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Cited by 24Nanoplatforms for cancer theranosticsPhotodynamic Therapy Research StudiesRadiation Therapy and Dosimetry

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MnO2 coated multi-layer nanoplatform for enhanced sonodynamic therapy and MR imaging of breast cancer

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Xu, Yan, Tan, Wanlin, Chen, Mingyu, Chen, Sijie, Tang, Kui, Liao, Haiqin, Niu, Chengcheng·2022·Frontiers in Bioengineering and Biotechnology
DOI 10.3389/fbioe.2022.955127PMC PMC9627152
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Abstract

Sonodynamic therapy (SDT) is a promising new anti-tumor therapy that inhibits tumor growth by ultrasound activation of sonosensitizers to produce reactive oxygen species (ROS). However, the problems of hypoxia in the microenvironment within solid tumors and the effectiveness of SDT will decrease due to the little accumulation of sonosensitizers at the tumor site, as well as tumor cell tolerance, have limited the development of SDT. To overcome these problems, a core-shell structured nanoparticle (IR780/PLGA@MnO 2 NPs) loaded with IR780 and manganese dioxide (MnO 2 ) was developed as a nanocarrier to transport the sonosensitizer IR780 and the generated oxygen into the tumor tissue. The MnO 2 shell layer of IR780/PLGA@MnO 2 NPs can prevent the premature release of IR780 in the blood and also it can react with acidic and high H 2 O 2 , the generated oxygen can relieve tumor tissue hypoxia, and the generated Mn can enhance magnetic resonance imaging (MRI) signal intensity by acting as a contrast agent for MRI. More importantly, the released IR780 can produce ROS to kill tumor cells under ultrasound excitation. This PH-responsive and H 2 O 2 -triggered SDT based on the IR780/PLGA@MnO 2 NPs is an effective platform to inhibit tumor growth with negligible systemic toxicity. This work develops a multifunctional therapeutic integrated nanoplatform for breast cancer treatment, which is expected to be used in the clinic.

