2020; Accepted: January 31, 2020; Published online: February 10, 2020

How to cite this article: Đorđević M, Grdović N, Mihailović M, Arambašić Jovanović J, Uskoković A, Rajić J, Đorđević M, Tolić A, Mišić D, Šiler B, Poznanović G, Vidaković M, Dinić S. Centaurium erythraea extract reduces redox imbalance and improves insulin expression and secretion in pancreatic β-cells exposed to oxidative and nitrosative stress. Arch Biol Sci. 2020;72(1):117-28.

Downloads

Download data is not yet available.

References

Cernea S, Dobreanu M. Diabetes and beta cell function: from mechanisms to evaluation and clinical implications. Biochem Med (Zagreb). 2013;23(3):266-80.

Newsholme P, Cruzat VF, Keane KN, Carlessi R, de Bittencourt PI Jr. Molecular mechanisms of ROS production and oxidative stress in diabetes. Biochem J. 2016;473(24):4527-50.

Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44-84.

Pi J, Zhang Q, Fu J, Woods CG, Hou Y, Corkey BE, Collins BE, Andersen ME. ROS signaling, oxidative stress and Nrf2 in pancreatic beta-cell function. Toxicol Appl Pharmacol. 2010;244(1):77-83.

Smukler SR, Tang L, Wheeler MB, Salapatek AM. Exogenous nitric oxide and endogenous glucose-stimulated beta-cell nitric oxide augment insulin release. Diabetes. 2002;51(12):3450-60.

Ježek P, Jabůrek M, Plecitá-Hlavatá L. Contribution of Oxidative Stress and Impaired Biogenesis of Pancreatic β-Cells to Type 2 Diabetes. Antioxid Redox Signal. 2019;31(10):722-51.

Fridovich I. Superoxide anion radical (O2-.), superoxide dismutases, and related matters. J Biol Chem. 1997;272(30):18515-7.

Johansson LH, Borg LA. A spectrophotometric method for determination of catalase activity in small tissue samples. Anal Biochem. 1988;174(1):331-6.

Ursini F, Maiorino M, Brigelius-Flohe R, Aumann KD, Roveri A, Schomburg D, Flohe L. Diversity of glutathione peroxidases. Methods Enzymol. 1995;252:38-53.

Cole L, Kramer PR. Chapter 1.3 - Sugars, Fatty Acids, and Energy Physiology. In: Cole L, Kramer PR, editors. Human Physiology, Biochemistry and Basic Medicine. Boston: Academic Press; 2016. p. 17-30

Sun R, Eriksson S, Wang L. Oxidative stress induced S-glutathionylation and proteolytic degradation of mitochondrial thymidine kinase 2. J Biol Chem. 2012;287(29):24304-12.

Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008;51(2):216-26.

Jarić S, Macukanović-Jocić M, Djurdjević L, Mitrović M, Kostić O, Karadžić B, Pavlović P. An ethnobotanical survey of traditionally used plants on Suva planina mountain (south-eastern Serbia). J Ethnopharmacol. 2015;175:93-108.

Đorđević M, Mihailović M, Arambašić Jovanović J, Grdović N, Uskoković A, Tolić A, Sinadinović M, Rajić J, Mišić D, Šiler B, Poznanović G, Vidaković M, Dinić S. Centaurium erythraea methanol extract protects red blood cells from oxidative damage in streptozotocin-induced diabetic rats. J Ethnopharmacol. 2017;202:172-83.

Đorđević M, Grdović N, Mihailović M, Arambašić Jovanović J, Uskoković A, Rajić J, Sinadinović M, Tolić A, Mišić D, Šiler B, Poznanović G, Vidaković M, Dinić S. Centaurium erythraea extract improves survival and functionality of pancreatic beta-cells in diabetes through multiple routes of action. J Ethnopharmacol. 2019;242:112043.

Halliwell B, Gutteridge J. Free radicals in biology and medicine. 5th ed. Oxford: Oxford University Press; 2015.

