857
Views
0
CrossRef citations to date
0
Altmetric
Acute Kidney Injury

Mitophagy mediated by HIF-1α/FUNDC1 signaling in tubular cells protects against renal ischemia/reperfusion injury

, , , , , , , , , , , & show all
Article: 2332492 | Received 12 Oct 2023, Accepted 14 Mar 2024, Published online: 07 Apr 2024

References

  • Hashemi SS, Janfeshan S, Karimi Z. Acute lung injury induced by acute uremia and renal ischemic-reperfusion injury: the role of toll-like receptors 2 and 4, and oxidative stress. Iran J Basic Med Sci. 2022;25(5):1–14. doi: 10.22038/ijbms.2022.64025.14099.
  • Ostermann M, Bellomo R, Burdmann EA, et al. Controversies in acute kidney injury: conclusions from a Kidney Disease: Improving Global Outcomes (KDIGO) Conference. Kidney Int. 2020;98(2):294–309. doi: 10.1016/j.kint.2020.04.020.
  • Noble RA, Lucas BJ, Selby NM. Long-term outcomes in patients with acute kidney injury. Clin J Am Soc Nephrol. 2020;15(3):423–429. doi: 10.2215/cjn.10410919.
  • Schödel J, Ratcliffe PJ. Mechanisms of hypoxia signalling: new implications for nephrology. Nat Rev Nephrol. 2019;15(10):641–659. doi: 10.1038/s41581-019-0182-z.
  • de Ponte MC, Cardoso VG, Gonçalves GL, et al. Early type 1 diabetes aggravates renal ischemia/reperfusion-induced acute kidney injury. Sci Rep. 2021;11(1):19028. doi: 10.1038/s41598-021-97839-7.
  • Zhang Z, Haimovich B, Kwon YS, et al. Unilateral partial nephrectomy with warm ischemia results in acute hypoxia inducible factor 1-alpha (HIF-1α) and Toll-like receptor 4 (TLR4) overexpression in a porcine model. PLOS One. 2016;11(5):e0154708. doi: 10.1371/journal.pone.0154708.
  • Shu S, Wang Y, Zheng M, et al. Hypoxia and hypoxia-inducible factors in kidney injury and repair. Cells. 2019;8(3):207. doi: 10.3390/cells8030207.
  • Bernhardt WM, Câmpean V, Kany S, et al. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol. 2006;17(7):1970–1978. doi: 10.1681/asn.2005121302.
  • Xu ZH, Wang C, He YX, et al. Hypoxia-inducible factor protects against acute kidney injury via the Wnt/β-catenin signaling pathway. Am J Physiol Renal Physiol. 2022;322(6):F611–F624. doi: 10.1152/ajprenal.00023.2022.
  • Rajendran G, Schonfeld MP, Tiwari R, et al. Inhibition of endothelial PHD2 suppresses post-ischemic kidney inflammation through hypoxia-inducible factor-1. J Am Soc Nephrol. 2020;31(3):501–516. doi: 10.1681/asn.2019050523.
  • Li X, Fang P, Mai J, et al. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J Hematol Oncol. 2013;6:19. doi: 10.1186/1756-8722-6-19.
  • Livingston MJ, Wang J, Zhou J, et al. Clearance of damaged mitochondria via mitophagy is important to the protective effect of ischemic preconditioning in kidneys. Autophagy. 2019;15(12):2142–2162. doi: 10.1080/15548627.2019.1615822.
  • Scott SV, Klionsky DJ. Delivery of proteins and organelles to the vacuole from the cytoplasm. Curr Opin Cell Biol. 1998;10(4):523–529. doi: 10.1016/s0955-0674(98)80068-9.
  • Tang C, Han H, Yan M, et al. PINK1-PRKN/PARK2 pathway of mitophagy is activated to protect against renal ischemia–reperfusion injury. Autophagy. 2018;14(5):880–897. doi: 10.1080/15548627.2017.1405880.
  • Liu L, Feng D, Chen G, et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol. 2012;14(2):177–185. doi: 10.1038/ncb2422.
  • Li X, Liu Q, Bao W, et al. Impact of blood pressure changes on myocardial work indices in hypertensive patients in a day. J Clin Hypertens. 2022;24(1):3–14. doi: 10.1111/jch.14379.
  • Li Q, Liu Y, Huang Q, et al. Hypoxia acclimation protects against heart failure postacute myocardial infarction via Fundc1-mediated mitophagy. Oxid Med Cell Longev. 2022;2022:8192552. doi: 10.1155/2022/8192552.
