Cold Atmospheric Plasma Induces Growth Arrest and Apoptosis in Neurofibromatosis Type 1-Associated Peripheral Nerve Sheath Tumor Cells
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Basu, T.N.; Gutmann, D.H.; Fletcher, J.A.; Glover, T.W.; Collins, F.S.; Downward, J. Aberrant Regulation of Ras Proteins in Malignant Tumour Cells from Type 1 Neurofibromatosis Patients. Nature 1992, 356, 713–715. [Google Scholar] [CrossRef]
- Mowery, A.; Clayburgh, D. Malignant Peripheral Nerve Sheath Tumors: Analysis of the National Cancer Database. Oral Oncol. 2019, 98, 13–19. [Google Scholar] [CrossRef] [PubMed]
- Fisher, M.J.; Blakeley, J.O.; Weiss, B.D.; Dombi, E.; Ahlawat, S.; Akshintala, S.; Belzberg, A.J.; Bornhorst, M.; Bredella, M.A.; Cai, W.; et al. Management of Neurofibromatosis Type 1-Associated Plexiform Neurofibromas. Neuro-Oncology 2022, 24, 1827–1844. [Google Scholar] [CrossRef] [PubMed]
- de Blank, P.M.K.; Gross, A.M.; Akshintala, S.; Blakeley, J.O.; Bollag, G.; Cannon, A.; Dombi, E.; Fangusaro, J.; Gelb, B.D.; Hargrave, D.; et al. MEK Inhibitors for Neurofibromatosis Type 1 Manifestations: Clinical Evidence and Consensus. Neuro-Oncology 2022, 24, 1845–1856. [Google Scholar] [CrossRef]
- Lu, X.; Naidis, G.V.; Laroussi, M.; Reuter, S.; Graves, D.B.; Ostrikov, K. Reactive Species in Non-Equilibrium Atmospheric-Pressure Plasmas: Generation, Transport, and Biological Effects. Phys. Rep. 2016, 630, 1–84. [Google Scholar] [CrossRef]
- Limanowski, R.; Yan, D.; Li, L.; Keidar, M. Preclinical Cold Atmospheric Plasma Cancer Treatment. Cancers 2022, 14, 3461. [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]
- Canady, J.; Murthy, S.R.K.; Zhuang, T.; Gitelis, S.; Nissan, A.; Ly, L.; Jones, O.Z.; Cheng, X.; Adileh, M.; Blank, A.T.; et al. The First Cold Atmospheric Plasma Phase I Clinical Trial for the Treatment of Advanced Solid Tumors: A Novel Treatment Arm for Cancer. Cancers 2023, 15, 3688. [Google Scholar] [CrossRef]
- Kugler, P.; Becker, S.; Welz, C.; Wiesmann, N.; Sax, J.; Buhr, C.R.; Thoma, M.H.; Brieger, J.; Eckrich, J. Cold Atmospheric Plasma Reduces Vessel Density and Increases Vascular Permeability and Apoptotic Cell Death in Solid Tumors. Cancers 2022, 14, 2432. [Google Scholar] [CrossRef]
- Keidar, M.; Walk, R.; Shashurin, A.; Srinivasan, P.; Sandler, A.; Dasgupta, S.; Ravi, R.; Guerrero-Preston, 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]
- Chen, Z.; Wirz, R.E. Cold Atmospheric Plasma (CAP) Technology and Applications; Synthesis Lectures on Mechanical Engineering; Springer International Publishing: Cham, Switzerland, 2021; ISBN 978-3-031-79700-2. [Google Scholar]
- Chen, Z.; Garcia, G.; Arumugaswami, V.; Wirz, R.E. Cold Atmospheric Plasma for SARS-CoV-2 Inactivation. Phys. Fluids (1994) 2020, 32, 111702. [Google Scholar] [CrossRef]
- Chen, Z.; Obenchain, R.; Wirz, R.E. Tiny Cold Atmospheric Plasma Jet for Biomedical Applications. Processes 2021, 9, 249. [Google Scholar] [CrossRef]
