Chemically different non-thermal plasmas target distinct cell death pathways
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
28377599
PubMed Central
PMC5428849
DOI
10.1038/s41598-017-00689-5
PII: 10.1038/s41598-017-00689-5
Knihovny.cz E-zdroje
- MeSH
- apoptóza účinky léků MeSH
- buněčná smrt účinky léků MeSH
- buněčné linie MeSH
- buňky NIH 3T3 MeSH
- helium chemie farmakologie MeSH
- myši MeSH
- nekróza metabolismus MeSH
- oxidační stres účinky léků MeSH
- plazmové plyny analýza chemie farmakologie MeSH
- poškození DNA účinky léků MeSH
- reaktivní formy dusíku metabolismus MeSH
- reaktivní formy kyslíku metabolismus MeSH
- signální transdukce účinky léků MeSH
- spektroskopie infračervená s Fourierovou transformací MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- helium MeSH
- plazmové plyny MeSH
- reaktivní formy dusíku MeSH
- reaktivní formy kyslíku MeSH
A rigorous biochemical analysis of interactions between non-thermal plasmas (NTPs) and living cells has become an important research topic, due to recent developments in biomedical applications of non-thermal plasmas. Here, we decouple distinct cell death pathways targeted by chemically different NTPs. We show that helium NTP cells treatment, results in necrosome formation and necroptosis execution, whereas air NTP leads to mTOR activation and autophagy inhibition, that induces mTOR-related necrosis. On the contrary, ozone (abundant component of air NTP) treatment alone, exhibited the highest levels of reactive oxygen species production leading to CypD-related necrosis via the mitochondrial permeability transition. Our findings offer a novel insight into plasma-induced cellular responses, and reveal distinct cell death pathways triggered by NTPs.
Institute for Clinical and Experimental Medicine Prague 14021 Czech Republic
Institute of Experimental Medicine AS CR Prague 14220 Czech Republic
Institute of Physics of the Academy of Sciences of the Czech Republic Prague 18221 Czech Republic
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Fridman G, et al. Applied plasma medicine. Plasma Process. Polym. 2008;5:503–533. doi: 10.1002/ppap.200700154. DOI
Laroussi M. From killing bacteria to destroying cancer cells: 20 years of plasma medicine. Plasma Process. Polym. 2014;11:1138–1141. doi: 10.1002/ppap.201400152. DOI
Lu X, Laroussi M, Puech V. On atmospheric-pressure non-equilibrium plasma jets and plasma bullets. Plasma Sources Sci. Technol. 2012;21:034005. doi: 10.1088/0963-0252/21/3/034005. DOI
Cheng XQ, et al. The effect of tuning cold plasma composition on glioblastoma cell viability. PLoS One. 2014;9:e98652. doi: 10.1371/journal.pone.0098652. PubMed DOI PMC
Lunov O, et al. Cell death induced by ozone and various non-thermal plasmas: therapeutic perspectives and limitations. Sci. Rep. 2014;4:7129. doi: 10.1038/srep07129. PubMed DOI PMC
Kalghatgi S, et al. Effects of non-thermal plasma on mammalian cells. PLoS One. 2011;6:e16270. doi: 10.1371/journal.pone.0016270. PubMed DOI PMC
Ahn HJ, et al. Targeting cancer cells with reactive oxygen and nitrogen species generated by atmospheric-pressure air plasma. PLoS One. 2014;9:e86173. doi: 10.1371/journal.pone.0086173. PubMed DOI PMC
Kong MG, et al. Plasma medicine: an introductory review. New J. Phys. 2009;11:115012. doi: 10.1088/1367-2630/11/11/115012. DOI
Rumbach P, Witzke M, Sankaran RM, Go DB. Decoupling interfacial reactions between plasmas and liquids: charge transfer vs plasma neutral reactions. J. Am. Chem. Soc. 2013;135:16264–16267. doi: 10.1021/ja407149y. PubMed DOI
