Targeting ferroptosis as a prospective therapeutic approach for diabetic nephropathy

References

• Federation I. IDF Diabetes Atlas, tenth. International Diabetes. 2021.
   Google Scholar
• Jager KJ, Kovesdy C, Langham R, et al. A single number for advocacy and communication-worldwide more than 850 million individuals have kidney diseases. Kidney Int. 2019;96(5):1–11. doi: 10.1016/j.kint.2019.07.012.
   Web of Science ®Google Scholar
• Anders H-J, Huber TB, Isermann B, et al. CKD in diabetes: diabetic kidney disease versus nondiabetic kidney disease. Nat Rev Nephrol. 2018;14(6):361–377. doi: 10.1038/s41581-018-0001-y.
   PubMed Web of Science ®Google Scholar
• Rico-Fontalvo J, Aroca G, Cabrales J, et al. Molecular mechanisms of diabetic kidney disease. Int J Mol Sci. 2022;23(15):8668. doi: 10.3390/ijms23158668.
   PubMedGoogle Scholar
• Volpe CMO, Villar-Delfino PH, Dos Anjos PMF, et al. Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death Dis. 2018;9(2):119. doi: 10.1038/s41419-017-0135-z.
   PubMed Web of Science ®Google Scholar
• Wu Y, Chen Y. Research progress on ferroptosis in diabetic kidney disease. Front Endocrinol (Lausanne). 2022;13:945976. doi: 10.3389/fendo.2022.945976.
   PubMed Web of Science ®Google Scholar
• Wang Y, Bi R, Quan F, et al. Ferroptosis involves in renal tubular cell death in diabetic nephropathy. Eur J Pharmacol. 2020;888:173574. doi: 10.1016/j.ejphar.2020.173574.
   PubMed Web of Science ®Google Scholar
• Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5):1060–1072. doi: 10.1016/j.cell.2012.03.042.
   PubMed Web of Science ®Google Scholar
• Stockwell BR. Ferroptosis turns 10: emerging mechanisms, physiological functions, and therapeutic applications. Cell. 2022;185(14):2401–2421. doi: 10.1016/j.cell.2022.06.003.
   PubMed Web of Science ®Google Scholar
• Fang X, Ardehali H, Min J, et al. The molecular and metabolic landscape of iron and ferroptosis in cardiovascular disease. Nat Rev Cardiol. 2023;20(1):7–23. doi: 10.1038/s41569-022-00735-4.
   PubMed Web of Science ®Google Scholar
• Fang X, Cai Z, Wang H, et al. Loss of cardiac ferritin H facilitates cardiomyopathy via Slc7a11-Mediated ferroptosis. Circ Res. 2020;127(4):486–501. doi: 10.1161/CIRCRESAHA.120.316509.
   PubMed Web of Science ®Google Scholar
• Anandhan A, Dodson M, Shakya A, et al. NRF2 controls iron homeostasis and ferroptosis through HERC2 and VAMP8. Sci Adv. 2023;9(5):eade9585. doi: 10.1126/sciadv.ade9585.
   PubMed Web of Science ®Google Scholar
• Yu Y, Jiang L, Wang H, et al. Hepatic transferrin plays a role in systemic iron homeostasis and liver ferroptosis. Blood. 2020;136(6):726–739. doi: 10.1182/blood.2019002907.
   PubMed Web of Science ®Google Scholar
• Shen Z, Liu T, Li Y, et al. Fenton-reaction-acceleratable magnetic nanoparticles for ferroptosis therapy of orthotopic brain tumors. ACS Nano. 2018;12(11):11355–11365. doi: 10.1021/acsnano.8b06201.
   PubMed Web of Science ®Google Scholar
• He YJ, Liu XY, Xing L, et al. Fenton reaction-independent ferroptosis therapy via glutathione and iron redox couple sequentially triggered lipid peroxide generator. Biomaterials. 2020;241:119911. doi: 10.1016/j.biomaterials.2020.119911.
   PubMed Web of Science ®Google Scholar
• Das UN. Saturated fatty acids, MUFAs and PUFAs regulate ferroptosis. Cell Chem Biol. 2019;26(3):309–311. doi: 10.1016/j.chembiol.2019.03.001.
