Combined effect of protein and oxygen on reactive oxygen and nitrogen species in the plasma treatment of tissue

Applied Physics Letters

Volumn 107, Issue 10, 2015, Pages

  Gaur, Nishtha ^a,b   Szili, Endre J ^a,b   Oh, Jun Seok ^c   Hong, Sung Ha ^a,b   Michelmore, Andrew ^a   Graves, David B ^d   Hatta, Akimitsu ^c   Short, Robert D ^a,b  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b Wound Management Innovation Cooperation Research Centre   (Australia)

^c KOCHI UNIVERSITY OF TECHNOLOGY   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; FIGHTER AIRCRAFT; GROUND STATE; MOLECULAR OXYGEN; NITROGEN; NITROGEN OXIDES; NITROGEN PLASMA; OXYGEN; PLASMA APPLICATIONS; PLASMA DIAGNOSTICS; PROTEINS;

BOVINE SERUM ALBUMINS; COLD ATMOSPHERIC PLASMAS; FOOD MANUFACTURING; GROUND STATE OXYGEN; MICROPLATE READERS; PHOSPHATE-BUFFERED SALINES; REACTIVE OXYGEN AND NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

TISSUE;

EID: 84941343805     PISSN: 00036951     EISSN: None     Source Type: Journal    
DOI: 10.1063/1.4930874     Document Type: Article

References (75)

