Plasma-Treated Solutions (PTS) in Cancer Therapy
Abstract
:Simple Summary
Abstract
1. Introduction
2. Terminology
3. In Vitro Experiments of Plasma-Treated Solutions (PTSs) for Cancer Treatment
3.1. Reactive Species in Plasma-Treated Solutions (PTSs)
3.2. Factors Affecting the Anticancer Efficacy of Plasma-Treated Solutions (PTSs)
3.3. Intracellular Molecular Mechanism of Cancer Cell Death Induced by Plasma-Treated Solution (PTS)
3.4. Some Guidelines to Make PTS
3.5. The Storage of Plasma-Treated Solutions (PTSs)
4. In Vivo Experiments of Plasma-Treated Solutions (PTSs) for Cancer Treatment
4.1. The Anticancer Efficacy of Plasma-Treated Solutions (PTSs)
4.2. The Safety of Plasma-Treated Solutions (PTSs)
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2018, 68, 394–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arnér, E.S.; Holmgren, A. The thioredoxin system in cancer. Semin. Cancer Biol. 2006, 16, 420–426. [Google Scholar] [CrossRef]
- Lorenzen, I.; Mullen, L.; Bekeschus, S.; Hanschmann, E.-M. Redox Regulation of Inflammatory Processes Is Enzymatically Controlled. Oxidative Med. Cell. Longev. 2017, 2017, 1–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bansal, A.; Simon, M.C. Glutathione metabolism in cancer progression and treatment resistance. J. Cell Biol. 2018, 217, 2291–2298. [Google Scholar] [CrossRef] [Green Version]
- Laroussi, M. Sterilization of contaminated matter with an atmospheric pressure plasma. IEEE Trans. Plasma Sci. 1996, 24, 1188–1191. [Google Scholar] [CrossRef]
- Laroussi, M. Nonthermal decontamination of biological media by atmospheric-pressure plasmas: Review, analysis, and prospects. IEEE Trans. Plasma Sci. 2002, 30, 1409–1415. [Google Scholar] [CrossRef]
- Isbary, G.; Heinlin, J.; Shimizu, T.; Zimmermann, J.; Morfill, G.; Schmidt, H.-U.; Monetti, R.; Steffes, B.; Bunk, W.; Li, Y.; et al. Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: Results of a randomized controlled trial. Br. J. Dermatol. 2012, 167, 404–410. [Google Scholar] [CrossRef] [PubMed]
- Nosenko, T.; Shimizu, T.; Morfill, G.E. Designing plasmas for chronic wound disinfection. New J. Phys. 2009, 11, 115013. [Google Scholar] [CrossRef] [Green Version]
- Privat-Maldonado, A.; Schmidt, A.; Lin, A.; Weltmann, K.-D.; Wende, K.; Bogaerts, A.; Bekeschus, S. ROS from Physical Plasmas: Redox Chemistry for Biomedical Therapy. Oxidative Med. Cell. Longev. 2019, 2019, 1–29. [Google Scholar] [CrossRef] [Green Version]
- Lu, X.; Naidis, G.; Laroussi, M.; Reuter, S.; Graves, D.; Ostrikov, K. Reactive species in non-equilibrium atmospheric-pressure plasmas: Generation, transport, and biological effects. Phys. Rep. 2016, 630, 1–84. [Google Scholar] [CrossRef] [Green Version]
- Stratmann, B.; Costea, T.-C.; Nolte, C.; Hiller, J.; Schmidt, J.; Reindel, J.; Masur, K.; Motz, W.; Timm, J.; Kerner, W.; et al. Effect of Cold Atmospheric Plasma Therapy vs Standard Therapy Placebo on Wound Healing in Patients with Diabetic Foot Ulcers. JAMA Netw. Open 2020, 3, e2010411. [Google Scholar] [CrossRef] [PubMed]
