Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy

Abstract Background Nanotheranostics advances anticancer management by providing therapeutic and diagnostic functions, that combine programmed cell death (PCD) initiation and imaging-guided treatment, thus increasing the efficacy of tumor ablation and efficiently fighting against cancer. However, mi...

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Main Authors: Zhe Zhang, Hsuan Lo, Xingyang Zhao, Wenya Li, Ke Wu, Fanchu Zeng, Shiying Li, Hongzan Sun
Format: Article
Language:English
Published: BMC 2023-05-01
Series:Journal of Nanobiotechnology
Subjects:
Online Access:https://doi.org/10.1186/s12951-023-01910-6
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author Zhe Zhang
Hsuan Lo
Xingyang Zhao
Wenya Li
Ke Wu
Fanchu Zeng
Shiying Li
Hongzan Sun
author_facet Zhe Zhang
Hsuan Lo
Xingyang Zhao
Wenya Li
Ke Wu
Fanchu Zeng
Shiying Li
Hongzan Sun
author_sort Zhe Zhang
collection DOAJ
description Abstract Background Nanotheranostics advances anticancer management by providing therapeutic and diagnostic functions, that combine programmed cell death (PCD) initiation and imaging-guided treatment, thus increasing the efficacy of tumor ablation and efficiently fighting against cancer. However, mild photothermal/radiation therapy with imaging-guided precise mediating PCD in solid tumors, involving processes related to apoptosis and ferroptosis, enhanced the effect of breast cancer inhibition is not fully understood. Results Herein, targeted peptide conjugated gold nano cages, iRGD-PEG/AuNCs@FePt NPs ternary metallic nanoparticles (Au@FePt NPs) were designed to achieve photoacoustic imaging (PAI)/Magnetic resonance imaging (MRI) guided synergistic therapy. Tumor-targeting Au@FePt forms reactive oxygen species (ROS), initiated by X-ray-induced dynamic therapy (XDT) in collaboration with photothermal therapy (PTT), inducing ferroptosis-augmented apoptosis to realize effective antitumor therapeutics. The relatively high photothermal conversion ability of Au@FePt increases the temperature in the tumor region and hastens Fenton-like processes to achieve enhanced synergistic therapy. Especially, RNA sequencing found Au@FePt inducting the apoptosis pathway in the transcriptome profile. Conclusion Au@FePt combined XDT/PTT therapy activate apoptosis and ferroptosis related proteins in tumors to achieve breast cancer ablation in vitro and in vivo. PAI/MRI images demonstrated Au@FePt has real-time guidance for monitoring synergistic anti-cancer therapy effect. Therefore, we have provided a multifunctional nanotheranostics modality for tumor inhibition and cancer management with high efficacy and limited side effects. Graphical Abstract
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spelling doaj.art-22c58ed63e1d4e279bc13b87483bce1b2023-05-14T11:26:37ZengBMCJournal of Nanobiotechnology1477-31552023-05-0121112010.1186/s12951-023-01910-6Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategyZhe Zhang0Hsuan Lo1Xingyang Zhao2Wenya Li3Ke Wu4Fanchu Zeng5Shiying Li6Hongzan Sun7Department of Radiology, Shengjing Hospital of China Medical UniversityGuangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical SciencesMedical Research Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical UniversityMedical Research Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical UniversityDepartment of Radiology, Shengjing Hospital of China Medical UniversityGuangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical SciencesGuangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical SciencesDepartment of Radiology, Shengjing Hospital of China Medical UniversityAbstract Background Nanotheranostics advances anticancer management by providing therapeutic and diagnostic functions, that combine programmed cell death (PCD) initiation and imaging-guided treatment, thus increasing the efficacy of tumor ablation and efficiently fighting against cancer. However, mild photothermal/radiation therapy with imaging-guided precise mediating PCD in solid tumors, involving processes related to apoptosis and ferroptosis, enhanced the effect of breast cancer inhibition is not fully understood. Results Herein, targeted peptide conjugated gold nano cages, iRGD-PEG/AuNCs@FePt NPs ternary metallic nanoparticles (Au@FePt NPs) were designed to achieve photoacoustic imaging (PAI)/Magnetic resonance imaging (MRI) guided synergistic therapy. Tumor-targeting Au@FePt forms reactive oxygen species (ROS), initiated by X-ray-induced dynamic therapy (XDT) in collaboration with photothermal therapy (PTT), inducing ferroptosis-augmented apoptosis to realize effective antitumor therapeutics. The relatively high photothermal conversion ability of Au@FePt increases the temperature in the tumor region and hastens Fenton-like processes to achieve enhanced synergistic therapy. Especially, RNA sequencing found Au@FePt inducting the apoptosis pathway in the transcriptome profile. Conclusion Au@FePt combined XDT/PTT therapy activate apoptosis and ferroptosis related proteins in tumors to achieve breast cancer ablation in vitro and in vivo. PAI/MRI images demonstrated Au@FePt has real-time guidance for monitoring synergistic anti-cancer therapy effect. Therefore, we have provided a multifunctional nanotheranostics modality for tumor inhibition and cancer management with high efficacy and limited side effects. Graphical Abstracthttps://doi.org/10.1186/s12951-023-01910-6MR/PA imagingTernary metallic nanoparticlesSensitized apoptosisPhotothermal/radiation therapySensitized ferroptosis
spellingShingle Zhe Zhang
Hsuan Lo
Xingyang Zhao
Wenya Li
Ke Wu
Fanchu Zeng
Shiying Li
Hongzan Sun
Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy
Journal of Nanobiotechnology
MR/PA imaging
Ternary metallic nanoparticles
Sensitized apoptosis
Photothermal/radiation therapy
Sensitized ferroptosis
title Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy
title_full Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy
title_fullStr Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy
title_full_unstemmed Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy
title_short Mild photothermal/radiation therapy potentiates ferroptosis effect for ablation of breast cancer via MRI/PA imaging guided all-in-one strategy
title_sort mild photothermal radiation therapy potentiates ferroptosis effect for ablation of breast cancer via mri pa imaging guided all in one strategy
topic MR/PA imaging
Ternary metallic nanoparticles
Sensitized apoptosis
Photothermal/radiation therapy
Sensitized ferroptosis
url https://doi.org/10.1186/s12951-023-01910-6
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