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Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach
Advanced Therapeutics, Volume: 6, Issue: 2, Start page: 2200179
Swansea University Authors: Marc Bilbao Asensio, James Cronin , Saul Michue-Seijas, Juan Mareque-Rivas
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DOI (Published version): 10.1002/adtp.202200179
Abstract
The efficacy of therapies is often hampered by limited tumor drug accumulation achieved through their intravenous administration, and by the lack of selectivity in targeting and killing cancer cells. Amplification of tumor redox stress and ferroptotic cell death to achieve selective killing of cance...
Published in: | Advanced Therapeutics |
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ISSN: | 2366-3987 2366-3987 |
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Wiley
2022
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URI: | https://cronfa.swan.ac.uk/Record/cronfa61668 |
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v2 61668 2022-10-27 Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach ae3834a12e3216058248bf0c83b90a4d Marc Bilbao Asensio Marc Bilbao Asensio true false 9cfd17551c0d1f7438895121e4fbb6e8 0000-0002-0590-9462 James Cronin James Cronin true false 7fcde209a4da147b056cefdb554f81b5 Saul Michue-Seijas Saul Michue-Seijas true false 14faad807724ffe1fb168c3fc225be0e 0000-0002-7405-3338 Juan Mareque-Rivas Juan Mareque-Rivas true false 2022-10-27 The efficacy of therapies is often hampered by limited tumor drug accumulation achieved through their intravenous administration, and by the lack of selectivity in targeting and killing cancer cells. Amplification of tumor redox stress and ferroptotic cell death to achieve selective killing of cancer cells using iron-containing agents has attracted considerable interest. However, these agents need high doses and multiple injection regimens and had limited success in the treatment of cancers such as melanoma. Melanoma often metastasizes via lymphatic vessels, where the metastasizing cells experience less redox stress and are protected from ferroptosis. Here we show that phospholipid-modified Pt(IV) prodrug-loaded iron oxide nanoparticle (IONP)-filled micelles (mIONP-PL-Pt(IV)), which integrate redox reactivity and iron-enabled catalytic therapeutic features with effective nanoparticle-assisted lymphatic delivery, provide significantly enhanced suppression of melanoma tumor growth compared to cisplatin-based chemotherapy and iron oxide nanoparticle treatments. Peroxidase-like activity, redox-triggered release of cisplatin and reactivity with hydrogen peroxide and ascorbic acid are contributors towards the induction of a combined ferroptosis-based and cisplatin anti-melanoma treatment. Treatment with mIONP-PL-Pt(IV) provided significant tumor control using cumulative treatment doses 10 to 100-fold lower than reported in intravenously administered treatments. This work demonstrates the potential of enhancing chemotherapeutic and iron-based catalytic nanomedicine efficacy exploiting nanoparticle-enabled lymphatic trafficking. Journal Article Advanced Therapeutics 6 2 2200179 Wiley 2366-3987 2366-3987 Ferroptosis; Platinum(IV) prodrugs; Iron oxide nanoparticles; ROS, Lymphatic system; Drug delivery; Melanoma treatment 14 11 2022 2022-11-14 10.1002/adtp.202200179 COLLEGE NANME COLLEGE CODE Swansea University SU Library paid the OA fee (TA Institutional Deal) Medical Research Council (GrantNumber(s): MC_PC_19053) Engineering and Physical Sciences Research Council (GrantNumber(s): 2105067) Cancer Research UK (GrantNumber(s): DCRPGF\100009) Cancer Research Institute (GrantNumber(s): Wade F.B. Thompson CLIP grant (CRI3645)) 2024-07-15T12:05:12.4026920 2022-10-27T10:52:22.0824373 Faculty of Science and Engineering School of Engineering and Applied Sciences - Chemistry Marc Bilbao Asensio 1 Ane Ruiz‐de‐Angulo 2 Amaia Garaikoetxea Arguinzoniz 3 James Cronin 0000-0002-0590-9462 4 Jordi Llop 5 Aintzane Zabaleta 6 Saul Michue-Seijas 7 Dominika Sosnowska 8 James N. Arnold 9 Juan Mareque-Rivas 0000-0002-7405-3338 10 61668__25797__fce6f6f39aa24ea1b52b26fe2e122f60.pdf 61668.pdf 2022-11-16T12:21:38.9843386 Output 4781909 application/pdf Version of Record true © 2022 The Authors. This is an open access article under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/ |
