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Review

Aged kidney: can we protect it? Autophagy, mitochondria and mechanisms of ischemic preconditioning

ORCID Icon, , , , , , & show all
Pages 1291-1309 | Received 31 Dec 2017, Accepted 23 May 2018, Published online: 25 Jul 2018

References

  • United Nations. Department of Economic and Social Affairs, Population Division. World Population Ageing 2015. 2015; (ST/ESA/SER.A/390).
  • Rewa O, Bagshaw SM. Acute kidney injury-epidemiology, outcomes and economics. Nat Rev Nephrol. 2014;10:193–207. PMID:24445744
  • Bagshaw SM, Laupland KB, Doig CJ, et al. Prognosis for long-term survival and renal recovery in critically ill patients with severe acute renal failure: a population-based study. Crit Care. 2005;9:R700–9. PMID:16280066
  • Xue JL. Incidence and mortality of acute renal failure in medicare beneficiaries, 1992 to 2001. J Am Soc Nephrol. 2006;17:1135–1142. PMID:16495381
  • Huang J, Klionsky DJ. Autophagy and human disease. Cell Cycle. 2007;6:1837–1849. PMID:17671424
  • Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;19:5720–5728. PMID:11060023
  • Periyasamy-Thandavan S, Jiang M, Wei Q, et al. Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells. Kidney Int. 2008;74:631–640. PMID:18509315
  • Takahashi A, Kimura T, Takabatake Y, et al. Autophagy guards against cisplatin-induced acute kidney injury. Am J Pathol. 2012;180:517–525. PMID:22265049
  • Liu S, Hartleben B, Kretz O, et al. Autophagy plays a critical role in kidney tubule maintenance, aging and ischemia-reperfusion injury. Autophagy. 2012;8:826–837. PMID:22617445
  • Li L, Wang ZV, Hill JA, et al. New autophagy reporter mice reveal dynamics of proximal tubular autophagy. J Am Soc Nephrol. 2014;25:305–315. PMID:24179166
  • Zhang Y-L, Zhang J, Cui L-Y, et al. Autophagy activation attenuates renal ischemia-reperfusion injury in rats. Exp Biol Med. 2015;240:1590–1598. PMID:25898836
  • Isaka Y, Suzuki C, Abe T, et al. Bcl-2 protects tubular epithelial cells from ischemia/reperfusion injury by dual mechanisms. Transplant Proc. 2009;41:52–54. PMID:19249473
  • Ko GJ, Bae SY, Hong YA, et al. Radiocontrast-induced nephropathy is attenuated by autophagy through regulation of apoptosis and inflammation. Hum Exp Toxicol. 2016;35:724–736. PMID:26384705
  • Li T, Liu Y, Zhao J, et al. Aggravation of acute kidney injury by mPGES-2 down regulation is associated with autophagy inhibition and enhanced apoptosis. Sci Rep. 2017;7. PMID:28860615. DOI:10.1038/s41598-017-10271-8
  • Mei S, Livingston M, Hao J, et al. Autophagy is activated to protect against endotoxic acute kidney injury. Sci Rep. 2016;6. PMID:26916346. DOI:10.1038/srep22171
  • Karagiannidis I, Kataki A, Glustianou G, et al. Extended cytoprotective effect of autophagy in the late stages of sepsis and fluctuations in signal transduction pathways in a rat experimental model of kidney injury. Shock. 2016;45:139–147.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222. PMID:26799652
  • Jankauskas SS, Pevzner IB, Andrianova NV, et al. The age-associated loss of ischemic preconditioning in the kidney is accompanied by mitochondrial dysfunction, increased protein acetylation and decreased autophagy. Sci Rep. 2017;7. PMID:28294175. DOI:10.1038/srep44430
  • Wesselborg S, Stork B. Autophagy signal transduction by ATG proteins: from hierarchies to networks. Cell Mol Life Sci. 2015;72:4721–4757. PMID:26390974
  • Kimura T, Takabatake Y, Takahashi A, et al. Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J Am Soc Nephrol. 2011;22:902–913. PMID:21493778
  • Jiang M, Wei Q, Dong G, et al. Autophagy in proximal tubules protects against acute kidney injury. Kidney Int. 2012;82:1271–1283. PMID:22854643
  • Maejima I, Takahashi A, Omori H, et al. Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J. 2013;32:2336–2347. PMID:23921551
  • Jiang M, Liu K, Luo J, et al. Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. Am J Pathol. 2010;176:1181–1192. PMID:20075199
  • Todorovic Z, Medic B, Basta-Jovanovic G, et al. Acute pretreatment with chloroquine attenuates renal I/R injury in rats. PLoS ONE. 2014;9. PMID:24681567. DOI:10.1371/journal.pone.0092673
  • Ling H, Chen H, Wei M, et al. The effect of autophagy on inflammation cytokines in renal ischemia/Reperfusion injury. Inflammation. 2016;39:347–356. PMID:26412257
  • Li H, Peng X, Wang Y, et al. Atg5-mediated autophagy deficiency in proximal tubules promotes cell cycle G 2/M arrest and renal fibrosis. Autophagy. 2016;12:1472–1486.
