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State of the art in medical applications using non-thermal atmospheric pressure plasma

Abstract

Plasma medical science is a novel interdisciplinary field that combines studies on plasma science and medical science, with the anticipation that understanding the scientific principles governing plasma medical science will lead to innovations in the field. Non-thermal atmospheric pressure plasma has been used for medical treatments, such as for cancer, blood coagulation, and wound healing. The interactions that occur between plasma and cells/tissues have been analyzed extensively. Direct and indirect treatment of cells with plasma has broadened the applications of non-thermal atmospheric pressure plasma in medicine. Examples of indirect treatment include plasma-assisted immune-therapy and plasma-activated medium. Controlling intracellular redox balance may be key in plasma cancer treatment. Animal studies are required to test the effectiveness and safety of these treatments for future clinical applications.

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(Adapted from Akihiro Kono’s lecture notes)

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From (Schutze et al. 1998)

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From Akihiro Kono’s lecture note

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Abbreviations

ALK:

Anaplastic lymphoma kinase

AMD:

Age-related macular degeneration

APF:

Aminophenyl Fluorescein

CNV:

Choroidal neovascularization

DAPI:

4′,6-diamidino-2-phenylindole

DBD:

Dielectric barrier discharge

DNA:

deoxyribonucleic acid

DSB:

Double-strand break

EGFR:

Epidermal growth factor receptor

ERK:

Extracellular signal-regulated kinase

ESR:

Electron spin resonance

FACS:

Fluoresence-activated cell sorting

GFP:

Green fluorescent protein

H2DCFDA:

2′,7′-dichlorodihydrofluorescein diacetate

HNE:

4-Hydroxy-2-nonenal (HNE)

HPF:

Hydroxyphenyl Fluorescein

ICD:

Immunogenic cell death

iPS:

induced pluripotent stem cells

LDH:

Lactate dehydrogenase

LIF:

Laser-induced fluorescence

MAPK:

Mitogen-activated protein kinase

mRNA:

Messenger RNA

mTOR:

Mammalian target of rapamycin

mTORC1:

mTOR complex 1

mTORC2:

mTOR complex 2

MTS:

5-(3-carboxymethoxyphenyl)-2-(4,5-dimenthylthiazoly)-3-(4-sulfophenyl)tetrazo-lium, inner salt

NAC:

N-acetyl cysteine

NEAPP:

Non equilibrium atmospheric pressure plasma

NHDFs:

Normal human dermal fibroblasts

OES:

Optical emission spectroscopy

PAL:

Plasma-activated Ringer’s lactate solution

PAM:

PAM

PARP:

Poly (ADP-ribose) polymerase

PCR:

Polymerase chain reaction

PD-L1:

Programmed death ligand 1

PI:

Propidium iodide

PI3K:

Phosphatidylinositol-4,5-bisphosphate 3-kinase

PIP2:

Phosphatidylinositol 4,5-bisphosphate

PIP3:

Phosphatidylinositol (3,4,5) trisphosphates

PTEN:

Phosphatase and tensin homolog

RAS:

Rat sarcoma

ROS:

Reactive oxygen species

RNA:

Ribonucleic acid

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

RT-PCR:

Real-time polymerase chain reaction

SEM:

Scanning electron microscope

SDS:

Sodium dodecyl sulfate

SDS-PAGE:

SDS polyacrylamide gel electrophoresis

SOD:

Superoxide dismutase

TBARS:

Thiobarbituric acid reactive substances

TALIF:

Two-photon absorption laser-induced fluorescence

TP53:

Tumor suppressor protein p53

TUNEL:

Terminal deoxynucleotidyl transferase (TdT)-mediated dUTP nick end labeling

VEGFR:

Vascular endothelial growth factor receptor

VUVAS:

Vacuum ultraviolet absorption spectroscopy

References

  1. T. Adachi, S. Nonomura, M. Horiba, T. Hirayama, T. Kamiya, H. Nagasawa, H. Hara, Iron stimulates plasma-activated medium-induced A549 cell injury. Sci. Rep. 6, 20928 (2016)

