Ebselen ameliorates renal ischemia-reperfusion injury via enhancing autophagy in rats.
Autophagy
Ebselen
Nrf2-signaling pathway
Oxidative stress
Renal ischemia–reperfusion injury
Journal
Molecular and cellular biochemistry
ISSN: 1573-4919
Titre abrégé: Mol Cell Biochem
Pays: Netherlands
ID NLM: 0364456
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
12
10
2021
accepted:
10
03
2022
pubmed:
27
3
2022
medline:
7
5
2022
entrez:
26
3
2022
Statut:
ppublish
Résumé
Renal ischemia-reperfusion (I/R) injury is one of the most common causes of chronic kidney disease (CKD). It brings unfavorable outcomes to the patients and leads to a considerable socioeconomic burden. The study of renal I/R injury is still one of the hot topics in the medical field. Ebselen is an organic selenide that attenuates I/R injury in various organs. However, its effect and related mechanism underlying renal I/R injury remains unclear. In this study, we established a rat model of renal I/R injury to study the preventive effect of ebselen on renal I/R injury and further explore the potential mechanism of its action. We found that ebselen pretreatment reduced renal dysfunction and tissue damage caused by renal I/R. In addition, ebselen enhanced autophagy and inhibited oxidative stress. Additionally, ebselen pretreatment activated the nuclear factor erythroid 2-related factor 2 (Nrf2) signaling pathway. The protective effect of ebselen was suppressed by autophagy inhibitor wortmannin. In conclusion, ebselen could ameliorate renal I/R injury, probably by enhancing autophagy, activating the Nrf2 signaling pathway, and reducing oxidative stress.
Identifiants
pubmed: 35338455
doi: 10.1007/s11010-022-04413-4
pii: 10.1007/s11010-022-04413-4
doi:
Substances chimiques
Isoindoles
0
NF-E2-Related Factor 2
0
Organoselenium Compounds
0
ebselen
40X2P7DPGH
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1873-1885Subventions
Organisme : the National Natural Science Foundation of China
ID : 82160145
Organisme : the Science and Technology Fund of Guizhou Health Commission
ID : gzwkj2021-212
Organisme : the Science and Technology Fund of Guizhou Health Commission
ID : gzwjkj2020-1-113
Organisme : the Guizhou Science and Technology Project
ID : QKHZC [2021]085
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Bonventre JV, Yang L (2011) Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 121:4210–4221. https://doi.org/10.1172/jci45161
doi: 10.1172/jci45161
pubmed: 22045571
pmcid: 3204829
Mir MC, Pavan N, Parekh DJ (2016) Current paradigm for ischemia in kidney surgery. J Urol 195:1655–1663. https://doi.org/10.1016/j.juro.2015.09.099
doi: 10.1016/j.juro.2015.09.099
pubmed: 26804756
Singh AP, Singh N, Pathak D, Bedi PMS (2019) Estradiol attenuates ischemia reperfusion-induced acute kidney injury through PPAR-γ stimulated eNOS activation in rats. Mol Cell Biochem 453:1–9. https://doi.org/10.1007/s11010-018-3427-4
doi: 10.1007/s11010-018-3427-4
pubmed: 30194582
Wszolek MF, Kenney PA, Libertino JA (2011) Nonclamping partial nephrectomy: towards improved nephron sparing. Nat Rev Urol 8:523–527. https://doi.org/10.1038/nrurol.2011.103
doi: 10.1038/nrurol.2011.103
pubmed: 21811227
Bomer N, Grote Beverborg N, Hoes MF, Streng KW, Vermeer M, Dokter MM, IJmker J, Anker SD, Cleland JGF, Hillege HL, Lang CC, Ng LL, Samani NJ, Tromp J, van Veldhuisen DJ, Touw DJ, Voors AA, van der Meer PP (2020) Selenium and outcome in heart failure. Eur J Heart Fail 22:1415–1423. https://doi.org/10.1002/ejhf.1644
doi: 10.1002/ejhf.1644
pubmed: 31808274