1. G. Isbary, J. Heinlin, T. Shimizu, J. L. Zimmermann, G. Morfill, H. U. Schmidt, R. Monetti, B. Steffes, W. Bunk, Y. Li, T. Klaempfl, S. Karrer, M. Landthaler, and W. Stolz, Br. J. Dermatol. 167, 404 (2012). 10.1111/j.1365-2133.2012.10923.x
2. G. Isbary, G. Morfill, H. U. Schmidt, M. Georgi, K. Ramrath, J. Heinlin, S. Karrer, M. Landthaler, T. Shimizu, B. Steffes, W. Bunk, R. Monetti, J. L. Zimmermann, R. Pompl, and W. Stolz, Br. J. Dermatol. 163, 78 (2010). 10.1111/j.1365-2133.2010.09744.x
3. G. Isbary, W. Stolz, T. Shimizu, R. Monetti, W. Bunk, H. U. Schmidt, G. E. Morfill, T. G. Klämpfl, B. Steffes, H. M. Thomas, J. Heinlin, S. Karrer, M. Landthaler, and J. L. Zimmermann, Clin. Plasma Med. 1, 25 (2013). 10.1016/j.cpme.2013.06.001
4. S. Emmert, F. Brehmer, H. Hänßle, A. Helmke, N. Mertens, R. Ahmed, D. Simon, D. Wandke, W. Maus-Friedrichs, G. Däschlein, M. P. Schön, and W. Viöl, Clin. Plasma Med. 1, 24 (2013). 10.1016/j.cpme.2012.11.002
5. J. Heinlin, G. Isbary, W. Stolz, G. Morfill, M. Landthaler, T. Shimizu, B. Steffes, T. Nosenko, J. L. Zimmermann, and S. Karrer, J. Eur. Acad. Dermatol. Venereol. 25, 1 (2011). 10.1111/j.1468-3083.2010.03702.x
6. S. A. Norberg, W. Tian, A. M. Lietz, and M. J. Kushner, " Strategies for customizing reactive fluxes in plasma treatment of liquid covered tissue," in Proceedings of the Second International Workshop on Plasma for Cancer Treatment, Nagoya, Japan (2015).
7. J. M. Pouvesle, G. Collet, E. Robert, L. Ridou, and S. Dozias, " Potential of plasma based soft and/or combined cancer treatments," in Proceedings of the Second International Workshop on Plasma for Cancer Treatment, Nagoya, Japan (2015).
8. Y. Sakai, V. Khajoee, Y. Ogawa, K. Kusuhara, Y. Katayama, and T. Hara, J. Biotechnol. 121, 299 (2006). 10.1016/j.jbiotec.2005.08.020
9. Y. Ogawa, N. Morikawa, A. Ohkubo-Suzuki, S. Miyoshi, H. Arakawa, Y. Kita, and S. Nishimura, Biotechnol. Bioeng. 92, 865 (2005). 10.1002/bit.20659
10. M. Leduc, D. Guay, R. L. Leask, and S. Coulombe, New J. Phys. 11, 115021 (2009). 10.1088/1367-2630/11/11/115021
11. Z. Xiong, S. Zhao, X. Mao, X. Lu, G. He, G. Yang, M. Chen, M. Ishaq, and K. Ostrikov, Stem Cell Res. 12, 387 (2014). 10.1016/j.scr.2013.11.003
12. J. E. Kim, D.-U. Lee, and S. C. Min, Food Microbiol. 38, 128 (2014). 10.1016/j.fm.2013.08.019
13. N. N. Misra, S. Patil, T. Moiseev, P. Bourke, J. P. Mosnier, K. M. Keener, and P. J. Cullen, J. Food Eng. 125, 131 (2014). 10.1016/j.jfoodeng.2013.10.023
14. B. A. Niemira, G. Boyd, and J. Sites, J. Food Sci. 79, M917 (2014). 10.1111/1750-3841.12379
15. B. A. Niemira, Annu. Rev. Food Sci. Technol. 3, 125 (2012). 10.1146/annurev-food-022811-101132
16. B. Ahlfeld, Y. Li, A. Boulaaba, A. Binder, U. Schotte, J. L. Zimmermann, G. Morfill, and G. Klein, mBio 6, e02300-14 (2015). 10.1128/mBio.02300-14
17. P. Attri, N. Kumar, J. H. Park, D. K. Yadav, S. Choi, H. S. Uhm, I. T. Kim, E. H. Choi, and W. Lee, Sci. Rep. 5, 8221 (2015). 10.1038/srep08221
18. A. Antoniu, T. Nakajima, H. Kurita, and A. Mizuno, J. Electrost. 72, 210 (2014). 10.1016/j.elstat.2014.02.004
19. Y. Tanaka, H. Yasuda, H. Kurita, K. Takashima, and A. Mizuno, IEEE Trans. Ind. Gen. Appl. 50, 1397 (2014). 10.1109/TIA.2013.2274260
20. H. Yasuda, M. Hashimoto, M. M. Rahman, K. Takashima, and A. Mizuno, Plasma Processes Polym. 5, 615 (2008). 10.1002/ppap.200800036
21. H. Yasuda, T. Miura, H. Kurita, K. Takashima, and A. Mizuno, Plasma Processes Polym. 7, 301 (2010). 10.1002/ppap.200900088
22. E. Takai, T. Kitamura, J. Kuwabara, S. Ikawa, S. Yoshizawa, K. Shiraki, H. Kawasaki, R. Arakawa, and K. Kitano, J. Phys. D: Appl. Phys. 47, 285403 (2014). 10.1088/0022-3727/47/28/285403