- Von Woedtke, T.; Schmidt, A.; Bekeschus, S.; Wende, K.; Weltmann, K.-D. Plasma Medicine: A Field of Applied Redox Biology. In Vivo 2019, 33, 1011–1026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fridman, G.; Shereshevsky, A.; Jost, M.M.; Brooks, A.D.; Fridman, A.; Gutsol, A.; Vasilets, V.; Friedman, G. Floating Electrode Dielectric Barrier Discharge Plasma in Air Promoting Apoptotic Behavior in Melanoma Skin Cancer Cell Lines. Plasma Chem. Plasma Process. 2007, 27, 163–176. [Google Scholar] [CrossRef]
- Schlegel, J.; Köritzer, J.; Boxhammer, V. Plasma in cancer treatment. Clin. Plasma Med. 2013, 1, 2–7. [Google Scholar] [CrossRef]
- Barekzi, N.; Laroussi, M. Effects of Low Temperature Plasmas on Cancer Cells. Plasma Process. Polym. 2013, 10, 1039–1050. [Google Scholar] [CrossRef]
- Keidar, M.; Walk, R.M.; Shashurin, A.; Srinivasan, P.; Sandler, A.B.; Dasgupta, S.; Ravi, R.; Guerreropreston, R.; Trink, B. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br. J. Cancer 2011, 105, 1295–1301. [Google Scholar] [CrossRef]
- Vandamme, M.; Robert, E.; Lerondel, S.; Sarron, V.; Ries, D.; Dozias, S.; Sobilo, J.; Gosset, D.; Kieda, C.; Legrain, B.; et al. ROS implication in a new antitumor strategy based on non-thermal plasma. Int. J. Cancer 2012, 130, 2185–2194. [Google Scholar] [CrossRef]
- Semmler, M.L.; Bekeschus, S.; Schäfer, M.; Bernhardt, T.; Fischer, T.; Witzke, K.; Seebauer, C.; Rebl, H.; Grambow, E.; Vollmar, B.; et al. Molecular Mechanisms of the Efficacy of Cold Atmospheric Pressure Plasma (CAP) in Cancer Treatment. Cancers 2020, 12, 269. [Google Scholar] [CrossRef] [Green Version]
- Keidar, M. Plasma Cancer Therapy; Springer: Berlin/Heidelberg, Germany, 2020. [Google Scholar]
- Metelmann, H.-R.; Seebauer, C.; Miller, V.; Fridman, A.; Bauer, G.; Graves, D.B.; Pouvesle, J.-M.; Rutkowski, R.; Schuster, M.; Bekeschus, S.; et al. Clinical experience with cold plasma in the treatment of locally advanced head and neck cancer. Clin. Plasma Med. 2018, 9, 6–13. [Google Scholar] [CrossRef]
- Metelmann, H.-R.; Seebauer, C.; Rutkowski, R.; Schuster, M.; Bekeschus, S.; Metelmann, P. Treating cancer with cold physical plasma: On the way to evidence-based medicine. Contrib. Plasma Phys. 2018, 58, 415–419. [Google Scholar] [CrossRef]
- Bekeschus, S.; Schmidt, A.; Weltmann, K.-D.; Von Woedtke, T. The plasma jet kINPen—A powerful tool for wound healing. Clin. Plasma Med. 2016, 4, 19–28. [Google Scholar] [CrossRef]
- Tanaka, H.; Mizuno, M.; Ishikawa, K.; Nakamura, K.; Kajiyama, H.; Kano, H.; Kikkawa, F.; Hori, M. Plasma-Activated Medium Selectively Kills Glioblastoma Brain Tumor Cells by Down-Regulating a Survival Signaling Molecule, AKT Kinase. Plasma Med. 2011, 1, 265–277. [Google Scholar] [CrossRef] [Green Version]
- Kaushik, N.K.; Ghimire, B.; Li, Y.; Adhikari, M.; Veerana, M.; Kaushik, N.; Jha, N.; Adhikari, B.; Lee, S.-J.; Masur, K.; et al. Biological and medical applications of plasma-activated media, water and solutions. Biol. Chem. 2018, 400, 39–62. [Google Scholar] [CrossRef]
- Wende, K.; von Woedtke, T.; Weltmann, K.D.; Bekeschus, S. Chemistry and biochemistry of cold physical plasma derived reactive species in liquids. Biol. Chem. 2018, 400, 19–38. [Google Scholar] [CrossRef] [PubMed]