  • Baisantry A, Bhayana S, Rong S, et al. Autophagy induces prosenescent changes in proximal tubular S3 segments. J Am Soc Nephrol. 2016;27:1609–1616. PMID:26487561
  • Rabb H, Griffin MD, McKay DB, et al. Inflammation in AKI: current understanding, key questions, and knowledge gaps. J Am Soc Nephrol. 2016;27:371–379. PMID:26561643
  • Costello-White R, Ryff CD, Coe CL. Aging and low-grade inflammation reduce renal function in middle-aged and older adults in Japan and the USA. Age (Dordr). 2015;37. PMID:26187318. DOI:10.1007/s11357-015-9808-7.
  • Lapaquette P, Guzzo J, Bretillon L, et al. Cellular and molecular connections between autophagy and inflammation. Mediators Inflamm. 2015;2015:398483. PMID:26221063
  • Isaka Y, Takabatake Y, Takahashi A, et al. Hyperuricemia-induced inflammasome and kidney diseases. Nephrol Dial Transplant. 2016;31:890–896. PMID:25829326
  • Deretic V, Kimura T, Timmins G, et al. Immunologic manifestations of autophagy. J Clin Invest. 2015;125:75–84. PMID:25654553
  • Nakahira K, Haspel JA, Rathinam VAK, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 2011;12:222–230. PMID:21151103
  • O’Neill LAJ, Kishton RJ, Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol. 2016;16:553–565. PMID:27396447
  • Bolignano D, Mattace-Raso F, Sijbrands EJG, et al. The aging kidney revisited: a systematic review. Ageing Res Rev. 2014;14:65–80. PMID:24548926
  • Yamamoto T, Takabatake Y, Kimura T, et al. Time-dependent dysregulation of autophagy: implications in aging and mitochondrial homeostasis in the kidney proximal tubule. Autophagy. 2016;12:801–813. PMID:26986194
  • Hartleben B, Gödel M, Meyer-Schwesinger C, et al. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J Clin Invest. 2010;120:1084–1096. PMID:20200449. doi:10.1172/JCI39492.
  • Kimura T, Jia J, Kumar S, et al. Dedicated SNAREs and specialized TRIM cargo receptors mediate secretory autophagy. EMBO J. 2017;36:42–60. PMID:27932448
  • Dupont N, Jiang S, Pilli M, et al. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. EMBO J. 2011;30:4701–4711. PMID:22068051
  • Baisantry A, Bhayana S, Wrede C, et al. The impact of autophagy on the development of senescence in primary tubular epithelial cells. Cell Cycle. 2016;15:2973–2979. PMID:27715411
  • Sturmlechner I, Durik M, Sieben CJ, et al. Cellular senescence in renal ageing and disease. Nat Rev Nephrol. 2017;13:77–89. PMID:28029153
  • Cui J, Bai X-Y, Shi S, et al. Age-related changes in the function of autophagy in rat kidneys. Age. 2012;34:329–339.
  • Kume S, Uzu T, Horiike K, et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Investig. 2010;120:1043–1055.
  • Sato T, Tauchi H, Kohtani K. Morphometric studies on the age changes of autofluorescent granules and lysosomes in the epithelial cells of rat kidneys. Mech Ageing Dev. 1984;25:237–242.
  • Xu H, Ren D. Lysosomal Physiology. Annu Rev Physiol. 2015;77:57–80. PMID:25668017.
