Ferroptosis in Cancer Therapy: Mechanisms, Small Molecule Inducers, and Novel Approaches

Figures & data

Figure 1 Ferroptosis in cancer therapy.

Figure 2 Ferroptosis mechanisms and their associated inducers of ferroptosis.

Abbreviations: TF, Serum Transferrin; TFR1, The membrane protein Transferrin Receptor1; NCOA4, Nuclear receptor coactivator 4; STEAP3, Six-Transmembrane Epithelial Antigen of Prostate 3; DMT1, Divalent Metal Transporter 1; PE-PUFA, Phosphatidyl Ethanolamine-Polyunsaturated Fatty Acids; LOX, Lipoxygenase; Ferroportin1, FPN1, Ferritin; Membrane iron transport protein 1; PL-PUFA-OOH, Lipid hydroperoxide; ACSL4, Acyl-CoA Synthetase Long-Chain Family Member 4; SLC3A2, Recombinant Solute Carrier Family 3, Member 2; MDA, Malondialdehyde; 4HNE, 4-hydroxynonenal; POR, Cytochrome P450 oxidoreductase; FMN, Flavin mononucleotide; FAD, Flavin adenine dinucleotide; SLC7A11, Recombinant Solute Carrier Family 7, Member 11; GCL, Glutamate-cysteine ligase; GSS, Glutathione synthase; GSH, Glutathione; GPX4, Glutathione Peroxidase 4; GSSG, Oxidized glutathione; Glu, Glutamic acid; Nrf2, Nuclear factor E2-related factor 2; tumor suppressor, p53; Keap1, Recombinant Kelch-like ECH Associated Protein 1; ARE, Antioxidant response element; HO-1, Heme oxygenase-1; FSP1, Ferroptosis Inhibitory Protein 1; CoQ10, Coenzyme Q10; CoQ10H2, Panthenol; NADPH, Nicotinamide Adenine Dinucleotide Phosphate; Ipp, Isopentenyl pyrophosphate.

