Login Register Cart 0
Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Ferroptotic Cell Death: New Regulatory Mechanisms for Metabolic Diseases

Author(s): Yifei Le, Zhijie Zhang , Cui Wang and Dezhao Lu*

Volume 21, Issue 5, 2021

Published on: 31 July, 2020

Page: [785 - 800] Pages: 16

DOI: 10.2174/1871530320666200731175328

Price: $65

Abstract

Background: Cell death is a fundamental biological phenomenon that contributes to the pathogenesis of various diseases. Regulation of iron and iron metabolism has received considerable research interests especially concerning the progression of metabolic diseases.

Discussion: Emerging evidence shows that ferroptosis, a non-apoptotic programmed cell death induced by iron-dependent lipid peroxidation, contributes to the development of complex diseases such as non-alcoholic steatohepatitis, cardiomyopathy, renal ischemia-reperfusion, and neurodegenerative diseases. Therefore, inhibiting ferroptosis can improve the pathophysiology of associated metabolic diseases. This review describes the vital role of ferroptosis in mediating the development of certain metabolic diseases. Besides, the potential risk of iron and ferroptosis in atherosclerosis and cardiovascular diseases is also described. Iron overload and ferroptosis are potential secondary causes of death in metabolic diseases. Moreover, this review also provides potential novel approaches against ferroptosis based on recent research advances.

Conclusion: Several controversies exist concerning mechanisms underlying ferroptotic cell death in metabolic diseases, particularly in atherosclerosis. Since ferroptosis participates in the progression of metabolic diseases such as non-alcoholic steatohepatitis (NASH), there is a need to develop new drugs targeting ferroptosis to alleviate such diseases.

Keywords: Ferroptosis, iron, atherosclerosis, non-alcoholic steatohepatitis, cardiomyopathy, metabolism.

« Previous Next »
Graphical Abstract

[1]
Muckenthaler, M.U.; Rivella, S.; Hentze, M.W.; Galy, B. a red carpet for iron metabolism. Cell, 2017, 168(3), 344-361.
[http://dx.doi.org/10.1016/j.cell.2016.12.034] [PMID: 28129536]
[2]
Donovan, A.; Lima, C.A.; Pinkus, J.L.; Pinkus, G.S.; Zon, L.I.; Robine, S.; Andrews, N.C. The iron exporter ferroportin/Slc40a1 is essential for iron homeostasis. Cell Metab., 2005, 1(3), 191-200.
[http://dx.doi.org/10.1016/j.cmet.2005.01.003] [PMID: 16054062]
[3]
Hurrell, R.; Egli, I. Iron bioavailability and dietary reference values. Am. J. Clin. Nutr., 2010, 91(5), 1461S-1467S.
[http://dx.doi.org/10.3945/ajcn.2010.28674F] [PMID: 20200263]
[4]
Nemeth, E.; Tuttle, M.S.; Powelson, J.; Vaughn, M.B.; Donovan, A.; Ward, D.M.; Ganz, T.; Kaplan, J. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science, 2004, 306(5704), 2090-2093.
[http://dx.doi.org/10.1126/science.1104742] [PMID: 15514116]
[5]
Ganz, T.; Nemeth, E. Iron imports. IV. Hepcidin and regulation of body iron metabolism. Am. J. Physiol. Gastrointest. Liver Physiol., 2006, 290(2), G199-G203.
[http://dx.doi.org/10.1152/ajpgi.00412.2005] [PMID: 16407589]
[6]
Brissot, P.; Ropert, M.; Le Lan, C.; Loréal, O. Non-transferrin bound iron: a key role in iron overload and iron toxicity. Biochim. Biophys. Acta, 2012, 1820(3), 403-410.
[http://dx.doi.org/10.1016/j.bbagen.2011.07.014] [PMID: 21855608]
[7]
Auerbach, M.; Schrier, S. Treatment of iron deficiency is getting trendy. Lancet Haematol., 2017, 4(11), e500-e501.
[http://dx.doi.org/10.1016/S2352-3026(17)30194-1] [PMID: 29032958]
[8]
Li, H.; Ning, S.; Ghandi, M.; Kryukov, G.V.; Gopal, S.; Deik, A.; Souza, A.; Pierce, K.; Keskula, P.; Hernandez, D.; Ann, J.; Shkoza, D.; Apfel, V.; Zou, Y.; Vazquez, F.; Barretina, J.; Pagliarini, R.A.; Galli, G.G.; Root, D.E.; Hahn, W.C.; Tsherniak, A.; Giannakis, M.; Schreiber, S.L.; Clish, C.B.; Garraway, L.A.; Sellers, W.R. The landscape of cancer cell line metabolism. Nat. Med., 2019, 25(5), 850-860.
[http://dx.doi.org/10.1038/s41591-019-0404-8] [PMID: 31068703]
[9]
Patel, M.; Ramavataram, D.V.S.S. Non transferrin bound iron: nature, manifestations and analytical approaches for estimation. Indian J. Clin. Biochem., 2012, 27(4), 322-332.
[http://dx.doi.org/10.1007/s12291-012-0250-7] [PMID: 24082455]
[10]
Aljwaid, H.; White, D.L.; Collard, K.J.; Moody, A.J.; Pinkney, J.H. Non-transferrin-bound iron is associated with biomarkers of oxidative stress, inflammation and endothelial dysfunction in type 2 diabetes. J. Diabetes Complications, 2015, 29(7), 943-949.
[http://dx.doi.org/10.1016/j.jdiacomp.2015.05.017] [PMID: 26104728]
[11]
Baek, J.H.; Shin, H.K.H.; Gao, Y.; Buehler, P.W. Ferroportin inhibition attenuates plasma iron, oxidant stress, and renal injury following red blood cell transfusion in guinea pigs. Transfusion, 2020, 60(3), 513-523.
[http://dx.doi.org/10.1111/trf.15720] [PMID: 32064619]
[12]
Fang, X.; Wang, H.; Han, D.; Xie, E.; Yang, X.; Wei, J.; Gu, S.; Gao, F.; Zhu, N.; Yin, X.; Cheng, Q.; Zhang, P.; Dai, W.; Chen, J.; Yang, F.; Yang, H-T.; Linkermann, A.; Gu, W.; Min, J.; Wang, F. Ferroptosis as a target for protection against cardiomyopathy. Proc. Natl. Acad. Sci. USA, 2019, 116(7), 2672-2680.
[http://dx.doi.org/10.1073/pnas.1821022116] [PMID: 30692261]
[13]
Dixon, S.J.; Lemberg, K.M.; Lamprecht, M.R.; Skouta, R.; Zaitsev, E.M.; Gleason, C.E.; Patel, D.N.; Bauer, A.J.; Cantley, A.M.; Yang, W.S.; Morrison, B., III; Stockwell, B.R. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell, 2012, 149(5), 1060-1072.
[http://dx.doi.org/10.1016/j.cell.2012.03.042] [PMID: 22632970]
[14]
Ingold, I.; Berndt, C.; Schmitt, S.; Doll, S.; Poschmann, G.; Buday, K.; Roveri, A.; Peng, X.; Porto Freitas, F.; Seibt, T.; Mehr, L.; Aichler, M.; Walch, A.; Lamp, D.; Jastroch, M.; Miyamoto, S.; Wurst, W.; Ursini, F.; Arnér, E.S.J.; Fradejas-Villar, N.; Schweizer, U.; Zischka, H.; Friedmann Angeli, J.P.; Conrad, M. selenium utilization by gpx4 is required to prevent hydroperoxide-induced ferroptosis. Cell, 2018, 172(3), 409-422.e21.
[http://dx.doi.org/10.1016/j.cell.2017.11.048] [PMID: 29290465]
[15]
Lei, P.; Bai, T.; Sun, Y. Mechanisms of ferroptosis and relations with regulated cell death: a review. Front. Physiol., 2019, 10, 139.
[http://dx.doi.org/10.3389/fphys.2019.00139] [PMID: 30863316]
[16]
Shintoku, R.; Takigawa, Y.; Yamada, K.; Kubota, C.; Yoshimoto, Y.; Takeuchi, T.; Koshiishi, I.; Torii, S. Lipoxygenase-mediated generation of lipid peroxides enhances ferroptosis induced by erastin and RSL3. Cancer Sci., 2017, 108(11), 2187-2194.
