Progress in the Mechanism of the Effect of Fe3O4 Nanomaterials on Ferroptosis in Tumor Cells
Abstract
:1. Introduction
2. Ferroptosis
- (1)
- GSH synthesis pathway is inhibited and LPO accumulates, thus inducing ferroptosis in cells [55].
- (2)
- Iron metabolism is altered. Iron is a redox-active metal involved in ROS formation and LPO diffusion, and a rising iron level could increase cellular susceptibility to iron-dependent cell death [56]. The accepted explanation today is that Fe2+ can transfer electrons to intracellular oxygen, and then react with intracellular lipids to form LPO, which further induces ferroptosis [57,58]. Iron metabolism genes and iron metabolism regulation genes play a key role in intracellular system iron homeostasis. For example, the gene of Iron Responsive Element Binding Protein 2 (IREB2) is a key player in the Erastin-induced ferroptosis of HT-1080 fibrosarcoma cells and Calu-1 lung cancer cells [59]. Thus, intracellular iron overload is critical for ferroptosis [60].
- (3)
- ROS metabolic pathway effects. This pathway also plays an important role in ferroptosis. Cytosolic cystine/glutamate transport receptor (System Xc-) and voltage-dependent anion channels (VDACs) [18] in the outer mitochondrial membrane, GPX4 and ferroptosis suppressor protein 1 (FSP1) ferroptosis-related proteins [61,62], and p62/keap1/Nrf2 [63], p53-related pathway [64,65], and ACSL4/LPCTA3/LOX [66] ferroptosis-related pathways play their roles in regulating ferroptosis by affecting ROS metabolism pathways [67].
3. Mechanism of the Effect of Fe3O4-NPs on Ferroptosis in Tumor Cells
3.1. Effect of Fe3O4-NPs on the Expression of Ferroptosis-Related Genes
3.2. Fe3O4-NPs Enhance the Sensitivity of Tumor Cells to Anticancer Drugs
3.3. Fe3O4-NPs Can Enhance the Efficacy of Drugs or Synergize with Them to Promote Ferroptosis
4. Fe3O4-NPs in Combination with PDT, Heat Stress, and SDT Further Induced Ferroptosis in Tumor Cells
4.1. Synergy of Photodynamic Therapy (PDT)
4.2. Metabolism Modulation by Heat Stress
4.3. Promotion of Sonodynamic Therapy (SDT)
5. Conclusions and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef] [PubMed]
- Hassannia, B.; Vandenabeele, P.; Vanden Berghe, T. Targeting Ferroptosis to Iron Out Cancer. Cancer Cell 2019, 35, 830–849. [Google Scholar] [CrossRef] [PubMed]
- Li, F.; Wang, Z.; Huang, Y.; Xu, H.; He, L.; Deng, Y.; Zeng, X.; He, N. Delivery of PUMA Apoptosis Gene Using Polyethyleneimine-SMCC-TAT/DNA Nanoparticles: Biophysical Characterization and In Vitro Transfection Into Malignant Melanoma Cells. J. Biomed. Nanotechnol. 2015, 11, 1776–1782. [Google Scholar] [CrossRef] [PubMed]
- Fu, J.; Dang, Z.; Deng, Y.; Lu, G. Regulation of c-Myc and Bcl-2 induced apoptosis of human bronchial epithelial cells by zinc oxide nanoparticles. J. Biomed. Nanotechnol. 2012, 8, 669–675. [Google Scholar] [CrossRef]