Table 1 Small Molecular Ferroptosis Inducers

Inducers	Structure	Types	Mechanism of Action	Experimental Models	Ref.
Erastin		Quinazolinone derivatives	Inhibition of the expression of SLC7A11	ALL xenograft model; Melanoma xenograft model; Hepatocellular carcinoma xenograft model	[56–58]
Piperazine erastin (PE)		Piperazine fragment-containing derivatives of Erastin	Inhibition of SLC7A11 expression	Fibrosarcoma xenograft model	[59]
Imidazole ketone erastin (IKE)		Carbonyl-containing derivatives of Erastin	Inhibition of SLC7A11 expression	DLBCL xenograft model; Lymphoma xenograft model; CIA mouse model	[60]
FA16		2-Trifluoromethyl benzimidazole derivative	Suppression system Xc^−	Hepatocellular carcinoma xenograft model	[61]
Lepadin H		Natural product alkaloid	Suppression of SLC7A11 expression in a p53-dependent manner	Hela cells; Melanoma xenograft model	[62]
Lepadin E		Natural product alkaloid	Suppression of SLC7A11 expression in a p53-dependent manner	Hela cells; B16F10 cells	[62]
Sulfasalazine (SAS)		Sulfonamide antibiotic	Inhibition of SLC7A11 expression	TE-1 cells; DU-145 cells; Prostate cancer xenograft model; Melanoma xenograft model; Glioblastoma xenograft model	[63–65]
Sorafenib		Protein kinase inhibitor	Inhibition of SLC7A11 expression; Inhibition of FSP1	Hepatic stellate cell	[66]
Olaparib		Poly ADP transferase inhibitor	Suppression of SLC7A11 expression in a p53-dependent manner	Ovarian cancer xenograft model	[66]
Flubendazole		Anti-malarial medicine	Suppression of SLC7A11 expression in a p53-dependent manner	Prostate cancer xenograft model	[67]
6-Thioguanine (6-TG)		Anti-leukemic drug	Suppression system Xc^−	Gastric cancer xenograft model	[68]
Metformin		Antidiabetic medication	Suppression of SLC7A11 expression; Suppression of Nrf2 expression	H1299 cells; A549 cells; Breast cancer xenograft model	[69,70]
Solasonine (SS)		Natural product alkaloid	Suppression of SLC7A11 expression in a p53-dependent manner	Nasopharyngeal cancer xenograft model; Pancreatic cancer xenograft model	[71,72]
Curcumin		Natural polyphenols	Upregulation of SLC1A5 expression; Activation of autophagy	Breast cancer Xenograft model; Non-small cell lung cancer xenograft model	[73,74]
RAS-selective lethal 3 (RSL3)		Tetrahydro-β-carboline derivative	Covalent inhibition of GPX4; increased ROS and cellular LAP	Fibrosarcoma xenograft model; Hepatocellular carcinoma xenograft model	[75,76]
Compound 26a		RSL3 derivative	Inhibition of GPX4	Breast Cancer Xenograft Model	[77]
Compound 24		RSL3 derivative	Inhibition of GPX4	A xenograft model of diffuse large B lymphoma	[78]
ML162		GPX4 covalent inhibitor	Covalent inhibition of GPX4	HRASG12V cell line	[79]
ML210		GPX4 covalent inhibitor	Covalent inhibition of GPX4	HRASG12V cell line	[79]
Compound C18		GPX4 covalent inhibitor	Covalent inhibition of GPX4	TNBC xenograft model	[80]
FIN56		GPX4 inhibitor	Induction of GPX4 degradation; activation of SQS	NCI60 cell line; Glioblastoma xenograft model	[81]
N6F11		GPX4 degradant	Induction of GPX4 degradation	Hs 578T cells; BxPC-3 cells; Hela cells	[82]
Metamizole sodium		COX inhibitor	Inhibition of GPX4-u46c - c10a - c66a enzyme activity		[83]
LOC1886		GPX4 inhibitor	Covalent inhibition of GPX4	G401 cell line	[84]
CH004		CBS inhibitor	Inhibition of CBS activity	Hepatocellular carcinoma xenograft model	[85]
BSO		GCL inhibitor	Inhibition of GSH synthesis	Breast cancer xenograft model; M14 cells	[86]
Simvastatin		Statin hypolipidemic drug	Mevalonate pathway	LX-2 cells	[87]
Orlistat		Lipase inhibitor	Induction of lipid peroxidation; inhibition of GPX4	Lung cancer xenograft model; Pancreatic cancer xenograft model	[88,89]
Tubastatin A		HDAC6 inhibitor	Inhibition of GPX4	TNBC xenograft model	[90]
Gliotoxin		Mycotoxins	Inhibition of GPX4; Targeted protein SLC7A11	H1975 cells; MCF-7 cells	[91]
Timosaponin AIII		Steroidal saponin	Promotes GPX4 ubiquitination and degradation; lipophagy	Non-small cell lung cancer xenograft tumor models	[92]
Compound31		Indirubin derivative	Promotes GPX4 ubiquitination	Colon cancer xenograft tumor model	[93]
Sulforaphane		Natural isothiocyanate	GSH depletion; decreased GPX4 expression	U-937 cells	[94]
iFSP1		Inhibitor targeting FSP1	Inhibition of FSP1	HCC cells	[95]