Dominiak A, Wilkaniec A, Wroczynski P, Jesko H, Adamczyk A. Protective Effects of Selol Against Sodium Nitroprusside-Induced Cell Death and Oxidative Stress in PC12 Cells. Neurochem Res. 2016;41(12):3215-26.

Hottinger DG, Beebe DS, Kozhimannil T, Prielipp RC, Belani KG. Sodium nitroprusside in 2014: A clinical concepts review. J Anaesthesiol Clin Pharmacol. 2014;30(4):462-71.

Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351-8.

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265-75.

Grdović N, Dinić S, Arambašić J, Mihailović M, Uskoković A, Marković J, Poznanović G, Vidović S, Zeković Z, Mujić A, Mujić I, Vidaković M. The protective effect of a mix of Lactarius deterrimus and Castanea sativa extracts on streptozotocin-induced oxidative stress and pancreatic beta-cell death. Br J Nutr. 2012;108(7):1163-76.

Beutler E. Catalase. In: Beutler E, editor. Red cell metabolism, a manual of biochemical methods. New York: Grune and Stratton, Inc; 1982. p. 105-6.

Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10):3170-5.

Tamura M, Oshino N, Chance B. Some characteristics of hydrogen- and alkylhydroperoxides metabolizing systems in cardiac tissue. J Biochem. 1982;92(4):1019-31.

Glatzle D, Vuilleumier JP, Weber F, Decker K. Glutathione reductase test with whole blood, a convenient procedure for the assessment of the riboflavin status in humans. Experientia. 1974;30(6):665-7.

Sefi M, Fetoui H, Lachkar N, Tahraoui A, Lyoussi B, Boudawara T, Zeghal N. Centaurium erythrea (Gentianaceae) leaf extract alleviates streptozotocin-induced oxidative stress and beta-cell damage in rat pancreas. J Ethnopharmacol. 2011;135(2):243-50.

Stefkov G, Miova B, Dinevska-Kjovkarovska S, Stanoeva JP, Stefova M, Petrusevska G, Kulevanova S. Chemical characterization of Centaurium erythrea L. and its effects on carbohydrate and lipid metabolism in experimental diabetes. J Ethnopharmacol. 2014;152(1):71-7.

Fabricant DS, Farnsworth NR. The Value of Plants Used in Traditional Medicine for Drug Discovery. Environ Health Perspect. 2001;109(Supl.1):69-75.

Tafesse TB., Hymete A, Mekonnen Y, Tadesse M. Antidiabetic activity and phytochemical screening of extracts of the leaves of Ajuga remota Benth on alloxan-induced diabetic mice. BMC Complement Altern Med. 2017;17:243.

Halliwell B. Lipid peroxidation, antioxidants and cardiovascular disease: how should we move forward? Cardiovasc Res. 2000;47(3):410-8.

Kohen R, Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol. 2002;30(6):620-50.

Panasenko OM, Gorudko IV, Sokolov AV. Hypochlorous acid as a precursor of free radicals in living systems. Biochemistry (Mosc). 2013;78(13):1466-89.

Cardaci S, Filomeni G, Rotilio G, Ciriolo MR. Reactive oxygen species mediate p53 activation and apoptosis induced by sodium nitroprusside in SH-SY5Y cells. Mol Pharmacol. 2008;74(5):1234-45.

Terwel D, Nieland LJ, Schutte B, Reutelingsperger CP, Ramaekers FC, Steinbusch HW. S-nitroso-N-acetylpenicillamine and nitroprusside induce apoptosis in a neuronal cell line by the production of different reactive molecules. Eur J Pharmacol. 2000;400(1):19-33.

Modak MA, Parab PB, Ghaskadbi SS. Pancreatic Islets Are Very Poor in Rectifying Oxidative DNA Damage. Pancreas. 2009;38(1):23-9.

