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Photothermal nanofibres enable safe engineering of therapeutic cells

Ranhua Xiong (UGent) , Dawei Hua (UGent) , Jelter Van Hoeck (UGent) , Dominika Berdecka (UGent) , Laurens Léger (UGent) , Stijn De Munter (UGent) , Juan Fraire (UGent) , Laurens Raes (UGent) , Aranit Harizaj (UGent) , Félix Sauvage (UGent) , et al.
(2021) NATURE NANOTECHNOLOGY. 16(11). p.1281-1291
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Abstract
Nanoparticle-mediated photoporation is used to temporarily permeabilize cell membranes for intracellular delivery of macromolecules, but cell exposure to nanoparticles might cause cellular damage and hamper application of the technique to therapeutic cell engineering. Here the authors show that, under photothermal heating, nanofibre-embedded iron oxide nanoparticles can be used to deliver effector macromolecules to different types of cells, in a contactless manner, with no cellular toxicity or diminished therapeutic potency. Nanoparticle-sensitized photoporation is an upcoming approach for the intracellular delivery of biologics, combining high efficiency and throughput with excellent cell viability. However, as it relies on close contact between nanoparticles and cells, its translation towards clinical applications is hampered by safety and regulatory concerns. Here we show that light-sensitive iron oxide nanoparticles embedded in biocompatible electrospun nanofibres induce membrane permeabilization by photothermal effects without direct cellular contact with the nanoparticles. The photothermal nanofibres have been successfully used to deliver effector molecules, including CRISPR-Cas9 ribonucleoprotein complexes and short interfering RNA, to adherent and suspension cells, including embryonic stem cells and hard-to-transfect T cells, without affecting cell proliferation or phenotype. In vivo experiments furthermore demonstrated successful tumour regression in mice treated with chimeric antibody receptor T cells in which the expression of programmed cell death protein 1 (PD1) is downregulated after nanofibre photoporation with short interfering RNA to PD1. In conclusion, cell membrane permeabilization with photothermal nanofibres is a promising concept towards the safe and more efficient production of engineered cells for therapeutic applications, including stem cell or adoptive T cell therapy.
Keywords
Electrical and Electronic Engineering, Condensed Matter Physics, General Materials Science, Biomedical Engineering, Atomic and Molecular Physics, and Optics, Bioengineering, GOLD NANOPARTICLES, IN-VITRO, DELIVERY, MOLECULES, TOXICITY

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Citation

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MLA
Xiong, Ranhua, et al. “Photothermal Nanofibres Enable Safe Engineering of Therapeutic Cells.” NATURE NANOTECHNOLOGY, vol. 16, no. 11, 2021, pp. 1281–91, doi:10.1038/s41565-021-00976-3.
APA
Xiong, R., Hua, D., Van Hoeck, J., Berdecka, D., Léger, L., De Munter, S., … Braeckmans, K. (2021). Photothermal nanofibres enable safe engineering of therapeutic cells. NATURE NANOTECHNOLOGY, 16(11), 1281–1291. https://doi.org/10.1038/s41565-021-00976-3
Chicago author-date
Xiong, Ranhua, Dawei Hua, Jelter Van Hoeck, Dominika Berdecka, Laurens Léger, Stijn De Munter, Juan Fraire, et al. 2021. “Photothermal Nanofibres Enable Safe Engineering of Therapeutic Cells.” NATURE NANOTECHNOLOGY 16 (11): 1281–91. https://doi.org/10.1038/s41565-021-00976-3.
Chicago author-date (all authors)
Xiong, Ranhua, Dawei Hua, Jelter Van Hoeck, Dominika Berdecka, Laurens Léger, Stijn De Munter, Juan Fraire, Laurens Raes, Aranit Harizaj, Félix Sauvage, Glenn Goetgeluk, Melissa Pille, Jeffrey Aalders, Joke Belza, Thibaut Van Acker, Eduardo Bolea Fernandez, Ting Si, Frank Vanhaecke, Winnok De Vos, Bart Vandekerckhove, Jolanda van Hengel, Koen Raemdonck, Chaobo Huang, Stefaan De Smedt, and Kevin Braeckmans. 2021. “Photothermal Nanofibres Enable Safe Engineering of Therapeutic Cells.” NATURE NANOTECHNOLOGY 16 (11): 1281–1291. doi:10.1038/s41565-021-00976-3.
Vancouver
1.
Xiong R, Hua D, Van Hoeck J, Berdecka D, Léger L, De Munter S, et al. Photothermal nanofibres enable safe engineering of therapeutic cells. NATURE NANOTECHNOLOGY. 2021;16(11):1281–91.
IEEE
[1]
R. Xiong et al., “Photothermal nanofibres enable safe engineering of therapeutic cells,” NATURE NANOTECHNOLOGY, vol. 16, no. 11, pp. 1281–1291, 2021.
@article{8725688,
  abstract     = {{Nanoparticle-mediated photoporation is used to temporarily permeabilize cell membranes for intracellular delivery of macromolecules, but cell exposure to nanoparticles might cause cellular damage and hamper application of the technique to therapeutic cell engineering. Here the authors show that, under photothermal heating, nanofibre-embedded iron oxide nanoparticles can be used to deliver effector macromolecules to different types of cells, in a contactless manner, with no cellular toxicity or diminished therapeutic potency.