    ADS  Article  Google Scholar 

  2. T. Adachi, H. Tanaka, S. Nonomura, H. Hara, S.I. Kondo, M. Hori, Plasma-activated medium induces A549 cell injury via a spiral apoptotic cascade involving the mitochondrial-nuclear network. Free Radic. Biol. Med. 79C, 28–44 (2014)

    Google Scholar 

  3. S. Adler, M. Scherrer, F.D. Daschner, Costs of low-temperature plasma sterilization compared with other sterilization methods. J. Hosp. Infect. 40, 125–134 (1998)

    Article  Google Scholar 

  4. H.J. Ahn, K.I. Kim, G. Kim, E. Moon, S.S. Yang, J.S. Lee, Atmospheric-pressure plasma jet induces apoptosis involving mitochondria via generation of free radicals. Plos One 6, e28154 (2011)

    ADS  Article  Google Scholar 

  5. Y. Akimoto, S. Ikehara, T. Yamaguchi, J. Kim, H. Kawakami, N. Shimizu, M. Hori, H. Sakakita, Y. Ikehara, Galectin expression in healing wounded skin treated with low-temperature plasma: comparison with treatment by electronical coagulation. Arch. Biochem. Biophys. 605, 86–94 (2016)

    Article  Google Scholar 

  6. S. Arena, B. Bellosillo, G. Siravegna, A. Martinez, I. Canadas, L. Lazzari, N. Ferruz, M. Russo, S. Misale, I. Gonzalez et al., Emergence of multiple EGFR extracellular mutations during cetuximab treatment in colorectal cancer. Clin. Cancer Res. 21, 2157–2166 (2015)

    Article  Google Scholar 

  7. P. Awakowicz, N. Bibinov, M. Born, B. Busse, R. Gesche, A. Helmke, A. Kaemling, V. Kolb-Bachofen, R. Kovacs, S. Kuehn et al., Biological stimulation of the human skin applying health-promoting light and plasma sources. Contrib. Plasma Phys. 49, 641–647 (2009)

    ADS  Article  Google Scholar 

  8. S. Bavcar, D.J. Argyle, Receptor tyrosine kinase inhibitors: molecularly targeted drugs for veterinary cancer therapy. Vet. Comp. Oncol. 10, 163–173 (2012)

    Article  Google Scholar 

  9. S.G. Belostotskiy, R. Khandelwal, Q. Wang, V.M. Donnelly, D.J. Economou, N. Sadeghi, Measurement of electron temperature and density in an argon microdischarge by laser Thomson scattering. Appl. Phys. Lett. 92, 221507 (2008)

    ADS  Article  Google Scholar 

  10. B. Benstaali, P. Boubert, B.G. Cheron, A. Addou, J.L. Brisset, Density and rotational temperature measurements of the OH degrees and NO degrees radicals produced by a gliding arc in humid air. Plasma Chem. Plasma Process. 22, 553–571 (2002)

    Article  Google Scholar 

  11. M.A. Bogle, K.A. Arndt, J.S. Dover, Evaluation of plasma skin regeneration technology in low-energy full-facial rejuvenation. Arch. Dermatol. 143, 168–174 (2007)

    Article  Google Scholar 

  12. A. Bourdon, T. Darny, F. Pechereau, J.M. Pouvesle, P. Viegas, S. Iseni, E. Robert, Numerical and experimental study of the dynamics of a mu s helium plasma gun discharge with various amounts of N-2 admixture. Plasma Sources Sci. Technol. 25, 035002 (2016)

    ADS  Article  Google Scholar 

  13. J.L. Brisset, J. Pawlat, Chemical effects of air plasma species on aqueous solutes in direct and delayed exposure modes: discharge, post-discharge and plasma activated water. Plasma Chem. Plasma Process. 36, 355–381 (2016)

    Article  Google Scholar 

  14. P. Bruggeman, C. Leys, Non-thermal plasmas in and in contact with liquids. J. Phys. D Appl. Phys. 42, 053001 (2009)

    ADS  Article  Google Scholar 

  15. J.G. Carneiro, P.G. Couto, L. Bastos-Rodrigues, M.A. Bicalho, P.V. Vidigal, A. Vilhena, N.F. Amaral, A.E. Bale, E. Friedman, L. De Marco, Spectrum of somatic EGFR, KRAS, BRAF, PTEN mutations and TTF-1 expression in Brazilian lung cancer patients. Genet. Res. 96, e002 (2014)

