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Research Articles

Aristolochic acid I aggravates oxidative stress-mediated apoptosis by inhibiting APE1/Nrf2/HO-1 signaling

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Pages 20-31 | Received 26 Jun 2023, Accepted 16 Aug 2023, Published online: 31 Aug 2023

References

  • Anger EE, Yu F, Li J. 2020. Aristolochic acid-induced nephrotoxicity: molecular mechanisms and potential protective approaches. Int J Mol Sci. 21(3):1157.
  • Balachandran P, Wei F, Lin RC, Khan IA, Pasco DS. 2005. Structure activity relationships of aristolochic acid analogues: toxicity in cultured renal epithelial cells. Kidney Int. 67(5):1797–1805. doi: 10.1111/j.1523-1755.2005.00277.x.
  • Barchiesi A, Bazzani V, Tolotto V, Elancheliyan P, Wasilewski M, Chacinska A, Vascotto C. 2020. Mitochondrial oxidative stress induces rapid intermembrane space/matrix translocation of apurinic/apyrimidinic endonuclease 1 protein through TIM23 complex. J Mol Biol. 432(24):166713. doi: 10.1016/j.jmb.2020.11.012.
  • Barta F, Dedikova A, Bebova M, Duskova S, Mraz J, Schmeiser HH, Arlt VM, Hodek P, Stiborova M. 2021. Co-exposure to aristolochic acids I and II increases DNA adduct formation responsible for aristolochic acid I-mediated carcinogenicity in rats. Int J Mol Sci. 22(19):10479.
  • Bhattacharyya A, Chattopadhyay R, Burnette BR, Cross JV, Mitra S, Ernst PB, Bhakat KK, Crowe SE. 2009. Acetylation of apurinic/apyrimidinic endonuclease-1 regulates Helicobacter pylori-mediated gastric epithelial cell apoptosis. Gastroenterology. 136(7):2258–2269. doi: 10.1053/j.gastro.2009.02.014.
  • Chang Q, Cai H, Wei L, Lan R. 2022. Chitosan oligosaccharides alleviate acute heat stress-induced oxidative damage by activating ERK1/2-mediated HO-1 and GSH-Px gene expression in breast muscle of broilers. Poult Sci. 101(1):101515. doi: 10.1016/j.psj.2021.101515.
  • Chen YY, Hong H, Lei YT, Zou J, Yang YY, He LY. 2021. IkappaB kinase promotes Nrf2 ubiquitination and degradation by phosphorylating cylindromatosis, aggravating oxidative stress injury in obesity-related nephropathy. Mol Med. 27(1):137. doi: 10.1186/s10020-021-00398-w.
  • Daenen K, Andries A, Mekahli D, Van Schepdael A, Jouret F, Bammens B. 2019. Oxidative stress in chronic kidney disease. Pediatr Nephrol. 34(6):975–991. doi: 10.1007/s00467-018-4005-4.
  • Dang R, Wang M, Li X, Wang H, Liu L, Wu Q, Zhao J, Ji P, Zhong L, Licinio J, et al. 2022. Edaravone ameliorates depressive and anxiety-like behaviors via Sirt1/Nrf2/HO-1/Gpx4 pathway. J Neuroinflammation. 19(1):41. doi: 10.1186/s12974-022-02400-6.
  • Eid BG, El-Shitany NA. 2021. Captopril downregulates expression of Bax/cytochrome C/caspase-3 apoptotic pathway, reduces inflammation, and oxidative stress in cisplatin-induced acute hepatic injury. Biomed Pharmacother. 139:111670. doi: 10.1016/j.biopha.2021.111670.
  • Fleming AM, Tran R, Omaga CA, Howpay Manage SA, Burrows CJ, Conboy JC. 2022. Second harmonic generation interrogation of the endonuclease APE1 binding interaction with G-quadruplex DNA. Anal Chem. 94(43):15027–15032. doi: 10.1021/acs.analchem.2c02951.
