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Review

Emerging therapeutic strategies for transplantation-induced acute kidney injury: protecting the organelles and the vascular bed

, ORCID Icon, , , , , , , , , , & ORCID Icon show all
Pages 495-509 | Received 06 Feb 2019, Accepted 16 Apr 2019, Published online: 03 May 2019

References

  • Chawla LS, Bellomo R, Bihorac A, et al. Acute kidney disease and renal recovery: consensus report of the Acute Disease Quality Initiative (ADQI) 16 Workgroup. Nat Rev Nephrol. 2017;13:241–257.
  • Husain-Syed F, Ronco C. The odyssey of risk stratification in acute kidney injury. Nat Rev Nephrol. 2018;14:660–662.
  • Pereira M, Rodrigues N, Godinho I, et al. Acute kidney injury in patients with severe sepsis or septic shock: a comparison between the “Risk, Injury, Failure, Loss of kidney function, End-stage kidney disease” (RIFLE), Acute Kidney Injury Network (AKIN) and Kidney Disease: improving Global Outcomes (KDIGO) classifications. Clin Kidney J. 2017;10:332–340.
  • Zuk A, Bonventre JV. Acute Kidney Injury. Annu Rev Med. 2016;67:293–307.
  • Ow CPC, Ngo JP, Ullah MM, et al. Renal hypoxia in kidney disease: cause or consequence? Acta Physiol Oxf Eng. 2018;222:e12999.
  • Favreau F, Giraud S, Bon D, et al. (Ischemia reperfusion control: the key of kidney graft outcome). Méd Sci MS. 2013;29:183–188.
  • Le Pape S, Pasini-Chabot O, Couturier P, et al. Decoding cold ischaemia time impact on kidney graft: the kinetics of the unfolded protein response pathways. Artif Cells Nanomed Biotechnol. 2018;1–13. doi:10.1080/21691401.2018.1518908.
  • Giraud S, Steichen C, Allain G, et al. Dynamic transcriptomic analysis of ischemic injury in a porcine pre-clinical model mimicking donors deceased after circulatory death. Sci Rep. 2018;8:5986.
  • Russo MJ, Chen JM, Sorabella RA, et al. The effect of ischemic time on survival after heart transplantation varies by donor age: an analysis of the united network for organ sharing database. J Thorac Cardiovasc Surg. 2007;133:554–559.
  • Patel ND, Weiss ES, Nwakanma LU, et al. Impact of donor-to-recipient weight ratio on survival after heart transplantation analysis of the united network for organ sharing database. Circulation. 2008;118:S83–8.
  • Morizane R, Miyoshi T, Bonventre JV. Concise review: kidney generation with human pluripotent stem cells. Stem Cells Dayt Ohio. 2017;35:2209–2217.
  • Okouchi Y, Sasaki K, Tamaki T. Ultrastructural changes in hepatocytes, sinusoidal endothelial cells and macrophages in hypothermic preservation of the rat liver with university of Wisconsin solution. Virchows Arch Int J Pathol. 1994;424:477–484.
  • Mosbah IB, Zaouali MA, Martel C, et al. IGL-1 solution reduces endoplasmic reticulum stress and apoptosis in rat liver transplantation. Cell Death Dis. 2012;3:e279.
  • Fougeray S, Bouvier N, Beaune P, et al. Metabolic stress promotes renal tubular inflammation by triggering the unfolded protein response. Cell Death Dis. 2011;2:e143.
  • Hetz C, Chevet E, Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013;12:703–719.
  • Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8:519–529.
  • Jonikas MC, Collins SR, Denic V, et al. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science. 2009;323:1693–1697.
  • Ameri K, Harris AL. Activating transcription factor 4. Int J Biochem Cell Biol. 2008;40:14–21.
  • Hetz C, Glimcher LH. Fine-tuning of the unfolded protein response: assembling the IRE1α interactome. Mol Cell. 2009;35:551–561.
  • Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mrnas during the unfolded protein response. Science. 2006;313:104–107.
  • Upton J-P, Wang L, Han D, et al. IRE1α cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science. 2012;338:818–822.
  • Jackson RJ, Hellen CUT, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol. 2010;11:113–127.
  • Harding HP, Zhang Y, Scheuner D, et al. Ppp1r15 gene knockout reveals an essential role for translation initiation factor 2 alpha (eIF2α) dephosphorylation in mammalian development. Proc Natl Acad Sci. 2009;106:1832–1837.