icFSP1		3-phenylquinazolinone	Inhibition of FSP1	Melanoma xenograft tumor model	[96]
FSEN1		Non-competitive inhibitor of FSP1	Inhibition of FSP1	A549 cells; H460 cells	[97]
ViFSP1		FSP1 inhibitor	Inhibition of FSP1	HT-1080 cells; A375 cells; Huh7 cells	[98]
NPD4928		FSP1 inhibitor	Inhibition of FSP1	PC-3 cells; MKN74 cells; DU145 cells	[99]
ShtIX		Natural novel isoflavonoid	Inhibition of the Nrf2/HO-1 signaling pathway	Non-small cell lung cancer xenograft tumor models	[100]
Trigonelline		Natural alkaloid	Inhibition of Nrf2	Non-small cell lung cancer xenograft tumor models	[101]
APAP		NSAIDs	Inhibition of Nrf2	Non-small cell lung cancer xenograft tumor models	[102]
Sunitinib		Multitargeted tyrosine kinase inhibitor	Inhibition of Nrf2	H9c2 cells	[103]
Baicalin		Natural-derived flavonoid	Downregulation of FTH1; inhibition of Nrf2	Bladder cancer xenograft tumor model; Osteosarcoma xenograft tumor model	[104]
Matrine		Natural alkaloid	Inhibition of x-CT; activation of TFR; inhibition of Nrf2; activation of Piezo1-Ca2+ signaling	Cervical cancer xenograft tumor model; L02 cells	[105]
NCTD		Demethylated analogue of cantharidin	Suppression of NRF2/HO-1/GPX4/xCT Axis	Ovarian cancer xenograft tumor model	[106]
Wogonin		Natural-derived Flavonoid	Suppression of Nrf2/GPX4 axes	Pancreatic cancer xenograft tumor model	[107]
Glyphosate		Organophosphorus herbicide	Suppression of Nrf2/GSH/GPX4 axes	Normal mouse model	[108]
Pizotifen malate (PZM)		5-HT2 receptor antagonist	Inhibition of Nrf2	Xenograft tumor model of esophageal squamous carcinoma	[109]
Brusatol (Bru)		Bioactive compound	Inhibition of GSH synthesis; inhibition of Nrf2	Xenograft tumor model of esophageal squamous carcinoma	[110]
S-3’-hydroxy-7’, 2’, 4’-trimethoxyisoxane (ShtIX)		Isoflavans compound	Inhibition of Nrf2/HO-1 pathway	Non-small cell lung cancer xenograft tumor models	[100]
Lapatinib		Tyrosine kinase inhibitor	Targeting ELOVL6/ACSL4; Inhibition of VEGFR2/Nrf2/Keap1 pathway; Inhibition of GSH	HCT116 cells; Glioma xenograft tumor model; Gastric cancer xenograft tumor model	[111]
Erianin		Bioactive natural compound	Blockade of the JAK2/STAT3/SLC7A11 pathway; promotion of N6-Methyladenosine modification of ALOX12/P53 mRNA; inhibition of Nrf2	Hepatocellular carcinoma xenograft tumor model; Kidney cancer xenograft tumor model	[112]
Artesunate		Artemisia extract	Increased lipid peroxidation; inhibition of GSH	Hepatocellular carcinoma xenograft tumor model	[113]
QD394		ROS inducer	Add ROS	PANC-1 cells	[114]
QD394-Me		ROS inducer	Add ROS	PANC-1 cells	[114]
Imetelstat		Telomerase inhibitor	Increased synthesis and subsequent oxidation of PUFA phospholipids; lipid phagocytosis	Patients with (AML)	[115]
Disulfiram		ALDH1 inhibitor	Induction of lipid peroxidation	U251 cells; LN229 cells	[116]
Quercetin		Flavonoid compound	Increased ROS generation; increased TFR	MCF-7 cells; MDA-MB-231 cells; HEC-1-A cells	[117]
Darapladib		Lp-PLA2 inhibitor	Inhibition of Lp-PLA2	Hs746T cells; SNU-484 cells	[118]
Auranofin (AUR)		Drug for rheumatoid arthritis	Inhibits TXNRD activity; increases lipid peroxidation	Huh7 cells; HEK293T cells; Normal mouse model	[119]
Fe(hino)3		Redox-active complex	Increase in Fe	TNBC xenograft tumor model	[120]
SSPH I		Natural steroidal saponin	Up-regulation of SLC7A5 expression; up-regulation of TFR and FPN protein expression	HepG2 cells	[121]
Polyphyllin B		Natural product	Promotes ferric ion transport and ferritin autophagy; binds GPX4	Orthotopic gastric cancer mouse model	[122]
Ochratoxin		Mycotoxin	Up-regulation of TFR1 and FTH expression; down-regulation of FPN expression	HEK-293 cells	[123]
BPDE		In vivo metabolites of BP	Upregulates iron metabolism; promotes GPX4 catabolism	Swan 71 cells; HTR-8/Svneo cells	[124]
Juglone		Natural quinone	Increased iron accumulation; GSH depletion	A549 cells	[125]
Withaferin A		Natural steroidal lactone	Increased iron accumulation; inhibition of GPX4; inhibition of Nrf2	Pancreatic cancer metastasis model; Hepatocellular carcinoma xenograft tumor model	[126]
10p		Urea derivative	Add ROS	HT-29 cells	[127]
JB3		Sorafenib derivative	Suppression system Xc^−	Lung cancer xenograft model	[128]
GIC-20		ML162 derivative	Covalent inhibition of GPX4	HT1080 xenograft model	[129]