title |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach |
spellingShingle |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach Marc Bilbao Asensio James Cronin Saul Michue-Seijas Juan Mareque-Rivas |
title_short |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach |
title_full |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach |
title_fullStr |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach |
title_full_unstemmed |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach |
title_sort |
Redox‐Triggered Nanomedicine via Lymphatic Delivery: Inhibition of Melanoma Growth by Ferroptosis Enhancement and a Pt(IV)‐Prodrug Chemoimmunotherapy Approach |
author_id_str_mv |
ae3834a12e3216058248bf0c83b90a4d 9cfd17551c0d1f7438895121e4fbb6e8 7fcde209a4da147b056cefdb554f81b5 14faad807724ffe1fb168c3fc225be0e |
author_id_fullname_str_mv |
ae3834a12e3216058248bf0c83b90a4d_***_Marc Bilbao Asensio 9cfd17551c0d1f7438895121e4fbb6e8_***_James Cronin 7fcde209a4da147b056cefdb554f81b5_***_Saul Michue-Seijas 14faad807724ffe1fb168c3fc225be0e_***_Juan Mareque-Rivas |
author |
Marc Bilbao Asensio James Cronin Saul Michue-Seijas Juan Mareque-Rivas |
author2 |
Marc Bilbao Asensio Ane Ruiz‐de‐Angulo Amaia Garaikoetxea Arguinzoniz James Cronin Jordi Llop Aintzane Zabaleta Saul Michue-Seijas Dominika Sosnowska James N. Arnold Juan Mareque-Rivas |
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Journal article |
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Advanced Therapeutics |
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6 |
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2200179 |
publishDate |
2022 |
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Swansea University |
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2366-3987 2366-3987 |
doi_str_mv |
10.1002/adtp.202200179 |
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Wiley |
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Faculty of Science and Engineering |
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facultyofscienceandengineering |
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Faculty of Science and Engineering |
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facultyofscienceandengineering |
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Faculty of Science and Engineering |
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School of Engineering and Applied Sciences - Chemistry{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Engineering and Applied Sciences - Chemistry |
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description |
The efficacy of therapies is often hampered by limited tumor drug accumulation achieved through their intravenous administration, and by the lack of selectivity in targeting and killing cancer cells. Amplification of tumor redox stress and ferroptotic cell death to achieve selective killing of cancer cells using iron-containing agents has attracted considerable interest. However, these agents need high doses and multiple injection regimens and had limited success in the treatment of cancers such as melanoma. Melanoma often metastasizes via lymphatic vessels, where the metastasizing cells experience less redox stress and are protected from ferroptosis. Here we show that phospholipid-modified Pt(IV) prodrug-loaded iron oxide nanoparticle (IONP)-filled micelles (mIONP-PL-Pt(IV)), which integrate redox reactivity and iron-enabled catalytic therapeutic features with effective nanoparticle-assisted lymphatic delivery, provide significantly enhanced suppression of melanoma tumor growth compared to cisplatin-based chemotherapy and iron oxide nanoparticle treatments. Peroxidase-like activity, redox-triggered release of cisplatin and reactivity with hydrogen peroxide and ascorbic acid are contributors towards the induction of a combined ferroptosis-based and cisplatin anti-melanoma treatment. Treatment with mIONP-PL-Pt(IV) provided significant tumor control using cumulative treatment doses 10 to 100-fold lower than reported in intravenously administered treatments. This work demonstrates the potential of enhancing chemotherapeutic and iron-based catalytic nanomedicine efficacy exploiting nanoparticle-enabled lymphatic trafficking. |
published_date |
2022-11-14T12:05:11Z |
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1804642823830503424 |
score |
11.03559 |