[http://dx.doi.org/10.1111/cas.13380] [PMID: 28837253]
[17]
Tsurusaki, S.; Tsuchiya, Y.; Koumura, T.; Nakasone, M.; Sakamoto, T.; Matsuoka, M.; Imai, H.; Yuet-Yin Kok, C.; Okochi, H.; Nakano, H.; Miyajima, A.; Tanaka, M. Hepatic ferroptosis plays an important role as the trigger for initiating inflammation in nonalcoholic steatohepatitis. Cell Death Dis., 2019, 10(6), 449.
[http://dx.doi.org/10.1038/s41419-019-1678-y] [PMID: 31209199]
[18]
Zhou, Z.; Ye, T.J.; Bonavita, G.; Daniels, M.; Kainrad, N.; Jogasuria, A.; You, M. Adipose-specific Lipin-1 overexpression renders hepatic ferroptosis and exacerbates alcoholic steatohepatitis in mice. Hepatol. Commun., 2019, 3(5), 656-669.
[http://dx.doi.org/10.1002/hep4.1333] [PMID: 31061954]
[19]
Qi, J.; Kim, J-W.; Zhou, Z.; Lim, C-W.; Kim, B. Ferroptosis affects the progression of nonalcoholic steatohepatitis via the modulation of lipid peroxidation-mediated cell death in mice. Am. J. Pathol., 2020, 190(1), 68-81.
[http://dx.doi.org/10.1016/j.ajpath.2019.09.011] [PMID: 31610178]
[20]
Su, L.; Jiang, X.; Yang, C.; Zhang, J.; Chen, B.; Li, Y.; Yao, S.; Xie, Q.; Gomez, H.; Murugan, R.; Peng, Z. Pannexin 1 mediates ferroptosis that contributes to renal ischemia/reperfusion injury. J. Biol. Chem., 2019, 294(50), 19395-19404.
[http://dx.doi.org/10.1074/jbc.RA119.010949] [PMID: 31694915]
[21]
Schaftenaar, F.; Frodermann, V.; Kuiper, J.; Lutgens, E. Atherosclerosis: the interplay between lipids and immune cells. Curr. Opin. Lipidol., 2016, 27(3), 209-215.
[http://dx.doi.org/10.1097/MOL.0000000000000302] [PMID: 27031276]
[22]
Vinchi, F.; Porto, G.; Simmelbauer, A.; Altamura, S.; Passos, S.T.; Garbowski, M.; Silva, A.M.N.; Spaich, S.; Seide, S.E.; Sparla, R.; Hentze, M.W.; Muckenthaler, M.U. Atherosclerosis is aggravated by iron overload and ameliorated by dietary and pharmacological iron restriction. Eur. Heart J., 2019, 41(28), 2681-2695.
[http://dx.doi.org/10.1093/eurheartj/ehz112] [PMID: 30903157]
[23]
Marques, V.B.; Leal, M.A.S.; Mageski, J.G.A.; Fidelis, H.G.; Nogueira, B.V.; Vasquez, E.C.; Meyrelles, S.D.S.; Simões, M.R.; Dos Santos, L. Chronic iron overload intensifies atherosclerosis in apolipoprotein E deficient mice: role of oxidative stress and endothelial dysfunction. Life Sci., 2019, 233116702
[http://dx.doi.org/10.1016/j.lfs.2019.116702] [PMID: 31356905]
[24]
Zhang, Y.; Tan, H.; Daniels, J.D.; Zandkarimi, F.; Liu, H.; Brown, L.M.; Uchida, K.; O’Connor, O.A.; Stockwell, B.R. Imidazole ketone erastin induces ferroptosis and slows tumor growth in a mouse lymphoma model. Cell Chem. Biol., 2019, 26(5), 623-633.e9.
[http://dx.doi.org/10.1016/j.chembiol.2019.01.008] [PMID: 30799221]
[25]
Su, Y.; Zhao, B.; Zhou, L.; Zhang, Z.; Shen, Y.; Lv, H.; AlQudsy, L.H.H.; Shang, P. Ferroptosis, a novel pharmacological mechanism of anti-cancer drugs. Cancer Lett., 2020, 483, 127-136.
[http://dx.doi.org/10.1016/j.canlet.2020.02.015] [PMID: 32067993]
[26]
Liang, C.; Zhang, X.; Yang, M.; Dong, X. Recent progress in ferroptosis inducers for cancer therapy. Adv. Mater., 2019, 31(51)e1904197
[http://dx.doi.org/10.1002/adma.201904197] [PMID: 31595562]
[27]
Xie, Y.; Hou, W.; Song, X.; Yu, Y.; Huang, J.; Sun, X.; Kang, R.; Tang, D. Ferroptosis: process and function. Cell Death Differ., 2016, 23(3), 369-379.
[http://dx.doi.org/10.1038/cdd.2015.158] [PMID: 26794443]
[28]
Cai, J.; Zhang, X-J.; Ji, Y-X.; Zhang, P.; She, Z-G.; Li, H. Nonalcoholic fatty liver disease pandemic fuels the upsurge in cardiovascular diseases. Circ. Res., 2020, 126(5), 679-704.
[http://dx.doi.org/10.1161/CIRCRESAHA.119.316337] [PMID: 32105577]
[29]
Matteoni, C.A.; Younossi, Z.M.; Gramlich, T.; Boparai, N.; Liu, Y.C.; McCullough, A.J. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology, 1999, 116(6), 1413-1419.
[http://dx.doi.org/10.1016/S0016-5085(99)70506-8] [PMID: 10348825]
[30]
Yatsuji, S.; Hashimoto, E.; Tobari, M.; Taniai, M.; Tokushige, K.; Shiratori, K. Clinical features and outcomes of cirrhosis due to non-alcoholic steatohepatitis compared with cirrhosis caused by chronic hepatitis C. J. Gastroenterol. Hepatol., 2009, 24(2), 248-254.
[http://dx.doi.org/10.1111/j.1440-1746.2008.05640.x] [PMID: 19032450]
[31]
Fracanzani, A.L.; Valenti, L.; Bugianesi, E.; Vanni, E.; Grieco, A.; Miele, L.; Consonni, D.; Fatta, E.; Lombardi, R.; Marchesini, G.; Fargion, S. Risk of nonalcoholic steatohepatitis and fibrosis in patients with nonalcoholic fatty liver disease and low visceral adiposity. J. Hepatol., 2011, 54(6), 1244-1249.
[http://dx.doi.org/10.1016/j.jhep.2010.09.037] [PMID: 21145841]
[32]
Eguchi, A.; Wree, A.; Feldstein, A.E. Biomarkers of liver cell death. J. Hepatol., 2014, 60(5), 1063-1074.
[http://dx.doi.org/10.1016/j.jhep.2013.12.026] [PMID: 24412608]
[33]
Luedde, T.; Kaplowitz, N.; Schwabe, R.F. Cell death and cell death responses in liver disease: mechanisms and clinical relevance. Gastroenterology, 2014, 147(4), 765-783.e4.
[http://dx.doi.org/10.1053/j.gastro.2014.07.018] [PMID: 25046161]
[34]
Barreyro, F.J.; Holod, S.; Finocchietto, P.V.; Camino, A.M.; Aquino, J.B.; Avagnina, A.; Carreras, M.C.; Poderoso, J.J.; Gores, G.J. The pan-caspase inhibitor Emricasan (IDN-6556) decreases liver injury and fibrosis in a murine model of non-alcoholic steatohepatitis. Liver Int., 2015, 35(3), 953-966.
[http://dx.doi.org/10.1111/liv.12570] [PMID: 24750664]
[35]
Gautheron, J.; Vucur, M.; Reisinger, F.; Cardenas, D.V.; Roderburg, C.; Koppe, C.; Kreggenwinkel, K.; Schneider, A.T.; Bartneck, M.; Neumann, U.P.; Canbay, A.; Reeves, H.L.; Luedde, M.; Tacke, F.; Trautwein, C.; Heikenwalder, M.; Luedde, T. A positive feedback loop between RIP3 and JNK controls non-alcoholic steatohepatitis. EMBO Mol. Med., 2014, 6(8), 1062-1074.
[http://dx.doi.org/10.15252/emmm.201403856] [PMID: 24963148]
[36]
Köhn-Gaone, J.; Dwyer, B.J.; Grzelak, C.A.; Miller, G.; Shackel, N.A.; Ramm, G.A.; McCaughan, G.W.; Elsegood, C.L.; Olynyk, J.K.; Tirnitz-Parker, J.E.E. Divergent inflammatory, fibrogenic, and liver progenitor cell dynamics in two common mouse models of chronic liver injury. Am. J. Pathol., 2016, 186(7), 1762-1774.
