دورية أكاديمية

Non-thermal atmospheric pressure plasma induces selective cancer cell apoptosis by modulating redox homeostasis.

التفاصيل البيبلوغرافية
العنوان: Non-thermal atmospheric pressure plasma induces selective cancer cell apoptosis by modulating redox homeostasis.
المؤلفون: Yun JH; Department of Otorhinolaryngology-Head and Neck Surgery, College of Medicine, Ewha Womans University, Seoul, Korea, 07985., Yang YH; Department of Biomedical Sciences, Graduate School of Medicine, Ajou University, Suwon, Korea, 16499., Han CH; Department of Otolaryngology, School of Medicine, Ajou University, Suwon, Korea, 16499., Kang SU; Department of Otolaryngology, School of Medicine, Ajou University, Suwon, Korea, 16499. cows79@ajou.ac.kr., Kim CH; Department of Otolaryngology, School of Medicine, Ajou University, Suwon, Korea, 16499. ostium@ajou.ac.kr.
المصدر: Cell communication and signaling : CCS [Cell Commun Signal] 2024 Sep 26; Vol. 22 (1), pp. 452. Date of Electronic Publication: 2024 Sep 26.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: BioMed Central Country of Publication: England NLM ID: 101170464 Publication Model: Electronic Cited Medium: Internet ISSN: 1478-811X (Electronic) Linking ISSN: 1478811X NLM ISO Abbreviation: Cell Commun Signal Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : BioMed Central, c2003-
مواضيع طبية MeSH: Plasma Gases*/pharmacology , Apoptosis*/drug effects , Reactive Oxygen Species*/metabolism , Oxidation-Reduction*/drug effects , NF-E2-Related Factor 2*/metabolism , NF-E2-Related Factor 2*/genetics , Homeostasis*/drug effects, Humans ; Cell Line, Tumor ; Mitochondria/metabolism ; Mitochondria/drug effects ; Autophagy/drug effects
مستخلص: Background: Anticancer treatments aim to selectively target cancer cells without harming normal cells. While non-thermal atmospheric pressure plasma (NTAPP) has shown anticancer potential across various studies, the mechanisms behind its selective action on cancer cells remain inadequately understood. This study explores the mechanism of NTAPP-induced selective cell death and assesses its application in cancer therapy.
Methods: We treated HT1080 fibrosarcoma cells with NTAPP and assessed the intracellular levels of mitochondria-derived reactive oxygen species (ROS), mitochondrial function, and cell death mechanisms. We employed N-acetylcysteine to investigate ROS's role in NTAPP-induced cell death. Additionally, single-cell RNA sequencing was used to compare gene expression in NTAPP-treated HT1080 cells and human normal fibroblasts (NF). Western blotting and immunofluorescence staining examined the expression and nuclear translocation of nuclear factor erythroid 2-related factor 2 (NRF2), a key antioxidant gene transcription factor. We also evaluated autophagy activity through fluorescence staining and transmission electron microscopy.
Results: NTAPP treatment increased ROS levels and induced mitochondrial dysfunction, leading to apoptosis in HT1080 cells. The involvement of ROS in selective cancer cell death was confirmed by N-acetylcysteine treatment. Distinct gene expression patterns were observed between NTAPP-treated NF and HT1080 cells, with NF showing upregulated antioxidant gene expression. Notably, NRF2 expression and nuclear translocation increased in NF but not in HT1080 cells. Furthermore, autophagy activity was significantly higher in normal cells compared to cancer cells.
Conclusions: Our study demonstrates that NTAPP induces selective cell death in fibrosarcoma cells through the downregulation of the NRF2-induced ROS scavenger system and inhibition of autophagy. These findings suggest NTAPP's potential as a cancer therapy that minimizes damage to normal cells while effectively targeting cancer cells.
(© 2024. The Author(s).)
References: Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49. (PMID: 10.3322/caac.2166033538338)
Wang K-L, Yu Y-C, Chen H-Y, Chiang Y-F, Ali M, Shieh T-M, Hsia S-M. Recent advances in Glycyrrhiza glabra (Licorice)-Containing herbs alleviating radiotherapy-and chemotherapy-induced adverse reactions in cancer treatment. Metabolites. 2022;12:535. (PMID: 10.3390/metabo12060535357364679227067)
Rébé C, Ghiringhelli F. Cytotoxic effects of chemotherapy on cancer and immune cells: how can it be modulated to generate novel therapeutic strategies? Future Oncol. 2015;11:2645–54. (PMID: 10.2217/fon.15.19826376787)
Kong MG, Kroesen G, Morfill G, Nosenko T, Shimizu T, Van Dijk J, Zimmermann J. Plasma medicine: an introductory review. New J Phys. 2009;11:115012. (PMID: 10.1088/1367-2630/11/11/115012)
Metelmann H-R, Von Woedtke T, Weltmann K-D. Comprehensive clinical plasma medicine: cold physical plasma for medical application. Springer; 2018.
Kim S, Kim CH. Applications of plasma-activated liquid in the Medical Field. Biomedicines 2021, 9.
