ANKRD1 aggravates renal ischaemia‒reperfusion injury via promoting TRIM25-mediated ubiquitination of ACSL3

Shangting Han , Jiayu Guo , Chenyang Kong , Jun Li , Fangyou Lin , Jiefu Zhu , Tianyu Wang , Qi Chen , Yiting Liu , Haochong Hu , Tao Qiu , Fan Cheng , Jiangqiao Zhou

Clinical and Translational Medicine ›› 2024, Vol. 14 ›› Issue (9) : e70024

PDF
Clinical and Translational Medicine ›› 2024, Vol. 14 ›› Issue (9) : e70024 DOI: 10.1002/ctm2.70024
RESEARCH ARTICLE

ANKRD1 aggravates renal ischaemia‒reperfusion injury via promoting TRIM25-mediated ubiquitination of ACSL3

Author information +
History +
PDF

Abstract

•Ankyrin repeat domain 1 (ANKRD1) is rapidly activated in renal ischaemia‒reperfusion injury (IRI) models in vivo and in vitro.

•ANKRD1 knockdown mitigates kidney damage and preserves renal function.

•Ferroptosis contributes to the deteriorating function of ANKRD1 in renal IRI.

•ANKRD1 promotes acyl-coenzyme A synthetase long-chain family member 3 (ACSL3) degradation via the ubiquitin‒proteasome pathway.

•The E3 ligase tripartite motif containing 25 (TRIM25) is responsible for ANKRD1-mediated ubiquitination of ACSL3.

Keywords

ACSL3 / ANKRD1 / ferroptosis / renal ischaemic‒reperfusion injury / TRIM25 / ubiquitination

Cite this article

Download citation ▾
Shangting Han, Jiayu Guo, Chenyang Kong, Jun Li, Fangyou Lin, Jiefu Zhu, Tianyu Wang, Qi Chen, Yiting Liu, Haochong Hu, Tao Qiu, Fan Cheng, Jiangqiao Zhou. ANKRD1 aggravates renal ischaemia‒reperfusion injury via promoting TRIM25-mediated ubiquitination of ACSL3. Clinical and Translational Medicine, 2024, 14(9): e70024 DOI:10.1002/ctm2.70024

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

BonventreJV, Weinberg JM. Recent advances in the pathophysiology of ischemic acute renal failure. J Am Soc Nephrol. 2003; 14: 2199-2210.

[2]

AgarwalA, DongZ, HarrisR, et al. Cellular and molecular mechanisms of AKI. J Am Soc Nephrol. 2016; 27: 1288-1299.

[3]

LinkermannA, ChenG, DongG, Kunzendorf U, KrautwaldS, DongZ. Regulated cell death in AKI. J Am Soc Nephrol. 2014; 25: 2689-2701.

[4]

HavasiA, BorkanSC. Apoptosis and acute kidney injury. Kidney Int. 2011; 80: 29-40.

[5]

ZhaoM, WangY, LiL, et al. Mitochondrial ROS promote mitochondrial dysfunction and inflammation in ischemic acute kidney injury by disrupting TFAM-mediated mtDNA maintenance. Theranostics. 2021; 11: 1845-1863.

[6]

ArimuraT, BosJM, SatoA, et al. Cardiac ankyrin repeat protein gene (ANKRD1) mutations in hypertrophic cardiomyopathy. J Am Coll Cardiol. 2009; 54: 334-342.

[7]

ZhangY, ZhouL, FuQ, LiuZ. ANKRD1 activates the Wnt signaling pathway by modulating CAV3 expression and thus promotes BMSC osteogenic differentiation and bone formation in ovariectomized mice. Biochim Biophys Acta Mol Basis Dis. 2023; 1869: 166693.

[8]

LingS, ChenYT, WangJ, Richards AM, LiewOW. Ankyrin repeat domain 1 protein: a functionally pleiotropic protein with cardiac biomarker potential. Int J Mol Sci. 2017; 18:1362.

[9]

SamarasSE, Almodovar-Garcia K, WuN, YuF, Davidson JM. Global deletion of Ankrd1 results in a wound-healing phenotype associated with dermal fibroblast dysfunction. Am J Pathol. 2015; 185: 96-109.