   PubMed Web of Science ®Google Scholar
• Dierge E, Debock E, Guilbaud C, et al. Peroxidation of n-3 and n-6 polyunsaturated fatty acids in the acidic tumor environment leads to ferroptosis-mediated anticancer effects. Cell Metab. 2021;33(8):1701–1715.e5. doi: 10.1016/j.cmet.2021.05.016.
   PubMed Web of Science ®Google Scholar
• Friedmann Angeli JP, Xavier da Silva TN, Schilling B. CD8(+) T cells PUF(A)ing the flames of cancer ferroptotic cell death. Cancer Cell. 2022;40(4):346–348. doi: 10.1016/j.ccell.2022.03.003.
   PubMed Web of Science ®Google Scholar
• Zhang HL, Hu BX, Li ZL, et al. PKCβII phosphorylates ACSL4 to amplify lipid peroxidation to induce ferroptosis. Nat Cell Biol. 2022;24(1):88–98. doi: 10.1038/s41556-021-00818-3.
   PubMed Web of Science ®Google Scholar
• Cui Y, Zhang Y, Zhao X, et al. ACSL4 exacerbates ischemic stroke by promoting ferroptosis-induced brain injury and neuroinflammation. Brain Behav Immun. 2021;93:312–321. doi: 10.1016/j.bbi.2021.01.003.
   PubMed Web of Science ®Google Scholar
• Chen D, Chu B, Yang X, et al. iPLA2β-mediated lipid detoxification controls p53-driven ferroptosis independent of GPX4. Nat Commun. 2021;12(1):3644. doi: 10.1038/s41467-021-23902-6.
   PubMed Web of Science ®Google Scholar
• Ingold I, Berndt C, Schmitt S, et al. Selenium utilization by GPX4 is required to prevent Hydroperoxide-Induced ferroptosis. Cell. 2018;172(3):409–422.e21. e421. doi: 10.1016/j.cell.2017.11.048.
   PubMed Web of Science ®Google Scholar
• Ye Y, Chen A, Li L, et al. Repression of the antiporter SLC7A11/glutathione/glutathione peroxidase 4 axis drives ferroptosis of vascular smooth muscle cells to facilitate vascular calcification. Kidney Int. 2022;102(6):1259–1275. doi: 10.1016/j.kint.2022.07.034.
   PubMed Web of Science ®Google Scholar
• Parker JL, Deme JC, Kolokouris D, et al. Molecular basis for redox control by the human cystine/glutamate antiporter system xc. Nat Commun. 2021;12(1):7147. () doi: 10.1038/s41467-021-27414-1.
   PubMed Web of Science ®Google Scholar
• Wang Y, Yan S, Liu X, et al. PRMT4 promotes ferroptosis to aggravate doxorubicin-induced cardiomyopathy via inhibition of the Nrf2/GPX4 pathway. Cell Death Differ. 2022;29(10):1982–1995. doi: 10.1038/s41418-022-00990-5.
   PubMed Web of Science ®Google Scholar
• Lu Y, Qin H, Jiang B, et al. KLF2 inhibits cancer cell migration and invasion by regulating ferroptosis through GPX4 in clear cell renal cell carcinoma. Cancer Lett. 2021;522:1–13. doi: 10.1016/j.canlet.2021.09.014.
   PubMed Web of Science ®Google Scholar
• Mao C, Liu X, Zhang Y, et al. DHODH-mediated ferroptosis defence is a targetable vulnerability in cancer. Nature. 2021;593(7860):586–590. doi: 10.1038/s41586-021-03539-7.
   PubMed Web of Science ®Google Scholar
• Deng F, Sharma I, Dai Y, et al. Myo-inositol oxygenase expression profile modulates pathogenic ferroptosis in the renal proximal tubule. J Clin Invest. 2019;129(11):5033–5049. doi: 10.1172/JCI129903.
   PubMed Web of Science ®Google Scholar
• Fan X, Zhang X, Liu LC, et al. Hemopexin accumulates in kidneys and worsens acute kidney injury by causing hemoglobin deposition and exacerbation of iron toxicity in proximal tubules. Kidney Int. 2022;102(6):1320–1330. doi: 10.1016/j.kint.2022.07.024.
