The Effect of Resveratrol on Sphingosine-1 and Oxidative/ Nitrosative Stress in an Experimental Heart Ischemia Reperfusion Model

Avnioglu, Seda; Güngör, Meltem; Kurutas, Ergul; Ozturk, Unal; Demirhan, Ilter; Bakaris, Sevgi; Velioglu, Halil A.; Cankaya, Seyda; Yulug, Burak

doi:10.2478/rrlm-2021-0036

Abstract

Objectives: Resveratrol (RSV) is a natural polyphenolic compound showing significant antioxidant effects. In this study, we aimed to investigate the effects of resveratrol on the sphingosine-1-phosphate (S1P) and oxidative stress biomarkers in hearth ischemia-reperfusion (I/R).

Materials and Methods: The biochemical and histopathological effects of RSV on cardiac ischemia-reperfusion injury were investigated through ELISA- and light microscope.

Results: We observed statistically significant differences between the treatment group and the control group in terms of malondialdehyde (MDA) level, catalase (CAT) and superoxide dismutase (SOD) activities (p<0.05). Histopathologically, we also observed decreased Polymorphonuclear Leucocyte (PMNL) infiltration, myocardial edema, miyositolysis in the treatment group compared to the I/R and sham groups.

Conclusion: Resveratrol may play an important role in cardiac I/R injury through its anti-inflammatory and antioxidant effects which were biochemically and histopathologically confirmed in the present study.