- Bauer, G. Intercellular singlet oxygen-mediated bystander signaling triggered by long-lived species of cold atmospheric plasma and plasma-activated medium. Redox Biol. 2019, 26, 101301. [Google Scholar] [CrossRef]
- Freund, E.; Bekeschus, S. Gas plasma-oxidized liquids for cancer treatment: Pre-clinical relevance, immuno-oncology, and clinical obstacles. IEEE Trans. Radiat. Plasma Med. Sci. 2020, 1. [Google Scholar] [CrossRef]
- Hasse, S.; Meder, T.; Freund, E.; Von Woedtke, T.; Bekeschus, S. Plasma Treatment Limits Human Melanoma Spheroid Growth and Metastasis Independent of the Ambient Gas Composition. Cancers 2020, 12, 2570. [Google Scholar] [CrossRef]
- Tanaka, H.; Mizuno, M.; Ishikawa, K.; Takeda, K.; Nakamura, K.; Utsumi, F.; Kajiyama, H.; Kano, H.; Okazaki, Y.; Toyokuni, S.; et al. Plasma medical science for cancer therapy: Toward cancer therapy using Nonthermal Atmospheric Pressure Plasma. IEEE Trans. Plasma Sci. 2014, 42, 3760–3764. [Google Scholar] [CrossRef]
- Yan, D.; Sherman, J.H.; Keidar, M. The application of the cold atmospheric plasma-activated solutions in cancer treatment. Anti-Cancer Agents Med. Chem. 2018, 18, 769–775. [Google Scholar] [CrossRef] [PubMed]
- Yan, D.; Nourmohammadi, N.; Bian, K.; Murad, F.; Sherman, J.H.; Keidar, M. Stabilizing the cold plasma-stimulated medium by regulating medium’s composition. Sci. Rep. 2016, 6, 26016. [Google Scholar] [CrossRef]
- Sato, Y.; Yamada, S.; Takeda, S.; Hattori, N.; Nakamura, K.; Tanaka, H.; Mizuno, M.; Hori, M.; Kodera, Y. Effect of plasma-activated lactated ringer’s solution on pancreatic cancer cells in vitro and in vivo. Ann. Surg. Oncol. 2017, 25, 299–307. [Google Scholar] [CrossRef] [PubMed]
- Verlackt, C.C.W.; Van Boxem, W.; Bogaerts, A. Transport and accumulation of plasma generated species in aqueous solution. Phys. Chem. Chem. Phys. 2018, 20, 6845–6859. [Google Scholar] [CrossRef] [PubMed]
- Bekeschus, S.; Freund, E.; Wende, K.; Gandhirajan, R.K.; Schmidt, A. Hmox1 Upregulation Is a Mutual Marker in Human Tumor Cells Exposed to Physical Plasma-Derived Oxidants. Antioxidants 2018, 7, 151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, D.; Cui, Q.; Xu, Y.; Wang, B.; Tian, M.; Li, Q.; Liu, Z.; Liu, D.; Chen, H.; Kong, M.G. Systemic study on the safety of immuno-deficient nude mice treated by atmospheric plasma-activated water. Plasma Sci. Technol. 2018, 20, 044003. [Google Scholar] [CrossRef] [Green Version]
- Tanaka, H.; Nakamura, K.; Mizuno, M.; Ishikawa, K.; Takeda, K.; Kajiyama, H.; Utsumi, F.; Kikkawa, F.; Hori, M. Non-thermal atmospheric pressure plasma activates lactate in Ringer’s solution for anti-tumor effects. Sci. Rep. 2016, 6, 36282. [Google Scholar] [CrossRef] [Green Version]
- Freund, E.; Liedtke, K.R.; Gebbe, R.; Heidecke, A.K.; Partecke, L.-I.; Bekeschus, S. In Vitro Anticancer Efficacy of Six Different Clinically Approved Types of Liquids Exposed to Physical Plasma. IEEE Trans. Radiat. Plasma Med Sci. 2019, 3, 588–596. [Google Scholar] [CrossRef]
- Wende, K.; Reuter, S.; Von Woedtke, T.; Weltmann, K.-D.; Masur, K. Redox-Based Assay for Assessment of Biological Impact of Plasma Treatment. Plasma Process. Polym. 2014, 11, 655–663. [Google Scholar] [CrossRef]