[http://dx.doi.org/10.1016/j.ajpath.2016.03.005] [PMID: 27181403]
[37]
Machado, M.V.; Diehl, A.M. Pathogenesis of nonalcoholic steatohepatitis. Gastroenterology, 2016, 150(8), 1769-1777.
[http://dx.doi.org/10.1053/j.gastro.2016.02.066] [PMID: 26928243]
[38]
Casoinic, F.; Sampelean, D.; Buzoianu, A.D.; Hancu, N.; Baston, D. Serum levels of oxidative stress markers in patients with type 2 diabetes mellitus and non-alcoholic steatohepatitis. Rom. J. Intern. Med., 2016, 54(4), 228-236.
[http://dx.doi.org/10.1515/rjim-2016-0035] [PMID: 28002036]
[39]
Loguercio, C.; De Girolamo, V.; de Sio, I.; Tuccillo, C.; Ascione, A.; Baldi, F.; Budillon, G.; Cimino, L.; Di Carlo, A.; Di Marino, M.P.; Morisco, F.; Picciotto, F.; Terracciano, L.; Vecchione, R.; Verde, V.; Del Vecchio Blanco, C. Non-alcoholic fatty liver disease in an area of southern Italy: main clinical, histological, and pathophysiological aspects. J. Hepatol., 2001, 35(5), 568-574.
[http://dx.doi.org/10.1016/S0168-8278(01)00192-1] [PMID: 11690701]
[40]
Sanyal, A.J.; Chalasani, N.; Kowdley, K.V.; McCullough, A.; Diehl, A.M.; Bass, N.M.; Neuschwander-Tetri, B.A.; Lavine, J.E.; Tonascia, J.; Unalp, A.; Van Natta, M.; Clark, J.; Brunt, E.M.; Kleiner, D.E.; Hoofnagle, J.H.; Robuck, P.R. NASH CRN. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N. Engl. J. Med., 2010, 362(18), 1675-1685.
[http://dx.doi.org/10.1056/NEJMoa0907929] [PMID: 20427778]
[41]
Li, X.; Wang, T.X.; Huang, X.; Li, Y.; Sun, T.; Zang, S.; Guan, K.L.; Xiong, Y.; Liu, J.; Yuan, H.X. Targeting ferroptosis alleviates methionine-choline deficient (MCD)-diet induced NASH by suppressing liver lipotoxicity. Liver Int., 2020, 40(6), 1378-1394.
[http://dx.doi.org/10.1111/liv.14428] [PMID: 32145145]
[42]
Nelson, J.E.; Wilson, L.; Brunt, E.M.; Yeh, M.M.; Kleiner, D.E.; Unalp-Arida, A.; Kowdley, K.V. Nonalcoholic steatohepatitis clinical research network. Relationship between the pattern of hepatic iron deposition and histological severity in nonalcoholic fatty liver disease. Hepatology, 2011, 53(2), 448-457.
[http://dx.doi.org/10.1002/hep.24038] [PMID: 21274866]
[43]
Valenti, L.; Moscatiello, S.; Vanni, E.; Fracanzani, A.L.; Bugianesi, E.; Fargion, S.; Marchesini, G. Venesection for non-alcoholic fatty liver disease unresponsive to lifestyle counselling--a propensity score-adjusted observational study. QJM, 2011, 104(2), 141-149.
[http://dx.doi.org/10.1093/qjmed/hcq170] [PMID: 20851820]
[44]
Bonkovsky, H.L.; Jawaid, Q.; Tortorelli, K.; LeClair, P.; Cobb, J.; Lambrecht, R.W.; Banner, B.F. Non-alcoholic steatohepatitis and iron: increased prevalence of mutations of the HFE gene in non-alcoholic steatohepatitis. J. Hepatol., 1999, 31(3), 421-429.
[http://dx.doi.org/10.1016/S0168-8278(99)80032-4] [PMID: 10488699]
[45]
Zhang, Z.; Guo, M.; Li, Y.; Shen, M.; Kong, D.; Shao, J.; Ding, H.; Tan, S.; Chen, A.; Zhang, F.; Zheng, S. RNA-binding protein ZFP36/TTP protects against ferroptosis by regulating autophagy signaling pathway in hepatic stellate cells. Autophagy, 2020, 16(8), 1482-1505.
[http://dx.doi.org/10.1080/15548627.2019.1687985] [PMID: 31679460]
[46]
Zhang, Z.; Yao, Z.; Wang, L.; Ding, H.; Shao, J.; Chen, A.; Zhang, F.; Zheng, S. Activation of ferritinophagy is required for the RNA-binding protein ELAVL1/HuR to regulate ferroptosis in hepatic stellate cells. Autophagy, 2018, 14(12), 2083-2103.
[http://dx.doi.org/10.1080/15548627.2018.1503146] [PMID: 30081711]
[47]
Whelan, R.S.; Kaplinskiy, V.; Kitsis, R.N. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu. Rev. Physiol., 2010, 72(1), 19-44.
[http://dx.doi.org/10.1146/annurev.physiol.010908.163111] [PMID: 20148665]
[48]
Bai, Y-T.; Chang, R.; Wang, H.; Xiao, F-J.; Ge, R-L.; Wang, L-S. ENPP2 protects cardiomyocytes from erastin-induced ferroptosis. Biochem. Biophys. Res. Commun., 2018, 499(1), 44-51.
[http://dx.doi.org/10.1016/j.bbrc.2018.03.113] [PMID: 29551679]
[49]
Liu, B.; Zhao, C.; Li, H.; Chen, X.; Ding, Y.; Xu, S. Puerarin protects against heart failure induced by pressure overload through mitigation of ferroptosis. Biochem. Biophys. Res. Commun., 2018, 497(1), 233-240.
[http://dx.doi.org/10.1016/j.bbrc.2018.02.061] [PMID: 29427658]
[50]
Park, T-J.; Park, J.H.; Lee, G.S.; Lee, J-Y.; Shin, J.H.; Kim, M.W.; Kim, Y.S.; Kim, J-Y.; Oh, K-J.; Han, B-S.; Kim, W-K.; Ahn, Y.; Moon, J.H.; Song, J.; Bae, K-H.; Kim, D.H.; Lee, E-W.; Lee, S.C. Quantitative proteomic analyses reveal that GPX4 downregulation during myocardial infarction contributes to ferroptosis in cardiomyocytes. Cell Death Dis., 2019, 10(11), 835.
[http://dx.doi.org/10.1038/s41419-019-2061-8] [PMID: 31685805]
[51]
Wang, J.; Aung, L.H.H.; Prabhakar, B.S.; Li, P. The mitochondrial ubiquitin ligase plays an anti-apoptotic role in cardiomyocytes by regulating mitochondrial fission. J. Cell. Mol. Med., 2016, 20(12), 2278-2288.
[http://dx.doi.org/10.1111/jcmm.12914] [PMID: 27444773]
[52]
Zhu, P.; Hu, S.; Jin, Q.; Li, D.; Tian, F.; Toan, S.; Li, Y.; Zhou, H.; Chen, Y. Ripk3 promotes ER stress-induced necroptosis in cardiac IR injury: A mechanism involving calcium overload/XO/ROS/mPTP pathway. Redox Biol., 2018, 16, 157-168.
[http://dx.doi.org/10.1016/j.redox.2018.02.019] [PMID: 29502045]
[53]
Zhou, H.; Li, D.; Zhu, P.; Ma, Q.; Toan, S.; Wang, J.; Hu, S.; Chen, Y.; Zhang, Y. Inhibitory effect of melatonin on necroptosis via repressing the Ripk3-PGAM5-CypD-mPTP pathway attenuates cardiac microvascular ischemia-reperfusion injury. J. Pineal Res., 2018, 65(3)e12503
[http://dx.doi.org/10.1111/jpi.12503] [PMID: 29770487]
[54]
Benninger, R.K.P.; Remedi, M.S.; Head, W.S.; Ustione, A.; Piston, D.W.; Nichols, C.G. Defects in beta cell Ca2+ signalling, glucose metabolism and insulin secretion in a murine model of K(ATP) channel-induced neonatal diabetes mellitus. Diabetologia, 2011, 54(5), 1087-1097.
