Photothermia at the nanoscale induces ferroptosis via nanoparticle degradation

Alexandre Fromain, Jose Efrain Perez, Aurore Van de Walle, Yoann Lalatonne and Claire Wilhelm ()
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Alexandre Fromain: Sorbonne University, PSL University
Jose Efrain Perez: Sorbonne University, PSL University
Aurore Van de Walle: Sorbonne University, PSL University
Yoann Lalatonne: Université Sorbonne Paris Nord, Université Paris Cité, Laboratory for Vascular Translational Science, LVTS, INSERM, UMR 1148
Claire Wilhelm: Sorbonne University, PSL University

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract The Fe(II)-induced ferroptotic cell death pathway is an asset in cancer therapy, yet it calls into question the biocompatibility of magnetic nanoparticles. In the latter, Fe(II) is sequestered within the crystal structure and is released only upon nanoparticle degradation, a transition that is not well understood. Here, we dissect the chemical environment necessary for nanoparticle degradation and subsequent Fe(II) release. Importantly, temperature acts as an accelerator of the process and can be triggered remotely by laser-mediated photothermal conversion, as evidenced by the loss of the nanoparticles’ magnetic fingerprint. Remarkably, the local hot-spot temperature generated at the nanoscale can be measured in operando, in the vicinity of each nanoparticle, by comparing the photothermal-induced nanoparticle degradation patterns with those of global heating. Further, remote photothermal irradiation accelerates degradation inside cancer cells in a tumor spheroid model, with efficiency correlating with the endocytosis progression state of the nanoparticles. High-throughput imaging quantification of Fe2+ release, ROS generation, lipid peroxidation and cell death at the spheroid level confirm the synergistic thermo-ferroptotic therapy due to the photothermal degradation at the nanoparticle level.

Date: 2023
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DOI: 10.1038/s41467-023-40258-1

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