   PubMed Web of Science ®Google Scholar
• Tonnus W, Meyer C, Steinebach C, et al. Dysfunction of the key ferroptosis-surveilling systems hypersensitizes mice to tubular necrosis during acute kidney injury. Nat Commun. 2021;12(1):4402. doi: 10.1038/s41467-021-24712-6.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang M, Bi R, et al. ACSL4 deficiency confers protection against ferroptosis-mediated acute kidney injury. Redox Biol. 2022;51:102262. doi: 10.1016/j.redox.2022.102262.
   PubMed Web of Science ®Google Scholar
• Kim DH, Choi HI, Park JS, et al. Farnesoid X receptor protects against cisplatin-induced acute kidney injury by regulating the transcription of ferroptosis-related genes. Redox Biol. 2022;54:102382. doi: 10.1016/j.redox.2022.102382.
   PubMed Web of Science ®Google Scholar
• Zou Y, Palte MJ, Deik AA, et al. A GPX4-dependent cancer cell state underlies the clear-cell morphology and confers sensitivity to ferroptosis. Nat Commun. 2019;10(1):1617. doi: 10.1038/s41467-019-09277-9.
   PubMed Web of Science ®Google Scholar
• Zhang B, Chen X, Ru F, et al. Liproxstatin-1 attenuates unilateral ureteral obstruction-induced renal fibrosis by inhibiting renal tubular epithelial cells ferroptosis. Cell Death Dis. 2021;12(9):843. doi: 10.1038/s41419-021-04137-1.
   PubMed Web of Science ®Google Scholar
• Oshima M, Shimizu M, Yamanouchi M, et al. Trajectories of kidney function in diabetes: a clinicopathological update. Nat Rev Nephrol. 2021;17(11):740–750. doi: 10.1038/s41581-021-00462-y.
   PubMed Web of Science ®Google Scholar
• van Swelm RPL, Wetzels JFM, Swinkels DW. The multifaceted role of iron in renal health and disease. Nat Rev Nephrol. 2020;16(2):77–98. doi: 10.1038/s41581-019-0197-5.
   PubMed Web of Science ®Google Scholar
• Feng X, Wang S, Sun Z, et al. Ferroptosis enhanced diabetic renal tubular injury via HIF-1α/HO-1 pathway in db/db mice. Front Endocrinol (Lausanne). 2021;12:626390. doi: 10.3389/fendo.2021.626390.
   PubMed Web of Science ®Google Scholar
• Tsai YC, Kuo MC, Huang JC, et al. Single-cell transcriptomic profiles in the pathophysiology within the microenvironment of early diabetic kidney disease. Cell Death Dis. 2023;14(7):442. doi: 10.1038/s41419-023-05947-1.
   PubMed Web of Science ®Google Scholar
• Kim S, Kang SW, Joo J, et al. Characterization of ferroptosis in kidney tubular cell death under diabetic conditions. Cell Death Dis. 2021;12(2):160. doi: 10.1038/s41419-021-03452-x.
   PubMed Web of Science ®Google Scholar
• Dodson M, Castro-Portuguez R, Zhang DD. NRF2 plays a critical role in mitigating lipid peroxidation and ferroptosis. Redox Biol. 2019;23:101107. doi: 10.1016/j.redox.2019.101107.
   PubMed Web of Science ®Google Scholar
• Li S, Zheng L, Zhang J, et al. Inhibition of ferroptosis by up-regulating Nrf2 delayed the progression of diabetic nephropathy. Free Radic Biol Med. 2021;162:435–449. doi: 10.1016/j.freeradbiomed.2020.10.323.
   PubMed Web of Science ®Google Scholar
• Jin T, Chen C. Umbelliferone delays the progression of diabetic nephropathy by inhibiting ferroptosis through activation of the nrf-2/HO-1 pathway. Food Chem Toxicol. 2022;163:112892. doi: 10.1016/j.fct.2022.112892.
   PubMed Web of Science ®Google Scholar
• Lu Q, Yang L, Xiao JJ, et al. Empagliflozin attenuates the renal tubular ferroptosis in diabetic kidney disease through AMPK/NRF2 pathway. Free Radic Biol Med. 2023;195:89–102. doi: 10.1016/j.freeradbiomed.2022.12.088.
