Bone marrow mesenchymal stem cells inhibit ferroptosis via regulating the Nrf2-keap1/p53 pathway to ameliorate chronic kidney disease injury in the rats

References

• Hill NR, Fatoba ST, Oke JL, et al. Global prevalence of chronic kidney disease – A systematic review and meta-analysis. PLOS One. 2016;11(7):e0158765.
   PubMed Web of Science ®Google Scholar
• Go AS, Chertow GM, Fan D, et al. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004; 351(13):1296–1305.
   PubMed Web of Science ®Google Scholar
• Keith DS, Nichols GA, Gullion CM, et al. Longitudinal follow-up and outcomes among a population with chronic kidney disease in a large managed care organization. Arch Intern Med. 2004; 164(6):659–663.
   PubMed Web of Science ®Google Scholar
• Fan M, Zhang J, Xin H, et al. Current perspectives on role of MSC in renal pathophysiology. Front Physiol. 2018;9:1323.
   PubMedGoogle Scholar
• Nigam e S, Lieberthal W. Acute renal failure. III. The role of growth factors in the process of renal regeneration and repair. Am J Physiol Renal Physiol. 2000;279(1):F3–F11.
   PubMedGoogle Scholar
• Li J, Cao F, Yin HL, et al. Ferroptosis: past, present and future. Cell Death Dis. 2020;11(2):88.
   PubMed Web of Science ®Google Scholar
• Yang WS, SriRamaratnam R, Welsch ME, et al. Regulation of ferroptotic cancer cell death by GPX4. Cell. 2014; 156(1–2):317–331.
   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 e421.
   PubMed Web of Science ®Google Scholar
• Imai H, Matsuoka M, Kumagai T, et al. Lipid peroxidation-dependent cell death regulated by GPx4 and ferroptosis. Curr Top Microbiol Immunol. 2017;403:143–170.
   PubMed Web of Science ®Google Scholar
• Probst L, Dachert J, Schenk B, et al. Lipoxygenase inhibitors protect acute lymphoblastic leukemia cells from ferroptotic cell death. Biochem Pharmacol. 2017;140:41–52.
   PubMed Web of Science ®Google Scholar
• Wang J, Wang Y, Liu Y, et al. Ferroptosis, a new target for treatment of renal injury and fibrosis in a 5/6 nephrectomy-induced CKD rat model. Cell Death Discov. 2022;8(1):127.
   PubMedGoogle Scholar
• Dodson M, Castro-Portuguez R, Zhang DD. NRF2 plays a critical role in mitigating lipid peroxidation and ferroptosis. Redox Biol. 2019 May;23:101107.
   PubMed Web of Science ®Google Scholar
• Kerins MJ, Ooi A. The roles of NRF2 in modulating cellular iron homeostasis. Antioxid Redox Signal. 2018;29(17):1756–1773.
   PubMed Web of Science ®Google Scholar
• Harada N, Kanayama M, Maruyama A, et al. Nrf2 regulates ferroportin 1-mediated iron efflux and counteracts lipopolysaccharide-induced ferroportin 1 mRNA suppression in macrophages. Arch Biochem Biophys. 2011;508(1):101–109.
   PubMedGoogle Scholar
• Agyeman AS, Chaerkady R, Shaw PG, et al. Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles. Breast Cancer Res Treat. 2012; 132(1):175–187.
   PubMedGoogle Scholar
• Fan Z, Wirth AK, Chen D, et al. Nrf2-Keap1 pathway promotes cell proliferation and diminishes ferroptosis. Oncogenesis. 2017;6(8):e371.
   PubMedGoogle Scholar
• Jiang L, Kon N, Li T, et al. Ferroptosis as a p53-mediated activity during tumour suppression. Nature. 2015; 520(7545):57–62.
   PubMed Web of Science ®Google Scholar
• Xie Y, Zhu S, Song X, et al. The tumor suppressor p53 limits ferroptosis by blocking DPP4 activity. Cell Rep. 2017;20(7):1692–1704.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang YP, Tay YC, et al. Progressive adriamycin nephropathy in mice: sequence of histologic and immunohistochemical events. Kidney Int. 2000; Oct58(4):1797–1804.
   PubMed Web of Science ®Google Scholar
• Zhou J, Jiang L, Long X, et al. Bone-marrow-derived mesenchymal stem cells inhibit gastric aspiration lung injury and inflammation in rats. J Cell Mol Med. 2016; 20(9):1706–1717.