[http://dx.doi.org/10.1007/s00125-010-2039-7] [PMID: 21271337]
[55]
Paolillo, S.; Marsico, F.; Prastaro, M.; Renga, F.; Esposito, L.; De Martino, F.; Di Napoli, P.; Esposito, I.; Ambrosio, A.; Ianniruberto, M.; Mennella, R.; Paolillo, R.; Gargiulo, P. Diabetic cardiomyopathy. Heart Fail. Clin., 2019, 15(3), 341-347.
[http://dx.doi.org/10.1016/j.hfc.2019.02.003] [PMID: 31079692]
[56]
Cai, L.; Kang, Y.J. Cell death and diabetic cardiomyopathy. Cardiovasc. Toxicol., 2003, 3(3), 219-228.
[http://dx.doi.org/10.1385/CT:3:3:219] [PMID: 14555788]
[57]
Donahoe, S.M.; Stewart, G.C.; McCabe, C.H.; Mohanavelu, S.; Murphy, S.A.; Cannon, C.P.; Antman, E.M. Diabetes and mortality following acute coronary syndromes. JAMA, 2007, 298(7), 765-775.
[http://dx.doi.org/10.1001/jama.298.7.765] [PMID: 17699010]
[58]
Ndumele, C.E.; Matsushita, K.; Lazo, M.; Bello, N.; Blumenthal, R.S.; Gerstenblith, G.; Nambi, V.; Ballantyne, C.M.; Solomon, S.D.; Selvin, E.; Folsom, A.R.; Coresh, J. Obesity and subtypes of incident cardiovascular disease. J. Am. Heart Assoc., 2016, 5(8)e003921
[http://dx.doi.org/10.1161/JAHA.116.003921] [PMID: 27468925]
[59]
Li, W.; Li, W.; Leng, Y.; Xiong, Y.; Xia, Z. Ferroptosis is involved in diabetes myocardial ischemia/reperfusion injury through endoplasmic reticulum stress. DNA Cell Biol., 2020, 39(2), 210-225.
[http://dx.doi.org/10.1089/dna.2019.5097] [PMID: 31809190]
[60]
Maio, N.; Rouault, T.A. Iron-sulfur cluster biogenesis in mammalian cells: new insights into the molecular mechanisms of cluster delivery. Biochim. Biophys. Acta, 2015, 1853(6), 1493-1512.
[http://dx.doi.org/10.1016/j.bbamcr.2014.09.009] [PMID: 25245479]
[61]
Abrahão, A.; Pedroso, J.L.; Braga-Neto, P.; Bor-Seng-Shu, E.; de Carvalho Aguiar, P.; Barsottini, O.G.P. Milestones in Friedreich ataxia: more than a century and still learning. Neurogenetics, 2015, 16(3), 151-160.
[http://dx.doi.org/10.1007/s10048-015-0439-z] [PMID: 25662948]
[62]
Cnop, M.; Igoillo-Esteve, M.; Rai, M.; Begu, A.; Serroukh, Y.; Depondt, C.; Musuaya, A.E.; Marhfour, I.; Ladrière, L.; Moles Lopez, X.; Lefkaditis, D.; Moore, F.; Brion, J-P.; Cooper, J.M.; Schapira, A.H.V.; Clark, A.; Koeppen, A.H.; Marchetti, P.; Pandolfo, M.; Eizirik, D.L.; Féry, F. Central role and mechanisms of β-cell dysfunction and death in friedreich ataxia-associated diabetes. Ann. Neurol., 2012, 72(6), 971-982.
[http://dx.doi.org/10.1002/ana.23698] [PMID: 23280845]
[63]
Abeti, R.; Parkinson, M.H.; Hargreaves, I.P.; Angelova, P.R.; Sandi, C.; Pook, M.A.; Giunti, P.; Abramov, A.Y. ‘Mitochondrial energy imbalance and lipid peroxidation cause cell death in Friedreich’s ataxia’. Cell Death Dis., 2016, 7(5), e2237-e2237.
[http://dx.doi.org/10.1038/cddis.2016.111] [PMID: 27228352]
[64]
Kemp, K.; Mallam, E.; Hares, K.; Witherick, J.; Scolding, N.; Wilkins, A. Mesenchymal stem cells restore frataxin expression and increase hydrogen peroxide scavenging enzymes in Friedreich ataxia fibroblasts. PLoS One, 2011, 6(10)e26098
[http://dx.doi.org/10.1371/journal.pone.0026098] [PMID: 22016819]
[65]
Irazusta, V.; Obis, E.; Moreno-Cermeño, A.; Cabiscol, E.; Ros, J.; Tamarit, J. Yeast frataxin mutants display decreased superoxide dismutase activity crucial to promote protein oxidative damage. Free Radic. Biol. Med., 2010, 48(3), 411-420.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.11.010] [PMID: 19932164]
[66]
Anzovino, A.; Chiang, S.; Brown, B.E.; Hawkins, C.L.; Richardson, D.R.; Huang, M.L.H. Molecular alterations in a mouse cardiac model of friedreich ataxia: an impaired Nrf2 response mediated via upregulation of Keap1 and activation of the Gsk3β Axis. Am. J. Pathol., 2017, 187(12), 2858-2875.
[http://dx.doi.org/10.1016/j.ajpath.2017.08.021] [PMID: 28935570]
[67]
Sun, X.; Ou, Z.; Chen, R.; Niu, X.; Chen, D.; Kang, R.; Tang, D. Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology, 2016, 63(1), 173-184.
[http://dx.doi.org/10.1002/hep.28251] [PMID: 26403645]
[68]
Shin, D.; Kim, E.H.; Lee, J.; Roh, J-L. Nrf2 inhibition reverses resistance to GPX4 inhibitor-induced ferroptosis in head and neck cancer. Free Radic. Biol. Med., 2018, 129, 454-462.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.10.426] [PMID: 30339884]
[69]
Roh, J-L.; Kim, E.H.; Jang, H.; Shin, D. Nrf2 inhibition reverses the resistance of cisplatin-resistant head and neck cancer cells to artesunate-induced ferroptosis. Redox Biol., 2017, 11, 254-262.
[http://dx.doi.org/10.1016/j.redox.2016.12.010] [PMID: 28012440]
[70]
Turchi, R.; Tortolici, F.; Guidobaldi, G.; Iacovelli, F.; Falconi, M.; Rufini, S.; Faraonio, R.; Casagrande, V.; Federici, M.; De Angelis, L.; Carotti, S.; Francesconi, M.; Zingariello, M.; Morini, S.; Bernardini, R.; Mattei, M.; La Rosa, P.; Piemonte, F.; Lettieri-Barbato, D.; Aquilano, K. Frataxin deficiency induces lipid accumulation and affects thermogenesis in brown adipose tissue. Cell Death Dis., 2020, 11(1), 51.
[http://dx.doi.org/10.1038/s41419-020-2253-2] [PMID: 31974344]
[71]
Chondronikola, M.; Volpi, E.; Børsheim, E.; Porter, C.; Annamalai, P.; Enerbäck, S.; Lidell, M.E.; Saraf, M.K.; Labbe, S.M.; Hurren, N.M.; Yfanti, C.; Chao, T.; Andersen, C.R.; Cesani, F.; Hawkins, H.; Sidossis, L.S. Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes, 2014, 63(12), 4089-4099.
[http://dx.doi.org/10.2337/db14-0746] [PMID: 25056438]
[72]
Stanford, K.I.; Middelbeek, R.J.W.; Townsend, K.L.; An, D.; Nygaard, E.B.; Hitchcox, K.M.; Markan, K.R.; Nakano, K.; Hirshman, M.F.; Tseng, Y-H.; Goodyear, L.J. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J. Clin. Invest., 2013, 123(1), 215-223.
[http://dx.doi.org/10.1172/JCI62308] [PMID: 23221344]
[73]
Chondronikola, M.; Volpi, E.; Børsheim, E.; Porter, C.; Saraf, M.K.; Annamalai, P.; Yfanti, C.; Chao, T.; Wong, D.; Shinoda, K.; Labbė, S.M.; Hurren, N.M.; Cesani, F.; Kajimura, S.; Sidossis, L.S. Brown adipose tissue activation is linked to distinct systemic effects on lipid metabolism in humans. Cell Metab., 2016, 23(6), 1200-1206.
