Sodium hydrogen sulfide may not protect the kidney against ischemia/reperfusion damage in male and female rats

Majid Askaripour , Hamid Najafipour, Shadan Saberi , Shahriar Dabiri, Maryam Iranpour, Abbas Etminan , Mehdi Nematbakhsh

Abstract


Background and purpose: Renal ischemia/reperfusion (IR) injury is a pathologic phenomenon that caused to increase risk of mortality. The main objective of this study was to investigate the effect of sodium hydrogen sulfide (NaHS) on renal IR injury in male and female rats.

Experimental approach: Fifty-eight male and female rats were randomized into 4 groups of control, sham, IR, and IR + NaHS. The IR was performed by 45 min of ischemia by vessel clamping followed by 24 h reperfusion. The NaHS (100 µmol/kg) treatment was applied 10 min prior to IR. Finally, after 24 h of reperfusion, the measurements were performed.

Findings/Results: The serum levels of blood urea nitrogen, creatinine, tissue level of malondialdehyde, and kidney tissue damage score (KTDS) were increased by IR. Urine volume, creatinine, and urea clearances decreased by IR. NaHS administration improved some parameters in males but exacerbated KTDS and serum markers related to renal function.

Conclusions and implications: Our data demonstrated that NaHS didn’t protect female rats against renal IR injury. In males, it has null effects or just a few protective effects via antioxidant activity.


Keywords


Oxidative stress; Renal ischemia-reperfusion injury; Sodium hydrogen sulfide.

Full Text:

PDF

References


Tan S, Wang G, Guo Y, Gui D, Wang N. Preventive effects of a natural anti-inflammatory agent, astragaloside IV, on ischemic acute kidney injury in rats. Evid Based Complement Alternat Med. 2013;2013:284025,1-13. DOI: 10.1155/2013/284025.

Mazaheri B, Emami F, Moslemi F, Talebi A, Nematbakhsh M. Zinc supplementation and ischemia pre-conditioning in renal ischemia/reperfusion injury. Malays J Med Sci. 2019;26(4):39-46.DOI: 10.21315/mjms2019.26.4.5.

Xia Z, Chen Y, Fan Q, Xue M. Oxidative stress-mediated reperfusion injury: mechanism and therapies. Oxid Med Cell Longev. 2014;2014:373081,1-3. DOI: 10.1155/2014/373081.

Akcil E, Tug T, Doseyen Z. Antioxidant enzyme activities and trace element concentrations in ischemia-reperfusion. Biol Trace Elem Res. 2000;76(1):7-13. DOI: org/10.1385/BTER:76:1:13.

Safari T, Shahraki MR, Miri S, Mirakzehi Bakhshani N, Niazi AA, Komeili GR, et al. The effect of angiotensin 1-7 and losartan on renal ischemic/reperfusion injury in male rats. Res Pharm Sci. 2019;14(5):441-447. DOI: 10.4103/1735-5362.268205.

Plotnikov EY, Kazachenko AV, Vyssokikh MY, Vasileva AK, Tcvirkun DV, Isaev NK, et al. The role of mitochondria in oxidative and nitrosative stress during ischemia/reperfusion in the rat kidney. Kidney Int. 2007;72(12):1493-1502. DOI: 10.1038/sj.ki.5002568.

Reiniers MJ, van Golen RF, van Gulik TM, Heger M. Reactive oxygen and nitrogen species in steatotic hepatocytes: a molecular perspective on the pathophysiology of ischemia-reperfusion injury in the fatty liver. Antioxid Redox Signal. 2014;21(7):1119-1142. DOI: 10.1089/ars.2013.5486.

Lee G, Hosgood SA, Patel MS, Nicholson ML. Hydrogen sulphide as a novel therapy to ameliorate cyclosporine nephrotoxicity. J Surg Res. 2015;197(2):419-426. DOI: 10.1016/j.jss.2015.02.061.