[10]

ZhaoJ, WuY, ZhouK, et al. Ferroptosis in calcium oxalate kidney stone formation and the possible regulatory mechanism of ANKRD1. Biochim Biophys Acta Mol Cell Res. 2023; 1870: 119452.

[11]

NiL, YuanC, WuX. Targeting ferroptosis in acute kidney injury. Cell Death Dis. 2022; 13: 182.

[12]

JiangX, Stockwell BR, ConradM. Ferroptosis: mechanisms, biology and role in disease. Nat Rev Mol Cell Biol. 2021; 22: 266-282.

[13]

YangY, ZhuT, WangX, et al. ACSL3 and ACSL4, distinct roles in ferroptosis and cancers. Cancers. 2022; 14: 5896.

[14]

DollS, Proneth B, TyurinaYY, et al. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol. 2017; 13: 91-98.

[15]

ZhouS, PengJ, XiaoL, et al. TRIM25 regulates oxaliplatin resistance in colorectal cancer by promoting EZH2 stability. Cell Death Dis. 2021; 12: 463.

[16]

ZhouX, LiY, WuC, YuW, ChengF. Novel lncRNA XLOC_032768 protects against renal tubular epithelial cells apoptosis in renal ischemia-reperfusion injury by regulating FNDC3B/TGF-beta1. Ren Fail. 2020; 42: 994-1003.

[17]

NakamuraA, Imaizumi A, YanagawaY, KohsakaT, JohnsEJ. Beta(2)-adrenoceptor activation attenuates endotoxin-induced acute renal failure. J Am Soc Nephrol. 2004; 15: 316-325.

[18]

DingH, LiJ, LiY, et al. MicroRNA-10 negatively regulates inflammation in diabetic kidney via targeting activation of the NLRP3 inflammasome. Mol Ther. 2021; 29: 2308-2320.

[19]

LiuM, LiangK, ZhenJ, et al. Sirt6 deficiency exacerbates podocyte injury and proteinuria through targeting Notch signaling. Nat Commun. 2017; 8: 413.

[20]

WangX, LiuJ, ZhenJ, et al. Histone deacetylase 4 selectively contributes to podocyte injury in diabetic nephropathy. Kidney Int. 2014; 86: 712-725.

[21]

KimM, ChenSW, ParkSW, et al. Kidney-specific reconstitution of the A1 adenosine receptor in A1 adenosine receptor knockout mice reduces renal ischemia-reperfusion injury. Kidney Int. 2009; 75: 809-823.

[22]

ShiL, SongZ, LiY, et al. MiR-20a-5p alleviates kidney ischemia/reperfusion injury by targeting ACSL4-dependent ferroptosis. Am J Transplant. 2023; 23: 11-25.

[23]

ShangJ, WanQ, WangX, et al. Identification of NOD2 as a novel target of RNA-binding protein HuR: evidence from NADPH oxidase-mediated HuR signaling in diabetic nephropathy. Free Radic Bio Med. 2015; 79: 217-227.

[24]

ZhaoF, ZhuJ, ZhangM, et al. OGG1 aggravates renal ischemia-reperfusion injury by repressing PINK1-mediated mitophagy. Cell Prolif. 2023; 56: e13418.

[25]

LiC, HanS, ZhuJ, ChengF. MiR-132-3p activation aggravates renal ischemia-reperfusion injury by targeting Sirt1/PGC1alpha axis. Cell Signal. 2023; 110: 110801.

[26]

ChomczynskiP, SacchiN. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162: 156-159.

[27]

BalzerMS, DokeT, YangYW, et al. Single-cell analysis highlights differences in druggable pathways underlying adaptive or fibrotic kidney regeneration. Nat Commun. 2022; 13: 4018.

[28]

MeiP, XieF, PanJ, et al. E3 ligase TRIM25 ubiquitinates RIP3 to inhibit TNF induced cell necrosis. Cell Death Differ. 2021; 28: 2888-2899.

[29]

HeYM, ZhouXM, JiangSY, et al. TRIM25 activates AKT/mTOR by inhibiting PTEN via K63-linked polyubiquitination in non-small cell lung cancer. Acta Pharmacol Sin. 2022; 43: 681-691.

