Cargando…

Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer

BACKGROUND: Hypoxia is an important factor that contributes to chemoresistance and metastasis in triple negative breast cancer (TNBC), and alleviating hypoxia microenvironment can enhance the anti-tumor efficacy and also inhibit tumor invasion. METHODS: A near-infrared (NIR) responsive on-demand oxy...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Dong, You, Yuanyuan, Xu, Yuan, Cheng, Qingqing, Xiao, Zeyu, Chen, Tianfeng, Shi, Changzheng, Luo, Liangping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8896283/
https://www.ncbi.nlm.nih.gov/pubmed/35246149
http://dx.doi.org/10.1186/s12951-022-01294-z
_version_ 1784663129899139072
author Zhang, Dong
You, Yuanyuan
Xu, Yuan
Cheng, Qingqing
Xiao, Zeyu
Chen, Tianfeng
Shi, Changzheng
Luo, Liangping
author_facet Zhang, Dong
You, Yuanyuan
Xu, Yuan
Cheng, Qingqing
Xiao, Zeyu
Chen, Tianfeng
Shi, Changzheng
Luo, Liangping
author_sort Zhang, Dong
collection PubMed
description BACKGROUND: Hypoxia is an important factor that contributes to chemoresistance and metastasis in triple negative breast cancer (TNBC), and alleviating hypoxia microenvironment can enhance the anti-tumor efficacy and also inhibit tumor invasion. METHODS: A near-infrared (NIR) responsive on-demand oxygen releasing nanoplatform (O(2)-PPSiI) was successfully synthesized by a two-stage self-assembly process to overcome the hypoxia-induced tumor chemoresistance and metastasis. We embedded drug-loaded poly (lactic-co-glycolic acid) cores into an ultrathin silica shell attached with paramagnetic Gd-DTPA to develop a Magnetic Resonance Imaging (MRI)-guided NIR-responsive on-demand drug releasing nanosystem, where indocyanine green was used as a photothermal converter to trigger the oxygen and drug release under NIR irradiation. RESULTS: The near-infrared responsive on-demand oxygen releasing nanoplatform O(2)-PPSiI was chemically synthesized in this study by a two-stage self-assembly process, which could deliver oxygen and release it under NIR irradiation to relieve hypoxia, improving the therapeutic effect of chemotherapy and suppressed tumor metastasis. This smart design achieves the following advantages: (i) the O(2) in this nanosystem can be precisely released by an NIR-responsive silica shell rupture; (ii) the dynamic biodistribution process of O(2)-PPSiI was monitored in real-time and quantitatively analyzed via sensitive MR imaging of the tumor; (iii) O(2)-PPSiI could alleviate tumor hypoxia by releasing O(2) within the tumor upon NIR laser excitation; (iv) The migration and invasion abilities of the TNBC tumor were weakened by inhibiting the process of EMT as a result of the synergistic therapy of NIR-triggered O(2)-PPSiI. CONCLUSIONS: Our work proposes a smart tactic guided by MRI and presents a valid approach for the reasonable design of NIR-responsive on-demand drug-releasing nanomedicine systems for precise theranostics in TNBC. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-022-01294-z.
format Online
Article
Text
id pubmed-8896283
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-88962832022-03-14 Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer Zhang, Dong You, Yuanyuan Xu, Yuan Cheng, Qingqing Xiao, Zeyu Chen, Tianfeng Shi, Changzheng Luo, Liangping J Nanobiotechnology Research BACKGROUND: Hypoxia is an important factor that contributes to chemoresistance and metastasis in triple negative breast cancer (TNBC), and alleviating hypoxia microenvironment can enhance the anti-tumor efficacy and also inhibit tumor invasion. METHODS: A near-infrared (NIR) responsive on-demand oxygen releasing nanoplatform (O(2)-PPSiI) was successfully synthesized by a two-stage self-assembly process to overcome the hypoxia-induced tumor chemoresistance and metastasis. We embedded drug-loaded poly (lactic-co-glycolic acid) cores into an ultrathin silica shell attached with paramagnetic Gd-DTPA to develop a Magnetic Resonance Imaging (MRI)-guided NIR-responsive on-demand drug releasing nanosystem, where indocyanine green was used as a photothermal converter to trigger the oxygen and drug release under NIR irradiation. RESULTS: The near-infrared responsive on-demand oxygen releasing nanoplatform O(2)-PPSiI was chemically synthesized in this study by a two-stage self-assembly process, which could deliver oxygen and release it under NIR irradiation to relieve hypoxia, improving the therapeutic effect of chemotherapy and suppressed tumor metastasis. This smart design achieves the following advantages: (i) the O(2) in this nanosystem can be precisely released by an NIR-responsive silica shell rupture; (ii) the dynamic biodistribution process of O(2)-PPSiI was monitored in real-time and quantitatively analyzed via sensitive MR imaging of the tumor; (iii) O(2)-PPSiI could alleviate tumor hypoxia by releasing O(2) within the tumor upon NIR laser excitation; (iv) The migration and invasion abilities of the TNBC tumor were weakened by inhibiting the process of EMT as a result of the synergistic therapy of NIR-triggered O(2)-PPSiI. CONCLUSIONS: Our work proposes a smart tactic guided by MRI and presents a valid approach for the reasonable design of NIR-responsive on-demand drug-releasing nanomedicine systems for precise theranostics in TNBC. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12951-022-01294-z. BioMed Central 2022-03-04 /pmc/articles/PMC8896283/ /pubmed/35246149 http://dx.doi.org/10.1186/s12951-022-01294-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhang, Dong
You, Yuanyuan
Xu, Yuan
Cheng, Qingqing
Xiao, Zeyu
Chen, Tianfeng
Shi, Changzheng
Luo, Liangping
Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
title Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
title_full Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
title_fullStr Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
title_full_unstemmed Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
title_short Facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise MRI-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
title_sort facile synthesis of near-infrared responsive on-demand oxygen releasing nanoplatform for precise mri-guided theranostics of hypoxia-induced tumor chemoresistance and metastasis in triple negative breast cancer
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8896283/
https://www.ncbi.nlm.nih.gov/pubmed/35246149
http://dx.doi.org/10.1186/s12951-022-01294-z
work_keys_str_mv AT zhangdong facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT youyuanyuan facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT xuyuan facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT chengqingqing facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT xiaozeyu facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT chentianfeng facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT shichangzheng facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer
AT luoliangping facilesynthesisofnearinfraredresponsiveondemandoxygenreleasingnanoplatformforprecisemriguidedtheranosticsofhypoxiainducedtumorchemoresistanceandmetastasisintriplenegativebreastcancer