Protective role of exogenous recombinant peroxiredoxin 6 under ischemia-reperfusion injury of kidney

Abstract

Peroxiredoxin 6 (Prx6) is an important antioxidant enzyme with various functions in the cell. Prx6 reduces a wide range of peroxide substrates, playing a leading role in maintaining the redox homeostasis of mammalian cells. In addition to the peroxidase activity, a phospholipase A2-like activity was demonstrated for Prx6, which plays an important role in the metabolism of membrane phospholipids. Besides that, due to its peroxidase and phospholipase activities, Prx6 participates in intracellular and intercellular signal transduction, thus triggering regenerative processes in the cell, suppressing apoptosis caused by various factors, including ischemia-reperfusion injuries. A nephroprotective effect of exogenous recombinant Prx6 administered before ischemia-reperfusion injury was demonstrated on an animal model. Exogenous Prx6 effectively alleviates the severeness of renal ischemia-reperfusion injuries and facilitates normalization of their structural and functional conditions. Infusion of exogenous Prx6 increases the survival rate of experimental animals by almost 3 times. Application of exogenous Prx6 can be an effective approach in the prevention and treatment of renal ischemia-reperfusion kidney lesions and in preserving isolated kidneys during transplantation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Acarin L, González B, Castellano B (2000) Oral administration of the anti-inflammatory substance triflusal results in the downregulation of constitutive transcription factor NF-kappaB in the postnatal rat brain. Neurosci Lett 288:41–44. https://doi.org/10.1016/s0304-3940(00)01202-7

    CAS  Article  PubMed  Google Scholar 

  2. Aminzadeh MA, Nicholas SB, Norris KC, Vaziri ND (2013) Role of impaired Nrf2 activation in the pathogenesis of oxidative stress and inflammation in chronic tubulo-interstitial nephropathy. Nephrol Dial Transplant 28:2038–2045. https://doi.org/10.1093/ndt/gft022

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Baum N, Dichoso CC, Carlton CE (1975) Blood urea nitrogen and serum creatinine. Urology 5:583–588. https://doi.org/10.1016/0090-4295(75)90105-3

    CAS  Article  PubMed  Google Scholar 

  4. Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem. 282:1183–1192. https://doi.org/10.1074/jbc.M603761200

    Article  Google Scholar 

  5. Biet F, Locht C, Kremer L (2002) Immunoregulatory functions of interleukin 18 and its role in defense against bacterial pathogens. J Mol Med 80:147–162. https://doi.org/10.1007/s00109-001-0307-1

    CAS  Article  PubMed  Google Scholar 

  6. Bonventre JV (2014) Kidney injury molecule-1: a translational journey. TransAm Clin Climatolog Assoc 125:293–299

    Google Scholar 

  7. Chowhan R, Rajendrakumar Singh L, Nongdam P, Meetei P, Shahnaj S, Kakchingtabam P, Fisher A, Herojit Singh K, Rahaman H (2019) Hyperoxidation of peroxiredoxin 6 induces alteration from dimeric to oligomeric state. Antioxidants 8:33. https://doi.org/10.3390/antiox8020033

    CAS  Article  PubMed Central  Google Scholar 

  8. Eismann T, Huber N, Shin T, Kuboki S, Galloway E, Wyder M, Edwards MJ, Greis KD, Shertzer HG, Fisher AB, Lentsch AB (2009) Peroxiredoxin-6 protects against mitochondrial dysfunction and liver injury during ischemia-reperfusion in mice. Am J Physiol Gastrointest Liver Physiol 296:G266–G274. https://doi.org/10.1152/ajpgi.90583.2008

    CAS  Article  PubMed  Google Scholar 

  9. Eltzschig HK, Eckle T (2011) Ischemia and reperfusion—from mechanism to translation. Nat Med 17:1391–1401. https://doi.org/10.1038/nm.2507

    CAS  Article  PubMed  Google Scholar 

  10. Feldman N, Rotter-Maskowitz A, Okun E (2015) DAMPs as mediators of sterile inflammation in aging-related pathologies. Ageing Res Rev. 24:29–39. https://doi.org/10.1016/j.arr.2015.01.003

    CAS  Article  Google Scholar 

  11. Fisher AB (2018) The phospholipase A 2 activity of peroxiredoxin 6. J Lipid Res 59:1132–1147. https://doi.org/10.1194/jlr.R082578