- Ratner, N.; Williams, J.P.; Kordich, J.J.; Kim, H.A. Schwann Cell Preparation from Single Mouse Embryos: Analyses of Neurofibromin Function in Schwann Cells. In Methods in Enzymology; Regulators and Effectors of Small GTPases: Ras Family; Academic Press: Cambridge, MA, USA, 2006; Volume 407, pp. 22–33. [Google Scholar]
- Wu, J.; Williams, J.P.; Rizvi, T.A.; Kordich, J.J.; Witte, D.; Meijer, D.; Stemmer-Rachamimov, A.O.; Cancelas, J.A.; Ratner, N. Plexiform and Dermal Neurofibromas and Pigmentation Are Caused by Nf1 Loss in Desert Hedgehog-Expressing Cells. Cancer Cell 2008, 13, 105–116. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Chang, L.-J.; Neubauer, D.R.; Muir, D.F.; Wallace, M.R. Immortalization of Human Normal and NF1 Neurofibroma Schwann Cells. Lab. Investig. 2016, 96, 1105–1115. [Google Scholar] [CrossRef]
- Magallón-Lorenz, M.; Terribas, E.; Ortega-Bertran, S.; Creus-Bachiller, E.; Fernández, M.; Requena, G.; Rosas, I.; Mazuelas, H.; Uriarte-Arrazola, I.; Negro, A.; et al. Deep Genomic Analysis of Malignant Peripheral Nerve Sheath Tumor Cell Lines Challenges Current Malignant Peripheral Nerve Sheath Tumor Diagnosis. iScience 2023, 26, 106096. [Google Scholar] [CrossRef] [PubMed]
- Mahller, Y.Y.; Vaikunth, S.S.; Currier, M.A.; Miller, S.J.; Ripberger, M.C.; Hsu, Y.-H.; Mehrian-Shai, R.; Collins, M.H.; Crombleholme, T.M.; Ratner, N.; et al. Oncolytic HSV and Erlotinib Inhibit Tumor Growth and Angiogenesis in a Novel Malignant Peripheral Nerve Sheath Tumor Xenograft Model. Mol. Ther. 2007, 15, 279–286. [Google Scholar] [CrossRef]
- Yan, D.; Sherman, J.H.; Keidar, M. Cold Atmospheric Plasma, a Novel Promising Anti-Cancer Treatment Modality. Oncotarget 2016, 8, 15977–15995. [Google Scholar] [CrossRef]
- Yan, D.; Xu, W.; Yao, X.; Lin, L.; Sherman, J.H.; Keidar, M. The Cell Activation Phenomena in the Cold Atmospheric Plasma Cancer Treatment. Sci. Rep. 2018, 8, 15418. [Google Scholar] [CrossRef]
- Jung, J.-M.; Yoon, H.-K.; Kim, S.-Y.; Yun, M.-R.; Kim, G.-H.; Lee, W.-J.; Lee, M.-W.; Chang, S.-E.; Won, C.-H. Anticancer Effect of Cold Atmospheric Plasma in Syngeneic Mouse Models of Melanoma and Colon Cancer. Molecules 2023, 28, 4171. [Google Scholar] [CrossRef]
- Partecke, L.I.; Evert, K.; Haugk, J.; Doering, F.; Normann, L.; Diedrich, S.; Weiss, F.-U.; Evert, M.; Huebner, N.O.; Guenther, C.; et al. Tissue Tolerable Plasma (TTP) Induces Apoptosis in Pancreatic Cancer Cells in Vitro and in Vivo. BMC Cancer 2012, 12, 473. [Google Scholar] [CrossRef]
- Wang, Y.; Mang, X.; Li, X.; Cai, Z.; Tan, F. Cold Atmospheric Plasma Induces Apoptosis in Human Colon and Lung Cancer Cells through Modulating Mitochondrial Pathway. Front. Cell Dev. Biol. 2022, 10, 915785. [Google Scholar] [CrossRef]
- Turrini, E.; Laurita, R.; Stancampiano, A.; Catanzaro, E.; Calcabrini, C.; Maffei, F.; Gherardi, M.; Colombo, V.; Fimognari, C. Cold Atmospheric Plasma Induces Apoptosis and Oxidative Stress Pathway Regulation in T-Lymphoblastoid Leukemia Cells. Oxidative Med. Cell. Longev. 2017, 2017, 4271065. [Google Scholar] [CrossRef]