[http://dx.doi.org/10.1016/j.cmet.2016.04.029] [PMID: 27238638]
[74]
Hankir, M.K.; Klingenspor, M. Brown adipocyte glucose metabolism: a heated subject. EMBO Rep., 2018, 19(9)e46404
[http://dx.doi.org/10.15252/embr.201846404] [PMID: 30135070]
[75]
Bartelt, A.; Bruns, O.T.; Reimer, R.; Hohenberg, H.; Ittrich, H.; Peldschus, K.; Kaul, M.G.; Tromsdorf, U.I.; Weller, H.; Waurisch, C.; Eychmüller, A.; Gordts, P.L.S.M.; Rinninger, F.; Bruegelmann, K.; Freund, B.; Nielsen, P.; Merkel, M.; Heeren, J. Brown adipose tissue activity controls triglyceride clearance. Nat. Med., 2011, 17(2), 200-205.
[http://dx.doi.org/10.1038/nm.2297] [PMID: 21258337]
[76]
Du, J.; Zhou, Y.; Li, Y.; Xia, J.; Chen, Y.; Chen, S.; Wang, X.; Sun, W.; Wang, T.; Ren, X.; Wang, X.; An, Y.; Lu, K.; Hu, W.; Huang, S.; Li, J.; Tong, X.; Wang, Y. Identification of Frataxin as a regulator of ferroptosis. Redox Biol., 2020.32101483
[http://dx.doi.org/10.1016/j.redox.2020.101483] [PMID: 32169822]
[77]
Li, Y.; Yu, P.; Chang, S-Y.; Wu, Q.; Yu, P.; Xie, C.; Wu, W.; Zhao, B.; Gao, G.; Chang, Y-Z. Hypobaric hypoxia regulates brain iron homeostasis in rats. J. Cell. Biochem., 2017, 118(6), 1596-1605.
[http://dx.doi.org/10.1002/jcb.25822] [PMID: 27925282]
[78]
Altamura, S.; Muckenthaler, M.U. Iron toxicity in diseases of aging: Alzheimer’s disease, Parkinson’s disease and atherosclerosis. J. Alzheimers Dis., 2009, 16(4), 879-895.
[http://dx.doi.org/10.3233/JAD-2009-1010] [PMID: 19387120]
[79]
Alim, I.; Caulfield, J.T.; Chen, Y.; Swarup, V.; Geschwind, D.H.; Ivanova, E.; Seravalli, J.; Ai, Y.; Sansing, L.H.; Ste Marie, E.J.; Hondal, R.J.; Mukherjee, S.; Cave, J.W.; Sagdullaev, B.T.; Karuppagounder, S.S.; Ratan, R.R. Selenium drives a transcriptional adaptive program to block ferroptosis and treat stroke. Cell, 2019, 177(5), 1262-1279.e25.
[http://dx.doi.org/10.1016/j.cell.2019.03.032] [PMID: 31056284]
[80]
Kenny, E.M.; Fidan, E.; Yang, Q.; Anthonymuthu, T.S.; New, L.A.; Meyer, E.A.; Wang, H.; Kochanek, P.M.; Dixon, C.E.; Kagan, V.E.; Bayir, H. Ferroptosis contributes to neuronal death and functional outcome after traumatic brain injury. Crit. Care Med., 2019, 47(3), 410-418.
[http://dx.doi.org/10.1097/CCM.0000000000003555] [PMID: 30531185]
[81]
Bowler, J.V. Modern concept of vascular cognitive impairment. Br. Med. Bull., 2007, 83(1), 291-305.
[http://dx.doi.org/10.1093/bmb/ldm021] [PMID: 17675645]
[82]
Venkat, P.; Chopp, M.; Zacharek, A.; Cui, C.; Landschoot-Ward, J.; Qian, Y.; Chen, Z.; Chen, J. Sildenafil treatment of vascular dementia in aged rats. Neurochem. Int., 2019, 127, 103-112.
[http://dx.doi.org/10.1016/j.neuint.2018.12.015] [PMID: 30592970]
[83]
Iadecola, C. The pathobiology of vascular dementia. Neuron, 2013, 80(4), 844-866.
[http://dx.doi.org/10.1016/j.neuron.2013.10.008] [PMID: 24267647]
[84]
Weiland, A.; Wang, Y.; Wu, W.; Lan, X.; Han, X.; Li, Q.; Wang, J. Ferroptosis and its role in diverse brain diseases. Mol. Neurobiol., 2019, 56(7), 4880-4893.
[http://dx.doi.org/10.1007/s12035-018-1403-3] [PMID: 30406908]
[85]
Yan, N.; Zhang, J-J. The emerging roles of ferroptosis in vascular cognitive impairment. Front. Neurosci., 2019, 13, 811.
[http://dx.doi.org/10.3389/fnins.2019.00811] [PMID: 31447633]
[86]
Li, X.; Duan, L.; Yuan, S.; Zhuang, X.; Qiao, T.; He, J. Ferroptosis inhibitor alleviates Radiation-induced lung fibrosis (RILF) via down-regulation of TGF-β1. J. Inflamm. (Lond.), 2019, 16(1), 11.
[http://dx.doi.org/10.1186/s12950-019-0216-0] [PMID: 31160885]
[87]
Yoshida, M.; Minagawa, S.; Araya, J.; Sakamoto, T.; Hara, H.; Tsubouchi, K.; Hosaka, Y.; Ichikawa, A.; Saito, N.; Kadota, T.; Sato, N.; Kurita, Y.; Kobayashi, K.; Ito, S.; Utsumi, H.; Wakui, H.; Numata, T.; Kaneko, Y.; Mori, S.; Asano, H.; Yamashita, M.; Odaka, M.; Morikawa, T.; Nakayama, K.; Iwamoto, T.; Imai, H.; Kuwano, K. Involvement of cigarette smoke-induced epithelial cell ferroptosis in COPD pathogenesis. Nat. Commun., 2019, 10(1), 3145.
[http://dx.doi.org/10.1038/s41467-019-10991-7] [PMID: 31316058]
[88]
Hu, Z.; Zhang, H.; Yang, S.K.; Wu, X.; He, D.; Cao, K.; Zhang, W. Emerging role of ferroptosis in acute kidney injury. Oxid. Med. Cell. Longev., 2019, 20198010614
[http://dx.doi.org/10.1155/2019/8010614] [PMID: 31781351]
[89]
Huang, L.L.; Liao, X.H.; Sun, H.; Jiang, X.; Liu, Q.; Zhang, L. Augmenter of liver regeneration protects the kidney from ischaemia-reperfusion injury in ferroptosis. J. Cell. Mol. Med., 2019, 23(6), 4153-4164.
[http://dx.doi.org/10.1111/jcmm.14302] [PMID: 30993878]
[90]
Turpin-Nolan, S.M.; Brüning, J.C. The role of ceramides in metabolic disorders: when size and localization matters. Nat. Rev. Endocrinol., 2020, 16(4), 224-233.
[http://dx.doi.org/10.1038/s41574-020-0320-5] [PMID: 32060415]
[91]
Mechanick, J.I.; Farkouh, M.E.; Newman, J.D.; Garvey, W.T. Cardiometabolic-based chronic disease, addressing knowledge and clinical practice gaps: JACC state-of-the-art review. J. Am. Coll. Cardiol., 2020, 75(5), 539-555.
[http://dx.doi.org/10.1016/j.jacc.2019.11.046] [PMID: 32029137]
[92]
Benjamin, E.J.; Muntner, P.; Alonso, A.; Bittencourt, M.S.; Callaway, C.W.; Carson, A.P.; Chamberlain, A.M.; Chang, A.R.; Cheng, S.; Das, S.R.; Delling, F.N.; Djousse, L.; Elkind, M.S.V.; Ferguson, J.F.; Fornage, M.; Jordan, L.C.; Khan, S.S.; Kissela, B.M.; Knutson, K.L.; Kwan, T.W.; Lackland, D.T.; Lewis, T.T.; Lichtman, J.H.; Longenecker, C.T.; Loop, M.S.; Lutsey, P.L.; Martin, S.S.; Matsushita, K.; Moran, A.E.; Mussolino, M.E.; O’Flaherty, M.; Pandey, A.; Perak, A.M.; Rosamond, W.D.; Roth, G.A.; Sampson, U.K.A.; Satou, G.M.; Schroeder, E.B.; Shah, S.H.; Spartano, N.L.; Stokes, A.; Tirschwell, D.L.; Tsao, C.W.; Turakhia, M.P.; VanWagner, L.B.; Wilkins, J.T.; Wong, S.S.; Virani, S.S.; O’Flaherty, M.; Pandey, A.; Perak, A.M.; Rosamond, W.D.; Roth, G.A.; Sampson, U.K.A.; Satou, G.M.; Schroeder, E.B.; Shah, S.H.; Spartano, N.L.; Stokes, A.; Tirschwell, D.L.; Tsao, C.W.; Turakhia, M.P.; VanWagner, L.B.; Wilkins, J.T.; Wong, S.S.; Virani, S.S. American heart association council on epidemiology and prevention statistics committee and stroke statistics subcommittee. Heart disease and stroke statistics-2019 update: a report from the american heart association. Circulation, 2019, 139(10), e56-e528.