  • Harding HP, Novoa I, Zhang Y, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell. 2000;6:1099–1108.
  • Sano R, Reed JC. ER stress-induced cell death mechanisms. Biochim Biophys Acta BBA - Mol Cell Res. 2013;1833:3460–3470.
  • Schröder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res Mol Mech Mutagen. 2005;569:29–63.
  • Robbins SL, Kumar V, Cotran RS. Pathologic basis of disease. 8th ed. Philadelphia, PA: Saunders/Elsevier; 2010; p. 1–28.
  • Boyce M, Bryant KFJousse C, et al. A selective inhibitor of eif2alpha dephosphorylation protects cells from er stress. Science. 2005;307:935–939.
  • Dong B, Zhou H, Han C, et al. Ischemia/reperfusion-induced CHOP expression promotes apoptosis and impairs renal function recovery: the role of acidosis and GPR4. PloS One. 2014;9:e110944.
  • Debout A, Foucher Y, Trébern-Launay K, et al. Each additional hour of cold ischemia time significantly increases the risk of graft failure and mortality following renal transplantation. Kidney Int. 2015;87:343–349.
  • Saxena S, Cabuy E, Caroni P. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci. 2009;12:627–636.
  • Colla E, Coune P, Liu Y, et al. Endoplasmic reticulum stress is important for the manifestations of α-synucleinopathy in vivo. J Neurosci Off J Soc Neurosci. 2012;32:3306–3320.
  • Pandey VK, Mathur A, Khan MF, et al. Activation of PERK-eIF2α-ATF4 pathway contributes to diabetic hepatotoxicity: attenuation of ER stress by Morin. Cell Signal. 2019. DOI:10.1016/j.cellsig.2019.03.008.
  • Sidrauski C, McGeachy AM, Ingolia NT, et al. The small molecule ISRIB reverses the effects of eIF2α phosphorylation on translation and stress granule assembly. ELife. 2015;4. doi:10.7554/eLife.05033.
  • Wang L, Popko B, Tixier E, et al. Guanabenz, which enhances the unfolded protein response, ameliorates mutant SOD1-induced amyotrophic lateral sclerosis. Neurobiol Dis. 2014;71:317–324.
  • Das I, Krzyzosiak A, Schneider K, et al. Preventing proteostasis diseases by selective inhibition of a phosphatase regulatory subunit. Science. 2015;348:239–242.
  • Volkmann K, Lucas JL, Vuga D, et al. Potent and selective inhibitors of the inositol-requiring enzyme 1 endoribonuclease. J Biol Chem. 2011;286:12743–12755.
  • Papandreou I, Denko NC, Olson M, et al. Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma. Blood. 2011;117:1311–1314.
  • Mimura N, Fulciniti M, Gorgun G, et al. Blockade of XBP1 splicing by inhibition of IRE1α is a promising therapeutic option in multiple myeloma. Blood. 2012;119:5772–5781.
  • Lee A-H, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol. 2003;23:7448–7459.
  • Cross BCS, Bond PJ, Sadowski PG, et al. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci U S A. 2012;109:E869–878.
  • Wang L, Perera BGK, Hari SB, et al. Divergent allosteric control of the IRE1α endoribonuclease using kinase inhibitors. Nat Chem Biol. 2012;8:982–989.
  • Ali MMU, Bagratuni T, Davenport EL, et al. Structure of the Ire1 autophosphorylation complex and implications for the unfolded protein response. Embo J. 2011;30:894–905.
  • Jha BK, Polyakova I, Kessler P, et al. Inhibition of RNase L and RNA-dependent protein kinase (PKR) by sunitinib impairs antiviral innate immunity. J Biol Chem. 2011;286:26319–26326.
  • Ghosh R, Wang L, Wang ES, et al. Allosteric inhibition of the IRE1α RNase preserves cell viability and function during endoplasmic reticulum stress. Cell. 2014;158:534–548.
  • Ri M, Tashiro E, Oikawa D, et al. Identification of Toyocamycin, an agent cytotoxic for multiple myeloma cells, as a potent inhibitor of ER stress-induced XBP1 mRNA splicing. Blood Cancer J. 2012;2:e79.