23. S. Hasse, O. Hahn, S. Kindler, T. V. Woedtke, H.-R. Metelmann, and K. Masur, Plasma Med. 4, 117 (2014). 10.1615/PlasmaMed.2014011978
24. A. Schmidt, K. Wende, S. Bekeschus, L. Bundscherer, A. Barton, K. Ottmüller, K.-D. Weltmann, and K. Masur, Free Radical Res. 47, 577 (2013). 10.3109/10715762.2013.804623
25. J. Liebmann, J. Scherer, N. Bibinov, P. Rajasekaran, R. Kovacs, R. Gesche, P. Awakowicz, and V. Kolb-Bachofen, Nitric Oxide 24, 8 (2011). 10.1016/j.niox.2010.09.005
26. S. Kalghatgi, G. Friedman, A. Fridman, and A. Clyne, Ann. Biomed. Eng. 38, 748 (2010). 10.1007/s10439-009-9868-x
27. R. N. Ma, H. Q. Feng, Y. D. Liang, Q. Zhang, Y. Tian, B. Su, J. Zhang, and J. Fang, J. Phys. D: Appl. Phys. 46, 285401 (2013). 10.1088/0022-3727/46/28/285401
28. N. Kaushik, N. Kumar, C. H. Kim, N. K. Kaushik, and E. H. Choi, Plasma Processes Polym. 11, 1175 (2014). 10.1002/ppap.201400102
29. E. A. Ratovitski, X. Cheng, D. Yan, J. H. Sherman, J. Canady, B. Trink, and M. Keidar, Plasma Processes Polym. 11, 1128 (2014). 10.1002/ppap.201400071
30. K. P. Arjunan, G. Friedman, A. Fridman, and A. M. Clyne, J. R. Soc., Interface 9, 147 (2012). 10.1098/rsif.2011.0220
31. V. Miller, A. Lin, G. Fridman, D. Dobrynin, and A. Fridman, Plasma Processes Polym. 11, 1193 (2014). 10.1002/ppap.201400168
32. M. J. Steinbeck, N. Chernets, J. Zhang, D. S. Kurpad, G. Fridman, A. Fridman, and T. A. Freeman, PLoS One 8, e82143 (2013). 10.1371/journal.pone.0082143
33. B. Gweon, M. Kim, D. B. Kim, D. Kim, H. Kim, H. Jung, H. J. Shin, and W. Choe, Appl. Phys. Lett. 99, 063701 (2011). 10.1063/1.3622631
34. B. Gweon, D. Kim, D. B. Kim, H. Jung, W. Choe, and J. H. Shin, Appl. Phys. Lett. 96, 101501 (2010). 10.1063/1.3352316
35. B. Gweon, H. Kim, K. Kim, M. Kim, E. Shim, S. Kim, W. Choe, and J. H. Shin, Appl. Phys. Lett. 104, 133701 (2014). 10.1063/1.4870623
36. Z. Xiong, T. Du, X. Lu, Y. Cao, and Y. Pan, Appl. Phys. Lett. 98, 221503 (2011). 10.1063/1.3597622
37. M. Keidar, R. Walk, A. Shashurin, P. Srinivasan, A. Sandler, S. Dasgupta, R. Ravi, R. Guerrero-Preston, and B. Trink, Br. J. Cancer 105, 1295 (2011). 10.1038/bjc.2011.386
38. M. Keidar, A. Shashurin, O. Volotskova, M. A. Stepp, P. Srinivasan, A. Sandler, and B. Trink, Phys. Plasmas 20, 057101 (2013). 10.1063/1.4801516
39. E. J. Szili, S. A. Al-Bataineh, P. M. Bryant, R. D. Short, J. W. Bradley, and D. A. Steele, Plasma Processes Polym. 8, 38 (2011). 10.1002/ppap.201000082
40. G. Desmet, A. Michelmore, E. J. Szili, S.-J. Park, J. G. Eden, R. D. Short, and S. A. Al-Bataineh, RSC Adv. 3, 13437 (2013). 10.1039/c3ra42025f
41. R. M. France and R. D. Short, J. Chem. Soc., Faraday Trans. 93, 3173 (1997). 10.1039/a702311a
42. D. B. Graves, Clin. Plasma Med. 2, 38 (2014). 10.1016/j.cpme.2014.11.001
43. N. Barekzi and M. Laroussi, Plasma Processes Polym. 10, 1039 (2013). 10.1002/ppap.201300083
44. M. Laroussi, Plasma Processes Polym. 11, 1138 (2014). 10.1002/ppap.201400152
45. D. B. Graves, J. Phys. D: Appl. Phys. 45, 263001 (2012). 10.1088/0022-3727/45/26/263001
46. D. B. Graves, Plasma Processes Polym. 11, 1120 (2014). 10.1002/ppap.201400068
47. C. Chen, D. X. Liu, Z. C. Liu, A. J. Yang, H. L. Chen, G. Shama, and M. G. Kong, Plasma Chem. Plasma Process. 34, 403 (2014). 10.1007/s11090-014-9545-1
48. D.-X. Liu, M.-Z. Rong, X.-H. Wang, F. Iza, M. G. Kong, and P. Bruggeman, Plasma Processes Polym. 7, 846 (2010). 10.1002/ppap.201000049
49. W. Tian and M. J. Kushner, J. Phys. D: Appl. Phys. 47, 165201 (2014). 10.1088/0022-3727/47/16/165201
50. G. Collet, E. Robert, A. Lenoir, M. Vandamme, T. Darny, S. Dozias, C. Kieda, and J. M. Pouvesle, Plasma Sources Sci. Technol. 23, 012005 (2014). 10.1088/0963-0252/23/1/012005