[http://dx.doi.org/10.1161/CIR.0000000000000659] [PMID: 30700139]
[93]
Libby, P.; Theroux, P. Pathophysiology of coronary artery disease. Circulation, 2005, 111(25), 3481-3488.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.105.537878] [PMID: 15983262]
[94]
Sullivan, J.L. Iron and the sex difference in heart disease risk. Lancet, 1981, 1(8233), 1293-1294.
[http://dx.doi.org/10.1016/S0140-6736(81)92463-6] [PMID: 6112609]
[95]
Vinchi, F.; Muckenthaler, M.U.; Da Silva, M.C.; Balla, G.; Balla, J.; Jeney, V. Atherogenesis and iron: from epidemiology to cellular level. Front. Pharmacol., 2014, 5, 94.
[http://dx.doi.org/10.3389/fphar.2014.00094] [PMID: 24847266]
[96]
Xiao, L.; Luo, G.; Guo, X.; Jiang, C.; Zeng, H.; Zhou, F.; Li, Y.; Yu, J.; Yao, P. Macrophage iron retention aggravates atherosclerosis: Evidence for the role of autocrine formation of hepcidin in plaque macrophages. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2020, 1865(2)158531
[http://dx.doi.org/10.1016/j.bbalip.2019.158531] [PMID: 31666189]
[97]
Cancel, L.M.; Ebong, E.E.; Mensah, S.; Hirschberg, C.; Tarbell, J.M. Endothelial glycocalyx, apoptosis and inflammation in an atherosclerotic mouse model. Atherosclerosis, 2016, 252, 136-146.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.07.930] [PMID: 27529818]
[98]
Wang, Z.; Yang, B.; Chen, X.; Zhou, Q.; Li, H.; Chen, S.; Yin, D.; He, H.; He, M. Nobiletin Regulates ROS/ADMA/DDAHII/ENOS/NO Pathway and Alleviates Vascular Endothelium Injury by Iron Overload; Biol; Trace Elem, 2020.
[http://dx.doi.org/10.1007/s12011-020-02038-6]
[99]
Bouhlel, M.A.; Derudas, B.; Rigamonti, E.; Dièvart, R.; Brozek, J.; Haulon, S.; Zawadzki, C.; Jude, B.; Torpier, G.; Marx, N.; Staels, B.; Chinetti-Gbaguidi, G. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab., 2007, 6(2), 137-143.
[http://dx.doi.org/10.1016/j.cmet.2007.06.010] [PMID: 17681149]
[100]
Wunderer, F.; Traeger, L.; Sigurslid, H.H.; Meybohm, P.; Bloch, D.B.; Malhotra, R. The role of hepcidin and iron homeostasis in atherosclerosis. Pharmacol. Res., 2020, •••153104664
[http://dx.doi.org/10.1016/j.phrs.2020.104664] [PMID: 31991168]
[101]
Cornelissen, A.; Guo, L.; Sakamoto, A.; Virmani, R.; Finn, A.V. New insights into the role of iron in inflammation and atherosclerosis. EBioMedicine, 2019, 47, 598-606.
[http://dx.doi.org/10.1016/j.ebiom.2019.08.014] [PMID: 31416722]
[102]
Balla, G.; Jacob, H.S.; Eaton, J.W.; Belcher, J.D.; Vercellotti, G.M. Hemin: a possible physiological mediator of low density lipoprotein oxidation and endothelial injury. Arterioscler. Thromb., 1991, 11(6), 1700-1711.
[http://dx.doi.org/10.1161/01.ATV.11.6.1700] [PMID: 1931871]
[103]
Hu, X.; Cai, X.; Ma, R.; Fu, W.; Zhang, C.; Du, X. Iron-load exacerbates the severity of atherosclerosis via inducing inflammation and enhancing the glycolysis in macrophages. J. Cell. Physiol., 2019, 234(10), 18792-18800.
[http://dx.doi.org/10.1002/jcp.28518] [PMID: 30927265]
[104]
Handa, P.; Thomas, S.; Morgan-Stevenson, V.; Maliken, B.D.; Gochanour, E.; Boukhar, S.; Yeh, M.M.; Kowdley, K.V. Iron alters macrophage polarization status and leads to steatohepatitis and fibrogenesis. J. Leukoc. Biol., 2019, 105(5), 1015-1026.
[http://dx.doi.org/10.1002/JLB.3A0318-108R] [PMID: 30835899]
[105]
Ley, K.; Miller, Y.I.; Hedrick, C.C. Monocyte and macrophage dynamics during atherogenesis. Arterioscler. Thromb. Vasc. Biol., 2011, 31(7), 1506-1516.
[http://dx.doi.org/10.1161/ATVBAHA.110.221127] [PMID: 21677293]
[106]
Boytard, L.; Spear, R.; Chinetti-Gbaguidi, G.; Acosta-Martin, A.E.; Vanhoutte, J.; Lamblin, N.; Staels, B.; Amouyel, P.; Haulon, S.; Pinet, F. Role of proinflammatory CD68(+) mannose receptor(-) macrophages in peroxiredoxin-1 expression and in abdominal aortic aneurysms in humans. Arterioscler. Thromb. Vasc. Biol., 2013, 33(2), 431-438.
[http://dx.doi.org/10.1161/ATVBAHA.112.300663] [PMID: 23241402]
[107]
Recalcati, S.; Gammella, E.; Buratti, P.; Doni, A.; Anselmo, A.; Locati, M.; Cairo, G. Macrophage ferroportin is essential for stromal cell proliferation in wound healing. Haematologica, 2019, 104(1), 47-58.
[http://dx.doi.org/10.3324/haematol.2018.197517] [PMID: 30115660]
[108]
Wang, L.; Johnson, E.E.; Shi, H.N.; Walker, W.A.; Wessling-Resnick, M.; Cherayil, B.J. Attenuated inflammatory responses in hemochromatosis reveal a role for iron in the regulation of macrophage cytokine translation. J. Immunol., 2008, 181(4), 2723-2731.
[http://dx.doi.org/10.4049/jimmunol.181.4.2723] [PMID: 18684963]
[109]
She, H.; Xiong, S.; Lin, M.; Zandi, E.; Giulivi, C.; Tsukamoto, H. Iron activates NF-kappaB in Kupffer cells. Am. J. Physiol. Gastrointest. Liver Physiol., 2002, 283(3), G719-G726.
[http://dx.doi.org/10.1152/ajpgi.00108.2002] [PMID: 12181188]
[110]
Finn, A.V.; Nakano, M.; Polavarapu, R.; Karmali, V.; Saeed, O.; Zhao, X.; Yazdani, S.; Otsuka, F.; Davis, T.; Habib, A.; Narula, J.; Kolodgie, F.D.; Virmani, R. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J. Am. Coll. Cardiol., 2012, 59(2), 166-177.
[http://dx.doi.org/10.1016/j.jacc.2011.10.852] [PMID: 22154776]
[111]
Nielsen, M.J.; Møller, H.J.; Moestrup, S.K. Hemoglobin and heme scavenger receptors. Antioxid. Redox Signal., 2010, 12(2), 261-273.
[http://dx.doi.org/10.1089/ars.2009.2792] [PMID: 19659436]
[112]
Kawada, S.; Nagasawa, Y.; Kawabe, M.; Ohyama, H.; Kida, A.; Kato-Kogoe, N.; Nanami, M.; Hasuike, Y.; Kuragano, T.; Kishimoto, H.; Nakasho, K.; Nakanishi, T. Iron-induced calcification in human aortic vascular smooth muscle cells through interleukin-24 (IL-24), with/without TNF-alpha. Sci. Rep., 2018, 8(1), 658.
[http://dx.doi.org/10.1038/s41598-017-19092-1] [PMID: 29330517]
[113]
Martinet, W.; Coornaert, I.; Puylaert, P.; De Meyer, G.R.Y. Macrophage death as a pharmacological target in atherosclerosis. Front. Pharmacol., 2019, 10, 306.