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FIGURE 1 Schematic illustration of the IR780/PLGA@MnO2 NPs used for enhance SDT and MR imaging of breast cancer.
FIGURE 1 Schematic illustration of the IR780/PLGA@MnO2 NPs used for enhance SDT and MR imaging of breast cancer.CC BY · PubMed Central
FIGURE 2 Characterization of IR780/PLGA@MnO2 NPs. (A–C) The TEM images of IR780/PLGA@MnO2 NPs (A) and IR780/PLGA NPs (B), the white arrow indicated the MnO2 on the shell of IR780/PLGA@MnO2 NPs (C). (D) The elemental mapping of Mn and O of IR780/PLGA@MnO 2. (E) Size and (F) zeta potential of IR780/PLGA NPs with and without MnO2 shell. (G) UV−vis−NIR absorption spectra of IR780/PLGA NPs, PLGA NPs, IR780/PLGA@MnO2 NPs. (H) Size distributions of IR780/PLGA@MnO2 NPs in PBS and 10% FBS for 7 days.
FIGURE 2 Characterization of IR780/PLGA@MnO2 NPs. (A–C) The TEM images of IR780/PLGA@MnO2 NPs (A) and IR780/PLGA NPs (B), the white arrow indicated the MnO2 on the shell of IR780/PLGA@MnO2 NPs (C). (D) The elemental mapping of Mn and O of IR780/PLGA@MnO 2. (E) Size and (F) zeta potential of IR780/PLGA NPs with and without MnO2 shell. (G) UV−vis−NIR absorption spectra of IR780/PLGA NPs, PLGA NPs, IR780/PLGA@MnO2 NPs. (H) Size distributions of IR780/PLGA@MnO2 NPs in PBS and 10% FBS for 7 days.CC BY · PubMed Central
FIGURE 3 (A) The IR780 release from IR780/PLGA@MnO2 NPs at pH 7.4 or 5.5 with or without H2O2. (B) Oxygen content of IR780/PLGA MnO2 NPs with H2O2. (C) Time-dependent 1O2 generation of IR780/PLGA MnO2 NPs irradiated by US (1 MHz, 1.0 W/cm2). (D) Time-dependent fluorescence increasement of SOSG with different treatments under ultrasound irradiation.
FIGURE 3 (A) The IR780 release from IR780/PLGA@MnO2 NPs at pH 7.4 or 5.5 with or without H2O2. (B) Oxygen content of IR780/PLGA MnO2 NPs with H2O2. (C) Time-dependent 1O2 generation of IR780/PLGA MnO2 NPs irradiated by US (1 MHz, 1.0 W/cm2). (D) Time-dependent fluorescence increasement of SOSG with different treatments under ultrasound irradiation.CC BY · PubMed Central
FIGURE 4 (A) Fluorescence images of 4T1 cells incubated with IR780/PLGA@MnO2 NPs for 0, 4, 12 and 24 h (scale bar: 20 μm). (B) Fluorescence microscope images of DCFH-DA stained 4T1 cells subjected to different treatments: (Hussain and Nguyen, 2014) PBS, (Wells, 2006) US, (Wu et al., 2005) IR780/PLGA NPs, (Ahmadi et al., 2020) IR780/PLGA@MnO2 NPs, (Qian et al., 2016) IR780/PLGA NPs + US, (Wood and Sehgal, 2015) IR780/PLGA@MnO2 + US (scale bar, 50 µm).
FIGURE 4 (A) Fluorescence images of 4T1 cells incubated with IR780/PLGA@MnO2 NPs for 0, 4, 12 and 24 h (scale bar: 20 μm). (B) Fluorescence microscope images of DCFH-DA stained 4T1 cells subjected to different treatments: (Hussain and Nguyen, 2014) PBS, (Wells, 2006) US, (Wu et al., 2005) IR780/PLGA NPs, (Ahmadi et al., 2020) IR780/PLGA@MnO2 NPs, (Qian et al., 2016) IR780/PLGA NPs + US, (Wood and Sehgal, 2015) IR780/PLGA@MnO2 + US (scale bar, 50 µm).CC BY · PubMed Central
FIGURE 5 (A,B) Cell viability of 4T1 and MCF-7 cells incubated with different concentrations of IR780/PLGA@MnO2 NPs under normoxia environment (A) and hypoxia environment (B). (C,D) Cell viability of 4T1 and MCF-7 cells under different treatments: (I) PBS, (II) US, (III) IR780/PLGA NPs, (IV) IR780/PLGA@MnO2, (V) IR780/PLGA NPs + US, (VI) IR780/PLGA@MnO2 + US) in normoxia environment (C) and hypoxia environment (D). (E) Fluorescence microscope images of DAPI and PI co-stained 4T1 cells after various treatments: (Hussain and Nguyen, 2014) PBS, (Wells, 2006) US only, (Wu et al., 2005) IR780/PLGA NPs, (Ahmadi et al., 2020) IR780/PLGA@MnO2 NPs, (Qian et al., 2016) IR780/PLGA NPs + US, (Wood and Sehgal, 2015) IR780/PLGA@MnO2 + US (scale bar, 100 µm). (*p < 0.05, compared with the control group).
FIGURE 5 (A,B) Cell viability of 4T1 and MCF-7 cells incubated with different concentrations of IR780/PLGA@MnO2 NPs under normoxia environment (A) and hypoxia environment (B). (C,D) Cell viability of 4T1 and MCF-7 cells under different treatments: (I) PBS, (II) US, (III) IR780/PLGA NPs, (IV) IR780/PLGA@MnO2, (V) IR780/PLGA NPs + US, (VI) IR780/PLGA@MnO2 + US) in normoxia environment (C) and hypoxia environment (D). (E) Fluorescence microscope images of DAPI and PI co-stained 4T1 cells after various treatments: (Hussain and Nguyen, 2014) PBS, (Wells, 2006) US only, (Wu et al., 2005) IR780/PLGA NPs, (Ahmadi et al., 2020) IR780/PLGA@MnO2 NPs, (Qian et al., 2016) IR780/PLGA NPs + US, (Wood and Sehgal, 2015) IR780/PLGA@MnO2 + US (scale bar, 100 µm). (*p < 0.05, compared with the control group).CC BY · PubMed Central