- Utsumi, F.; Kajiyama, H.; Nakamura, K.; Tanaka, H.; Mizuno, M.; Ishikawa, K.; Kondo, H.; Kano, H.; Hori, M.; Kikkawa, F. Effect of Indirect Nonequilibrium Atmospheric Pressure Plasma on Anti-Proliferative Activity against Chronic Chemo-Resistant Ovarian Cancer Cells In Vitro and In Vivo. PLoS ONE 2013, 8, e81576. [Google Scholar] [CrossRef] [Green Version]
- Freund, E.; Liedtke, K.R.; Van Der Linde, J.; Metelmann, H.-R.; Heidecke, C.-D.; Partecke, L.-I.; Bekeschus, S. Physical plasma-treated saline promotes an immunogenic phenotype in CT26 colon cancer cells in vitro and in vivo. Sci. Rep. 2019, 9, 1–18. [Google Scholar] [CrossRef]
- Adachi, T.; Tanaka, H.; Nonomura, S.; Hara, H.; Kondo, S.-I.; Hori, M. Plasma-activated medium induces A549 cell injury via a spiral apoptotic cascade involving the mitochondrial–nuclear network. Free Radic. Biol. Med. 2015, 79, 28–44. [Google Scholar] [CrossRef]
- Wende, K.; Bekeschus, S.; Schmidt, A.; Jatsch, L.; Hasse, S.; Weltmann, K.D.; Masur, K.; von Woedtke, T. Risk assessment of a cold argon plasma jet in respect to its mutagenicity. Mutat. Res. Genet. Toxicol Environ. Mutagen 2016, 798–799, 48–54. [Google Scholar] [CrossRef]
- Torii, K.; Yamada, S.; Nakamura, K.; Tanaka, H.; Kajiyama, H.; Tanahashi, K.; Iwata, N.; Kanda, M.; Kobayashi, D.; Tanaka, C.; et al. Effectiveness of plasma treatment on gastric cancer cells. Gastric Cancer 2015, 18, 635–643. [Google Scholar] [CrossRef]
- Hattori, N.; Yamada, S.; Torii, K.; Takeda, S.; Nakamura, K.; Tanaka, H.; Kajiyama, H.; Kanda, M.; Fujii, T.; Nakayama, G.; et al. Effectiveness of plasma treatment on pancreatic cancer cells. Int. J. Oncol. 2015, 47, 1655–1662. [Google Scholar] [CrossRef] [Green Version]
- Bekeschus, S.; Käding, A.; Schröder, T.; Wende, K.; Hackbarth, C.; Liedtke, K.R.; Van Der Linde, J.; Von Woedtke, T.; Heidecke, C.-D.; Partecke, L.-I. Cold Physical Plasma-Treated Buffered Saline Solution as Effective Agent Against Pancreatic Cancer Cells. Anti-Cancer Agents Med. Chem. 2018, 18, 824–831. [Google Scholar] [CrossRef]
- Liedtke, K.-R.; Freund, E.; Hermes, M.; Oswald, S.; Heidecke, C.-D.; Partecke, L.-I.; Bekeschus, S. Gas Plasma-Conditioned Ringer’s Lactate Enhances the Cytotoxic Activity of Cisplatin and Gemcitabine in Pancreatic Cancer In Vitro and In Ovo. Cancers 2020, 12, 123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bundscherer, L.; Bekeschus, S.; Tresp, H.; Hasse, S.; Reuter, S.; Weltmann, K.-D.; Lindequist, U.; Masur, K. Viability of Human Blood Leukocytes Compared with Their Respective Cell Lines after Plasma Treatment. Plasma Med. 2013, 3, 71–80. [Google Scholar] [CrossRef]
- Schmidt, A.; Rödder, K.; Hasse, S.; Masur, K.; Toups, L.; Lillig, C.H.; Von Woedtke, T.; Wende, K.; Bekeschus, S. Redox-regulation of activator protein 1 family members in blood cancer cell lines exposed to cold physical plasma-treated medium. Plasma Process. Polym. 2016, 13, 1179–1188. [Google Scholar] [CrossRef]
- Schmidt, A.; Bekeschus, S.; Von Woedtke, T.; Hasse, S. Cell migration and adhesion of a human melanoma cell line is decreased by cold plasma treatment. Clin. Plasma Med. 2015, 3, 24–31. [Google Scholar] [CrossRef]