Nanoparticle-sensitized photoporation is an upcoming approach for the intracellular delivery of biologics, combining high efficiency and throughput with excellent cell viability. However, as it relies on close contact between nanoparticles and cells, its translation towards clinical applications is hampered by safety and regulatory concerns. Here we show that light-sensitive iron oxide nanoparticles embedded in biocompatible electrospun nanofibres induce membrane permeabilization by photothermal effects without direct cellular contact with the nanoparticles. The photothermal nanofibres have been successfully used to deliver effector molecules, including CRISPR-Cas9 ribonucleoprotein complexes and short interfering RNA, to adherent and suspension cells, including embryonic stem cells and hard-to-transfect T cells, without affecting cell proliferation or phenotype. In vivo experiments furthermore demonstrated successful tumour regression in mice treated with chimeric antibody receptor T cells in which the expression of programmed cell death protein 1 (PD1) is downregulated after nanofibre photoporation with short interfering RNA to PD1. In conclusion, cell membrane permeabilization with photothermal nanofibres is a promising concept towards the safe and more efficient production of engineered cells for therapeutic applications, including stem cell or adoptive T cell therapy.}},
  author       = {{Xiong, Ranhua and Hua, Dawei and Van Hoeck, Jelter and Berdecka, Dominika and Léger, Laurens and De Munter, Stijn and Fraire, Juan and Raes, Laurens and Harizaj, Aranit and Sauvage, Félix and Goetgeluk, Glenn and Pille, Melissa and Aalders, Jeffrey and Belza, Joke and Van Acker, Thibaut and Bolea Fernandez, Eduardo and Si, Ting and Vanhaecke, Frank and De Vos, Winnok and Vandekerckhove, Bart and van Hengel, Jolanda and Raemdonck, Koen and Huang, Chaobo and De Smedt, Stefaan and Braeckmans, Kevin}},
  issn         = {{1748-3387}},
  journal      = {{NATURE NANOTECHNOLOGY}},
  keywords     = {{Electrical and Electronic Engineering,Condensed Matter Physics,General Materials Science,Biomedical Engineering,Atomic and Molecular Physics,and Optics,Bioengineering,GOLD NANOPARTICLES,IN-VITRO,DELIVERY,MOLECULES,TOXICITY}},
  language     = {{eng}},
  number       = {{11}},
  pages        = {{1281--1291}},
  title        = {{Photothermal nanofibres enable safe engineering of therapeutic cells}},
  url          = {{http://dx.doi.org/10.1038/s41565-021-00976-3}},
  volume       = {{16}},
  year         = {{2021}},
}

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