[http://dx.doi.org/10.3389/fphar.2019.00306] [PMID: 31019462]
[114]
Kapralov, A.A.; Yang, Q.; Dar, H.H.; Tyurina, Y.Y.; Anthonymuthu, T.S.; Kim, R.; St Croix, C.M.; Mikulska-Ruminska, K.; Liu, B.; Shrivastava, I.H.; Tyurin, V.A.; Ting, H-C.; Wu, Y.L.; Gao, Y.; Shurin, G.V.; Artyukhova, M.A.; Ponomareva, L.A.; Timashev, P.S.; Domingues, R.M.; Stoyanovsky, D.A.; Greenberger, J.S.; Mallampalli, R.K.; Bahar, I.; Gabrilovich, D.I.; Bayır, H.; Kagan, V.E. Redox lipid reprogramming commands susceptibility of macrophages and microglia to ferroptotic death. Nat. Chem. Biol., 2020, 16(3), 278-290.
[http://dx.doi.org/10.1038/s41589-019-0462-8] [PMID: 32080625]
[115]
Martin-Sanchez, D.; Ruiz-Andres, O.; Poveda, J.; Carrasco, S.; Cannata-Ortiz, P.; Sanchez-Niño, M.D.; Ruiz Ortega, M.; Egido, J.; Linkermann, A.; Ortiz, A.; Sanz, A.B. Ferroptosis, but not necroptosis, is important in nephrotoxic folic acid-induced Aki. J. Am. Soc. Nephrol., 2017, 28(1), 218-229.
[http://dx.doi.org/10.1681/ASN.2015121376] [PMID: 27352622]
[116]
Prasai, P.K.; Shrestha, B.; Orr, A.W.; Pattillo, C.B. Decreases in GSH:GSSG activate vascular endothelial growth factor receptor 2 (VEGFR2) in human aortic endothelial cells. Redox Biol., 2018, 19, 22-27.
[http://dx.doi.org/10.1016/j.redox.2018.07.015] [PMID: 30096614]
[117]
Ursini, F.; Maiorino, M. Lipid peroxidation and ferroptosis: the role of GSH and GPx4. Free Radic. Biol. Med., 2020, 152, 175-185.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.02.027] [PMID: 32165281]
[118]
Valerio, V.; Myasoedova, V.A.; Moschetta, D.; Porro, B.; Perrucci, G.L.; Cavalca, V.; Cavallotti, L.; Songia, P.; Poggio, P. Impact of oxidative stress and protein S-Glutathionylation in aortic valve sclerosis patients with overt atherosclerosis. J. Clin. Med., 2019, 8(4), 552.
[http://dx.doi.org/10.3390/jcm8040552] [PMID: 31022838]
[119]
Guo, Z.; Ran, Q.; Roberts, L.J., II; Zhou, L.; Richardson, A.; Sharan, C.; Wu, D.; Yang, H. Suppression of atherogenesis by overexpression of glutathione peroxidase-4 in apolipoprotein E-deficient mice. Free Radic. Biol. Med., 2008, 44(3), 343-352.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.09.009] [PMID: 18215741]
[120]
Banning, A.; Schnurr, K.; Böl, G.F.; Kupper, D.; Müller-Schmehl, K.; Viita, H.; Ylä-Herttuala, S.; Brigelius-Flohé, R. Inhibition of basal and interleukin-1-induced VCAM-1 expression by phospholipid hydroperoxide glutathione peroxidase and 15-lipoxygenase in rabbit aortic smooth muscle cells. Free Radic. Biol. Med., 2004, 36(2), 135-144.
[http://dx.doi.org/10.1016/j.freeradbiomed.2003.10.027] [PMID: 14744625]
[121]
Wang, H.; Liu, C.; Zhao, Y.; Gao, G. Mitochondria regulation in ferroptosis. Eur. J. Cell Biol., 2020, 99(1)151058
[http://dx.doi.org/10.1016/j.ejcb.2019.151058] [PMID: 31810634]
[122]
Bock, F.J.; Tait, S.W.G. Mitochondria as multifaceted regulators of cell death. Nat. Rev. Mol. Cell Biol., 2020, 21(2), 85-100.
[http://dx.doi.org/10.1038/s41580-019-0173-8] [PMID: 31636403]
[123]
Leermakers, P.A.; Remels, A.H.V.; Zonneveld, M.I.; Rouschop, K.M.A.; Schols, A.M.W.J.; Gosker, H.R. Iron deficiency-induced loss of skeletal muscle mitochondrial proteins and respiratory capacity; the role of mitophagy and secretion of mitochondria-containing vesicles. FASEB J., 2020, 34(5), 6703-6717.
[http://dx.doi.org/10.1096/fj.201901815R] [PMID: 32202346]
[124]
Yang, W.S.; Stockwell, B.R. Ferroptosis: death by lipid peroxidation. Trends Cell Biol., 2016, 26(3), 165-176.
[http://dx.doi.org/10.1016/j.tcb.2015.10.014] [PMID: 26653790]
[125]
Kagan, V.E.; Mao, G.; Qu, F.; Angeli, J.P.F.; Doll, S.; Croix, C.S.; Dar, H.H.; Liu, B.; Tyurin, V.A.; Ritov, V.B.; Kapralov, A.A.; Amoscato, A.A.; Jiang, J.; Anthonymuthu, T.; Mohammadyani, D.; Yang, Q.; Proneth, B.; Klein-Seetharaman, J.; Watkins, S.; Bahar, I.; Greenberger, J.; Mallampalli, R.K.; Stockwell, B.R.; Tyurina, Y.Y.; Conrad, M.; Bayır, H. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat. Chem. Biol., 2017, 13(1), 81-90.
[http://dx.doi.org/10.1038/nchembio.2238] [PMID: 27842066]
[126]
Hofmans, S.; Vanden Berghe, T.; Devisscher, L.; Hassannia, B.; Lyssens, S.; Joossens, J.; Van Der Veken, P.; Vandenabeele, P.; Augustyns, K. Novel ferroptosis inhibitors with improved potency and ADME properties. J. Med. Chem., 2016, 59(5), 2041-2053.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01641] [PMID: 26696014]
[127]
Reppert, S.M.; Weaver, D.R. Coordination of circadian timing in mammals. Nature, 2002, 418(6901), 935-941.
[http://dx.doi.org/10.1038/nature00965] [PMID: 12198538]
[128]
Yang, M.; Chen, P.; Liu, J.; Zhu, S.; Kroemer, G.; Klionsky, D.J.; Lotze, M.T.; Zeh, H.J.; Kang, R.; Tang, D. Clockophagy is a novel selective autophagy process favoring ferroptosis. Sci. Adv., 2019, 5(7)eaaw2238
[http://dx.doi.org/10.1126/sciadv.aaw2238] [PMID: 31355331]
[129]
Doll, S.; Freitas, F.P.; Shah, R.; Aldrovandi, M.; da Silva, M.C.; Ingold, I.; Goya Grocin, A.; Xavier da Silva, T.N.; Panzilius, E.; Scheel, C.H.; Mourão, A.; Buday, K.; Sato, M.; Wanninger, J.; Vignane, T.; Mohana, V.; Rehberg, M.; Flatley, A.; Schepers, A.; Kurz, A.; White, D.; Sauer, M.; Sattler, M.; Tate, E.W.; Schmitz, W.; Schulze, A.; O’Donnell, V.; Proneth, B.; Popowicz, G.M.; Pratt, D.A.; Angeli, J.P.F.; Conrad, M. FSP1 is a glutathione-independent ferroptosis suppressor. Nature, 2019, 575(7784), 693-698.
[http://dx.doi.org/10.1038/s41586-019-1707-0] [PMID: 31634899]
[130]
Bersuker, K.; Hendricks, J.M.; Li, Z.; Magtanong, L.; Ford, B.; Tang, P.H.; Roberts, M.A.; Tong, B.; Maimone, T.J.; Zoncu, R.; Bassik, M.C.; Nomura, D.K.; Dixon, S.J.; Olzmann, J.A. The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis. Nature, 2019, 575(7784), 688-692.
[http://dx.doi.org/10.1038/s41586-019-1705-2] [PMID: 31634900]
[131]
Murphy, M.E. Ironing out how p53 regulates ferroptosis. Proc. Natl. Acad. Sci. USA, 2016, 113(44), 12350-12352.
