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Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells

Caroline Bissardon Orcid Logo, Olivier Proux Orcid Logo, Salvatore Gazze, Odile Filhol Orcid Logo, BENOIT TOUBHANS, Lucie Sauzéat Orcid Logo, Sylvain Bouchet, Aled Lewis, Thierry Maffeis Orcid Logo, Jean-Louis Hazemann Orcid Logo, Sam Bayat Orcid Logo, Peter Cloetens, Steve Conlan Orcid Logo, Laurent Charlet, Sylvain Bohic Orcid Logo

Nanomaterials, Volume: 13, Issue: 23, Start page: 2999

Swansea University Authors: Salvatore Gazze, BENOIT TOUBHANS, Aled Lewis, Thierry Maffeis Orcid Logo, Steve Conlan Orcid Logo

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DOI (Published version): 10.3390/nano13232999

Abstract

Selenium 0 (Se0) is a powerful anti-proliferative agent in cancer research. We investigated the impact of sub-toxic concentrations of Se0 functionalized nanoparticles (SeNPs) on prostate cancer PC-3 cells and determined their intracellular localization and fate. An in-depth characterization of funct...

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Published in: Nanomaterials
ISSN: 2079-4991
Published: MDPI AG 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa65073
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BSA coating could prevent interactions between the reactive surface of the nanoparticles and the plasma membrane, mitigating the generation of reactive oxygen species. The intracellular localization showed interaction with mitochondria and also a localization in the lysosome-related organelle. The SeNPs-BSA localization in mitochondria constitute a possible explanation for our result showing a very significant dampening of the PC-3 cell proliferation capabilities. The purpose of the use of sublethal compound concentrations was to limit adverse effects resulting from high cell death to best evaluate some cellular changes and the fate of these SeNPs on PC-3. 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spelling v2 65073 2023-11-22 Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells 586f1f49652b97c5c3ab99a45a1c58bf Salvatore Gazze Salvatore Gazze true false e44b952350e531414d9288079b9a7c12 BENOIT TOUBHANS BENOIT TOUBHANS true false cbe9351b9fa294c53774638830286089 Aled Lewis Aled Lewis true false 992eb4cb18b61c0cd3da6e0215ac787c 0000-0003-2357-0092 Thierry Maffeis Thierry Maffeis true false 0bb6bd247e32fb4249de62c0013b51cb 0000-0002-2562-3461 Steve Conlan Steve Conlan true false 2023-11-22 ONDF Selenium 0 (Se0) is a powerful anti-proliferative agent in cancer research. We investigated the impact of sub-toxic concentrations of Se0 functionalized nanoparticles (SeNPs) on prostate cancer PC-3 cells and determined their intracellular localization and fate. An in-depth characterization of functionalized selenium nanoparticles composition is proposed to certify that no chemical bias relative to synthesis issues might have impacted the study. Selenium is an extremely diluted element in the biological environment and therefore requires high-performance techniques with a very low detection limit and high spatial resolution for intracellular imaging. This was explored with state-of-the-art techniques, but also with cryopreparation to preserve the chemical and structural integrity of the cells for spatially resolved and speciation techniques. Monodisperse solutions of SeNPs capped with bovine serum albumin (BSA) were shown to slow down the migration capacity of aggressive prostate cancer cells compared to polydisperse solutions of SeNPs capped with chitosan. BSA coating could prevent interactions between the reactive surface of the nanoparticles and the plasma membrane, mitigating the generation of reactive oxygen species. The intracellular localization showed interaction with mitochondria and also a localization in the lysosome-related organelle. The SeNPs-BSA localization in mitochondria constitute a possible explanation for our result showing a very significant dampening of the PC-3 cell proliferation capabilities. The purpose of the use of sublethal compound concentrations was to limit adverse effects resulting from high cell death to best evaluate some cellular changes and the fate of these SeNPs on PC-3. Our findings provide new insight to further study the various mechanisms of cytotoxicity of SeNPs. Journal Article Nanomaterials 13 23 2999 MDPI AG 2079-4991 Prostate cancer, selenium, nanoparticle-correlative synchrotron imaging, X-ray fluorescence, speciation, cytotoxicity 22 11 2023 2023-11-22 10.3390/nano13232999 http://dx.doi.org/10.3390/nano13232999 COLLEGE NANME Other/Subsidiary Companies - Not Defined COLLEGE CODE ONDF Swansea University This research and C.B. were funded by the INCA (grant INCa-INSERM- ASC16019CSA “SEDMAC”). 