Nath KA, Paller MS (1990) Dietary deficiency of antioxidants exacerbates ischemic injury in the rat kidney. Kidney Int 38:1109–1117. https://doi.org/10.1038/ki.1990.320
doi: 10.1038/ki.1990.320
pubmed: 2074654
Liu L, Liu C, Hou L, Lv J, Wu F, Yang X, Ren S, Ji W, Wang M, Chen L (2015) Protection against ischemia/reperfusion─induced renal injury by co─treatment with erythropoietin and sodium selenite. Mol Med Rep 12:7933–7940. https://doi.org/10.3892/mmr.2015.4426
doi: 10.3892/mmr.2015.4426
pubmed: 26647839
pmcid: 4758319
Ostróżka-Cieślik A, Dolińska B, Ryszka F (2020) Therapeutic potential of selenium as a component of preservation solutions for kidney transplantation. Molecules. https://doi.org/10.3390/molecules25163592
doi: 10.3390/molecules25163592
pubmed: 32784639
pmcid: 7463670
Zhang J, Saad R, Taylor EW, Rayman MP (2020) Selenium and selenoproteins in viral infection with potential relevance to COVID-19. Redox Biol 37:101715. https://doi.org/10.1016/j.redox.2020.101715
doi: 10.1016/j.redox.2020.101715
pubmed: 32992282
pmcid: 7481318
Noguchi N (2016) Ebselen, a useful tool for understanding cellular redox biology and a promising drug candidate for use in human diseases. Arch Biochem Biophys 595:109–112. https://doi.org/10.1016/j.abb.2015.10.024
doi: 10.1016/j.abb.2015.10.024
pubmed: 27095225
Kil J, Lobarinas E, Spankovich C, Griffiths SK, Antonelli PJ, Lynch ED, Le Prell CG (2017) Safety and efficacy of ebselen for the prevention of noise-induced hearing loss: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet 390:969–979. https://doi.org/10.1016/s0140-6736(17)31791-9
doi: 10.1016/s0140-6736(17)31791-9
pubmed: 28716314
Aras M, Altaş M, Meydan S, Nacar E, Karcıoğlu M, Ulutaş KT, Serarslan Y (2014) Effects of ebselen on ischemia/reperfusion injury in rat brain. Int J Neurosci 124:771–776. https://doi.org/10.3109/00207454.2013.879581
doi: 10.3109/00207454.2013.879581
pubmed: 24405262
Namura S, Nagata I, Takami S, Masayasu H, Kikuchi H (2001) Ebselen reduces cytochrome c release from mitochondria and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Stroke 32:1906–1911. https://doi.org/10.1161/01.str.32.8.1906
doi: 10.1161/01.str.32.8.1906
pubmed: 11486124
Kizilgun M, Poyrazoglu Y, Oztas Y, Yaman H, Cakir E, Cayci T, Akgul OE, Kurt YG, Yaren H, Kunak ZI, Macit E, Ozkan E, Taslipinar MY, Turker T, Ozcan A (2011) Beneficial effects of N-acetylcysteine and ebselen on renal ischemia/reperfusion injury. Ren Fail 33:512–517. https://doi.org/10.3109/0886022x.2011.574767
doi: 10.3109/0886022x.2011.574767
pubmed: 21545313
Zheng X, Xie L, Qin J, Shen H, Chen Z, Jin Y (2008) Effects of wortmannin on phosphorylation of PDK1, GSK3-beta, PTEN and expression of Skp2 mRNA after ischemia/reperfusion injury in the mouse kidney. Int Urol Nephrol 40:185–192. https://doi.org/10.1007/s11255-007-9215-9
doi: 10.1007/s11255-007-9215-9
pubmed: 17975737
He GQ, Chen Y, Liao HJ, Xu WM, Zhang W, He GL (2020) Associations between Huwe1 and autophagy in rat cerebral neuron oxygen─glucose deprivation and reperfusion injury. Mol Med Rep 22:5083–5094. https://doi.org/10.3892/mmr.2020.11611
doi: 10.3892/mmr.2020.11611
pubmed: 33173969
pmcid: 7646962
Paller MS, Hoidal JR, Ferris TF (1984) Oxygen free radicals in ischemic acute renal failure in the rat. J Clin Invest 74:1156–1164. https://doi.org/10.1172/jci111524
doi: 10.1172/jci111524
pubmed: 6434591
pmcid: 425281
Levine B, Kroemer G (2019) Biological functions of autophagy genes: a disease perspective. Cell 176:11–42. https://doi.org/10.1016/j.cell.2018.09.048
doi: 10.1016/j.cell.2018.09.048
pubmed: 30633901
pmcid: 6347410