   PubMed Web of Science ®Google Scholar
• Liu Z, Nan P, Gong Y, et al. Endoplasmic reticulum stress-triggered ferroptosis via the XBP1-Hrd1-Nrf2 pathway induces EMT progression in diabetic nephropathy. Biomed Pharmacother. 2023;164:114897. doi: 10.1016/j.biopha.2023.114897.
   PubMed Web of Science ®Google Scholar
• Wang WJ, Jiang X, Gao CC, et al. Salusin‑β participates in high glucose‑induced HK‑2 cell ferroptosis in a nrf‑2‑dependent manner. Mol Med Rep. 2021;24(3):674. doi: 10.3892/mmr.2021.12313.
   Web of Science ®Google Scholar
• Zhang S, Li Y, Liu X, et al. Carnosine alleviates kidney tubular epithelial injury by targeting NRF2 mediated ferroptosis in diabetic nephropathy. Amino Acids. 2023;55(9):1141–1155. doi: 10.1007/s00726-023-03301-5.
   PubMed Web of Science ®Google Scholar
• Wang YH, Chang DY, Zhao MH, et al. Glutathione peroxidase 4 is a predictor of diabetic kidney disease progression in type 2 diabetes mellitus. Oxid Med Cell Longev. 2022;2022:2948248–2948210. doi: 10.1155/2022/2948248.
   PubMed Web of Science ®Google Scholar
• Huang J, Chen G, Wang J, et al. Platycodin D regulates high glucose-induced ferroptosis of HK-2 cells through glutathione peroxidase 4 (GPX4). Bioengineered. 2022;13(3):6627–6637. doi: 10.1080/21655979.2022.2045834.
   PubMed Web of Science ®Google Scholar
• Li Q, Liao J, Chen W, et al. NAC alleviative ferroptosis in diabetic nephropathy via maintaining mitochondrial redox homeostasis through activating SIRT3-SOD2/Gpx4 pathway. Free Radic Biol Med. 2022;189:1–170. doi: 10.1016/j.freeradbiomed.2022.05.024.
   PubMed Web of Science ®Google Scholar
• Song SH, Han D, Park K, et al. Bone morphogenetic protein-7 attenuates pancreatic damage under diabetic conditions and prevents progression to diabetic nephropathy via inhibition of ferroptosis. Front Endocrinol (Lausanne). 2023;14:1172199. doi: 10.3389/fendo.2023.1172199.
   PubMed Web of Science ®Google Scholar
• Huang B, Wen W, Ye S. Dapagliflozin ameliorates renal tubular ferroptosis in diabetes via SLC40A1 stabilization. Oxid Med Cell Longev. 2022;2022:9735555–9735517. doi: 10.1155/2022/9735555.
   PubMed Web of Science ®Google Scholar
• Wu K, Fei L, Wang X, et al. ZIP14 is involved in iron deposition and triggers ferroptosis in diabetic nephropathy. Metallomics. 2022;14(7):mfac034. doi: 10.1093/mtomcs/mfac034.
   Web of Science ®Google Scholar
• Tan H, Chen J, Li Y, et al. Glabridin, a bioactive component of licorice, ameliorates diabetic nephropathy by regulating ferroptosis and the VEGF/akt/ERK pathways. Mol Med. 2022;28(1):58. doi: 10.1186/s10020-022-00481-w.
   PubMed Web of Science ®Google Scholar
• Wu Z, Li D, Tian D, et al. Aspirin mediates protection from diabetic kidney disease by inducing ferroptosis inhibition. PLoS One. 2022;17(12):e0279010. doi: 10.1371/journal.pone.0279010.
   PubMed Web of Science ®Google Scholar
• Huang D, Shen P, Wang C, et al. Calycosin plays a protective role in diabetic kidney disease through the regulation of ferroptosis. Pharm Biol. 2022;60(1):990–996. doi: 10.1080/13880209.2022.2067572.
   PubMed Web of Science ®Google Scholar
• Wang MZ, Cai YF, Fang QJ, et al. Inhibition of ferroptosis of renal tubular cells with total flavones of abelmoschus manihot alleviates diabetic tubulopathy. Anat Rec (Hoboken). 2022;306(12):3199–3213. doi: 10.1002/ar.25123.
