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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

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Front. Med.    2023, Vol. 17 Issue (2) : 173-206    https://doi.org/10.1007/s11684-023-0992-z
REVIEW
Zooming in and out of ferroptosis in human disease
Xue Wang1,2, Ye Zhou3, Junxia Min1(), Fudi Wang1,2()
1. The Second Affiliated Hospital, The First Affiliated Hospital, Institute of Translational Medicine, School of Public Health, State Key Laboratory of Experimental Hematology, Zhejiang University School of Medicine, Hangzhou 310058, China
2. The First Affiliated Hospital, Basic Medical Sciences, School of Public Health, Hengyang Medical School, University of South China, Hengyang 421001, China
3. Department of Endocrinology and Metabolism, Ningbo First Hospital, Ningbo 315000, China
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Abstract

Ferroptosis is defined as an iron-dependent regulated form of cell death driven by lipid peroxidation. In the past decade, it has been implicated in the pathogenesis of various diseases that together involve almost every organ of the body, including various cancers, neurodegenerative diseases, cardiovascular diseases, lung diseases, liver diseases, kidney diseases, endocrine metabolic diseases, iron-overload-related diseases, orthopedic diseases and autoimmune diseases. Understanding the underlying molecular mechanisms of ferroptosis and its regulatory pathways could provide additional strategies for the management of these disease conditions. Indeed, there are an expanding number of studies suggesting that ferroptosis serves as a bona-fide target for the prevention and treatment of these diseases in relevant pre-clinical models. In this review, we summarize the progress in the research into ferroptosis and its regulatory mechanisms in human disease, while providing evidence in support of ferroptosis as a target for the treatment of these diseases. We also discuss our perspectives on the future directions in the targeting of ferroptosis in human disease.
Keywords ferroptosis      human disease      iron metabolism      lipid peroxidation      antioxidation     
Corresponding Author(s): Junxia Min,Fudi Wang   
Just Accepted Date: 28 February 2023   Online First Date: 28 April 2023    Issue Date: 26 May 2023
 Cite this article:   
Xue Wang,Ye Zhou,Junxia Min, et al. Zooming in and out of ferroptosis in human disease[J]. Front. Med., 2023, 17(2): 173-206.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-023-0992-z
https://academic.hep.com.cn/fmd/EN/Y2023/V17/I2/173
Fig.1  The relationship between ferroptosis and various diseases. Ferroptosis is implicated in the regulation of multiple systemic diseases, including cancers, neurological diseases, cardiovascular diseases, respiratory diseases, liver diseases, digestive system diseases, urogenital system diseases, endocrine system diseases, iron overload diseases, musculoskeletal system diseases and autoimmune system diseases, and diseases of the visual system.
Fig.2  The molecular mechanisms of ferroptosis. The metabolic pathways that mediate ferroptosis mainly include iron metabolism, the antioxidant system and lipid metabolism. Iron metabolism: non-heme iron binds to TF and is released into the cytoplasm by TFR1 and can also be transported into cells through non-TF-bound iron uptake mediated by metal transporter SLC39A14. The metalloreductase STEAP3 reduces Fe3+ to Fe2+ in endosomes. Iron can be released from TF and exported to the cytoplasm by DMT1 or TRPML1. Heme releases iron under the catalyzed degradation of HO-1. Ferritin also releases a large amount of iron by ferritinophagy mediated by NCOA4. Further, hepcidin inhibits FPN to reduce the release of iron from the cell. Together, these processes can increase the LIP, thereby sensitizing cells to ferroptosis via the Fenton reaction. Antioxidant system: this pathway mainly involves the cysteine-GSH-GPX4 axis and FSP1-CoQ10 axis. Cystine is transported into the cell via system Xc–, and promotes the synthesis of GSH. Coenzyme Q10 and VK can be reduced to CoQ10H2 and VKH2, respectively, by FSP1, inhibiting lipid peroxidation by trapping lipid peroxidation free radicals. Lipid metabolism: MUFAs incorporate into phospholipids in an ACSL3-dependent manner to inhibit lipid peroxidation. PUFAs are metabolized by ACSL4/ACSL1, and LPCAT and then oxidized by PEBP1, POR, and ALOXs to promote lipid peroxidation and ferroptosis. In addition, PKCβII senses initial lipid peroxidation events and phosphorylates ACSL4 to drive pACSL4 activation to promote PUFA incorporation into PLs. Abbreviations: TF, transferrin; TFR1, transferrin receptor protein 1; SLC39A14, solute carrier family 39 member 14; TRPML1, transient receptor potential mucolipin 1; DMT1, divalent metal transporter 1; LIP, labile iron pool; NCOA4, nuclear receptor coactivator 4; FPN, ferroportin; GSH, glutathione; GTP, guanosine triphosphate; BH4, tetrahydrobiopterin; VKH2, vitamin K hydroquinone; GCLC, glutamate-cysteine ligase catalytic subunit; GPX4, glutathione peroxidase 4; IL4i1, interleukin-4-induced-1; GCH1, GTP cyclohydrolase-1; FSP1, ferroptosis suppressor protein 1; MRP1, multidrug resistance protein 1; ACC, acetyl CoA carboxylase; AMPK, adenosine-monophosphate-activated protein kinase; PUFA-PL, polyunsaturated fatty acid-containing phospholipid; LPCAT3, lysophosphatidylcholine acyltransferase 3; ACSL, acyl-CoA synthetase long-chain family; ALOXs, arachidonate lipoxygenases; POR, P450 oxidoreductase; PKCβII, protein kinase C beta type isoform 2; MUFA, monounsaturated fatty acid; PEBP1, phosphatidylethanolamine-binding protein 1; iPLA2β, group VI calcium-independent phospholipase A2β.
