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Frontiers of Chemical Science and Engineering

ISSN 2095-0179

ISSN 2095-0187(Online)

CN 11-5981/TQ

Postal Subscription Code 80-969

2018 Impact Factor: 2.809

Front. Chem. Sci. Eng.    2019, Vol. 13 Issue (2) : 253-263    https://doi.org/10.1007/s11705-018-1786-8
REVIEW ARTICLE
Plasma for cancer treatment: How can RONS penetrate through the cell membrane? Answers from computer modeling
Annemie Bogaerts(), Maksudbek Yusupov, Jamoliddin Razzokov, Jonas Van der Paal
Research group PLASMANT, Department of Chemistry, University of Antwerp, BE-2610 Antwerp-Wilrijk, Belgium
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Abstract

Plasma is gaining increasing interest for cancer treatment, but the underlying mechanisms are not yet fully understood. Using computer simulations at the molecular level, we try to gain better insight in how plasma-generated reactive oxygen and nitrogen species (RONS) can penetrate through the cell membrane. Specifically, we compare the permeability of various (hydrophilic and hydrophobic) RONS across both oxidized and non-oxidized cell membranes. We also study pore formation, and how it is hampered by higher concentrations of cholesterol in the cell membrane, and we illustrate the much higher permeability of H2O2 through aquaporin channels. Both mechanisms may explain the selective cytotoxic effect of plasma towards cancer cells. Finally, we also discuss the synergistic effect of plasma-induced oxidation and electric fields towards pore formation.

Keywords plasma medicine      cancer treatment      computer modelling      cell membrane      reactive oxygen and nitrogen species     
Corresponding Author(s): Annemie Bogaerts   
Online First Date: 21 March 2019    Issue Date: 22 May 2019
 Cite this article:   
Annemie Bogaerts,Maksudbek Yusupov,Jamoliddin Razzokov, et al. Plasma for cancer treatment: How can RONS penetrate through the cell membrane? Answers from computer modeling[J]. Front. Chem. Sci. Eng., 2019, 13(2): 253-263.
 URL:  
https://academic.hep.com.cn/fcse/EN/10.1007/s11705-018-1786-8
https://academic.hep.com.cn/fcse/EN/Y2019/V13/I2/253
Fig.1  Overview of the computational methods that allow to obtain atomic/molecular level insight in the interaction of plasma species with biomolecular systems, as a function of the attainable system sizes and time scales (QM= quantum mechanics, DFTB= density functional-tight binding, QM/MM= quantum mechanics/molecular mechanics, rMD= reactive molecular dynamics, nrMD= non-reactive molecular dynamics, uaMD= united-atom molecular dynamics, cgMD= coarse-grained molecular dynamics). Adopted from [35] with copyright permission
Fig.2  FEPs of the hydrophilic (a,b) and hydrophobic (c,d) ROS and RNS, across native and 50% oxidized PLBs. The PLB structure is drawn in pale color at the background, to indicate the position of the water layer, head groups and lipid tails
Fig.3  FEPs of H2O2 (upper part) and O2 (lower part) across the PLB, for various cholesterol concentrations in the cell membrane. Adopted from [12] with permission
Fig.4  Snapshot of MD simulations, at (a) 10 ns, (b) 40 ns and (c) 80 ns, illustrating pore formation in a model system of a PLB without cholesterol and 100% oxidation. A pore with diameter of ca. 15 Å is formed in (c). Adopted from [11] with permission
Fig.5  Calculated average water density in the center of the PLB, for model systems with 100% oxidation, as a function of cholesterol concentration in the PLB, indicating that pore formation occurs more easily in cell membranes containing less cholesterol, which is typical for cancer cells. This might be one of the explanations of the selectivity of plasma treatment for cancer cells vs. normal cells. Adopted from [11] with permission
