Understanding the Novel Approach of Nanoferroptosis for Cancer Therapy

doi:10.1007/s40820-024-01399-0

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Abstract

As a new form of regulated cell death, ferroptosis has unraveled the unsolicited theory of intrinsic apoptosis resistance by cancer cells. The molecular mechanism of ferroptosis depends on the induction of oxidative stress through excessive reactive oxygen species accumulation and glutathione depletion to damage the structural integrity of cells. Due to their high loading and structural tunability, nanocarriers can escort the delivery of ferro-therapeutics to the desired site through enhanced permeation or retention effect or by active targeting. This review shed light on the necessity of iron in cancer cell growth and the fascinating features of ferroptosis in regulating the cell cycle and metastasis. Additionally, we discussed the effect of ferroptosis-mediated therapy using nanoplatforms and their chemical basis in overcoming the barriers to cancer therapy.

Key words： Ferroptosis Nanoparticles Ferrotherapy Cancer Genes Nanotechnology Toxicity Reactive oxygen species

Received: 03 January 2024 Published: 02 May 2024

Corresponding Authors: Prashant Kesharwani, Fei Gao

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Afsana Sheikh and Prashant Kesharwani have contributed equally to this work.

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	Articles by authors
	Afsana Sheikh
	Prashant Kesharwani
	Waleed H. Almalki
	Salem Salman Almujri
	Linxin Dai
	Zhe-Sheng Chen
	Amirhossein Sahebkar
	Fei Gao

Cite this article:

Afsana Sheikh,Prashant Kesharwani,Waleed H. Almalki, et al. Understanding the Novel Approach of Nanoferroptosis for Cancer Therapy[J]. Nano-Micro Letters, 2024, 16(1): 188-.

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https://www.qk.sjtu.edu.cn/nml/EN/10.1007/s40820-024-01399-0 OR https://www.qk.sjtu.edu.cn/nml/EN/Y2024/V16/I1/188

Table 1

Representation of characteristic features of various forms of cell death

Table 2

Kinds of ferroptosis inducers

Fig. 1 Representation of the ferroptosis mechanism in cancer therapy. Three pathways are primarily associated; inhibition of GPX4, iron metabolism and lipid peroxidation. 1 Erastin, which is a prototype of ferroptosis inducer, blocks the uptake of cysteine (cys) by directly inhibiting system Xc-, which in turn promotes GPX4 degradation by encouraging chaperone-mediated autophagy, 2 increase in LIP downregulate DMT1 to promote oxidative stress causing ferroptosis, 3 recombinant lysophosphatidylcholine acyltransferase 3 (LPCAT3) and Acyl-CoA synthetase long-chain family member 4 (ACSL4) are the catalysts required for the synthesis of PUFA-containing phospholipids which under oxidative stress promotes ferroptosis

101]">

Fig. 2 Representation of ferroptosis effect of endothelin-3 targeted nanoparticle in production of highly reactive hydroxyl radical [<xref ref-type="bibr" rid="b101">101</xref>]

103]">

Fig. 3 The cascade of cell death inducing mechanism of nanomicelles. The theranostic nanomicelles produced highly reactive hydroxyl radical by releasing of AscH−, Fe2+ and the adjuvant Cy7QB [<xref ref-type="bibr" rid="b103">103</xref>]

105]">

Fig. 4 a pH-responsive polyethylene glycolpoly(allylamine)-dimethylmaleic anhydride (PEG-PAH-DMMA)-coated tamoxifen-loaded copper peroxide nanoparticle-capped hollow mesoporous organosilica nanoparticle (HMON), b illustration of ROS storm generation by developed nanoparticle,c lscm images showing GPX4, ROS and lipoxygenase level, d estimation of ROS level by flow cytometry in 4T1 cells laden mice, e relative complex I activity measurement and f lactate level measurement in 4T1 cells laden mice, g measurement of GSH level [<xref ref-type="bibr" rid="b105">105</xref>]

111]">

Fig. 5 a Representation of formation of Lapa-loaded HAS-Fe2O3 NP. b Following intravenous administration, the EPR effect caused HAS-Fe2O3 NP to concentrate in tumor tissues and be absorbed by tumor cells. Superoxide dismutase (SOD) then transformed the O2· into a mass of H2O2 as a result of the excessive O2· produced by the catalytic release of Lapa by the overexpressed NQO1 enzyme. Meanwhile, in the acidic endosomal environment, ferrous ions from self-sacrificing Fe3O4 combined with accumulating H2O2 via Fenton reactions to form extremely harmful ·OH leading to cell death. Additionally, consumption of NADPH in the Lapa futile cycle led to GSH depletion, impairing the antioxidant defense system and increasing the sensitivity of tumor cells to •OH produced in the Fe2+-mediated Fenton chemical reaction, intensifying the anticancer impact [<xref ref-type="bibr" rid="b111">111</xref>]