Fig.3  Mitochondria iron metabolism in ferroptosis. As a major source of cellular ROS, mitochondrial metabolism plays a key role in the execution of ferroptosis. The key mitochondrial iron importer SLC25A28 is engaged in heme and Fe-S biogenesis. HO-1 catalyzes the degradation of heme to produce Fe2+, which leads to mitochondrial iron overload and promotes ferroptosis. Separate mitochondria-localized defense systems have evolved to prevent mitochondrial lipid peroxidation and ferroptosis. For example, either the mitochondrial version of phospholipid hydroperoxide GPX4 or DHODH can specifically detoxify mitochondrial lipid peroxides. Mitochondrial ferritin protects mitochondria from iron overload-induced oxidative injury. In addition, CISD1 and CISD2 suppresses ferroptosis by limiting mitochondrial iron uptake. Abbreviations: ROS, reactive oxygen species; TCA, tricarboxylic acid; DHODH, dihydroorotate dehydrogenase; CoQ10, coenzyme Q10; FSP1, ferroptosis suppressor protein 1; FTMT, mitochondrial ferritin; HO-1, heme oxygenase 1; CISD, CDGSH iron sulfur domain; GPX4, glutathione peroxidase 4; GSH, glutathione; GSSG, glutathione disulfide; LIP, labile iron pool; PL-PUFA-OOH, polyunsaturated fatty acid-containing phospholipid hydroperoxides; PLOO·, phospholipid peroxyl radical; SCL25A28, also known as MFRN2, mitoferrin 2; SLC39A14, solute carrier family 39 member 14; SLC25A39, solute carrier family 25 member 39; NFS1, cysteine desulfurase; TF, transferrin; TFR1, transferrin receptor protein 1; RNF217, E3 ubiquitin protein ligase RNF217; FPN, ferroportin.
Organs/systems Diseases Key mechanisms Inhibitors Inducers
Brain AD Decreased GPX4, GSH and increased 4-HNE and MDA protein levels [116,117]Increased lipid peroxidation [116,117]Increased ROS level [118]Iron overload [119] Lip-1 [116]ALDH2 [121]TSG [122]Eriodictyol [124]FA [123]LA [126]Apolipoprotein E [125] –
PD Increased lipid peroxidation [128]Reduced GPX4 and SLC7A11 expression and GSH depletion [129,130]Increased ROS level [129,130]Deficiency of CoQ10 [127]Downregulate FTH1 [131] TRX-1 [132]Deferiprone [133]CQ [134] –
HD Increased lipid peroxidation [137,138]GSH depletion [139]Iron overload [140] DFO [142]Fer-1 [143] –
Brain trauma Iron overload [282] Fer-1 [282] –
FRDA Iron overload [283] EPI-743 and SFN [287] –
Heart IRI Increased lipid peroxidation [150]Increased the levels of ACSL4, iron and MDA [149]Decreased GPX4 level [149]Iron overload [154]Increased the transcription of FTH and FTL [66] Fer-1 [66]Lip-1 [158]DFO [161]2, 2-bipyridyl [162]mTOR [163,164]Dex [160]Baicalin [167]Britanin [168]Xanthohumol and naringenin [169,170]Resveratrol [171]Cyanidin-3-glucoside [172] –
HF Increased ROS level [181]Decreased GPX4 level [178]Downregulate the expression of FTH1 [181]Iron overload [181] Puerarin [184]DFO [66]Canagliflozin [185] Doxorubicin [179,180]
Atherosclerosis Accumulation of lipid peroxides and reduced GSH synthesis [186]Iron overload [189] PDSS2 [187]Fer-1 [190] –
Lung ALI Decreased GSH, GPX4 and SLC7A11 [195,196]Iron overload [195]MDA and 4-HNE accumulation [196] Fer-1 [196]iASPP [197]PX [198]Dimethyl fumarate [199] –