   PubMedGoogle Scholar
• Jin J, Wang Y, Zheng D, et al. A novel identified circular RNA, mmu_mmu_circRNA_0000309, involves in Germacrone-Mediated improvement of diabetic nephropathy through regulating ferroptosis by targeting miR-188-3p/GPX4 signaling axis. Antioxid Redox Signal. 2022;36(10-12):740–759. doi: 10.1089/ars.2021.0063.
   PubMed Web of Science ®Google Scholar
• Chen J, Ou Z, Gao T, et al. Ginkgolide B alleviates oxidative stress and ferroptosis by inhibiting GPX4 ubiquitination to improve diabetic nephropathy. Biomed Pharmacother. 2022;156:113953. doi: 10.1016/j.biopha.2022.113953.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Hu Y, Hu JE, et al. Sp1-mediated upregulation of Prdx6 expression prevents podocyte injury in diabetic nephropathy via mitigation of oxidative stress and ferroptosis. Life Sci. 2021;278:119529. doi: 10.1016/j.lfs.2021.119529.
   PubMed Web of Science ®Google Scholar
• Zhao C, Pu Z, Gao J, et al. Multiomics" analyses combined with systems pharmacology reveal the renoprotection of mangiferin monosodium salt in rats with diabetic nephropathy: focus on improvements in renal ferroptosis, renal inflammation, and podocyte insulin resistance. J Agric Food Chem. 2023;71(1):358–381. doi: 10.1021/acs.jafc.2c05595.
   PubMed Web of Science ®Google Scholar
• Li Q, Meng X, Hua Q. Circ ASAP2 decreased inflammation and ferroptosis in diabetic nephropathy through SOX2/SLC7A11 by miR-770-5p. Acta Diabetol. 2023;60(1):29–42. doi: 10.1007/s00592-022-01961-5.
   PubMed Web of Science ®Google Scholar
• Wang X, Li Q, Sui B, et al. Schisandrin a from schisandra chinensis attenuates ferroptosis and NLRP3 Inflammasome-Mediated pyroptosis in diabetic nephropathy through mitochondrial damage by AdipoR1 ubiquitination. Oxid Med Cell Longev. 2022;2022:5411462. doi: 10.1155/2022/5411462.
   PubMed Web of Science ®Google Scholar
• Wu Y, Zhao Y, Yang HZ, et al. HMGB1 regulates ferroptosis through Nrf2 pathway in mesangial cells in response to high glucose. Biosci Rep. 2021;41(2):41.
   Web of Science ®Google Scholar
• Lv S, Li H, Zhang T, et al. San-Huang-Yi-Shen capsule ameliorates diabetic nephropathy in mice through inhibiting ferroptosis. Biomed Pharmacother. 2023;165:115086. doi: 10.1016/j.biopha.2023.115086.
   PubMed Web of Science ®Google Scholar
• Ji J, Tao P, Wang Q, et al. Emodin attenuates diabetic kidney disease by inhibiting ferroptosis via upregulating Nrf2 expression. Aging (Albany NY). 2023;15:7673–7688.
   PubMedGoogle Scholar
• Zhang S, Zhang S, Wang H, et al. Vitexin ameliorated diabetic nephropathy via suppressing GPX4-mediated ferroptosis. Eur J Pharmacol. 2023;951:175787. doi: 10.1016/j.ejphar.2023.175787.
   PubMed Web of Science ®Google Scholar
• Feng Q, Yang Y, Qiao Y, et al. Quercetin ameliorates diabetic kidney injury by inhibiting ferroptosis via activating Nrf2/HO-1 signaling pathway. Am J Chin Med. 2023;51(4):997–1018. doi: 10.1142/S0192415X23500465.
   PubMedGoogle Scholar
• Kim M, Bae JY, Yoo S, et al. 2-Deoxy-d-ribose induces ferroptosis in renal tubular epithelial cells via ubiquitin-proteasome system-mediated xCT protein degradation. Free Radic Biol Med. 2023;208:384–393. doi: 10.1016/j.freeradbiomed.2023.08.027.
   PubMed Web of Science ®Google Scholar