Metformin attenuates PM_2.5-induced oxidative stress by inhibiting the AhR/CYP1A1 pathway in proximal renal tubular epithelial cells

References

• Alanazi FE, As Sobeai HM, Alhazzani K, Al-Dhfyan A, Alshammari MA, Alotaibi M, Al-Hosaini K, Korashy HM, Alhoshani A. 2022. Metformin attenuates V-domain Ig suppressor of T-cell activation through the aryl hydrocarbon receptor pathway in Melanoma: in vivo and in vitro studies. Saudi Pharm J. 30(2):138–149. doi: 10.1016/j.jsps.2021.12.014.
   PubMed Web of Science ®Google Scholar
• Alhoshani A, Alotaibi M, As Sobeai HM, Alharbi N, Alhazzani K, Al-Dhfyan A, Alanazi FE, Korashy HM. 2021. In vivo and in vitro studies evaluating the chemopreventive effect of metformin on the aryl hydrocarbon receptor-mediated breast carcinogenesis. Saudi J Biol Sci. 28(12):7396–7403. doi: 10.1016/j.sjbs.2021.08.051.
   PubMed Web of Science ®Google Scholar
• Blum MF, Surapaneni A, Stewart JD, Liao D, Yanosky JD, Whitsel EA, Power MC, Grams ME. 2020. Particulate matter and albuminuria, glomerular filtration rate, and incident CKD. Clin J Am Soc Nephrol. 15(3):311–319. doi: 10.2215/CJN.08350719.
   PubMed Web of Science ®Google Scholar
• Bobb JF, Claus Henn B, Valeri L, Coull BA. 2018. Statistical software for analyzing the health effects of multiple concurrent exposures via Bayesian kernel machine regression. Environ Health. 17(1):67. doi: 10.1186/s12940-018-0413-y.
   PubMedGoogle Scholar
• Chan JKW, Charrier JG, Kodani SD, Vogel CF, Kado SY, Anderson DS, Anastasio C, Van Winkle LS. 2013. Combustion-derived flame generated ultrafine soot generates reactive oxygen species and activates Nrf2 antioxidants differently in neonatal and adult rat lungs. Part Fibre Toxicol. 10(1):34. doi: 10.1186/1743-8977-10-34.
   PubMedGoogle Scholar
• Chen J, Zhang M, Zou H, Aniagu S, Jiang Y, Chen T. 2023. PM2.5 induces mitochondrial dysfunction via AHR-mediated cyp1a1 overexpression during zebrafish heart development. Toxicology. 487:153466. doi: 10.1016/j.tox.2023.153466.
   PubMed Web of Science ®Google Scholar
• Chen W, Luo Y, Quan J, Zhou J, Yi B, Huang Z. 2023. PM2.5 induces renal tubular injury by activating NLRP3-mediated pyroptosis. Ecotoxicol Environ Saf. 265:115490. doi: 10.1016/j.ecoenv.2023.115490.
   PubMed Web of Science ®Google Scholar
• Chen Z, Liu P, Xia X, Wang L, Li X. 2022. The underlying mechanism of PM2.5-induced ischemic stroke. Environ Pollut. 310:119827. doi: 10.1016/j.envpol.2022.119827.
   PubMed Web of Science ®Google Scholar
• Cheng L, Li Z, Huang YZ, Zhang X, Dai XY, Shi L, Xi PW, Wei JF, Ding Q. 2019. TCDD-inducible Poly-ADP-Ribose Polymerase (TIPARP), a novel therapeutic target of breast cancer. Cancer Manag Res. 11:8991–9004. doi: 10.2147/CMAR.S219289.
   PubMed Web of Science ®Google Scholar
• Cuevas S, Pelegrín P. 2021. Pyroptosis and redox balance in kidney diseases. Antioxidants & Redox Signaling. 35(1):40–60. doi: 10.1089/ars.2020.8243.
