Cold atmospheric plasma, a novel promising anti-cancer treatment modality

Oncotarget

Volumn 8, Issue 9, 2017, Pages 15977-15995

  Yan, Dayun ^a   Sherman, Jonathan H ^b   Keidar, Michael ^a  

^a The George Washington University   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Cancer treatment; Cold plasma; Reactive species; Selectivity

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BLADDER TUMOR; CANCER CELL DESTRUCTION; CANCER CELL LINE; CELL MEMBRANE; CELL SHAPE; COLD ATMOSPHERIC PLASMA; CYTOTOXICITY; DIFFUSION; DNA DAMAGE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; NONHUMAN; OXIDATION REDUCTION STATE; PHYSICAL MEDICINE; REVIEW; TUMOR XENOGRAFT; COLD; DRUG THERAPY; NEOPLASM; PLASMA GAS;

COLD TEMPERATURE; HUMANS; NEOPLASMS; PLASMA GASES;

EID: 85014095449     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.13304     Document Type: Review

References (162)

1. Tendero C, Tixier C, Tristant P, Desmaison J and Leprince P. Atmospheric pressure plasmas: A review. Spectrochimica Acta Part B: Atomic Spectroscopy. 2006; 61(1):2-30.
2. Lee HJ, Shon CH, Kim YS, Kim S, Kim GC and Kong MG. Degradation of adhesion molecules of G361 melanoma cells by a non-thermal atmospheric pressure microplasma. New Journal of Physics. 2009; 11(11):115026.
3. Park GY, Park SJ, Choi MY, Koo IG, Byun JH, Hong JW, Sim JY, Collins GJ and Lee JK. Atmospheric-pressure plasma sources for biomedical applications. Plasma Sources Science and Technology. 2012; 21(4):043001.
4. Cheng X, Sherman J, Murphy W, Ratovitski E, Canady J and Keidar M. The Effect of Tuning Cold Plasma Composition on Glioblastoma Cell Viability. PloS one. 2014; 9(5):e98652.
5. Kalghatgi S, Kelly CM, Cerchar E, Torabi B, Alekseev O, Fridman A, Friedman G and Azizkhan-Clifford J. Effects of non-thermal plasma on mammalian cells. PloS one. 2011; 6(1):e16270.
6. Laroussi M and Akan T. Arc-Free Atmospheric Pressure Cold Plasma Jets: A Review. Plasma Processes and Polymers. 2007; 4(9):777-788.
7. Fridman G, Friedman G, Gutsol A, Shekhter AB, Vasilets VN and Fridman A. Applied Plasma Medicine. Plasma Processes and Polymers. 2008; 5(6):503-533.
8. Laroussi M. Low-temperature plasmas for medicine? Plasma Science, IEEE Transactions on. 2009; 37(6):714-725.
9. Graves DB. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. Journal of Physics D: Applied Physics. 2012; 45(26):263001.
10. Weltmann KD, Kindel E, von Woedtke T, Hähnel M, Stieber M and Brandenburg R. Atmospheric-pressure plasma sources: prospective tools for plasma medicine. Pure and Applied Chemistry. 2010; 82(6):1223-1237.
11. Jeong J, Babayan S, Tu V, Park J, Henins I, Hicks R and Selwyn G. Etching materials with an atmospheric-pressure plasma jet. Plasma Sources Science and Technology. 1998; 7(3):282.
12. Kogelschatz U. Dielectric-barrier discharges: their history, discharge physics, and industrial applications. Plasma chemistry and plasma processing. 2003; 23(1):1-46.
13. Wagner H-E, Brandenburg R, Kozlov K, Sonnenfeld A, Michel P and Behnke J. The barrier discharge: basic properties and applications to surface treatment. Vacuum. 2003; 71(3):417-436.
14. Shashurin A, Shneider MN, Dogariu A, Miles RB and Keidar M. Temporary-resolved measurement of electron density in small atmospheric plasmas. Applied Physics Letters. 2010; 96(17):171502.
15. Georgescu N and Lupu AR. Tumoral and normal cells treatment with high-voltage pulsed cold atmospheric plasma jets. Plasma Science, IEEE Transactions on. 2010; 38(8):1949-1955.
16. Kim JY, Kim S-O, Wei Y and Li J. A flexible cold microplasma jet using biocompatible dielectric tubes for cancer therapy. Applied Physics Letters. 2010; 96(20):203701.
17. Yan X, Xiong Z, Zou F, Zhao S, Lu X, Yang G, He G and Ostrikov KK. Plasma-Induced Death of HepG2 Cancer Cells: Intracellular Effects of Reactive Species. Plasma Processes and Polymers. 2012; 9(1):59-66.
18. Ja Kim S, Min Joh H and Chung TH. Production of intracellular reactive oxygen species and change of cell viability induced by atmospheric pressure plasma in normal and cancer cells. Applied Physics Letters. 2013; 103(15):153705.
