|
|
Application of Low-Temperature Atmospheric-Pressure Plasma in Oncology |
Qi Ying1, Yu Mengjie2, Hou Zhongyu2, Yao Yu1* |
1(Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, China) 2(School of Electronic Information and ElectricalEngineering,Shanghai Jiaotong University, Shanghai 200240, China) |
|
|
Abstract Plasma medicine is an emerging field focusing on the application of plasma in medicine. In this review, we provided a brief overview of the low-temperature atmospheric-pressure plasma (LT-APP) first, and then focused on the application of LT-APP in oncology. In oncological application, direct plasma treatment to tumor cells can induce the apoptosis, necrosis and autophagy by generating large amounts of reactive agents; Plasma can also kill the cancer cells indirectly via the cytotoxicity of plasma activated liquids. On the other hand, plasma also has several non-fatal effects on tumors as well. In addition, plasma plays an important role in the field of anti-cancer drugs by participating in the construction of sustained-release systems of chemotherapeutic drugs, assisting drug transportation, and having a synergistic anti-tumor effect with traditional chemotherapeutic drugs.
|
Received: 01 November 2018
|
|
|
|
|
[1] Fridman G, Friedman G, Gutsol A, et al. Applied plasma medicine[J]. Plasma Processes and Polymers, 2008, 5(6): 503-533. [2] Fridman G, Brooks A D, Balasubramanian M, et al. Comparison of direct and indirect effects of non-thermal atmospheric-pressure plasma on bacteria[J]. Plasma Processes and Polymers, 2007, 4(4): 370-375. [3] Kalghatgi SU, Fridman G, Cooper M, et al. Mechanism of blood coagulation by nonthermal atmospheric pressure dielectric barrier discharge plasma[J]. IEEE Transactions on plasma science, 2007, 35(5): 1559-1566. [4] Heinlin J, Morfill G, Landthaler M, et al. Plasma medicine: possible applications in dermatology[J]. JDDG: Journal der Deutschen Dermatologischen Gesellschaft, 2010, 8(12): 968-976. [5] Von Woedtke T, Haertel B, Weltmann KD, et al. Plasma pharmacy–physical plasma in pharmaceutical applications[J]. Die Pharmazie-An International Journal of Pharmaceutical Sciences, 2013, 68(7): 492-498. [6] Hirst AM, Frame FM, Arya M, et al. Low temperature plasmas as emerging cancer therapeutics: The state of play and thoughts for the future[J]. Tumor Biology, 2016, 37(6): 7021-7031. [7] Morozov A I. Introduction to plasma dynamics[M]. New York: CRC Press, 2012. [8] Biberman L M, Vorob'Ev V S, Yakubov I T, et al. Kinetics of Nonequilibrium Low-Temperature Plasmas[J]. Physics Today, 1989, 42(4): 65-66. [9] Schutze A, Jeong JY, Babayan SE, et al. The atmospheric-pressure plasma jet: a review and comparison to other plasma sources[J]. IEEE Transactions on Plasma Science, 1998, 26(6): 1685-1694. [10] Setsuhara Y. Low-temperature atmospheric-pressure plasma sources for plasma medicine[J]. Archives of biochemistry and biophysics, 2016, 605: 3-10. [11] Stoffels E, Sakiyama Y, Graves DB. Cold atmospheric plasma: charged species and their interactions with cells and tissues[J]. IEEE Transactions on Plasma Science, 2008, 36(4): 1441-1457. [12] Graves DB. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology[J]. Journal of Physics D: Applied Physics, 2012, 45(26): 263001. [13] Graves DB. Mechanisms of plasma medicine: Coupling plasma physics, biochemistry, and biology[J]. IEEE Transactions on Radiation and Plasma Medical Sciences, 2017, 1(4): 281-292. [14] Sosnin EA, Stoffels E, Erofeev MV, et al. The effects of UV irradiation and gas plasma treatment on living mammalian cells and bacteria: a comparative approach[J]. IEEE Transactions on Plasma Science, 2004, 32(4): 1544-1550. [15] Gakidou E, Afshin A, Abajobir A A, et al. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016[J]. The Lancet, 2017, 390(10100): 1345-1422. [16] Vandamme M, Robert E, Lerondel S, et al. ROS implication in a new antitumor strategy based on non-thermal plasma[J]. International Journal of Cancer, 2012, 130(9): 2185-2194. [17] Gorrini C, Harris IS, Mak TW. Modulation of oxidative stress as an anticancer strategy[J]. Nature reviews Drug Discovery, 2013, 12(12): 931-947. [18] Raj L, Ide T, Gurkar AU, et al. Selective killing of cancer cells by a small molecule targeting the stress response to ROS[J]. Nature, 2011, 475(7355): 231-234. [19] Yan X, Xiong Z, Zou F, et al. Plasma-induced death of HepG2 cancer cells: intracellular effects of reactive species[J]. Plasma Processes and Polymers, 2012, 9(1): 59-66. [20] Marla SS, Lee J, Groves JT. Peroxynitrite rapidly permeates phospholipid membranes[J]. Proceedings of the National Academy of Sciences, 1997, 94(26): 14243-14248. [21] Yan D, Talbot A, Nourmohammadi N, et al. Toward understanding the selective anticancer capacity of cold atmospheric plasma—A model based on aquaporins[J]. Biointerphases, 2015, 10(4): 040801. [22] Lee HJ, Shon CH, Kim YS, et al. Degradation of adhesion molecules of G361 melanoma cells by a non-thermal atmospheric pressure microplasma[J]. New Journal of Physics, 2009, 11(11): 115026. [23] Shashurin A, Stepp MA, Hawley TS, et al. Influence of cold plasma atmospheric jet on surface integrin expression of living cells[J]. Plasma Processes and Polymers, 2010, 7(3-4): 294-300. [24] Chang J W, Kang S U, Shin Y S, et al. Non-thermal atmospheric pressure plasma inhibits thyroid papillary cancer cell invasion via cytoskeletal modulation, altered MMP-2/-9/uPA activity[J]. PLoS ONE, 2014, 9(3): e92198. [25] Wang M, Holmes B, Cheng X, et al. Cold atmospheric plasma for selectively ablating metastatic breast cancer cells[J]. PLoS ONE, 2013, 8(9): e73741. [26] Ja Kim S, Min Joh H, Chung TH. Production of intracellular reactive oxygen species and change of cell viability induced by atmospheric pressure plasma in normal and cancer cells[J]. Applied Physics Letters, 2013, 103(15): 153705. [27] Ahn HJ, Kim KI, Hoan NN, et al. Targeting cancer cells with reactive oxygen and nitrogen species generated by atmospheric-pressure air plasma[J]. PLoS ONE, 2014, 9(1): e86173. [28] Ninomiya K, Ishijima T, Imamura M, et al. Evaluation of extra-and intracellular OH radical generation, cancer cell injury, and apoptosis induced by a non-thermal atmospheric-pressure plasma jet[J]. Journal of Physics D: Applied Physics, 2013, 46(42): 425401. [29] Ishaq M, Evans MD, Ostrikov KK. Atmospheric pressure gas plasma-induced colorectal cancer cell death is mediated by Nox2-ASK1 apoptosis pathways and oxidative stress is mitigated by Srx-Nrf2 anti-oxidant system[J]. Biochim Biophys Acta, 2014, 1843(12): 2827-2837. [30] Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species[J]. Biochemistry (Moscow), 2005, 70(2): 200-214. [31] Kaushik NK, Kaushik N, Park D, et al. Altered antioxidant system stimulates dielectric barrier discharge plasma-induced cell death for solid tumor cell treatment[J]. PLoS ONE, 2014, 9(7): e103349. [32] Weiss M, Gümbel D, Hanschmann E-M, et al. Cold atmospheric plasma treatment induces anti-proliferative effects in prostate cancer cells by redox and apoptotic signaling pathways[J]. PLoS ONE, 2015, 10(7): e0130350. [33] Judée F, Fongia C, Ducommun B, et al. Short and long time effects of low temperature plasma activated media on 3D multicellular tumor spheroids[J]. Scientific Reports, 2016, 6: 21421. [34] Kang SU, Cho JH, Chang JW, et al. Nonthermal plasma induces head and neck cancer cell death: the potential involvement of mitogen-activated protein kinase-dependent mitochondrial reactive oxygen species[J]. Cell Death & Disease, 2014, 5(2): e1056. [35] Hong SH, Szili EJ, Fenech M, et al. Genotoxicity and cytotoxicity of the plasma jet-treated medium on lymphoblastoid WIL2-NS cell line using the cytokinesis block micronucleus cytome assay[J]. Scientific Reports, 2017, 7(1): 3854. [36] Yan D, Sherman JH, Keidar M. Cold atmospheric plasma, a novel promising anti-cancer treatment modality[J]. Oncotarget, 2017, 8(9): 15977. [37] Han X, Klas M, Liu Y, et al. DNA damage in oral cancer cells induced by nitrogen atmospheric pressure plasma jets[J]. Applied Physics Letters, 2013, 102(23): 233703. [38] Kim GJ, Kim W, Kim KT, et al. DNA damage and mitochondria dysfunction in cell apoptosis induced by nonthermal air plasma[J]. Applied Physics Letters, 2010, 96(2): 021502. [39] Ma Y, Ha CS, Hwang SW, et al. Non-thermal atmospheric pressure plasma preferentially induces apoptosis in p53-mutated cancer cells by activating ROS stress-response pathways[J]. PLoS ONE, 2014, 9(4): e91947. [40] Ishaq M, Kumar S, Varinli H, et al. Atmospheric gas plasma–induced ROS production activates TNF-ASK1 pathway for the induction of melanoma cancer cell apoptosis[J]. Molecular Biology of the Cell, 2014, 25(9): 1523-1531. [41] Hirst AM, Simms MS, Mann VM, et al. Low-temperature plasma treatment induces DNA damage leading to necrotic cell death in primary prostate epithelial cells[J]. British Journal of Cancer, 2015, 112(9): 1536-1545. [42] Siu A, Volotskova O, Cheng X, et al. Differential effects of cold atmospheric plasma in the treatment of malignant glioma[J]. PLoS ONE, 2015, 10(6): e0126313. [43] Dobrynin D, Fridman G, Friedman G, et al. Physical and biological mechanisms of direct plasma interaction with living tissue[J]. New Journal of Physics, 2009, 11(11): 115020. [44] Fridman G, Shereshevsky A, Jost MM, et al. Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines[J]. Plasma Chemistry and Plasma Processing, 2007, 27(2): 163-176. [45] Yan D, Talbot A, Nourmohammadi N, et al. Principles of using cold atmospheric plasma stimulated media for cancer treatment[J]. Scientific Reports, 2015, 5: 18339. [46] Cheng X, Sherman J, Murphy W, et al. The effect of tuning cold plasma composition on glioblastoma cell viability[J]. PLoS ONE, 2014, 9(5): e98652. [47] Kaushik N, Attri P, Kaushik N, et al. A preliminary study of the effect of DBD plasma and osmolytes on T98G brain cancer and HEK non-malignant cells[J]. Molecules, 2013, 18(5): 4917-4928. [48] Cheng X, Murphy W, Recek N, et al. Synergistic effect of gold nanoparticles and cold plasma on glioblastoma cancer therapy[J]. Journal of Physics D: Applied Physics, 2014, 47(33): 335402. [49] Kaushik N, Lee S J, Choi T G, et al. Non-thermal plasma with 2-deoxy-D-glucose synergistically induces cell death by targeting glycolysis in blood cancer cells[J]. Scientific Reports, 2015, 5: 8726. [50] Boehm D, Curtin J, Cullen PJ, et al. Hydrogen peroxide and beyond-the potential of high-voltage plasma-activated liquids against cancerous cells[J]. Anti-Cancer Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry-Anti-Cancer Agents), 2018, 18(6): 815-823. [51] Zhang Q, Liang Y, Feng H, et al. A study of oxidative stress induced by non-thermal plasma-activated water for bacterial damage[J]. Applied Physics Letters, 2013, 102(20): 203701. [52] Oehmigen K, Winter J, Hähnel M, et al. Estimation of possible mechanisms of Escherichia coli inactivation by plasma treated sodium chloride solution[J]. Plasma Processes and Polymers, 2011, 8(10): 904-913. [53] Boehm D, Heslin C, Cullen PJ, et al. Cytotoxic and mutagenic potential of solutions exposed to cold atmospheric plasma[J]. Scientific Reports, 2016, 6: 21464. [54] Tanaka H, Mizuno M, Ishikawa K, et al. Cell survival and proliferation signaling pathways are