219
Views
9
CrossRef citations to date
0
Altmetric
Original Research

Hypermethylation of the Nrf2 Promoter Induces Ferroptosis by Inhibiting the Nrf2-GPX4 Axis in COPD

, , , , , , , & show all
Pages 3347-3362 | Published online: 14 Dec 2021

References

  • Leonardo F, Pauwels RA, Hurd SS. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary updated 2003. Am J Respir Crit Care Med. 2007;1:104.
  • Prange R, Thiedmann M, Bhandari A, et al. A Drosophila model of cigarette smoke induced COPD identifies Nrf2 signaling as an expedient target for intervention. Aging. 2018;10(8):2122–2135. doi:10.18632/aging.101536
  • Tuder RM, Zhen L, Cho CY, et al. Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. Am J Respir Cell Mol Biol. 2003;29(1):88–97. doi:10.1165/rcmb.2002-0228OC
  • Giangreco A, Groot KR, Janes SM. Lung cancer and lung stem cells: strange bedfellows? Am J Respir Crit Care Med. 2007;175(6):547–553. doi:10.1164/rccm.200607-984PP
  • Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet. 2004;364(9435):709–721. doi:10.1016/S0140-6736(04)16900-6
  • de Marco R, Accordini S, Marcon A, et al. Risk factors for chronic obstructive pulmonary disease in a European cohort of young adults. Am J Respir Crit Care Med. 2011;183(7):891–897. doi:10.1164/rccm.201007-1125OC
  • Toledo-Pons N, Cosio BG, Velasco MD, Casanova C. Chronic obstructive pulmonary disease in non-smokers. Arch Bronconeumol. 2017;53(2):45–46. doi:10.1016/j.arbr.2016.11.033
  • Martinez FD. Early-life origins of chronic obstructive pulmonary disease. N Engl J Med. 2016;375(9):871–878. doi:10.1056/NEJMra1603287
  • Higashi T, Mai Y, Noya Y, et al. A simple and rapid method for standard preparation of gas phase extract of cigarette smoke. PLoS One. 2014;9(9):e107856. doi:10.1371/journal.pone.0107856
  • Linkermann A, Stockwell BR, Krautwald S, Anders HJ. Regulated cell death and inflammation: an auto-amplification loop causes organ failure. Nat Rev Immunol. 2014;14(11):759–767. doi:10.1038/nri3743
  • Barnes PJ. Cellular and molecular mechanisms of chronic obstructive pulmonary disease. Clin Chest Med. 2014;35(1):71–86. doi:10.1016/j.ccm.2013.10.004
  • Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003;43:233–260. doi:10.1146/annurev.pharmtox.43.100901.140229
  • Kuang F, Liu J, Tang D, Kang R. Oxidative damage and antioxidant defense in ferroptosis. Front Cell Dev Biol. 2020;8:586578. doi:10.3389/fcell.2020.586578
  • Kobayashi M, Li L, Iwamoto N, et al. The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol Cell Biol. 2009;29(2):493–502. doi:10.1128/MCB.01080-08
  • McMahon M, Lamont DJ, Beattie KA, Hayes JD. Keap1 perceives stress via three sensors for the endogenous signaling molecules nitric oxide, zinc, and alkenals. Proc Natl Acad Sci U S A. 2010;107(44):18838–18843. doi:10.1073/pnas.1007387107
  • Foronjy R, D’Armiento J. The effect of cigarette smoke-derived oxidants on the inflammatory response of the lung. Clin Appl Immunol Rev. 2006;6(1):53–72. doi:10.1016/j.cair.2006.04.002
  • Dong H, Qiang Z, Chai D, et al. Nrf2 inhibits ferroptosis and protects against acute lung injury due to intestinal ischemia reperfusion via regulating SLC7A11 and HO-1. Aging. 2020;12(13):12943–12959. doi:10.18632/aging.103378