Fig.6  Average pore formation time for three different electric field values, as a function of the oxidation degree of the PLB, for lipid oxidation into aldehydes. Adopted from [31] with permission
Fig.7  FEPs of H2O2 across (a) AQP1 and (b) the PLB. The cytoplasmic and extracellular water layers are shown in pink color. The associated standard deviations of the FEPs are shown in grey
1 MKeidar, R Walk, AShashurin, PSrinivasan, ASandler, SDasgupta, RRavi, R Guerrero-Preston, BTrink. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. British Journal of Cancer, 2011, 105(9): 1295–1301
https://doi.org/10.1038/bjc.2011.386
2 D BGraves. Reactive species from cold atmospheric plasma: Implications for cancer therapy. Plasma Processes and Polymers, 2014, 11(12): 1120–1127
https://doi.org/10.1002/ppap.201400068
3 XLu, G V Naidis, M Laroussi, SReuter, D BGraves, KOstrikov. Reactive species in non-equilibrium atmospheric-pressure plasmas: Generation, transport, and biological effects. Physics Reports, 2016, 630: 1–84
https://doi.org/10.1016/j.physrep.2016.03.003
4 P SHole, J Zabkiewicz, CMunje, ZNewton, LPearn, PWhite, NMarquez, R KHills, A KBurnett, ATonks, R LDarley. Overproduction of NOX-derived ROS in AML promotes proliferation and is associated with defective oxidative stress signaling. Blood, 2013, 122(19): 3322–3330
https://doi.org/10.1182/blood-2013-04-491944
5 M CPapadopoulos, SSaadoun. Key roles of aquaporins in tumor biology. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2015, 1848(10): 2576–2583
https://doi.org/10.1016/j.bbamem.2014.09.001
6 R MCordeiro. Molecular dynamics simulations of the transport of reactive oxygen species by mammalian and plant aquaporins. Biochimica et Biophysica Acta (BBA) - General Subjects, 2015, 1850(9): 1786–1794
https://doi.org/10.1016/j.bbagen.2015.05.007
7 DYan, A Talbot, NNourmohammadi, J HSherman, XCheng, MKeidar. Toward understanding the selective anticancer capacity of cold atmospheric plasma—a model based on aquaporins. Biointerphases, 2015, 10(4): 040801
https://doi.org/10.1116/1.4938020
8 JWong-Ekkabut, Z Xu, WTriampo, I MTang, D PTieleman, LMonticelli. Effect of lipid peroxidation on the properties of lipid bilayers: A molecular dynamics study. Biophysical Journal, 2007, 93(12): 4225–4236
https://doi.org/10.1529/biophysj.107.112565
9 LBeranova, L Cwiklik, PJurkiewicz, MHof, P Jungwirth. Oxidation changes physical properties of phospholipid bilayers: Fluorescence spectroscopy and molecular simulations. Langmuir, 2010, 26(9): 6140–6144
https://doi.org/10.1021/la100657a
10 LCwiklik, P Jungwirth. Massive oxidation of phospholipid membranes leads to pore creation and bilayer disintegration. Chemical Physics Letters, 2010, 486(4-6): 99–103
https://doi.org/10.1016/j.cplett.2010.01.010
11 JVan der Paal, E CNeyts, C C WVerlackt, ABogaerts. Effect of lipid peroxidation on membrane permeability of cancer and normal cells subjected to oxidative stress. Chemical Science (Cambridge), 2016, 7(1): 489–498
https://doi.org/10.1039/C5SC02311D
12 JVan der Paal, CVerheyen, E CNeyts, ABogaerts. Hampering effect of cholesterol on the permeation of reactive oxygen species through phospholipids bilayer: Possible explanation for plasma cancer selectivity. Scientific Reports, 2017, 7(1): 39526
https://doi.org/10.1038/srep39526
13 PSvarnas, S H Matrali, K Gazeli, S GAntimisiaris. Assessment of atmospheric-pressure guided streamer (plasma bullet) influence on liposomes with different composition and physicochemical properties. Plasma Processes and Polymers, 2015, 12(7): 655–665
https://doi.org/10.1002/ppap.201400218
14 A MHirst, F M Frame, M Arya, N JMaitland, DO’Connell. Low temperature plasmas as emerging cancer therapeutics: The state of play and thoughts for the future. Tumour Biology, 2016, 37(6): 7021–7031