  • Kawamura T, Tashiro E, Shindo K, et al. SAR study of a novel triene-ansamycin group compound, quinotrierixin, and related compounds, as inhibitors of ER stress-induced XBP1 activation. J Antibiot (Tokyo). 2008;61:312–317.
  • Gallagher CM, Garri C, Cain EL, et al. Ceapins are a new class of unfolded protein response inhibitors, selectively targeting the ATF6α branch. ELife. 2016;5. doi:10.7554/eLife.11878.
  • Kim D-S, Ha K-C, Kwon D-Y, et al. Kaempferol protects ischemia/reperfusion-induced cardiac damage through the regulation of endoplasmic reticulum stress. Immunopharmacol Immunotoxicol. 2008;30:257–270.
  • Bu L-J, Yu H-Q, Fan -L-L, et al. Melatonin, a novel selective ATF-6 inhibitor, induces human hepatoma cell apoptosis through COX-2 downregulation. World J Gastroenterol. 2017;23:986–998.
  • Mukhopadhyay P, Horváth B, Zsengellėr Z, et al. Mitochondrial reactive oxygen species generation triggers inflammatory response and tissue injury associated with hepatic ischemia-reperfusion: therapeutic potential of mitochondrially targeted antioxidants. Free Radic Biol Med. 2012;53:1123–1138.
  • Cohen JJ. Relationship between energy requirements for Na+ reabsorption and other renal functions. Kidney Int. 1986;29:32–40.
  • Chevalier RL. The proximal tubule is the primary target of injury and progression of kidney disease: role of the glomerulotubular junction. Am J Physiol - Ren Physiol. 2016;311:F145–61.
  • Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry. 2010;49:835–842.
  • Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol CB. 2014;24:R453–62.
  • Hoeksma D, Rebolledo RA, Hottenrott M, et al. Inadequate antioxidative responses in kidneys of brain-dead rats. Transplantation. 2017;101:746–753.
  • Vance JE. Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem. 1990;265:7248–7256.
  • Raturi A, Simmen T. Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM). Biochim Biophys Acta. 2013;1833:213–224.
  • van Vliet AR, Agostinis P. Mitochondria-Associated Membranes and ER Stress. Curr Top Microbiol Immunol. 2018;414:73–102.
  • Morita M, Gravel S-P, Hulea L, et al. mTOR coordinates protein synthesis, mitochondrial activity and proliferation. Cell Cycle. 2015;14:473–480.
  • Lebeau J, Saunders JM, Moraes VWR, et al. The PERK arm of the unfolded protein response regulates mitochondrial morphology during acute endoplasmic reticulum stress. Cell Rep. 2018;22:2827–2836.
  • Szeto HH. Pharmacologic approaches to improve mitochondrial function in AKI and CKD. J Am Soc Nephrol JASN. 2017;28:2856–2865. .
  • Dare AJ, Bolton EA, Pettigrew GJ, et al. Protection against renal ischemia-reperfusion injury in vivo by the mitochondria targeted antioxidant MitoQ. Redox Biol. 2015;5:163–168.
  • Liang HL, Sedlic F, Bosnjak Z, et al. SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery. Free Radic Biol Med. 2010;49:1550–1560.
  • Jankauskas SS, Andrianova NV, Alieva IB, et al. Dysfunction of kidney endothelium after ischemia/reperfusion and its prevention by mitochondria-targeted antioxidant. Biochem Biokhimiia. 2016;81:1538–1548.
  • Szeto HH, Liu S, Soong Y, et al. Mitochondria protection after acute ischemia prevents prolonged upregulation of IL-1β and IL-18 and arrests CKD. J Am Soc Nephrol JASN. 2017;28:1437–1449.
  • Erpicum P, Rowart P, Defraigne J-O, et al. What we need to know about lipid-associated injury in case of renal ischemia-reperfusion. Am J Physiol Renal Physiol. 2018;315:F1714–9.
  • Singh AP, Singh N, Bedi PMS. Pioglitazone ameliorates renal ischemia reperfusion injury through NMDA receptor antagonism in rats. Mol Cell Biochem. 2016;417:111–118.
  • Cameron RB, Gibbs WS, Miller SR, et al. Proximal tubule β2-adrenergic receptor mediates formoterol-induced recovery of mitochondrial and renal function after ischemia-reperfusion injury. J Pharmacol Exp Ther. 2019;369:173–180.