19. Fridman G, Shereshevsky A, Jost MM, Brooks AD, Fridman A, Gutsol A, Vasilets V and Friedman G. Floating Electrode Dielectric Barrier Discharge Plasma in Air Promoting Apoptotic Behavior in Melanoma Skin Cancer Cell Lines. Plasma Chemistry and Plasma Processing. 2007; 27(2):163-176.
20. Vandamme M, Robert E, Dozias S, Sobilo J, Lerondel S, Le Pape A and Pouvesle J-M. Response of human glioma U87 xenografted on mice to non thermal plasma treatment. Plasma medicine. 2011; 1(1):27-43.
21. Kaushik NK, Uhm H and Ha Choi E. Micronucleus formation induced by dielectric barrier discharge plasma exposure in brain cancer cells. Applied Physics Letters. 2012; 100(8):084102.
22. Arjunan KP, Friedman G, Fridman A and Clyne AM. Non-thermal dielectric barrier discharge plasma induces angiogenesis through reactive oxygen species. Journal of the Royal Society, Interface /the Royal Society. 2012; 9(66):147-157.
23. Barekzi N and Laroussi M. Dose-dependent killing of leukemia cells by low-temperature plasma. Journal of Physics D: Applied Physics. 2012; 45(42):422002.
24. Laroussi M, Mohades S and Barekzi N. Killing adherent and nonadherent cancer cells with the plasma pencil. Biointerphases. 2015; 10(2):029401.
25. Zhang X, Li M, Zhou R, Feng K and Yang S. Ablation of liver cancer cells in vitro by a plasma needle. Applied Physics Letters. 2008; 93(2):021502.
26. Zirnheld JL, Zucker SN, DiSanto TM, Berezney R and Etemadi K. Nonthermal plasma needle: development and targeting of melanoma cells. Plasma Science, IEEE Transactions on. 2010; 38(4):948-952.
27. Vandamme M, Robert E, Lerondel S, Sarron V, Ries D, Dozias S, Sobilo J, Gosset D, Kieda C, Legrain B, Pouvesle JM and Pape AL. ROS implication in a new antitumor strategy based on non-thermal plasma. International journal of cancer. 2012; 130(9):2185-2194.
28. Laroussi M, Richardson JP and Dobbs FC. Effects of nonequilibrium atmospheric pressure plasmas on the heterotrophic pathways of bacteria and on their cell morphology. Applied Physics Letters. 2002; 81(4):772.
29. Shashurin A, Stepp MA, Hawley TS, Pal-Ghosh S, Brieda L, Bronnikov S, Jurjus RA and Keidar M. Influence of Cold Plasma Atmospheric Jet on Surface Integrin Expression of Living Cells. Plasma Processes and Polymers. 2010; 7(3-4):294-300.
30. Brulle L, Vandamme M, Ries D, Martel E, Robert E, Lerondel S, Trichet V, Richard S, Pouvesle JM and Le Pape A. Effects of a non thermal plasma treatment alone or in combination with gemcitabine in a MIA PaCa2-luc orthotopic pancreatic carcinoma model. PloS one. 2012; 7(12):e52653.
31. Iseki S, Nakamura K, Hayashi M, Tanaka H, Kondo H, Kajiyama H, Kano H, Kikkawa F and Hori M. Selective killing of ovarian cancer cells through induction of apoptosis by nonequilibrium atmospheric pressure plasma. Applied Physics Letters. 2012; 100(11):113702.
32. Partecke LI, Evert K, Haugk J, Doering F, Normann L, Diedrich S, Weiss FU, Evert M, Huebner NO, Guenther C, Heidecke CD, Kramer A, Bussiahn R, Weltmann KD, Pati O, Bender C, et al. Tissue tolerable plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo. BMC cancer. 2012; 12:473.
33. Panngom K, Baik KY, Nam MK, Han JH, Rhim H and Choi EH. Preferential killing of human lung cancer cell lines with mitochondrial dysfunction by nonthermal dielectric barrier discharge plasma. Cell death & disease. 2013; 4:e642.
34. Ma RN, Feng HQ, Liang YD, Zhang Q, Tian Y, Su B, Zhang J and Fang J. An atmospheric-pressure cold plasma leads to apoptosis inSaccharomyces cerevisiaeby accumulating intracellular reactive oxygen species and calcium. Journal of Physics D: Applied Physics. 2013; 46(28):285401.
35. Reuter S, Tresp H, Wende K, Hammer MU, Winter J, Masur K, Schmidt-Bleker A and Weltmann K. From RONS to ROS: tailoring plasma jet treatment of skin cells. Plasma Science, IEEE Transactions on. 2012; 40(11):2986-2993.
36. Han X, Klas M, Liu Y, Sharon Stack M and Ptasinska S. DNA damage in oral cancer cells induced by nitrogen atmospheric pressure plasma jets. Applied Physics Letters. 2013; 102(23):233703.
37. Zhao S, Xiong Z, Mao X, Meng D, Lei Q, Li Y, Deng P, Chen M, Tu M, Lu X, Yang G and He G. Atmospheric pressure room temperature plasma jets facilitate oxidative and nitrative stress and lead to endoplasmic reticulum stress dependent apoptosis in HepG2 cells. PloS one. 2013; 8(8):e73665.