  • Schneider JL, Villarroya J, Diaz-Carretero A, et al. Loss of hepatic chaperone-mediated autophagy accelerates proteostasis failure in aging. Aging Cell. 2015;14:249–264. PMID:25620427
  • Mariño G, Pietrocola F, Madeo F, et al. Caloric restriction mimetics: natural/physiological pharmacological autophagy inducers. Autophagy. 2014;10:1879–1882. PMID:25484097
  • Wohlgemuth SE, Julian D, Akin DE, et al. Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation Res. 2007;10:281–292. PMID:17665967
  • Jia K, Levine B. Autophagy is required for dietary restriction-mediated life span extension in C. elegans. Autophagy. 2007;3:597–599.
  • Lee SH, Min KJ. Caloric restriction and its mimetics. BMB Rep. 2013;46:181–187. PMID:23615258
  • Mitchell JR, Verweij M, Brand K, et al. Short term dietary restriction and fasting precondition against ischemia reperfusion injury in mice. Aging Cell. 2010;9:40–53.
  • Lempiäinen J, Finckenberg P, Mervaala EE, et al. Caloric restriction ameliorates kidney ischaemia/reperfusion injury through PGC-1α-eNOS pathway and enhanced autophagy. Acta Physiologica. 2013;208:410–421. PMID:23710679
  • Ning Y-C, Cai G-Y, Zhuo L, et al. Beneficial effects of short-term calorie restriction against cisplatin-induced acute renal injury in aged rats. Nephron Exp Nephrology. 2013;124:19–27. PMID:24401898
  • Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci. 2009;122:3589–3594. PMID:19812304
  • Harrison DE, Strong R, Sharp ZD, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009;460:392–395. PMID:19587680
  • Speakman JR, Mitchell SE, Mazidi M. Calories or protein? The effect of dietary restriction on lifespan in rodents is explained by calories alone. Exp Gerontol. 2016;86:28–38. PMID:27006163
  • Chen J, Gao J, Sun W, et al. Involvement of exogenous H2S in recovery of cardioprotection from ischemic post-conditioning via increase of autophagy in the aged hearts. Int J Cardiol. 2016;220:681–692. PMID:27393850
  • Grahammer F, Haenisch N, Steinhardt F, et al. mTORC1 maintains renal tubular homeostasis and is essential in response to ischemic stress. Proc Natl Acad Sci. 2014;111:E2817–26. PMID:24958889
  • Nakagawa S, Nishihara K, Inui KI, et al. Involvement of autophagy in the pharmacological effects of the mTOR inhibitor everolimus in acute kidney injury. Eur J Pharmacol. 2012;696:143–154. PMID:23022334
  • Lieberthal W, Fuhro R, Andry CC, et al. Rapamycin impairs recovery from acute renal failure: role of cell-cycle arrest and apoptosis of tubular cells. Am J Physiol Renal Physiol. 2001;281:F693–706.
  • Lui SL, Chan KW, Tsang R, et al. Effect of rapamycin on renal ischemia-reperfusion injury in mice. Transpl Int. 2006;19:834–839. PMID:16961776
  • Goncalves GM, Cenedeze MA, Feitoza CQ, et al. The role of heme oxygenase 1 in rapamycin-induced renal dysfunction after ischemia and reperfusion injury. Kidney Int. 2006;70:1742–1749. PMID:17003813
  • Demyanenko IA, Popova EN, Zakharova VV, et al. Mitochondria-targeted antioxidant SkQ1 improves impaired dermal wound healing in old mice. Aging. 2015;7:475–485. PMID:26187706
  • Cheng H, Fan X, Lawson WE, et al. Telomerase deficiency delays renal recovery in mice after ischemia-reperfusion injury by impairing autophagy. Kidney Int. 2015;88:85–94. PMID:25760322
  • Fervenza FC, Fitzpatrick PM, Mertz J, et al. Acute rapamycin nephrotoxicity in native kidneys of patients with chronic glomerulopathies. Nephrol Dial Transplant. 2004;19:1288–1292. PMID:15102967
  • Coombes JD, Mreich E, Liddle C, et al. Rapamycin worsens renal function and intratubular cast formation in protein overload nephropathy. Kidney Int. 2005;68:2599–2607. PMID:16316336
  • Hommos MS, Glassock RJ, Rule AD. Structural and functional changes in human kidneys with healthy aging. J Am Soc Nephrol. 2017;28:2838–2844. PMID:28790143
  • Declèves AE, Sharma K, Satriano J. Beneficial effects of AMP-activated protein kinase agonists in kidney ischemia-reperfusion: autophagy and cellular stress markers. Nephron Exp Nephrol. 2014;128:98–110.