Bekeschus S, et al. Hydrogen peroxide: A central player in physical plasma-induced oxidative stress in human blood cells. Free Radic. Res. 2014;48:542–549. doi: 10.3109/10715762.2014.892937. PubMed DOI
Lee S, Lee H, Bae H, Choi EH, Kim SJ. Epigenetic silencing of miR-19a-3p by cold atmospheric plasma contributes to proliferation inhibition of the MCF-7 breast cancer cell. Sci. Rep. 2016;6:30005. doi: 10.1038/srep30005. PubMed DOI PMC
Zhong SY, et al. Surface air plasma-induced cell death and cytokine release of human keratinocytes in the context of psoriasis. Br. J. Dermatol. 2016;174:542–552. doi: 10.1111/bjd.14236. PubMed DOI
Panngom K, et al. Preferential killing of human lung cancer cell lines with mitochondrial dysfunction by nonthermal dielectric barrier discharge plasma. Cell Death Dis. 2013;4:e642. doi: 10.1038/cddis.2013.168. PubMed DOI PMC
Virard F, et al. Cold atmospheric plasma induces a predominantly necrotic cell death via the microenvironment. PLoS One. 2015;10:e0133120. doi: 10.1371/journal.pone.0133120. PubMed DOI PMC
Kang SU, et al. 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. doi: 10.1038/cddis.2014.33. PubMed DOI PMC
Hirst AM, et al. Low-temperature plasma treatment induces DNA damage leading to necrotic cell death in primary prostate epithelial cells. Br. J. Cancer. 2015;112:1536–1545. doi: 10.1038/bjc.2015.113. PubMed DOI PMC
Vanden Berghe T, Kaiser WJ, Bertrand MJM, Vandenabeele P. Molecular crosstalk between apoptosis, necroptosis, and survival signaling. Mol. Cell Oncol. 2015;2:e975093. doi: 10.4161/23723556.2014.975093. PubMed DOI PMC
Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochim. Biophys. Acta-Mol. Cell. 2013;1833:3448–3459. doi: 10.1016/j.bbamcr.2013.06.001. PubMed DOI
Ehlbeck J, et al. Low temperature atmospheric pressure plasma sources for microbial decontamination. J. Phys. D-Appl. Phys. 2011;44:013002. doi: 10.1088/0022-3727/44/1/013002. DOI
Lunov O, et al. The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma. Biomaterials. 2016;82:71–83. doi: 10.1016/j.biomaterials.2015.12.027. PubMed DOI
Lunov O, et al. Towards the understanding of non-thermal air plasma action: effects on bacteria and fibroblasts. RSC Adv. 2016;6:25286–25292. doi: 10.1039/C6RA02368A. DOI
Balzer J, et al. Non-thermal dielectric barrier discharge (DBD) effects on proliferation and differentiation of human fibroblasts are primary mediated by hydrogen peroxide. PLoS One. 2015;10:e0144968. doi: 10.1371/journal.pone.0144968. PubMed DOI PMC
Lee JH, et al. Selective killing effects of cold atmospheric pressure plasma with NO induced dysfunction of epidermal growth factor receptor in oral squamous cell carcinoma. PLoS One. 2016;11:e0150279. doi: 10.1371/journal.pone.0150279. PubMed DOI PMC
Flynn PB, et al. Non-thermal plasma exposure rapidly attenuates bacterial AHL-dependent quorum sensing and virulence. Sci. Rep. 2016;6:26320. doi: 10.1038/srep26320. PubMed DOI PMC
Latonen L, Taya Y, Laiho M. UV-radiation induces dose-dependent regulation of p53 response and modulates p53-HDM2 interaction in human fibroblasts. Oncogene. 2001;20:6784–6793. doi: 10.1038/sj.onc.1204883. PubMed DOI
Laroussi M, Leipold F. Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure. Int. J. Mass Spectrom. 2004;233:81–86. doi: 10.1016/j.ijms.2003.11.016. DOI
Opinion on biological effects of ultraviolet radiation relevant to health with particular reference to sunbeds for cosmetic purposes. SCCP European Commission Report 0949/05 (2006).