38. Kim GJ, Kim W, Kim KT and Lee JK. DNA damage and mitochondria dysfunction in cell apoptosis induced by nonthermal air plasma. Applied Physics Letters. 2010; 96(2):021502.
39. Lu X, Naidis GV, Laroussi M, Reuter S, Graves DB and Ostrikov K. Reactive species in non-equilibrium atmospheric-pressure plasmas: Generation, transport, and biological effects. Physics Reports. 2016; 630:1-84.
40. Barekzi N and Laroussi M. Effects of Low Temperature Plasmas on Cancer Cells. Plasma Processes and Polymers. 2013; 10(12):1039-1050.
41. Keidar M, Shashurin A, Volotskova O, Ann Stepp M, Srinivasan P, Sandler A and Trink B. Cold atmospheric plasma in cancer therapy. Physics of Plasmas. 2013; 20(5):057101.
42. Schlegel J, Köritzer J and Boxhammer V. Plasma in cancer treatment. Clinical Plasma Medicine. 2013; 1(2):2-7.
43. Ratovitski EA, Cheng X, Yan D, Sherman JH, Canady J, Trink B and Keidar M. Anti-Cancer Therapies of 21st Century: Novel Approach to Treat Human Cancers Using Cold Atmospheric Plasma. Plasma Processes and Polymers. 2014; 11(12):1128-1137.
44. Keidar M. Plasma for cancer treatment. Plasma Sources Science and Technology. 2015; 24(3):033001.
45. Hirst AM, Frame FM, Arya M, Maitland NJ and O'Connell D. Low temperature plasmas as emerging cancer therapeutics: the state of play and thoughts for the future. Tumour biology. 2016; 37(6):7021-7031.
46. Keidar M, Walk R, Shashurin A, Srinivasan P, Sandler A, Dasgupta S, Ravi R, Guerrero-Preston R and Trink B. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. British journal of cancer. 2011; 105(9):1295-1301.
47. Tanaka H, Mizuno M, Ishikawa K, Nakamura K, Kajiyama H, Kano H, Kikkawa F and Hori M. Plasma-Activated Medium Selectively Kills Glioblastoma Brain Tumor Cells by Down-Regulating a Survival Signaling Molecule, AKT Kinase. Plasma Medicine. 2011; 1(3-4).
48. Kaushik NK, Attri P, Kaushik N and Choi EH. A preliminary study of the effect of DBD plasma and osmolytes on T98G brain cancer and HEK non-malignant cells. Molecules. 2013; 18(5):4917-4928.
49. Kim GC, Kim GJ, Park SR, Jeon SM, Seo HJ, Iza F and Lee JK. Air plasma coupled with antibody-conjugated nanoparticles: a new weapon against cancer. Journal of Physics D: Applied Physics. 2009; 42(3):032005.
50. Kim SJ, Chung TH, Bae SH and Leem SH. Induction of apoptosis in human breast cancer cells by a pulsed atmospheric pressure plasma jet. Applied Physics Letters. 2010; 97(2):023702.
51. Ninomiya K, Ishijima T, Imamura M, Yamahara T, Enomoto H, Takahashi K, Tanaka Y, Uesugi Y and Shimizu N. Evaluation of extra-and intracellular OH radical generation, cancer cell injury, and apoptosis induced by a non-thermal atmospheric-pressure plasma jet. Journal of Physics D: Applied Physics. 2013; 46(42):425401.
52. Wang M, Holmes B, Cheng X, Zhu W, Keidar M and Zhang LG. Cold Atmospheric Plasma for Selectively Ablating Metastatic Breast Cancer Cells. PloS one. 2013; 8(9):e73741.
53. Ishaq M, Evans MDM and Ostrikov K. 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. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2014; 1843(12):2827-2837.
54. Plewa J-M, Yousfi M, Frongia C, Eichwald O, Ducommun B, Merbahi N and Lobjois V. Low-temperature plasmainduced antiproliferative effects on multi-cellular tumor spheroids. New Journal of Physics. 2014; 16(4):043027.
55. Kim JY, Ballato J, Foy P, Hawkins T, Wei Y, Li J and Kim SO. Apoptosis of lung carcinoma cells induced by a flexible optical fiber-based cold microplasma. Biosensors & bioelectronics. 2011; 28(1):333-338.
56. Ahn HJ, Kim KI, Hoan NN, Kim CH, Moon E, Choi KS, Yang SS and Lee JS. Targeting cancer cells with reactive oxygen and nitrogen species generated by atmosphericpressure air plasma. PloS one. 2014; 9(1):e86173.
57. Kim K, Jun Ahn H, Lee J-H, Kim J-H, Sik Yang S and Lee J-S. Cellular membrane collapse by atmospheric-pressure plasma jet. Applied Physics Letters. 2014; 104(1):013701.
58. Tan X, Zhao S, Lei Q, Lu X, He G and Ostrikov K. Single-Cell-Precision Microplasma-Induced Cancer Cell Apoptosis. PloS one. 2014; 9(6):e101299.