  • Glaumann B, Glaumann H, Berezesky IK, et al. Studies on the pathogenesis of ischemic cell injury. II. Morphological changes of the pars convoluta (P1 and P2) of the proximal tubule of the rat kidney made ischemic in vivo. Virchows Arch B Cell Pathol. 1975;19:281–302.
  • Glaumann B, Trump BF. Studies on the pathogenesis of ischemic cell injury. III. Morphological changes of the proximal pars recta tubules (P3) of the rat kidney made ischemic in vivo. Virchows Arch B Cell Pathol. 1975;19:303–323.
  • Zorov DB, Popkov VA, Zorova LD, et al. Mitochondrial aging: is there a mitochondrial clock? J Gerontol A Biol Sci Med Sci. 2017;72:1171–1179. PMID:27927758
  • Plotnikov EY, Kazachenko AV, Vyssokikh MY, et al. The role of mitochondria in oxidative and nitrosative stress during ischemia/reperfusion in the rat kidney. Kidney Int. 2007;72:1493–1502.
  • Vogt MT, Farber E. On the molecular pathology of ischemic renal cell death. Reversible and irreversible cellular and mitochondrial metabolic alterations. Am J Pathol. 1968;53:1–26.
  • Wilson DR, Arnold PE, Burke TJ, et al. Mitochondrial calcium accumulation and respiration in ischemic acute renal failure in the rat. Kidney Int. 1984;25:519–526. PMID:6737843
  • Morales AI, Detaille D, Prieto M, et al. Metformin prevents experimental gentamicin-induced nephropathyby a mitochondria-dependent pathway. Kidney Int. 2010;77:861–869. PMID:20164825
  • Patil NK, Parajuli N, MacMillan-Crow LA, et al. Inactivation of renal mitochondrial respiratory complexes and manganese superoxide dismutase during sepsis: mitochondria-targeted antioxidant mitigates injury. AJP: Ren Physiol. 2014;306:F734–43. PMID:24500690
  • Lowes DA, Webster NR, Murphy MP, et al. Antioxidants that protect mitochondria reduce interleukin-6 and oxidative stress, improve mitochondrial function, and reduce biochemical markers of organ dysfunction in a rat model of acute sepsis. Br J Anaesth. 2013;110:472–480. PMID:23381720
  • Molitoris BA. Actin cytoskeleton in ischemic acute renal failure. Kidney Int. 2004;66:871–883. PMID:15253754
  • Schrier RW, Wang W, Poole B, et al. Acute renal failure: definitions, diagnosis, pathogenesis, and therapy. J Clin Investig. 2004;114:5–14. PMID:15232604
  • St-Pierre J, Brand MD, Boutilier RG. Mitochondria as ATP consumers: cellular treason in anoxia. Proc Natl Acad Sci. 2000;97:8670–8674. PMID:10890886
  • Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev. 2014;94:909–950. PMID:24987008
  • Dikalov S. Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med. 2011;51:1289–1301. PMID:21777669
  • Plotnikov EY, Grebenchikov OA, Babenko VA, et al. Nephroprotective effect of GSK-3β inhibition by lithium ions and δ-opioid receptor agonist dalargin on gentamicin-induced nephrotoxicity. Toxicol Lett. 2013;220:303–308. PMID:23651617
  • Walker PD, Shah SV. Evidence suggesting a role for hydroxyl radical in gentamicin-induced acute renal failure in rats. J Clin Investig. 1988;81:334–341. PMID:3123518
  • Plotnikov EY, Chupyrkina AA, Pevzner IB, et al. Myoglobin causes oxidative stress, increase of NO production and dysfunction of kidney’s mitochondria. Biochim Biophys Acta. 2009;1792:796–803. PMID:19545623
  • Sahu BD, Kuncha M, Putcha UK, et al. Effect of metformin against cisplatin induced acute renal injury in rats: A biochemical and histoarchitectural evaluation. Exp Toxicologic Pathol. 2013;65:933–940. PMID:23395153
  • Bin DS, Yang SK, Zhou QY, et al. Mitochondria-targeted peptides prevent on contrast-induced acute kidney injury in the rats with hypercholesterolemia. Ren Fail. 2013;35:1124–1129. PMID:23879473
  • Walker PD, Shah SV. Gentamicin enhanced production of hydrogen peroxide by renal cortical mitochondria. Am J Physiol. 1987;253:C495–9.