- Mohades, S.; Barekzi, N.; Laroussi, M. Efficacy of Low Temperature Plasma against SCaBER Cancer Cells. Plasma Process. Polym. 2014, 11, 1150–1155. [Google Scholar] [CrossRef]
- Tornin, J.; Mateu-Sanz, M.; Rodríguez, A.; Labay, C.; Rodríguez, R.; Canal, C. Pyruvate Plays a Main Role in the Antitumoral Selectivity of Cold Atmospheric Plasma in Osteosarcoma. Sci. Rep. 2019, 9, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Biscop, E.; Lin, A.; Van Boxem, W.; Van Loenhout, J.; De Backer, J.; Deben, C.; Dewilde, S.; Smits, E.; Bogaerts, A.A. Influence of Cell Type and Culture Medium on Determining Cancer Selectivity of Cold Atmospheric Plasma Treatment. Cancers 2019, 11, 1287. [Google Scholar] [CrossRef] [Green Version]
- Reuter, S.; Von Woedtke, T.; Weltmann, K.-D. The kINPen—A review on physics and chemistry of the atmospheric pressure plasma jet and its applications. J. Phys. D Appl. Phys. 2018, 51, 233001. [Google Scholar] [CrossRef] [Green Version]
- Bekeschus, S.; Kolata, J.; Winterbourn, C.; Kramer, A.; Turner, R.; Weltmann, K.D.; Bröker, B.; Masur, K. Hydrogen peroxide: A central player in physical plasma-induced oxidative stress in human blood cells. Free Radic. Res. 2014, 48, 542–549. [Google Scholar] [CrossRef]
- Bauer, G. Targeting Protective Catalase of Tumor Cells with Cold Atmospheric Plasma- Activated Medium (PAM). Anti-Cancer Agents Med. Chem. 2018, 18, 784–804. [Google Scholar] [CrossRef]
- Bauer, G. The synergistic effect between hydrogen peroxide and nitrite, two long-lived molecular species from cold atmospheric plasma, triggers tumor cells to induce their own cell death. Redox Biol. 2019, 26, 101291. [Google Scholar] [CrossRef] [PubMed]
- Kurake, N.; Tanaka, H.; Ishikawa, K.; Kondo, T.; Sekine, M.; Nakamura, K.; Kajiyama, H.; Kikkawa, F.; Mizuno, M.; Hori, M. Cell survival of glioblastoma grown in medium containing hydrogen peroxide and/or nitrite, or in plasma-activated medium. Arch. Biochem. Biophys. 2016, 605, 102–108. [Google Scholar] [CrossRef] [PubMed]
- Yan, D.; Cui, H.; Zhu, W.; Nourmohammadi, N.; Milberg, J.; Zhang, L.G.; Sherman, J.H.; Keidar, M. The specific vulnerabilities of cancer cells to the cold atmospheric plasma-stimulated solutions. Sci. Rep. 2017, 7, 4479. [Google Scholar] [CrossRef] [PubMed]
- Kalghatgi, S.; Kelly, C.M.; Cerchar, E.; Torabi, B.; Alekseev, O.; Fridman, A.; Friedman, G.; Azizkhan-Clifford, J. Effects of Non-Thermal Plasma on Mammalian Cells. PLoS ONE 2011, 6, e16270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Furuta, R.; Kurake, N.; Ishikawa, K.; Takeda, K.; Hashizume, H.; Tanaka, H.; Kondo, H.; Sekine, M.; Hori, M. Intracellular responses to reactive oxygen and nitrogen species, and lipid peroxidation in apoptotic cells cultivated in plasma-activated medium. Plasma Process. Polym. 2017, 14, 1700123. [Google Scholar] [CrossRef]
- Winterbourn, C.C. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochim. Biophys. Acta (BBA) Gen. Subj. 2014, 1840, 730–738. [Google Scholar] [CrossRef]