  • Rasbach KA, Funk JA, Jayavelu T, et al. 5-hydroxytryptamine receptor stimulation of mitochondrial biogenesis. J Pharmacol Exp Ther. 2010;332:632–639.
  • Lemoine S, Pillot B, Augeul L, et al. Dose and timing of injections for effective cyclosporine A pretreatment before renal ischemia reperfusion in mice. PloS One. 2017;12:e0182358.
  • Sumida M, Doi K, Ogasawara E, et al. Regulation of mitochondrial dynamics by dynamin-related protein-1 in acute cardiorenal syndrome. J Am Soc Nephrol JASN. 2015;26:2378–2387.
  • McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med. 1985;312:159–163.
  • Land W, Schneeberger H, Schleibner S, et al. The beneficial effect of human recombinant superoxide dismutase on acute and chronic rejection events in recipients of cadaveric renal transplants. Transplantation. 1994;57:211–217.
  • Mundt HM, Yard BA, Krämer BK, et al. Optimized donor management and organ preservation before kidney transplantation. Transpl Int Off J Eur Soc Organ Transplant. 2016;29:974–984.
  • Orban J-C, Quintard H, Cassuto E, et al. Effect of N-acetylcysteine pretreatment of deceased organ donors on renal allograft function: a randomized controlled trial. Transplantation. 2015;99:746–753.
  • Jafari A, Khatami M-R, Dashti-Khavidaki S, et al. Protective effects of L-carnitine against delayed graft function in kidney transplant recipients: A pilot, randomized, double-blinded, placebo-controlled clinical trial. J Ren Nutr Off J Counc Ren Nutr Natl Kidney Found. 2017;27:113–126.
  • Ambrosi N, Arrosagaray V, Guerrieri D, et al. α-lipoic acid protects against ischemia-reperfusion injury in simultaneous kidney-pancreas transplantation. Transplantation. 2016;100:908–915.
  • Thuillier R, Allain G, Giraud S, et al. Cyclodextrin curcumin formulation improves outcome in a preclinical pig model of marginal kidney transplantation. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2014;14:1073–1083.
  • Bolisetty S, Zarjou A, Agarwal A. Heme oxygenase 1 as a therapeutic target in acute kidney injury. Am J Kidney Dis Off J Natl Kidney Found. 2017;69:531–545.
  • Lan R, Geng H, Singha PK, et al. Mitochondrial pathology and glycolytic shift during proximal tubule atrophy after ischemic AKI. J Am Soc Nephrol. 2016;27:3356–3367.
  • Wei Q, Xiao X, Fogle P, et al. Changes in metabolic profiles during acute kidney injury and recovery following ischemia/reperfusion. PloS One. 2014;9:e106647.
  • Vigne P, Frelin C. The role of polyamines in protein-dependent hypoxic tolerance of Drosophila. BMC Physiol. 2008;8:22.
  • Park MH, Nishimura K, Zanelli CF, et al. Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids. 2010;38:491–500.
  • Melis N, Rubera I, Cougnon M, et al. Targeting eIF5A hypusination prevents anoxic cell death through mitochondrial silencing and improves kidney transplant outcome. J Am Soc Nephrol JASN. 2017;28:811–822. .
  • Drury ER, Zsengeller ZK, Stillman IE, et al. Renal PGC1α may be associated with recovery after delayed graft function. Nephron. 2018;138:303–309.
  • Chen S-D, Yang D-I, Lin T-K, et al. Roles of oxidative stress, apoptosis, PGC-1α and mitochondrial biogenesis in cerebral ischemia. Int J Mol Sci. 2011;12:7199–7215.
  • Tarjus A, Amador C, Michea L, et al. Vascular mineralocorticoid receptor and blood pressure regulation. Curr Opin Pharmacol. 2015;21:138–144.
  • Messaoudi S, Azibani F, Delcayre C, et al. Aldosterone, mineralocorticoid receptor, and heart failure. Mol Cell Endocrinol. 2012;350:266–272.
  • Pitt B, Remme W, Zannad F, et al. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med. 2003;348:1309–1321.
  • Zannad F, McMurray JJV, Krum H, et al. Eplerenone in patients with systolic heart failure and mild symptoms. N Engl J Med. 2011;364:11–21.
  • Bertocchio J-P, Warnock DG, Jaisser F. Mineralocorticoid receptor activation and blockade: an emerging paradigm in chronic kidney disease. Kidney Int. 2011;79:1051–1060.