59. Thiyagarajan M, Waldbeser L and Whitmill A. THP-1 leukemia cancer treatment using a portable plasma device. Studies in health technology and informatics. 2011; 173:515-517.
60. Thiyagarajan M, Anderson H and Gonzales XF. Induction of apoptosis in human myeloid leukemia cells by remote exposure of resistive barrier cold plasma. Biotechnology and bioengineering. 2014; 111(3):565-574.
61. Guerrero-Preston R, Ogawa T, Uemura M, Shumulinsky G, Valle BL, Pirini F, Ravi R, Sidransky D, Keidar M and Trink B. Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells. International journal of molecular medicine. 2014; 34(4):941-946.
62. Kang SU, Cho JH, Chang JW, Shin YS, Kim KI, Park JK, Yang SS, Lee JS, Moon E, Lee K and Kim CH. Nonthermal plasma induces head and neck cancer cell death: the potential involvement of mitogen-activated protein kinasedependent mitochondrial reactive oxygen species. Cell death & disease. 2014; 5:e1056.
63. Metelmann H-R, Nedrelow DS, Seebauer C, Schuster M, von Woedtke T, Weltmann K-D, Kindler S, Metelmann PH, Finkelstein SE, Von Hoff DD and Podmelle F. Head and neck cancer treatment and physical plasma. Clinical Plasma Medicine. 2015; 3(1):17-23.
64. Koritzer J, Boxhammer V, Schafer A, Shimizu T, Klampfl TG, Li YF, Welz C, Schwenk-Zieger S, Morfill GE, Zimmermann JL and Schlegel J. Restoration of sensitivity in chemo-resistant glioma cells by cold atmospheric plasma. PloS one. 2013; 8(5):e64498.
65. Ishaq M, Han ZJ, Kumar S, Evans MD and Ostrikov KK. Atmospheric-Pressure Plasma-and TRAIL-Induced Apoptosis in TRAIL-Resistant Colorectal Cancer Cells. Plasma Processes and Polymers. 2015; 12(6):574-582.
66. Yan D, Nourmohammadi N, Talbot A, Sherman JH and Keidar M. The strong anti-glioblastoma capacity of the plasma-stimulated lysine-rich medium. Journal of Physics D: Applied Physics. 2016; 49(27):274001.
67. Cheng X, Murphy W, Recek N, Yan D, Cvelbar U, Vesel A, Mozetic M, Canady J, Keidar M and Sherman JH. Synergistic effect of gold nanoparticles and cold plasma on glioblastoma cancer therapy. Journal of Physics D: Applied Physics. 2014; 47(33):335402.
68. Lee JH, Om JY, Kim YH, Kim KM, Choi EH and Kim KN. 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(2):e0150279.
69. Park JH, Kumar N, Park DH, Yusupov M, Neyts EC, Verlackt CC, Bogaerts A, Kang MH, Uhm HS, Choi EH and Attri P. A comparative study for the inactivation of multidrug resistance bacteria using dielectric barrier discharge and nano-second pulsed plasma. Scientific reports. 2015; 5:13849.
70. Yan D, Sherman JH, Cheng X, Ratovitski E, Canady J and Keidar M. Controlling plasma stimulated media in cancer treatment application. Applied Physics Letters. 2014; 105(22):224101.
71. Utsumi F, Kajiyama H, Nakamura K, Tanaka H, Mizuno M, Ishikawa K, Kondo H, Kano H, Hori M and Kikkawa F. Effect of indirect nonequilibrium atmospheric pressure plasma on anti-proliferative activity against chronic chemoresistant ovarian cancer cells in vitro and in vivo. PloS one. 2013; 8(12):e81576.
72. Yokoyama M, Johkura K and Sato T. Gene expression responses of HeLa cells to chemical species generated by an atmospheric plasma flow. Biochem Biophys Res Commun. 2014; 450(4):1266-1271.
73. Mohades S, Laroussi M, Sears J, Barekzi N and Razavi H. Evaluation of the effects of a plasma activated medium on cancer cells. Physics of Plasmas. 2015; 22(12):122001.
74. Yang H, Lu R, Xian Y, Gan L, Lu X and Yang X. Effects of atmospheric pressure cold plasma on human hepatocarcinoma cell and its 5-fluorouracil resistant cell line. Physics of Plasmas. 2015; 22(12):122006.
75. Yan D, Nourmohammadi N, Bian K, Murad F, Sherman JH and Keidar M. Stabilizing the cold plasma-stimulated medium by regulating medium's composition. Scientific reports. 2016; 6:26016.
76. Adachi T, Nonomura S, Horiba M, Hirayama T, Kamiya T, Nagasawa H and Hara H. Iron stimulates plasma-activated medium-induced A549 cell injury. Scientific reports. 2016; 6:20928.
77. Judee F, Fongia C, Ducommun B, Yousfi M, Lobjois V and Merbahi N. Short and long time effects of low temperature Plasma Activated Media on 3D multicellular tumor spheroids. Scientific reports. 2016; 6:21421.