  • Bernardi P, Krauskopf A, Basso E, et al. The mitochondrial permeability transition from in vitro artifact todisease target. FEBS J. 2006;273:2077–2099.
  • Ravagnan L, Roumier T, Kroemer G. Mitochondria, the killer organelles and their weapons. J Cell Physiol. 2002;192:131–137. PMID:12115719
  • Nakagawa T, Shimizu S, Watanabe T, et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 2005;434:652–658. PMID:15800626
  • Jankauskas SS, Andrianova NV, Alieva IB, et al. Dysfunction of kidney endothelium after ischemia/reperfusion and its prevention by mitochondria-targeted antioxidant. Biochemistry (Moscow). 2016;81:1538–1548. PMID:28259131
  • Dikalova AE, Itani HA, Nazarewicz RR, et al. Sirt3 impairment and SOD2 hyperacetylation in vascular oxidative stress and hypertension. Circ Res. 2017;121:564–574. PMID:28684630
  • Kwon O, Phillips CL, Molitoris BA. Ischemia induces alterations in actin filaments in renal vascular smooth muscle cells. Am J Physiol Renal Physiol. 2002;282:F1012–9. PMID:11997317
  • Bienert GP, Schjoerring JK, Jahn TP. Membrane transport of hydrogen peroxide. Biochim Biophys Acta. 2006;1758:994–1003. PMID:16566894
  • Koyner JL, Sher Ali R, Murray PT. Antioxidants. Do they have a place in the prevention or therapy of acute kidney injury? Nephron Exp Nephrology. 2008;109:e109–17. PMID:18802373
  • Zorov DB, Plotnikov EY, Jankauskas SS, et al. The phenoptosis problem: what is causing the death of an organism? Lessons from acute kidney injury. Biochemistry (Mosc). 2012;77:742–753. PMID:22817538
  • Plotnikov EY, Silachev DN, Jankauskas SS, et al. Mild uncoupling of respiration and phosphorylation as a mechanism providing nephro- and neuroprotective effects of penetrating cations of the SkQ family. Biochemistry (Moscow). 2012;77:1029–1037. PMID:23157263
  • Jankauskas SS, Plotnikov EY, Morosanova MA, et al. Mitochondria-targeted antioxidant SkQR1 ameliorates gentamycin-induced renal failure and hearing loss. Biochemistry (Moscow). 2012;77:666–670. PMID:22817467
  • Plotnikov EY, Chupyrkina AA, Jankauskas SS, et al. Mechanisms of nephroprotective effect of mitochondria-targeted antioxidants under rhabdomyolysis and ischemia/reperfusion. Biochimica Biophysica Acta Molecular Basis Disease. 2011; 1812:77–86. PMID:20884348. DOI:10.1016/j.bbadis.2010.09.008.
  • Plotnikov EY, Morosanova MA, Pevzner IB, et al. Protective effect of mitochondria-targeted antioxidants in an acute bacterial infection. Proc Natl Acad Sci U S A. 2013;110:E3100–8. PMID:23898194
  • Mitchell T, Rotaru D, Saba H, et al. The mitochondria-targeted antioxidant mitoquinone protects against cold storage injury of renal tubular cells and rat kidneys. J Pharmacol Exp Ther. 2011;336:682–692. PMID:21159749
  • Mukhopadhyay P, Horváth B, Zsengellér Z, et al. Mitochondrial-targeted antioxidants represent a promising approach for prevention of cisplatin-induced nephropathy. Free Radic Biol Med. 2012;52:497–506. PMID:22120494
  • Ramsey H, Wu MX. Mitochondrial anti-oxidant protects IEX-1 deficient mice from organ damage during endotoxemia. Int Immunopharmacol. 2014;23:658–663. PMID:25466275
  • Birk AV, Liu S, Soong Y, et al. The mitochondrial-targeted compound SS-31 re-energizes ischemic mitochondria by interacting with cardiolipin. J Am Soc Nephrol. 2013;24:1250–1261. PMID:23813215
  • Szeto HH, Liu S, Soong Y, et al. Mitochondria-targeted peptide accelerates ATP recovery and reduces ischemic kidney injury. J Am Soc Nephrol. 2011;22:1041–1052. PMID:21546574
  • Mizuguchi Y, Chen J, Seshan SV, et al. A novel cell-permeable antioxidant peptide decreases renal tubular apoptosis and damage in unilateral ureteral obstruction. Am J Physiology-Renal Physiol. 2008;295:F1545–53. PMID:18784263
  • Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997;416:15–18.