https://doi.org/10.1007/s13277-016-4911-7
15 ERobert, T Darny, SDozias, SIseni, J MPouvesle. New insights on the propagation of pulsed atmospheric plasma streams: From single jet to multi jet arrays. Physics of Plasmas, 2015, 22(12): 122007
https://doi.org/10.1063/1.4934655
16 ABegum, M Laroussi, M RPervez. Atmospheric pressure He-air plasma jet: Breakdown process and propagation phenomenon. AIP Advances, 2013, 3(6): 062117
https://doi.org/10.1063/1.4811464
17 J CWeaver, K C Smith, A T Esser, R S Son, T Gowrishankar. A brief overview of electroporation pulse strength-duration space: A region where additional intracellular effects are expected. Bioelectrochemistry (Amsterdam, Netherlands), 2012, 87: 236–243
https://doi.org/10.1016/j.bioelechem.2012.02.007
18 P TVernier, M J Ziegler. Nanosecond field alignment of head group and water dipoles in electroporating phospholipid bilayers. Journal of Physical Chemistry B, 2007, 111(45): 12993–12996
https://doi.org/10.1021/jp077148q
19 MCasciola, M Tarek. A molecular insight into the electro-transfer of small molecules through electropores driven by electric fields. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2016, 1858(10): 2278–2289
https://doi.org/10.1016/j.bbamem.2016.03.022
20 S JMarrink, A H de Vries, D P Tieleman. Lipids on the move: simulations of membrane pores, domains, stalks and curves. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2009, 1788(1): 149–168
https://doi.org/10.1016/j.bbamem.2008.10.006
21 W YTai, Y C Yang, H J Lin, C P Huang, Y L Cheng, M F Chan, H L Yen, I Liau. Interplay between structure and fluidity of model lipid membranes under oxidative attack. Journal of Physical Chemistry B, 2010, 114(47): 15642–15649
https://doi.org/10.1021/jp1014719
22 EGrzelinska, G Bartosz, KGwozdzinski, WLeyko. A spin-label study of the effect of gamma radiation on erythrocyte membrane. Influence of lipid peroxidation on membrane structure. International Journal of Radiation Biology, 1979, 36: 325–334
23 M LWratten, G Van Ginkel, A AVan’t Veld, ABekker, E EVan Faassen, ASevanian. Structural and dynamic effects of oxidatively modified phospholipids in unsaturated lipid membranes. Biochemistry, 1992, 31(44): 10901–10907
https://doi.org/10.1021/bi00159a034
24 J JChen, B P Yu. Alterations in mitochondrial membrane fluidity by lipid peroxidation products. Free Radical Biology & Medicine, 1994, 17(5): 411–418
https://doi.org/10.1016/0891-5849(94)90167-8
25 CRichter. Biophysical consequences of lipid peroxidation in membranes. Chemistry and Physics of Lipids, 1987, 44(2-4): 175–189
https://doi.org/10.1016/0009-3084(87)90049-1
26 R PMason, M F Walter, P E Mason. Effect of oxidative stress on membrane structure: Small-angle X-ray diffraction analysis. Free Radical Biology & Medicine, 1997, 23(3): 419–425
https://doi.org/10.1016/S0891-5849(97)00101-9
27 E JSzili, S H Hong, R D Short. On the effect of serum on the transport of reactive oxygen species across phospholipid membranes. Biointerphases, 2015, 10(2): 029511
https://doi.org/10.1116/1.4918765
28 E HLee, J Hsin, MSotomayor, GComellas, KSchulten. Discovery through the computational microscope. Structure (London, England), 2009, 17(10): 1295–1306
https://doi.org/10.1016/j.str.2009.09.001
29 R MCordeiro. Reactive oxygen species at phospholipid bilayers: Distribution, mobility and permeation. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2014, 1838(1): 438–444
https://doi.org/10.1016/j.bbamem.2013.09.016
30 RMiotto, E B Costa, E B Trellese, A J P Neto, M S Baptista, A C Ferraz, R M Cordeiro. Biomembranes under oxidative stress, Insights from molecular dynamics simulations. In: Tran Q N, Arabnia H R, eds. Emerging Trends in Applications and Infrastructures for Computational Biology, Bioinformatics, and Systems Biology: Systems and Applications. Amsterdam: Elsevier, 2016, 197–211