downregulated by plasma-activated medium in glioblastoma brain tumor cells[J]. Plasma Medicine, 2012, 2(4): 207-220. [55] Winter J, Tresp H, Hammer MU, et al. Tracking plasma generated H2O2 from gas into liquid phase and revealing its dominant impact on human skin cells[J]. Journal of Physics D: Applied Physics, 2014, 47(28): 285401. [56] Van Gils CAJ, Hofmann S, Boekema B, et al. Mechanisms of bacterial inactivation in the liquid phase induced by a remote RF cold atmospheric pressure plasma jet[J]. Journal of Physics D: Applied Physics, 2013, 46(17): 175203. [57] Mokhtari H, Farahmand L, Yaserian K, et al. The antiproliferative effects of cold atmospheric plasma-activated media on different cancer cell lines, the implication of ozone as a possible underlying mechanism[J]. J Cell Physiol, 2019, 234(5): 6778-6782. [58] Lukes P, Dolezalova E, Sisrova I, et al. Aqueous-phase chemistry and bactericidal effects from an air discharge plasma in contact with water: evidence for the formation of peroxynitrite through a pseudo-second-order post-discharge reaction of H2O2 and HNO2[J]. Plasma Sources Science and Technology, 2014, 23(1): 015019. [59] Wende K, Williams P, Dalluge J, et al. Identification of the biologically active liquid chemistry induced by a nonthermal atmospheric pressure plasma jet[J]. Biointerphases, 2015, 10(2): 029518. [60] Lu X, Naidis G V, Laroussi M, et al. Reactive species in non-equilibrium atmospheric-pressure plasmas: Generation, transport, and biological effects[J]. Physics Reports, 2016, 630: 1-84. [61] Metelmann HR, Seebauer C, Miller V, et al. Clinical experience with cold plasma in the treatment of locally advanced head and neck cancer[J]. Clinical Plasma Medicine, 2018, 9: 6-13. [62] Kos S, Blagus T, Cemazar M, et al. Safety aspects of atmospheric pressure helium plasma jet operation on skin: In vivo study on mouse skin[J]. PLoS ONE, 2017, 12(4): e0174966. [63] Chakravarthy K, Dobrynin D, Fridman G, et al. Cold spark discharge plasma treatment of inflammatory bowel disease in an animal model of ulcerative colitis[J]. Plasma Medicine, 2011, 1(1): 3-19. [64] Utsumi F, Kajiyama H, Nakamura K, et al. Effect of indirect nonequilibrium atmospheric pressure plasma on anti-proliferative activity against chronic chemo-resistant ovarian cancer cells in vitro and in vivo[J]. PLoS ONE, 2013, 8(12): e81576. [65] Gweon B, Kim H, Kim K, et al. Suppression of angiogenesis by atmospheric pressure plasma in human aortic endothelial cells[J]. Applied Physics Letters, 2014, 104(13): 133701. [66] Xu D, Luo X, Xu Y, et al. The effects of cold atmospheric plasma on cell adhesion, differentiation, migration, apoptosis and drug sensitivity of multiple myeloma[J]. Biochemical and Biophysical Research Communications, 2016, 473(4): 1125-1132. [67] Ikeda JI, Tsuruta Y, Nojima S, et al. Anti-cancer effects of nonequilibrium atmospheric pressure plasma on cancer-initiating cells in human endometrioid adenocarcinoma cells[J]. Plasma Processes and Polymers, 2015, 12(12): 1370-1376. [68] Schierholz JM, Steinhauser H, Rump AFE, et al. Controlled release of antibiotics from biomedical polyurethanes: morphological and structural features[J]. Biomaterials, 1997, 18(12): 839-844. [69] Lu J, Choi E, Tamanoi F, et al. Light-activated nanoimpeller-controlled drug release in cancer cells[J]. Small, 2008, 4(4): 421-426. [70] Vilar G, Tulla-Puche J, Albericio F. Polymers and drug delivery systems[J]. Current Drug Delivery, 2012, 9(4): 367-394. [71] Uhrich KE, Cannizzaro SM, Langer RS, et al. Polymeric systems for controlled drug release[J]. Chemical Reviews, 1999, 99(11): 3181-3198. [72] Schröder K, MeyerPlath A, Keller D, et al. Plasma-induced surface functionalization of polymeric biomaterials in ammonia