  • Antonenko YN, Denisov SS, Silachev DN, et al. A long-linker conjugate of fluorescein and triphenylphosphonium as mitochondria-targeted uncoupler and fluorescent neuro- and nephroprotector. Biochimica Et Biophysica Acta - General Subjects. 2016; 1860:2463–2473. PMID:27450891. DOI:10.1016/j.bbagen.2016.07.014.
  • Zakharova VV, Pletjushkina OY, Galkin II, et al. Low concentration of uncouplers of oxidative phosphorylation decreases the TNF-induced endothelial permeability and lethality in mice. Biochimica Biophysica Acta Molecular Basis Disease. 2017;1863:968–977. PMID:28131916
  • Romaschenko VP, Zinovkin RA, Galkin II, et al. Low concentrations of uncouplers of oxidative phosphorylation prevent inflammatory activation of endothelial cells by tumor necrosis factor. Biochemistry Biokhimii︠A︡. 2015;80:610–619. PMID:26071781
  • Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124–1136. PMID:3769170
  • Kapitsinou PP, Haase VH. Molecular mechanisms of ischemic preconditioning in the kidney. Am J Physiol Ren Physiol. 2015. ajprenal.00224.2015. PMID:26311114. DOI:10.1152/ajprenal.00224.2015
  • Cochrane J, Williams BT, Banerjee A, et al. Ischemic preconditioning attenuates functional, metabolic, and morphologic injury from ischemic acute renal failure in the rat. Ren Fail. 1999;21:135–145.
  • Park KM, Chen A, Bonventre JV. Prevention of kidney ischemia/reperfusion-induced functional injury and JNK, p38, and MAPK kinase activation by remote ischemic pretreatment. J Biol Chem. 2001;276:11870–11876. PMID:11150293
  • Weng X, Shen H, Kuang Y, et al. Ischemic postconditioning inhibits the renal fibrosis induced by ischemia-reperfusion injury in rats. Urology. 2012;80:484 e1–7. PMID:22578919
  • Diwan V, Jaggi AS, Singh M, et al. Possible involvement of erythropoietin in remote renal preconditioning- induced cardioprotection in rats. J Cardiovasc Pharmacol. 2008;51:126–130. PMID:18287879
  • Silachev DN, Isaev NK, Pevzner IB, et al. The mitochondria-targeted antioxidants and remote kidney preconditioning ameliorate brain damage through kidney-to-brain cross-talk. PloS One. 2012;7:e51553. PMID:23272118
  • Sedaghat Z, Kadkhodaee M, Seifi B, et al. Remote preconditioning reduces oxidative stress, downregulates cyclo-oxygenase-2 expression and attenuates ischaemia-reperfusion-induced acute kidney injury. Clin Exp Pharmacol Physiol. 2013;40:97–103. PMID:23240616
  • Hausenloy DJ, Lim SY, Ong SG, et al. Mitochondrial cyclophilin-D as a critical mediator of ischaemic preconditioning. Cardiovasc Res. 2010;88:67–74. PMID:20400621
  • Devalaraja-Narashimha K, Diener AM, Padanilam BJ. Cyclophilin D gene ablation protects mice from ischemic renal injury. Am J Physiol Renal Physiol. 2009;297:F749–59. PMID:19553348
  • Ying Y, Padanilam BJ. Regulation of necrotic cell death: p53, PARP1 and cyclophilin D-overlapping pathways of regulated necrosis? Cell Mol Life Sci. 2016;73:2309–2324. PMID:27048819
  • Lemoine S, Pillot B, Rognant N, et al. Postconditioning with cyclosporine a reduces early renal dysfunction by inhibiting mitochondrial permeability transition. Transplantation. 2015;99:717–723. PMID:25793558
  • Singh D, Chander V, Chopra K. Cyclosporine protects against ischemia/reperfusion injury in rat kidneys. Toxicology. 2005;207:339–347. PMID:15664262
  • Bao H, Ge Y, Zhuang S, et al. Inhibition of glycogen synthase kinase-3Β prevents NSAID-induced acute kidney injury. Kidney Int. 2012;81:662–673. PMID:22258319