Repetto M, Semprine J, Boveris A. Lipid Peroxidation: Chemical Mechanism, Biological Implications and Analytical Determination. In: Catala A, editor. Lipid Peroxidation. Rijeka, Croatia: Intech Open; 2012. p. 2-30.

Cooper AJ, Pinto JT, Callery PS. Reversible and irreversible protein glutathionylation: biological and clinical aspects. Expert Opin Drug Metab Toxicol. 2011;7(7):891-910.

Grek CL, Zhang J, Manevich Y, Townsend DM, Tew KD. Causes and consequences of cysteine S-glutathionylation. J Biol Chem. 2013;288(37):26497-504.

Boguszewska-Mańkowska D, Nykiel M, Zagdańska B. Protein Oxidation and Redox Regulation of Proteolysis. In: Gowder SJT, editor. Basic Principles and Clinical Significance of Oxidative Stress. Rijeka, Croatia: IntechOpen; 2015. p. 17-35.

Erkan N, Akgonen S, Ovat S, Goksel G, Ayranci E. Phenolic compounds profile and antioxidant activity of Dorystoechas hastata L. Boiss et Heldr. Food Res Int. 2011;44(9):3013-20.

Nićiforović N, Abramovič H. Sinapic Acid and Its Derivatives: Natural Sources and Bioactivity. Compr Rev Food Sci Food Saf. 2014;13(1):34-51.

Romanova D, Vachalkova A, Cipak L, Ovesna Z, Rauko P. Study of antioxidant effect of apigenin, luteolin and quercetin by DNA protective method. Neoplasma. 2001;48(2):104-7.

Asahi M, Fujii J, Suzuki K, Seo HG, Kuzuya T, Hori M, Tada M, Fujii S, Taniguchi N. Inactivation of Glutathione Peroxidase by Nitric Oxide. Implication for Cytotoxicity. J Biol Chem. 1995;270(36):21035-9.

Brown GC. Reversible binding and inhibition of catalase by nitric oxide. Eur J Biochem. 1995;232(1):188-91.

Corbett JA, Sweetland MA, Lancaster JR Jr, McDaniel ML. A 1-hour pulse with IL-1 beta induces formation of nitric oxide and inhibits insulin secretion by rat islets of Langerhans: evidence for a tyrosine kinase signaling mechanism. FASEB J. 1993;7(2):369-74.

Quintana-Lopez L, Blandino-Rosano M, Perez-Arana G, Cebada-Aleu A, Lechuga-Sancho A, Aguilar-Diosdado M, Segundo C. Nitric Oxide Is a Mediator of Antiproliferative Effects Induced by Proinflammatory Cytokines on Pancreatic Beta Cells. Mediators Inflamm. 2013;2013:10.

Pi J, Bai Y, Zhang Q, Wong V, Floering LM, Daniel K, Reece JM, Deeney JT, Andersen ME, Corkey BE, Collins S. Reactive Oxygen Species as a Signal in Glucose-Stimulated Insulin Secretion. Diabetes. 2007;56(7):1783-91.

Newsholme P, Keane KN, Carlessi R, Cruzat V. Oxidative stress pathways in pancreatic β-cells and insulin-sensitive cells and tissues: importance to cell metabolism, function, and dysfunction. Am J Physiol Cell Physiol. 2019;317(3):C420-33.

Downloads

Published

2020-03-24

How to Cite

1.
Đorđević M, Grdović N, Mihailović M, Arambašić Jovanović J, Uskoković A, Rajić J, Đorđević M, Tolić A, Mišić D, Šiler B, Poznanović G, Vidaković M, Dinić S. Centaurium erythraea extract reduces redox imbalance and improves insulin expression and secretion in pancreatic β-cells exposed to oxidative and nitrosative stress. Arch Biol Sci [Internet]. 2020Mar.24 [cited 2024Dec.22];72(1):117-28. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/5029

Issue

Vol. 72 No. 1 (2020)

Section

Articles

License

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.

Most read articles by the same author(s)