journal article
Open Access
Oct 05, 2023
Combined Effect of Plasma-Activated Water and Topotecan in Glioblastoma Cells
Abstract
The increase in cancer diagnoses and cancer deaths, severe side effects of existing treatments and resistance to traditional treatments have generated a need for new anticancer treatments. Glioblastoma multiforme (GBM) is the most common, malignant and aggressive brain cancer. Despite many innovations regarding GBM treatment, the final outcome is still very poor, making it necessary to develop new therapeutic approaches. Cold atmospheric plasma (CAP) as well as plasma-activated liquids (PAL) are being studied as new possible approaches against cancer. The anticancer activity of PAL such as “plasma-activated water” (PAW) is dependent on the reactive chemical compounds present in the solution. Possible combinatory effects with conventional therapies, such as chemotherapeutics, may expand the potential of PAL for cancer treatment. We aim to explore the therapeutic properties of a combination of PAW and topotecan (TPT), an antineoplastic agent with major cytotoxic effects during the S phase of the cell cycle, on a GBM cancer cell line (U-251mg). Combined treatments with PAW and TPT showed a reduction in the metabolic activity and cell mass, an increase in apoptotic cell death and a reduction in the long-term survival. Single applications of PAW+TPT treatments showed a cytotoxic effect in the short term and an antiproliferative effect in the long term, warranting future exploration of combining PAW with chemotherapeutic agents as new therapeutic approaches.
Topics
No keywords indexed for this article. Browse by subject →
References
48
[1]
Lapointe "Primary brain tumours in adults" Lancet (2018) 10.1016/s0140-6736(18)30990-5
[2]
Batash "Glioblastoma Multiforme, Diagnosis and Treatment; Recent Literature Review" Curr. Med. Chem. (2017) 10.2174/0929867324666170516123206
[3]
Bi "Altered cellular metabolism in gliomas—An emerging landscape of actionable co-dependency targets" Nat. Rev. Cancer (2020) 10.1038/s41568-019-0226-5
[4]
Wanigasekara "Plasma induced reactive oxygen species-dependent cytotoxicity in glioblastoma 3D tumourspheres" Plasma Process. Polym. (2022) 10.1002/ppap.202100157
[5]
Nieland "Advances in local therapy for glioblastoma—Taking the fight to the tumour" Nat. Rev. Neurol. (2022) 10.1038/s41582-022-00621-0
[6]
Mariappan "Trends and challenges in modeling glioma using 3D human brain organoids" Cell Death Differ. (2021) 10.1038/s41418-020-00679-7
[7]
Rezaei, S., Assaran Darban, R., Javid, H., and Hashemy, S.I. (2022). The Therapeutic Potential of Aprepitant in Glioblastoma Cancer Cells through Redox Modification. Biomed Res. Int., 2022.
10.1155/2022/8540403
[8]
Rubinstein "Controlling the release rate of topotecan from PLGA spheres and increasing its cytotoxicity towards glioblastoma cells by co-loading with calcium chloride" Int. J. Pharm. (2021) 10.1016/j.ijpharm.2021.120616
[9]
Neira "Validation of an effective implantable pump-infusion system for chronic convection-enhanced delivery of intracerebral topotecan in a large animal model" J. Neurosurg. (2021)
[10]
Aghi "Convection-enhanced drug delivery for glioblastoma: A review" J Neurooncol. (2021) 10.1007/s11060-020-03408-9
[11]
Joslin "Aqueous plasma pharmacy: Preparation methods, chemistry, and therapeutic applications" Plasma Med. (2016) 10.1615/plasmamed.2016018618
[12]
Sersenová, D., Machala, Z., Repiská, V., and Gbelcová, H. (2021). Selective apoptotic effect of plasma activated liquids on human cancer cell lines. Molecules, 26.
10.3390/molecules26144254
[13]
Achieving reactive species specificity within plasma‐activated water through selective generation using air spark and glow discharges
Peng Lu, Daniela Boehm, Paula Bourke et al.
Plasma Processes and Polymers
2017
10.1002/ppap.201600207
[14]
Lu "Controlled cytotoxicity of plasma treated water formulated by open-air hybrid mode discharge" Appl. Phys. Lett. (2017) 10.1063/1.4990525
[15]
Chen, Z., Simonyan, H., Cheng, X., Gjika, E., Lin, L., Canady, J., Sherman, J.H., Young, C., and Keidar, M. (2017). A novel micro cold atmospheric plasma device for glioblastoma both in vitro and in vivo. Cancers, 9.