31 MYusupov, J Van der Paal, E CNeyts, ABogaerts. Synergistic effect of electric field and lipid oxidation on the permeability of cell membranes. Biochimica et Biophysica Acta (BBA) - General, 2017, 1861: 839–847
32 MYusupov, K Wende, SKupsch, E CNeyts, SReuter, ABogaerts. Effect of head group and lipid tail oxidation in the cell membrane revealed through integrated simulations and experiments. Scientific Reports, 2017, 7(1): 5761
https://doi.org/10.1038/s41598-017-06412-8
33 MYusupov, D Yan, R MCordeiro, ABogaerts. Atomic scale simulation of H2O2 permeation through aquaporin: Toward the understanding of plasma-cancer treatment. Journal of Physics. D, Applied Physics, 2018, 51(12): 125401
https://doi.org/10.1088/1361-6463/aaae7a
34 JRazzokov, M Yusupov, R MCordeiro, ABogaerts. Atomic scale understanding of the permeation of plasma species across native and oxidized membranes. Journal of Physics. D, Applied Physics, 2018, 51(36): 365203
https://doi.org/10.1088/1361-6463/aad524
35 ABogaerts, N Khosravian, JVan der Paal, C C WVerlackt, MYusupov, BKamaraj, E CNeyts. Multi-level molecular modeling for plasma medicine. Journal of Physics. D, Applied Physics, 2016, 49(5): 054002
https://doi.org/10.1088/0022-3727/49/5/054002
36 MElstner, D Porezag, GJungnickel, JElsner, MHaugk, ThFrauenheim, SSuhai, GSeifert. Self-consistent-charge density-functional tight-binding method for simulations of complex materials properties. Physical Review. B, 1998, 58(11): 7260–7268
https://doi.org/10.1103/PhysRevB.58.7260
37 NKhosravian, B Kamaraj, E CNeyts, ABogaerts. Structural modification of P-glycoprotein induced by OH radicals: Insights from atomistic simulations. Scientific Reports, 2016, 6(1): 19466
https://doi.org/10.1038/srep19466
38 C C WVerlackt, WVan Boxem, DDewaele, FLemière, FSobott, JBenedikt, E CNeyts, ABogaerts. Mechanisms of peptide oxidation by hydroxyl radicals: Insight at the molecular scale. Journal of Physical Chemistry C, 2017, 121(10): 5787–5799
https://doi.org/10.1021/acs.jpcc.6b12278
39 C C WVerlackt, E CNeyts, ABogaerts. Atomic scale behavior of oxygen-based radicals in water. Journal of Physics. D, Applied Physics, 2017, 50(11): 11LT01
https://doi.org/10.1088/1361-6463/aa5c60
40 D WBrenner. Empirical potential for hydrocarbons for use in simulating the chemical vapor deposition of diamond films. Physical Review. B, 1990, 42(15): 9458–9471
https://doi.org/10.1103/PhysRevB.42.9458
41 A C Tvan Duin, SDasgupta, FLorant, W AGoddard, F FReax. A reactive force field for hydrocarbons. Journal of Physical Chemistry A, 2001, 105(41): 9396–9409
https://doi.org/10.1021/jp004368u
42 MYusupov, E C Neyts, U Khalilov, RSnoeckx, A C Tvan Duin, ABogaerts. Atomic scale simulations of plasma species interacting with bacterial cell walls. New Journal of Physics, 2012, 14(9): 093043
https://doi.org/10.1088/1367-2630/14/9/093043
43 MYusupov, A Bogaerts, SHuygh, SSnoeckx, A C Tvan Duin, E CNeyts. Plasma-induced destruction of bacterial cell wall components: A reactive molecular dynamics simulation. Journal of Physical Chemistry C, 2013, 117(11): 5993–5998
https://doi.org/10.1021/jp3128516
44 MYusupov, E C Neyts, C C Verlackt, U Khalilov, A C Tvan Duin, ABogaerts. Inactivation of the endotoxic biomolecule lipid A by oxygen plasma species: A reactive molecular dynamics study. Plasma Processes and Polymers, 2015, 12(2): 162–171
https://doi.org/10.1002/ppap.201400064
45 N YBabaeva, N Ning, D BGraves, M JKushner. Ion activation energy delivered to wounds by atmospheric pressure dielectric-barrier discharges: Sputtering of lipid-like surfaces. Journal of Physics. D, Applied Physics, 2012, 45(11): 115203