51. J. W. Fluhr, S. Sassning, O. Lademann, M. E. Darvin, S. Schanzer, A. Kramer, H. Richter, W. Sterry, and J. Lademann, Exp. Dermatol. 21, 130 (2012). 10.1111/j.1600-0625.2011.01411.x
52. O. Lademann, H. Richter, A. Kramer, A. Patzelt, M. C. Meinke, C. Graf, Q. Gao, E. Korotianskiy, E. Rühl, K. D. Weltmann, J. Lademann, and S. Koch, Laser Phys. Lett. 8, 758 (2011). 10.1002/lapl.201110055
53. J. Lademann, A. Patzelt, H. Richter, O. Lademann, G. Baier, L. Breucker, and K. Landfester, Laser Phys. Lett. 10, 083001 (2013). 10.1088/1612-2011/10/8/083001
54. O. Lademann, H. Richter, M. C. Meinke, A. Patzelt, A. Kramer, P. Hinz, K.-D. Weltmann, B. Hartmann, and S. Koch, Exp. Dermatol. 20, 488 (2011). 10.1111/j.1600-0625.2010.01245.x
55. E. J. Szili, J. W. Bradley, and R. D. Short, J. Phys. D: Appl. Phys. 47, 152002 (2014). 10.1088/0022-3727/47/15/152002
56. S. E. Marshall, A. T. A. Jenkins, S. A. Al-Bataineh, R. D. Short, S.-H. Hong, N. T. Thet, J.-S. Oh, J. W. Bradley, and E. J. Szili, J. Phys. D: Appl. Phys. 46, 185401 (2013). 10.1088/0022-3727/46/18/185401
57. M. J. Traylor, M. J. Pavlovich, S. Karim, P. Hait, Y. Sakiyama, D. S. Clark, and D. B. Graves, J. Phys. D: Appl. Phys. 44, 472001 (2011). 10.1088/0022-3727/44/47/472001
58. B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, 4th ed. (Oxford University Press, 2007).
59. N. Milan-Segovia, Y. Wang, F. S. Cannon, R. C. Voigt, and J. C. Furness, Ozone: Sci. Eng. 29, 461 (2007). 10.1080/01919510701615433
60. S. Kanazawa, T. Furuki, T. Nakaji, S. Akamine, and R. Ichiki, J. Phys.: Conf. Ser. 418, 012102 (2013). 10.1088/1742-6596/418/1/012102
61. Y. Kim, Y. Hong, K. Baik, G. Kwon, J. Choi, G. Cho, H. Uhm, D. Kim, and E. Choi, Plasma Chem. Plasma Process. 34, 457 (2014). 10.1007/s11090-014-9538-0
62. Z.-S. Wu, S.-B. Zhang, M.-M., Guo, C.-R. Chen, G.-L. Shen, and R.-Q. Yu, Anal. Chim. Acta 584, 122 (2007). 10.1016/j.aca.2006.11.003
63. S. Reuter, H. Tresp, K. Wende, M. U. Hammer, J. Winter, K. Masur, A. Schmidt-Bleker, and K. Weltmann, IEEE Trans. Plasma Sci. 40, 2986 (2012). 10.1109/TPS.2012.2207130
64. S.-H. Hong, E. J. Szili, A. T. A. Jenkins, and R. D. Short, J. Phys. D: Appl. Phys. 47, 362001 (2014). 10.1088/0022-3727/47/36/362001
65. See supplementary material at http://dx.doi.org/10.1063/1.4930874 E-APPLAB-107-039537 for experimental methods and supporting data.
66. A. Ní Annaidh, K. Bruyère, M. Destrade, M. D. Gilchrist, and M. Otténio, J. Mech. Behav. Biomed. Mater. 5, 139 (2012). 10.1016/j.jmbbm.2011.08.016
67. M. Vandamme, E. Robert, S. Pesnel, E. Barbosa, S. Dozias, J. Sobilo, S. Lerondel, A. Le Pape, and J.-M. Pouvesle, Plasma Processes Polym. 7, 264 (2010). 10.1002/ppap.200900080
68. E. J. Szili, J.-S. Oh, S.-H. Hong, A. Hatta, and R. D. Short, J. Phys. D: Appl. Phys. 48, 202001 (2015). 10.1088/0022-3727/48/20/202001
69. P. Attri, Y. H. Kim, D. H. Park, J. H. Park, Y. J. Hong, H. S. Uhm, K.-N. Kim, A. Fridman, and E. H. Choi, Sci. Rep. 5, 9332 (2015). 10.1038/srep09332
70. J.-S. Oh, E. J. Szili, N. Gaur, S.-H. Hong, H. Furuta, R. D. Short, and A. Hatta, J. Photopolym. Sci. Technol. 28, 439 (2015).
71. S.-H. Hong, E. J. Szili, A. T. A. Jenkins, and R. D. Short, J. Phys. D: Appl. Phys. 48, 029501 (2015). 10.1088/0022-3727/48/2/029501
72. E. Damiani, B. Kalinska, A. Canapa, S. Canestrari, M. Wozniak, E. Olmo, and L. Greci, Free Radical Biol. Med. 28, 1257 (2000). 10.1016/S0891-5849(00)00242-2
73. K.-I. Setsukinai, Y. Urano, K. Kakinuma, H. J. Majima, and T. Nagano, J. Biol. Chem. 278, 3170 (2003). 10.1074/jbc.M209264200
74. S. Gebicki and J. M. Gebicki, Biochem. J. 289, 743 (1993). 10.1042/bj2890743
75. D. Yan, J. H. Sherman, X. Cheng, E. Ratovitski, J. Canady, and M. Keidar, Appl. Phys. Lett. 105, 224101 (2014). 10.1063/1.4902875