[http://dx.doi.org/10.1073/pnas.1615159113] [PMID: 27791175]
[132]
Karni-Schmidt, O.; Lokshin, M.; Prives, C. The roles of MDM2 and MDMX in cancer. Annu. Rev. Pathol., 2016, 11(1), 617-644.
[http://dx.doi.org/10.1146/annurev-pathol-012414-040349] [PMID: 27022975]
[133]
Venkatesh, D.; O’Brien, N.A.; Zandkarimi, F.; Tong, D.R.; Stokes, M.E.; Dunn, D.E.; Kengmana, E.S.; Aron, A.T.; Klein, A.M.; Csuka, J.M.; Moon, S-H.; Conrad, M.; Chang, C.J.; Lo, D.C.; D’Alessandro, A.; Prives, C.; Stockwell, B.R. MDM2 and MDMX promote ferroptosis by PPARα-mediated lipid remodeling. Genes Dev., 2020, 34(7-8), 526-543.
[http://dx.doi.org/10.1101/gad.334219.119] [PMID: 32079652]
[134]
Conrad, M.; Pratt, D.A. The chemical basis of ferroptosis. Nat. Chem. Biol., 2019, 15(12), 1137-1147.
[http://dx.doi.org/10.1038/s41589-019-0408-1] [PMID: 31740834]
[135]
Wenzel, S.E.; Tyurina, Y.Y.; Zhao, J.; St Croix, C.M.; Dar, H.H.; Mao, G.; Tyurin, V.A.; Anthonymuthu, T.S.; Kapralov, A.A.; Amoscato, A.A.; Mikulska-Ruminska, K.; Shrivastava, I.H.; Kenny, E.M.; Yang, Q.; Rosenbaum, J.C.; Sparvero, L.J.; Emlet, D.R.; Wen, X.; Minami, Y.; Qu, F.; Watkins, S.C.; Holman, T.R.; VanDemark, A.P.; Kellum, J.A.; Bahar, I.; Bayır, H.; Kagan, V.E. PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell, 2017, 171(3), 628-641.e26.
[http://dx.doi.org/10.1016/j.cell.2017.09.044] [PMID: 29053969]
[136]
Shah, R.; Shchepinov, M.S.; Pratt, D.A. Resolving the role of lipoxygenases in the initiation and execution of ferroptosis. ACS Cent. Sci., 2018, 4(3), 387-396.
[http://dx.doi.org/10.1021/acscentsci.7b00589] [PMID: 29632885]
[137]
Zou, Y.; Li, H.; Graham, E.T.; Deik, A.A.; Eaton, J.K.; Wang, W.; Sandoval-Gomez, G.; Clish, C.B.; Doench, J.G.; Schreiber, S.L. Cytochrome P450 oxidoreductase contributes to phospholipid peroxidation in ferroptosis. Nat. Chem. Biol., 2020, 16(3), 302-309.
[http://dx.doi.org/10.1038/s41589-020-0472-6] [PMID: 32080622]
[138]
Bast, A.; Brenninkmeijer, J.W.; Savenije-Chapel, E.M.; Noordhoek, J. Cytochrome P450 oxidase activity and its role in NADPH dependent lipid peroxidation. FEBS Lett., 1983, 151(2), 185-188.
[http://dx.doi.org/10.1016/0014-5793(83)80065-9] [PMID: 6832351]
[139]
Morehouse, L.A.; Thomas, C.E.; Aust, S.D. Superoxide generation by NADPH-cytochrome P-450 reductase: the effect of iron chelators and the role of superoxide in microsomal lipid peroxidation. Arch. Biochem. Biophys., 1984, 232(1), 366-377.
[http://dx.doi.org/10.1016/0003-9861(84)90552-6] [PMID: 6331320]
[140]
Hardie, D.G.; Ross, F.A.; Hawley, S.A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol., 2012, 13(4), 251-262.
[http://dx.doi.org/10.1038/nrm3311] [PMID: 22436748]
[141]
Hardie, D.G.; Schaffer, B.E.; Brunet, A. AMPK: an energy-sensing pathway with multiple inputs and outputs. Trends Cell Biol., 2016, 26(3), 190-201.
[http://dx.doi.org/10.1016/j.tcb.2015.10.013] [PMID: 26616193]
[142]
Lee, H.; Zandkarimi, F.; Zhang, Y.; Meena, J.K.; Kim, J.; Zhuang, L.; Tyagi, S.; Ma, L.; Westbrook, T.F.; Steinberg, G.R.; Nakada, D.; Stockwell, B.R.; Gan, B. Energy-stress-mediated AMPK activation inhibits ferroptosis. Nat. Cell Biol., 2020, 22(2), 225-234.
[http://dx.doi.org/10.1038/s41556-020-0461-8] [PMID: 32029897]
[143]
Song, X.; Zhu, S.; Chen, P.; Hou, W.; Wen, Q.; Liu, J.; Xie, Y.; Liu, J.; Klionsky, D.J.; Kroemer, G.; Lotze, M.T.; Zeh, H.J.; Kang, R.; Tang, D. AMPK-mediated BECN1 phosphorylation promotes ferroptosis by directly blocking system Xc- activity. Curr. Biol., 2018, 28(15), 2388-2399.e5.
[http://dx.doi.org/10.1016/j.cub.2018.05.094] [PMID: 30057310]
[144]
Kang, R.; Zeng, L.; Zhu, S.; Xie, Y.; Liu, J.; Wen, Q.; Cao, L.; Xie, M.; Ran, Q.; Kroemer, G.; Wang, H.; Billiar, T.R.; Jiang, J.; Tang, D. Lipid peroxidation drives Gasdermin D-mediated pyroptosis in lethal polymicrobial sepsis. Cell Host Microbe, 2018, 24(1), 97-108.e4.
[http://dx.doi.org/10.1016/j.chom.2018.05.009] [PMID: 29937272]
[145]
Kagan, V.E.; Tyurina, Y.Y.; Sun, W.Y.; Vlasova, I.I.; Dar, H.; Tyurin, V.A.; Amoscato, A.A.; Mallampalli, R.; van der Wel, P.C.A.; He, R.R.; Shvedova, A.A.; Gabrilovich, D.I.; Bayir, H. Redox phospholipidomics of enzymatically generated oxygenated phospholipids as specific signals of programmed cell death. Free Radic. Biol. Med., 2020, 147, 231-241.
[http://dx.doi.org/10.1016/j.freeradbiomed.2019.12.028] [PMID: 31883467]
[146]
Liu, J.; Kuang, F.; Kroemer, G.; Klionsky, D.J.; Kang, R.; Tang, D. Autophagy-dependent ferroptosis: machinery and regulation. Cell Chem. Biol., 2020, 27(4), 420-435.
[http://dx.doi.org/10.1016/j.chembiol.2020.02.005] [PMID: 32160513]
[147]
Wei, S.; Qiu, T.; Yao, X.; Wang, N.; Jiang, L.; Jia, X.; Tao, Y.; Wang, Z.; Pei, P.; Zhang, J.; Zhu, Y.; Yang, G.; Liu, X.; Liu, S.; Sun, X. Arsenic induces pancreatic dysfunction and ferroptosis via mitochondrial ROS-autophagy-lysosomal pathway. J. Hazard. Mater., 2020, 384121390
[http://dx.doi.org/10.1016/j.jhazmat.2019.121390] [PMID: 31735470]
[148]
Tang, Q.; Bai, L.; Zou, Z.; Meng, P.; Xia, Y.; Cheng, S.; Mu, S.; Zhou, J.; Wang, X.; Qin, X.; Cao, X.; Jiang, X.; Chen, C. Ferroptosis is newly characterized form of neuronal cell death in response to arsenite exposure. Neurotoxicology, 2018, 67, 27-36.
[http://dx.doi.org/10.1016/j.neuro.2018.04.012] [PMID: 29678591]
[149]
Zhang, C.; Liu, Z.; Zhang, Y.; Ma, L.; Song, E.; Song, Y. “Iron free” zinc oxide nanoparticles with ion-leaking properties disrupt intracellular ROS and iron homeostasis to induce ferroptosis. Cell Death Dis., 2020, 11(3), 183.
[http://dx.doi.org/10.1038/s41419-020-2384-5] [PMID: 32170066]
[150]
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.
[http://dx.doi.org/10.1016/j.envpol.2019.07.105] [PMID: 31401526]

Rights & Permissions Print Cite
Article Metrics
91
3
1
© 2024 Bentham Science Publishers | Privacy Policy