    Google Scholar 

  16. E. Caron, S. Ghosh, Y. Matsuoka, D. Ashton-Beaucage, M. Therrien, S. Lemieux, C. Perreault, P.P. Roux, H. Kitano, A comprehensive map of the mTOR signaling network. Mol. Syst. Biol. 6, 453 (2010)

    Article  Google Scholar 

  17. M. Chalfie, Y. Tu, G. Euskirchen, W.W. Ward, D.C. Prasher, Green fluorescent protein as a marker for gene expression. Science 263, 802–805 (1994)

    ADS  Article  Google Scholar 

  18. A.H. Cory, T.C. Owen, J.A. Barltrop, J.G. Cory, Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 3, 207–212 (1991)

    Google Scholar 

  19. C.V. Dang, MYC on the path to cancer. Cell 149, 22–35 (2012)

    Article  Google Scholar 

  20. F. De Andres-Trelles, Discovery and development of molecularly targeted drugs: regulatory perspectives. J. Chemother. 16(Suppl 4), 19–21 (2004)

    Article  Google Scholar 

  21. T. Decker, M.L. Lohmann-Matthes, A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Methods 115, 61–69 (1988)

    Article  Google Scholar 

  22. A.S. Dhillon, S. Hagan, O. Rath, W. Kolch, MAP kinase signalling pathways in cancer. Oncogene 26, 3279–3290 (2007)

    Article  Google Scholar 

  23. D. Dobrynin, G. Fridman, G. Friedman, A. Fridman, Physical and biological mechanisms of direct plasma interaction with living tissue. New J. Phys. 11, 115020 (2009)

    ADS  Article  Google Scholar 

  24. A. Fridman, S. Nester, L.A. Kennedy, A. Saveliev, O. Mutaf-Yardimci, Gliding arc gas discharge. Prog. Energy Combust. Sci. 25, 211–231 (1999)

    Article  Google Scholar 

  25. G. Fridman, G. Friedman, A. Gutsol, A.B. Shekhter, V.N. Vasilets, A. Fridman, Applied plasma medicine. Plasma Process. Polym. 5, 503–533 (2008)

    Article  Google Scholar 

  26. G. Fridman, M. Peddinghaus, H. Ayan, A. Fridman, M. Balasubramanian, A. Gutsol, A. Brooks, G. Friedman, Blood coagulation and living tissue sterilization by floating-electrode dielectric barrier discharge in air. Plasma Chem. Plasma Process. 26, 425–442 (2006)

    Article  Google Scholar 

  27. G. Fridman, A. Shereshevsky, M.M. Jost, A.D. Brooks, A. Fridman, A. Gutsol, V. Vasilets, G. Friedman, Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines. Plasma Chem. Plasma Process. 27, 163–176 (2007)

    Article  Google Scholar 

  28. A.F. Frijhoff, C.J. Conti, A.M. Senderowicz, Advances in molecular carcinogenesis: current and future use of mouse models to screen and validate molecularly targeted anticancer drugs. Mol. Carcinog. 39, 183–194 (2004)

    Article  Google Scholar 

  29. M.J. Fulwyler, Electronic separation of biological cells by volume. Science 150, 910–911 (1965)

    ADS  Article  Google Scholar 

  30. Y. Gavrieli, Y. Sherman, S.A. Ben-Sasson, Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell. Biol. 119, 493–501 (1992)

    Article  Google Scholar 

  31. G.G. Ginsberg, A.N. Barkun, J.J. Bosco, J.S. Burdick, G.A. Isenberg, N.L. Nakao, B.T. Petersen, W.B. Silverman, A. Slivka, P.B. Kelsey et al., The argon plasma coagulator. Gastrointest. Endosc. 55, 807–810 (2002)

    Article  Google Scholar 

  32. J. Golda, J. Held, B. Redeker, M. Konkowski, P. Beijer, A. Sobota, G. Kroesen, N.S. Braithwaite, S. Reuter, M.M. Turner et al., Concepts and characteristics of the ‘COST Reference Microplasma Jet’. J Phys. D Appl. Phys. 49, 084003 (2016)