- Bauer, G.; Sersenová, D.; Graves, D.B.; Machala, Z. Cold Atmospheric Plasma and Plasma-Activated Medium Trigger RONS-Based Tumor Cell Apoptosis. Sci. Rep. 2019, 9, 14210. [Google Scholar] [CrossRef]
- Kim, A.; Lu, Y.; Okuno, S.H.; Reinke, D.; Maertens, O.; Perentesis, J.; Basu, M.; Wolters, P.L.; De Raedt, T.; Chawla, S.; et al. Targeting Refractory Sarcomas and Malignant Peripheral Nerve Sheath Tumors in a Phase I/II Study of Sirolimus in Combination with Ganetespib (SARC023). Sarcoma 2020, 2020, 5784876. [Google Scholar] [CrossRef]
- De Raedt, T.; Walton, Z.; Yecies, J.L.; Li, D.; Chen, Y.; Malone, C.F.; Maertens, O.; Jeong, S.M.; Bronson, R.T.; Lebleu, V.; et al. Exploiting Cancer Cell Vulnerabilities to Develop a Combination Therapy for Ras-Driven Tumors. Cancer Cell 2011, 20, 400–413. [Google Scholar] [CrossRef] [PubMed]
- Pfeffer, C.M.; Singh, A.T.K. Apoptosis: A Target for Anticancer Therapy. Int. J. Mol. Sci. 2018, 19, 448. [Google Scholar] [CrossRef]
- Zhou, B.-B.S.; Elledge, S.J. The DNA Damage Response: Putting Checkpoints in Perspective. Nature 2000, 408, 433–439. [Google Scholar] [CrossRef] [PubMed]
- Wyllie, F.S.; Haughton, M.F.; Bond, J.A.; Rowson, J.M.; Jones, C.J.; Wynford-Thomas, D. S Phase Cell-Cycle Arrest Following DNA Damage Is Independent of the P53/P21(WAF1) Signalling Pathway. Oncogene 1996, 12, 1077–1082. [Google Scholar]
- Agarwal, M.L.; Agarwal, A.; Taylor, W.R.; Chernova, O.; Sharma, Y.; Stark, G.R. A P53-Dependent S-Phase Checkpoint Helps to Protect Cells from DNA Damage in Response to Starvation for Pyrimidine Nucleotides. Proc. Natl. Acad. Sci. USA 1998, 95, 14775–14780. [Google Scholar] [CrossRef]
- Vaquero, J.; Judée, F.; Vallette, M.; Decauchy, H.; Arbelaiz, A.; Aoudjehane, L.; Scatton, O.; Gonzalez-Sanchez, E.; Merabtene, F.; Augustin, J.; et al. Cold-Atmospheric Plasma Induces Tumor Cell Death in Preclinical In Vivo and In Vitro Models of Human Cholangiocarcinoma. Cancers 2020, 12, 1280. [Google Scholar] [CrossRef]
- Volotskova, O.; Hawley, T.S.; Stepp, M.A.; Keidar, M. Targeting the Cancer Cell Cycle by Cold Atmospheric Plasma. Sci. Rep. 2012, 2, 636. [Google Scholar] [CrossRef] [PubMed]
- Nakai, N.; Fujita, R.; Kawano, F.; Takahashi, K.; Ohira, T.; Shibaguchi, T.; Nakata, K.; Ohira, Y. Retardation of C2C12 Myoblast Cell Proliferation by Exposure to Low-Temperature Atmospheric Plasma. J. Physiol. Sci. 2014, 64, 365–375. [Google Scholar] [CrossRef] [PubMed]
- Gross, A.M.; Wolters, P.L.; Dombi, E.; Baldwin, A.; Whitcomb, P.; Fisher, M.J.; Weiss, B.; Kim, A.; Bornhorst, M.; Shah, A.C.; et al. Selumetinib in Children with Inoperable Plexiform Neurofibromas. N. Engl. J. Med. 2020, 382, 1430–1442. [Google Scholar] [CrossRef]
- Lu, Z.; Xu, S. ERK1/2 MAP Kinases in Cell Survival and Apoptosis. IUBMB Life 2006, 58, 621–631. [Google Scholar] [CrossRef] [PubMed]
- Adhikari, M.; Adhikari, B.; Ghimire, B.; Baboota, S.; Choi, E.H. Cold Atmospheric Plasma and Silymarin Nanoemulsion Activate Autophagy in Human Melanoma Cells. Int. J. Mol. Sci. 2020, 21, 1939. [Google Scholar] [CrossRef]