Galluzzi L, Green DR (2019) Autophagy-independent functions of the autophagy machinery. Cell 177:1682–1699. https://doi.org/10.1016/j.cell.2019.05.026
doi: 10.1016/j.cell.2019.05.026
pubmed: 31199916
pmcid: 7173070
Hou J, Rao M, Zheng W, Fan J, Law BYK (2019) Advances on cell autophagy and its potential regulatory factors in renal ischemia-reperfusion injury. DNA Cell Biol 38:895–904. https://doi.org/10.1089/dna.2019.4767
doi: 10.1089/dna.2019.4767
pubmed: 31347925
Jiang M, Wei Q, Dong G, Komatsu M, Su Y, Dong Z (2012) Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 82:1271–1283. https://doi.org/10.1038/ki.2012.261
doi: 10.1038/ki.2012.261
pubmed: 22854643
pmcid: 3491167
Tan X, Zhu H, Tao Q, Guo L, Jiang T, Xu L, Yang R, Wei X, Wu J, Li X, Zhang JS (2018) FGF10 protects against renal ischemia/reperfusion injury by regulating autophagy and inflammatory signaling. Front Genet 9:556. https://doi.org/10.3389/fgene.2018.00556
doi: 10.3389/fgene.2018.00556
pubmed: 30532765
pmcid: 6265307
Kaushal GP (2012) Autophagy protects proximal tubular cells from injury and apoptosis. Kidney Int 82:1250–1253. https://doi.org/10.1038/ki.2012.337
doi: 10.1038/ki.2012.337
pubmed: 23203020
pmcid: 4068008
Zhang YL, Zhang J, Cui LY, Yang S (2015) Autophagy activation attenuates renal ischemia-reperfusion injury in rats. Exp Biol Med (Maywood) 240:1590–1598. https://doi.org/10.1177/1535370215581306
doi: 10.1177/1535370215581306
Liu S, Yang Y, Gao H, Zhou N, Wang P, Zhang Y, Zhang A, Jia Z, Huang S (2020) Trehalose attenuates renal ischemia-reperfusion injury by enhancing autophagy and inhibiting oxidative stress and inflammation. Am J Physiol Renal Physiol 318:F994-f1005. https://doi.org/10.1152/ajprenal.00568.2019
doi: 10.1152/ajprenal.00568.2019
pubmed: 32068461
Zhang YL, Qiao SK, Wang RY, Guo XN (2018) NGAL attenuates renal ischemia/reperfusion injury through autophagy activation and apoptosis inhibition in rats. Chem Biol Interact 289:40–46. https://doi.org/10.1016/j.cbi.2018.04.018
doi: 10.1016/j.cbi.2018.04.018
pubmed: 29704511
Choi EK, Jung H, Kwak KH, Yi SJ, Lim JA, Park SH, Park JM, Kim S, Jee DL, Lim DG (2017) Inhibition of oxidative stress in renal ischemia-reperfusion injury. Anesth Analg 124:204–213. https://doi.org/10.1213/ane.0000000000001565
doi: 10.1213/ane.0000000000001565
pubmed: 27607480
Liang HL, Sedlic F, Bosnjak Z, Nilakantan V (2010) SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery. Free Radic Biol Med 49:1550–1560. https://doi.org/10.1016/j.freeradbiomed.2010.08.018
doi: 10.1016/j.freeradbiomed.2010.08.018
pubmed: 20736062
Rovcanin B, Medic B, Kocic G, Cebovic T, Ristic M, Prostran M (2016) Molecular dissection of renal ischemia-reperfusion: oxidative stress and cellular events. Curr Med Chem 23:1965–1980. https://doi.org/10.2174/0929867323666160112122858
doi: 10.2174/0929867323666160112122858
pubmed: 26758795
Scherz-Shouval R, Elazar Z (2011) Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 36:30–38. https://doi.org/10.1016/j.tibs.2010.07.007
doi: 10.1016/j.tibs.2010.07.007
pubmed: 20728362
Li L, Tan J, Miao Y, Lei P, Zhang Q (2015) ROS and autophagy: interactions and molecular regulatory mechanisms. Cell Mol Neurobiol 35:615–621. https://doi.org/10.1007/s10571-015-0166-x
doi: 10.1007/s10571-015-0166-x
pubmed: 25722131
Underwood BR, Imarisio S, Fleming A, Rose C, Krishna G, Heard P, Quick M, Korolchuk VI, Renna M, Sarkar S, García-Arencibia M, O’Kane CJ, Murphy MP, Rubinsztein DC (2010) Antioxidants can inhibit basal autophagy and enhance neurodegeneration in models of polyglutamine disease. Hum Mol Genet 19:3413–3429. https://doi.org/10.1093/hmg/ddq253