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Fisher AB (2017) Peroxiredoxin 6 in the repair of peroxidized cell membranes and cell signaling. Arch Biochem Biophys 617:68–83. https://doi.org/10.1016/j.abb.2016.12.003

    CAS  Article  PubMed  Google Scholar 

  13. Fisher AB, Vasquez-Medina JP, Dodia C, Sorokina EM, Tao J-Q, Feinstein SI (2018) Peroxiredoxin 6 phospholipid hydroperoxidase activity in the repair of peroxidized cell membranes. Redox Biol 14:41–46. https://doi.org/10.1016/j.redox.2017.08.008

    CAS  Article  PubMed  Google Scholar 

  14. Godoy JR, Oesteritz S, Hanschmann EM, Ockenga W, Ackermann W, Lillig CH (2011) Segment-specific overexpression of redoxins after renal ischemia and reperfusion: protective roles of glutaredoxin 2, peroxiredoxin 3, and peroxiredoxin 6. Free Radic Biol Med 51:552–561. https://doi.org/10.1016/j.freeradbiomed.2011.04.036

    CAS  Article  PubMed  Google Scholar 

  15. Gordeeva AE, Temnov AA, Charnagalov AA, Sharapov MG, Fesenko EE, Novoselov VI (2015) Protective effect of peroxiredoxin 6 in ischemia/reperfusion-induced damage of small intestine. Dig Dis Sci 60:3610–3619. https://doi.org/10.1007/s10620-015-3809-3

    CAS  Article  PubMed  Google Scholar 

  16. Gowda S, Desai PB, Kulkarni SS, Hull VV, Math AAK, Vernekar SN (2010) Markers of renal function tests. N Am J Med Sci 2:170–173

    PubMed  PubMed Central  Google Scholar 

  17. Granger DN, Kvietys PR (2015) Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox Biol 6:524–551. https://doi.org/10.1016/j.redox.2015.08.020

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Haga Y, Ohtsubo T, Murakami N, Noguchi H, Kansui Y, Goto K, Matsumura K, Kitazono T (2017) Disruption of xanthine oxidoreductase gene attenuates renal ischemia reperfusion injury in mice. Life Sci. 182:73–79. https://doi.org/10.1016/j.lfs.2017.06.011

    CAS  Article  Google Scholar 

  19. Hanschmann E-M, Godoy JR, Berndt C, Hudemann C, Lillig CH (2013) Thioredoxins, glutaredoxins, and peroxiredoxins—molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling. Antioxid Redox Signal 19:1539–1605. https://doi.org/10.1089/ars.2012.4599

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Hellweg CE (2015) The Nuclear Factor κB pathway: A link to the immune system in the radiation response. Cancer Lett. 368:275–289. https://doi.org/10.1016/j.canlet.2015.02.019

    CAS  Article  Google Scholar 

  21. Hesketh EE, Czopek A, Clay M, Borthwick G, Ferenbach D, Kluth D, Hughes J (2014) Renal ischaemia reperfusion injury: a mouse model of injury and regeneration. J Vis Exp : JoVE 15:e51816. https://doi.org/10.3791/51816

    Article  Google Scholar 

  22. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK (2004) Distinct Subcellular Localizations of Nox1 and Nox4 in Vascular Smooth Muscle Cells. Arterioscler Thromb Vasc Biol. 24:677–683. https://doi.org/10.1161/01.ATV.0000112024.13727.2c

    CAS  Article  Google Scholar 

  23. Hobson CE, Yavas S, Segal MS, Schold JD, Tribble CG, Layon AJ, Bihorac A (2009) Acute kidney injury is associated with increased long-term mortality after cardiothoracic surgery. Circulation 119:2444–2453. https://doi.org/10.1161/CIRCULATIONAHA.108.800011

    Article  PubMed  Google Scholar 

  24. Ishii T (2015) Close teamwork between Nrf2 and peroxiredoxins 1 and 6 for the regulation of prostaglandin D2 and E2 production in macrophages in acute inflammation. Free Radic Biol Med 88:189–198. https://doi.org/10.1016/j.freeradbiomed.2015.04.034

    CAS  Article  PubMed  Google Scholar 

  25. Ishimura T, Fujisawa M, Isotani S, Iijima K, Yoshikawa N, Kamidono S (2002) Endothelial nitric oxide synthase expression in ischemia-reperfusion injury after living related-donor renal transplantation. TransplInt 15:635–640