  • Boutten A, Goven D, Boczkowski J, Bonay M. Oxidative stress targets in pulmonary emphysema: focus on the Nrf2 pathway. Expert Opin Ther Targets. 2010;14(3):329–346. doi:10.1517/14728221003629750
  • Suzuki M, Betsuyaku T, Ito Y, et al. Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol. 2008;39(6):673–682. doi:10.1165/rcmb.2007-0424OC
  • Goven D, Boutten A, Lecon-Malas V, et al. Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema. Thorax. 2008;63(10):916–924. doi:10.1136/thx.2007.091181
  • Rangasamy T, Cho CY, Thimmulappa RK, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest. 2004;114(9):1248–1259. doi:10.1172/JCI200421146
  • 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
  • Wen Q, Liu J, Kang R, Zhou B, Tang D. The release and activity of HMGB1 in ferroptosis. Biochem Biophys Res Commun. 2019;510(2):278–283. doi:10.1016/j.bbrc.2019.01.090
  • Yoshida M, Minagawa S, Araya J, et al. Involvement of cigarette smoke-induced epithelial cell ferroptosis in COPD pathogenesis. Nat Commun. 2019;10(1):3145. doi:10.1038/s41467-019-10991-7
  • Kerins MJ, Ooi A. The Roles of NRF2 in Modulating Cellular Iron Homeostasis. Antioxid Redox Signal. 2018;29(17):1756–1773. doi:10.1089/ars.2017.7176
  • Anandhan A, Dodson M, Schmidlin CJ, Liu P, Zhang DD. Breakdown of an ironclad defense system: the critical role of NRF2 in mediating ferroptosis. Cell Chem Biol. 2020;27(4):436–447. doi:10.1016/j.chembiol.2020.03.011
  • 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
  • Yang Y, Di T, Zhang Z, et al. Dynamic evolution of emphysema and airway remodeling in two mouse models of COPD. BMC Pulm Med. 2021;21(1):134. doi:10.1186/s12890-021-01456-z
  • He S, Li L, Sun S, Zeng Z, Lu J, Xie L. A novel murine chronic obstructive pulmonary disease model and the pathogenic role of MicroRNA-21. Front Physiol. 2018;9:503. doi:10.3389/fphys.2018.00503
  • Lun FM, Chiu RW, Sun K, et al. Noninvasive prenatal methylomic analysis by genomewide bisulfite sequencing of maternal plasma DNA. Clin Chem. 2013;59(11):1583–1594. doi:10.1373/clinchem.2013.212274
  • Liu Z, Lv X, Yang B, Qin Q, Song E, Song Y. Tetrachlorobenzoquinone exposure triggers ferroptosis contributing to its neurotoxicity. Chemosphere. 2021;264(Pt 1):128413. doi:10.1016/j.chemosphere.2020.128413
  • Barrera G. Oxidative stress and lipid peroxidation products in cancer progression and therapy. ISRN Oncol. 2012;2012:137289. doi:10.5402/2012/137289
  • Miotto G, Rossetto M, Di Paolo ML, et al. Insight into the mechanism of ferroptosis inhibition by ferrostatin-1. Redox Biol. 2020;28:101328. doi:10.1016/j.redox.2019.101328
  • Sun Y, Chen P, Zhai B, et al. The emerging role of ferroptosis in inflammation. Biomed Pharmacother. 2020;127:110108. doi:10.1016/j.biopha.2020.110108
  • Shin D, Kim EH, Lee J, Roh JL. Nrf2 inhibition reverses resistance to GPX4 inhibitor-induced ferroptosis in head and neck cancer. Free Radic Biol Med. 2018;129:454–462. doi:10.1016/j.freeradbiomed.2018.10.426
  • Yang WS, SriRamaratnam R, Welsch ME, et al. Regulation of ferroptotic cancer cell death by GPX4. Cell. 2014;156(1–2):317–331. doi:10.1016/j.cell.2013.12.010