  • Bao H, Ge Y, Wang Z, et al. Delayed administration of a single dose of lithium promotes recovery from AKI. J Am Soc Nephrol. 2014;25:488–500. PMID:24408869
  • Talab SS, Elmi A, Emami H, et al. Protective effects of acute lithium preconditioning against renal ischemia/reperfusion injury in rat: role of nitric oxide and cyclooxygenase systems. Eur J Pharmacol. 2012;681:94–99. PMID:22342279
  • Ma D, Lim T, Xu J, et al. Xenon preconditioning protects against renal ischemic-reperfusion injury via HIF-1 activation. J Am Soc Nephrol. 2009;20:713–720. PMID:19144758
  • Zhao H, Yoshida A, Xiao W, et al. Xenon treatment attenuates early renal allograft injury associated with prolonged hypothermic storage in rats. FASEB J. 2013;27:4076–4088. PMID:23759444
  • Jia P, Teng J, Zou J, et al. Intermittent exposure to xenon protects against gentamicin-induced nephrotoxicity. PLoS ONE. 2013;8. PMID:23737979. DOI:10.1371/journal.pone.0064329
  • Wang Y, Huang WC, Wang CY, et al. Inhibiting glycogen synthase kinase-3 reduces endotoxaemic acute renal failure by down-regulating inflammation and renal cell apoptosis. Br J Pharmacol. 2009;157:1004–1013. PMID:19508392
  • Lochhead KM, Kharasch ED, Zager RA. Anesthetic effects on the glycerol model of rhabdomyolysis-induced acute renal failure in rats. J Am Soc Nephrol. 1998;9:305–309.
  • Meerwein C, Korom S, Arni S, et al. The effect of low-dose continuous erythropoietin receptor activator in an experimental model of acute Cyclosporine A induced renal injury. Eur J Pharmacol. 2011;671:113–119. PMID:21968143
  • Eshraghi-Jazi F, Nematbakhsh M, Pezeshki Z, et al. Sex differences in protective effect of recombinant human erythropoietin against cisplatin-induced nephrotoxicity in rats. Iran J Kidney Dis. 2013;7:383–389. PMID: 24072151
  • Salahudeen AK, Haider N, Jenkins J, et al. Antiapoptotic properties of erythropoiesis-stimulating proteins in models of cisplatin-induced acute kidney injury. AJP: Ren Physiol. 2008;294:F1354–65. PMID:18385271
  • Nemoto T, Yokota N, Keane WF, et al. Recombinant erythropoietin rapidly treats anemia in ischemic acute renal failure. Kidney Int. 2001;59:246–251. PMID:11135077
  • Sharples EJ, Patel N, Brown P, et al. Erythropoietin protects the kidney against the injury and dysfunction caused by ischemia-reperfusion. J Am Soc Nephrol. 2004;15:2115–2124. PMID:15284297
  • Yang FL, Subeq YM, Chiu YH, et al. Recombinant human erythropoietin reduces rhabdomyolysis-induced acute renal failure in rats. Injury. 2012;43:367–373. PMID:22209169
  • Mitra A, Bansal S, Wang W, et al. Erythropoietin ameliorates renal dysfunction during endotoxaemia. Nephrol Dial Transplant. 2007;22:2349–2353. PMID:17438005
  • Stoyanoff TR, Todaro JS, Aguirre MV, et al. Amelioration of lipopolysaccharide-induced acute kidney injury by erythropoietin: involvement of mitochondria-regulated apoptosis. Toxicology. 2014;318:13–21. PMID:24561306
  • Harman D. The aging process. Proc Natl Acad Sci U S A. 1981.;78:7124–7128. PMID: 6947277
  • Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Moscow). 2005;70:200–214. PMID:15807660
  • Trifunovic A, Wredenberg A, Falkenberg M, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature. 2004;429:417–423. PMID:15164064
  • Latorre-Pellicer A, Moreno-Loshuertos R, Lechuga-Vieco AV, et al. Corrigendum: mitochondrial and nuclear DNA matching shapes metabolism and healthy ageing. Nature. 2016;542:124. PMID:27926738