    ADS  Article  Google Scholar 

  33. M. Goldman, L. Pruitt, Comparison of the effects of gamma radiation and low temperature hydrogen peroxide gas plasma sterilization on the molecular structure, fatigue resistance, and wear behavior of UHMWPE. J. Biomed. Mater. Res. 40, 378–384 (1998)

    Article  Google Scholar 

  34. G.S. Graham, T.J. Mielnik, Industrial low-temperature gas plasma sterilization. Med. Device Technol. 8, 28–30 (1997)

    Google Scholar 

  35. D.B. Graves, 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 Appl. Phys. 45, 263001 (2012)

    ADS  Article  Google Scholar 

  36. D.A. Guertin, D.M. Sabatini, Defining the role of mTOR in cancer. Cancer Cell 12, 9–22 (2007)

    Article  Google Scholar 

  37. D. Hanahan, R.A. Weinberg, Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011)

    Article  Google Scholar 

  38. H. Hara, M. Taniguchi, M. Kobayashi, T. Kamiya, T. Adachi, Plasma-activated medium-induced intracellular zinc liberation causes death of SH-SY5Y cells. Arch. Biochem. Biophys. 584, 51–60 (2015)

    Article  Google Scholar 

  39. D.R. Harper, M.L. Kit, H.O. Kangro, Protein blotting: ten years on. J. Virol. Methods 30, 25–39 (1990)

    Article  Google Scholar 

  40. N. Hattori, S. Yamada, K. Torii, S. Takeda, K. Nakamura, H. Tanaka, H. Kajiyama, M. Kanda, T. Fujii, G. Nakayama et al., Effectiveness of plasma treatment on pancreatic cancer cells. Int. J. Oncol. 47, 1655–1662 (2015)

    Article  Google Scholar 

  41. J. Heinlin, G. Morfill, M. Landthaler, W. Stolz, G. Isbary, J.L. Zimmermann, T. Shimizu, S. Karrer, Plasma medicine: possible applications in dermatology. J. Dtsch. Dermatol. Ges. 8, 968–976 (2010)

    Google Scholar 

  42. L.A. Herzenberg, D. Parks, B. Sahaf, O. Perez, M. Roederer, The history and future of the fluorescence activated cell sorter and flow cytometry: a view from Stanford. Clin. Chem. 48, 1819–1827 (2002)

    Google Scholar 

  43. R. Higuchi, C. Fockler, G. Dollinger, R. Watson, Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology (N Y) 11, 1026–1030 (1993)

    Google Scholar 

  44. P.M. Holland, R.D. Abramson, R. Watson, D.H. Gelfand, Detection of specific polymerase chain reaction product by utilizing the 5′—3′ exonuclease activity of Thermus aquaticus DNA polymerase. Proc. Natl. Acad. Sci. USA. 88, 7276–7280 (1991)

    ADS  Article  Google Scholar 

  45. M. Hori, M. Laroussi, K. Masur, Y. Ikehara, Plasma processes and cancer—special topical cluster of the 2nd IWPCT meeting. Plasma Process. Polym. 12, 1336–1337 (2015)

    Article  Google Scholar 

  46. L. Huang, H. Fernandes, H. Zia, P. Tavassoli, H. Rennert, D. Pisapia, M. Imielinski, A. Sboner, M.A. Rubin, M. Kluk et al., The cancer precision medicine knowledge base for structured clinical-grade mutations and interpretations. J. Am. Med. Inform. Assoc. JAMIA 24, 513 (2016)

    Google Scholar 

  47. M. Huang, D.S. Hanselman, P. Yang, G.M. Hieftje, Isocontour maps of electron temperature, electron number density and gas kinetic temperature in the Ar inductively coupled plasma obtained by laser-light Thomson and Rayleigh scattering. Spectrochim. Acta B 47, 765–785 (1992)

    ADS  Article  Google Scholar 

  48. M. Huang, A. Shen, J. Ding, M. Geng, Molecularly targeted cancer therapy: some lessons from the past decade. Trends Pharmacol. Sci. 35, 41–50 (2014)

    Article  Google Scholar 

  49. S. Hubner, S. Hofmann, E.M. van Veldhuizen, P.J. Bruggeman, Electron densities and energies of a guided argon streamer in argon and air environments. Plasma Sources Sci. Technol. 22, 065011 (2013)