   PubMed Web of Science ®Google Scholar
• Delgado C, Baweja M, Crews DC, Eneanya ND, Gadegbeku CA, Inker LA, Mendu ML, Miller WG, Moxey-Mims MM, Roberts GV, et al. 2022. A unifying approach for GFR estimation: recommendations of the NKF-ASN task force on reassessing the inclusion of race in diagnosing kidney disease. Am J Kidney Dis. 79(2):268–288.e1. doi: 10.1053/j.ajkd.2021.08.003.
   PubMed Web of Science ®Google Scholar
• Denison MS, Nagy SR. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol. 43(1):309–334. doi: 10.1146/annurev.pharmtox.43.100901.135828.
   PubMed Web of Science ®Google Scholar
• Do MT, Kim HG, Tran TTP, Khanal T, Choi JH, Chung YC, Jeong TC, Jeong HG. 2014. Metformin suppresses CYP1A1 and CYP1B1 expression in breast cancer cells by down-regulating aryl hydrocarbon receptor expression. Toxicol Appl Pharmacol. 280(1):138–148. doi: 10.1016/j.taap.2014.07.021.
   PubMed Web of Science ®Google Scholar
• Dou L, Poitevin S, Sallée M, Addi T, Gondouin B, McKay N, Denison MS, Jourde-Chiche N, Duval-Sabatier A, Cerini C, et al. 2018. Aryl hydrocarbon receptor is activated in patients and mice with chronic kidney disease. Kidney Int. 93(4):986–999. doi: 10.1016/j.kint.2017.11.010.
   PubMed Web of Science ®Google Scholar
• Du X, Zeng X, Pan K, Zhang J, Song L, Zhou J, Chen R, Xie Y, Sun Q, Zhao J, et al. 2020. Metabolomics analysis of urine from healthy wild type mice exposed to ambient PM2.5. Sci Total Environ. 714:136790. doi: 10.1016/j.scitotenv.2020.136790.
   PubMed Web of Science ®Google Scholar
• Everett CJ, Thompson OM. 2014. Dioxins, furans and dioxin-like PCBs in human blood: causes or consequences of diabetic nephropathy? Environ Res. 132:126–131. doi: 10.1016/j.envres.2014.03.043.
   PubMed Web of Science ®Google Scholar
• Everett CJ, Thompson OM. 2016. Association of dioxins, furans and dioxin-like PCBs in human blood with nephropathy among US teens and young adults. Rev Environ Health. 31(2):195–201. doi: 10.1515/reveh-2015-0031.
   PubMed Web of Science ®Google Scholar
• Fan X, Dong T, Yan K, Ci X, Peng L. 2023. PM2.5 increases susceptibility to acute exacerbation of COPD via NOX4/Nrf2 redox imbalance-mediated mitophagy. Redox Biol. 59:102587. doi: 10.1016/j.redox.2022.102587.
   PubMed Web of Science ®Google Scholar
• Gao J, Yuan J, Wang Q, Lei T, Shen X, Cui B, Zhang F, Ding W, Lu Z. 2020. Metformin protects against PM2.5-induced lung injury and cardiac dysfunction independent of AMP-activated protein kinase α2. Redox Biol. 28:101345. doi: 10.1016/j.redox.2019.101345.
   PubMed Web of Science ®Google Scholar
• Ge C, Xu M, Qin Y, Gu T, Lv J, Wang M, Wang S, Ma Y, Lou D, Li Q, et al. 2018. iRhom2 loss alleviates renal injury in long-term PM2.5-exposed mice by suppression of inflammation and oxidative stress. Redox Biol. 19:147–157. doi: 10.1016/j.redox.2018.08.009.
   PubMed Web of Science ®Google Scholar
• He J, Huang T, Zhao L. 2019. 3,3′-Diindolylmethane mitigates lipopolysaccharide-induced acute kidney injury in mice by inhibiting NOX-mediated oxidative stress and the apoptosis of renal tubular epithelial cells. Mol Med Rep. 19(6):5115–5122. doi: 10.3892/mmr.2019.10178.
   PubMed Web of Science ®Google Scholar
• Hou T, Zhu L, Wang Y, Peng L. 2023. Oxidative stress is the pivot for PM2.5-induced lung injury. Food Chem Toxicol. 184:114362. doi: 10.1016/j.fct.2023.114362.