Xia M, Chen L, Muh RW, Li PL, Li N. Production and actions of hydrogen sulfide, a novel gaseous bioactive substance, in the kidneys. J Pharmacol Exp Ther. 2009;329(3):1056-1062. DOI: 10.1124/jpet.108.149963.

Ge SN, Zhao MM, Wu DD, Chen Y, Wang Y, Zhu JH, et al. Hydrogen sulfide targets EGFRCys797/Cys798 residues to induce Na(C)/K(C)-ATPase endocytosis and inhibition in renal tubular epithelial cells and increase sodium excretion in chronic salt-loaded rats. Antioxid Redox Signal. 2014;21(15):2061-2082. DOI: 10.1089/ars.2013.5304.

Lu M, Liu YH, Goh HS, Wang JJ, Yong QC, Wang R, et al. Hydrogen sulfide inhibits plasma renin activity. J Am Soc Nephrol. 2010;21(6),993-1002. DOI: 10.1681/ASN.2009090949.

Ibrahim MY, Aziz NM, Kamel MY, Rifaai RA. Sodium hydrosulphide against renal ischemia/reperfusion and the possible contribution of nitric oxide in adult male albino rats. Bratisl Lek Listy. 2015;116(11):681-688.DOI: 10.4149/bll_2015_133.

Azizi F, Seifi B, Kadkhodaee M, Ahghari P. Administration of hydrogen sulfide protects ischemia reperfusion-induced acute kidney injury by reducing the oxidative stress. Ir J Med Sci. 2016;185(3):649-654. DOI: 10.1007/s11845-015-1328-z.

Maleki M, Nematbakhsh M. Mas receptor antagonist (A779) alters the renal hemodynamics responses to angiotensin II administration after renal moderate ischemia/reperfusion in rats: gender related differences. Res Pharm Sci. 2019;14(1):12-19. DOI: 10.4103/1735-5362.251848.

Askaripour M, Najafipour H, Saberi S, Jafari E, Rajabi S. Daidzein mitigates oxidative stress and inflammation in the injured kidney of ovariectomized rats: AT1 and Mas receptor functions. Iran J Kidney Dis. 2022;16(1):32-43.

PMID: 35271498.

Choi EK, Park SH, Lim JA, Hong SW, Kwak KH, Park SS, et al. Beneficial role of hydrogen sulfide in renal ischemia reperfusion injury in rats. Yonsei Med J. 2018;59(8):960-967. DOI: 10.3349/ymj.2018.59.8.960.

Gholampour F, Khangah L, Vatanparast J, Karbalaei-Heidari HR, Owji SM, Bahaoddini A. The role of nitric oxide in the protective action of remote ischemic per-conditioning against ischemia/reperfusion-induced acute renal failure in rat. Iran J Basic Med Sci. 2018;21(6):600-606. DOI: 10.22038/IJBMS.2018.25810.6354.

Gharib-Naseri MK, Saberi S, Mard SA, Latifi SM. Bronchodilatory effect of hydrogen sulfide in rat. Iran J Basic Med Sci. 2012;15(4):907-915. PMID: 23493917.

Patel S, Fedinec AL, Liu J, Weiss MA, Pourcyrous M, Harsono M, et al. H2S mediates the vasodilator effect of endothelin-1 in the cerebral circulation. Am J Physiol Heart Circ Physiol. 2018;315(6):H1759-H1764. DOI: 10.1152/ajpheart.00451.2018.

Marutani E, Yamada M, Ida T, Tokuda K, Ikeda K, Kai S, et al. Thiosulfate mediates cytoprotective effects of hydrogen sulfide against neuronal ischemia. J Am Heart Assoc. 2015;4(11):e002125,1-10. DOI: 10.1161/JAHA.115.002125.

Hunter JP, Hosgood SA, Patel M, Rose R, Read K, Nicholson ML. Effects of hydrogen sulphide in an experimental model of renal ischaemia-reperfusion injury. Br J Surg. 2012;99(12):1665-1671.DOI: 10.1002/bjs.8956.