    ADS  Article  Google Scholar 

  50. S. Hubner, J.S. Sousa, V. Puech, G.M.W. Kroesen, N. Sadeghi, Electron properties in an atmospheric helium plasma jet determined by Thomson scattering. J. Phys. D: Appl. Phys. 47, 432001 (2014)

    Article  Google Scholar 

  51. S. Hubner, J.S. Sousa, J.J.A.M. van der Mullen, W.G. Graham, Thomson scattering on non-thermal atmospheric pressure plasma jets. Plasma Sources Sci. Tech. 24, 1–15 (2015)

    Google Scholar 

  52. S. Ikawa, K. Kitano, S. Hamaguchi, Effects of pH on bacterial inactivation in aqueous solutions due to low-temperature atmospheric pressure plasma application. Plasma Process. Polym. 7, 33–42 (2010)

    Article  Google Scholar 

  53. S. Ikehara, H. Sakakita, K. Ishikawa, Y. Akimoto, T. Yamaguchi, M. Yamagishi, J. Kim, M. Ueda, J. Ikeda, H. Nakanishi et al., Plasma blood coagulation without involving the activation of platelets and coagulation factors. Plasma Process. Polym. 12, 1348–1353 (2015)

    Article  Google Scholar 

  54. Y. Ikehara, H. Sakakita, N. Shimizu, S. Ikehara, H. Nakanish, Formation of membrane-like structures in clotted blood by mild plasma treatment during hemostasis. J. Photopolym. Sci. Technol. 26, 555–557 (2013)

    Article  Google Scholar 

  55. G. Isbary, J. Heinlin, T. Shimizu, J.L. Zimmermann, G. Morfill, H.U. Schmidt, R. Monetti, B. Steffes, W. Bunk, Y. Li 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. 167, 404–410 (2012)

    Article  Google Scholar 

  56. G. Isbary, G. Morfill, H.U. Schmidt, M. Georgi, K. Ramrath, J. Heinlin, S. Karrer, M. Landthaler, T. Shimizu, B. Steffes 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. 163, 78–82 (2010)

    Google Scholar 

  57. G. Isbary, G. Morfill, J. Zimmermann, T. Shimizu, W. Stolz, Cold atmospheric plasma: a successful treatment of lesions in Hailey–Hailey disease. Arch. Dermatol. 147, 388–390 (2011)

    Article  Google Scholar 

  58. S. Iseki, H. Hashizume, F. Jia, K. Takeda, K. Ishikawa, T. Ohta, M. Ito, M. Hori, Inactivation of Penicillium digitatum spores by a high-density ground-state atomic oxygen-radical source employing an atmospheric-pressure plasma. Appl. Phys. Express 4(11), 116201 (2011)

    ADS  Article  Google Scholar 

  59. S. Iseki, K. Nakamura, M. Hayashi, H. Tanaka, H. Kondo, H. Kajiyama, H. Kano, F. Kikkawa, M. Hori, Selective killing of ovarian cancer cells through induction of apoptosis by nonequilibrium atmospheric pressure plasma. Appl. Phys. Lett. 100, 113702 (2012)

    ADS  Article  Google Scholar 

  60. S. Iseki, T. Ohta, A. Aomatsu, M. Ito, H. Kano, Y. Higashijima, M. Hori, Rapid inactivation of Penicillium digitatum spores using high-density nonequilibrium atmospheric pressure plasma. Appl. Phys. Lett. 96, 153704 (2010)

    ADS  Article  Google Scholar 

  61. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, M. Yamamoto, Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76–86 (1999)

    Article  Google Scholar 

  62. M. Iwasaki, H. Inui, Y. Matsudaira, H. Kano, N. Yoshida, M. Ito, M. Hori, Nonequilibrium atmospheric pressure plasma with ultrahigh electron density and high performance for glass surface cleaning. Appl. Phys. Lett. 92, 081503 (2008)