  • Garcia-Diaz B, Barca E, Balreira A, Lopez LC, Tadesse S, Krishna S, Naini A, Mariotti C, Castellotti B, Quinzii CM. 2015. Lack of aprataxin impairs mitochondrial functions via downregulation of the APE1/NRF1/NRF2 pathway. Hum Mol Genet. 24(16):4516–4529. doi: 10.1093/hmg/ddv183.
  • Grollman AP. 2013. Aristolochic acid nephropathy: harbinger of a global iatrogenic disease. Environ Mol Mutagen. 54(1):1–7. doi: 10.1002/em.21756.
  • Gupta KB, Dhiman M, Mantha AK. 2022. Gliadin induced oxidative stress and altered cellular responses in human intestinal cells: an in-vitro study to understand the cross-talk between the transcription factor Nrf-2 and multifunctional APE1 enzyme. J Biochem Mol Toxicol. 36(8):e23096.
  • Incalza MA, D'Oria R, Natalicchio A, Perrini S, Laviola L, Giorgino F. 2018. Oxidative stress and reactive oxygen species in endothelial dysfunction associated with cardiovascular and metabolic diseases. Vascul Pharmacol. 100:1–19. doi: 10.1016/j.vph.2017.05.005.
  • Jeon BH, Irani K. 2009. APE1/Ref-1: versatility in progress. Antioxid Redox Signal. 11(3):571–574. doi: 10.1089/ars.2008.2223.
  • Leak RK, Li P, Zhang F, Sulaiman HH, Weng Z, Wang G, Stetler RA, Shi Y, Cao G, Gao Y, et al. 2015. Apurinic/apyrimidinic endonuclease 1 upregulation reduces oxidative DNA damage and protects hippocampal neurons from ischemic injury. Antioxid Redox Signal. 22(2):135–148. doi: 10.1089/ars.2013.5511.
  • Liu X, Wu J, Wang J, Feng X, Wu H, Huang R, Fan J, Yu X, Yang X. 2020. Mitochondrial dysfunction is involved in aristolochic acid I-induced apoptosis in renal proximal tubular epithelial cells. Hum Exp Toxicol. 39(5):673–682. doi: 10.1177/0960327119897099.
  • Maremonti F, Meyer C, Linkermann A. 2022. Mechanisms and models of kidney tubular necrosis and nephron loss. J Am Soc Nephrol. 33(3):472–486. doi: 10.1681/ASN.2021101293.
  • Mu X, Wang J, He H, Li Q, Yang B, Wang J, Liu H, Gao Y, Ouyang L, Sun S, et al. 2021. An oligomeric semiconducting nanozyme with ultrafast electron transfers alleviates acute brain injury. Sci Adv. 7(46):eabk1210. doi: 10.1126/sciadv.abk1210.
  • Nezic L, Skrbic R, Amidzic L, Gajanin R, Milovanovic Z, Nepovimova E, Kuca K, Jacevic V. 2020. Protective effects of simvastatin on endotoxin-induced acute kidney injury through activation of tubular epithelial cells’ survival and hindering cytochrome C-mediated apoptosis. Int J Mol Sci. 21(19):7236.
  • Oliveira TT, Coutinho LG, de Oliveira LOA, Timoteo ARS, Farias GC, Agnez-Lima LF. 2022. APE1/Ref-1 role in inflammation and immune response. Front Immunol. 13:793096. doi: 10.3389/fimmu.2022.793096.
  • Peng H, You L, Yang C, Wang K, Liu M, Yin D, Xu Y, Dong X, Yin X, Ni J. 2021. Ginsenoside Rb1 attenuates triptolide-induced cytotoxicity in HL-7702 cells via the activation of Keap1/Nrf2/ARE pathway. Front Pharmacol. 12:723784. doi: 10.3389/fphar.2021.723784.