  • Maïga S, Allain G, Hauet T, et al. Renal auto-transplantation promotes cortical microvascular network remodeling in a preclinical porcine model. PloS One. 2017;12:e0181067.
  • Griol-Charhbili V, Fassot C, Messaoudi S, et al. Epidermal growth factor receptor mediates the vascular dysfunction but not the remodeling induced by aldosterone/salt. Hypertens Dallas Tex. 1979[2011];57:238–244.
  • Nguyen Dinh Cat A, Griol-Charhbili V, Loufrani L, et al. The endothelial mineralocorticoid receptor regulates vasoconstrictor tone and blood pressure. FASEB J Off Publ Fed Am Soc Exp Biol. 2010;24:2454–2463.
  • Galmiche G, Pizard A, Gueret A, et al. Smooth muscle cell mineralocorticoid receptors are mandatory for aldosterone-salt to induce vascular stiffness. Hypertens Dallas Tex. 1979[2014];63:520–526.
  • Amador CA, Bertocchio J-P, Andre-Gregoire G, et al. Deletion of mineralocorticoid receptors in smooth muscle cells blunts renal vascular resistance following acute cyclosporine administration. Kidney Int. 2016;89:354–362.
  • Usher MG, Duan SZ, Ivaschenko CY, et al. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J Clin Invest. 2010;120:3350–3364.
  • Huang LL, Nikolic-Paterson DJ, Han Y, et al. Myeloid mineralocorticoid receptor activation contributes to progressive kidney disease. J Am Soc Nephrol JASN. 2014;25:2231–2240.
  • Pitt B, Kober L, Ponikowski P, et al. Safety and tolerability of the novel non-steroidal mineralocorticoid receptor antagonist BAY 94-8862 in patients with chronic heart failure and mild or moderate chronic kidney disease: a randomized, double-blind trial. Eur Heart J. 2013;34:2453–2463.
  • Bertocchio J-P, Barbe C, Lavaud S, et al. Safety of eplerenone for kidney-transplant recipients with impaired renal function and receiving cyclosporine A. PloS One. 2016;11:e0153635.
  • Girerd S, Frimat L, Ducloux D, et al. EPURE transplant (Eplerenone in Patients Undergoing Renal Transplant) study: study protocol for a randomized controlled trial. Trials. 2018;19:595.
  • Mejía-Vilet JM, Ramírez V, Cruz C, et al. Renal ischemia-reperfusion injury is prevented by the mineralocorticoid receptor blocker spironolactone. Am J Physiol Renal Physiol. 2007;293:F78–86.
  • Sánchez-Pozos K, Barrera-Chimal J, Garzón-Muvdi J, et al. Recovery from ischemic acute kidney injury by spironolactone administration. Nephrol Dial Transplant Off Publ Eur Dial Transpl Assoc - Eur Ren Assoc. 2012;27:3160–3169.
  • Barrera-Chimal J, Pérez-Villalva R, Rodríguez-Romo R, et al. Spironolactone prevents chronic kidney disease caused by ischemic acute kidney injury. Kidney Int. 2013;83:93–103.
  • Barrera-Chimal J, Prince S, Fadel F, et al. Sulfenic acid modification of endothelin B receptor is responsible for the benefit of a nonsteroidal mineralocorticoid receptor antagonist in renal ischemia. J Am Soc Nephrol JASN. 2016;27:398–404. .
  • Barrera-Chimal J, Estrela GR, Lechner SM, et al. The myeloid mineralocorticoid receptor controls inflammatory and fibrotic responses after renal injury via macrophage interleukin-4 receptor signaling. Kidney Int. 2018;93:1344–1355. .
  • Barrera-Chimal J, André-Grégoire G, Nguyen Dinh Cat A, et al. Benefit of mineralocorticoid receptor antagonism in AKI: role of vascular smooth muscle rac1. J Am Soc Nephrol JASN. 2017;28:1216–1226.
  • Ohtake T, Kobayashi S, Slavin S, et al. Human peripheral blood mononuclear cells incubated in vasculogenic conditioning medium dramatically improve ischemia/reperfusion acute kidney injury in Mice. Cell Transplant. 2018;963689717753186. doi:10.1177/0963689717753186.
  • Liang C-J, Shen W-C, Chang F-B, et al. Endothelial progenitor cells derived from wharton’s jelly of human umbilical cord attenuate ischemic acute kidney injury by increasing vascularization and decreasing apoptosis, inflammation, and fibrosis. Cell Transplant. 2015;24:1363–1377.