    ADS  Article  Google Scholar 

  63. J.K. Jürgen Schlegel, Veronika Boxhammer, Plasma in cancer treatment. Clin. Plasma Med. 1, 2–7 (2013)

    Article  Google Scholar 

  64. M.C. Jaramillo, D.D. Zhang, The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev. 27, 2179–2191 (2013)

    Article  Google Scholar 

  65. F.D. Jia, N. Sumi, K. Ishikawa, H. Kano, H. Inui, J. Kularatne, K. Takeda, H. Kondo, M. Sekine, A. Kono et al., Laser scattering diagnosis of a 60-Hz non-equilibrium atmospheric pressure plasma jet. Appl. Phys. Express 4, 026101 (2011)

    ADS  Article  Google Scholar 

  66. M. Jinno, Y. Ikeda, H. Motomura, Y. Kido, S. Satoh, Investigation of plasma induced electrical and chemical factors and their contribution processes to plasma gene transfection. Arch. Biochem. Biophys. 605, 59–66 (2016)

    Article  Google Scholar 

  67. M. Jinno, Y. Ikeda, H. Motomura, Y. Kido, K. Tachibana, S. Satoh, The necessity of radicals for gene transfection by discharge plasma irradiation. J. Photopolym. Sci. Technol. 27, 309–404 (2014)

    Article  Google Scholar 

  68. H.M. Joh, S.J. Kim, T.H. Chung, S.H. Leem, Reactive oxygen species-related plasma effects on the apoptosis of human bladder cancer cells in atmospheric pressure pulsed plasma jets. Appl. Phys. Lett. 101, 053703 (2012)

    ADS  Article  Google Scholar 

  69. F. Judee, C. Fongia, B. Ducommun, M. Yousfi, V. Lobjois, N. Merbahi, Short and long time effects of low temperature Plasma Activated Media on 3D multicellular tumor spheroids. Sci. Rep-UK 6, 21421 (2016)

    ADS  Article  Google Scholar 

  70. H. Kajiyama, K. Nakamura, F. Utsumi, H. Tanaka, M. Hori, F. Kikkawa, Perspective of strategic plasma therapy in patients with epithelial ovarian cancer: a short review of plasma in cancer treatment. Jpn. J. Appl. Phys. 53, 1–4 (2014)

    Article  Google Scholar 

  71. H. Kajiyama, F. Utsumi, K. Nakamura, H. Tanaka, M. Mizuno, S. Toyokuni, M. Hori, F. Kikkawa, Possible therapeutic option of aqueous plasma for refractory ovarian cancer. Clin. Plasma Med. 4, 14–18 (2016)

    Article  Google Scholar 

  72. S.U. Kalghatgi, G. Fridman, M. Cooper, G. Nagaraj, M. Peddinghaus, M. Balasubramanian, V.N. Vasilets, A.F. Gutsol, A. Fridman, G. Friedman, Mechanism of blood coagulation by nonthermal atmospheric pressure dielectric barrier discharge plasma. IEEE Trans. Plasma Sci. 35, 1559–1566 (2007)

    ADS  Article  Google Scholar 

  73. S. Kanazawa, M. Kogoma, T. Moriwaki, S. Okazaki, Stable glow plasma at atmospheric-pressure. J. Phys. D Appl. Phys. 21, 838–840 (1988)

    ADS  Article  Google Scholar 

  74. J. Kapuscinski, DAPI: a DNA-specific fluorescent probe. Biotech. Histochem. 70, 220–233 (1995)

    Article  Google Scholar 

  75. M. Keidar, A. Shashurin, O. Volotskova, M.A. Stepp, P. Srinivasan, A. Sandler, B. Trink, Cold atmospheric plasma in cancer therapy. Phys. Plasmas 20, 057101 (2013)

    ADS  Article  Google Scholar 

  76. M. Keidar, R. Walk, A. Shashurin, P. Srinivasan, A. Sandler, S. Dasgupta, R. Ravi, R. Guerrero-Preston, B. Trink, Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br. J. Cancer 105, 1295–1301 (2011)

    Article  Google Scholar 

  77. M.M. Kekez, M.R. Barrault, J.D. Craggs, Spectroscopic investigation of the spark channel. J. Phys. D Appl. Phys. 5, 1886 (1970)

    ADS  Article  Google Scholar 

  78. I.E. Kieft, J.L.V. Broers, V. Caubet-Hilloutou, D.W. Slaaf, F.C.S. Ramaekers, E. Stoffels, Electric discharge plasmas influence attachment of cultured CHO k1 cells. Bioelectromagnetics 25, 362–368 (2004)