   PubMed Web of Science ®Google Scholar
• Hu J, Hou W, Ma N, Zhang Y, Liu X, Wang Y, Ci X. 2024. Aging-related NOX4-Nrf2 redox imbalance increases susceptibility to cisplatin-induced acute kidney injury by regulating mitophagy. Life Sci. 336:122352. doi: 10.1016/j.lfs.2023.122352.
   PubMed Web of Science ®Google Scholar
• Hu W, Wang Y, Wang T, Ji Q, Jia Q, Meng T, Ma S, Zhang Z, Li Y, Chen R, et al. 2021. Ambient particulate matter compositions and increased oxidative stress: exposure-response analysis among high-level exposed population. Environ Int. 147:106341. doi: 10.1016/j.envint.2020.106341.
   PubMed Web of Science ®Google Scholar
• Huang CY, Wu CL, Wu JS, Chang JW, Cheng YY, Kuo YC, Yang YC, Lee CC, Guo HR. 2016. Association between blood dioxin level and chronic kidney disease in an endemic area of exposure. PLoS One. 11(3):e0150248. doi: 10.1371/journal.pone.0150248.
   PubMed Web of Science ®Google Scholar
• Huang X, Shi X, Zhou J, Li S, Zhang L, Zhao H, Kuang X, Li J. 2020. The activation of antioxidant and apoptosis pathways involved in damage of human proximal tubule epithelial cells by PM2.5 exposure. Environ Sci Eur. 32(1):2. doi: 10.1186/s12302-019-0284-z.
   Web of Science ®Google Scholar
• İlhan S, Ateşşahin D, Ateşşahin A, Mutlu E, Onat E, Şahna E. 2015. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced hypertension: the beneficial effects of melatonin. Toxicol Ind Health. 31(4):298–303. doi: 10.1177/0748233712472521.
   PubMed Web of Science ®Google Scholar
• Inker LA, Astor BC, Fox CH, Isakova T, Lash JP, Peralta CA, Kurella Tamura M, Feldman HI. 2014. KDOQI US commentary on the 2012 KDIGO clinical practice guideline for the evaluation and management of CKD. Am J Kidney Dis. 63(5):713–735. doi: 10.1053/j.ajkd.2014.01.416.
   PubMed Web of Science ®Google Scholar
• Jain RB. 2021. Trends in concentrations of selected dioxins and furans across various stages of kidney function for US adults. Environ Sci Pollut Res Int. 28(32):43763–43776. doi: 10.1007/s11356-021-13844-3.
   PubMed Web of Science ®Google Scholar
• Jha JC, Banal C, Chow BSM, Cooper ME, Jandeleit-Dahm K. 2016. Diabetes and kidney disease: role of oxidative stress. Antioxid Redox Signal. 25(12):657–684. doi: 10.1089/ars.2016.6664.
   PubMed Web of Science ®Google Scholar
• Klein SG, Cambier S, Hennen J, Legay S, Serchi T, Nelissen I, Chary A, Moschini E, Krein A, Blömeke B, et al. 2017. Endothelial responses of the alveolar barrier in vitro in a dose-controlled exposure to diesel exhaust particulate matter. Part Fibre Toxicol. 14(1):7. doi: 10.1186/s12989-017-0186-4.
   PubMedGoogle Scholar
• Lee W, Wu X, Heo S, Kim JM, Fong KC, Son JY, Sabath MB, Trisovic A, Braun D, Park JY, et al. 2023. Air pollution and acute kidney injury in the U.S. medicare population: a longitudinal cohort study. Environ Health Perspect. 131(4):47008. doi: 10.1289/EHP10729.
   PubMed Web of Science ®Google Scholar
• Li D, Li Y, Li G, Zhang Y, Li J, Chen H. 2019. Fluorescent reconstitution on deposition of PM2.5 in lung and extrapulmonary organs. Proc Natl Acad Sci U S A. 116(7):2488–2493. doi: 10.1073/pnas.1818134116.