  • Qiu D, Song S, Wang Y, Bian Y, Wu M, Wu H, Shi Y, Duan H. 2022. NAD(P)H: quinone oxidoreductase 1 attenuates oxidative stress and apoptosis by regulating Sirt1 in diabetic nephropathy. J Transl Med. 20(1):44. doi: 10.1186/s12967-021-03197-3.
  • Romanov V, Whyard TC, Waltzer WC, Grollman AP, Rosenquist T. 2015. Aristolochic acid-induced apoptosis and G2 cell cycle arrest depends on ROS generation and MAP kinases activation. Arch Toxicol. 89(1):47–56. doi: 10.1007/s00204-014-1249-z.
  • Sasaki K, Terker AS, Tang J, Cao S, Arroyo JP, Niu A, Wang S, Fan X, Zhang Y, Bennett SR, et al. 2022. Macrophage interferon regulatory factor 4 deletion ameliorates aristolochic acid nephropathy via reduced migration and increased apoptosis. JCI Insight. 7(4):723. doi: 10.1172/jci.insight.150723.
  • Shan JL, He HT, Li MX, Zhu JW, Cheng Y, Hu N, Wang G, Wang D, Yang XQ, He Y, et al. 2015. APE1 promotes antioxidant capacity by regulating Nrf-2 function through a redox-dependent mechanism. Free Radic Biol Med. 78:11–22. doi: 10.1016/j.freeradbiomed.2014.10.007.
  • Sies H, Belousov VV, Chandel NS, Davies MJ, Jones DP, Mann GE, Murphy MP, Yamamoto M, Winterbourn C. 2022. Defining roles of specific reactive oxygen species (ROS) in cell biology and physiology. Nat Rev Mol Cell Biol. 23(7):499–515. doi: 10.1038/s41580-022-00456-z.
  • Sriramajayam K, Peng D, Lu H, Zhou S, Bhat N, McDonald OG, Que J, Zaika A, El-Rifai W. 2021. Activation of NRF2 by APE1/REF1 is redox-dependent in Barrett’s related esophageal adenocarcinoma cells. Redox Biol. 43:101970. doi: 10.1016/j.redox.2021.101970.
  • Stiborova M, Arlt VM, Schmeiser HH. 2017. DNA adducts formed by aristolochic acid are unique biomarkers of exposure and explain the initiation phase of upper urothelial cancer. Int J Mol Sci. 18(10):2144.
  • Stiborova M, Martinek V, Frei E, Arlt VM, Schmeiser HH. 2013. Enzymes metabolizing aristolochic acid and their contribution to the development of aristolochic acid nephropathy and urothelial cancer. Curr Drug Metab. 14(6):695–705. doi: 10.2174/1389200211314060006.
  • Su L, Zhang J, Gomez H, Kellum JA, Peng Z. 2023. Mitochondria ROS and mitophagy in acute kidney injury. Autophagy. 19(2):401–414. doi: 10.1080/15548627.2022.2084862.
  • Thakur S, Dhiman M, Mantha AK. 2018. APE1 modulates cellular responses to organophosphate pesticide-induced oxidative damage in non-small cell lung carcinoma A549 cells. Mol Cell Biochem. 441(1–2):201–216. doi: 10.1007/s11010-017-3186-7.
  • Thakur S, Sarkar B, Dhiman M, Mantha AK. 2021. Organophosphate-pesticides induced survival mechanisms and APE1-mediated Nrf2 regulation in non-small-cell lung cancer cells. J Biochem Mol Toxicol. 35(2):e22640. doi: 10.1002/jbt.22640.
  • Ullah A, Leong SW, Wang J, Wu Q, Ghauri MA, Sarwar A, Su Q, Zhang Y. 2021. Cephalomannine inhibits hypoxia-induced cellular function via the suppression of APEX1/HIF-1alpha interaction in lung cancer. Cell Death Dis. 12(5):490. doi: 10.1038/s41419-021-03771-z.
  • Urate S, Wakui H, Azushima K, Yamaji T, Suzuki T, Abe E, Tanaka S, Taguchi S, Tsukamoto S, Kinguchi S, et al. 2021. Aristolochic acid induces renal fibrosis and senescence in mice. Int J Mol Sci. 22(22):12432.