Kang SU, Kim YS, Kim YE, Park JK, Lee YS, Kang HY, Jang JW, Ryeo JB, Lee Y, Shin YS, Kim CH. Opposite effects of non-thermal plasma on cell migration and collagen production in keloid and normal fibroblasts. PLoS ONE. 2017;12:e0187978. (PMID: 10.1371/journal.pone.0187978291455205690474)
Sohbatzadeh F, Hosseinzadeh Colagar A, Mirzanejhad S, Mahmodi S. E. Coli, P. Aeruginosa, and B. cereus bacteria sterilization using afterglow of non-thermal plasma at atmospheric pressure. Appl Biochem Biotechnol. 2010;160:1978–84. (PMID: 10.1007/s12010-009-8817-319882114)
Yang X, Sun K, Zhu W, Li Y, Pan J. Time-dependent efficacy and safety of tooth bleaching with cold plasma and H2O2 gel. BMC Oral Health. 2022;22:1–9. (PMID: 10.1186/s12903-022-02601-8)
Ma J, Yu K, Cheng C, Ni G, Shen J, Han W. Targeting Nrf2-mediated heme oxygenase-1 enhances non-thermal plasma-induced cell death in non-small-cell lung cancer A549 cells. Arch Biochem Biophys. 2018;658:54–65. (PMID: 10.1016/j.abb.2018.09.01530248308)
Lin L, Wang L, Liu Y, Xu C, Tu Y, Zhou J. Non–thermal plasma inhibits tumor growth and proliferation and enhances the sensitivity to radiation in vitro and in vivo. Oncol Rep. 2018;40:3405–15. (PMID: 302723426196603)
Nima G, Harth-Chu E, Hiers RD, Pecorari VGA, Dyer DW, Khajotia SS, Giannini M, Florez FLE. Antibacterial efficacy of non-thermal atmospheric plasma against Streptococcus mutans biofilm grown on the surfaces of restorative resin composites. Sci Rep. 2021;11:23800. (PMID: 10.1038/s41598-021-03192-0348936878664839)
Singh R, Manna P. Reactive oxygen species in cancer progression and its role in therapeutics. Explor Med. 2022;3:43–57. (PMID: 10.37349/emed.2022.00073)
Sarmiento-Salinas FL, Perez-Gonzalez A, Acosta-Casique A, Ix-Ballote A, Diaz A, Treviño S, Rosas-Murrieta NH, Millán-Perez-Peña L, Maycotte P. Reactive oxygen species: role in carcinogenesis, cancer cell signaling and tumor progression. Life Sci. 2021;284:119942. (PMID: 10.1016/j.lfs.2021.11994234506835)
National Academies of Sciences E, Medicine. Plasma science: Enabling Technology, sustainability, security, and Exploration. Washington, DC: National Academies; 2021.
Stryczewska HD, Boiko O. Applications of plasma produced with electrical discharges in gases for agriculture and biomedicine. Appl Sci (Basel). 2022;12:4405. (PMID: 10.3390/app12094405)
Kim SY, Kim HJ, Kang SU, Kim YE, Park JK, Shin YS, Kim YS, Lee K, Kim CH. Non-thermal plasma induces AKT degradation through turn-on the MUL1 E3 ligase in head and neck cancer. Oncotarget. 2015;6:33382–96. (PMID: 10.18632/oncotarget.5407264509024741773)
Kang SU, Cho JH, Chang JW, Shin YS, Kim KI, Park JK, Yang SS, Lee JS, Moon E, Lee K, Kim CH. Nonthermal plasma induces head and neck cancer cell death: the potential involvement of mitogen-activated protein kinase-dependent mitochondrial reactive oxygen species. Cell Death Dis. 2014;5:e1056. (PMID: 10.1038/cddis.2014.33245257323944250)
Park JK, Kim YS, Kang SU, Lee YS, Won HR, Kim CH. Nonthermal atmospheric plasma enhances myoblast differentiation by eliciting STAT3 phosphorylation. Faseb j. 2019;33:4097–106. (PMID: 10.1096/fj.201800695RR30548079)
Chang JW, Kang SU, Choi JW, Shin YS, Baek SJ, Lee S-H, Kim C-H. Tolfenamic acid induces apoptosis and growth inhibition in anaplastic thyroid cancer: involvement of nonsteroidal anti-inflammatory drug-activated gene-1 expression and intracellular reactive oxygen species generation. Free Radic Biol Med. 2014;67:115–30. (PMID: 10.1016/j.freeradbiomed.2013.10.81824216474)
Kang SU, Kim DH, Lee YS, Huang M, Byeon HK, Lee S-H, Baek SJ, Kim C-H. DIM-C-pPhtBu induces lysosomal dysfunction and unfolded protein response-mediated cell death via excessive mitophagy. Cancer Lett. 2021;504:23–36. (PMID: 10.1016/j.canlet.2021.01.00533556544)
Shin YS, Kang SU, Park JK, Kim YE, Kim YS, Baek SJ, Lee S-H, Kim C-H. Anti-cancer effect of (-)-epigallocatechin-3-gallate (EGCG) in head and neck cancer through repression of transactivation and enhanced degradation of β-catenin. Phytomedicine. 2016;23:1344–55. (PMID: 10.1016/j.phymed.2016.07.00527765354)
Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, Abdellatif M, Abdoli A, Abel S, Abeliovich H, Abildgaard MH, Abudu YP, Acevedo-Arozena A et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)(1). Autophagy 2021;17:1-382.
Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo j. 2000;19:5720–8. (PMID: 10.1093/emboj/19.21.572011060023305793)
Liou G-Y, Storz P. Reactive oxygen species in cancer. Free Radic Res. 2010;44:479–96. (PMID: 10.3109/1071576100366755420370557)
Hayes JD, Dinkova-Kostova AT, Tew KD. Oxidative stress in cancer. Cancer Cell. 2020;38:167–97. (PMID: 10.1016/j.ccell.2020.06.001326498857439808)
Bellezza I, Giambanco I, Minelli A, Donato R. Nrf2-Keap1 signaling in oxidative and reductive stress. Biochim et Biophys Acta (BBA)-Molecular Cell Res. 2018;1865:721–33. (PMID: 10.1016/j.bbamcr.2018.02.010)
Gañán-Gómez I, Wei Y, Yang H, Boyano-Adánez MC, García-Manero G. Oncogenic functions of the transcription factor Nrf2. Free Radic Biol Med. 2013;65:750–64. (PMID: 10.1016/j.freeradbiomed.2013.06.04123820265)
Theodore M, Kawai Y, Yang J, Kleshchenko Y, Reddy SP, Villalta F, Arinze IJ. Multiple nuclear localization signals function in the nuclear import of the transcription factor Nrf2. J Biol Chem. 2008;283:8984–94. (PMID: 10.1074/jbc.M709040200182387772276363)
Kasai S, Shimizu S, Tatara Y, Mimura J, Itoh K. Regulation of Nrf2 by mitochondrial reactive oxygen species in physiology and pathology. Biomolecules. 2020;10:320. (PMID: 10.3390/biom10020320320793247072240)
Chae SW, Choi G, Kim WJ, Lee ES, Shin SH, Park JH, Choi JW. Treatment results of soft tissue sarcomas in the head and neck. Head Neck. 1998;41:1454–8.
Aljabab AS, Nason RW, Kazi R, Pathak KA. Head and neck soft tissue sarcoma. Indian J Surg Oncol. 2011;2:286–90. (PMID: 10.1007/s13193-012-0127-523204783)
Augsburger D, Nelson PJ, Kalinski T, Udelnow A, Knösel T, Hofstetter M, Qin JW, Wang Y, Gupta AS, Bonifatius S. Current diagnostics and treatment of fibrosarcoma–perspectives for future therapeutic targets and strategies. Oncotarget. 2017;8:104638. (PMID: 10.18632/oncotarget.20136292626675732833)
Jaramillo MC, Zhang DD. The emerging role of the Nrf2–Keap1 signaling pathway in cancer. Genes Dev. 2013;27:2179–91. (PMID: 10.1101/gad.225680.113241428713814639)
De Backer J, Lin A, Berghe WV, Bogaerts A, Hoogewijs D. Cytoglobin inhibits non-thermal plasma-induced apoptosis in melanoma cells through regulation of the NRF2-mediated antioxidant response. Redox Biol. 2022;55:102399. (PMID: 10.1016/j.redox.2022.102399358500099294208)
Jiang T, Harder B, De La Vega MR, Wong PK, Chapman E, Zhang DD. p62 links autophagy and Nrf2 signaling. Free Radic Biol Med. 2015;88:199–204. (PMID: 10.1016/j.freeradbiomed.2015.06.014261173254628872)
Katsuragi Y, Ichimura Y, Komatsu M. Regulation of the Keap1–Nrf2 pathway by p62/SQSTM1. Curr Opin Toxicol. 2016;1:54–61. (PMID: 10.1016/j.cotox.2016.09.005)
Dodson M, Redmann M, Rajasekaran NS, Darley-Usmar V, Zhang J. KEAP1–NRF2 signalling and autophagy in protection against oxidative and reductive proteotoxicity. Biochem J. 2015;469:347–55. (PMID: 10.1042/BJ2015056826205490)
معلومات مُعتمدة: RS-2023-00273483 Ministry of Science, ICT and Future Planning; HR21C1003 Ministry of Health and Welfare; 2021003350001 Ministry of Environment; RS-2024-00438448 Republic of Korea Korea Health Industry Development Institute
فهرسة مساهمة: Keywords: Autophagy; Fibrosarcoma; NRF2; Non-thermal atmospheric pressure plasma; Reactive oxygen species
المشرفين على المادة: 0 (Plasma Gases)
0 (Reactive Oxygen Species)
0 (NF-E2-Related Factor 2)
0 (NFE2L2 protein, human)
تواريخ الأحداث: Date Created: 20240926 Date Completed: 20240927 Latest Revision: 20240926
رمز التحديث: 20240927
DOI: 10.1186/s12964-024-01810-8
PMID: 39327567
قاعدة البيانات: MEDLINE
الوصف
تدمد:1478-811X
DOI:10.1186/s12964-024-01810-8