References

1. Moodie DS. The Global Burden of Cardiovascular Disease. Congenital heart disease. 2016;11(3):213. DOI: 10.1111/chd.1238310.1111/chd.12383
Search in Google Scholar Back to article
2. Andersen HR, Nielsen TT, Rasmussen K, Thuesen L, Kelbaek H, Thayssen P, et al. A comparison of coronary angioplasty with fibrinolytic therapy in acute myocar-dial infarction. New England J Med. 2003;349(8):733-42. DOI: 10.1056/NEJMoa02514210.1056/NEJMoa025142
Search in Google Scholar Back to article
3. Zimmerman BJ, Granger DN. Reperfusion Injury. Surg Clin North Am. 1992;72(1):65-83. DOI: 10.1016/S0039-6109(16)45628-810.1016/S0039-6109(16)45628-8
Search in Google Scholar Back to article
4. Paul A Lapchak JHZ. Neuroprotective therapy for stroke and ischemic disease 2017. DOI: 10.1007/978-3-319-45345-310.1007/978-3-319-45345-3
Search in Google Scholar Back to article
5. Pearson PJ, Schaff HV, Vanhoutte PM. Long-term impairment of endothelium-dependent relaxations to aggregating platelets after reperfusion injury in canine coronary arteries. Circulation. 1990;81(6):1921-7. DOI: 10.1161/01.CIR.81.6.192110.1161/01.CIR.81.6.19212344684
Search in Google Scholar Back to article
6. İkizler M DS, Erkasap N, Kaygısız Z, Sevin B, Kural T. The Hemodynamic Efficacy Of Resveratrol On Reper-fusion Injury In Isolated Rat Hearts. Turkish Journal Of Thoracic And Cardiovascular Surgery. 2003;11:91-5.
Search in Google Scholar Back to article
7. Nazari A, Sadr SS, Faghihi M, Imani A, Moghimian M. The cardioprotective effect of different doses of vasopressin (AVP) against ischemia-reperfusion injuries in the anesthetized rat heart. Peptides. 2011;32(12):2459-66. DOI: 10.1016/j.peptides.2011.10.02310.1016/j.peptides.2011.10.02322079221
Search in Google Scholar Back to article
8. Robicsek F, Schaper J. Reperfusion injury: fact or myth? J Card Surg. 1997;12(3):133-7; discussion 8. DOI: 10.1111/j.1540-8191.1997.tb00112.x10.1111/j.1540-8191.1997.tb00112.x9395941
Search in Google Scholar Back to article
9. Kurutas EB. The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutrition J. 2016;15(1):71. DOI: 10.1186/s12937-016-0186-510.1186/s12937-016-0186-5496074027456681
Search in Google Scholar Back to article
10. Qu X, Chen X, Shi Q, Wang X, Wang D, Yang L. Resveratrol alleviates ischemia/reperfusion injury of diabetic myocardium via inducing autophagy. Exp Ther Med. 2019;18(4):2719-25. DOI: 10.3892/etm.2019.784610.3892/etm.2019.7846675541331555372
Search in Google Scholar Back to article
11. Mao ZJ, Lin H, Hou JW, Zhou Q, Wang Q, Chen YH. A Meta-Analysis of Resveratrol Protects against Myocar-dial Ischemia/Reperfusion Injury: Evidence from Small Animal Studies and Insight into Molecular Mechanisms. Oxid Med Cell Longev. 2019;2019:5793867. DOI: 10.1155/2019/579386710.1155/2019/5793867651203531182995
Search in Google Scholar Back to article
12. Yulug B, Hanoglu L, Khanmammadov E, Duz OA, Polat B, Hanoglu T, et al. Beyond The Therapeutic Effect of rTMS in Alzheimer’s Disease: A Possible Neuroprotective Role of Hippocampal BDNF? : A Minireview. Mini Rev Med Chem. 2018;18(17):1479-85. DOI: 10.2 174/138955751766617092716253710.2174/1389557517666170927162537
Search in Google Scholar Back to article
13. Liu FC, Tsai HI, Yu HP. Organ-Protective Effects of Red Wine Extract, Resveratrol, in Oxidative Stress-Mediated Reperfusion Injury. Oxid Med Cell Longev. 2015;2015:568634. DOI: 10.1155/2015/56863410.1155/2015/568634
Search in Google Scholar Back to article
14. Kazemirad H, Kazerani HR. Cardioprotective effects of resveratrol following myocardial ischemia and reper-fusion. Molec biol reports. 2020;47(8):5843-50. DOI: 10.1007/s11033-020-05653-710.1007/s11033-020-05653-7
Search in Google Scholar Back to article
15. de la Lastra CA, Villegas I. Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochemical Society transactions. 2007;35(Pt 5):1156-60. DOI: 10.1042/BST035115610.1042/BST0351156
Search in Google Scholar Back to article
16. Xu H, Cheng J, Wang X, Liu H, Wang S, Wu J, et al. Resveratrol pretreatment alleviates myocardial ischemia/reperfusion injury by inhibiting STIM1-mediated intracellular calcium accumulation. J Physiol Biochem. 2019;75(4):607-18. DOI: 10.1007/s13105-019-00704-510.1007/s13105-019-00704-5
Search in Google Scholar Back to article
17. Arinno A, Apaijai N, Chattipakorn SC, Chattipakorn N. The roles of resveratrol on cardiac mitochondrial function in cardiac diseases. Eur J Nut. 2021;60(1):29-44. DOI: 10.1007/s00394-020-02256-710.1007/s00394-020-02256-7
Search in Google Scholar Back to article
18. Fourny N, Lan C, Sérée E, Bernard M, Desrois M. Protective Effect of Resveratrol against Ischemia-Reperfusion Injury via Enhanced High Energy Compounds and eNOS-SIRT1 Expression in Type 2 Diabetic Female Rat Heart. Nutrients. 2019;11(1):105. DOI: 10.3390/nu1101010510.3390/nu11010105
Search in Google Scholar Back to article
19. Das DK, Maulik N. Resveratrol in cardioprotection: a therapeutic promise of alternative medicine. Molecular interventions. 2006;6(1):36-47. DOI: 10.1124/mi.6.1.710.1124/mi.6.1.7
Search in Google Scholar Back to article
