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Article

High-Dose Exposure to Polymer-Coated Iron Oxide Nanoparticles Elicits Autophagy-Dependent Ferroptosis in Susceptible Cancer Cells

by
Thanpisit Lomphithak
1,2,
Selin Helvacioglu
1,3,
Ilaria Armenia
4,
Sandeep Keshavan
1,†,
Jesús G. Ovejero
5,6,
Giovanni Baldi
7,
Costanza Ravagli
7,
Valeria Grazú
4,8 and
Bengt Fadeel
1,*
1
Division of Molecular Toxicology, Institute of Environmental Medicine, Karolinska Institutet, 17177 Stockholm, Sweden
2
Department of Clinical Chemistry, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok 10330, Thailand
3
Department of Molecular Biology and Genetics, Izmir Institute of Technology, Izmir 35433, Turkey
4
Instituto de Nanociencia y Materiales de Aragón (INMA), CSIC-Universidad de Zaragoza, 50001 Zaragoza, Spain
5
Instituto de Ciencia de Materiales de Madrid (ICMM-CSIC), 28049 Madrid, Spain
6
Department of Dosimetry and Radioprotection, General University Hospital Gregorio Marañón, 28049 Madrid, Spain
7
Colorobbia Consulting S.R.L., Sovigliana, 50053 Vinci, Italy
8
Centro de Investigación Biomédica en Red de Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), 50018 Zaragoza, Spain
*
Author to whom correspondence should be addressed.
†
Current address: Adolphe Merkle Institute, University of Fribourg, CH-1700 Fribourg, Switzerland.
Nanomaterials 2023, 13(11), 1719; https://doi.org/10.3390/nano13111719
Submission received: 17 April 2023 / Revised: 10 May 2023 / Accepted: 18 May 2023 / Published: 24 May 2023
(This article belongs to the Special Issue Interaction of Nanomaterials with Biological Systems: In Vitro and In Vivo Studies)
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Abstract

Ferroptosis, a form of iron-dependent, lipid peroxidation-driven cell death, has been extensively investigated in recent years, and several studies have suggested that the ferroptosis-inducing properties of iron-containing nanomaterials could be harnessed for cancer treatment. Here we evaluated the potential cytotoxicity of iron oxide nanoparticles, with and without cobalt functionalization (Fe2O3 and Fe2O3@Co-PEG), using an established, ferroptosis-sensitive fibrosarcoma cell line (HT1080) and a normal fibroblast cell line (BJ). In addition, we evaluated poly (ethylene glycol) (PEG)-poly(lactic-co-glycolic acid) (PLGA)-coated iron oxide nanoparticles (Fe3O4-PEG-PLGA). Our results showed that all the nanoparticles tested were essentially non-cytotoxic at concentrations up to 100 μg/mL. However, when the cells were exposed to higher concentrations (200–400 μg/mL), cell death with features of ferroptosis was observed, and this was more pronounced for the Co-functionalized nanoparticles. Furthermore, evidence was provided that the cell death triggered by the nanoparticles was autophagy-dependent. Taken together, the exposure to high concentrations of polymer-coated iron oxide nanoparticles triggers ferroptosis in susceptible human cancer cells.
Keywords: autophagy; cobalt; ferroptosis; iron oxide nanoparticles; lipid peroxidation autophagy; cobalt; ferroptosis; iron oxide nanoparticles; lipid peroxidation

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MDPI and ACS Style

Lomphithak, T.; Helvacioglu, S.; Armenia, I.; Keshavan, S.; Ovejero, J.G.; Baldi, G.; Ravagli, C.; Grazú, V.; Fadeel, B. High-Dose Exposure to Polymer-Coated Iron Oxide Nanoparticles Elicits Autophagy-Dependent Ferroptosis in Susceptible Cancer Cells. Nanomaterials 2023, 13, 1719. https://doi.org/10.3390/nano13111719

AMA Style

Lomphithak T, Helvacioglu S, Armenia I, Keshavan S, Ovejero JG, Baldi G, Ravagli C, Grazú V, Fadeel B. High-Dose Exposure to Polymer-Coated Iron Oxide Nanoparticles Elicits Autophagy-Dependent Ferroptosis in Susceptible Cancer Cells. Nanomaterials. 2023; 13(11):1719. https://doi.org/10.3390/nano13111719

Chicago/Turabian Style

Lomphithak, Thanpisit, Selin Helvacioglu, Ilaria Armenia, Sandeep Keshavan, Jesús G. Ovejero, Giovanni Baldi, Costanza Ravagli, Valeria Grazú, and Bengt Fadeel. 2023. "High-Dose Exposure to Polymer-Coated Iron Oxide Nanoparticles Elicits Autophagy-Dependent Ferroptosis in Susceptible Cancer Cells" Nanomaterials 13, no. 11: 1719. https://doi.org/10.3390/nano13111719

APA Style

Lomphithak, T., Helvacioglu, S., Armenia, I., Keshavan, S., Ovejero, J. G., Baldi, G., Ravagli, C., Grazú, V., & Fadeel, B. (2023). High-Dose Exposure to Polymer-Coated Iron Oxide Nanoparticles Elicits Autophagy-Dependent Ferroptosis in Susceptible Cancer Cells. Nanomaterials, 13(11), 1719. https://doi.org/10.3390/nano13111719

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