   PubMedGoogle Scholar
• Kikawada E, Lenda DM, Kelley VR. IL-12 deficiency in MRL-Fas(lpr) mice delays nephritis and intrarenal IFN-gamma expression, and diminishes systemic pathology. J Immunol. 2003; 170(7):3915–3925.
   PubMed Web of Science ®Google Scholar
• Kim S, Baek J, Park S, et al. Effects of blood transfusion on hepatic ischemia-reperfusion injury-induced renal tubular injury. Exp Clin Transplant. 2020;18(1):19–26.
   PubMedGoogle Scholar
• Silva-Palacios A, Ostolga-Chavarria M, Zazueta C, et al. Nrf2: molecular and epigenetic regulation during aging. Ageing Res Rev. 2018; 47:31–40.
   PubMed Web of Science ®Google Scholar
• Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal. 2005; 7(3–4):385–394.
   PubMed Web of Science ®Google Scholar
• Stockwell BR, Friedmann Angeli JP, Bayir H, et al. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell. 2017;171(2):273–285.
   PubMed Web of Science ®Google Scholar
• van Raaij S, van Swelm R, Bouman K, et al. Tubular iron deposition and iron handling proteins in human healthy kidney and chronic kidney disease. Sci Rep. 2018; 8(1):9353.
   PubMedGoogle Scholar
• Sponsel HT, Alfrey AC, Hammond WS, et al. Effect of iron on renal tubular epithelial cells. Kidney Int. 1996;50(2):436–444.
   PubMed Web of Science ®Google Scholar
• Ueda N, Baliga R, Shah SV. Role of 'catalytic’ iron in an animal model of minimal change nephrotic syndrome. Kidney Int. 1996;49(2):370–373.
   PubMed Web of Science ®Google Scholar
• Klein D. Lung multipotent stem cells of mesenchymal nature: cellular basis, clinical relevance, and implications for stem cell therapy. Antioxid Redox Signal. 2021; 35(3):204–216.
   PubMedGoogle Scholar
• Ghasroldasht MM, Irfan-Maqsood M, Matin MM, et al. Mesenchymal stem cell-based therapy for osteo-diseases. Cell Biol Int. 2014; 38(10):1081–1085.
   PubMed Web of Science ®Google Scholar
• Sherman LS, Romagano MP, Williams SF, et al. Mesenchymal stem cell therapies in brain disease. Semin Cell Dev Biol. 2019; 95:111–119.
   PubMedGoogle Scholar
• Rodriguez-Fuentes DE, Fernandez-Garza LE, Samia-Meza JA, et al. Mesenchymal stem cells current clinical applications: a systematic review. Arch Med Res. 2021; 52(1):93–101.
   PubMedGoogle Scholar
• Galipeau J, Sensebe L. Mesenchymal stromal cells: clinical challenges and therapeutic opportunities. Cell Stem Cell. 2018; 22(6):824–833.
   PubMed Web of Science ®Google Scholar
• Elhusseini FM, Saad MA, Anber N, et al. Long term study of protective mechanisms of human adipose derived mesenchymal stem cells on cisplatin induced kidney injury in Sprague-Dawley rats. J Stem Cells Regen Med. 2016;12(1):36–48.
   PubMedGoogle Scholar
• Morsy S, Mansour MF, Abdo M, et al. Can mobilization of bone marrow stem cells be an alternative regenerative therapy to stem cell injection in a rat model of chronic kidney disease? Physiol Rep. 2022;10(17):e15448.
   PubMedGoogle Scholar
• Wang H, Liu C, Zhao Y, et al. Mitochondria regulation in ferroptosis. Eur J Cell Biol. 2020; 99(1):151058.
   PubMed Web of Science ®Google Scholar
• Zhou J, Xiao C, Zheng S, et al. MicroRNA-214-3p aggravates ferroptosis by targeting GPX4 in cisplatin-induced acute kidney injury. Cell Stress Chaperones. 2022; 27(4):325–336.
   PubMedGoogle Scholar
• Hu Z, Zhang H, Yi B, et al. VDR activation attenuate cisplatin induced AKI by inhibiting ferroptosis. Cell Death Dis. 2020; 11(1):73.
   PubMed Web of Science ®Google Scholar
• Liu L, Yang S, Wang H. alpha-Lipoic acid alleviates ferroptosis in the MPP(+) -induced PC12 cells via activating the PI3K/Akt/Nrf2 pathway. Cell Biol Int. 2021; Feb45(2):422–431.