112]">

Fig. 6 Representation of effect of molecularly engineered pH-responsive photothermal oxazine self-assembled nanoparticles (PTO-Biotin Nps) for spatiotemporal controlled tumor ferroptosis [<xref ref-type="bibr" rid="b112">112</xref>]

Table 3

Illustration of nanoferrotherapeutics involved in treatment of various cancers

Type of nanocarrier system	Chemotherapeutics	Genes	Cancer type	In vitro	In vivo	Inference	References
MOF	Doxorubicin	-	Breast cancer	4T1 cells	Balb/c mice	Doxorubicin-induced ferroptosis causing immunogenic cell death (ICD)	[251]
Gold mesoporousMOF	-	-	Breast cancer	4T1 cells	Balb/c mice	Cu and Fe ion bridged using disulfide bond induces ferroptosis by depleting GSH, finally inhibiting GPX-4 level	[137]
MOF	Doxorubicin	-	Breast cancer	4T1 and MCF-7	Mice (name not mentioned)	The drug-loaded nanoparticle showed great potency and clinical translation by targeting CD44 over-expressed cells	[141]
Fe(III)- porphyrin-MOF	Oxaliplatin	-	-	Breast cancer	4T1 cells	The therapy increased the level of H₂O₂ and (IFN-γ), which in turn caused ferroptosis of cells	[145]
Fe-MOF	-	-		Breast cancer	4T1 cells	Aptamer PD-L1-attached glucose oxidase and PEG-modified iron-based MOF were an innovative strategy to disrupt iron homeostasis and hinder intracellular redox	[21]
RBC membrane camouflaged MOF	Doxorubicin	-	Breast cancer	MCF-7	Balb/c nude mice	Results illustrated that self-assembled RBC membrane camouflaged MOF could amplify the oxidative stress of ROS, reduce glutathione potentiating remarkable anticancer effects	[146]
MOF	Doxorubicin	-	Breast cancer	4T1 cells	Balb/c mice	The nanoplatform downregulated GPX4 to induce ferroptosis	[251]
Nanophoto-sensitizer	-	-	Human melanoma cancer	A375	Nu/Nu female mice	A photodynamic therapy-based nanosheets of graphitic carbon nitride functionalized with mitochondria-targeting iridium (III) polypyridine complexes caused hypoxic environment resulting in cell death	[225]
Theranostic nanoparticle composed of iron ions, cinnamaldehyde prodrug and amphiphilic polymer skeletal (FCS/GCS)	-	-	Breast cancer	4T1 cells	Balb/c mice	The preparation with the help of CA induces Fenton reaction, generated ·OH and accelerated lipid peroxides (LPO) accumulation and accordingly augments ferroptosis	[229]
Bonsai-inspired AIE nanohybrid photosensitizer	-	-	Colon cancer	MC38 cells	Balb/c	The Bonsa-inspired nanopreparation in presence of white light irradiation produced hydroxyl radical and depleted GSH to induce ferroptosis in cancer cells	[240]
Cell membrane decorated iron-siRNA nanohybrid	-	Anti- SLC7A11 siRNA	Human oral squamous cell carcinoma	CAL-27	Male Balb/c	The nanohybrid system elevated the ROS level to show synergic anti-cancer effect in vivo	[96]
Magnetic lipid nanoparticle	-	siDECR1	Castration-resistant prostate cancer	C4-2B or C4-2BEnz cells	Nude mice (name not mentioned)	The biomimetic nanoparticles were stable, safe and effective in showing remarked inhibition of distant organ metastasis	[218]
Graphene oxide-PEG-PEI nanoparticle	Sorafenib	PD-L1 siRNA	Hepatocellular carcinoma	MHCC97H cells	C57BL/6 mice	The developed preparation reduced the expression of GPX4 in the intrahepatic tumor regions in immunocompetent mice	[219]
Liposome	Artemisinin	-	Lung carcinoma	LLC cells	Balb/c nude mice	The remarkable autophagy-mediated ferroptosis-involved cancer-therapeutic efficacy is suggested by therapeutic outcomes both in vitro and in vivo which is further confirmed by transcriptome sequencing	[160]
Nanostructured lipid carrier	Doxorubicin, ferrocene	-	Breast cancer	4T1 cells	Balb/c mice	TGF-β receptor inhibitor along with ferrocene and doxorubicin-loaded NLC inhibited mammary cancer metastasis by extracellular as well as intracellular hybrid mechanism	[164]
Liposomes	-	-	Breast cancer	4T1 cells	Balb/c mice	An amalgamation of sonosensitizing agent (PpIX) and ferumoxytol in liposomes induced apoptosis and ferroptosis overcoming the tumor resistance	[215]
Iron oxide nanoparticles	Paclitaxel	-	Glioblastoma	U251 and HMC3 cells	Balb/c-nu mice	PTX-IONP reduced the ability of cells to invade and migrate, elevated ROS, iron ions and lipid peroxidation, enhanced the expression of the autophagy-related proteins LC3II, and Beclin1 and suppressed the expression of the p62 and GPX4	[173]
Nanozyme	Cisplatin	-	Ovarian cancer	SKOV3/DDP cells	BALB/cJGpt-Foxn1nu/Gpt mice	The formulation was able to induce both apoptosis and ferroptosis with the help of ultrasound treatment for cisplatin-resistant cancer cells	[193]
Nanozyme	-	-	Triple-negative breast cancer	MDA-MB-231 cells	Balb/c nude mice	The imaging-based nanosystem used SPIO and Avastin to induce tumor starvation and ferroptosis	[263]
Nanozyme	-	-	Breast cancer	4T1 and MCF-7 cells	Balb/c mice	Tumor ablation was accomplished with Fenton reaction-independent ferroptosis driven by photothermal nanozyme	[197]
Nanozyme	Gemcitabine	-	Pancreatic cancer	PANC02	Balb/c mice	GEM and MnFe₂O₄ can synergistically improve anti-cancer profile via ferroptosis and GEM-mediated chemotherapy	[198]
Human serum albumin nanoparticle (HAS-NP)	Pt (IV)	-	Ovarian cancer	SKOV3	Mice (name not mentioned)	The prodrug of platinum in HAS nanoparticles was effective for ovarian cancer cell resistance to platinum	[241]
Iron-doped calcium carbonate nanoparticles	Pt(IV)	-	Breast cancer	4T1 and CT26 cells	Balb/c	Iron-doped platinum-SA-based CaCO₃ showed development of ROS and lipid peroxidation to mediate cancer cell death	[242]
Zeolite imidazolate framework (Zif-8)	-	-	Head and neck squamous cell carcinoma	HN6	Male Balb/c	DHA and SNP enveloped nanoreactor system prompted Fe²⁺ and NO release to initiate ferroptosis and apoptosis synergistically	[247]
Hypoxia-responsive nanoelicitor	Mitoxantrone	-	Colorectal cancer	CT26 cells	Balb/c nude mice	The simultaneous co-stimulating effects of CA and MIT resulted in an elevated antiproliferative and anti-cancer immunity, which in turn aborted the system Xc⁻ to GPX4 pathway and increased the iron-initiated tumor cell destruction	[248]