- Kalyanaraman, B.; Darleyusmar, V.M.; Davies, K.J.A.; Dennery, P.A.; Forman, H.J.; Grisham, M.B.; Mann, G.E.; Moore, K.; Roberts, L.J.; Ischiropoulos, H. Measuring reactive oxygen and nitrogen species with fluorescent probes: Challenges and limitations. Free Radic. Biol. Med. 2012, 52, 1–6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tanaka, H.; Mizuno, M.; Katsumata, Y.; Ishikawa, K.; Kondo, H.; Hashizume, H.; Okazaki, Y.; Toyokuni, S.; Nakamura, K.; Yoshikawa, N.; et al. Oxidative stress-dependent and -independent death of glioblastoma cells induced by non-thermal plasma-exposed solutions. Sci. Rep. 2019, 9, 13657. [Google Scholar] [CrossRef] [Green Version]
- Bekeschus, S.; Wende, K.; Hefny, M.M.; Rödder, K.; Jablonowski, H.; Schmidt, A.; Von Woedtke, T.; Weltmann, K.-D.; Benedikt, J. Oxygen atoms are critical in rendering THP-1 leukaemia cells susceptible to cold physical plasma-induced apoptosis. Sci. Rep. 2017, 7, 2791. [Google Scholar] [CrossRef] [Green Version]
- Bekeschus, S.; Wulf, C.P.; Freund, E.; Koensgen, D.; Mustea, A.; Weltmann, K.-D.; Stope, M.B. Plasma treatment of ovarian cancer cells mitigates their immuno-modulatory products active on THP-1 monocytes. Plasma 2018, 1, 201–217. [Google Scholar] [CrossRef] [Green Version]
- Privat-Maldonado, A.; Gorbanev, Y.; Dewilde, S.; Smits, E.; Bogaerts, A. Reduction of human glioblastoma spheroids using cold atmospheric plasma: The combined effect of short- and long-lived reactive species. Cancers 2018, 10, 394. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Masur, K.; Von Behr, M.; Bekeschus, S.; Weltmann, K.-D.; Hackbarth, C.; Heidecke, C.-D.; Von Bernstorff, W.; Von Woedtke, T.; Partecke, L.I. Synergistic inhibition of tumor cell proliferation by cold plasma and gemcitabine. Plasma Process. Polym. 2015, 12, 1377–1382. [Google Scholar] [CrossRef]
- Bekeschus, S.; Masur, K.; Kolata, J.; Wende, K.; Schmidt, A.; Bundscherer, L.; Barton, A.; Kramer, A.; Bröker, B.; Weltmann, K.-D. Human Mononuclear Cell Survival and Proliferation is Modulated by Cold Atmospheric Plasma Jet. Plasma Process. Polym. 2013, 10, 706–713. [Google Scholar] [CrossRef]
- Bekeschus, S.; Scherwietes, L.; Freund, E.; Liedtke, K.R.; Hackbarth, C.; Von Woedtke, T.; Partecke, L.-I. Plasma-treated medium tunes the inflammatory profile in murine bone marrow-derived macrophages. Clin. Plasma Med. 2018, 11, 1–9. [Google Scholar] [CrossRef]
- Yan, D.; Xiao, H.; Zhu, W.; Nourmohammadi, N.; Zhang, L.G.; Bian, K.; Keidar, M. The role of aquaporins in the anti-glioblastoma capacity of the cold plasma-stimulated medium. J. Phys. D Appl. Phys. 2017, 50, 055401. [Google Scholar] [CrossRef]
- Tanaka, H.; Mizuno, M.; Ishikawa, K.; Takeda, K.; Hashizume, H.; Nakamura, K.; Utsumi, F.; Kajiyama, H.; Okazaki, Y.; Toyokuni, S.; et al. Glioblastoma cell lines display different sensitivities to plasma-activated medium. IEEE Trans. Radiat. Plasma Med. Sci. 2017, 2, 99–102. [Google Scholar] [CrossRef]
- Utsumi, F.; Kajiyama, H.; Nakamura, K.; Tanaka, H.; Hori, M.; Kikkawa, F. Selective cytotoxicity of indirect nonequilibrium atmospheric pressure plasma against ovarian clear-cell carcinoma. SpringerPlus 2014, 3, 398. [Google Scholar] [CrossRef] [Green Version]