- Holohan, C.; Van Schaeybroeck, S.; Longley, D.B.; Johnston, P.G. Cancer drug resistance: An evolving paradigm. Nat. Rev. Cancer 2013, 13, 714–726. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Liu, Y.; Li, Z.; Shi, Y.; Deng, J.; Bai, J.; Ma, L.; Zeng, X.; Feng, S.; Ren, J.; et al. Unravelling the Role of LncRNA WT1-AS/miR-206/NAMPT Axis as Prognostic Biomarkers in Lung Adenocarcinoma. Biomolecules 2021, 11, 203. [Google Scholar] [CrossRef]
- Li, W.; Jia, M.; Deng, J.; Wang, J.; Lin, Q.; Tang, J.; Zeng, X.; Cai, F.; Ma, L.; Su, W.; et al. Down-regulation of microRNA-200b is a potential prognostic marker of lung cancer in southern-central Chinese population. Saudi J. Biol. Sci. 2019, 26, 173–177. [Google Scholar] [CrossRef]
- Li, W.; Jia, M.; Wang, J.; Lu, J.; Deng, J.; Tang, J.; Liu, C. Association of MMP9-1562C/T and MMP13-77A/G Polymorphisms with Non-Small Cell Lung Cancer in Southern Chinese Population. Biomolecules 2019, 9, 107. [Google Scholar] [CrossRef] [Green Version]
- Yang, S.; Guo, H.; Wei, B.; Zhu, S.; Cai, Y.; Jiang, P.; Tang, J. Association of miR-502-binding site single nucleotide polymorphism in the 3′-untranslated region of SET8 and TP53 codon 72 polymorphism with non-small cell lung cancer in Chinese population. Acta Biochim. Biophys. Sin. 2014, 46, 149–154. [Google Scholar] [CrossRef] [Green Version]
- ** of exoS in Pseudomonas aeruginosa Using Dual-Color Fluorescence Hybridization and Magnetic Separation. J. Biomed. Nanotechnol. 2018, 14, 206–214. [Google Scholar] [CrossRef]
- Mou, X.B.; Sheng, D.N.; Chen, Z.; Liu, M.; Liu, Y.; Deng, Y.; Xu, K.; Hou, R.X.; Zhao, J.Y.; Zhu, Y.B.; et al. In-Situ Mutation Detection by Magnetic Beads-Probe Based on Single Base Extension and Its Application in Genoty** of Hepatitis B Virus Pre-C Region 1896nt Locus Single Nucleotide Polymorphisms. J. Biomed. Nanotechnol. 2019, 15, 2393–2400. [Google Scholar] [CrossRef]
- Liu, B.; Jia, Y.Y.; Ma, M.; Li, Z.Y.; Liu, H.N.; Li, S.; Deng, Y.; Zhang, L.M.; Lu, Z.X.; Wang, W.; et al. High Throughput SNP Detection System Based on Magnetic Nanoparticles Separation. J. Biomed. Nanotechnol. 2013, 9, 247–256. [Google Scholar] [CrossRef] [Green Version]
- Li, S.; Liu, H.N.; Jia, Y.Y.; Mou, X.B.; Deng, Y.; Lin, L.; Liu, B.; He, N.Y. An Automatic High-Throughput Single Nucleotide Polymorphism Genoty** Approach Based on Universal Tagged Arrays and Magnetic Nanoparticles. J. Biomed. Nanotechnol. 2013, 9, 689–698. [Google Scholar] [CrossRef] [Green Version]
- Tang, C.L.; He, Z.Y.; Liu, H.M.; Xu, Y.Y.; Huang, H.; Yang, G.J.; ** cellular lipid composition. Nat. Chem. Biol. 2017, 13, 91–98. [Google Scholar] [CrossRef]
- Shen, Z.; Song, J.; Yung, B.C.; Zhou, Z.; Wu, A.; Chen, X. Emerging Strategies of Cancer Therapy Based on Ferroptosis. Adv. Mater. 2018, 30, e1704007. [Google Scholar] [CrossRef]