Table 3

Illustration of nanoferrotherapeutics involved in treatment of various cancers

137]">

Fig. 7 a Schematic illustration of synergistic effect of radiotherapy and ferroptosis mediated by Au-FCP-MOF-NP. The left side represents the negative role of GPX4 stimulated by radiotherapy to resist ferroptosis and finally radio-resistance, while the right side shows induction of ferroptosis due to intratumoral release of Fe-Cu dual ion along with Au NP which catalyzed β-D-glucose oxidation to develop gluconic acid. Increased amount of H2O2 released toxic hydroxyl radicals which induced ferroptosis. Overall, radiosensitization increased due to synergic effect of high Z element (Au) and ferroptosis; b fluorescence images of cell (4T1) treated with Au-FCP-MOF-NP to evaluate peroxidation with respective flow cytometry analysis; c Au-FCP-MOF-NP and IR treated 4T1 cells showing extend of colon formation and d western blotting results showing expression of GPX4 with various concentration of Au-FCP-MOF-NP with or without exposure of IR. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b137">137</xref>]

141]">

Fig. 8 a Schematic representation of development process of Dox-FeTHA-aMOF with its application in photothermal-assisted synergistic ferroptosis-apoptosis cancer therapy; b time-dependent fluorescence descriptions of 4T1 tumor-bearing mouse post-injection with dye (Cy5.5) labeled aMOF with detected fluorescence in major organs at 24 h post-treatment; c infrared thermal images under 808-nm laser irradiation; d representation of development of tumor model and respective treatment strategy; e illustration of tumor volume with f digital pictures of excised tumor lesions. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b141">141</xref>]

145]">

Fig. 9 The triple-hit effect of (PCN-Oxpt/PEG) for inducing chemotherapy, ferroptosis and immunotherapy, a representation of development of oxaliplatin prodrug and b PCN-Oxpt/PEG, c magnetic resonance images of mice after treatment with PBS, iron chloride and nanoparticles showing accumulation at tumor site [<xref ref-type="bibr" rid="b145">145</xref>]