   PubMed Web of Science ®Google Scholar
• Li G, Huang J, Wang J, Zhao M, Liu Y, Guo X, Wu S, Zhang L. 2021. Long-term exposure to ambient PM2.5 and increased risk of CKD prevalence in China. J Am Soc Nephrol. 32(2):448–458. doi: 10.1681/ASN.2020040517.
   PubMed Web of Science ®Google Scholar
• Liu CS, Wei Y, Yazdi MD, Qiu X, Castro E, Zhu Q, Li L, Koutrakis P, Ekenga CC, Shi L, et al. 2023. Long-term association of air pollution and incidence of lung cancer among older Americans: a national study in the Medicare cohort. Environ Int. 181:108266. doi: 10.1016/j.envint.2023.108266.
   PubMed Web of Science ®Google Scholar
• Maayah ZH, Ghebeh H, Alhaider AA, El-Kadi AOS, Soshilov AA, Denison MS, Ansari MA, Korashy HM. 2015. Metformin inhibits 7,12-dimethylbenz[a]anthracene-induced breast carcinogenesis and adduct formation in human breast cells by inhibiting the cytochrome P4501A1/aryl hydrocarbon receptor signaling pathway. Toxicol Appl Pharmacol. 284(2):217–226. doi: 10.1016/j.taap.2015.02.007.
   PubMed Web of Science ®Google Scholar
• Mehta AJ, Zanobetti A, Bind MAC, Kloog I, Koutrakis P, Sparrow D, Vokonas PS, Schwartz JD. 2016. Long-term exposure to ambient fine particulate matter and renal function in older men: the veterans administration normative aging study. Environ Health Perspect. 124(9):1353–1360. doi: 10.1289/ehp.1510269.
   PubMed Web of Science ®Google Scholar
• Nemmar A, Hoet PHM, Vanquickenborne B, Dinsdale D, Thomeer M, Hoylaerts MF, Vanbilloen H, Mortelmans L, Nemery B. 2002. Passage of inhaled particles into the blood circulation in humans. Circulation. 105(4):411–414. doi: 10.1161/hc0402.104118.
   PubMed Web of Science ®Google Scholar
• Paller MS, Hoidal JR, Ferris TF. 1984. Oxygen free radicals in ischemic acute renal failure in the rat. J Clin Invest. 74(4):1156–1164. doi: 10.1172/JCI111524.
   PubMed Web of Science ®Google Scholar
• Pan Q, Lu X, Zhao C, Liao S, Chen X, Guo F, Yang C, Liu H. 2020. Metformin: the updated protective property in kidney disease. Aging (Albany NY). 12(9):8742–8759. doi: 10.18632/aging.103095.
   PubMedGoogle Scholar
• Park B, London NR, Tharakan A, Rengasamy P, Rajagopalan S, Biswal S, Pinto JM, Ramanathan M. 2022. Particulate matter air pollution exposure disrupts the Nrf2 pathway in sinonasal epithelium via epigenetic alterations in a murine model. Int Forum Allergy Rhinol. 12(11):1424–1427. doi: 10.1002/alr.23010.
   PubMed Web of Science ®Google Scholar
• Park JY, Shigenaga MK, Ames BN. 1996. Induction of cytochrome P4501A1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin or indolo(3,2-b)carbazole is associated with oxidative DNA damage. Proc Natl Acad Sci U S A. 93(6):2322–2327. doi: 10.1073/pnas.93.6.2322.
   PubMed Web of Science ®Google Scholar
• Ran J, Yang A, Sun S, Han L, Li J, Guo F, Zhao S, Yang Y, Mason TG, Chan KP, et al. 2020. Long-term exposure to ambient fine particulate matter and mortality from renal failure: a retrospective cohort study in Hong Kong, China. Am J Epidemiol. 189(6):602–612. doi: 10.1093/aje/kwz282.
   PubMed Web of Science ®Google Scholar
• Rosa MJ, Politis MD, Tamayo-Ortiz M, Colicino E, Pantic I, Estrada-Gutierrez G, Tolentino MC, Espejel-Nuñez A, Solano-Gonzalez M, Kloog I, et al. 2022. Critical windows of perinatal particulate matter (PM2.5) exposure and preadolescent kidney function. Environ Res. 204(Pt B):112062. doi: 10.1016/j.envres.2021.112062.