Lunov O, et al. Non-thermal plasma mills bacteria: Scanning electron microscopy observations. Appl. Phys. Lett. 2015;106:053703. doi: 10.1063/1.4907624. DOI
Laroussi M. Low temperature plasma-based sterilization: overview and state-of-the-art. Plasma Process. Polym. 2005;2:391–400. doi: 10.1002/ppap.200400078. DOI
Zdenko M, Lenka C, Michal P. Plasma agents in bio-decontamination by dc discharges in atmospheric air. J. Phys. D-Appl. Phys. 2010;43:222001. doi: 10.1088/0022-3727/43/22/222001. DOI
Conway GE, et al. Non-thermal atmospheric plasma induces ROS-independent cell death in U373MG glioma cells and augments the cytotoxicity of temozolomide. Br. J. Cancer. 2016;114:435–443. doi: 10.1038/bjc.2016.12. PubMed DOI PMC
Jablonowski H, von Woedtke T. Research on plasma medicine-relevant plasma–liquid interaction: What happened in the past five years? Clinical Plasma Medicine. 2015;3:42–52. doi: 10.1016/j.cpme.2015.11.003. DOI
Girard PM, et al. Synergistic Effect of H2O2 and NO2 in Cell Death Induced by Cold Atmospheric He Plasma. Sci. Rep. 2016;6:29098. doi: 10.1038/srep29098. PubMed DOI PMC
Shiraiwa M, et al. The role of long-lived reactive oxygen intermediates in the reaction of ozone with aerosol particles. Nat. Chem. 2011;3:291–295. doi: 10.1038/nchem.988. PubMed DOI
Endre JS, James WB, Robert DSA. ‘tissue model’ to study the plasma delivery of reactive oxygen species. J. Phys. D-Appl. Phys. 2014;47:152002. doi: 10.1088/0022-3727/47/15/152002. DOI
Herbst SR, et al. Bactericidal efficacy of cold plasma at different depths of infected root canals in vitro. The Open Dentistry Journal. 2015;9:486–491. doi: 10.2174/1874210601509010486. PubMed DOI PMC
Hoffmann C, Berganza C, Zhang J. Cold Atmospheric Plasma: methods of production and application in dentistry and oncology. Med. Gas Res. 2013;3:21. doi: 10.1186/2045-9912-3-21. PubMed DOI PMC
Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell. 2004;116:205–219. doi: 10.1016/S0092-8674(04)00046-7. PubMed DOI
Gweon B, et al. Plasma effects on subcellular structures. Appl. Phys. Lett. 2010;96:101501. doi: 10.1063/1.3352316. DOI
Kang MA, So EY, Simons AL, Spitz DR, Ouchi T. DNA damage induces reactive oxygen species generation through the H2AX-Nox1/Rac1 pathway. Cell Death Dis. 2012;3:e249. doi: 10.1038/cddis.2011.134. PubMed DOI PMC
Fiers W, Beyaert R, Declercq W, Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene. 1999;18:7719–7730. doi: 10.1038/sj.onc.1203249. PubMed DOI
Linkermann A, Green DR. Necroptosis. New. Engl. J. Med. 2014;370:455–465. doi: 10.1056/NEJMra1310050. PubMed DOI PMC
Marino G, Niso-Santano M, Baehrecke EH, Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2014;15:81–94. doi: 10.1038/nrm3735. PubMed DOI PMC
Degterev A, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 2005;1:112–119. doi: 10.1038/nchembio711. PubMed DOI
Han JH, Zhong CQ, Zhang DW. Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nat. Immunol. 2011;12:1143–1149. doi: 10.1038/ni.2159. PubMed DOI
Seok J, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA. 2013;110:3507–3512. doi: 10.1073/pnas.1222878110. PubMed DOI PMC
Mestas J, Hughes CCW. Of Mice and Not Men: Differences between Mouse and Human Immunology. J. Immunol. 2004;172:2731–2738. doi: 10.4049/jimmunol.172.5.2731. PubMed DOI
Li J, et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell. 2012;150:339–350. doi: 10.1016/j.cell.2012.06.019. PubMed DOI PMC
Wu XN, et al. Distinct roles of RIP1-RIP3 hetero- and RIP3-RIP3 homo-interaction in mediating necroptosis. Cell Death Differ. 2014;21:1709–1720. doi: 10.1038/cdd.2014.77. PubMed DOI PMC
McComb S, et al. Type-I interferon signaling through ISGF3 complex is required for sustained Rip3 activation and necroptosis in macrophages. Proc. Natl. Acad. Sci. USA. 2014;111:E3206–E3213. doi: 10.1073/pnas.1407068111. PubMed DOI PMC
Quarato G, et al. Sequential engagement of distinct MLKL phosphatidylinositol-binding sites executes necroptosis. Mol. Cell. 2016;61:589–601. doi: 10.1016/j.molcel.2016.01.011. PubMed DOI PMC
Basit F, Cristofanon S, Fulda S. Obatoclax (GX15-070) triggers necroptosis by promoting the assembly of the necrosome on autophagosomal membranes. Cell Death Differ. 2013;20:1161–1173. doi: 10.1038/cdd.2013.45. PubMed DOI PMC
Wu YT, Tan HL, Huang Q, Ong CN, Shen HM. Activation of the PI3K-Akt-mTOR signaling pathway promotes necrotic cell death via suppression of autophagy. Autophagy. 2009;5:824–834. doi: 10.4161/auto.9099. PubMed DOI
Goodman, L. S., Gilman, A., Brunton, L. L., Lazo, J. S. & Parker, K. L. Goodman & Gilman’s the pharmacological basis of therapeutics. (McGraw-Hill, 2006).