  • Wang G, Zhang D, Yang S, Wang Y, Tang Z, Fu X. 2018. Co-administration of genistein with doxorubicin-loaded polypeptide nanoparticles weakens the metastasis of malignant prostate cancer by amplifying oxidative damage. Biomater Sci. 6(4):827–835. doi: 10.1039/c7bm01201b.
  • Wang Y, Liu Z, Ma J, Xv Q, Gao H, Yin H, Yan G, Jiang X, Yu W. 2022. Lycopene attenuates the inflammation and apoptosis in aristolochic acid nephropathy by targeting the Nrf2 antioxidant system. Redox Biol. 57:102494. doi: 10.1016/j.redox.2022.102494.
  • Yang B, Xie Y, Guo M, Rosner MH, Yang H, Ronco C. 2018. Nephrotoxicity and Chinese herbal medicine. Clin J Am Soc Nephrol. 13(10):1605–1611. doi: 10.2215/CJN.11571017.
  • Ye J, Qian Z, Xue M, Liu Y, Zhu S, Li Y, Liu X, Cai D, Rui J, Zhang L. 2019. Aristolochic acid I aggravates renal injury by activating the C3a/C3aR complement system. Toxicol Lett. 312:118–124. doi: 10.1016/j.toxlet.2019.04.027.
  • Zhang Q, Ye J, Zhang Z, Hu Y, Wang X, Jiang W, Guo X, Chen L, Cheng S, Li J, et al. 2023. Aristolocholic acid I promotes renal tubular epithelial fibrosis by upregulating matrix metalloproteinase-9 expression via activating the C3a/C3aR axis of macrophages. Toxicol Lett. 381:27–35. doi: 10.1016/j.toxlet.2023.04.009.
  • Zhang Y, Zhang Q, Li L, Mu D, Hua K, Ci S, Shen L, Zheng L, Shen B, Guo Z. 2020. Arginine methylation of APE1 promotes its mitochondrial translocation to protect cells from oxidative damage. Free Radic Biol Med. 158:60–73. doi: 10.1016/j.freeradbiomed.2020.06.027.
  • Zhao CR, Yang FF, Cui Q, Wang D, Zhou Y, Li YS, Zhang YP, Tang RZ, Yao WJ, Wang X, et al. 2021. Vitexin inhibits APEX1 to counteract the flow-induced endothelial inflammation. Proc Natl Acad Sci USA. 118(48):e2115158118.
  • Zhao H, Zhang R, Yan X, Fan K. 2021. Superoxide dismutase nanozymes: an emerging star for anti-oxidation. J Mater Chem B. 9(35):6939–6957. doi: 10.1039/d1tb00720c.
  • Zhao M, Wang Y, Li L, Liu S, Wang C, Yuan Y, Yang G, Chen Y, Cheng J, Lu Y, et al. 2021. Mitochondrial ROS promote mitochondrial dysfunction and inflammation in ischemic acute kidney injury by disrupting TFAM-mediated mtDNA maintenance. Theranostics. 11(4):1845–1863. doi: 10.7150/thno.50905.
  • Zhao YH, Shen CF, Kang Y, Qi A, Xu WJ, Shi WH, Liu JW. 2021. Curcumin prevents renal cell apoptosis in acute kidney injury in a rat model of dry-heat environment heatstroke via inhibition of the mitochondrial apoptotic pathway. Exp Ther Med. 21(2):126. doi: 10.3892/etm.2020.9558.
  • Zhou S, He Y, Zhang W, Xiong Y, Jiang L, Wang J, Cui X, Qu Y, Ge F. 2021. Ophiocordyceps lanpingensis polysaccharides alleviate chronic kidney disease through MAPK/NF-kappaB pathway. J Ethnopharmacol. 276:114189. doi: 10.1016/j.jep.2021.114189.

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