Ahmad A, Olah G, Szczesny B, Wood ME, Whiteman M, Szabo C. A mitochondrially targeted hydrogen sulfide donor, exerts protective effects in renal epithelial cells subjected to oxidative stress in vitro and in acute renal injury in vivo. Shock. 2016;45(1):88-97. DOI: 10.1097/SHK.0000000000000478.

Jeddi S, Gheibi S, Kashfi K, Carlström M, Ghasemi A. Dose-dependent effects of long-term administration of hydrogen sulfide on myocardial ischemia-reperfusion injury in male Wistar rats: modulation of RKIP, NF-κB, and oxidative stress. Int J Mol Sci. 2020;21(4):1415-1434. DOI: 10.3390/ijms21041415.

Sun WH, Liu F, Chen Y, Zhu YC. Hydrogen sulfide decreases the levels of ROS by inhibiting mitochondrial complex IV and increasing SOD activities in cardiomyocytes under ischemia/reperfusion. Biochem Biophys Res Commun. 2012;421(2):164-169. DOI: 10.1016/j.bbrc.2012.03.121.

Szabó C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6(11):917-935. DOI: 10.1038/nrd2425.

Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev. 2012;92(2):791-896. DOI: 10.1152/physrev.00017.2011.

Tripatara P, Patel NSA, Brancaleone V, Renshaw D, Rocha J, Sepodes B, et al. Characterisation of cystathionine gamma-lyase/hydrogen sulphide pathway in ischaemia/reperfusion injury of the mouse kidney: an in vivo study. Eur J Pharmacol. 2009;606(1-3):205-209. DOI: 10.1016/j.ejphar.2009.01.041

Melnyk AV, Zaichko NV, Khodakovskyi OA, Khodakivska OV. Sex characteristics of hydrogen sulfide effect on ischemia-reperfusion in rat myocardium. Int J Phys Pathophys. 2018;9(4):325-333. DOI: 10.1615/IntJPhysPathophys.v9.i4.50.

d’Emmanuele di Villa Bianca R, Fusco F, Mirone V, Cirino G, Sorrentino R. The role of the hydrogen sulfide pathway in male and female urogenital system in health and disease. Antioxid Redox Signal. 2017;27(10):654-668. DOI: 10.1089/ars.2017.7079.

Vitvitsky V, Prudova A, Stabler S, Dayal S, Lentz SR, Banerjee R. Testosterone regulation of renal cystathionine β-synthase: implications for sex-dependent differences in plasma homocysteine levels. Am J Physiol Renal Physiol. 2007;293(2):F594-F600. DOI: 10.1152/ajprenal.00171.2007.

Vitvitsky V, Dayal S, Stabler S, Zhou Y, Wang H, Lentz SR, et al. Perturbations in homocysteine-linked redox homeostasis in a murine model for hyperhomocysteinemia. Am J Physiol Regul Integr Comp Physiol. 2004;287(1):R39-R46.DOI: 10.1152/ajpregu.00036.2004.

Prathapasinghe GA, Siow YL, Karmin O. Detrimental role of homocysteine in renal ischemia-reperfusion injury. Am J Physiol Renal Physiol. 2007;292:F1354-F1363. DOI: 10.1152/ajprenal.00301.2006.

Melnyk AV, Zaichko NV, Khodakovskyi OA, Khodakivska OV. Sex characteristics of hydrogen sulfide effect on ischemia-reperfusion in rat myocardium. Int J Physiol Pathophysiol. 2018;9(4):325-333. DOI: 10.1615/IntJPhysPathophys.v9.i4.50.

Szabo C, Ransy C, Módis K, Andriamihaja M, Murghes B, Coletta C, et al. Regulation of mitochondrial bioenergetic function by hydrogen sulfide. Part I. Biochemical and physiological mechanisms. Br J Pharmacol. 2014;171(8):2099-2122.DOI: 10.1111/bph.12369.


Refbacks

  • There are currently no refbacks.


Creative Commons LicenseThis work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly.