Effects of atmospheric pressure plasmas on isolated and cellular DNA—a review

International Journal of Molecular Sciences

Volumn 16, Issue 2, 2015, Pages 2971-3016

  Arjunan, Krishna Priya ^a   Sharma, Virender K ^b   Ptasinska, Sylwia ^a,c  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; CYCLIN DEPENDENT KINASE; NUCLEIC ACID BASE; PROTEIN P21; PROTEIN P53; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; ATM PROTEIN; DNA; NUCLEOSIDE; PLASMA GAS;

ARTICLE; ATMOSPHERIC PRESSURE PLASMA; CELL CYCLE CHECKPOINT; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EXCISION REPAIR; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; INFRARED SPECTROSCOPY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OXIDATIVE STRESS; PLASMA; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RAMAN SPECTROMETRY; CHEMISTRY; METABOLISM; PLASMA GAS; RADIATION RESPONSE; TOXICITY;

EUKARYOTA; PROKARYOTA;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE CHECKPOINTS; DNA; DNA DAMAGE; HUMANS; NUCLEOSIDES; PLASMA GASES; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

EID: 84922263587     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16022971     Document Type: Article

References (171)

1. Von Woedtke, T.; Reuter, S.; Masur, K.; Weltmann, K.D. Plasmas for medicine. Phys. Rep. 2013, 530, 291–320.
2. Xiong, Q.; Lu, X.; Jiang, Z.H.; Tang, Z.Y.; Hu, J.; Xiong, Z.L.; Pan, Y. An atmospheric pressure nonequilibrium plasma jet device. Plasma Sci. IEEE Trans. 2008, 36, 986–987.
3. Graves, D.B. The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J. Phys. D 2012, 45, doi:10.1088/0022-3727/45/26/263001.
4. Isbary, G.; Shimizu, T.; Li, Y.; Stolz, W.; Thomas, H.M.; Morfill, G.E.; Zimmermann, J.L. Cold atmospheric plasma devices for medical issues. Expert Rev. Med. Devices 2013, 10, 367–377.
5. Arjunan, K.P.; Friedman, G.; Fridman, A.; Clyne, A.M. Non-thermal dielectric barrier discharge plasma induces angiogenesis through reactive oxygen species. J. R. Soc. Inter. 2011, doi:10.1098/rsif.2011.0220.
6. Fridman, G.; Peddinghaus, M.; Balasubramanian, M.; Ayan, H.; Fridman, A.; Gutsol, A.; Brooks, A. Blood coagulation and living tissue sterilization by floating-electrode dielectric barrier discharge in air. Plasma Chem. Plasma Process. 2006, 26, 425–442.
7. Kalghatgi, S.; Kelly, C.M.; Cerchar, E.; Torabi, B.; Alekseev, O.; Fridman, A.; Friedman, G.; Azizkhan-Clifford, J. Effects of non-thermal plasma on mammalian cells. PLoS One 2011, 6, e16270.
8. Blackert, S.; Haertel, B.; Wende, K.; von Woedtke, T.; Lindequist, U. Influence of non-thermal atmospheric pressure plasma on cellular structures and processes in human keratinocytes (HaCaT). J. Dermatol. Sci. 2013, 70, 173–181.
9. Wu, A.S.; Kalghatgi, S.; Dobrynin, D.; Sensenig, R.; Cerchar, E.; Podolsky, E.; Dulaimi, E.; Paff, M.; Wasko, K.; Arjunan, K. et al. Porcine intact and wounded skin responses to atmospheric nonthermal plasma. J. Surg. Res. 2013, 179, e1–e12.
10. Kuchenbecker, M.; Bibinov, N.; Kaemlimg, A.; Wandke, D.; Awakowicz, P.; Viöl, W. Characterization of DBD plasma source for biomedical applications. J. Phys. D 2009, 42, doi:10.1088/0022-3727/42/4/045212.
11. Fridman, G.; Shereshevsky, A.; Jost, M.M.; Brooks, A.D.; Fridman, A.; Gutsol, A.; Vasilets, V.; Friedman, G. Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines. Plasma Chem. Plasma Process. 2007, 27, 163–176.
12. Han, X.; Cantrell, W.A.; Escobar, E.E.; Ptasinska, S. Plasmid DNA damage induced by helium atmospheric pressure plasma jet. Eur. Phys. J. D 2014, 68, 1–7.
13. Han, X.; Klas, M.; Liu, Y.; Sharon S.M.; Ptasinska, S. DNA damage in oral cancer cells induced by nitrogen atmospheric pressure plasma jets. Appl. Phys. Lett. 2013, 102, doi:10.1063/1.4809830.
14. Wende, K.; Straßenburg, S.; Haertel, B.; Harms, M.; Holtz, S.; Barton, A.; Masur, K.; von Woedtke, T.; Lindequist, U. Atmospheric pressure plasma jet treatment evokes transient oxidative stress in HaCaT keratinocytes and influences cell physiology. Cell Biol. Int. 2014, 38, 412–425.
15. Isbary, G.; Köritzer, J.; Mitra, A.; Li, Y.F.; Shimizu, T.; Schroeder, J.; Schlegel, J.; Morfill, G.E.; Stolz, W.; Zimmermann, J.L. Ex vivo human skin experiments for the evaluation of safety of new cold atmospheric plasma devices. Clin. Plasma Med. 2013, 1, 36–44.
16. Morfill, G.E.; Shimizu, T.; Steffes, B.; Schmidt, H.U. Nosocomial infections—A new approach towards preventive medicine using plasmas. New J. Phys. 2009, 11, doi:10.1088/1367-2630/11/11/115019.
