7,793
Views
2
CrossRef citations to date
0
Altmetric
Research Paper

Melatonin attenuates sepsis-induced acute kidney injury by promoting mitophagy through SIRT3-mediated TFAM deacetylation

, , , , , , , , , , , , , , , & show all
Pages 151-165 | Received 16 Dec 2022, Accepted 21 Aug 2023, Published online: 31 Aug 2023

References

  • Uchino S, Kellum JA, Bellomo R, et al. Acute renal failure in critically ill patients: a multinational, multicenter study. JAMA. 2005 Aug 17;294(7):813–818. doi: 10.1001/jama.294.7.813
  • Poston JT, Koyner JL. Sepsis associated acute kidney injury. BMJ. 2019 Jan 9;364:k4891. doi: 10.1136/bmj.k4891
  • Hoffman RA, Reiter RJ. Pineal gland: influence on gonads of male hamsters. Science. 1965 Jun 18;148(3677):1609–1611. doi: 10.1126/science.148.3677.1609
  • Shen M, Cao Y, Jiang Y, et al. Melatonin protects mouse granulosa cells against oxidative damage by inhibiting FOXO1-mediated autophagy: Implication of an antioxidation-independent mechanism. Redox Biol. 2018 Sep;18:138–157.
  • Parikh SM, Yang Y, He L, et al. Mitochondrial function and disturbances in the septic kidney. Semin Nephrol. 2015 Jan;35(1):108–119. doi: 10.1016/j.semnephrol.2015.01.011
  • Qiu W, An S, Wang T, et al. Melatonin suppresses ferroptosis via activation of the Nrf2/HO-1 signaling pathway in the mouse model of sepsis-induced acute kidney injury. Int Immunopharmacol. 2022 Sep 5;112:109162. doi: 10.1016/j.intimp.2022.109162
  • Wang Y, Zhu J, Liu Z, et al. The PINK1/PARK2/optineurin pathway of mitophagy is activated for protection in septic acute kidney injury. Redox Biol. 2021 Jan;38:101767.
  • Deng Z, Sun M, Wu J, et al. SIRT1 attenuates sepsis-induced acute kidney injury via Beclin1 deacetylation-mediated autophagy activation. Cell Death Dis. 2021 Feb 26;12(2):217. doi: 10.1038/s41419-021-03508-y
  • Sun M, Li J, Mao L, et al. p53 deacetylation alleviates sepsis-induced acute kidney injury by promoting autophagy. Front Immunol. 2021;12:685523. doi: 10.3389/fimmu.2021.685523
  • Xu S, Gao Y, Zhang Q, et al. SIRT1/3 activation by resveratrol attenuates acute kidney injury in a septic rat model. Oxid Med Cell Longev. 2016;2016:7296092. doi: 10.1155/2016/7296092
  • Wei S, Gao Y, Dai X, et al. SIRT1-mediated HMGB1 deacetylation suppresses sepsis-associated acute kidney injury [journal article]. Am J Physiol Renal Physiol. 2019 Jan 01;316(1):F20–F31.
  • Kim SC, Sprung R, Chen Y, et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell. 2006 Aug;23(4):607–618. doi: 10.1016/j.molcel.2006.06.026
  • Jin L, Galonek H, Israelian K, et al. Biochemical characterization, localization, and tissue distribution of the longer form of mouse SIRT3. Protein Sci. 2009 Mar;18(3):514–525. doi: 10.1002/pro.50
  • Yu W, Gao B, Li N, et al. Sirt3 deficiency exacerbates diabetic cardiac dysfunction: role of foxo3A-Parkin-mediated mitophagy. Biochim Biophys Acta Mol Basis Dis. 2017 Aug;1863(8):1973–1983. doi: 10.1016/j.bbadis.2016.10.021
  • Guo Y, Jia X, Cui Y, et al. Sirt3-mediated mitophagy regulates AGEs-induced BMSCs senescence and senile osteoporosis. Redox Biol. 2021 May;41:101915.