- Lai, Y.X.; Deng, Y.; Yang, G.J.; Li, S.; Zhang, C.X.; Liu, X.Y. Molecular Imprinting Polymers Electrochemical Sensor Based on AuNPs/PTh Modified GCE for Highly Sensitive Detection of Carcinomaembryonic Antigen. J. Biomed. Nanotechnol. 2018, 14, 1688–1694. [Google Scholar] [CrossRef]
- Lai, Y.X.; Wang, L.J.; Liu, Y.; Yang, G.J.; Tang, C.L.; Deng, Y.; Li, S. Immunosensors Based on Nanomaterials for Detection of Tumor Markers. J. Biomed. Nanotechnol. 2018, 14, 44–65. [Google Scholar] [CrossRef]
- Su, W.; Ma, L.; Wu, S.H.; Li, W.; Tang, J.X.; Deng, J.; Liu, J.X. Effect of Surface Modification of Silver Nanoparticles on the Proliferation of Human Lung Squamous Cell Carcinoma (HTB182) and Bronchial Epithelial (HBE) Cells In Vitro. J. Biomed. Nanotechnol. 2017, 13, 1281–1291. [Google Scholar] [CrossRef]
- Wu, Y.Y.; Deng, P.H.; Tian, Y.L.; Ding, Z.Y.; Li, G.L.; Liu, J.; Zuberi, Z.; He, Q.G. Rapid recognition and determination of tryptophan by carbon nanotubes and molecularly imprinted polymer-modified glassy carbon electrode. Bioelectrochemistry 2020, 131, 107393. [Google Scholar] [CrossRef]
- Gong, L.; Zhao, L.; Tan, M.D.; Pan, T.; He, H.; Wang, Y.L.; He, X.L.; Li, W.J.; Tang, L.; Nie, L.B. Two-Photon Fluorescent Nanomaterials and Their Applications in Biomedicine. J. Biomed. Nanotechnol. 2021, 17, 509–528. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Su, E.B.; Liu, Y.; He, N.Y.; Deng, Y.; **, L.; Chen, Z.; Li, S. A microfluidic device for accurate detection of hs-cTnI. Chin. Chem. Lett. 2021, 32, 1555–1558. [Google Scholar] [CrossRef]
- ** based on multiplex PCR and microarray. Chin. Chem. Lett. 2016, 27, 1661–1665. [Google Scholar] [CrossRef]
- Wu, Y.Y.; Deng, P.H.; Tian, Y.L.; Feng, J.X.; **ao, J.Y.; Li, J.H.; Liu, J.; Li, G.L.; He, Q.G. Simultaneous and sensitive determination of ascorbic acid, dopamine and uric acid via an electrochemical sensor based on PVP-graphene composite. J. Nanobiotechnol. 2020, 18, 112. [Google Scholar] [CrossRef]
- Gao, Z.; He, T.; Zhang, P.; Li, X.; Zhang, Y.; Lin, J.; Hao, J.; Huang, P.; Cui, J. Polypeptide-Based Theranostics with Tumor-Microenvironment-Activatable Cascade Reaction for Chemo-ferroptosis Combination Therapy. ACS Appl. Mater. Interfaces 2020, 12, 20271–20280. [Google Scholar] [CrossRef] [PubMed]
- Guo, J.P.; Xu, B.F.; Han, Q.; Zhou, H.X.; **a, Y.; Gong, C.W.; Dai, X.F.; Li, Z.Y.; Wu, G. Ferroptosis: A Novel Anti-tumor Action for Cisplatin. Cancer Res. Treat. 2018, 50, 445–460. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, B.; Ji, Q.; Cheng, Y.; Liu, M.; Zhang, B.; Mei, Q.; Liu, D.; Zhou, S. Biomimetic GBM-targeted drug delivery system boosting ferroptosis for immunotherapy of orthotopic drug-resistant GBM. J. Nanobiotechnol. 2022, 20, 161. [Google Scholar] [CrossRef] [PubMed]