  • Yuan X, Li D, Chen X, et al. Extracellular vesicles from human-induced pluripotent stem cell-derived mesenchymal stromal cells (hiPSC-MSCs) protect against renal ischemia/reperfusion injury via delivering specificity protein (SP1) and transcriptional activating of sphingosine kinase 1 and inhibiting necroptosis. Cell Death Dis. 2017;8:3200.
  • Tarng D-C, Tseng W-C, Lee P-Y, et al. Induced pluripotent stem cell-derived conditioned medium attenuates acute kidney injury by downregulating the oxidative stress-related pathway in ischemia-reperfusion rats. Cell Transplant. 2016;25:517–530.
  • Zhou L, Xu L, Shen J, et al. Preischemic administration of nonexpanded adipose stromal vascular fraction attenuates acute renal ischemia/reperfusion injury and fibrosis. Stem Cells Transl Med. 2016;5:1277–1288.
  • Zhou L, Song Q, Shen J, et al. Comparison of human adipose stromal vascular fraction and adipose-derived mesenchymal stem cells for the attenuation of acute renal ischemia/reperfusion injury. Sci Rep. 2017;7:44058.
  • Erpicum P, Rowart P, Poma L, et al. Administration of mesenchymal stromal cells before renal ischemia/reperfusion attenuates kidney injury and may modulate renal lipid metabolism in rats. Sci Rep. 2017;7:8687.
  • Baulier E, Favreau F, Le Corf A, et al. Amniotic fluid-derived mesenchymal stem cells prevent fibrosis and preserve renal function in a preclinical porcine model of kidney transplantation. Stem Cells Transl Med. 2014;3:809–820. .
  • Cai J, Yu X, Xu R, et al. Maximum efficacy of mesenchymal stem cells in rat model of renal ischemia-reperfusion injury: renal artery administration with optimal numbers. PloS One. 2014;9:e92347.
  • Mori Da Cunha MGMC, Zia S, Beckmann DV, et al. Vascular endothelial growth factor up-regulation in human amniotic fluid stem cell enhances nephroprotection after ischemia-reperfusion injury in the rat. Crit Care Med. 2017;45:e86–96.
  • Xue J, Qin Z, Li X, et al. Protective effects of ischemic preconditioning-mediated homing of endothelial progenitor cells on renal acute ischemia and reperfusion injury in male rats. Ann Transplant. 2017;22:66–74.
  • Wang J, Wang F, Wang Z, et al. Protective effect of GDNF-engineered amniotic fluid-derived stem cells on the renal ischaemia reperfusion injury in vitro. Cell Prolif. 2018;51:e12400.
  • Aghajani Nargesi A, Lerman LO, Eirin A. Mesenchymal stem cell-derived extracellular vesicles for kidney repair: current status and looming challenges. Stem Cell Res Ther. 2017;8:273.
  • Ranghino A, Bruno S, Bussolati B, et al. The effects of glomerular and tubular renal progenitors and derived extracellular vesicles on recovery from acute kidney injury. Stem Cell Res Ther. 2017;8:24.
  • Dominguez JH, Liu Y, Gao H, et al. Renal tubular cell-derived extracellular vesicles accelerate the recovery of established renal ischemia reperfusion injury. J Am Soc Nephrol JASN. 2017;28:3533–3544.
  • Gu D, Zou X, Ju G, et al. Mesenchymal stromal cells derived extracellular vesicles ameliorate acute renal ischemia reperfusion injury by inhibition of mitochondrial fission through miR-30. Stem Cells Int. 2016;2016:2093940.
  • Zhang G, Zou X, Miao S, et al. The anti-oxidative role of micro-vesicles derived from human Wharton-Jelly mesenchymal stromal cells through NOX2/gp91(phox) suppression in alleviating renal ischemia-reperfusion injury in rats. PloS One. 2014;9:e92129.
  • Lin K-C, Yip H-K, Shao P-L, et al. Combination of adipose-derived mesenchymal stem cells (ADMSC) and ADMSC-derived exosomes for protecting kidney from acute ischemia-reperfusion injury. Int J Cardiol. 2016;216:173–185.