  • Ma H, Wang X, Zhang W, et al. Melatonin Suppresses Ferroptosis Induced by High Glucose via Activation of the Nrf2/HO-1 Signaling Pathway in Type 2 Diabetic Osteoporosis. Oxid Med Cell Longev. 2020;2020:9067610. doi:10.1155/2020/9067610
  • Tang H, Chen D, Li C, et al. Dual GSH-exhausting sorafenib loaded manganese-silica nanodrugs for inducing the ferroptosis of hepatocellular carcinoma cells. Int J Pharm. 2019;572:118782. doi:10.1016/j.ijpharm.2019.118782
  • Forcina GC, Dixon SJ. GPX4 at the Crossroads of Lipid Homeostasis and Ferroptosis. Proteomics. 2019;19(18):e1800311. doi:10.1002/pmic.201800311
  • Kammerl I. Expression of concern: decline in NRF2-regulated antioxidants in COPD lungs due to loss of its positive regulator, and heightened endoplasmic reticulum stress in the lungs of patients with COPD. Am J Respir Crit Care Med. 2014;190(10):1200. doi:10.1164/rccm.190101200
  • Gou Z, Su X, Hu X, et al. Melatonin improves hypoxic-ischemic brain damage through the Akt/Nrf2/Gpx4 signaling pathway. Brain Res Bull. 2020;163:40–48. doi:10.1016/j.brainresbull.2020.07.011
  • Ma CS, Lv QM, Zhang KR, et al. NRF2-GPX4/SOD2 axis imparts resistance to EGFR-tyrosine kinase inhibitors in non-small-cell lung cancer cells. Acta Pharmacol Sin. 2020. doi:10.1038/s41401-020-0443-1
  • Liu Q, Wang K. The induction of ferroptosis by impairing STAT3/Nrf2/GPx4 signaling enhances the sensitivity of osteosarcoma cells to cisplatin. Cell Biol Int. 2019;43(11):1245–1256. doi:10.1002/cbin.11121
  • Lu SC. Regulation of glutathione synthesis. Mol Aspects Med. 2009;30(1–2):42–59. doi:10.1016/j.mam.2008.05.005
  • Salazar M, Rojo AI, Velasco D, de Sagarra RM, Cuadrado A. Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2. J Biol Chem. 2006;281(21):14841–14851. doi:10.1074/jbc.M513737200
  • Abdalkader M, Lampinen R, Kanninen KM, Malm TM, Liddell JR. Targeting Nrf2 to suppress ferroptosis and mitochondrial dysfunction in neurodegeneration. Front Neurosci. 2018;12:466. doi:10.3389/fnins.2018.00466
  • Momparler RL. Epigenetic therapy of cancer with 5-aza-2ʹ-deoxycytidine (decitabine). Semin Oncol. 2005;32(5):443–451. doi:10.1053/j.seminoncol.2005.07.008
  • Liu CM, Ma JQ, Xie WR, et al. Quercetin protects mouse liver against nickel-induced DNA methylation and inflammation associated with the Nrf2/HO-1 and p38/STAT1/NF-kappaB pathway. Food Chem Toxicol. 2015;82:19–26. doi:10.1016/j.fct.2015.05.001
  • Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol. 2010;28(10):1057–1068. doi:10.1038/nbt.1685
  • Roman T, Aumüller E, Berner C, Haslberger AG. Interaction of Hereditary and Epigenetic Mechanisms in the Regulation of Gene Expression. In: Epigenetics and Human Health. 2009:13–34. doi:10.1002/9783527628384.ch4
  • Guerrero-Bosagna C, Valladares L. Epigenetically induced changes, and transgenerational transmission of characters and epigenetic states. Endocrine Disruptors. 2007; 175.
  • Vucic EA, Chari R, Thu KL, et al. DNA methylation is globally disrupted and associated with expression changes in chronic obstructive pulmonary disease small airways. Am J Respir Cell Mol Biol. 2014;50(5):912–922. doi:10.1165/rcmb.2013-0304OC