COPD Iron overload [201]Increased phospholipid peroxidation [202]Increased ROS level and decreased GSH and NADPH levels [203] DFO [201]Fer-1 [201] –
PF Reduced GPX4 expression and increased ROS [206] Lip-1 [206] Erastin [207]Paraquat [208]
Lung cancer Upregulate SCD1, FADS2, and FSP1 [45,314,315]Decreased intracellular Fe2+ and ROS levels [316,317] – Curcumin [91]Orlistat [98]DHA [318]Erianin [319]APAP [320]
Breast Breast cancer Not clear – 27-hydroxycholesterol [80]Metformin [321]Lidocaine [322]Sulfasalazine [323]Curcumin [109]EC330/EC359 [103]
Liver NAFLD Increased lipid peroxidation [209]Increased ACSL4 level [213]Increased GPX4 level (early stage) [220]Iron overload [210] IMA-1 [214]ECH1 [218]Lip-1 [215,216]ENO3 [220]Tβ4 [217]GB [219] –
ALD Increased lipid peroxidation [224]Decreased hepatic GSH levels [225]Iron overload [223] Fer-1 [222]Frataxin [226] Lipin-1 [224]Intestinal SIRT1 [225]
Liver fibrosis Increased lipid peroxidation [227]Inhibit xCT/SLC7A11 [229]Iron overload [227] – Wild bitter melon extract [230]ART [231,232]Artesunate [233]
HCC Upregulate ACSL3 and ACSL4 [93]
Stabilize SLC7A11 protein, increase intracellular GSH production, reduce lipid peroxidation [100,324]		 ABCC5 [100] IFNγ [325]MicroRNA-214-3p [326]Ceruloplasmin [106]Haloperidol [107]
Gastrointestinal Gastric cancer Upregulate SCD1, ELOVL5, and FADS1 [327,328]Decreased GPX4 expression [329] – Tanshinone IIA [330]ACP [331]Apatinib [329]
Colorectal cancer Upregulate SLC7A11 expression [332]Increased GSH and decreased ROS level [332] – Apatinib [92]TalaA [333]miRNA-15a-3p [334]SRSF9 [335]LCN2 [105]
Pancreas Pancreatic cancer Increased ROS level [336]Increased GSH synthesis [337] MGST1 [97]BCAT2 [104] Cyst(e)inase [337]Piperlongumine [338]Ponicidin [339]DHA [110]Ruscogenin [111]
Kidney AKI Increased lipid peroxidation [236]Decreased GPX4 and GSH levels [239]Iron overload [239,241] Quercetin [245]Nuciferine [246]Vitamin D receptors [247] Legumain [244]miR-182-5p [240]miR-378a-3p [240]
CKD Increased ACSL4 content [249]Increased lipid peroxidation [249,250]Decreased expression of SLC7A11 and GPX4 protein [250]Iron overload [249] Rosiglitazone [249]Fenofibrate [252]Tocilizumab mimotopes [254]Fer-1 and DFO [255] –
ADPKD Decreased expression of system Xc– and GPX4 [256] Increased expression of TFR1, DMT1 and HO-1 [256]Iron overload [256,257] Fer-1 [256]CPX-O [257] Erastin [256]
Endocrine T2DM Increased whole-body iron status [261] Cryptochlorogenic acid [262]Resveratrol [263]Polyphenols [264]Quercetin [259] Acrolein [263]
Obesity Upregulate ACSL4 [266]Iron overload [268] DFO [269] –
Blood HH Iron overload [273] Fer-1 [273]FGF21 [275] AUR [274]
Thalassemia Iron overload [278] Deferiprone [280]DFO [280] –
Orthopedic OA Iron overload [290]Decreased expression of SLC7A11 and GPX4 [290] Fer-1 [290]D-mannose [292] –
OP Iron overload (osteoblast) [294]Increased ROS level (osteoblast) [294] FTMT [294]Melatonin [295] 2ME2 [296]Artemisinin [297]
Autoimmune SLE Reduced GPX4 expression [301] Lip-1 [301]DFO [301] –
RA Increased expression of FTH1, GPX4, and SLC7A11 [303] – IKE [302]Glycine [303]
IBD Reduced GPX4 expression [306]Increased lipid peroxidation [306]Iron overload [307] Fer-1 [307]DFO [307] –
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