21]">

Fig. 10 a Schematic representation of development of PD-L1-targeted aptamer-grafted iron-based MOF, b the developed therapy based on ferroptosis-mediated immunotherapy disrupts iron homeostasis and redox balance through inactivation of GSH, ROS accumulation and transferrin 1 downregulation to finally suppress PD-L1 checkpoints, c illustration of blocking the targeted site (PD-L1), d illustration of therapy-induced in mouse models, e digital images of different treatment groups, f estimation of tumor volume (mm3) and g tumor weight of xenograft model of mouse bearing 4T1 cells, h tumor section analysis through H&E-stained images, analysis of Ki 67 and TUNEL test. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b21">21</xref>]

Fig. 11 Representation of ferrocene (Fc) and Dox-loaded cationic NLCs developed by emulsion solvent evaporation method, which was then decorated with β-cyclodextrins grafted heparin (β-CD-HEP) by the help of electrostatic interaction. The preparation triggered Fenton reaction, reduced TGF-β secretion and induced immune responses for ferroptosis-mediated anti-cancer therapy

193]">

Fig. 12 a Synthesis of SO2, •CF3 and •OH bearing nanoflower and its inhibiting mechanism for cisplatin resistance cancer under ultrasonic radiation, b ROS suppressing effect of nanoflower detected by 2,7-dichlorodihydrofluorescein diacetate (DCFH-DA), dihydroethidium (DHE) and hydroxyphenyl fluorescein (HPH), c determination of SO2 production capacity coumarin-hemicyanine dye, d cell cytotoxicity study of different nanopreparations under US irradiation. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b193">193</xref>]

215]">

Fig. 13 a Schematic representation of development method of ferumoxytol-loaded nanoliposome to induce synergistic anti-cancer response (by applying sonodynamic approach) using reverse evaporation method. Ferumoxytol successfully imported iron ions into the cell to stimulate ferroptosis, while photosensitizing agent induced apoptosis by making cancer cells responsive toward therapy, c, d apoptosis and destruction of 4T1 cells post-treatment with various formulations. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b215">215</xref>]

225]">

Fig. 14 a Representation of development of Ir-g-C3N4, b regeneration of different kinds of ROS using photosensitizer, c representation of mechanism of action of mitochondrial targeting nanosystem responsible for ferroptosis and apoptosis-mediated cell death, d blood circulation time post-treatment of Nu/Nu mice with Ir-g-C3N4, e biodistribution assay for evaluation of Ir in major organs, f luminescence intensity measurement of nanoplatforms at various time interval, g digital images of tumor after treatment. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b225">225</xref>]

240]">

Fig. 15 a Representation of bonsai-inspired AIE nanohybrid photosensitizer as a key driver in ferroptosis-mediated self-reliable PDT, b preparation steps of ultrathin vermiculite nanosystem showing vermiculite in bulk (i), its SEM image (ii) and vermiculite NSs solution (iii), c preparation steps of vermiculite NSs@DCPy and its TEM image, d In vivo study in mice model showing tumor bio-images with white dotted lines, e images of major organs post 24 h of therapy showing spleen (S), heart (H), kidney (K), tumor (T), liver (Li) and lungs (Lu), f bio-distribution of NSs@DCPy and DCPy in Balb/c mice model, g tumor growth curves, h estimation of expression of Caspase 3 and i GPX4 by immunohistochemical analysis. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b240">240</xref>]

246]">

Fig. 16 a, b Preparatory steps of mesoporous zeolite framework comprising of C6-PAMAM and tannic acid, which is then laden with p53 to deplete GSH which is attributed to SLC7A11 inhibition, further causing prominent downregulation of GPX4, c size determination using DLS, d TEM image, e high-angle annular dark-field scanning TEM (HAADF-STEM) image, f TEM images of preparation in pH (5.5 or 7.4), g estimation of expression of p53 post-incubation of H1299 cells with developed therapy, h cell apoptosis study with various treatment groups, i cell viability assay. Reproduced with permission from Ref. [<xref ref-type="bibr" rid="b246">246</xref>]

247,248]">

Fig. 17 a Development process of PEG-functionalized folic acid (FA)-modified zeolite imidazolate frameworks (Zifs) carrying dihydroartemisinin (DHA) as ferroptosis inducer and sodium nitroprusside (SNP) as apoptosis inducer for the treatment of HNSCC; b (1) folate receptor enhanced the cellular uptake after binding with FA-functionalized preparation, (2) location of tumor after treatment using imaging tool and (3) elevated anti-cancer effect, c representation of development process of MIT-based nanoelicitor to suppress GPX4 expression, enable lipid peroxidation to induce cell ferroptosis [<xref ref-type="bibr" rid="b247">247</xref>,<xref ref-type="bibr" rid="b248">248</xref>]

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