- Tanaka, H.; Mizuno, M.; Ishikawa, K.; Nakamura, K.; Utsumi, F.; Kajiyama, H.; Kano, H.; Maruyama, S.; Kikkawa, F.; Hori, M. Cell survival and proliferation signaling pathways are downregulated by plasma-activated medium in glioblastoma brain tumor cells. Plasma Med. 2012, 2, 207–220. [Google Scholar] [CrossRef] [Green Version]
- Gandhirajan, R.K.; Rödder, K.; Bodnar, Y.; Pasqual-Melo, G.; Emmert, S.; Griguer, C.E.; Weltmann, K.-D.; Bekeschus, S. Cytochrome C oxidase Inhibition and Cold Plasma-derived Oxidants Synergize in Melanoma Cell Death Induction. Sci. Rep. 2018, 8, 12734. [Google Scholar] [CrossRef]
- Yan, D.; Talbot, A.; Nourmohammadi, N.; Cheng, X.; Canady, J.; Sherman, J.H.; Keidar, M. Principles of using Cold Atmospheric Plasma Stimulated Media for Cancer Treatment. Sci. Rep. 2015, 5, 18339. [Google Scholar] [CrossRef] [Green Version]
- Boehm, D.; Heslin, C.; Cullen, P.J.; Bourke, P. Cytotoxic and mutagenic potential of solutions exposed to cold atmospheric plasma. Sci. Rep. 2016, 6, 21464. [Google Scholar] [CrossRef] [Green Version]
- Girard, P.-M.; Arbabian, A.; Fleury, M.; Bauville, G.; Puech, V.; Dutreix, M.; Sousa, J.S. Synergistic Effect of H2O2 and NO2 in Cell Death Induced by Cold Atmospheric He Plasma. Sci. Rep. 2016, 6, 29098. [Google Scholar] [CrossRef] [Green Version]
- Takeda, S.; Yamada, S.; Hattori, N.; Nakamura, K.; Tanaka, H.; Kajiyama, H.; Kanda, M.; Kobayashi, D.; Tanaka, C.; Fujii, T.; et al. Intraperitoneal Administration of Plasma-Activated Medium: Proposal of a Novel Treatment Option for Peritoneal Metastasis From Gastric Cancer. Ann. Surg. Oncol. 2017, 24, 1188–1194. [Google Scholar] [CrossRef] [PubMed]
- Mohades, S.; Laroussi, M.; Sears, J.; Barekzi, N.; Razavi, H. Evaluation of the effects of a plasma activated medium on cancer cells. Phys. Plasmas 2015, 22, 122001. [Google Scholar] [CrossRef]
- Yan, D.; Sherman, J.H.; Cheng, X.; Ratovitski, E.; Canady, J.; Keidar, M. Controlling plasma stimulated media in cancer treatment application. Appl. Phys. Lett. 2014, 105, 224101. [Google Scholar] [CrossRef] [Green Version]
- Judée, F.; Fongia, C.; Ducommun, B.; Yousfi, M.; Lobjois, V.; Merbahi, N. Short and long time effects of low temperature plasma activated media on 3D multicellular tumor spheroids. Sci. Rep. 2016, 6, 21421. [Google Scholar] [CrossRef]
- Mohades, S.; Barekzi, N.; Razavi, H.; Maruthamuthu, V.; Laroussi, M. Temporal evaluation of the anti-tumor efficiency of plasma-activated media. Plasma Process. Polym. 2016, 13, 1206–1211. [Google Scholar] [CrossRef]
- Van Loenhout, J.; Flieswasser, T.; Boullosa, L.F.; De Waele, J.; Van Audenaerde, J.; Marcq, E.; Jacobs, J.; Lin, A.; Lion, E.; Dewitte, H.; et al. Cold atmospheric plasma-treated PBS eliminates immunosuppressive pancreatic stellate cells and induces immunogenic cell death of pancreatic cancer cells. Cancers 2019, 11, 1597. [Google Scholar] [CrossRef] [Green Version]
- Heusler, T.; Bruno, G.; Bekeschus, S.; Lackmann, J.-W.; Von Woedtke, T.; Wende, K. Can the effect of cold physical plasma-derived oxidants be transported via thiol group oxidation? Clin. Plasma Med. 2019, 14, 100086. [Google Scholar] [CrossRef]