plasma[J]. Contributions to Plasma Physics, 2001, 41(6): 562-572. [73] Petlin DG, Tverdokhlebov SI, Anissimov YG. Plasma treatment as an efficient tool for controlled drug release from polymeric materials: a review[J]. Journal of Controlled Release, 2017, 266: 57-74. [74] Myung SW, Jung SC, Kim BH. Immobilization and controlled release of drug using plasma polymerized thin film[J]. Thin Solid Films, 2015, 584: 13-17. [75] Susut C, Timmons RB. Plasma enhanced chemical vapor depositions to encapsulate crystals in thin polymeric films: a new approach to controlling drug release rates[J]. International Journal of Pharmaceutics, 2005, 288(2): 253-261. [76] Stloukal P, Novák I, Micˇušík M, et al. Effect of plasma treatment on the release kinetics of a chemotherapy drug from biodegradable polyester films and polyester urethane films[J]. International Journal of Polymeric Materials and Polymeric Biomaterials, 2018, 67(3): 161-173. [77] Mayor S. Side-effects of cancer drugs are under-reported in trials[J]. Lancet Oncol, 2015, 16(3): e107. [78] Zhou J, Yu G, Huang F. Supramolecular chemotherapy based on host-guest molecular recognition: a novel strategy in the battle against cancer with a bright future[J]. Chem Soc Rev, 2017, 46(22): 7021-7053. [79] Stewart MP, Sharei A, Ding X, et al. In vitro and ex vivo strategies for intracellular delivery[J]. Nature, 2016, 538(7624): 183-192. [80] Leduc M, Guay D, Leask RL, et al. Cell permeabilization using a non-thermal plasma[J]. New Journal of Physics, 2009, 11(11): 115021. [81] Sasaki S, Honda R, Hokari Y, et al. Characterization of plasma-induced cell membrane permeabilization: focus on OH radical distribution[J]. Journal of Physics D: Applied Physics, 2016, 49(33): 334002. [82] Ikeda Y, Motomura H, Kido Y, et al. Effects of molecular size and chemical factor on plasma gene transfection[J]. Japanese Journal of Applied Physics, 2016, 55(7S2): 07LG06. [83] Fluhr JW, Sassning S, Lademann O, et al. In vivo skin treatment with tissue-tolerable plasma influences skin physiology and antioxidant profile in human stratum corneum[J]. Experimental Dermatology, 2012, 21(2): 130-134. [84] Lademann O, Richter H, Meinke MC, et al. Drug delivery through the skin barrier enhanced by treatment with tissue-tolerable plasma[J]. Experimental Dermatology, 2011, 20(6): 488-490. [85] Lademann J, Patzelt A, Richter H, et al. Nanocapsules for drug delivery through the skin barrier by tissue-tolerable plasma[J]. Laser Physics Letters, 2013, 10(8): 083001. [86] Choi J-H, Nam S-H, Song Y-S, et al. Treatment with low-temperature atmospheric pressure plasma enhances cutaneous delivery of epidermal growth factor by regulating E-cadherin-mediated cell junctions[J]. Archives of Dermatological Research, 2014, 306(7): 635-643. [87] Shimizu K, Hayashida K, Blajan M. Novel method to improve transdermal drug delivery by atmospheric microplasma irradiation[J]. Biointerphases, 2015, 10(2): 029517. [88] Conway GE, Casey A, Milosavljevic V, et al. Non-thermal atmospheric plasma induces ROS-independent cell death in U373MG glioma cells and augments the cytotoxicity of temozolomide[J]. British Journal of Cancer, 2016, 114(4): 435-443. [89] Köritzer J, Boxhammer V, Schäfer A, et al. Restoration of sensitivity in chemo—resistant glioma cells by cold atmospheric plasma[J]. PLoS ONE, 2013, 8(5): e64498. [90] Yang H, Lu R, Xian Y, et al. Effects of atmospheric pressure cold plasma on human hepatocarcinoma cell and its 5-fluorouracil resistant cell line[J]. Physics of Plasmas, 2015, 22(12): 122006. [91] Brullé L, Vandamme M, Riès D, et al. Effects of a non thermal plasma treatment alone or in combination with gemcitabine in a MIA PaCa2-luc orthotopic pancreatic carcinoma model[J]. PLoS ONE, 2012, 7(12): e52653. |
|
|
|