- Cloughesy, T.; Mochizuki, A.; Orpilla, J.; Hugo, W.; Lee, A.; Davidson, T.; Wang, A.; Ellingson, B.; Rytlewski, J.; Sanders, C.; et al. Neoadjuvant anti-PD-1 immunotherapy promotes a survival benefit with intratumoral and systemic immune responses in recurrent glioblastoma. Nat. Med. 2019, 25, 477–486. [Google Scholar] [CrossRef]
- Chen, M.; Li, J.; Shu, G.; Shen, L.; Qiao, E.; Zhang, N.; Fang, S.; Chen, X.; Zhao, Z.; Tu, J.; et al. Homogenous multifunctional microspheres induce ferroptosis to promote the anti-hepatocarcinoma effect of chemoembolization. J. Nanobiotechnol. 2022, 20, 179. [Google Scholar] [CrossRef]
- Wilhelm, S.; Tavares, A.J.; Dai, Q.; Ohta, S.; Audet, J.; Dvorak, H.F.; Chan, W.C.W. Analysis of nanoparticle delivery to tumours. Nat. Rev. Mater. 2016, 1, 16014. [Google Scholar] [CrossRef]
- Yao, X.; **e, R.; Cao, Y.; Tang, J.; Men, Y.; Peng, H.; Yang, W. Simvastatin induced ferroptosis for triple-negative breast cancer therapy. J. Nanobiotechnol. 2021, 19, 311. [Google Scholar] [CrossRef]
- Wu, F.; Du, Y.; Yang, J.; Shao, B.; Mi, Z.; Yao, Y.; Cui, Y.; He, F.; Zhang, Y.; Yang, P. Peroxidase-like Active Nanomedicine with Dual Glutathione Depletion Property to Restore Oxaliplatin Chemosensitivity and Promote Programmed Cell Death. ACS Nano 2022, 16, 3647–3663. [Google Scholar] [CrossRef]
- Wang, X.; Li, P.; **g, X.; Zhou, Y.; Shao, Y.; Zheng, M.; Wang, J.; Ran, H.; Tang, H. Folate-modified erythrocyte membrane nanoparticles loaded with Fe3O4 and artemisinin enhance ferroptosis of tumors by low-intensity focused ultrasound. Front. Oncol. 2022, 12, 864444. [Google Scholar] [CrossRef]
- Yang, H.W.; Liang, W.B.; Si, J.; Li, Z.Y.; He, N.Y. Long Spacer Arm-Functionalized Magnetic Nanoparticle Platform for Enhanced Chemiluminescent Detection of Hepatitis B Virus. J. Biomed. Nanotechnol. 2014, 10, 3610–3619. [Google Scholar] [CrossRef]
- Fang, Y.L.; Liu, H.R.; Wang, Y.; Su, X.Y.; **, L.; Wu, Y.Q.; Deng, Y.; Li, S.; Chen, Z.; Chen, H.; et al. Fast and Accurate Control Strategy for Portable Nucleic Acid Detection (PNAD) System Based on Magnetic Nanoparticles. J. Biomed. Nanotechnol. 2021, 17, 407–415. [Google Scholar] [CrossRef] [PubMed]
- Chen, H.; Wu, Y.Q.; Chen, Z.; Hu, Z.L.; Fang, Y.L.; Liao, P.; Deng, Y.; He, N.Y. Performance Evaluation of a Novel Sample In-Answer Out (SIAO) System Based on Magnetic Nanoparticles. J. Biomed. Nanotechnol. 2017, 13, 1619–1630. [Google Scholar] [CrossRef] [PubMed]
- Ma, C.; Li, C.Y.; Wang, F.; Ma, N.N.; Li, X.L.; Li, Z.Y.; Deng, Y.; Wang, Z.F.; **, Z.J.; Tang, Y.J.; et al. Magnetic Nanoparticles-Based Extraction and Verification of Nucleic Acids from Different Sources. J. Biomed. Nanotechnol. 2013, 9, 703–709. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.W.; Liu, M.; Jiang, H.R.; Zeng, Y.; **, L.; Luan, T.; Deng, Y.; He, N.Y.; Zhang, G.; Zeng, X. Copy Number Variation Analysis Based on Gold Magnetic Nanoparticles and Fluorescence Multiplex Ligation-Dependent Probe Amplification. J. Biomed. Nanotechnol. 2017, 13, 655–664. [Google Scholar] [CrossRef]