17. Hoffmann, C.; Berganza, C.; Zhang, J. Cold atmospheric plasma: Methods of production and application in dentistry and oncology. Med. Gas Res. 2013, 3, doi:10.1186/2045-9912-3-21.
18. Maisch, T.; Shimizu, T.; Isbary, G.; Heinlin, J.; Karrer, S.; Klämpfl, T.G.; Li, Y.; Morfill, G.; Zimmermann, J.L. Contact-free inactivation of candida albicans biofilms by cold atmospheric air plasma. Appl. Environ. Microbiol. 2012, 78, 4242–4247.
19. Zimmermann, J.L.; Dumler, K.; Shimizu, T.; Morfill, G.E.; Wolf, A.; Boxhammer, V.; Schlegel, J.; Gansbacher, B.; Anton, M. Effects of cold atmospheric plasmas on adenoviruses in solution. J. Phys. D 2011, 44, doi:10.1088/0022-3727/44/50/505201.
20. Hähnel, M.; von Woedtke, T.; Weltmann, K.-D. Influence of the air humidity on the reduction of bacillus spores in a defined environment at atmospheric pressure using a dielectric barrier surface discharge. Plasma Process. Polym. 2010, 7, 244–249.
21. Klämpfl, T.G.; Isbary, G.; Shimizu, T.; Li, Y.; Zimmermann, J.L.; Stolz, W.; Schlegel, J.; Morfill, G.E.; Schmidt, H. Cold atmospheric air plasma sterilization against spores and other microorganisms of clinical interest. Appl. Environ. Microbiol. 2012, 78, 5077–5082.
22. Kuo, S.P.; Tarasenko, O.; Chang, J.; Popovic, S.; Chen, C.Y.; Fan, H.W.; Scott, A.; Lahiani, M.; Alusta, P.; Drake, J.D. et al. Contribution of a portable air plasma torch to rapid blood coagulation as a method of preventing bleeding. New J. Phys. 2009, 11, doi:10.1088/1367-2630/11/11/115016.
23. Isbary, G.; Morfill, G.; Schmidt, H.U.; Georgi, M.; Ramrath, K.; Heinlin, J.; Karrer, S.; Landthaler, M.; Shimizu, T.; Steffes, B. et al. A first prospective randomized controlled trial to decrease bacterial load using cold atmospheric argon plasma on chronic wounds in patients. Br. J. Dermatol. 2010, 163, 78–82.
24. Isbary, G.; Heinlin, J.; Shimizu, T.; Zimmermann, J.L.; Morfill, G.; Schmidt, H.U.; Monetti, R.; Steffes, B.; Bunk, W.; Li, Y. et al. Successful and safe use of 2 min cold atmospheric argon plasma in chronic wounds: Results of a randomized controlled trial. Br. J. Dermatol. 2012, 167, 404–410.
25. Baxter, H.C.; Campbell, G.A.; Richardson, P.R.; Jones, A.C.; Whittle, I.R.; Casey, M.; Whittaker, A.G.; Baxter, R.L. Surgical instrument decontamination: Efficacy of introducing an argon:oxygen RF gas-plasma cleaning step as part of the cleaning cycle for stainless steel instruments. Plasma Sci. IEEE Trans. 2006, 34, 1337–1344.
26. Whittaker, A.G.; Graham, E.M.; Baxter, R.L.; Jones, A.C.; Richardson, P.R.; Meek, G.; Campbell, G.A.; Aitken, A.; Baxter, H.C. Plasma cleaning of dental instruments. J. Hosp. Infect. 2004, 56, 37–41.
27. Baxter, H.C.; Campbell, G.A.; Whittaker, A.G.; Jones, A.C.; Aitken, A.; Simpson, A.H.; Casey, M.; Bountiff, L.; Gibbard, L.; Baxter, R.L. Elimination of transmissible spongiform encephalopathy infectivity and decontamination of surgical instruments by using radio-frequency gas-plasma treatment. J. Gen. Virol. 2005, 86, 2393–2399.
28. Yildirim, E.D.; Ayan, H.; Vasilets, V.N.; Fridman, A.; Guceri, S.; Sun, W. Effect of dielectric barrier discharge plasma on the attachment and proliferation of osteoblasts cultured over poly(ε-caprolactone) scaffolds. Plasma Process. Polym. 2008, 5, 58–66.
29. Leduc, M.; Guay, D.; Leask, R.L.; Coulombe, S. Cell permeabilization using a non-thermal plasma. New J. Phys. 2009, 11, doi:10.1088/1367-2630/11/11/115021.
30. Sakai, Y., Khajoee, V.; Ogawa, Y.; Kusuhara, K.; Katayama, Y.; Hara, T. A novel transfection method for mammalian cells using gas plasma. J. Biotechnol. 2006, 121, 299–308.
31. Chang, Y.-T.; Chen, G. Oral bacterial inactivation using a novel low-temperature atmospheric-pressure plasma device. J. Dent. Sci. 2014, doi:10.1016/j.jds.2014.03.007.
32. Sun, P.; Pan, J.; Tian, Y.; Bai, N.; Wu, H.; Wang, L.; Yu, C.; Zhang, J.; Zhu, W.; Becker, K.H. et al. Tooth whitening with hydrogen peroxide assisted by a direct-current cold atmospheric-pressure air plasma microjet. Plasma Sci. IEEE Trans. 2010, 38, 1892–1896.
33. Vandamme, M.; Robert, E.; Dozias, S.; Sobilo, J.; Lerondel, S.; Le Pape, A.; Pouvesle, J. Response of Human Glioma U87 Xenografted on Mice to Non Thermal Plasma Treatment. Plasma Med. 2011, 1, 27–43.
34. Kim, S.J.; Chung, T.H.; Bae, S.H.; Leem, S.H. Induction of apoptosis in human breast cancer cells by a pulsed atmospheric pressure plasma jet. Appl. Phys. Lett. 2010, 97, doi:10.1063/1.3462293.
35. Partecke, L.I.; Evert, K.; Haugk, J.; Doering, F.; Normann, L.; Diedrich, S.; Weiss, F.; Evert, M.; Huebner, N.; Guenther, C. et al. Tissue tolerable plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo. BMC Cancer 2012, 12, doi:10.1186/1471-2407-12-473.
36. Kaushik, N.K.; Kim, Y.H.; Han, Y.G.; Choi, E.H. Effect of jet plasma on T98G human brain cancer cells. Curr. Appl. Phys. 2013, 13, 176–180.
37. Barekzi, N.; Laroussi, M. Dose-dependent killing of leukemia cells by low-temperature plasma. J. Phys. D 2012, 45, doi:10.1088/0022-3727/45/42/422002.
38. Kim, C.-H.; Kwon, S.; Bahn, J.H.; Lee, K.; Jun, S.I.; Rack, P.D.; Baek, S.J. Effects of atmospheric nonthermal plasma on invasion of colorectal cancer cells. Appl. Phys. Lett. 2010, 96, doi:10.1063/1.3449575.
39. Dröge, W. Free radicals in the physiological control of cell. Function 2002, 82, 47–95.
40. Smith, J.; Ladi, E.; Mayer-Pröschel, M.; Noble, M. Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc. Natl. Acad. Sci. USA 2000, 97, 10032–10037.
41. Circu, M.L.; Aw, T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48, 749–762.
42. Simon, H.U.; Haj-Yehia, A.; Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5, 415–418.
43. Barzilai, A.; Yamamoto, K.-I. DNA damage responses to oxidative stress. DNA Repair 2004, 3, 1109–1115.
44. Shackelford, R.E.; Kaufmann, W.K.; Paules, R.S. Oxidative stress and cell cycle checkpoint function. Free Radic. Biol. Med. 2000, 28, 1387–1404.
45. Alkawareek, M.Y.; Gorman, S.P.; Graham, W.G.; Gilmore, B.F. Potential cellular targets and antibacterial efficacy of atmospheric pressure non-thermal plasma. Int. J. Antimicrob. Agents 2014, 43, 154–160.
46. Leduc, M.; Guay, D.; Coulombe, S.; Leask, R.L. Effects of non-thermal plasmas on DNA and mammalian cells. Plasma Process. Polym. 2010, 7, 899–909.
47. Bahnev, B.; Bowden, M.D.; Stypczyńska, A.; Ptasińska, S.; Mason, N.J.; Braithwaite, N.J. A novel method for the detection of plasma jet boundaries by exploring DNA damage. Eur. Phys. J. D 2014, 68, 1–5.
48. Hosseinzadeh Colagar, A.; Memariani, H.; Sohbatzadeh, F.; Valinataj Omran, A. Nonthermal atmospheric argon plasma jet effects on Escherichia coli biomacromolecules. Appl. Biochem. Biotechnol. 2013, 171, 1617–1629.
49. Kim, S.-M.; Kim, J.-I. Decomposition of biological macromolecules by plasma generated with helium and oxygen. J. Microbiol. 2006, 44, 466–471.
50. Li, G.; Li, H.; Wang, L.; Wang, S.; Zhao, H.; Sun, W.; Xing, X.; Bao, C. Genetic effects of radio-frequency, atmospheric-pressure glow discharges with helium. Appl. Phys. Lett. 2008, 92, doi:10.1063/1.2938692.
51. Niemi, K.; O’Neill, C.; Cox, L.J.; Waskoenig, J.; Hyland, W.B.; McMahon, S.J.; Reuter, S.; Currell, F.J.; Graham, W.G.; O’Connell, D. et al. Cold atmospheric pressure plasma jets: Interaction with plasmid DNA and tailored electron heating using dual-frequency excitation. AIP Confer. Pro. 2012, 1438, 23–28.
52. O’Connell, D.; Cox, L.J.; Hyland, W.B.; McMahon, S.J.; Reuter, S.; Graham, W.G.; Gans, T.; Currell, F.J. Cold atmospheric pressure plasma jet interactions with plasmid DNA. Appl. Phys. Lett. 2011, 98, doi:10.1063/1.3521502.
53. Ptasinska, S.; Bahnev, B.; Stypczynska, A.; Bowden, M.; Mason, N.J.; Braithwaite, N.J. DNA strand scission induced by a non-thermal atmospheric pressure plasma jet. Phys. Chem. Chem. Phys. 2010, 12, 7779–7781.
54. Stypczyńska, A.; Ptasińska, S.; Bahnev, B.; Bowden, M.; Braithwaite, N.J.; Mason, N.J. The influence of amino acids on DNA damage induced by cold plasma radiation. Chem. Phys. Lett. 2010, 500, 313–317.
55. Yan, X.; Zou, F.; Lu, X.P.; He, G.; Shi, M.J.; Xiong, Q.; Gao, X.; Xiong, Z.; Li, Y.; Ma, F.Y. et al. Effect of the atmospheric pressure nonequilibrium plasmas on the conformational changes of plasmid DNA. Appl. Phys. Lett. 2009, 95, doi:10.1063/1.3212739.
56. Kim, J.Y.; Lee, D.; Ballato, J.; Cao, W.; Kim, S. Reactive oxygen species controllable non-thermal helium plasmas for evaluation of plasmid DNA strand breaks. Appl. Phys. Lett. 2012, 101, doi:10.1063/1.4768922.
57. Lackmann, J.-W.; Schneider, S.; Edengeiser, E.; Jarzina, F.; Brinckmann, S.; Steinborn, E.; Havenith, M.; Benedikt, J.; Bandow, J.E. Photons and particles emitted from cold atmospheric-pressure plasma inactivate bacteria and biomolecules independently and synergistically. J. R. Soc. Interface 2013, 10, doi:10.1098/rsif.2013.0591.
58. Lackmann, J.-W.; Schneider, S.; Narberhaus, F.; Benedikt, J.; Bandow, J.E. Characterization of Damage to Bacteria and Bio-macromolecules Caused by (V)UV Radiation and Particles Generated by a Microscale Atmospheric Pressure Plasma Jet. In Plasma for Bio-Decontamination, Medicine and Food Security; Machala, Z., Hensel, K.Y., Eds.; Springer Netherlands: Amsterdam, The Netherlands, 2012; pp. 17–29.
59. Antoniu, A.; Nakajima, T.; Kurita, H.; Mizuno, A. Safety evaluation of nonthermal atmospheric pressure plasma liquid treatment: Single DNA molecule-based method. J. Electrost. 2014, 72, 210–217.
60. Kurita, H.; Nakajima, T.; Yasuda, H.; Takashima, K.; Mizuno, A.; Wilson, J.I.B.; Cunningham, S. Single-molecule measurement of strand breaks on large DNA induced by atmospheric pressure plasma jet. Appl. Phys. Lett. 2011, 99, doi:10.1063/1.3660581.
61. Kurita, H.; Shimizu, M.; Sano, K.; Nakajima, T.; Yasuda, H.; Takashima, K.; Mizuno, A. Radical reaction in aqueous media injected by atmospheric pressure plasma jet and protective effect of antioxidant reagents evaluated by single-molecule DNA measurement. Jpn. J. Appl. Phys. 2014, 53, doi:10.7567/JJAP.53.05FR01.
62. Sousa, J.S.; Bauville, G.; Lacour, B.; Puech, V.; Touzeau, M.; Ravanat, J. DNA oxidation by singlet delta oxygen produced by atmospheric pressure microdischarges. Appl. Phys. Lett. 2010, 97, doi:10.1063/1.3499362.
63. Sousa, J.; Girard, P.; Sage, E.; Ravanat, J.; Puech, V. DNA Oxidation by Reactive Oxygen Species Produced by Atmospheric Pressure Microplasmas. In Plasma for Bio-Decontamination, Medicine and Food Security; Machala, Z., Hensel, K.Y., Eds.; Springer Netherlands: Amsterdam, The Netherlands, 2012; pp. 107–119.
64. Brun, P.; Vono, M.; Venier, P.; Tarricone, E.; Deligianni, V.; Martines, E.; Zuin, M.; Spagnolo, S.; Cavazzana, R.; Cardin, R. et al. Disinfection of ocular cells and tissues by atmospheric-pressure cold plasma. PLoS One 2012, 7, e33245.
65. Chang, J.W.; Kang, S.U.; Shin, Y.S.; Kim, K.I.; Seo, S.J.; Yang, S.S.; Lee, J.; Moon, E.; Baek, S.J.; Lee, K. et al. Non-thermal atmospheric pressure plasma induces apoptosis in oral cavity squamous cell carcinoma: Involvement of DNA-damage-triggering sub-G1 arrest via the ATM/p53 pathway. Arch. Biochem. Biophys. 2014, 545, 133–140.
66. Han, X.; Liu, Y.; Stack, M.S.; Ptasinska, S. 3D Mapping of plasma effective areas via detection of cancer cell damage induced by atmospheric pressure plasma jets. J. Phys. Conf. Ser. 2014, 565, 12011–12016.
67. Kalghatgi, S.; Azizkhan-Clifford, J. DNA damage in mammalian cells by atmospheric pressure microsecond-pulsed dielectric barrier discharge plasma is not. Mediated via lipid peroxidation. Plasma Med. J. 2011, 1, 167–177.
68. Kalghatgi, S.; Fridman, A.; Azizkhan-Clifford, J.; Friedman, G. DNA damage in mammalian cells by non-thermal atmospheric pressure microsecond pulsed dielectric barrier discharge plasma is not mediated by ozone. Plasma Process. Polym. 2012, 9, 726–732.
69. Kim, G.J.; Kim, W.; Kim, K.T.; Lee, J.K. DNA damage and mitochondria dysfunction in cell apoptosis induced by nonthermal air plasma. Appl. Phys. Lett. 2010, 96, doi:10.1063/1.3292206.
70. Kim, K.; Choi, J.D.; Hong, Y.C.; Kim, G.; Noh, E.J.; Lee, J.; Yang, S.S. Atmospheric-pressure plasma-jet from micronozzle array and its biological effects on living cells for cancer therapy. Appl. Phys. Lett. 2011, 98, doi:10.1063/1.3555434.
71. Ma, Y.; Ha, C.S.; Hwang, S.W.; Lee, H.J.; Kim, G.C.; Lee, K.; 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, e91947.
72. Morales-Ramírez, P.; Cruz-Vallejo, V.; Peña-Eguiluz, R.; López-Callejas, R.; Rodríguez-Méndez, B.G.; Valencia-Alvarado, R.; Mercado-Cabrera, A.; Muñoz-Castro, A.E. Assessing cellular DNA damage from a helium plasma needle. Radiat. Res. 2013, 179, 669–673.
73. Plewa, J.-M.; Yousfi, M.; Frongia, C.; Eichwald, O.; Ducommun, B.; Merbahi, N.; Lobjois, V. Low-temperature plasma-induced antiproliferative effects on multi-cellular tumor spheroids. New J. Phys. 2014, 16, doi:10.1088/1367-2630/16/4/043027.
74. Volotskova, O.; Hawley, T.S.; Stepp, M.A.; Keidar, M. Targeting the cancer cell cycle by cold atmospheric plasma. Sci. Rep. 2012, 2, doi:10.1038/srep00636.
75. Xu, Y.; Zou, F.; Zhao, S.; Lu, X.; He, G.; Xiong, Z.; Xiong, Q.; Zhao, Q.; Deng, P.; Huang, J. et al. On the mechanism of plasma inducing cell apoptosis. Plasma Sci. IEEE Trans. 2010, 38, 2451–2457.
76. Choi, J.-H.; Lee, H.; Lee, J.; Hong, J.; Kim, G. Low-temperature atmospheric plasma increases the expression of anti-aging genes of skin cells without causing cellular damages. Arch. Dermatol. Res. 2013, 305, 133–140.
77. Lazović, S.; Maletić, D.; Leskovac, A.; Filipović, J.; Puač, N.; Malović, G.; Joksić, G.; Petrović, Z.L. Plasma induced DNA damage: Comparison with the effects of ionizing radiation. Appl. Phys. Lett. 2014, 105, doi:10.1063/1.4896626.
78. Lee, Y.; Kim, K.; Kang, K.; Lee, J.; Yang, S.; Chung, W. Atmospheric-pressure plasma jet induces DNA double-strand breaks that require a Rad51-mediated homologous recombination for repair in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 2014, 560, 1–9.
79. Ryu, Y.-H.; Kim, Y.; Lee, J.; Shim, G.; Uhm, H.; Park, G.; Choi, E.H. Effects of background fluid on the efficiency of inactivating yeast with non-thermal atmospheric pressure plasma. PLoS One 2013, 8, e66231.
80. Joshi, S.G.; Cooper, M.; Yost, A.; Paff, M.; Ercan, U.K.; Fridman, G.; Friedman, G.; Fridman, A.; Brooks, A.D. Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob. Agents Chemother. 2011, 55, 1053–1062.
81. Kvam, E.; Davis, B.; Mondello, F.; Garner, A.L. Nonthermal atmospheric plasma rapidly disinfects multidrug-resistant microbes by inducing cell surface damage. Antimicrob. Agents Chemother. 2012, 56, 2028–2036.
82. Tseng, S.; Abramzon, N.; Jackson, J.O.; Lin, W. Gas. discharge plasmas are effective in inactivating Bacillus and Clostridium spores. Appl. Microbiol. Biotechnol. 2012, 93, 2563–2570.
83. Mols, M.; Mastwijk, H.; Nierop Groot, M.; Abee, T. Physiological and transcriptional response of Bacillus cereus treated with low-temperature nitrogen gas plasma. J. Appl. Microbiol. 2013, 115, 689–702.
84. Sharma, A.; Collins, G.; Pruden, A. Differential gene expression in Escherichia coli following exposure to nonthermal atmospheric pressure plasma. J. Appl. Microbiol. 2009, 107, 1440–1449.
85. Winter, T.; Winter, J.; Polak, M.; Kusch, K.; Mäder, U.; Sietmann, R.; Ehlbeck, J.; van Hijum, S.; Weltmann, K.; Hecker, M.; Kusch, H. Characterization of the global impact of low temperature gas plasma on vegetative microorganisms. Proteomics 2011, 11, 3518–3530.
86. Lu, H.; Patil, S.; Keener, K.M.; Cullen, P.J.; Bourke, P. Bacterial inactivation by high-voltage atmospheric cold plasma: Influence of process parameters and effects on cell leakage and DNA. J. Appl. Microbiol. 2014, 116, 784–794.
87. Venezia, R.; Orrico, M.; Houston, E.; Yin, S.; Naumova, Y.Y. Lethal activity of nonthermal plasma sterilization against microorganisms. Infect. Control Hosp. Epidemiol. 2008, 29, 430–436.
88. Yasuda, H.; Miura, T.; Kurita, H.; Takashima, K.; Mizuno, A. Biological evaluation of DNA damage in bacteriophages inactivated by atmospheric pressure cold plasma. Plasma Process. Polym. 2010, 7, 301–308.
89. Wang, L.Y.; Huang, Z.L.; Li, G.; Zhao, H.X.; Xing, X.H.; Sun, W.T.; Li, H.P.; Gou, Z.X.; Bao, C.Y. Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma. J. Appl. Microbiol. 2010, 108, 851–858.
90. Fang, M.; Jin, L.; Zhang, C.; Tan, Y.; Jiang, P.; Ge, N.; Li, H.; Xing, X. Rapid mutation of spirulina platensis by a new mutagenesis system of atmospheric and room temperature plasmas (ARTP) and generation of a mutant library with diverse phenotypes. PLoS One 2013, 8, e77046.
91. Halliwell, B. Oxidative stress and neurodegeneration: Where are we now? J. Neurochem. 2006, 97, 634–1658.
92. Kuznetsova, A.A.; Dmitrii, G.K.; Olga, S.F. Oxidation of DNA and its components with reactive oxygen species. Russ. Chem. Rev. 2009, 78, doi:10.1070/RC2009v078n07ABEH004038.
93. Shafirovich, V.; Crean, C.; Geacintov, N.E. Reactions of reactive nitrogen species and carbonate radical anions with DNA. In Radical and Radical Ion Reactivity in Nucleic Acid Chemistry; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2009; pp. 325–355.
94. Dedon, P.C.; Tannenbaum, S.R. Reactive nitrogen species in the chemical biology of inflammation. Arch. Biochem. Biophys. 2004, 423, 12–22.
95. Pacher, P.; Beckman, J.S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87, 315–424.
96. Buxton, G.V.; Greenstock, C.L.; Helman, W.P.; Ross, A.B. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (•OH/•O- in aqueous solution. J. Phys. Chem. Ref. Data 1988, 17, 513–886.
97. Neta, P.; Huie, R.E.; Ross, A.B. Rate constants for reactions of inorganic radicals in aqueous solution. J. Phys. Chem. Ref. Data 1988, 17, 1027-1284.
98. Lewis, R.S.; Deen, W.M. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem. Res. Toxicol. 1994, 7, 568-574.
99. Manoj, P.; Mohan, H.; Mittal, J.P.; Manoj, V.M.; Aravindakumar, C.T. Charge transfer from 2-aminopurine radical cation and radical anion to nucleobases: A pulse radiolysis study. Chem. Phys. 2007, 331, 351-358.
100. Von Sonntag, C. Free-Radical-Induced DNA Damage and Its Repair: A Chemical Perspective 2010; Springer: New York, NY, USA, 2010.
101. Sharma, V.K. Oxidation of Amino Acids, Peptides, and Proteins; Wiley: New Jersey, NJ, USA, 2013.
102. Dizdaroglu, M. Chemical determination of free radical-induced damage to DNA. Free Radic. Biol. Med. 1991, 10, 225-242.
103. Halliwell, B.; Aruoma, O.I. DNA damage by oxygen-derived species Its mechanism and measurement in mammalian systems. FEBS Lett. 1991, 281, 9-19.
104. Rai, P.; Wemmer, D.E.; Linn, S. Preferential binding and structural distortion by Fe2+ at RGGG-containing DNA sequences correlates with enhanced oxidative cleavage at such sequences. Nucleic Acids Res. 2005, 33, 497-510.
105. Flint, D.H.; Tuminello, J.F.; Emptage, M.H. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem. 1993, 268, 22369-22376.
106. Kuo, C.F.; Mashino, T.; Fridovich, I. a,P-Dihydroxyisovalerate dehydratase: A superoxide-sensitive enzyme. J. Biol. Chem. 1987, 262, 4724-4727.
107. Keyer, K.; Gort, A.S.; Imlay, J.A. Superoxide and the production of oxidative DNA damage. J. Bacteriol 1995, 177, 6782-6790.
108. Sies, H.; Menck, C.F.M. Singlet oxygen induced DNA damage. Mutat. Res. DNAging 1992, 275, 367-375.
109. Devasagayam, T.P.A.; di Mascio, P.; Kaiser, S.; Sies, H. Singlet oxygen induced single-strand breaks in plasmid pBR322 DNA: The enhancing effect of thiols. Biochim. Biophys. Acta Gene Struct. Expr. 1991, 1088, 409–412.
110. Ravanat, J.-L.; Cadet, J. Reaction of singlet oxygen with 2'-deoxyguanosine and DNA. Isolation and characterization of the main oxidation products. Chem. Res. Toxicol. 1995, 8, 379-388.
111. Schneider, J.E.; Price, S.; Maidt, L.; Gutteridge, J.M.; Floyd, R.A. Methylene blue plus light mediates 8-hydroxy 2'-deoxyguanosine formation in DNA preferentially over strand breakage. Nucleic Acids Res. 1990, 18, 631-635.
112. Cheng, T.-J.; Kao, H.; Chan, C.; Chang, W.P. Effects of ozone on DNA single-strand breaks and 8-oxoguanine formation in A549 cells. Environ. Res. 2003, 93, 279-284.
113. Ito, K.; Inoue, S.; Hiraku, Y.; Kawanishi, S. Mechanism of site-specific DNA damage induced by ozone. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2005, 585, 60-70.
114. Kuipers, GK.; Lafleur, M.V.M. Characterization of DNA damage induced by y-radiation-derived water radicals, using DNA repair enzymes. Int. J. Radiat. Biol. 1998, 74, 511-519.
115. Kumar, A.; Sevilla, M.D. Role of excited states in low-energy electron. (LEE) Induced strand breaks in DNA model systems: Influence of aqueous environment. ChemPhysChem 2009, 10, 1426-1430.
116. Kennedy, L.J.; Moore, K.; Caulfield, J.L.; Tannenbaum, S.R.; Dedon, P.C. Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem. Res. Toxicol. 1997, 10, 386–392.
117. Cadet, J.; Wagner, J.R. Oxidatively generated base damage to cellular DNA by hydroxyl radical and one-electron oxidants: Similarities and differences. Arch. Biochem. Biophys. 2014, 557, 47–54.
118. Steenken, S. Purine bases, nucleosides, and nucleotides: Aqueous solution redox chemistry and transformation reactions of their radical cations and e- and OH adducts. Chem. Rev. 1989, 89, 503–520.
119. Steenken, S.; Jovanovic, S.V. How easily oxidizable Is DNA? One-electron. Reduction potentials of adenosine and guanosine radicals in aqueous solution. J. Am. Chem. Soc. 1997, 119, 617–618.
120. Steenken, S.; Jovanovic, S.V.; Bietti, M.; Bernhard, K. The trap depth (in DNA) of 8-oxo-7,8-dihydro-2′deoxyguanosine as derived from electron-transfer equilibria in aqueous solution. J. Am. Chem. Soc. 2000, 122, 2373–2374.
121. Yuan, B.-F.; Feng, Y.-Q. Recent advances in the analysis of 5-methylcytosine and its oxidation products. TrAC Trends Anal. Chem. 2014, 54, 24–35.
122. Cadet, J.; Teoule, R. Comparative study of oxidation of nucleic acid components by hydroxyl radicals, singlet oxygen and superoxide anion radicals. Photochem. Photobiol. 1978, 28, 661–665.
123. Misiaszek, R.; Crean, C.; Joffe, A.; Geacintov, N.E.; Shafirovich, V. Oxidative DNA damage associated with combination of guanine and superoxide radicals and repair mechanisms via radical trapping. J. Biol. Chem. 2004, 279, 32106–32115.
124. Lafleur, M.V.M.; Nieuwint, A.W.M.; Aubry, J.M.; Kortbeek, H.; Arwert, F.; Joenje, H. DNA damage by chemically generated singlet oxygen. Free Radic. Res. 1987, 2, 343–350.
125. Luo, W.; Muller, J.G.; Rachlin, E.M.; Burrows, C.J. Characterization of hydantoin products from one-electron oxidation of 8-oxo-7,8-dihydroguanosine in a nucleoside model. Chem. Res. Toxicol. 2001, 14, 927–938.
126. Hayon, E.; Simic, M. Addition of hydroxyl radicals to pyrimidine bases and electron transfer reactions of intermediates to quinones. J. Am. Chem. Soc. 1973, 95, 1029–1035.
127. Yun, B.H.; Geacintov, N.E.; Shafirovich, V. Generation of guanine–thymidine cross-links in DNA by peroxynitrite/carbon dioxide. Chem. Res. Toxicol. 2011, 24, 1144–1152.
128. Lim, K.S.; Cui, L.; Taghizadeh, K.; Wishnok, J.S.; Chan, W.; DeMott, M.S.; Babu, I. R.; Tannenbaum, S.R.; Dedon, P.C. In Situ Analysis of 8-oxo-7,8-dihydro-2′-deoxyguanosine oxidation reveals sequence- and agent-specific damage spectra. J. Am. Chem. Soc. 2012, 134, 18053–18064.
129. Crean, C.; Uvaydov, Y.; Geacintov, N.E.; Shafirovich, V. Oxidation of single-stranded oligonucleotides by carbonate radical anions: Generating intrastrand cross-links between guanine and thymine bases separated by cytosines. Nucleic Acids Res. 2008, 36, 742–755.
130. Madugundu, G.S.; Wagner, J.R.; Cadet, J.; Kropachev, K.; Yun, B.H.; Geacintov, N.E.; Shafirovich, V. Generation of guanine-thymine cross-links in human cells by one-electron. Oxidation mechanisms. Chem. Res. Toxicol. 2013, 26, 1031–1033.
131. Mitra, J.; Guerrero, E.; Hegde, P.; Wang, H.; Boldogh, I.; Rao, K.; Mitra, S.; Hegde, M. New perspectives on oxidized genome damage and repair inhibition by pro-oxidant metals in neurological diseases. Biomolecules 2014, 4, 678–703.
132. McKinnon, P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 2009, 10, 100–112.
133. Mitra, S.; Boldogh, I.; Izumi, T.; Hazra, T.K. Complexities of the DNA base excision repair pathway for repair of oxidative DNA damage. Environ. Mol. Mutagen. 2001, 38, 180–190.
134. Mao, Z.; Bozzella, M.; Seluanov, A.; Gorbunova, V. DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells. Cell Cycle 2008, 7, 2902–2906.
135. Shrivastav, M.; de Haro, L.P.; Nickoloff, J.A. Regulation of DNA double-strand break repair pathway choice. Cell Res. 2008, 18, 134–147.
136. Takata, M.; Sasaki, M.S.; Sonoda, E.; Morrison, C.; Hashimoto, M.; Utsumi, H.; Yamaguchi-Iwai, Y.; Shinohara, A.; Takeda, S. Homologous recombination and non-homologous end-joining pathways of DNA double‐strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 1998, 17, 5497–5508.
137. Halliwell, B. Free radicals. Reactive oxygen species and human disease: A critical evaluation with special reference to atherosclerosis. Br. J. Exp. Pathol. 1989, 70, 737–757.
138. Burtscher, H.; Berner, S.; Seibl, R.; Muhlegger, K. Nucleic acids. In Ullmann’s Biotechnology and Biochemical Engineering; Wiley-VCH: Weinheim, Germany, 2007; pp. 157–194.
139. Deweese, J.E.; Osheroff, M.A.; Osheroff, N. DNA topology and topoisomerases: Teaching a “knotty” subject. Biochem. Mol. Biol. Educ. 2008, 37, 2–10.
140. Gaens, W.V.; Bogaerts, A. Kinetic modelling for an atmospheric pressure argon plasma jet in humid air. J. Phys. D 2013, 46, 275201.
141. Krisch, R.E.; Flick, M.B.; Trumbore, C.N. Radiation chemical mechanisms of single- and double-strand break formation in irradiated SV40 DNA. Radiat. Res. 1991, 126, 251–259.
142. Fridman, G.; Brooks, A.D.; Balasubramanian, M.; Fridman, A.; Gutsol, A.; Vasilets, V.N.; Ayan, H.; Friedman, G. Comparison of direct and indirect effects of non-thermal atmospheric-pressure plasma on bacteria. Plasma Process. Polym. 2007, 4, 370–375.
143. Neyts, E.C.; Yusupov, M.; Verlackt, C.C.; Bogaerts, A. Computer simulations of plasma-biomolecule and plasma-tissue interactions for a better insight in plasma medicine. J. Phys. D 2014, 47, 293001.