    CAS  Article  Google Scholar 

  26. Kalogeris T, Baines CP, Krenz M, Korthuis RJ (2012) Cell biology of ischemia/reperfusion injury. Int Rev Cell Mol Biol 298:229–317. https://doi.org/10.1016/B978-0-12-394309-5.00006-7.Cell

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Kang SW, Baines IC, Rhee SG (1998) Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. J Biol Chem 273:6303–6311. https://doi.org/10.1074/jbc.273.11.6303

    CAS  Article  PubMed  Google Scholar 

  28. Karplus PA, Hall A (2007) Structural survey of the peroxiredoxins. Subcell Biochem 44:41–60

    Article  Google Scholar 

  29. Kim KH, Lee W, Kim EEK (2016) Crystal structures of human peroxiredoxin 6 in different oxidation states. Biochem Biophys Res Commun 477:717–722. https://doi.org/10.1016/j.bbrc.2016.06.125

    CAS  Article  PubMed  Google Scholar 

  30. Kim SY, Jo H-Y, Kim MH, Cha Y-Y, Choi SW, Shim J-H, Kim TJ, Lee K-Y (2008) H2O2-dependent hyperoxidation of peroxiredoxin 6 (Prdx6) plays a role in cellular toxicity via up-regulation of iPLA2 activity. J Biol Chem 283:33563–33568. https://doi.org/10.1074/jbc.M806578200

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Kuang X, Wang L-F, Yu L, Li Y-J, Wang Y-N, He Q, Chen C, Du J-R (2014) Ligustilide ameliorates neuroinflammation and brain injury in focal cerebral ischemia/reperfusion rats: involvement of inhibition of TLR4/peroxiredoxin 6 signaling. Free Radic Biol Med 71:165–175. https://doi.org/10.1016/j.freeradbiomed.2014.03.028

    CAS  Article  PubMed  Google Scholar 

  32. Kümin A, Huber C, Rülicke T, Wolf E, Werner S (2006) Peroxiredoxin 6 is a potent cytoprotective enzyme in the epidermis. Am J Pathol 169:1194–1205. https://doi.org/10.2353/ajpath.2006.060119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Maksimenko AV (2016) Widening and elaboration of consecutive research into therapeutic antioxidant enzyme derivatives. Oxidative Med Cell Longev 2016:1–9. https://doi.org/10.1155/2016/3075695

    CAS  Article  Google Scholar 

  34. Maksimenko AV, Vavaev AV (2012) Antioxidant enzymes as potential targets in cardioprotection and treatment of cardiovascular diseases. Enzyme antioxidants: the next stage of pharmacological counterwork to the oxidative stress. Heart Int 7:7. https://doi.org/10.4081/hi.2012.e3

    CAS  Article  Google Scholar 

  35. Manevich Y, Fisher AB (2005) Peroxiredoxin 6, a 1-Cys peroxiredoxin, functions in antioxidant defense and lung phospholipid metabolism. Free Radic Biol Med 38:1422–1432. https://doi.org/10.1016/j.freeradbiomed.2005.02.011

    CAS  Article  PubMed  Google Scholar 

  36. Morgan MJ, Liu Z (2011) Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res 21:103–115. https://doi.org/10.1038/cr.2010.178

    CAS  Article  PubMed  Google Scholar 

  37. Novoselov SV, Peshenko IV, Popov VI, Novoselov VI, Bystrova MF, Evdokimov VJ, Kamzalov SS, Merkulova MI, Shuvaeva TM, Lipkin VM, Fesenko EE (1999) Localization of 28-kDa peroxiredoxin in rat epithelial tissues and its antioxidant properties. Cell Tissue Res 298:471–480. https://doi.org/10.1007/s004410050069

    CAS  Article  PubMed  Google Scholar 

  38. Palayoor ST, Youmell MY, Calderwood SK, Coleman CN, Price BD (1999) Constitutive activation of IκB kinase α and NF-κB in prostate cancer cells is inhibited by ibuprofen. Oncogene 18:7389–7394. https://doi.org/10.1038/sj.onc.1203160