[30]

MehtaRL, CerdaJ, BurdmannEA, et al. International Society of Nephrology’s 0by25 initiative for acute kidney injury (zero preventable deaths by 2025): a human rights case for nephrology. Lancet. 2015; 385: 2616-2643.

[31]

MehtaRL, Burdmann EA, CerdaJ, et al. Recognition and management of acute kidney injury in the International Society of Nephrology 0by25 Global Snapshot: a multinational cross-sectional study. Lancet. 2016; 387: 2017-2025.

[32]

ZhuJ, XiangX, HuX, LiC, SongZ, Dong Z. miR-147 represses NDUFA4, inducing mitochondrial dysfunction and tubular damage in cold storage kidney transplantation. J Am Soc Nephrol. 2023; 34: 1381-1397.

[33]

SharfuddinAA, Molitoris BA. Pathophysiology of ischemic acute kidney injury. Nat Rev Nephrol. 2011; 7: 189-200.

[34]

FengQ, YangY, RenK, et al. Broadening horizons: the multifaceted functions of ferroptosis in kidney diseases. Int J Biol Sci. 2023; 19: 3726-3743.

[35]

PefanisA, IerinoFL, MurphyJM, Cowan PJ. Regulated necrosis in kidney ischemia-reperfusion injury. Kidney Int. 2019; 96: 291-301.

[36]

BayirH, DixonSJ, TyurinaYY, Kellum JA, KaganVE. Ferroptotic mechanisms and therapeutic targeting of iron metabolism and lipid peroxidation in the kidney. Nat Rev Nephrol. 2023; 19: 315-336.

[37]

LinkermannA, SkoutaR, HimmerkusN, et al. Synchronized renal tubular cell death involves ferroptosis. Proc Natl Acad Sci U S A. 2014; 111: 16836-16841.

[38]

FriedmannAJ, Schneider M, PronethB, et al. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat Cell Biol. 2014; 16: 1180-1191.

[39]

ZhangN, XieXJ, WangJA. Multifunctional protein: cardiac ankyrin repeat protein. J Zhejiang Univ Sci B. 2016; 17: 333-341.

[40]

ChuW, BurnsDK, SwerlickRA, Presky DH. Identification and characterization of a novel cytokine-inducible nuclear protein from human endothelial cells. J Biol Chem. 1995; 270: 10236-10245.

[41]

JeyaseelanR, PoizatC, BakerRK, et al. A novel cardiac-restricted target for doxorubicin. CARP, a nuclear modulator of gene expression in cardiac progenitor cells and cardiomyocytes. J Biol Chem. 1997; 272: 22800-22808.

[42]

MosaviLK, Cammett TJ, DesrosiersDC, PengZY. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 2004; 13: 1435-1448.

[43]

LaureL, Daniele N, SuelL, et al. A new pathway encompassing calpain 3 and its newly identified substrate cardiac ankyrin repeat protein is involved in the regulation of the nuclear factor-kappaB pathway in skeletal muscle. FEBS J. 2010; 277: 4322-4337.

[44]

ZouY, EvansS, ChenJ, Kuo HC, HarveyRP, ChienKR. CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development. 1997; 124: 793-804.

[45]

Duboscq-BidotL, Charron P, RuppertV, et al. Mutations in the ANKRD1 gene encoding CARP are responsible for human dilated cardiomyopathy. Eur Heart J. 2009; 30: 2128-2136.

[46]

AiharaY, Kurabayashi M, SaitoY, et al. Cardiac ankyrin repeat protein is a novel marker of cardiac hypertrophy: role of M-CAT element within the promoter. Hypertension. 2000; 36: 48-53.

[47]

MatsuuraK, UesugiN, HijiyaN, Uchida T, MoriyamaM. Upregulated expression of cardiac ankyrin-repeated protein in renal podocytes is associated with proteinuria severity in lupus nephritis. Hum Pathol. 2007; 38: 410-419.

[48]

GuiY, LiJ, LuQ, et al. Yap/Taz mediates mTORC2-stimulated fibroblast activation and kidney fibrosis. J Biol Chem. 2018; 293: 16364-16375.

[49]

WenzelSE, Tyurina YY, ZhaoJ, et al. PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell. 2017; 171: 628-641.

