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Silicane Derivative Increases Doxorubicin Efficacy in an Ovarian Carcinoma Mouse Model: Fighting Drug Resistance

  • Michaela Fojtů
    Michaela Fojtů
    Center for Advanced Functional Nanorobots, Department of Inorganic Chemistry, Faculty of Chemical Technology, University of Chemistry and Technology in Prague, Technická 5, Prague 16628, Czech Republic
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
  • Jan Balvan
    Jan Balvan
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    More by Jan Balvan
  • Tomáš Vičar
    Tomáš Vičar
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
  • Hana Holcová Polanská
    Hana Holcová Polanská
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
  • Barbora Peltanová
    Barbora Peltanová
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
  • Stanislava Matějková
    Stanislava Matějková
    Institute of Organic Chemistry and Biochemistry ASCR, v.v.i. Flemingovo nam. 2, Prague 166 10 6, Czech Republic
  • Martina Raudenská
    Martina Raudenská
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
  • Jiří Šturala
    Jiří Šturala
    Department of Inorganic Chemistry, Faculty of Chemical Technology, University of Chemistry and Technology Prague, Technická 5, Prague 16628, Czech Republic
  • Paula Mayorga-Burrezo
    Paula Mayorga-Burrezo
    Future Energy and Innovation Laboratory, Central European Institute of Technology, Brno University of Technology, Purkyňova 656/123, Brno 61600, Czech Republic
  • Michal Masařík
    Michal Masařík
    Center for Advanced Functional Nanorobots, Department of Inorganic Chemistry, Faculty of Chemical Technology, University of Chemistry and Technology in Prague, Technická 5, Prague 16628, Czech Republic
    Department of Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic
    BIOCEV, First Faculty of Medicine, Charles University, Průmyslová 595, 252 50 Vestec, Czech Republic
  • , and 
  • Martin Pumera*
    Martin Pumera
    Center for Advanced Functional Nanorobots, Department of Inorganic Chemistry, Faculty of Chemical Technology, University of Chemistry and Technology in Prague, Technická 5, Prague 16628, Czech Republic
    Future Energy and Innovation Laboratory, Central European Institute of Technology, Brno University of Technology, Purkyňova 656/123, Brno 61600, Czech Republic
    Department of Food Technology, Mendel University in Brno, Zemedelska 1, CZ-613 00 Brno, Czech Republic
    Department of Chemical and Biomolecular Engineering, Yonsei University, 50 Yonsei-ro, Seoaemun-gu, Seoul 03722, South Korea
    Department of Medical Research, China Medical University Hospital, China Medical University, No. 91 Hsueh-Shih Road, Taichung 40402, Taiwan
    *Email: [email protected]
Cite this: ACS Appl. Mater. Interfaces 2021, 13, 27, 31355–31370
Publication Date (Web):July 4, 2021
https://doi.org/10.1021/acsami.0c20458
Copyright © 2021 American Chemical Society

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    Abstract

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    The development of cancer resistance continues to represent a bottleneck of cancer therapy. It is one of the leading factors preventing drugs to exhibit their full therapeutic potential. Consequently, it reduces the efficacy of anticancer therapy and causes the survival rate of therapy-resistant patients to be far from satisfactory. Here, an emerging strategy for overcoming drug resistance is proposed employing a novel two-dimensional (2D) nanomaterial polysiloxane (PSX). We have reported on the synthesis of PSX nanosheets (PSX NSs) and proved that they have favorable properties for biomedical applications. PSX NSs evinced unprecedented cytocompatibility up to the concentration of 300 μg/mL, while inducing very low level of red blood cell hemolysis and were found to be highly effective for anticancer drug binding. PSX NSs enhanced the efficacy of the anticancer drug doxorubicin (DOX) by around 27.8–43.4% on average and, interestingly, were found to be especially effective in the therapy of drug-resistant tumors, improving the effectiveness of up to 52%. Fluorescence microscopy revealed improved retention of DOX within the drug-resistant cells when bound on PSX NSs. DOX bound on the surface of PSX NSs, i.e., PSX@DOX, improved, in general, the DOX cytotoxicity in vitro. More importantly, PSX@DOX reduced the growth of DOX-resistant tumors in vivo with 3.5 times better average efficiency than the free drug. Altogether, this paper represents an introduction of a new 2D nanomaterial derived from silicane and pioneers its biomedical application. As advances in the field of material synthesis are rapidly progressing, novel 2D nanomaterials with improved properties are being synthesized and await thorough exploration. Our findings further provide a better understanding of the mechanisms involved in the cancer resistance and can promote the development of a precise cancer therapy.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.0c20458.