78. Kumar N, Park JH, Jeon SN, Park BS, Choi EH and Attri P. The action of microsecond-pulsed plasma-activated media on the inactivation of human lung cancer cells. Journal of Physics D: Applied Physics. 2016; 49(11):115401.
79. Kurake N, Tanaka H, Ishikawa K, Kondo T, Sekine M, Nakamura K, Kajiyama H, Kikkawa F, Mizuno M and Hori M. Cell survival of glioblastoma grown in medium containing hydrogen peroxide and/or nitrite, or in plasmaactivated medium. Arch Biochem Biophys. 2016; 605:102-108.
80. Boehm D, Heslin C, Cullen PJ and Bourke P. Cytotoxic and mutagenic potential of solutions exposed to cold atmospheric plasma. Scientific reports. 2016; 6:21464.
81. Kaushik N, Kumar N, Kim CH, Kaushik NK and Choi EH. Dielectric Barrier Discharge Plasma Efficiently Delivers an Apoptotic Response in Human Monocytic Lymphoma. Plasma Processes and Polymers. 2014; 11(12):1175-1187.
82. Takai E, Kitamura T, Kuwabara J, Ikawa S, Yoshizawa S, Shiraki K, Kawasaki H, Arakawa R and Kitano K. Chemical modification of amino acids by atmospheric-pressure cold plasma in aqueous solution. Journal of Physics D: Applied Physics. 2014; 47(28):285403.
83. Yan D, Talbot A, Nourmohammadi N, Cheng X, Canady J, Sherman J and Keidar M. Principles of using Cold Atmospheric Plasma Stimulated Media for Cancer Treatment. Scientific reports. 2015; 5:18339.
84. Ma Y, Ha CS, Hwang SW, Lee HJ, Kim GC, Lee K-W and Song K. Non-Thermal Atmospheric Pressure Plasma Preferentially Induces Apoptosis in p53-Mutated Cancer Cells by Activating ROS Stress-Response Pathways. PloS one. 2014; 9(4):e91947.
85. Gibson AR, McCarthy HO, Ali AA, O'Connell D and Graham WG. Interactions of a non-thermal atmospheric pressure plasma effluent with PC-3 prostate cancer cells. Plasma Processes and Polymers. 2014; 11(12):1142-1149.
86. Lukes P, Dolezalova E, Sisrova I and Clupek M. Aqueousphase chemistry and bactericidal effects from an air discharge plasma in contact with water: evidence for the formation of peroxynitrite through a pseudo-secondorder post-discharge reaction of H2O2and HNO2. Plasma Sources Science and Technology. 2014; 23(1):015019.
87. Walk RM, Snyder JA, Srinivasan P, Kirsch J, Diaz SO, Blanco FC, Shashurin A, Keidar M and Sandler AD. Cold atmospheric plasma for the ablative treatment of neuroblastoma. Journal of pediatric surgery. 2013; 48(1):67-73.
88. Mirpour S, Piroozmand S, Soleimani N, Jalali Faharani N, Ghomi H, Fotovat Eskandari H, Sharifi AM, Mirpour S, Eftekhari M and Nikkhah M. Utilizing the micron sized non-thermal atmospheric pressure plasma inside the animal body for the tumor treatment application. Scientific reports. 2016; 6:29048.
89. Yajima I, Iida M, Kumasaka MY, Omata Y, Ohgami N, Chang J, Ichihara S, Hori M and Kato M. Non-equilibrium atmospheric pressure plasmas modulate cell cycle-related gene expressions in melanocytic tumors of RET-transgenic mice. Experimental dermatology. 2014; 23(6):424-425.
90. Chernets N, Kurpad DS, Alexeev V, Rodrigues DB and Freeman TA. Reaction Chemistry Generated by Nanosecond Pulsed Dielectric Barrier Discharge Treatment is Responsible for the Tumor Eradication in the B16 Melanoma Mouse Model. Plasma Processes and Polymers. 2015; 12(12):1400-1409.
91. Gaur N, Szili EJ, Oh J-S, Hong S-H, Michelmore A, Graves DB, Hatta A and Short RD. Combined effect of protein and oxygen on reactive oxygen and nitrogen species in the plasma treatment of tissue. Applied Physics Letters. 2015; 107(10):103703.
92. Miller V, Lin A and Fridman A. Why target immune cells for plasma treatment of cancer. Plasma Chemistry and Plasma Processing. 2016; 36(1):259-268.
93. Lin A, Truong B, Pappas A, Kirifides L, Oubarri A, Chen S, Lin S, Dobrynin D, Fridman G and Fridman A. Uniform Nanosecond Pulsed Dielectric Barrier Discharge Plasma Enhances Anti-Tumor Effects by Induction of Immunogenic Cell Death in Tumors and Stimulation of Macrophages. Plasma Processes and Polymers. 2015; 12(12):1392-1399.
