Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression

Background: Acoustic cavitation is a foundational mechanism in ultrasound therapy, primarily through inertial cavitation resulting from microbubble collapse. Sonodynamic therapy, with inertial acoustic cavitation threshold and low-dose radiation in the presence of sensitizers, may provide significan...

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Main Authors: Ali Neshastehriz, Zeinab Hormozi-Moghaddam, Zahra Abedi Kichi, Seyedeh Mona Taheri, Seyed Mohammad Amini, Amir Aghaei
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Photodiagnosis and Photodynamic Therapy
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Online Access:http://www.sciencedirect.com/science/article/pii/S1572100024004691
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author Ali Neshastehriz
Zeinab Hormozi-Moghaddam
Zahra Abedi Kichi
Seyedeh Mona Taheri
Seyed Mohammad Amini
Amir Aghaei
author_facet Ali Neshastehriz
Zeinab Hormozi-Moghaddam
Zahra Abedi Kichi
Seyedeh Mona Taheri
Seyed Mohammad Amini
Amir Aghaei
author_sort Ali Neshastehriz
collection DOAJ
description Background: Acoustic cavitation is a foundational mechanism in ultrasound therapy, primarily through inertial cavitation resulting from microbubble collapse. Sonodynamic therapy, with inertial acoustic cavitation threshold and low-dose radiation in the presence of sensitizers, may provide significant effects for cancer treatment, potentially overcoming resistance encountered with single therapies. Methods: MCF7 breast cancer cells were subjected to sonodynamic therapy either alone or combined with ionizing radiation, gold nanoparticles coated with apigenin, and methylene blue. Several parameters were evaluated, including reactive oxygen species (ROS) generation and colonization. Additionally, the investigation included assessing the long non-coding RNA (lncRNA) PTV1 with miRNA1204 and related genes using Real-Time PCR. Results: Sonodynamic therapy at a mechanical index of 0.31 as acoustic cavitation threshold increased intracellular ROS. Combining sonodynamic therapy and 2 Gy X-ray radiation with methylene blue and gold nanoparticles coated with apigenin significantly decreased plating efficiency (4.44±1.69), and survival fraction (2.75±1.98) compared with control (Ctrl.) (98.77±4.49) and (97.59± 2.94), respectively. This was associated with a marked increase in ROS with a mean fluorescence intensity of 20,576.2 ± 4.6 (>4.5 times). The combined treatment also increased p53 expression and decreased the expression of PVT1, miR-1204, and related genes. Conclusion: Sonodynamic therapy in inertial acoustic cavitation threshold, combined with ionizing radiation in the presence of biocompatible nanoparticles, could enhance the therapeutic effects on the miR-1204, derived from lncRNA PVT1, that functions as an oncogenic microRNA in breast cancer. This approach has the potential to overcome treatment resistance encountered with single therapies.
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spelling doaj-art-91b5cf9841ef4681bb7aca387874a5cc2025-02-01T04:11:41ZengElsevierPhotodiagnosis and Photodynamic Therapy1572-10002025-02-0151104433Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expressionAli Neshastehriz0Zeinab Hormozi-Moghaddam1Zahra Abedi Kichi2Seyedeh Mona Taheri3Seyed Mohammad Amini4Amir Aghaei5Radiation Biology Research center, Iran University of Medical Sciences (IUMS), Tehran, Iran; Department of Radiation Sciences, Allied Medicine Faculty, Iran University of Medical Sciences, Tehran, IranRadiation Biology Research center, Iran University of Medical Sciences (IUMS), Tehran, Iran; Department of Radiation Sciences, Allied Medicine Faculty, Iran University of Medical Sciences, Tehran, Iran; Corresponding authors.Department of Genetics, Faculty of biological Sciences, Tarbiat Modares University, Tehran, IranDepartment of Radiation Sciences, Allied Medicine Faculty, Iran University of Medical Sciences, Tehran, IranRadiation Biology Research center, Iran University of Medical Sciences (IUMS), Tehran, Iran; Corresponding authors.Department of Radiation Sciences, Allied Medicine Faculty, Iran University of Medical Sciences, Tehran, IranBackground: Acoustic cavitation is a foundational mechanism in ultrasound therapy, primarily through inertial cavitation resulting from microbubble collapse. Sonodynamic therapy, with inertial acoustic cavitation threshold and low-dose radiation in the presence of sensitizers, may provide significant effects for cancer treatment, potentially overcoming resistance encountered with single therapies. Methods: MCF7 breast cancer cells were subjected to sonodynamic therapy either alone or combined with ionizing radiation, gold nanoparticles coated with apigenin, and methylene blue. Several parameters were evaluated, including reactive oxygen species (ROS) generation and colonization. Additionally, the investigation included assessing the long non-coding RNA (lncRNA) PTV1 with miRNA1204 and related genes using Real-Time PCR. Results: Sonodynamic therapy at a mechanical index of 0.31 as acoustic cavitation threshold increased intracellular ROS. Combining sonodynamic therapy and 2 Gy X-ray radiation with methylene blue and gold nanoparticles coated with apigenin significantly decreased plating efficiency (4.44±1.69), and survival fraction (2.75±1.98) compared with control (Ctrl.) (98.77±4.49) and (97.59± 2.94), respectively. This was associated with a marked increase in ROS with a mean fluorescence intensity of 20,576.2 ± 4.6 (>4.5 times). The combined treatment also increased p53 expression and decreased the expression of PVT1, miR-1204, and related genes. Conclusion: Sonodynamic therapy in inertial acoustic cavitation threshold, combined with ionizing radiation in the presence of biocompatible nanoparticles, could enhance the therapeutic effects on the miR-1204, derived from lncRNA PVT1, that functions as an oncogenic microRNA in breast cancer. This approach has the potential to overcome treatment resistance encountered with single therapies.http://www.sciencedirect.com/science/article/pii/S1572100024004691Sonodynamic therapyRadiationReactive oxygen speciesApoptosislncRNA PVT1miR-1204
spellingShingle Ali Neshastehriz
Zeinab Hormozi-Moghaddam
Zahra Abedi Kichi
Seyedeh Mona Taheri
Seyed Mohammad Amini
Amir Aghaei
Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression
Photodiagnosis and Photodynamic Therapy
Sonodynamic therapy
Radiation
Reactive oxygen species
Apoptosis
lncRNA PVT1
miR-1204
title Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression
title_full Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression
title_fullStr Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression
title_full_unstemmed Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression
title_short Overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncRNA PVT1 and miR-1204 expression
title_sort overcoming breast cancer cell treatment resistance by optimizing sonodynamic therapy and radiation sensitizers on lncrna pvt1 and mir 1204 expression
topic Sonodynamic therapy
Radiation
Reactive oxygen species
Apoptosis
lncRNA PVT1
miR-1204
url http://www.sciencedirect.com/science/article/pii/S1572100024004691
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