    CAS  Article  PubMed  Google Scholar 

  39. Park KM, Byun JY, Kramers C, Kim JI, Huang PL, Bonventre JV (2003) Inducible nitric-oxide synthase is an important contributor to prolonged protective effects of ischemic preconditioning in the mouse kidney. J Biol Chem 278:27256–27266. https://doi.org/10.1074/jbc.M301778200

    CAS  Article  PubMed  Google Scholar 

  40. Perkins A, Poole LB, Karplus PA (2014) Tuning of peroxiredoxin catalysis for various physiological roles. Biochemistry 53:7693–7705. https://doi.org/10.1021/bi5013222

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30:e36. https://doi.org/10.1093/nar/30.9.e36

    Article  Google Scholar 

  42. Pires BRB, Silva RCMC, Ferreira GM, Abdelhay E (2018) NF-kappaB: two sides of the same coin. Genes 9:E24. https://doi.org/10.3390/genes9010024

    CAS  Article  PubMed  Google Scholar 

  43. Reuther-Madrid JY, Kashatus D, Chen S, Li X, Westwick J, Davis RJ, Earp HS, Wang C-Y, Baldwin AS Jr (2002) The p65/RelA subunit of NF-kappaB suppresses the sustained, antiapoptotic activity of Jun kinase induced by tumor necrosis factor. Mol Cell Biol 22:8175–8183. https://doi.org/10.1128/MCB.22.23.8175-8183.2002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Rhee SG (2016) Overview on peroxiredoxin. Mol Cell 39:1–5. https://doi.org/10.14348/molcells.2016.2368

    CAS  Article  Google Scholar 

  45. Riddell JR, Maier P, Sass SN, Moser MT, Foster BA, Gollnick SO (2012) Peroxiredoxin 1 stimulates endothelial cell expression of VEGF via TLR4 dependent activation of HIF-1α. PloS one 7:e50394. https://doi.org/10.1371/journal.pone.0050394

    CAS  Article  Google Scholar 

  46. Rosenblum ND (2013) Kidney development. In: National Kidney Foundation’s Primer on Kidney Diseases, Sixth Edition. pp 19–25

    Google Scholar 

  47. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S (2011) The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta Mol Cell Res 1813:878–888. https://doi.org/10.1016/j.bbamcr.2011.01.034

    CAS  Article  Google Scholar 

  48. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73

    CAS  Article  Google Scholar 

  49. Sharapov MG, Gordeeva AE, Goncharov RG, Tikhonova IV, Ravin VK, Temnov AA, Fesenko EE, Novoselov VI (2017a) The effect of exogenous peroxiredoxin 6 on the state of mesenteric vessels and the small intestine in ischemia–reperfusion injury. Biophysics 62:998–1008. https://doi.org/10.1134/S0006350917060239

    CAS  Article  Google Scholar 

  50. Sharapov MG, Gudkov SV, Gordeeva AE, Karp OE, Ivanov VE, Shelkovskaya OV, Bruskov VI, Novoselov VI, Fesenko EE (2016) Peroxiredoxin 6 is a natural radioprotector. Dokl Biochem Biophys 467:110–112. https://doi.org/10.1134/S1607672916020095

    CAS  Article  PubMed  Google Scholar 

  51. Sharapov MG, Novoselov VI, Fesenko EE, Bruskov VI, Gudkov SV (2017b) The role of peroxiredoxin 6 in neutralization of X-ray mediated oxidative stress: effects on gene expression, preservation of radiosensitive tissues and postradiation survival of animals. Free Radic Res 51:148–166. https://doi.org/10.1080/10715762.2017.1289377

    CAS  Article  PubMed  Google Scholar 

  52. Sharapov MG, Novoselov VI, Gudkov SV (2019) Radioprotective role of peroxiredoxin 6. Antioxidants 8:1–23. https://doi.org/10.3390/antiox8010015

    CAS  Article  Google Scholar 

  53. Sharapov MG, Novoselov VI, Ravin VK (2009) The cloning, expression, and comparative analysis of peroxiredoxin 6 from various sources. Mol Biol 43:465–471. https://doi.org/10.1134/S0026893309030145

    CAS  Article  Google Scholar 

  54. Sharapov MG, Penkov NV, Gudkov SV, Goncharov RG (2018) The role of intermolecular disulfide bonds in stabilizing the structure of peroxiredoxins. Biophysics 63:154–161. https://doi.org/10.1134/S0006350918020203