https://doi.org/10.1088/0022-3727/45/11/115203
46 JVan der Paal, SAernouts, A C Tvan Duin, E CNeyts, ABogaerts. Interaction of O and OH radicals with a simple model system for lipids in the skin barrier: A reactive molecular dynamics simulation for plasma medicine. Journal of Physics. D, Applied Physics, 2013, 46(39): 395201
https://doi.org/10.1088/0022-3727/46/39/395201
47 JVan der Paal, C CVerlackt, MYusupov, E CNeyts, ABogaerts. Structural modification of the skin barrier by OH radicals: A reactive molecular dynamics study for plasma medicine. Journal of Physics. D, Applied Physics, 2015, 48(15): 155202
https://doi.org/10.1088/0022-3727/48/15/155202
48 R MAbolfath, P K Biswas, R Rajnarayanam, TBrabec, RKodym, LPapiez. Multiscale QM/MM molecular dynamics study on the first steps of guanine damage by free hydroxyl radicals in solution. Journal of Physical Chemistry A, 2012, 116(15): 3940–3945
https://doi.org/10.1021/jp300258n
49 C C MVerlackt, E CNeyts, TJacob, DFantauzzi, MGolkaram, Y KShin, A C Tvan Duin, ABogaerts. Atomic-scale insight in the interactions between hydroxyl radicals and DNA in solution using the ReaxFF reactive force field. New Journal of Physics, 2015, 17(10): 103005
https://doi.org/10.1088/1367-2630/17/10/103005
50 MYusupov, E C Neyts, P Simon, GBergiyorov, RSnoeckx, A C Tvan Duin, ABogaerts. Reactive molecular dynamics simulations of oxygen species in a liquid water layer of interest for plasma medicine. Journal of Physics. D, Applied Physics, 2014, 47(2): 025205
https://doi.org/10.1088/0022-3727/47/2/025205
51 NKhosravian, A Bogaerts, SHuygh, MYusupov, E CNeyts. How do plasma-generated OH radicals react with biofilm components? Insights from atomic scale simulations. Biointerphases, 2015, 10(2): 029501
https://doi.org/10.1116/1.4904339
52 OBerger, O Edholm, FJähnig. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophysical Journal, 1997, 72(5): 2002–2013
https://doi.org/10.1016/S0006-3495(97)78845-3
53 W DCornell, P Cieplak, C IBayly, I RGould, K MMerz Jr, D MFerguson, D CSpellmeyer, TFox, J W Caldwell, P A Kollman. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. Journal of the American Chemical Society, 1995, 117(19): 5179–5197
https://doi.org/10.1021/ja00124a002
54 WYu, X He, KVanommeslaeghe, A DMacKerell Jr. Extension of the CHARMM general force field to sulfonyl-containing compounds and its utility in biomolecular simulations. Journal of Computational Chemistry, 2012, 33(31): 2451–2468
https://doi.org/10.1002/jcc.23067
55 W Fvan Gunsteren, H J CBerendsen. Groningen Molecular Simulation (GROMOS) Library Manual. Groningen, The Netherlands: Biomos, 1987, 1–221
56 S JMarrink, H J Risselada, S Yefimov, D PTieleman, A HDe Vries. The MARTINI force field: Coarse grained model for biomolecular simulations. Journal of Physical Chemistry B, 2007, 111(27): 7812–7824
https://doi.org/10.1021/jp071097f
57 JÅqvist, A Warshel. Simulation of enzyme reactions using valence bond force fields and other hybrid quantum/classical approaches. Chemical Reviews, 1993, 93(7): 2523–2544
https://doi.org/10.1021/cr00023a010
58 E CNeyts, M Yusupov, C CVerlackt, ABogaerts. Computer simulations of plasma-biomolecule and plasma-tissue interactions for a better insight in plasma medicine. Journal of Physics. D, Applied Physics, 2014, 47(29): 293001
https://doi.org/10.1088/0022-3727/47/29/293001
59 M NMöller, QLi, J R Jr Lancaster, A Denicola. Acceleration of nitric oxide autoxidation and nitrosation by membranes. IUBMB Life, 2007, 59(4): 243–248
https://doi.org/10.1080/15216540701311147
60 W KSubczynski, MLomnicka, J SHyde. Permeability of nitric oxide through lipid bilayer membranes. Free Radical Research, 1996, 24(5): 343–349