Figure 3 (a) Chemical structural formula of PROTAC-like ferroptosis inducers. (b) The process of PROTAC-mediated ubiquitination and proteasomal degradation of GPX4.

Table 2 Nanomaterials for Inducing Ferroptosis

Compound	Mechanism	In vivo	Reference
D@FMN-M	Release Fe^3+ and DHA	√	[235]
DOX/Fe^3+/EGCG (DF) NPs	Release DOX and Fe^3+	√	[236]
Fe3O4-PLGA-Ce6	Release Fe^3+ and Ce6	√	[237]
BSO/ZIF-8@Au@MPN@HA(BZAMH)	Inhibit GSH synthesis	√	[238]
MTX-LDH@MnO2	Promoting ROS generation	√	[239]
GDY-FIN56-RAP (GFR)	Inhibit GPX4	√	[240]
Gel@WA-cRGD	Release WA	√	[241]
Fe3O4@PCBMA	Inhibit MVA pathway and GPX4	√	[242]
DMSN/Fe3O4-Mn@CB-839	Inhibit GSH	√	[243]
AuFCSP MOFs	Inhibit GSH and GPX4	√	[244]
SRF@Hb-Ce6	Inhibit GSH and GPX4	√	[245]
UCNP	Increase Fe^2+ and Fe^3+	√	[246]
CSO-SS-Cy7-Hex/SPION/Srfn	Increase Fe^2+ and Fe^3+	√	[247]
NMIL-100@GOx@C	Increase Fe^2+ and H2O2	√	[248]
ChA CQDs	Inhibit GPX4	√	[249]
RSL3@COF-Fc (2b)	Increase Fe^2+ and inhibit GPX4	√	[250]
AMSNs	Inhibit GPX4	√	[251]
[e-mail]^2+-CaSi-PAMAMFA/mPEG	Inhibit GSH	√	[252]
FGLC	Inhibit GSH	√	[253]
Fe3O4@PGL NPs	Increase Fe^3+ and ROS	√	[254]
DOX-TAF@FN	Increase Fe^2+ and Fe^3+	√	[255]
GNPIPP12MA	Inhibit GSH	√	[256]
Pa-M/Ti-NCs	Increase Fe^2+ and H2O2	√	[257]
IONPs	Increase Fe^2+ and ROS	√	[258]
AFN@CM	Release Fe^3+ and inhibit GPX4	√	[259]
PPA/TF	Increase Fe^2+ and ROS	√	[260]
IONP-HA	Increase Fe^2+	√	[261]
mIONP-PL-Pt(IV)	Increase Fe^2+ and Pt	√	[262]
ovs‐MnO2	Induces the release of intracellular free iron (Fe^2+)	√	[263]
ApoE-UPGs-DHA	Increase Fe^2+ and release DHA	√	[264]
FeO-PEI@TDN-DOX	Increase Fe^2+ and release DOX	√	[265]
Cu2O@Au	Promote the Fenton reaction and deplete GSH	√	[266]
MP-FA@R-F NPs	Increase Fe^2+ and Rhein	√	[267]
I@P-ss-FRT	Increase Fe^2+	√	[268]
USPBNPs@MCSNs (UPM)	Inhibit Xc^−-GSH-GPX4	√	[269]
FeE@PEG NPs	Increase Fe^2+ and release EGCG	√	[270]
HNK@Ir-HMONs- LOD(HIHL)	Release HNK and Ir	√	[271]
sora@Fe-MIL	Increase Fe^2+ and release sorafenib	√	[272]
Oxa@Mil-100(Fe)	Induce apoptosis and release Fe^3+	√	[273]
AsIr@PDA	Relase IrFN	√	[274]
MitCuOHA	Inhibit GSH	√	[275]

Figure 4 Chemical structural formula of PDTAC-like and SDTAC-like ferroptosis inducers.

Figure 5 Ferroptosis-inducing therapy in PDT and SDT.

Table 3 Comparing the Advantages and Disadvantages of Different Ferroptosis Inducers Methods

	Traditional Small Molecular Compounds	PROTACs	Nanomaterials	PDT and SDT
Advantages	Small molecular weight; Can penetrate the cell membrane; Can cross blood-brain barrier; Most do not involve immunogenicity; Good stability; Can be taken orally; Easily absorbed; Mature synthesis technology	Catalytic properties; Great target; Longer half-life; Low toxicity; Overcome drug resistance; Wide range of targets	Great target; Good stability; Longer half-life; Overcome drug resistance; High effectiveness; High oral bioavailability	High controllability; High selectivity; Low toxicity
Disadvantages	Poor solubility; Short half-life; Low specificity; drug resistance; Limited effectiveness	High molecular weight; Poor solubility; Low oral bioavailability; Poor drugability; Difficult to synthesize	Low biosecurity; Having some toxic effects; Off-target effect; Difficult to repeat synthesis	High dependence on tissue oxygen concentration; Weak penetration into deep tissues; Limited therapeutic effect
Ref.	[299,300]	[301,302]	[303–305]	[306–308]

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