   PubMed Web of Science ®Google Scholar
• Chen HY, Xiao ZZ, Ling X, et al. ELAVL1 is transcriptionally activated by FOXC1 and promotes ferroptosis in myocardial ischemia/reperfusion injury by regulating autophagy. Mol Med. 2021; 27(1):14.
   PubMed Web of Science ®Google Scholar
• Wen Y, Chen H, Zhang L, et al. Glycyrrhetinic acid induces oxidative/nitrative stress and drives ferroptosis through activating NADPH oxidases and iNOS, and depriving glutathione in triple-negative breast cancer cells. Free Radic Biol Med. 2021; 173:41–51.
   PubMed Web of Science ®Google Scholar
• Sun L, Wang H, Yu S, et al. Herceptin induces ferroptosis and mitochondrial dysfunction in H9c2 cells. Int J Mol Med. 2022;49(2):17.
   Google Scholar
• Wang Y, Tang M. PM2.5 induces ferroptosis in human endothelial cells through iron overload and redox imbalance. Environ Pollut. 2019; 254(Pt A):112937.
   PubMedGoogle Scholar
• Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5):1060–1072.
   PubMed Web of Science ®Google Scholar
• Yang WS, Kim KJ, Gaschler MM, et al. Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc Natl Acad Sci U S A. 2016; 113(34):E4966–4975.
   PubMed Web of Science ®Google Scholar
• Yuan H, Li X, Zhang X, et al. Identification of ACSL4 as a biomarker and contributor of ferroptosis. Biochem Biophys Res Commun. 2016; 478(3):1338–1343.
   PubMed Web of Science ®Google Scholar
• Bellezza I, Giambanco I, Minelli A, et al. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim Biophys Acta Mol Cell Res. 2018; 1865(5):721–733.
   PubMed Web of Science ®Google Scholar
• Hwang I, Lee J, Huh JY, et al. Catalase deficiency accelerates diabetic renal injury through peroxisomal dysfunction. Diabetes. 2012; 61(3):728–738.
   PubMedGoogle Scholar
• Goven D, Boutten A, Lecon-Malas V, et al. Prolonged cigarette smoke exposure decreases heme oxygenase-1 and alters Nrf2 and Bach1 expression in human macrophages: roles of the MAP kinases ERK(1/2) and JNK. FEBS Lett. 2009; 583(21):3508–3518.
   PubMedGoogle Scholar
• Guo Y, Hu M, Ma J, et al. Protective effect of panaxydol against repeated administration of aristolochic acid on renal function and lipid peroxidation products via activating Keap1-Nrf2/ARE pathway in rat kidney. J Biochem Mol Toxicol. 2021; 35(1):e22619.
   PubMedGoogle 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.
   PubMed Web of Science ®Google Scholar
• Li Y, Cao Y, Xiao J, et al. Inhibitor of apoptosis-stimulating protein of p53 inhibits ferroptosis and alleviates intestinal ischemia/reperfusion-induced acute lung injury. Cell Death Differ. 2020; 27(9):2635–2650.
   PubMed Web of Science ®Google Scholar
• Wang D, Zhang S, Ge X, et al. Mesenchymal stromal cell treatment attenuates repetitive mild traumatic brain injury-induced persistent cognitive deficits via suppressing ferroptosis. J Neuroinflammation. 2022;19(1):185.
   PubMedGoogle Scholar
• Song Y, Wang B, Zhu X, et al. Human umbilical cord blood-derived MSCs exosome attenuate myocardial injury by inhibiting ferroptosis in acute myocardial infarction mice. Cell Biol Toxicol. 2021;37(1):51–64.
   PubMed Web of Science ®Google Scholar
• Zhang JK, Zhang Z, Guo ZA, et al. The BMSC-derived exosomal lncRNA Mir9-3hg suppresses cardiomyocyte ferroptosis in ischemia-reperfusion mice via the Pum2/PRDX6 axis. Nutr MetabCardiovascu Dis. 2022;32(2):515–527.
   PubMedGoogle Scholar
• Lin F, Chen W, Zhou J, et al. Mesenchymal stem cells protect against ferroptosis via exosome-mediated stabilization of SLC7A11 in acute liver injury. Cell Death Dis. 2022;13(3):271.
   PubMed Web of Science ®Google Scholar