- Guo, L.L.; Wang, T.; Chen, Z.; He, N.Y.; Chen, Y.Z.; Yuan, T. Light scattering based analyses of the effects of bovine serum proteins on interactions of magnetite spherical particles with cells. Chin. Chem. Lett. 2018, 29, 1291–1295. [Google Scholar] [CrossRef]
- Liang, H.; Wu, X.; Zhao, G.; Feng, K.; Ni, K.; Sun, X. Renal Clearable Ultrasmall Single-Crystal Fe Nanoparticles for Highly Selective and Effective Ferroptosis Therapy and Immunotherapy. J. Am. Chem. Soc. 2021, 143, 15812–15823. [Google Scholar] [CrossRef]
- Zhang, Y.; Wang, F.M.; Liu, C.Q.; Wang, Z.Z.; Kang, L.H.; Huang, Y.Y.; Dong, K.; Ren, J.S.; Qu, X.G. Nanozyme Decorated Metal-Organic Frameworks for Enhanced Photodynamic Therapy. ACS Nano 2018, 12, 651–661. [Google Scholar] [CrossRef]
- Shen, Z.Y.; Liu, T.; Li, Y.; Lau, J.; Yang, Z.; Fan, W.P.; Zhou, Z.J.; Shi, C.R.; Ke, C.M.; Bregadze, V.I.; et al. Fenton-Reaction-Acceleratable Magnetic Nanoparticles for Ferroptosis Therapy of Orthotopic Brain Tumors. ACS Nano 2018, 12, 11355–11365. [Google Scholar] [CrossRef]
- Tang, Z.; Liu, Y.; He, M.; Bu, W. Chemodynamic Therapy: Tumour Microenvironment-Mediated Fenton and Fenton-like Reactions. Angew. Chem. Int. Ed. Engl. 2019, 58, 946–956. [Google Scholar] [CrossRef]
- Chen, Q.; Ma, X.; **e, L.; Chen, W.; Xu, Z.; Song, E.; Zhu, X.; Song, Y. Iron-based nanoparticles for MR imaging-guided ferroptosis in combination with photodynamic therapy to enhance cancer treatment. Nanoscale 2021, 13, 4855–4870. [Google Scholar] [CrossRef]
- Liang, X.; Chen, M.; Bhattarai, P.; Hameed, S.; Tang, Y.; Dai, Z. Complementing Cancer Photodynamic Therapy with Ferroptosis through Iron Oxide Loaded Porphyrin-Grafted Lipid Nanoparticles. ACS Nano 2021, 15, 20164–20180. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.Y.; Zhao, X.H.; Huang, J.G.; Li, J.C.; Upputuri, P.K.; Sun, H.; Han, X.; Pramanik, M.; Miao, Y.S.; Duan, H.W.; et al. Transformable hybrid semiconducting polymer nanozyme for second near-infrared photothermal ferrotherapy. Nat. Commun. 2020, 11, 1857. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Whiteside, T.L. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008, 27, 5904–5912. [Google Scholar] [CrossRef] [Green Version]
- **e, S.; Sun, W.; Zhang, C.; Dong, B.; Yang, J.; Hou, M.; **ong, L.; Cai, B.; Liu, X.; Xue, W. Metabolic Control by Heat Stress Determining Cell Fate to Ferroptosis for Effective Cancer Therapy. ACS Nano 2021, 15, 7179–7194. [Google Scholar] [CrossRef]