doi: 10.1093/hmg/ddq253
pubmed: 20566712
pmcid: 2916709
Cao L, Xu J, Lin Y, Zhao X, Liu X, Chi Z (2009) Autophagy is upregulated in rats with status epilepticus and partly inhibited by vitamin E. Biochem Biophys Res Commun 379:949–953. https://doi.org/10.1016/j.bbrc.2008.12.178
doi: 10.1016/j.bbrc.2008.12.178
pubmed: 19138675
Mason RP, Casu M, Butler N, Breda C, Campesan S, Clapp J, Green EW, Dhulkhed D, Kyriacou CP, Giorgini F (2013) Glutathione peroxidase activity is neuroprotective in models of Huntington’s disease. Nat Genet 45:1249–1254. https://doi.org/10.1038/ng.2732
doi: 10.1038/ng.2732
pubmed: 23974869
pmcid: 4040417
Ahn CB, Je JY, Kim YS, Park SJ, Kim BI (2017) Induction of Nrf2-mediated phase II detoxifying/antioxidant enzymes in vitro by chitosan-caffeic acid against hydrogen peroxide-induced hepatotoxicity through JNK/ERK pathway. Mol Cell Biochem 424:79–86. https://doi.org/10.1007/s11010-016-2845-4
doi: 10.1007/s11010-016-2845-4
pubmed: 27743232
Loboda A, Damulewicz M, Pyza E, Jozkowicz A, Dulak J (2016) Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci 73:3221–3247. https://doi.org/10.1007/s00018-016-2223-0
doi: 10.1007/s00018-016-2223-0
pubmed: 27100828
pmcid: 4967105
Ucar BI, Ucar G, Saha S, Buttari B, Profumo E, Saso L (2021) Pharmacological protection against ischemia-reperfusion injury by regulating the Nrf2-Keap1-ARE signaling pathway. Antioxidants (Basel). https://doi.org/10.3390/antiox10060823
doi: 10.3390/antiox10060823
Wang Y, Mandal AK, Son YO, Pratheeshkumar P, Wise JTF, Wang L, Zhang Z, Shi X, Chen Z (2018) Roles of ROS, Nrf2, and autophagy in cadmium-carcinogenesis and its prevention by sulforaphane. Toxicol Appl Pharmacol 353:23–30. https://doi.org/10.1016/j.taap.2018.06.003
doi: 10.1016/j.taap.2018.06.003
pubmed: 29885333
pmcid: 6281793
Park JS, Kang DH, Lee DH, Bae SH (2015) Fenofibrate activates Nrf2 through p62-dependent Keap1 degradation. Biochem Biophys Res Commun 465:542–547. https://doi.org/10.1016/j.bbrc.2015.08.056
doi: 10.1016/j.bbrc.2015.08.056
pubmed: 26282199
Gao Y, Chu S, Zhang Z, Zuo W, Xia C, Ai Q, Luo P, Cao P, Chen N (2017) Early stage functions of mitochondrial autophagy and oxidative stress in acetaminophen-induced liver injury. J Cell Biochem 118:3130–3141. https://doi.org/10.1002/jcb.25788
doi: 10.1002/jcb.25788
pubmed: 27862231
Yang Y, Luo H, Hui K, Ci Y, Shi K, Chen G, Shi L, Xu C (2016) Selenite-induced autophagy antagonizes apoptosis in colorectal cancer cells in vitro and in vivo. Oncol Rep 35:1255–1264. https://doi.org/10.3892/or.2015.4484
doi: 10.3892/or.2015.4484
pubmed: 26676801
Zang H, Qian S, Li J, Zhou Y, Zhu Q, Cui L, Meng X, Zhu G, Wang H (2020) The effect of selenium on the autophagy of macrophage infected by Staphylococcus aureus. Int Immunopharmacol 83:106406. https://doi.org/10.1016/j.intimp.2020.106406
doi: 10.1016/j.intimp.2020.106406
pubmed: 32193097
Song GL, Chen C, Wu QY, Zhang ZH, Zheng R, Chen Y, Jia SZ, Ni JZ (2018) Selenium-enriched yeast inhibited β-amyloid production and modulated autophagy in a triple transgenic mouse model of Alzheimer’s disease. Metallomics 10:1107–1115. https://doi.org/10.1039/c8mt00041g
doi: 10.1039/c8mt00041g
pubmed: 30043821
Olson GE, Whitin JC, Hill KE, Winfrey VP, Motley AK, Austin LM, Deal J, Cohen HJ, Burk RF (2010) Extracellular glutathione peroxidase (Gpx3) binds specifically to basement membranes of mouse renal cortex tubule cells. Am J Physiol Renal Physiol 298:F1244–F1253. https://doi.org/10.1152/ajprenal.00662.2009
doi: 10.1152/ajprenal.00662.2009
pubmed: 20015939