  • Cai Y, Yang E, Yao X, et al. FUNDC1-dependent mitophagy induced by tPA protects neurons against cerebral ischemia–reperfusion injury. Redox Biol. 2021;38:101792. doi: 10.1016/j.redox.2020.101792.
  • Li S, Zhou Y, Gu X, et al. NLRX1/FUNDC1/NIPSNAP1-2 axis regulates mitophagy and alleviates intestinal ischaemia/reperfusion injury. Cell Prolif. 2021;54(3):e12986. doi: 10.1111/cpr.12986.
  • Xiao Y, Chen W, Zhong Z, et al. Electroacupuncture preconditioning attenuates myocardial ischemia–reperfusion injury by inhibiting mitophagy mediated by the mTORC1–ULK1–FUNDC1 pathway. Biomed Pharmacother. 2020;127:110148. doi: 10.1016/j.biopha.2020.110148.
  • Lin Q, Li S, Jiang N, et al. Inhibiting NLRP3 inflammasome attenuates apoptosis in contrast-induced acute kidney injury through the upregulation of HIF1A and BNIP3-mediated mitophagy. Autophagy. 2021;17(10):2975–2990. doi: 10.1080/15548627.2020.1848971.
  • Wang J, Zhu P, Li R, et al. Fundc1-dependent mitophagy is obligatory to ischemic preconditioning-conferred renoprotection in ischemic AKI via suppression of Drp1-mediated mitochondrial fission. Redox Biol. 2020;30:101415. doi: 10.1016/j.redox.2019.101415.
  • Zhang W. The mitophagy receptor FUN14 domain-containing 1 (FUNDC1): a promising biomarker and potential therapeutic target of human diseases. Genes Dis. 2021;8(5):640–654. doi: 10.1016/j.gendis.2020.08.011.
  • Wu H, Wang Y, Li W, et al. Deficiency of mitophagy ­receptor FUNDC1 impairs mitochondrial quality and ­aggravates dietary-induced obesity and metabolic syndrome. Autophagy. 2019;15(11):1882–1898. doi: 10.1080/15548627.2019.1596482.
  • Cao Z, Wu Z, Duan T, et al. Curcumin ameliorates HO-induced injury through SIRT1–PERK–CHOP pathway in pancreatic beta cells. Acta Biochim Biophys Sin. 2022;54(3):370–377. doi: 10.3724/abbs.2022004.
  • Liao W, Fu Z, Zou Y, et al. MicroRNA-140-5p attenuated oxidative stress in cisplatin induced acute kidney injury by activating Nrf2/ARE pathway through a Keap1-independent mechanism. Exp Cell Res. 2017;360(2):292–302. doi: 10.1016/j.yexcr.2017.09.019.
  • Hosszu A, Antal Z, Lenart L, et al. σ1-receptor agonism protects against renal ischemia–reperfusion injury. J Am Soc Nephrol. 2017;28(1):152–165. doi: 10.1681/asn.2015070772.
  • Wei Q, Sun H, Song S, et al. MicroRNA-668 represses MTP18 to preserve mitochondrial dynamics in ischemic acute kidney injury. J Clin Invest. 2018;128(12):5448–5464. doi: 10.1172/jci121859.
  • Wang H, Liu N, Li R, et al. Nephropreventing effect of hypoxia-inducible factor 1α in a rat model of ischaemic/reperfusion acute kidney injury. Clin Exp Pharmacol Physiol. 2018;45(10):1076–1082. doi: 10.1111/1440-1681.12947.
  • Fu ZJ, Wang ZY, Xu L, et al. HIF-1α-BNIP3-mediated mitophagy in tubular cells protects against renal ischemia/reperfusion injury. Redox Biol. 2020;36:101671. doi: 10.1016/j.redox.2020.101671.
  • Li R, Zhou Y, Zhang S, et al. The natural (poly)phenols as modulators of microglia polarization via TLR4/NF-κB pathway exert anti-inflammatory activity in ischemic stroke. Eur J Pharmacol. 2022;914:174660. doi: 10.1016/j.ejphar.2021.174660.
  • Yu L, Wang Y, Guo YH, et al. HIF-1α alleviates high-glucose-induced renal tubular cell injury by promoting parkin/PINK1-mediated mitophagy. Front Med. 2021;8:803874. doi: 10.3389/fmed.2021.803874.