  • Reiter RJ, Tan DX, Rosales-Corral S, et al. Melatonin mitigates mitochondrial meltdown: interactions with SIRT3. Int J Mol Sci. 2018 Aug 18;19(8):2439. doi: 10.3390/ijms19082439
  • Xu S, Li L, Wu J, et al. Melatonin attenuates sepsis-induced small-intestine injury by upregulating SIRT3-mediated oxidative-stress inhibition, mitochondrial protection, and autophagy induction. Front Immunol. 2021;12:625627. doi: 10.3389/fimmu.2021.625627
  • Zhang C, Suo M, Liu L, et al. Melatonin alleviates contrast-induced acute kidney injury by activation of Sirt3. Oxid Med Cell Longev. 2021;2021:1–21. doi: 10.1155/2021/6668887
  • Bonekamp NA, Jiang M, Motori E, et al. High levels of TFAM repress mammalian mitochondrial DNA transcription in vivo. Life Sci Alliance. 2021 Nov;4(11):e202101034. doi: 10.26508/lsa.202101034
  • Baixauli F, Acin-Perez R, Villarroya-Beltri C, et al. Mitochondrial respiration controls lysosomal function during inflammatory T Cell responses. Cell Metab. 2015 Sep 1;22(3):485–498. doi: 10.1016/j.cmet.2015.07.020
  • Liu H, Li S, Liu X, et al. SIRT3 overexpression Inhibits growth of kidney tumor cells and enhances mitochondrial biogenesis. J Proteome Res. 2018 Sep 7;17(9):3143–3152. doi: 10.1021/acs.jproteome.8b00260
  • Hu Q, Ren J, Ren H, et al. Urinary mitochondrial DNA Identifies renal dysfunction and mitochondrial damage in sepsis-induced acute kidney injury. Oxid Med Cell Longev. 2018;2018:8074936. doi: 10.1155/2018/8074936
  • Bailey TL, Johnson J, Grant CE, et al. The MEME suite. Nucleic Acids Res. 2015 Jul 1;43(W1):W39–49. doi: 10.1093/nar/gkv416
  • Maekawa H, Inoue T, Ouchi H, et al. Mitochondrial damage causes inflammation via cGAS-STING signaling in acute kidney injury. Cell Rep. 2019 Oct 29;29(5):1261–1273 e6. doi: 10.1016/j.celrep.2019.09.050
  • Han Y, Wu J, Qin Z, et al. Melatonin and its analogues for the prevention of postoperative delirium: a systematic review and meta-analysis. J Pineal Res. 2020 May;68(4):e12644. doi: 10.1111/jpi.12644
  • Galley HF, Lowes DA, Allen L, et al. Melatonin as a potential therapy for sepsis: a phase I dose escalation study and an ex vivo whole blood model under conditions of sepsis. J Pineal Res. 2014 May;56(4):427–438. doi: 10.1111/jpi.12134
  • Hasan ZT, Atrakji D, Mehuaiden DAK. The effect of melatonin on thrombosis, sepsis and mortality rate in COVID-19 patients. Int J Infect Dis. 2022 Jan;114:79–84. doi: 10.1016/j.ijid.2021.10.012
  • El-Gendy FM, El-Hawy MA, Hassan MG. Beneficial effect of melatonin in the treatment of neonatal sepsis. J Matern Fetal Neonatal Med. 2018 Sep;31(17):2299–2303. doi: 10.1080/14767058.2017.1342794
  • Hong TS, Briscese K, Yuan M, et al. Renoprotective effects of melatonin against vancomycin-related acute kidney injury in hospitalized patients: a retrospective cohort study. Antimicrob Agents Chemother. 2021 Aug 17;65(9):e0046221. doi: 10.1128/AAC.00462-21
  • Suofu Y, Li W, Jean-Alphonse FG, et al. Dual role of mitochondria in producing melatonin and driving GPCR signaling to block cytochrome c release. Proc Natl Acad Sci U S A. 2017 Sep 19;114(38):E7997–E8006. doi: 10.1073/pnas.1705768114
  • Jou MJ, Peng TI, Hsu LF, et al. Visualization of melatonin’s multiple mitochondrial levels of protection against mitochondrial Ca(2+)-mediated permeability transition and beyond in rat brain astrocytes. J Pineal Res. 2010 Jan;48(1):20–38. doi: 10.1111/j.1600-079X.2009.00721.x