2023-12-13T15:02:39.5953439 2023-11-22T15:30:06.9840926 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Caroline Bissardon 0000-0002-2161-3776 1 Olivier Proux 0000-0003-0385-1815 2 Salvatore Gazze 3 Odile Filhol 0000-0003-1964-7958 4 BENOIT TOUBHANS 5 Lucie Sauzéat 0000-0001-8723-1351 6 Sylvain Bouchet 7 Aled Lewis 8 Thierry Maffeis 0000-0003-2357-0092 9 Jean-Louis Hazemann 0000-0002-3717-2151 10 Sam Bayat 0000-0002-8565-0293 11 Peter Cloetens 12 Steve Conlan 0000-0002-2562-3461 13 Laurent Charlet 14 Sylvain Bohic 0000-0001-6355-7592 15 65073__29264__cfe4c550a38c49179753968aabf563ca.pdf 65073.VOR.pdf 2023-12-13T14:59:57.8893673 Output 19546335 application/pdf Version of Record true © 2023 by the authors. Licensee MDPI, Basel, Switzerland. Distributed under the terms of a Creative Commons Attribution 4.0 International License (CC BY 4.0). true eng https://creativecommons.org/licenses/by/4.0/
title Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
spellingShingle Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
Salvatore Gazze
BENOIT TOUBHANS
Aled Lewis
Thierry Maffeis
Steve Conlan
title_short Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
title_full Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
title_fullStr Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
title_full_unstemmed Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
title_sort Intracellular Fate of Sub-Toxic Concentration of Functionalized Selenium Nanoparticles in Aggressive Prostate Cancer Cells
author_id_str_mv 586f1f49652b97c5c3ab99a45a1c58bf
e44b952350e531414d9288079b9a7c12
cbe9351b9fa294c53774638830286089
992eb4cb18b61c0cd3da6e0215ac787c
0bb6bd247e32fb4249de62c0013b51cb
author_id_fullname_str_mv 586f1f49652b97c5c3ab99a45a1c58bf_***_Salvatore Gazze
e44b952350e531414d9288079b9a7c12_***_BENOIT TOUBHANS
cbe9351b9fa294c53774638830286089_***_Aled Lewis
992eb4cb18b61c0cd3da6e0215ac787c_***_Thierry Maffeis
0bb6bd247e32fb4249de62c0013b51cb_***_Steve Conlan
author Salvatore Gazze
BENOIT TOUBHANS
Aled Lewis
Thierry Maffeis
Steve Conlan
author2 Caroline Bissardon
Olivier Proux
Salvatore Gazze
Odile Filhol
BENOIT TOUBHANS
Lucie Sauzéat
Sylvain Bouchet
Aled Lewis
Thierry Maffeis
Jean-Louis Hazemann
Sam Bayat
Peter Cloetens
Steve Conlan
Laurent Charlet
Sylvain Bohic
format Journal article
container_title Nanomaterials
container_volume 13
container_issue 23
container_start_page 2999
publishDate 2023
institution Swansea University
issn 2079-4991
doi_str_mv 10.3390/nano13232999
publisher MDPI AG
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
url http://dx.doi.org/10.3390/nano13232999
document_store_str 1
active_str 0
description Selenium 0 (Se0) is a powerful anti-proliferative agent in cancer research. We investigated the impact of sub-toxic concentrations of Se0 functionalized nanoparticles (SeNPs) on prostate cancer PC-3 cells and determined their intracellular localization and fate. An in-depth characterization of functionalized selenium nanoparticles composition is proposed to certify that no chemical bias relative to synthesis issues might have impacted the study. Selenium is an extremely diluted element in the biological environment and therefore requires high-performance techniques with a very low detection limit and high spatial resolution for intracellular imaging. This was explored with state-of-the-art techniques, but also with cryopreparation to preserve the chemical and structural integrity of the cells for spatially resolved and speciation techniques. Monodisperse solutions of SeNPs capped with bovine serum albumin (BSA) were shown to slow down the migration capacity of aggressive prostate cancer cells compared to polydisperse solutions of SeNPs capped with chitosan. BSA coating could prevent interactions between the reactive surface of the nanoparticles and the plasma membrane, mitigating the generation of reactive oxygen species. The intracellular localization showed interaction with mitochondria and also a localization in the lysosome-related organelle. The SeNPs-BSA localization in mitochondria constitute a possible explanation for our result showing a very significant dampening of the PC-3 cell proliferation capabilities. The purpose of the use of sublethal compound concentrations was to limit adverse effects resulting from high cell death to best evaluate some cellular changes and the fate of these SeNPs on PC-3. Our findings provide new insight to further study the various mechanisms of cytotoxicity of SeNPs.
published_date 2023-11-22T15:02:40Z
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