  • Bai M, Zhang L, Fu B, et al. IL-17A improves the efficacy of mesenchymal stem cells in ischemic-reperfusion renal injury by increasing Treg percentages by the COX-2/PGE2 pathway. Kidney Int. 2018;93:814–825.
  • Zhang W, Liu L, Huo Y, et al. Hypoxia-pretreated human MSCs attenuate acute kidney injury through enhanced angiogenic and antioxidative capacities. BioMed Res Int. 2014;2014:462472.
  • Hussein AM, Barakat N, Awadalla A, et al. Modulation of renal ischemia/reperfusion in rats by a combination of ischemic preconditioning and adipose-derived mesenchymal stem cells (ADMSCs). Can J Physiol Pharmacol. 2016;94:936–946.
  • Lee Y, Kim M, Han J, et al. MicroRNA genes are transcribed by RNA polymerase II. Embo J. 2004;23:4051–4060.
  • Godwin JG, Ge X, Stephan K, et al. Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci U S A. 2010;107:14339–14344.
  • Kaucsár T, Révész C, Godó M, et al. Activation of the miR-17 family and miR-21 during murine kidney ischemia-reperfusion injury. Nucleic Acid Ther. 2013;23:344–354.
  • Narayanan SV, Dave KR, Perez-Pinzon MA. Ischemic preconditioning and clinical scenarios. Curr Opin Neurol. 2013;26:1–7.
  • Xu X, Kriegel AJ, Liu Y, et al. Delayed ischemic preconditioning contributes to renal protection by upregulation of miR-21. Kidney Int. 2012;82:1167–1175.
  • Yu S-Y, Tang L, Zhou S-H. Long noncoding RNAs: new players in ischaemia-reperfusion injury. Heart Lung Circ. 2018;27:322–332.
  • Kölling M, Genschel C, Kaucsar T, et al. Hypoxia-induced long non-coding RNA Malat1 is dispensable for renal ischemia/reperfusion-injury. Sci Rep. 2018;8. doi:10.1038/s41598-018-21720-3.
  • Chatauret N, Thuillier R, Hauet T. Preservation strategies to reduce ischemic injury in kidney transplantation: pharmacological and genetic approaches. Curr Opin Organ Transpl. 2011;16:180–187.
  • Jiang S-J, Li W, An W. Adenoviral gene transfer of hepatic stimulator substance confers resistance against hepatic ischemia-reperfusion injury by improving mitochondrial function. Hum Gene Ther. 2013;24:443–456.
  • Zhao Y-P, Li L, Ma J-P, et al. LXRalpha gene downregulation by lentiviral-based RNA interference enhances liver function after fatty liver transplantation in rats. Hepatobiliary Pancreat Dis Int HBPD INT. 2015;14:386–393.
  • Del Sorbo L, Costamagna A, Muraca G, et al. Intratracheal administration of small interfering RNA targeting fas reduces lung ischemia-reperfusion injury. Crit Care Med. 2016;44:e604–613.
  • Hou L, Chen G, Feng B, et al. Small interfering RNA targeting TNF-α gene significantly attenuates renal ischemia-reperfusion injury in mice. J Huazhong Univ Sci Technol Med Sci Hua Zhong Ke Ji Xue Xue Bao Yi Xue Ying Wen Ban Huazhong Keji Daxue Xuebao Yixue Yingdewen Ban. 2016;36:634–638.
  • Zheng X, Zang G, Jiang J, et al. Attenuating ischemia-reperfusion injury in kidney transplantation by perfusing donor organs with siRNA cocktail solution. Transplantation. 2016;100:743–752. .
  • de Ramon L, Jarque M, Ripoll E, et al. RNAi-based therapy in experimental ischemia-reperfusion injury. The New Targets Curr Pharm Des. 2016;22:4651–4657.
  • Yoshitomi T, Hirayama A, Nagasaki Y. The ROS scavenging and renal protective effects of pH-responsive nitroxide radical-containing nanoparticles. Biomaterials. 2011;32:8021–8028.
  • Jedrzejczyk D, Gendaszewska-Darmach E, Pawlowska R, et al. Designing synthetic RNA for delivery by nanoparticles. J Phys Condens Matter Inst Phys J. 2017;29:123001.
  • Zuk A, Palevsky PM, Fried L, et al. Overcoming translational barriers in acute kidney injury: A report from an NIDDK workshop. Clin J Am Soc Nephrol CJASN. 2018;13:1113–1123.

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