  • Hevia D, Gonzalez-Menendez P, Quiros-Gonzalez I, et al. Melatonin uptake through glucose transporters: a new target for melatonin inhibition of cancer. J Pineal Res. 2015 Mar;58(2):234–250. doi: 10.1111/jpi.12210
  • Huo X, Wang C, Yu Z, et al. Human transporters, PEPT1/2, facilitate melatonin transportation into mitochondria of cancer cells: an implication of the therapeutic potential. J Pineal Res. 2017 May;62(4):e12390. doi: 10.1111/jpi.12390
  • Osellame LD, Rahim AA, Hargreaves IP, et al. Mitochondria and quality control defects in a mouse model of gaucher disease–links to parkinson’s disease. Cell Metab. 2013 Jun 4;17(6):941–953. doi: 10.1016/j.cmet.2013.04.014
  • Santidrian AF, Matsuno-Yagi A, Ritland M, et al. Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression. J Clin Invest. 2013 Mar;123(3):1068–1081. doi: 10.1172/JCI64264
  • Larsson NG, Wang J, Wilhelmsson H, et al. Mitochondrial transcription factor a is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet. 1998 Mar;18(3):231–236. doi: 10.1038/ng0398-231
  • Yagi M, Toshima T, Amamoto R, et al. Mitochondrial translation deficiency impairs NAD(+) -mediated lysosomal acidification. EMBO J. 2021 Apr 15;40(8):e105268. doi: 10.15252/embj.2020105268
  • Wei T, Huang G, Gao J, et al. Sirtuin 3 deficiency accelerates hypertensive cardiac remodeling by impairing angiogenesis. J Am Heart Assoc. 2017 Aug 19;6(8). doi: 10.1161/JAHA.117.006114
  • Ma S, Chen J, Feng J, et al. Melatonin ameliorates the progression of atherosclerosis via mitophagy activation and NLRP3 inflammasome inhibition. Oxid Med Cell Longev. 2018;2018:9286458. doi: 10.1155/2018/9286458
  • Kim TS, Jin YB, Kim YS, et al. SIRT3 promotes antimycobacterial defenses by coordinating mitochondrial and autophagic functions. Autophagy. 2019 Aug;15(8):1356–1375. doi: 10.1080/15548627.2019.1582743
  • Wu J, Yang Y, Gao Y, et al. Melatonin attenuates anoxia/reoxygenation injury by inhibiting excessive mitophagy through the MT2/SIRT3/FoxO3a signaling pathway in H9c2 cells. Drug Des Devel Ther. 2020;14:2047–2060. doi: 10.2147/DDDT.S248628
  • Bai Y, Yang Y, Gao Y, et al. Melatonin postconditioning ameliorates anoxia/reoxygenation injury by regulating mitophagy and mitochondrial dynamics in a SIRT3-dependent manner. Eur J Pharmacol. 2021 Aug 5;904:174157. doi: 10.1016/j.ejphar.2021.174157
  • Zhang Y, Wang Y, Xu J, et al. Melatonin attenuates myocardial ischemia-reperfusion injury via improving mitochondrial fusion/mitophagy and activating the AMPK-OPA1 signaling pathways. J Pineal Res. 2019 Mar;66(2):e12542. doi: 10.1111/jpi.12542
  • Zhou H, Du W, Li Y, et al. Effects of melatonin on fatty liver disease: The role of NR4A1/DNA-PKcs/p53 pathway, mitochondrial fission, and mitophagy. J Pineal Res. 2018 Jan;64(1):e12450. doi: 10.1111/jpi.12450
  • Zhu HL, Shi XT, Xu XF, et al. Melatonin protects against environmental stress-induced fetal growth restriction via suppressing ROS-mediated GCN2/ATF4/BNIP3-dependent mitophagy in placental trophoblasts. Redox Biol. 2021 Apr;40:101854.
  • 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 Aug;98(2):294–309. doi: 10.1016/j.kint.2020.04.020
  • Zhao GJ, Xu C, Ying JC, et al. Association between furosemide administration and outcomes in critically ill patients with acute kidney injury. Crit Care. 2020 Mar 4;24(1):75. doi: 10.1186/s13054-020-2798-6
  • Rittirsch D, Huber-Lang MS, Flierl MA, et al. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc. 2009;4(1):31–36. doi: 10.1038/nprot.2008.214