https://doi.org/10.3109/10715769609088032
61 MShinitzky. Membrane fluidity in malignancy adversative and recuperative. Biochimica et Biophysica Acta (BBA) - Revue Canadienne, 1984, 738: 251–261
62 AReis, M R M Domingues, F M L Amado, A J V Ferrer-Correia, P Domingues. Separation of peroxidation products of diacyl-phosphatidylcholines by reversed-phase liquid chromatography-mass spectrometry. Biomedical Chromatography, 2005, 19(2): 129–137
https://doi.org/10.1002/bmc.429
63 C KHaluska, M S Baptista, A U Fernades, A P Schroder, C M Marques, R Itri. Photo-activated phase separation in giant vesicles made from different lipid mixture. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2012, 1818: 666–672
https://doi.org/10.1016/j.bbamem.2011.11.025
64 J WLackmann, S Schneider, EEdengeiser, FJarzina, SBrinckmann, ESteinborn, MHavenith, JBenedikt, J EBandow. Photons and particles emitted from cold atmospheric-pressure plasma inactivate bacteria and biomolecules independently and synergistically. Journal of the Royal Society, Interface, 2013, 10(89): 20130591
https://doi.org/10.1098/rsif.2013.0591
65 T YChung, N Ning, J WChu, D BGraves, EBartis, JSeog, G S Oehrlein. Plasma deactivation of endotoxic biomolecules: Vacuum ultraviolet photon and radical beam effects on Lipid A. Plasma Processes and Polymers, 2013, 10(2): 167–180
https://doi.org/10.1002/ppap.201200087
66 E A JBartis, D BGraves, JSeog, G S Oehrlein. Atmospheric pressure plasma treatment of lipopolysaccharide in a controlled environment. Journal of Physics. D, Applied Physics, 2013, 46(31): 312002 doi:10.1088/0022-3727/46/31/312002
67 E A JBartis, CBarrett, T YChung, NNing, J W Chu, D B Graves, J Seog, G SOehrlein. Deactivation of lipopolysaccharide by Ar and H2 inductively coupled low-pressure plasma. Journal of Physics. D, Applied Physics, 2014, 47(4): 045202
https://doi.org/10.1088/0022-3727/47/4/045202
68 J HPark, N Kumar, D HPark, MYusupov, E CNeyts, C C WVerlackt, ABogaerts, M HKang, H SUhm, E HChoi, et al. A comparative study for the inactivation of multidrug resistance bacteria using dielectric barrier discharge and nano-second pulsed plasma. Scientific Reports, 2015, 5(1): 13849
https://doi.org/10.1038/srep13849
69 MMarschewski, J Hirschberg, TOmairi, OHofft, WViol, S Emmert, WMaus-Friedrichs. Electron spectroscopic analysis of the human lipid skin barrier: Cold atmospheric plasma-induced changes in lipid composition. Experimental Dermatology, 2012, 21(12): 921–925
https://doi.org/10.1111/exd.12043
70 ETakai, T Kitamura, JKuwabara, SIkawa, SYoshizawa, KShiraki, HKawasaki, RArakawa, KKitano. Chemical modification of amino acids by atmospheric-pressure cold plasma in aqueous solution. Journal of Physics. D, Applied Physics, 2014, 47(28): 285403
https://doi.org/10.1088/0022-3727/47/28/285403
71 G SMadugundu, JCadet, J RWagner. Hydroxyl-radical-induced oxidation of 5-methylcytosine in isolated and cellular DNA. Nucleic Acids Research, 2014, 42(11): 7450–7460
https://doi.org/10.1093/nar/gku334
72 S HHong, E J Szili, A T A Jenkins, R D Short. Ionized gas (plasma) delivery of reactive oxygen species (ROS) into artificial cells. Journal of Physics. D, Applied Physics, 2014, 47(36): 362001
https://doi.org/10.1088/0022-3727/47/36/362001
73 E JSzili, J W Bradley, R D Short. A ‘tissue model’ to study the plasma delivery of reactive oxygen species. Journal of Physics. D, Applied Physics, 2014, 47(15): 152002
https://doi.org/10.1088/0022-3727/47/15/152002
74 M UHammer, E Forbrig, SKupsch, K DWeltmann, SReuter. Influence of plasma treatment on the structure and function of lipids. Plasma Medicine, 2013, 3(1-2): 97–114
https://doi.org/10.1615/PlasmaMed.2014009708
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