144. Vilenchik, M.M.; Knudson, A.G. Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. USA 2003, 100, 12871–12876.
145. Murray, A.W.; Hunt, T. The Cell Cycle: An Introduction; Oxford University Press: New York, NY, USA, 1993.
146. Ward, I.M.; Chen, J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 2001, 276, 47759–47762.
147. Bohgaki, T.; Bohgaki, M.; Hakem, R. DNA double-strand break signaling and human disorders. Genome Integr. 2010, 1, doi:10.1186/2041-9414-1-15.
148. Jazayeri, A.; Falck, J.; Lukas, C.; Bartek, J.; Smith, G.C.M.; Lukas, J.; Jackson, S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 2006, 8, 37–45.
149. Adams, K.E.; Medhurst, A.L.; Dart, D.A.; Lakin, N.D. Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components of the MRN protein complex. Oncogene 2006, 25, 3894–3904.
150. Cuadrado, M.; Martinez-Pastor, B.; Murga, M.; Toledo, L.I.; Gutierrez-Martinez, P.; Lopez, E.; Fernandez-Capetillo, O. ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J. Exp. Med. 2006, 203, 297–303.
151. Myers, J.S.; Cortez, D. Rapid Activation of ATR by Ionizing Radiation Requires ATM and Mre11. J. Biol. Chem. 2006, 281, 9346–9350.
152. Stiff, T.; Walker, S.A.; Cerosaletti, K.; Goodarzi, A.A.; Petermann, E.; Concannon, P.; O’Driscoll, M.; Jeggo, P.A. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J. 2006, 25, 5775–5782.
153. Helton, E.S.; Chen, X. p53 modulation of the DNA damage response. J. Cell. Biochem. 2007, 100, 883–896.
154. Jung, Y.-S.; Qian, Y.; Chen, X. Examination of the expanding pathways for the regulation of p21 expression and activity. Cell Signal. 2010, 22, 1003–1012.
155. Huang, X.; Okafuji, M.; Traganos, F.; Luther, E.; Holden, E.; Darzynkiewicz, Z. Assessment of histone H2AX phosphorylation induced by DNA topoisomerase I and II inhibitors topotecan and mitoxantrone and by the DNA cross-linking agent cisplatin. Cytom. Part A 2004, 58, 99–110.
156. Slupphaug, G.; Kavli, B.; Krokan, H.E. The interacting pathways for prevention and repair of oxidative DNA damage. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2003, 531, 231–251.
157. Breen, A.P.; Murphy, J.A. Reactions of oxyl radicals with DNA. Free Radic. Biol. Med. 1995, 18, 1033–1077.
158. Wang, Y. Bulky DNA lesions induced by reactive oxygen species. Chem. Res. Toxicol. 2008, 21, 276–281.
159. Wilson, D.M., III; McNeill, D.R. Base excision repair and the central nervous system. Neuroscience 2007, 145, 1187–1200.
160. Le May, N.; Egly, J.; Coin, F. True lies: The double life of the nucleotide excision repair factors in transcription and DNA repair. J. Nucleic Acids 2010, 2010, doi:10.4061/2010/616342.
161. Sinha, R.P.; Hader, D.-P. UV-induced DNA damage and repair: A review. Photochem. Photobiol. Sci. 2002, 1, 225–236.
162. Graham, W.G.; Schaper, L.; Muir, M.; Currell, F.J. The effect of electrical discharges in the cell media on their viability and DNA damage and comparison with the effect of X-rays. Plasma Med. J. 2012, 2, 169–178.
163. Vandamme, M.; Robert, E.; Lerondel, S.; Sarron, V.; Ries, D.; Dozias, S.; Sobilo, J.; Gosset, D.; Kieda, C.; Legrain, B. et al. ROS implication in a new antitumor strategy based on non-thermal plasma. Int. J. Cancer 2012, 130, 2185–2194.
164. Rogakou, E.P.; Pilch, D.R.; Orr, A.H.; Ivanova, V.S.; Bonner, W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273, 5858–5868.
165. Arends, M.J.; Morris, R.G.; Wyllie, A.H. Apoptosis the role of the endonuclease. Am. J. Pathol. 1990, 136, 593–608.
166. Oberhammer, F.; Wilson, J.W.; Dive, C.; Morris, I.D.; Hickman, J.A.; Wakeling, A.E.; Walker, P.R.; Sikorska, M. Apoptotic death in epithelial cells: Cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J. 1993, 12, 3679–3684.
167. MacPhail, S.H.; Banáth, J.P.; Yu, Y.; Chu, E.; Olive, P.L. Cell cycle-dependent expression of phosphorylated histone H2AX: Reduced expression in unirradiated but not X-irradiated G1-phase cells. Radiat. Res. 2003, 159, 759–767.
168. Sharma, A.; Singh, K.; Almasan, A. Histone H2AX phosphorylation: A marker for DNA damage. In DNA Repair Protocols; Humana Press-Springer: New York, NY, USA, 2012.
169. Dantzer, F.; de la Rubia, G.; Ménissier-de Murcia, J.; Hostomsky, Z.; de Murcia, G.; Schreiber, V. Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry 2000, 39,7559–7569.
170. Kaufmann, S.H.; Desnoyers, S.; Ottaviano, Y.; Davidson, N.E.; Poirier, G.G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res. 1993, 53, 3976–3985.
171. Los, M.; Mozoluk, M.; Ferrari, D.; Stepczynska, A.; Stroh, C.; Renz, A.; Herceg, Z.; Wang, Z.; Schulze-Osthoff, K. Activation and caspase-mediated inhibition of PARP: A molecular switch between fibroblast necrosis and apoptosis in death receptor signaling. Mol. Biol. Cell 2002, 13.