- Schmidt, A.; Bekeschus, S.; Jarick, K.; Hasse, S.; von Woedtke, T.; Wende, K. Cold Physical Plasma Modulates P53 and Mitogen-Activated Protein Kinase Signaling in Keratinocytes. Oxidative Med. Cell. Longev. 2019, 2019, 7017363. [Google Scholar] [CrossRef]
- Lin, L.; Keidar, M. A Map of Control for Cold Atmospheric Plasma Jets: From Physical Mechanisms to Optimizations. Appl. Phys. Rev. 2021, 8, 011306. [Google Scholar] [CrossRef]
- Lin, L.; Hou, Z.; Yao, X.; Liu, Y.; Sirigiri, J.R.; Lee, T.; Keidar, M. Introducing Adaptive Cold Atmospheric Plasma: The Perspective of Adaptive Cold Plasma Cancer Treatments Based on Real-Time Electrochemical Impedance Spectroscopy. Phys. Plasmas 2020, 27, 063501. [Google Scholar] [CrossRef]
- Gidon, D.; Pei, X.; Bonzanini, A.D.; Graves, D.B.; Mesbah, A. Machine Learning for Real-Time Diagnostics of Cold Atmospheric Plasma Sources. IEEE Trans. Radiat. Plasma Med. Sci. 2019, 3, 597–605. [Google Scholar] [CrossRef]
- Hoffmann, C.; Berganza, C.; Zhang, J. Cold Atmospheric Plasma: Methods of Production and Application in Dentistry and Oncology. Med. Gas Res. 2013, 3, 21. [Google Scholar] [CrossRef]
- Kim, J.Y.; Wei, Y.; Li, J.; Kim, S.-O. 15-Μm-Sized Single-Cellular-Level and Cell-Manipulatable Microplasma Jet in Cancer Therapies. Biosens. Bioelectron. 2010, 26, 555–559. [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]
- Szili, E.J.; Hong, S.-H.; Oh, J.-S.; Gaur, N.; Short, R.D. Tracking the Penetration of Plasma Reactive Species in Tissue Models. Trends Biotechnol. 2018, 36, 594–602. [Google Scholar] [CrossRef] [PubMed]
- Chen, G.; Chen, Z.; Wen, D.; Wang, Z.; Li, H.; Zeng, Y.; Dotti, G.; Wirz, R.E.; Gu, Z. Transdermal Cold Atmospheric Plasma-Mediated Immune Checkpoint Blockade Therapy. Proc. Natl. Acad. Sci. USA 2020, 117, 3687–3692. [Google Scholar] [CrossRef]
- 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] [PubMed]
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Na, B.; Haist, B.; Shah, S.R.; Sabiston, G.; Jonas, S.J.; Vitte, J.; Wirz, R.E.; Giovannini, M. Cold Atmospheric Plasma Induces Growth Arrest and Apoptosis in Neurofibromatosis Type 1-Associated Peripheral Nerve Sheath Tumor Cells. Biomedicines 2024, 12, 1986. https://doi.org/10.3390/biomedicines12091986
Na B, Haist B, Shah SR, Sabiston G, Jonas SJ, Vitte J, Wirz RE, Giovannini M. Cold Atmospheric Plasma Induces Growth Arrest and Apoptosis in Neurofibromatosis Type 1-Associated Peripheral Nerve Sheath Tumor Cells. Biomedicines. 2024; 12(9):1986. https://doi.org/10.3390/biomedicines12091986
Chicago/Turabian StyleNa, Brian, Blake Haist, Shilp R. Shah, Graeme Sabiston, Steven J. Jonas, Jeremie Vitte, Richard E. Wirz, and Marco Giovannini. 2024. "Cold Atmospheric Plasma Induces Growth Arrest and Apoptosis in Neurofibromatosis Type 1-Associated Peripheral Nerve Sheath Tumor Cells" Biomedicines 12, no. 9: 1986. https://doi.org/10.3390/biomedicines12091986