[50]

ZhangJ, WangB, YuanS, He Q, JinJ. The role of ferroptosis in acute kidney injury. Front Mol Biosci. 2022; 9: 951275.

[51]

SanzAB, Sanchez-Nino MD, RamosAM, OrtizA. Regulated cell death pathways in kidney disease. Nat Rev Nephrol. 2023; 19: 281-299.

[52]

Martin-SanchezD, Fontecha-Barriuso M, Martinez-MorenoJM, et al. Ferroptosis and kidney disease. Nefrologia (Engl Ed). 2020; 40: 384-394.

[53]

ZhengJ, ConradM. The metabolic underpinnings of ferroptosis. Cell Metab. 2020; 32: 920-937.

[54]

SoupeneE, Kuypers FA. Mammalian long-chain acyl-CoA synthetases. Exp Biol Med. 2008; 233: 507-521.

[55]

MagtanongL, KoPJ, ToM, et al. Exogenous monounsaturated fatty acids promote a ferroptosis-resistant cell state. Cell Chem Biol. 2019; 26: 420-432.

[56]

KlassonTD, LaGoryEL, ZhaoH, et al. ACSL3 regulates lipid droplet biogenesis and ferroptosis sensitivity in clear cell renal cell carcinoma. Cancer Metab. 2022; 10: 14.

[57]

MaM, KongP, HuangY, et al. Activation of MAT2A-ACSL3 pathway protects cells from ferroptosis in gastric cancer. Free Radic Bio Med. 2022; 181: 288-299.

[58]

LiM, MengZ, YuS, et al. Baicalein ameliorates cerebral ischemia-reperfusion injury by inhibiting ferroptosis via regulating GPX4/ACSL4/ACSL3 axis. Chem-Biol Interact. 2022; 366: 110137.

[59]

Meyer-SchwesingerC. The ubiquitin-proteasome system in kidney physiology and disease. Nat Rev Nephrol. 2019; 15: 393-411.

[60]

MulaySR, Thomasova D, RyuM, AndersHJ. MDM2 (murine double minute-2) links inflammation and tubular cell healing during acute kidney injury in mice. Kidney Int. 2012; 81: 1199-1211.

[61]

YuJT, HuXW, YangQ, et al. Insulin-like growth factor binding protein 7 promotes acute kidney injury by alleviating poly ADP ribose polymerase 1 degradation. Kidney Int. 2022; 102: 828-844.

[62]

DuY, ChuCM, ZhuoD, Ning JZ. The inhibition of TRIM35-mediated TIGAR ubiquitination enhances mitochondrial fusion and alleviates renal ischemia-reperfusion injury. Int J Biol Macromol. 2022; 209: 725-736.

[63]

HenshallTL, Manning JA, AlfassyOS, et al. Deletion of Nedd4-2 results in progressive kidney disease in mice. Cell Death Differ. 2017; 24: 2150-2160.

[64]

GuM, TanM, ZhouL, et al. Protein phosphatase 2Acalpha modulates fatty acid oxidation and glycolysis to determine tubular cell fate and kidney injury. Kidney Int. 2022; 102: 321-336.

[65]

BaileyJL, WangX, EnglandBK, Price SR, DingX, MitchWE. The acidosis of chronic renal failure activates muscle proteolysis in rats by augmenting transcription of genes encoding proteins of the ATP-dependent ubiquitin-proteasome pathway. J Clin Invest. 1996; 97: 1447-1453.

[66]

ObaraY, Nagasawa R, NemotoW, et al. ERK5 induces ankrd1 for catecholamine biosynthesis and homeostasis in adrenal medullary cells. Cell Signal. 2016; 28: 177-189.

[67]

WittCC, WittSH, LercheS, Labeit D, BackW, LabeitS. Cooperative control of striated muscle mass and metabolism by MuRF1 and MuRF2. EMBO J. 2008; 27: 350-360.

RIGHTS & PERMISSIONS

2024 The Author(s). Clinical and Translational Medicine published by John Wiley & Sons Australia, Ltd on behalf of Shanghai Institute of Clinical Bioinformatics.

AI Summary AI Mindmap
PDF

120

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/