    CAS  Article  Google Scholar 

  55. Sharapov MG, Ravin VK, Novoselov VI (2014) Peroxiredoxins as multifunctional enzymes. Mol Biol 48:520–545. https://doi.org/10.1134/S0026893314040128

    CAS  Article  Google Scholar 

  56. Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131–E136. https://doi.org/10.1038/ncb0502-e131

    CAS  Article  PubMed  Google Scholar 

  57. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 93:13176–13181. https://doi.org/10.1073/pnas.93.23.13176

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R, Takada I, Sekiya T, Ooboshi H, Kitazono T, Yanagawa T, Ishii T, Takahashi H, Mori S, Nishibori M, Kuroda K, Akira S, Miyake K, Yoshimura A (2012) Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain. Nat Med.18:911–7. https://doi.org/10.1038/nm.2749

    CAS  Article  Google Scholar 

  59. Sorrell SL, Golder ZJ, Johnstone DB, Karet Frankl FE (2015) Renal peroxiredoxin 6 interacts with anion exchanger 1 and plays a novel role in pH homeostasis. Kidney Int 89:105–112. https://doi.org/10.1038/ki.2015.277

    CAS  Article  Google Scholar 

  60. Staal FJ, Roederer M, Herzenberg LA (1990) Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc Natl Acad Sci U S A 87:9943–9947

    CAS  Article  Google Scholar 

  61. Tornroth-Horsefield S, Hedfalk K, Fischer G, Lindkvist-Petersson K, Neutze R. (2010) Structural insights into eukaryotic aquaporin regulation. FEBS Lett. 584:2580–2588. https://doi.org/10.1016/j.febslet.2010.04.037

    Article  Google Scholar 

  62. Tulsawani R, Kelly LS, Fatma N, Chhunchha B, Kubo E, Kumar A, Singh DP (2010) Neuroprotective effect of peroxiredoxin 6 against hypoxia-induced retinal ganglion cell damage. BMC Neurosci 11:125. https://doi.org/10.1186/1471-2202-11-125

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Uchino S, Kellum JA, Bellomo R, Doig GS, Morimatsu H, Morgera S, Schetz M, Tan I, Bouman C, Macedo E, Gibney N, Tolwani A, Ronco C, Beginning and Ending Supportive Therapy for the Kidney (BEST Kidney) Investigators (2005) Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA 294:813–818. https://doi.org/10.1001/jama.294.7.813

    CAS  Article  PubMed  Google Scholar 

  64. Veal EA, Underwood ZE, Tomalin LE, Morgan BA, Ché S (2017) Hyperoxidation of peroxiredoxins: gain or loss of function? Antioxid Redox Signal 28(7):574–590 7625. https://doi.org/10.1089/ars.2017.7214

    CAS  Article  PubMed  Google Scholar 

  65. Vénéreau E, Ceriotti C, Bianchi ME (2015) DAMPs from Cell Death to New Life. Front Immunol. 6:422. https://doi.org/10.3389/fimmu.2015.00422

  66. Vickers S, Schiller HJ, Hildreth JEK, Bulkley GB (1998) Immunoaffinity localization of the enzyme xanthine oxidase on the outside surface of the endothelial cell plasma membrane. Surgery 124:551–560. https://doi.org/10.1016/S0039-6060(98)70102-3

    CAS  Article  Google Scholar 

  67. Volkova AG, Sharapov MG, Ravin VK, Gordeeva AE, Karaduleva EV, Mubarakshina EK, Temnov AA, Fesenko EE, Novoselov VI (2014) Effects of different antioxidant enzymes on the tracheal epithelium regeneration after chemical burn. Russian Pulmonol 6:84–90. https://doi.org/10.18093/0869-0189-2014-0-2-84-90

    Article  Google Scholar 

  68. Waikar SS, Liu KD, Chertow GM (2008) Diagnosis, epidemiology and outcomes of acute kidney injury. Clin J Am Soc Nephrol 3:844–861. https://doi.org/10.2215/CJN.05191107

    Article  PubMed  Google Scholar 

  69. Wald R, Quinn RR, Luo J, Li P, Scales DC, Mamdani MM, Ray JG, University of Toronto Acute Kidney Injury Research Group (2009) Chronic dialysis and death among survivors of acute kidney injury requiring dialysis. JAMA 302:1179–1185. https://doi.org/10.1001/jama.2009.1322