94. Miller V, Lin A, Fridman G, Dobrynin D and Fridman A. Plasma Stimulation of Migration of Macrophages. Plasma Processes and Polymers. 2014; 11(12):1193-1197.
95. Schoenbach KH, Abou-Ghazala A, Vithoulkas T, Alden RW, Turner R and Beebe S. (1997). The effect of pulsed electrical fields on biological cells. Pulsed Power Conference, 1997 Digest of Technical Papers 1997 11th IEEE International: IEEE), pp. 73-78.
96. Kaushik NK, Kaushik N, Park D and Choi EH. Altered Antioxidant System Stimulates Dielectric Barrier Discharge Plasma-Induced Cell Death for Solid Tumor Cell Treatment. PloS one. 2014; 9(7):e103349.
97. Gibson AR, McCarthy HO, Ali AA, O'Connell D and Graham WG. Interactions of a Non-Thermal Atmospheric Pressure Plasma Effluent with PC-3 Prostate Cancer Cells. Plasma Processes and Polymers. 2014; 11(12):1142-1149.
98. Tanaka H, Mizuno M, Toyokuni S, Maruyama S, Kodera Y, Terasaki H, Adachi T, Kato M, Kikkawa F and Hori M. Cancer therapy using non-thermal atmospheric pressure plasma with ultra-high electron density. Physics of Plasmas. 2015; 22(12):122004.
99. Adachi T, Tanaka H, Nonomura S, Hara H, Kondo S and Hori M. Plasma-activated medium induces A549 cell injury via a spiral apoptotic cascade involving the mitochondrialnuclear network. Free radical biology & medicine. 2014; 79C:28-44.
100. Bekeschus S, Kolata J, Winterbourn C, Kramer A, Turner R, Weltmann KD, Bröker B and Masur K. Hydrogen peroxide: A central player in physical plasma-induced oxidative stress in human blood cells. Free Radical Research. 2014; 48(5):542-549.
101. Lopez-Lazaro M. Dual role of hydrogen peroxide in cancer: possible relevance to cancer chemoprevention and therapy. Cancer letters. 2007; 252(1):1-8.
102. Nathan CF and Cohn ZA. Antitumor effects of hydrogen peroxide in vivo. The Journal of experimental medicine. 1981; 154(5):1539-1553.
103. Girard PM, Arbabian A, Fleury M, Bauville G, Puech V, Dutreix M and Sousa JS. Synergistic Effect of H2O2 and NO2 in Cell Death Induced by Cold Atmospheric He Plasma. Scientific reports. 2016; 6:29098.
104. Chang JW, Kang SU, Shin YS, Kim KI, Seo SJ, Yang SS, Lee J-S, Moon E, Lee K and Kim C-H. Non-Thermal Atmospheric Pressure Plasma Inhibits Thyroid Papillary Cancer Cell Invasion via Cytoskeletal Modulation, Altered MMP-2/-9/uPA Activity. PloS one. 2014; 9(3):e92198.
105. Recek N, Cheng X, Keidar M, Cvelbar U, Vesel A, Mozetic M and Sherman J. Effect of cold plasma on glial cell morphology studied by atomic force microscopy. PloS one. 2015; 10(3):e0119111.
106. Naciri M, Dowling D and Al-Rubeai M. Differential Sensitivity of Mammalian Cell Lines to Non-Thermal Atmospheric Plasma. Plasma Processes and Polymers. 2014; 11(4):391-400.
107. Marla SS, Lee J and Groves JT. Peroxynitrite rapidly permeates phospholipid membranes. Proceedings of the National Academy of Sciences. 1997; 94(26):14243-14248.
108. Denicola A, Souza JM and Radi R. Diffusion of peroxynitrite across erythrocyte membranes. Proceedings of the National Academy of Sciences. 1998; 95(7):3566-3571.
109. Galvan A and Fernandez E. Eukaryotic nitrate and nitrite transporters. Cellular and Molecular Life Sciences. 2001; 58(2):225-233.
110. Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P and Yasui M. Characterization of aquaporin-6 as a nitrate channel in mammalian cells requirement of pore-lining residue threonine 63. Journal of Biological Chemistry. 2002; 277(42):39873-39879.
111. Agre P. Aquaporin water channels (Nobel Lecture). Angewandte Chemie. 2004; 43(33):4278-4290.
112. Wu B and Beitz E. Aquaporins with selectivity for unconventional permeants. Cellular and molecular life sciences. 2007; 64(18):2413-2421.
113. Bienert GP and Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochimica et biophysica acta. 2014; 1840(5):1596-1604.
114. Miller EW, Dickinson BC and Chang CJ. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proceedings of the National Academy of Sciences. 2010; 107(36):15681-15686.
115. Almasalmeh A, Krenc D, Wu B and Beitz E. Structural determinants of the hydrogen peroxide permeability of aquaporins. The FEBS journal. 2014; 281(3):647-656.
116. Kawasaki T, Kusumegi S, Kudo A, Sakanoshita T, Tsurumaru T, Sato A, Uchida G, Koga K and Shiratani M. Effects of irradiation distance on supply of reactive oxygen species to the bottom of a Petri dish filled with liquid by an atmospheric O2/He plasma jet. Journal of Applied Physics. 2016; 119(17):173301.