    Article  Google Scholar 

  79. I.E. Kieft, M. Kurdi, E. Stoffels, Reattachment and apoptosis after plasma-needle treatment of cultured cells. IEEE Trans. Plasma Sci. 34, 1331–1336 (2006)

    ADS  Article  Google Scholar 

  80. K. Kim, J.D. Choi, Y.C. Hong, G. Kim, E.J. Noh, J.S. Lee, S.S. Yang, Atmospheric-pressure plasma-jet from micronozzle array and its biological effects on living cells for cancer therapy. Appl. Phys. Lett. 98, 073701 (2011)

    ADS  Article  Google Scholar 

  81. H. Kitano, Systems biology: a brief overview. Science 295, 1662–1664 (2002)

    ADS  Article  Google Scholar 

  82. M.G. Kong, G. Kroesen, G. Morfill, T. Nosenko, T. Shimizu, J. van Dijk, J.L. Zimmermann, Plasma medicine: an introductory review. New J. Phys. 11, 115012 (2009)

    ADS  Article  Google Scholar 

  83. A. Kono, K. Iwamoto, High-spatial-resolution multichannel Thomson scattering measurements for atmospheric pressure microdischarge. Japan. J. Appl. Phys. 43, 8A (2004)

    ADS  Article  Google Scholar 

  84. Y.D. Korolev, O.B. Frants, N.V. Landl, A.V. Bolotov, V.O. Nekhoroshev, Features of a near-cathode region in a gliding arc discharge in air flow. Plasma Sources Sci. Technol. 23, 054016 (2014)

    ADS  Article  Google Scholar 

  85. N. Kumar, J.H. Park, S.N. Jeon, B.S. Park, E.H. Choi, P. Attri, The action of microsecond-pulsed plasma-activated media on the inactivation of human lung cancer cells. J. Phys. D Appl. Phys. 49, 115401 (2016)

    ADS  Article  Google Scholar 

  86. L.J. Kuo, L.X. Yang, Gamma-H2AX—a novel biomarker for DNA double-strand breaks. In Vivo 22, 305–309 (2008)

    Google Scholar 

  87. N. Kurake, H. Tanaka, K. Ishikawa, K. Takeda, H. Hashizume, K. Nakamura, H. Kajiyama, T. Kondo, F. Kikkawa, M. Mizuno et al., Effects of ·OH and ·NO radicals in the aqueous phase on H2O2 and NO2- generated in plasma-activated medium. J. Phys. D Appl. Phys. 50, 155202 (2017)

    ADS  Article  Google Scholar 

  88. N. Kurake, H. Tanaka, K. Ishikawa, T. Kondo, M. Sekine, K. Nakamura, H. Kajiyama, F. Kikkawa, M. Mizuno, M. Hori, Cell survival of glioblastoma grown in medium containing hydrogen peroxide and/or nitrite, or in plasma-activated medium. Arch. Biochem. Biophys. 605, 102–108 (2016)

    Article  Google Scholar 

  89. B.T. Kurien, R.H. Scofield, Western blotting. Methods 38, 283–293 (2006)

    Article  Google Scholar 

  90. O. Lademann, H. Richter, A. Patzelt, A. Alborova, D. Humme, K.D. Weltmann, B. Hartmann, P. Hinz, A. Kramer, S. Koch, Application of a plasma-jet for skin antisepsis: analysis of the thermal action of the plasma by laser scanning microscopy. Laser Phys. Lett. 7, 458–462 (2010)

    ADS  Article  Google Scholar 

  91. D.P. Lane, Cancer. p53, guardian of the genome. Nature 358, 15–16 (1992)

    ADS  Article  Google Scholar 

  92. M. Laroussi, Nonthermal decontamination of biological media by atmospheric-pressure plasmas: review, analysis, and prospects. IEEE Trans. Plasma Sci. 30, 1409–1415 (1992)

    ADS  Article  Google Scholar 

  93. M. Laroussi, Sterilization of contaminated matter with an atmospheric pressure plasma. IEEE Trans. Plasma Sci. 24, 1188–1191 (1996)