Nakagawa T, et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature. 2005;434:652–658. doi: 10.1038/nature03317. PubMed DOI
Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010;11:700–714. doi: 10.1038/nrm2970. PubMed DOI
Roca FJ, Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell. 2013;153:521–534. doi: 10.1016/j.cell.2013.03.022. PubMed DOI PMC
Linkermann A, et al. Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc. Natl. Acad. Sci. USA. 2013;110:12024–12029. doi: 10.1073/pnas.1305538110. PubMed DOI PMC
Temkin V, Karin M. From death receptor to reactive oxygen species and c-Jun N-terminal protein kinase: the receptor-interacting protein 1 odyssey. Immunol. Rev. 2007;220:8–21. doi: 10.1111/j.1600-065X.2007.00560.x. PubMed DOI
Woo HA, et al. Inactivation of peroxiredoxin I by phosphorylation allows localized H2O2 accumulation for cell signaling. Cell. 2010;140:517–528. doi: 10.1016/j.cell.2010.01.009. PubMed DOI
Jun-Seok O, et al. How to assess the plasma delivery of RONS into tissue fluid and tissue. J. Phys. D-Appl. Phys. 2016;49:304005. doi: 10.1088/0022-3727/49/30/304005. DOI
Lopez-Rivera E, et al. Inducible nitric oxide synthase drives mTOR pathway activation and proliferation of human melanoma by reversible nitrosylation of TSC2. Cancer Res. 2014;74:1067–1078. doi: 10.1158/0008-5472.CAN-13-0588. PubMed DOI PMC
Clydesdale GJ, Dandie GW, Muller HK. Ultraviolet light induced injury: Immunological and inflammatory effects. Immunol. Cell Biol. 2001;79:547–568. doi: 10.1046/j.1440-1711.2001.01047.x. PubMed DOI
Silve A, Leray I, Poignard C, Mir LM. Impact of external medium conductivity on cell membrane electropermeabilization by microsecond and nanosecond electric pulses. Sci. Rep. 2016;6:19957. doi: 10.1038/srep19957. PubMed DOI PMC
Zablotskii V, Syrovets T, Schmidt ZW, Dejneka A, Simmet T. Modulation of monocytic leukemia cell function and survival by high gradient magnetic fields and mathematical modeling studies. Biomaterials. 2014;35:3164–3171. doi: 10.1016/j.biomaterials.2013.12.098. PubMed DOI
Tukmachev D, et al. Injectable Extracellular Matrix Hydrogels as Scaffolds for Spinal Cord Injury Repair. Tissue Eng. Part A. 2016;22:306–317. doi: 10.1089/ten.tea.2015.0422. PubMed DOI PMC
Gavet O, Pines J. Progressive activation of cyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell. 2010;18:533–543. doi: 10.1016/j.devcel.2010.02.013. PubMed DOI PMC
Syrovets T, Jendrach M, Rohwedder A, Schule A, Simmet T. Plasmin-induced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKK beta-mediated NF-kappa B activation. Blood. 2001;97:3941–3950. doi: 10.1182/blood.V97.12.3941. PubMed DOI
Burysek L, Syrovets T, Simmet T. The serine protease plasmin triggers expression of MCP-1 and CD40 in human primary monocytes via activation of p38 MAPK and Janus kinase (JAK)/STAT signaling pathways. J. Biol. Chem. 2002;277:33509–33517. doi: 10.1074/jbc.M201941200. PubMed DOI
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