117. Herrera M, Hong NJ and Garvin JL. Aquaporin-1 transports NO across cell membranes. Hypertension. 2006; 48(1):157-164.
118. Finkel T. Signal transduction by reactive oxygen species. The Journal of cell biology. 2011; 194(1):7-15.
119. Yan D, Talbot A, Nourmohammadi N, Sherman JH, Cheng X and Keidar M. Toward understanding the selective anticancer capacity of cold atmospheric plasma-A model based on aquaporins (Review). Biointerphases. 2015; 10(4):040801.
120. Ahn HJ, Kim KI, Kim G, Moon E, Yang SS and Lee J-S. Atmospheric-pressure plasma jet induces apoptosis involving mitochondria via generation of free radicals. PloS one. 2011; 6(11):e28154.
121. Cox AG, Winterbourn CC and Hampton MB. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. The Biochemical journal. 2010; 425(2):313-325.
122. Sandalova T, Zhong L, Lindqvist Y, Holmgren A and Schneider G. Three-dimensional structure of a mammalian thioredoxin reductase: implications for mechanism and evolution of a selenocysteine-dependent enzyme. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98(17):9533-9538.
123. Fritz-Wolf K, Kehr S, Stumpf M, Rahlfs S and Becker K. Crystal structure of the human thioredoxin reductasethioredoxin complex. Nature communications. 2011; 2:383.
124. Andreyev AY, Kushnareva YE and Starkov A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Moscow). 2005; 70(2):200-214.
125. Filomeni G, Rotilio G and Ciriolo MR. Cell signalling and the glutathione redox system. Biochemical pharmacology. 2002; 64(5-6):1057-1064.
126. Weiss M, Gumbel D, Hanschmann EM, Mandelkow R, Gelbrich N, Zimmermann U, Walther R, Ekkernkamp A, Sckell A, Kramer A, Burchardt M, Lillig CH and Stope MB. Cold Atmospheric Plasma Treatment Induces Anti-Proliferative Effects in Prostate Cancer Cells by Redox and Apoptotic Signaling Pathways. PloS one. 2015; 10(7):e0130350.
127. Ishaq M, Kumar S, Varinli H, Han ZJ, Rider AE, Evans MD, Murphy AB and Ostrikov K. Atmospheric gas plasmainduced ROS production activates TNF-ASK1 pathway for the induction of melanoma cancer cell apoptosis. Molecular biology of the cell. 2014; 25(9):1523-1531.
128. Kastan MB. DNA Damage Responses: Mechanisms and Roles in Human Disease 2007 GHA Clowes Memorial Award Lecture. Molecular Cancer Research. 2008; 6(4):517-524.
129. Chang JW, Kang SU, Shin YS, Kim KI, Seo SJ, Yang SS, Lee J-S, Moon E, Baek SJ, Lee K and Kim C-H. Nonthermal atmospheric pressure plasma induces apoptosis in oral cavity squamous cell carcinoma: Involvement of DNA-damage-triggering sub-G1 arrest via the ATM/p53 pathway. Archives of Biochemistry and Biophysics. 2014; 545(0):133-140.
130. Arndt S, Wacker E, Li YF, Shimizu T, Thomas HM, Morfill GE, Karrer S, Zimmermann JL and Bosserhoff AK. Cold atmospheric plasma, a new strategy to induce senescence in melanoma cells. Experimental dermatology. 2013; 22(4):284-289.
131. Ishaq M, Bazaka K and Ostrikov K. Intracellular effects of atmospheric-pressure plasmas on melanoma cancer cells. Physics of Plasmas. 2015; 22(12):122003.
132. Joerger AC and Fersht AR. Structural biology of the tumor suppressor p53. Annual review of biochemistry. 2008; 77:557-582.
133. Volotskova O, Hawley TS, Stepp MA and Keidar M. Targeting the cancer cell cycle by cold atmospheric plasma. Scientific reports. 2012; 2:636.
134. Gherardi M, Turrini E, Laurita R, De Gianni E, Ferruzzi L, Liguori A, Stancampiano A, Colombo V and Fimognari C. Atmospheric Non-Equilibrium Plasma Promotes Cell Death and Cell-Cycle Arrest in a Lymphoma Cell Line. Plasma Processes and Polymers. 2015; 12(12):1354-1363.
135. Yan N and Shi Y. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol. 2005; 21:35-56.
136. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES and Wang X. Cytochrome c and dATPdependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997; 91(4):479-489.
137. Yuan S, Yu X, Asara JM, Heuser JE, Ludtke SJ and Akey CW. The holo-apoptosome: activation of procaspase-9 and interactions with caspase-3. Structure. 2011; 19(8):1084-1096.
138. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang H-G, Reed JC, Nicholson DW and Alnemri ES. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2,-3,-6,-7,-8, and-10 in a caspase-9-dependent manner. The Journal of cell biology. 1999; 144(2):281-292.