FIGURE 6 (A) Biodistribution of IR780/PLGA@MnO2 NPs in tumor-bearing mice at different time points by in vivo fluorescent imaging. (B,C) Fluorescence imaging of major organs and tumor at 8 h after injection of the IR780/PLGA@MnO2 NPs. (D) H&E-staining images of major organs collected from the IR780/PLGA@MnO2 NPs and saline groups.
FIGURE 6 (A) Biodistribution of IR780/PLGA@MnO2 NPs in tumor-bearing mice at different time points by in vivo fluorescent imaging. (B,C) Fluorescence imaging of major organs and tumor at 8 h after injection of the IR780/PLGA@MnO2 NPs. (D) H&E-staining images of major organs collected from the IR780/PLGA@MnO2 NPs and saline groups.CC BY · PubMed Central
FIGURE 7 (A) T1-weighted MR images of IR780/PLGA@MnO2 NPs suspensions at different Mn concentrations and pH values with H2O2. (B) The longitudinal (r1) relaxation rate vs. the concentration of the IR780/PLGA@MnO2 NPs (in terms of Mn). (C) In vivo MR images of mice bearing implanted 4T1 cancer before and after 24 h of the intravenous injection of IR780/PLGA@MnO2 NPs.
FIGURE 7 (A) T1-weighted MR images of IR780/PLGA@MnO2 NPs suspensions at different Mn concentrations and pH values with H2O2. (B) The longitudinal (r1) relaxation rate vs. the concentration of the IR780/PLGA@MnO2 NPs (in terms of Mn). (C) In vivo MR images of mice bearing implanted 4T1 cancer before and after 24 h of the intravenous injection of IR780/PLGA@MnO2 NPs.CC BY · PubMed Central
FIGURE 8 Representative immunofluorescence images of tumor slices stained by the HIF-1α under different treatments (scale bar, 200 µm).
FIGURE 8 Representative immunofluorescence images of tumor slices stained by the HIF-1α under different treatments (scale bar, 200 µm).CC BY · PubMed Central
FIGURE 9 (A) The relative tumor growth curves and (B) photographs of tumors during the various treatments after 14 days. (C) The weight growth curves of different groups of mice after various treatments. (D) Microscopy images of TUNEL and PCNA assays of stained tumor tissues at different treatments: (Hussain and Nguyen, 2014) Saline, (Wells, 2006) US, (Wu et al., 2005) IR780/PLGA NPs, (Ahmadi et al., 2020) IR780/PLGA@MnO2NPs, (Qian et al., 2016) IR780/PLGA NPs + US, (Wood and Sehgal, 2015) IR780/PLGA@MnO2 NPs + US (scale bar, 200 µm). (E) The relative quantification of TUNEL and (F) PCNA after different treatments. (*p < 0.05).
FIGURE 9 (A) The relative tumor growth curves and (B) photographs of tumors during the various treatments after 14 days. (C) The weight growth curves of different groups of mice after various treatments. (D) Microscopy images of TUNEL and PCNA assays of stained tumor tissues at different treatments: (Hussain and Nguyen, 2014) Saline, (Wells, 2006) US, (Wu et al., 2005) IR780/PLGA NPs, (Ahmadi et al., 2020) IR780/PLGA@MnO2NPs, (Qian et al., 2016) IR780/PLGA NPs + US, (Wood and Sehgal, 2015) IR780/PLGA@MnO2 NPs + US (scale bar, 200 µm). (E) The relative quantification of TUNEL and (F) PCNA after different treatments. (*p < 0.05).CC BY · PubMed Central

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Citations

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Metadata

Authors
Xu, Y., Tan, W., Chen, M., Chen, S., Tang, K., Liao, H., & Niu, C.
Affiliations
Central South University (CN)
Corresponding author
Niu, Chengcheng
ORCID
Venue
Frontiers in Bioengineering and Biotechnology
Publisher
Frontiers Media SA
Published
2022-10-19
Volume
10
Pages
955127-955127
ISSN
2296-4185 (ISSN-L)
DOI
10.3389/fbioe.2022.955127
PMC
PMC9627152
OpenAlex
W4306842424
Cited by
24
References
1
Citations by year
2026: 11 · 2025: 5 · 2024: 5 · 2023: 3
FWCI
0.94
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Bioengineering and Biotechnology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China
  • Science and Technology Program of Hunan Province
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Photodynamic Therapy Research Studies
  • Physical Sciences › Physics and Astronomy › Radiation › Radiation Therapy and Dosimetry
Keywords
sonodynamic therapy, breast cancer, IR780, manganese dioxide, PLGA nanoparticles, core-shell nanoparticles, tumor hypoxia, reactive oxygen species, pH-responsive drug release, MRI contrast agents

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