- Van Boxem, W.; Van Der Paal, J.; Gorbanev, Y.; Vanuytsel, S.; Smits, E.; Dewilde, S.; Bogaerts, A. Anti-cancer capacity of plasma-treated PBS: Effect of chemical composition on cancer cell cytotoxicity. Sci. Rep. 2017, 7, 16478. [Google Scholar] [CrossRef] [Green Version]
- Liedtke, K.R.; Bekeschus, S.; Kaeding, A.; Hackbarth, C.; Kuehn, J.-P.; Heidecke, C.-D.; Von Bernstorff, W.; Von Woedtke, T.; Partecke, L.I. Non-thermal plasma-treated solution demonstrates antitumor activity against pancreatic cancer cells in vitro and in vivo. Sci. Rep. 2017, 7, 8319. [Google Scholar] [CrossRef]
- Liedtke, K.R.; Freund, E.; Hackbarth, C.; Heidecke, C.-D.; Partecke, L.-I.; Bekeschus, S. A myeloid and lymphoid infiltrate in murine pancreatic tumors exposed to plasma-treated medium. Clin. Plasma Med. 2018, 11, 10–17. [Google Scholar] [CrossRef]
- Obeid, M.; Tesniere, A.; Ghiringhelli, F.; Fimia, G.M.; Apetoh, L.; Perfettini, J.-L.; Castedo, M.; Mignot, G.; Panaretakis, T.; Casares, N.; et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 2007, 13, 54–61. [Google Scholar] [CrossRef]
- Bekeschus, S.; Clemen, R.; Nießner, F.; Sagwal, S.K.; Freund, E.; Schmidt, A. Medical gas plasma jet technology targets murine melanoma in an immunogenic fashion. Adv. Sci. 2020, 7, 1903438. [Google Scholar] [CrossRef] [PubMed] [Green Version]
HES | NaCl | G-5 | E153 | Ri-Lac | Gela | PBS | R10F | |
---|---|---|---|---|---|---|---|---|
main component | 60 g/L hydroxyethyl starch | 9 g/500 mL sodium chloride | 50 g/L glucose | 153 mval/L ions | Ringer’s solution with 28 mmol/L | Gelatine 40 g/L | 12 mM phosphate | Amino acids, vitamins and 10% FCS |
pH-range | 4.0–5.5 | 4.5–7.0 | 3.5–5.5 | 5.0–7.0 | 5.0–7.0 | 7.1–7.7 | 7.3–7.5 | 8.0 |
pH-treated | 5.2 | 5.1 | 5.6 | 6.2 | 6.0 | 7.0 | 7.3 | 8.3 |
osmolarity (mOsm) | 308 | 308 | 278 | 303 | 277 | 274 | 280 | - |
acetions | X | |||||||
amino acids | X | |||||||
Ca | X | X | X | |||||
calcium hydrochloride-dihydrate | X | X | ||||||
calcium nitrate | X | |||||||
carbohydrates | X | X | X | |||||
Cl | X | |||||||
gelatine poly succinate | X | |||||||
HCl | X | |||||||
K | X | |||||||
KCl | X | X | X | |||||
lactate | X | |||||||
magnesium sulfate | X | |||||||
magnesium chlorid-hecyhydrat | X | |||||||
Mg | X | |||||||
NaCl | X | X | X | X | X | X | X | |
phosphate | X | X | ||||||
protein | X | |||||||
sodium acetate | X | X | ||||||
sodium hydroxide | X | |||||||
vitamins | X |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tanaka, H.; Bekeschus, S.; Yan, D.; Hori, M.; Keidar, M.; Laroussi, M. Plasma-Treated Solutions (PTS) in Cancer Therapy. Cancers 2021, 13, 1737. https://doi.org/10.3390/cancers13071737
Tanaka H, Bekeschus S, Yan D, Hori M, Keidar M, Laroussi M. Plasma-Treated Solutions (PTS) in Cancer Therapy. Cancers. 2021; 13(7):1737. https://doi.org/10.3390/cancers13071737
Chicago/Turabian StyleTanaka, Hiromasa, Sander Bekeschus, Dayun Yan, Masaru Hori, Michael Keidar, and Mounir Laroussi. 2021. "Plasma-Treated Solutions (PTS) in Cancer Therapy" Cancers 13, no. 7: 1737. https://doi.org/10.3390/cancers13071737