139. Zou H, Li Y, Liu X and Wang X. An APAF-1[middle dot]Cytochrome c Multimeric Complex Is a Functional Apoptosome That Activates Procaspase-9. Journal of Biological Chemistry. 1999; 274(17):11549-11556.
140. Zou H, Henzel WJ, Liu X, Lutschg A and Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997; 90(3):405-413.
141. Ishaq M, Bazaka K and Ostrikov K. Pro-apoptotic NOXA is implicated in atmospheric-pressure plasma-induced melanoma cell death. Journal of Physics D: Applied Physics. 2015; 48(46):464002.
142. Kaushik N, Uddin N, Sim GB, Hong YJ, Baik KY, Kim CH, Lee SJ, Kaushik NK and Choi EH. Responses of solid tumor cells in DMEM to reactive oxygen species generated by non-thermal plasma and chemically induced ROS systems. Scientific reports. 2015; 5:8587.
143. Wang C, Zhang H, Xue Z, Yin H, Niu Q and Chen H. The relation between doses or post-plasma time points and apoptosis of leukemia cells induced by dielectric barrier discharge plasma. AIP Advances. 2015; 5(12):127220.
144. Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Molecular cell. 2002; 9(3):459-470.
145. Kim SJ and Chung TH. Cold atmospheric plasma jet generated RONS and their selective effects on normal and carcinoma cells. Scientific reports. 2016; 6:20332.
146. Hirst AM, Simms MS, Mann VM, Maitland NJ, O'Connell D and Frame FM. Low-temperature plasma treatment induces DNA damage leading to necrotic cell death in primary prostate epithelial cells. British journal of cancer. 2015; 112(9):1536-1545.
147. Trachootham D, Alexandre J and Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nature reviews Drug discovery. 2009; 8(7):579-591.
148. Cairns RA, Harris IS and Mak TW. Regulation of cancer cell metabolism. Nature reviews Cancer. 2011; 11(2):85-95.
149. Wang J and Yi J. Cancer cell killing via ROS. Cancer Biol Ther. 2008; 7(12):1875-1884.
150. Cairns RA, Harris I, McCracken S and Mak TW. Cancer cell metabolism. Cold Spring Harbor symposia on quantitative biology. 2011; 76:299-311.
151. Papadopoulos MC and Saadoun S. Key roles of aquaporins in tumor biology. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2015; 1848(10):2576-2583.
152. Zhu SJ, Wang KJ, Gan SW, Xu J, Xu SY and Sun SQ. Expression of aquaporin8 in human astrocytomas: correlation with pathologic grade. Biochem Biophys Res Commun. 2013; 440(1):168-172.
153. Bienert GP, Schjoerring JK and Jahn TP. Membrane transport of hydrogen peroxide. Biochimica et biophysica acta. 2006; 1758(8):994-1003.
154. Glorieux C, Dejeans N, Sid B, Beck R, Calderon PB and Verrax J. Catalase overexpression in mammary cancer cells leads to a less aggressive phenotype and an altered response to chemotherapy. Biochemical pharmacology. 2011; 82(10):1384-1390.
155. Matés JM, Pérez-Gómez C and De Castro IN. Antioxidant enzymes and human diseases. Clinical biochemistry. 1999; 32(8):595-603.
156. Nguyen NH, Park HJ, Yang SS, Choi KS and Lee JS. Anticancer efficacy of nonthermal plasma dissolved in a liquid, liquid plasma in heterogeneous cancer cells. Scientific reports. 2016; 6:29020.
157. Glorieux C, Zamocky M, Sandoval JM, Verrax J and Calderon PB. Regulation of catalase expression in healthy and cancerous cells. Free radical biology & medicine. 2015; 87:84-97.
158. Hasegawa Y, Takano T, Miyauchi A, Matsuzuka F, Yoshida H, Kuma K and Amino N. Decreased expression of catalase mRNA in thyroid anaplastic carcinoma. Japanese journal of clinical oncology. 2003; 33(1):6-9.
159. Asaduzzaman Khan M, Tania M, Zhang D-Z and Chen H-c. Antioxidant enzymes and cancer. Chinese Journal of Cancer Research. 2010; 22(2):87-92.
160. Kaynar H, Meral M, Turhan H, Keles M, Celik G and Akcay F. Glutathione peroxidase, glutathione-Stransferase, catalase, xanthine oxidase, Cu-Zn superoxide dismutase activities, total glutathione, nitric oxide, and malondialdehyde levels in erythrocytes of patients with small cell and non-small cell lung cancer. Cancer letters. 2005; 227(2):133-139.
161. Hwang TS, Choi HK and Han HS. Differential expression of manganese superoxide dismutase, copper/zinc superoxide dismutase, and catalase in gastric adenocarcinoma and normal gastric mucosa. European journal of surgical oncology. 2007; 33(4):474-479.
162. Hempel N, Ye H, Abessi B, Mian B and Melendez JA. Altered redox status accompanies progression to metastatic human bladder cancer. Free radical biology & medicine. 2009; 46(1):42-50.