   PubMedGoogle Scholar
• Sheng Y, Zhang C, Cai D, Xu G, Chen S, Li W, Dong J, Shen B, Tang J, Xu L. 2024. 2,2′,4,4′-Tetrabromodiphenyl ether and cadmium co-exposure activates aryl hydrocarbon receptor pathway to induce ROS and GSDME-dependent pyroptosis in renal tubular epithelial cells. Environ Toxicol. 39(1):289–298. doi: 10.1002/tox.23957.
   PubMed Web of Science ®Google Scholar
• Shi L, Zhu Q, Wang Y, Hao H, Zhang H, Schwartz J, Amini H, van Donkelaar A, Martin RV, Steenland K, et al. 2023. Incident dementia and long-term exposure to constituents of fine particle air pollution: A national cohort study in the United States. Proc Natl Acad Sci U S A. 120(1):e2211282119. doi: 10.1073/pnas.2211282119.
   PubMed Web of Science ®Google Scholar
• Soberanes S, Misharin AV, Jairaman A, Morales-Nebreda L, McQuattie-Pimentel AC, Cho T, Hamanaka RB, Meliton AY, Reyfman PA, Walter JM, et al. 2019. Metformin targets mitochondrial electron transport to reduce air-pollution-induced thrombosis. Cell Metab. 29(2):335–347.e5. doi: 10.1016/j.cmet.2018.09.019.
   PubMed Web of Science ®Google Scholar
• Song J, Han K, Wang Y, Qu R, Liu Y, Wang S, Wang Y, An Z, Li J, Wu H, et al. 2022. Microglial activation and oxidative stress in PM2.5-induced neurodegenerative disorders. Antioxidants (Basel). 11(8):1482. doi: 10.3390/antiox11081482.
   PubMedGoogle Scholar
• Stejskalova L, Dvorak Z, Pavek P. 2011. Endogenous and exogenous ligands of aryl hydrocarbon receptor: current state of art. Curr Drug Metab. 12(2):198–212. doi: 10.2174/138920011795016818.
   PubMed Web of Science ®Google Scholar
• Sterling T, Irwin JJ. 2015. ZINC 15 – ligand discovery for everyone. J Chem Inf Model. 55(11):2324–2337. doi: 10.1021/acs.jcim.5b00559.
   PubMed Web of Science ®Google Scholar
• Wagener FATG, Dekker D, Berden JH, Scharstuhl A, van der Vlag J. 2009. The role of reactive oxygen species in apoptosis of the diabetic kidney. Apoptosis. 14(12):1451–1458. doi: 10.1007/s10495-009-0359-1.
   PubMed Web of Science ®Google Scholar
• Wang BH, Tang LL, Sun XH, Zhang Q, Liu CY, Zhang XN, Yu KY, Yang Y, Hu J, Shi XL, et al. 2024. Qufeng Xuanbi Formula inhibited benzo[a]pyrene-induced aggravated asthma airway mucus secretion by AhR/ROS/ERK pathway. J Ethnopharmacol. 319(Pt 1):117203. doi: 10.1016/j.jep.2023.117203.
   PubMedGoogle Scholar
• Wang T, Huang K, Chen C, Chang Y, Chen H, Hsueh C, Liu Y, Yang S, Yang P, Chen C. 2023. PM2.5 promotes lung cancer progression through activation of the AhR‐TMPRSS2‐IL18 pathway. EMBO Mol Med. 15(6):e17014. doi: 10.15252/emmm.202217014.
   PubMed Web of Science ®Google Scholar
• Wu Q, Huang F. 2024. Targeting ferroptosis as a prospective therapeutic approach for diabetic nephropathy. Ann Med. 56(1):2346543. doi: 10.1080/07853890.2024.2346543.