- Qian, X.; Zhang, J.; Gu, Z.; Chen, Y. Nanocatalysts-augmented Fenton chemical reaction for nanocatalytic tumor therapy. Biomaterials 2019, 211, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Wu, F.X.; Chen, H.R.; Liu, R.Q.; Suo, Y.K.; Li, Q.Q.; Zhang, Y.L.; Liu, H.G.; Cheng, Z.; Chang, Y.L. An active-passive strategy for enhanced synergistic photothermal-ferroptosis therapy in the NIR-I/II biowindows. Biomater. Sci. 2022, 10, 1104–1112. [Google Scholar] [CrossRef] [PubMed]
- Antoniak, M.A.; Pazik, R.; Bazylinska, U.; Wiwatowski, K.; Tomaszewska, A.; Kulpa-Greszta, M.; Adamczyk-Grochala, J.; Wnuk, M.; Mackowski, S.; Lewinska, A.; et al. Multimodal polymer encapsulated CdSe/Fe3O4 nanoplatform with improved biocompatibility for two-photon and temperature stimulated bioapplications. Mater. Sci. Eng. C Mater. Biol. Appl. 2021, 127, 112224. [Google Scholar] [CrossRef]
- Mura, S.; Nicolas, J.; Couvreur, P. Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 2013, 12, 991–1003. [Google Scholar] [CrossRef]
- Li, B.B.; Xu, Q.N.; Li, X.F.; Zhang, P.; Zhao, X.; Wang, Y.X. Redox-responsive hyaluronic acid nanogels for hyperthermia-assisted chemotherapy to overcome multidrug resistance. Carbohydr. Polym. 2019, 203, 378–385. [Google Scholar] [CrossRef]
- Chen, M.J.; Zhang, F.; Song, J.J.; Weng, Q.Y.; Li, P.C.; Li, Q.; Qian, K.; Ji, H.X.; Pietrini, S.; Ji, J.S.; et al. Image-Guided Peri-Tumoral Radiofrequency Hyperthermia-Enhanced Direct Chemo-Destruction of Hepatic Tumor Margins. Front. Oncol. 2021, 11, 593996. [Google Scholar] [CrossRef]
- Zhu, M.T.; Wu, P.Y.; Li, Y.; Zhang, L.; Zong, Y.J.; Wan, M.X. Synergistic therapy for orthotopic gliomas via biomimetic nanosonosensitizer-mediated sonodynamic therapy and ferroptosis. Biomater. Sci. 2022, 10, 3911–3923. [Google Scholar] [CrossRef] [PubMed]
- Liang, C.; Zhang, X.L.; Yang, M.S.; Dong, X.C. Recent Progress in Ferroptosis Inducers for Cancer Therapy. Adv. Mater. 2019, 31, 1904197. [Google Scholar] [CrossRef] [PubMed]
- Galadari, S.; Rahman, A.; Pallichankandy, S.; Thayyullathil, F. Reactive oxygen species and cancer paradox: To promote or to suppress? Free Radic. Biol. Med. 2017, 104, 144–164. [Google Scholar] [CrossRef] [PubMed]
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Wang, Y.; Wu, X.; Bao, X.; Mou, X. Progress in the Mechanism of the Effect of Fe3O4 Nanomaterials on Ferroptosis in Tumor Cells. Molecules 2023, 28, 4562. https://doi.org/10.3390/molecules28114562
Wang Y, Wu X, Bao X, Mou X. Progress in the Mechanism of the Effect of Fe3O4 Nanomaterials on Ferroptosis in Tumor Cells. Molecules. 2023; 28(11):4562. https://doi.org/10.3390/molecules28114562
Chicago/Turabian StyleWang, Yaxuan, **ao Wu, **aoying Bao, and **anbo Mou. 2023. "Progress in the Mechanism of the Effect of Fe3O4 Nanomaterials on Ferroptosis in Tumor Cells" Molecules 28, no. 11: 4562. https://doi.org/10.3390/molecules28114562