  • Bailey PJ, Webster GC. Lowered rates of protein synthesis by mitochondria isolated from organisms of increasing age. Mech Ageing Dev. 1984;24:233–241. PMID:6425575
  • Pokkunuri I, Ali Q, Asghar M. Grape powder improves age-related decline in mitochondrial and kidney functions in fischer 344 rats. Oxid Med Cell Longev. 2016;2016. DOI:10.1155/2016/6135319
  • Yarian CS, Toroser D, Sohal RS. Aconitase is the main functional target of aging in the citric acid cycle of kidney mitochondria from mice. Mech Ageing Dev. 2006;127:79–84. PMID:16289253
  • Choksi KB, Nuss JE, DeFord JH, et al. Mitochondrial electron transport chain functions in long-lived Ames dwarf mice. Aging. 2011;3:754–767. PMID:21934186
  • Rocha-Rodrigues S, Santos-Alves E, Coxito PM, et al. Combined effects of aging and in vitro non-steroid anti-inflammatory drugs on kidney and liver mitochondrial physiology. Life Sci. 2013;93:329–337.
  • Larsson N-G. Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem. 2010;79:683–706. PMID:20350166
  • Ahlqvist KJ, Hämäläinen RH, Yatsuga S, et al. Somatic progenitor cell vulnerability to mitochondrial DNA mutagenesis underlies progeroid phenotypes in polg mutator mice. Cell Metab. 2012;15:100–109. PMID:22225879
  • Katajisto P, Döhla J, Chaffer CL, et al. Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science. 2015;348:340–343. PMID:25837514
  • Popkov VA, Plotnikov EY, Lyamzaev KG, et al. Mitodiversity. Biochemistry Biokhimiia. 2015;80:532–541. PMID:26071770
  • Chen H, Xing B, Wang L, et al. Aged kidneys are refractory to ischemic postconditioning in a rat model. Ren Fail. 2014;36:1575–1580. PMID:25156634
  • Zorov DB, Filburn CR, Klotz L-O, et al. Reactive oxygen species (Ros-Induced) Ros Release. J Exp Med. 2000;192:1001–1014. PMID:11015441
  • Boddi M, Sacchi S, Lammel RM, et al. Age-related and vasomotor stimuli-induced changes in renal vascular resistance detected by Doppler ultrasound. Am J Hypertens. 1996;9:461–466. PMID:8735177
  • Fuiano G, Sund S, Mazza G, et al. Renal hemodynamic response to maximal vasodilating stimulus in healthy older subjects. Kidney Int. 2001;59:1052–1058. PMID:11231360
  • Kim D. The activation of NF-kB through Akt-induced FOX01 phosphorylation during aging and its modulation by caloric restriction. Biogerontology. 2008;9:33–47.
  • Zhu J, Rebecchi MJ, Glass PSA, et al. Cardioprotection of the aged rat heart by GSK-3beta inhibitor is attenuated: age-related changes in mitochondrial permeability transition pore modulation. Am J Physiol Lung Cell Mol Physiol. 2011;300:H922–30. PMID:21217064
  • Saotome M, Katoh H, Yaguchi Y, et al. Transient opening of mitochondrial permeability transition pore by reactive oxygen species protects myocardium from ischemia-reperfusion injury. Am J Physiology-Heart Circulatory Physiol. 2009;296:H1125–32. PMID:19202002
  • Hausenloy D, Wynne A, Duchen M, et al. Transient mitochondrial permeability transition pore opening mediates ischemic preconditioning-induced protection. Circulation. 2004;109:1714–1717.
  • Arias E, Koga H, Diaz A, et al. Lysosomal mTORC2/PHLPP1/Akt regulate chaperone-mediated autophagy. Mol Cell. 2015;59:270–284. PMID:26118642
  • Moreno-Blas D, Gorostieta-Salas E, Castro-Obregón S. Connecting chaperone-mediated autophagy dysfunction to cellular senescence. Ageing Res Rev. 2018;41:34–41. PMID:29113832

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