  • Zheng Y, Huang C, Lu L, et al. STOML2 potentiates metastasis of hepatocellular carcinoma by promoting PINK1-mediated mitophagy and regulates sensitivity to lenvatinib. J Hematol Oncol. 2021;14(1):16. doi: 10.1186/s13045-020-01029-3.
  • Sun Y, Wen F, Yan C, et al. Mitophagy protects the retina against anti-vascular endothelial growth factor therapy-driven hypoxia via hypoxia-inducible factor-1α signaling. Front Cell Dev Biol. 2021;9:727822. doi: 10.3389/fcell.2021.727822.
  • Zhou H, Zhu P, Wang J, et al. Pathogenesis of cardiac ischemia reperfusion injury is associated with CK2α-disturbed mitochondrial homeostasis via suppression of FUNDC1-related mitophagy. Cell Death Differ. 2018;25(6):1080–1093. doi: 10.1038/s41418-018-0086-7.
  • Molitoris BA. Actin cytoskeleton in ischemic acute renal failure. Kidney Int. 2004;66(2):871–883. doi: 10.1111/j.1523-1755.2004.00818.x.
  • Dan Dunn J, Alvarez LA, Zhang X, et al. Reactive oxygen species and mitochondria: a nexus of cellular homeostasis. Redox Biol. 2015;6:472–485. doi: 10.1016/j.redox.2015.09.005.
  • Cai C, Guo Z, Chang X, et al. Empagliflozin attenuates cardiac microvascular ischemia/reperfusion through activating the AMPKα1/ULK1/FUNDC1/mitophagy pathway. Redox Biol. 2022;63:102738. doi: 10.1016/j.redox.2022.102288.
  • Li L, Tan J, Miao Y, et al. ROS and autophagy: interactions and molecular regulatory mechanisms. Cell Mol Neurobiol. 2015;35(5):615–621. doi: 10.1007/s10571-015-0166-x.
  • De Gaetano A, Gibellini L, Zanini G, et al. Mitophagy and oxidative stress: the role of aging. Antioxidants. 2021;10(5):794. doi: 10.3390/antiox10050794.
  • Zhou H, Zhu P, Guo J, et al. Ripk3 induces mitochondrial apoptosis via inhibition of FUNDC1 mitophagy in cardiac IR injury. Redox Biol. 2017;13:498–507. doi: 10.1016/j.redox.2017.07.007.
  • Zhou H, Wang J, Zhu P, et al. NR4A1 aggravates the cardiac microvascular ischemia reperfusion injury through suppressing FUNDC1-mediated mitophagy and promoting Mff-required mitochondrial fission by CK2α. Basic Res Cardiol. 2018;113(4):23. doi: 10.1007/s00395-018-0682-1.
  • Yu W, Xu M, Zhang T, et al. Mst1 promotes cardiac ischemia–reperfusion injury by inhibiting the ERK–CREB pathway and repressing FUNDC1-mediated mitophagy. J Physiol Sci. 2019;69(1):113–127. doi: 10.1007/s12576-018-0627-3.
  • Zhou H, Li D, Zhu P, et al. Melatonin suppresses platelet activation and function against cardiac ischemia/reperfusion injury via PPARγ/FUNDC1/mitophagy pathways. J Pineal Res. 2017;63(4). doi: 10.1111/jpi.12438.
  • Chen N, Hao C, Liu BC, et al. Roxadustat treatment for anemia in patients undergoing long-term dialysis. N Engl J Med. 2019;381(11):1011–1022. doi: 10.1056/NEJMoa1901713.
  • Chen N, Hao C, Peng X, et al. Roxadustat for anemia in patients with kidney disease not receiving dialysis. N Engl J Med. 2019;381(11):1001–1010. doi: 10.1056/NEJMoa1813599.
  • Yang Y, Yu X, Zhang Y, et al. Hypoxia-inducible factor prolyl hydroxylase inhibitor roxadustat (FG-4592) protects against cisplatin-induced acute kidney injury. Clin Sci. 2018;132(7):825–838. doi: 10.1042/cs20171625.
  • Wu M, Chen W, Miao M, et al. Anti-anemia drug FG4592 retards the AKI-to-CKD transition by improving vascular regeneration and antioxidative capability. Clin Sci. 2021;135(14):1707–1726. doi: 10.1042/cs20210100.
  • Regolisti G, Maggiore U, Cademartiri C, et al. Renal resistive index by transesophageal and transparietal echo-Doppler imaging for the prediction of acute kidney injury in patients undergoing major heart surgery. J Nephrol. 2017;30(2):243–253. doi: 10.1007/s40620-016-0289-2.