    • Colloidal stability of PSX NSs; average PSX NSs size in PBS, cell culture media, acidic environment, and reducing environment after incubation at room temperature for 4, 24, and 48 h; material composition and characterization of PSX NSs; relative viability of ovarian and breast cancer cell lines after 48 h treatment with PSX NSs; viability of the selected cell lines after PSX NSs exposure for 48 h; comparison of the half-maximal inhibition concentration values (IC50) and 80% inhibitory concentration (IC80); BE of PSX NSs in culture media showing percentage of the surface-bound DOX on the nanomaterial after the 24 and 48 h incubation; FTIR spectra of PSX NSs in PBS, PSX NSs incubated with DOX for 24 and 48 h; photographs of samples for FTIR analysis; PSX NSs in PBS and PSX NSs incubated with DOX for 24 and 48 h; relative cell viability of the A2780, A2780/ADR, MCF-7, and MDA-MB-231 cells after administration of DOX and PSX@DOX for 48 h; potentiation of the DOX anticancer effect by PSX NSs, 48 h after the initiation of treatment; and colocalization experiment of PSX NSs and PSX@DOX in the A2780/ADR cells carried out by merging of amplitude and phase images 0, 0.5, 2, 12, and 24 h after nanomaterial administration (PDF)

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    Cited By

    This article is cited by 6 publications.

    1. Hau-Lun Huang, Kuo-Wei Chen, Hsiao-Wei Liao, Ling-Yu Wang, Shin-Lei Peng, Chih-Ho Lai, Yu-Hsin Lin. Nanoparticles for Augmenting Therapeutic Potential and Alleviating the Effect of Di(2-ethylhexyl) Phthalate on Gastric Cancer. ACS Applied Materials & Interfaces 2024, 16 (15) , 18285-18299. https://doi.org/10.1021/acsami.3c15976
    2. Jian Meng, Lei Wang, Bocheng Zou, Shilei Ren, Zirui Yan, Jinfang Gao, Ruiping Zhang. Fluorescent-Based Nanoplatform with Real-Time Quantification of Drug Release. ACS Applied Polymer Materials 2023, 5 (2) , 1539-1544. https://doi.org/10.1021/acsapm.2c02025
    3. Miaojuan Qiu, Junzong Chen, Xiuyu Huang, Binbin Li, Shiqiang Zhang, Peng Liu, Qiang Wang, Zhi Rong Qian, Yihang Pan, Yu Chen, Jing Zhao. Engineering Chemotherapeutic-Augmented Calcium Phosphate Nanoparticles for Treatment of Intraperitoneal Disseminated Ovarian Cancer. ACS Applied Materials & Interfaces 2022, 14 (19) , 21954-21965. https://doi.org/10.1021/acsami.2c02552
    4. Xiangyi Kong, Peng Gao, Jing Wang, Yi Fang, Kuo Chu Hwang. Advances of medical nanorobots for future cancer treatments. Journal of Hematology & Oncology 2023, 16 (1) https://doi.org/10.1186/s13045-023-01463-z
    5. I. V. Kosarev, A. A. Kistanov, R. I. Babicheva, E. A. Korznikova, J. A. Baimova, S. V. Dmitriev. Topological defects in silicene. Europhysics Letters 2023, 141 (6) , 66001. https://doi.org/10.1209/0295-5075/acbfda
    6. Seid Reza Falsafi, Yong Wang, Tolulope Joshua Ashaolu, Minaxi Sharma, Shruti Rawal, Kaushika Patel, Gholamreza Askari, Shaghayegh Haghjooy Javanmard, Hadis Rostamabadi. Biopolymer Nanovehicles for Oral Delivery of Natural Anticancer Agents. Advanced Functional Materials 2023, 33 (4) https://doi.org/10.1002/adfm.202209419

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