   PubMed Web of Science ®Google Scholar
• Xu C, Zhang Q, Huang G, Huang J, Fu X, Liu M, Sun Y, Zhang H. 2023. Vitamin B ameliorates PM2.5-induced kidney damage by reducing endoplasmic reticulum stress and oxidative stress in pregnant mice and HK-2. Toxicology. 494:153568. doi: 10.1016/j.tox.2023.153568.
   PubMed Web of Science ®Google Scholar
• Xu MX, Qin YT, Ge CX, Gu TT, Lou DS, Li Q, Hu LF, Li YY, Yang WW, Tan J. 2018. Activated iRhom2 drives prolonged PM 2.5 exposure-triggered renal injury in Nrf2-defective mice. Nanotoxicology. 12(9):1045–1067. doi: 10.1080/17435390.2018.1513093.
   PubMed Web of Science ®Google Scholar
• Xu X, Wang G, Chen N, Lu T, Nie S, Xu G, Zhang P, Luo Y, Wang Y, Wang X, et al. 2016. Long-term exposure to air pollution and increased risk of membranous nephropathy in China. J Am Soc Nephrol. 27(12):3739–3746. doi: 10.1681/ASN.2016010093.
   PubMed Web of Science ®Google Scholar
• Ye G, Hu M, Xiao L. 2023. Forkhead box A2‐mediated lncRNA SOX2OT up‐regulation alleviates oxidative stress and apoptosis of renal tubular epithelial cells by promoting SIRT1 expression in diabetic nephropathy. Nephrology (Carlton). 28(3):196–207. doi: 10.1111/nep.14139.
   PubMed Web of Science ®Google Scholar
• Yuan Q, Chen Y, Li X, Zhang Z, Chu H. 2019. Ambient fine particulate matter (PM2.5) induces oxidative stress and pro-inflammatory response via up-regulating the expression of CYP1A1/1B1 in human bronchial epithelial cells in vitro. Mutat Res Genet Toxicol Environ Mutagen. 839:40–48. doi: 10.1016/j.mrgentox.2018.12.005.
   PubMed Web of Science ®Google Scholar
• Zhan Z, Li A, Zhang W, Wu X, He J, Li Z, Li Y, Sun J, Zhang H. 2022. ATP-citrate lyase inhibitor improves ectopic lipid accumulation in the kidney in a db/db mouse model. Front Endocrinol (Lausanne). 13:914865. doi: 10.3389/fendo.2022.914865.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu D, Liu Z. 2021. Fine particulate matter (PM2.5) and chronic kidney disease. Rev Environ Contam Toxicol. 254:183–215. doi: 10.1007/398_2020_62.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Xia Y, Chang Q, Ji C, Zhao Y, Zhang H. 2023. Exposure to ambient air pollution and metabolic kidney diseases: evidence from the Northeast China Biobank. Nephrol Dial Transplant. 38(10):2222–2231. doi: 10.1093/ndt/gfad042.
   PubMed Web of Science ®Google Scholar
• Zhao C, Wang Y, Su Z, Pu W, Niu M, Song S, Wei L, Ding Y, Xu L, Tian M, et al. 2020. Respiratory exposure to PM2.5 soluble extract disrupts mucosal barrier function and promotes the development of experimental asthma. Sci Total Environ. 730:139145. doi: 10.1016/j.scitotenv.2020.139145.
   PubMed Web of Science ®Google Scholar
• Zhao J, Ma X, Li S, Liu C, Liu Y, Tan J, Yu L, Li X, Li W. 2023. Berberine hydrochloride ameliorates PM2.5-induced pulmonary fibrosis in mice through inhibiting oxidative stress and inflammatory. Chem Biol Interact. 386:110731. doi: 10.1016/j.cbi.2023.110731.
   PubMed Web of Science ®Google Scholar
• Zhu L, Zhang Q, Hua C, Ci X. 2023. Melatonin alleviates particulate matter-induced liver fibrosis by inhibiting ROS-mediated mitophagy and inflammation via Nrf2 activation. Ecotoxicol Environ Saf. 268:115717. doi: 10.1016/j.ecoenv.2023.115717.
   PubMed Web of Science ®Google Scholar