10.3390/cancers9060061
[16]
Volotskova "Targeting the cancer cell cycle by cold atmospheric plasma" Sci. Rep. (2012) 10.1038/srep00636
[17]
Ng "Characterization of an atmospheric pressure air plasma device under different modes of operation and their impact on the liquid chemistry" J. Appl. Phys. (2021) 10.1063/5.0039171
[18]
Tsoukou, E., Delit, M., Treint, L., Bourke, P., and Boehm, D. (2021). Distinct chemistries define the diverse biological effects of plasma activated water generated with spark and glow plasma discharges. Appl. Sci., 11.
10.3390/app11031178
[19]
Boehm "Cytotoxic and mutagenic potential of solutions exposed to cold atmospheric plasma" Sci. Rep. (2016) 10.1038/srep21464
[20]
Bijnsdorp "Chapter 34 Analysis of Drug Interactions" Cancer Cell Culture Methods and Protocols (2011) 10.1007/978-1-61779-080-5_34
[21]
Laranjo "Plasma activated media and direct exposition can selectively ablate retinoblastoma cells" Free Radic. Biol. Med. (2021) 10.1016/j.freeradbiomed.2021.05.027
[22]
Dubey "Emerging innovations in cold plasma therapy against cancer: A paradigm shift" Drug Discov. Today (2022) 10.1016/j.drudis.2022.05.014
[23]
Dubuc "Use of cold-atmospheric plasma in oncology: A concise systematic review" Ther. Adv. Med. Oncol. (2018) 10.1177/1758835918786475
[24]
Almeida "Cold Atmospheric Plasma as an Adjunct to Immunotherapy for Glioblastoma Multiforme" World Neurosurg. (2019) 10.1016/j.wneu.2019.06.209
[25]
Murillo, D., Huergo, C., Gallego, B., Rodríguez, R., and Tornín, J. (2023). Exploring the Use of Cold Atmospheric Plasma to Overcome Drug Resistance in Cancer. Biomedicines, 11.
10.3390/biomedicines11010208
[26]
Lee "Anticancer Activity of Liquid Treated with Microwave Plasma-Generated Gas through Macrophage Activation" Oxidative Med. Cell. Longev. (2020) 10.1155/2020/2946820
[27]
Schmidt "ROS from Physical Plasmas: Redox Chemistry for Biomedical Therapy" Oxidative Med. Cell. Longev. (2019)
[28]
Min "Therapeutic Effects of Cold Atmospheric Plasma on Solid Tumor" Front. Med. (2022) 10.3389/fmed.2022.884887
[29]
Motaln, H., Recek, N., and Rogelj, B. (2021). Intracellular responses triggered by cold atmospheric plasma and plasma-activated media in cancer cells. Molecules, 26.
10.3390/molecules26051336
[30]
Solé-Martí, X., Espona-Noguera, A., Ginebra, M.P., and Canal, C. (2021). Plasma-conditioned liquids as anticancer therapies In Vivo: Current state and future directions. Cancers, 13.
10.3390/cancers13030452
[31]
Molotkov, A., Carberry, P., Dolan, M.A., Joseph, S., Idumonyi, S., Oya, S., Castrillon, J., Konofagou, E.E., Doubrovin, M., and Lesser, G.J. (2021). Real-time positron emission tomography evaluation of topotecan brain kinetics after ultrasound-mediated blood–brain barrier permeability. Pharmaceutics, 13.
10.3390/pharmaceutics13030405
[32]
Hedaya "Comparative brain tissue distribution of camptothecin and topotecan in the rat" Cancer Chemother. Pharmacol. (1999) 10.1007/s002800050908
[33]
Bruce "Regression of Recurrent Malignant Gliomas with Convection-Enhanced Delivery of Topotecan" Neurosurgery (2011) 10.1227/neu.0b013e3182233e24
[34]
Lorusso "Topotecan in the treatment of brain metastases. A phase II study of GOIM (Gruppo Oncologico dell’Italia Meridionale)" Anticancer Res. (2006)
[35]
Spinazzi "Chronic convection-enhanced delivery of topotecan for patients with recurrent glioblastoma: A first-in-patient, single-centre, single-arm, phase 1b trial" Lancet Oncol. (2022) 10.1016/s1470-2045(22)00599-x
[36]
Upadhyayula, P.S., Spinazzi, E.F., Argenziano, M.G., Canoll, P., and Bruce, J.N. (2021). Convection enhanced delivery of topotecan for gliomas: A single-center experience. Pharmaceutics, 13.