20. Zweier JL. Measurement of superoxide-derived free radicals in the reperfused heart. Evidence for a free radical mechanism of reperfusion injury. J Biol Chem. 1988;263(3):1353-7. DOI: 10.1016/S0021-9258(19)57309-410.1016/S0021-9258(19)57309-4
Search in Google Scholar Back to article
21. Hung LM, Su MJ, Chu WK, Chiao CW, Chan WF, Chen JK. The protective effect of resveratrols on ischaemia-reperfusion injuries of rat hearts is correlated with antioxidant efficacy. British J Pharmacol. 2002;135(7):1627-33. DOI: 10.1038/sj.bjp.070463710.1038/sj.bjp.0704637157330211934802
Search in Google Scholar Back to article
22. Moskaug J, Carlsen H, Myhrstad MC, Blomhoff R. Polyphenols and glutathione synthesis regulation. American J Clin Nut. 2005;81(1 Suppl):277s-83s. DOI: 10.1093/ajcn/81.1.277S10.1093/ajcn/81.1.277S
Search in Google Scholar Back to article
23. Brito PM, Mariano A, Almeida LM, Dinis TC. Resveratrol affords protection against peroxynitrite-mediated endothelial cell death: A role for intracellular glutathione. Chemico-biological interactions. 2006;164(3):157-66. DOI: 10.1016/j.cbi.2006.09.00710.1016/j.cbi.2006.09.007
Search in Google Scholar Back to article
24. Shen C, Cheng W, Yu P, Wang L, Zhou L, Zeng L, et al. Resveratrol pretreatment attenuates injury and promotes proliferation of neural stem cells following oxygen-glucose deprivation/reoxygenation by upregulating the expression of Nrf2, HO-1 and NQO1 in vitro. Mol Med Reports. 2016;14(4):3646-54. DOI: 10.3892/mmr.2016.567010.3892/mmr.2016.5670
Search in Google Scholar Back to article
25. Cheng L, Jin Z, Zhao R, Ren K, Deng C, Yu S. Resveratrol attenuates inflammation and oxidative stress induced by myocardial ischemia-reperfusion injury: role of Nrf2/ARE pathway. Int J Clin Exp Med. 2015;8(7):10420-8.
Search in Google Scholar Back to article
26. Caglayan B, Kilic E, Dalay A, Altunay S, Tuzcu M, Erten F, et al. Allyl isothiocyanate attenuates oxidative stress and inflammation by modulating Nrf2/HO-1 and NF-κB pathways in traumatic brain injury in mice. Molec Biol Rep. 2019;46(1):241-50. DOI: 10.1007/s11033-018-4465-410.1007/s11033-018-4465-4
Search in Google Scholar Back to article
27. Verzijl D, Peters SL, Alewijnse AE. Sphingosine-1-phosphate receptors: zooming in on ligand-induced intracellular trafficking and its functional implications. Molecules and cells. 2010;29(2):99-104. DOI: 10.1007/s10059-010-0041-z10.1007/s10059-010-0041-z
Search in Google Scholar Back to article
28. Kluk MJ, Hla T. Role of the sphingosine 1-phosphate receptor EDG-1 in vascular smooth muscle cell proliferation and migration. Circ Res. 2001;89(6):496-502. DOI: 10.1161/hh1801.09633810.1161/hh1801.096338
Search in Google Scholar Back to article
29. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends in cell biology. 2012;22(1):50-60. DOI: 10.1016/j.tcb.2011.09.00310.1016/j.tcb.2011.09.003
Search in Google Scholar Back to article
30. Snider AJ. Sphingosine kinase and sphingosine-1-phosphate: regulators in autoimmune and inflammatory disease. Int J Clin Rheum. 2013;8(4). DOI: 10.2217/ijr.13.4010.2217/ijr.13.40
Search in Google Scholar Back to article
31. Fridovich I. Superoxide dismutases. Advances in enzymology and related areas of molecular biology. 1974;41(0):35-97. DOI: 10.1002/9780470122860.ch210.1002/9780470122860.ch2
Search in Google Scholar Back to article
32. Ernest Beutler. Red Cell Metabolism. A Manual of Biochemical Methods 2nd ed. ed. New York: Grune and Stratton Inc 1984. 68-70 p
Search in Google Scholar Back to article
33. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351-8. DOI: 10.1016/0003-2697(79)90738-310.1016/0003-2697(79)90738-3
Search in Google Scholar Back to article
34. Annapurna A, Mudagal MP, Ansari A, Rao AS. Cardioprotective activity of chalcones in ischemia/reperfusion-induced myocardial infarction in albino rats. Exp Clin Cardiol. 2012;17(3):110-4.
Search in Google Scholar Back to article
35. Sener G, Tuğtepe H, Yüksel M, Cetinel S, Gedik N, Yeğen BC. Resveratrol improves ischemia/reper-fusion-induced oxidative renal injury in rats. Arch Med Res. 2006;37(7):822-9. DOI: 10.1016/j.arcmed.2006.04.00310.1016/j.arcmed.2006.04.00316971220
Search in Google Scholar Back to article
36. Aktaş HS, Ozel Y, Ahmad S, Pençe HH, Ayaz-Adakul B, Kudas I, et al. Protective effects of resveratrol on hepatic ischemia reperfusion injury in streptozotocin-induced diabetic rats. Mol Cell Biochem. 2019;460(1-2):217-24. DOI: 10.1007/s11010-019-03582-z10.1007/s11010-019-03582-z31280437
Search in Google Scholar Back to article
37. Dong W, Yang R, Yang J, Yang J, Ding J, Wu H, et al. Resveratrol pretreatment protects rat hearts from ischemia/reperfusion injury partly via a NALP3 inflammasome pathway. Int J Clin Exp Pathol. 2015;8(8):8731-41.
Search in Google Scholar Back to article
38. Nusshold C, Uellen A, Bernhart E, Hammer A, Damm S, Wintersperger A, et al. Endocytosis and intracellular processing of BODIPY-sphingomy-elin by murine CATH.a neurons. Biochim Biophys Acta. 2013;1831(12):1665-78. DOI: 10.1016/j. bbalip.2013.08.007
Search in Google Scholar Back to article

The Effect of Resveratrol on Sphingosine-1 and Oxidative/ Nitrosative Stress in an Experimental Heart Ischemia Reperfusion Model

Abstract

Paradigm

My account