    CAS  Article  PubMed  Google Scholar 

  70. Wang T, Zhang X, Li JJ (2002) The role of NF-kappaB in the regulation of cell stress responses. Int Immunopharmacol 2:1509–1520. https://doi.org/10.1016/S1567-5769(02)00058-9

    CAS  Article  PubMed  Google Scholar 

  71. Wang X, Phelan SA, Forsman-Semb K, Taylor EF, Petros C, Brown A, Lerner CP, Paigen B (2003) Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J Biol Chem 278:25179–25190. https://doi.org/10.1074/jbc.M302706200

    CAS  Article  PubMed  Google Scholar 

  72. Wang Y, Feinstein SI, Fisher AB (2008) Peroxiredoxin 6 as an antioxidant enzyme: protection of lung alveolar epithelial type II cells from H2O2-induced oxidative stress. J Cell Biochem 104:1274–1285. https://doi.org/10.1002/jcb.21703

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Wei Q, Dong Z (2012) Mouse model of ischemic acute kidney injury: technical notes and tricks. Am J Physiol Ren Physiol 303:F1487–F1494. https://doi.org/10.1152/ajprenal.00352.2012

    CAS  Article  Google Scholar 

  74. Williams P, Lopez H, Britt D, Chan C, Ezrin A, Hottendorf R (1997) Characterization of renal ischemia-reperfusion injury in rats. J Pharmacol Toxicol Methods 37:1–7

    CAS  Article  Google Scholar 

  75. Wood ZA, Poole LB, Karplus PA (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650–653. https://doi.org/10.1126/science.1080405

    CAS  Article  PubMed  Google Scholar 

  76. Yamamoto Y, Yin MJ, Lin KM, Gaynor RB (1999) Sulindac inhibits activation of the NF-kappaB pathway. J Biol Chem 274:27307–27314. https://doi.org/10.1074/jbc.274.38.27307

    CAS  Article  PubMed  Google Scholar 

  77. Yu TM, Palanisamy K, Sun KT, Day YJ, Shu KH, Wang IK, Shyu WC, Chen P, Chen YL, Li CY (2016) RANTES mediates kidney ischemia reperfusion injury through a possible role of HIF-1α and LncRNA PRINS. Sci Rep 6:1–11. https://doi.org/10.1038/srep18424

    CAS  Article  Google Scholar 

  78. Zhang L, Wang K, Lei Y, Li Q, Nice EC, Huang C (2015) Redox signaling: potential arbitrator of autophagy and apoptosis in therapeutic response. Free Radic Biol Med 89:452–465. https://doi.org/10.1016/j.freeradbiomed.2015.08.030

    CAS  Article  Google Scholar 

  79. Zhang S, Wang W, Gu Q, Xue J, Cao H, Tang Y, Xu X, Cao J, Zhou J, Wu J, Ding W-QQ (2014) Protein and miRNA profiling of radiation-induced skin injury in rats: the protective role of peroxiredoxin-6 against ionizing radiation. Free Radic Biol Med 69:96–107. https://doi.org/10.1016/j.freeradbiomed.2014.01.019

    CAS  Article  PubMed  Google Scholar 

  80. Zhou S, Lien YC, Shuvaeva T, Debolt K, Feinstein SI, Fisher AB (2013) Functional interaction of glutathione S-transferase pi and peroxiredoxin 6 in intact cells. Int J Biochem Cell Biol 45:401–407. https://doi.org/10.1016/j.biocel.2012.11.005

    CAS  Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Russian Foundation for Basic Research (grant nos. 17-04-00356-a and 19-04-00080-a) and the “Molecular and Cell Biology” program of the Presidium of the Russian Academy of Sciences.

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. G. Sharapov.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving animals

The study protocol was approved by the institutional Ethics Committee of Institute of Cell Biophysics RAS and all experiments were carried out according to international regulations listed in the European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (ETS 123) and ICB RAS Manual for Working with Laboratory Animal no. 57 (30.12.2011).

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Goncharov, R.G., Rogov, K.A., Temnov, A.A. et al. Protective role of exogenous recombinant peroxiredoxin 6 under ischemia-reperfusion injury of kidney. Cell Tissue Res 378, 319–332 (2019). https://doi.org/10.1007/s00441-019-03073-z

Download citation

Keywords

  • Peroxiredoxin 6
  • Oxidative stress
  • Kidney
  • Ischemia-reperfusion injury