10.3390/pharmaceutics13010039
[37]
Bigner "Heterogeneity of Genotypic and Phenotypic Characteristics of Fifteen Permanent Cell Lines Derived from Human Gliomas" J. Neuropathol. Exoerimental Neurol. (1981) 10.1097/00005072-198105000-00001
[38]
Belot "Molecular Characterization of Cell Substratum Attachments in Human Glial Tumors Relates to Prognostic Features" Glia (2001) 10.1002/glia.1124
[39]
Ke "Linking differential radiation responses to glioma heterogeneity" Oncotarget (2014) 10.18632/oncotarget.1823
[40]
Alshammari, M.K., Alghazwni, M.K., Alharbi, A.S., Alqurashi, G.G., Kamal, M., Alnufaie, S.R., Alshammari, S.S., Alshehri, B.A., Tayeb, R.H., and Bougeis, R.J.M. (2023). Nanoplatform for the Delivery of Topotecan in the Cancer Milieu: An Appraisal of its Therapeutic Efficacy. Cancers, 15.
10.3390/cancers15010065
[41]
Pommier "Topoisomerase I inhibitors: Camptothecins and beyond" Nat. Rev. Cancer (2006) 10.1038/nrc1977
[42]
Gjika "Combination therapy of cold atmospheric plasma (CAP) with temozolomide in the treatment of U87MG glioblastoma cells" Sci. Rep. (2020) 10.1038/s41598-020-73457-7
[43]
Soni, V., Adhikari, M., Simonyan, H., Lin, L., Sherman, J.H., Young, C.N., and Keidar, M. (2021). In vitro and in vivo enhancement of temozolomide effect in human glioblastoma by non-invasive application of cold atmospheric plasma. Cancers, 13.
10.3390/cancers13174485
[44]
Shaw, P., Kumar, N., Privat-maldonado, A., Smits, E., and Bogaerts, A. (2021). Cold atmospheric plasma increases temozolomide sensitivity of three-dimensional glioblastoma spheroids via oxidative stress-mediated dna damage. Cancers, 13.
10.3390/cancers13081780
[45]
Di Marzo, N., Chisci, E., and Giovannoni, R. (2018). The role of hydrogen peroxide in redox-dependent signaling: Homeostatic and pathological responses in mammalian cells. Cells, 7.
10.3390/cells7100156
[46]
Alves "Role of glioblastoma stem cells in cancer therapeutic resistance: A perspective on antineoplastic agents from natural sources and chemical derivatives" Stem Cell Res. Ther. (2021) 10.1186/s13287-021-02231-x
[47]
Athanasopoulos "Synergistic effect of cold atmospheric pressure plasma and free or liposomal doxorubicin on melanoma cells" Sci. Rep. (2021) 10.1038/s41598-021-94130-7
[48]
Ginebra "Cold atmospheric plasma enhances doxorubicin selectivity in metastasic bone cancer" Free Radic. Biol. Med. (2022) 10.1016/j.freeradbiomed.2022.07.007
Metrics
14
Citations
48
References
Details
- Published
- Oct 05, 2023
- Vol/Issue
- 15(19)
- Pages
- 4858
- License
- View
Authors
Cite This Article
Beatriz Pinheiro Lopes, Liam O’Neill, Paula Bourke, et al. (2023). Combined Effect of Plasma-Activated Water and Topotecan in Glioblastoma Cells. Cancers, 15(19), 4858. https://doi.org/10.3390/cancers15194858
Related
You May Also Like
Epidermal Growth Factor Receptor Cell Proliferation Signaling Pathways
Ping Wee, Zhixiang Wang · 2017
1,666 citations
Breast Cancer—Epidemiology, Risk Factors, Classification, Prognostic Markers, and Current Treatment Strategies—An Updated Review
Sergiusz Łukasiewicz, Marcin Czeczelewski · 2021
1,540 citations
Review of Indications of FDA-Approved Immune Checkpoint Inhibitors per NCCN Guidelines with the Level of Evidence
Raju K. Vaddepally, Prakash Kharel · 2020
1,051 citations
A Comprehensive Review on MAPK: A Promising Therapeutic Target in Cancer
Cornelia Braicu, Mihail Buse · 2019
820 citations
A Review of Colorectal Cancer in Terms of Epidemiology, Risk Factors, Development, Symptoms and Diagnosis
Tomasz Sawicki, Monika Ruszkowska · 2021
756 citations