    ADS  Article  Google Scholar 

  94. M. Laroussi, M. Keidar, Plasma processes and polymers special issue on: plasma and cancer. Plasma Process. Polym. 11, 1118–1119 (2014)

    Article  Google Scholar 

  95. M. Laroussi, J.P. Richardson, F.C. Dobbs, Effects of nonequilibrium atmospheric pressure plasmas on the heterotrophic pathways of bacteria and on their cell morphology. Appl. Phys. Lett. 81, 772–774 (2002)

    ADS  Article  Google Scholar 

  96. A.J. Levine, M. Oren, The first 30 years of p53: growing ever more complex. Nat. Rev. Cancer 9, 749–758 (2009)

    Article  Google Scholar 

  97. A. Lin, B. Truong, A. Pappas, L. Kirifides, A. Oubarri, S.Y. Chen, S.J. Lin, D. Dobrynin, G. Fridman, A. Fridman et al., Uniform nanosecond pulsed dielectric barrier discharge plasma enhances anti-tumor effects by induction of immunogenic cell death in tumors and stimulation of macrophages. Plasma Process. Polym. 12, 1392–1399 (2015)

    Article  Google Scholar 

  98. L.A. Loeb, K.R. Loeb, J.P. Anderson, Multiple mutations and cancer. Proc. Natl. Acad. Sci. USA. 100, 776–781 (2003)

    ADS  Article  Google Scholar 

  99. R. Matsumoto, K. Shimizu, T. Nagashima, H. Tanaka, M. Mizuno, F. Kikkawa, M. Hori, H. Honda, Plasma-activated medium selectively eliminates undifferentiated human induced pluripotent stem cells. Regener. Ther. 5, 55–63 (2016)

    Article  Google Scholar 

  100. H.-R. Metelmann, David S. Nedrelow, C. Seebauer, M. Schuster, T. von Woedtke, K.-D. Weltmann, S. Kindler, P.H. Metelmann, S.E. Finkelstein, D.D. Von Hoff et al., Head and neck cancer treatment and physical plasma. Clin. Plasma Med. 3, 17–23 (2015)

    Article  Google Scholar 

  101. N. Meyer, L.Z. Penn, Reflecting on 25 years with MYC. Nat. Rev. Cancer 8, 976–990 (2008)

    Article  Google Scholar 

  102. J.M. Miller, D.V. Palanker, A. Vankov, M.F. Marmor, M.S. Blumenkranz, Precision and safety of the pulsed electron avalanche knife in vitreoretinal surgery. Arch. Ophthalmol. Chic 121, 871–877 (2003)

    Article  Google Scholar 

  103. V. Miller, A. Lin, A. Fridman, Why target immune cells for plasma treatment of cancer. Plasma Chem. Plasma Process. 36, 259–268 (2016)

    Article  Google Scholar 

  104. V. Miller, A. Lin, G. Fridman, D. Dobrynin, A. Fridman, Plasma stimulation of migration of macrophages. Plasma Process. Polym. 11, 1193–1197 (2014)

    Article  Google Scholar 

  105. K. Miyamoto, S. Ikehara, H. Sakakita, Y. Ikehara, Low temperature plasma equipment applied on surgical hemostasis and wound healings. J. Clin. Biochem. Nutr. 60, 25–28 (2017)

    Article  Google Scholar 

  106. K. Miyamoto, S. Ikehara, H. Takei, Y. Akimoto, H. Sakakita, K. Ishikawa, M. Ueda, J.I. Ikeda, M. Yamagishi, J. Kim et al., Red blood cell coagulation induced by low-temperature plasma treatment. Arch. Biochem. Biophys. 605, 95–101 (2016)

    Article  Google Scholar 

  107. A. Mizuno, Y. Hori, Destruction of living cells by pulsed high-voltage application. IEEE Trans. Ind. Appl. 24, 387–394 (1988)

    Article  Google Scholar 

  108. S. Mohades, M. Laroussi, J. Sears, N. Barekzi, H. Razavi, Evaluation of the effects of a plasma activated medium on cancer cells. Phys. Plasmas 22, 122001 (2015)

    ADS  Article  Google Scholar 

  109. G.E. Morfill, M.G. Kong, J.L. Zimmermann, Focus on plasma medicine. New J. Phys. 11, 115011 (2009)

    ADS  Article  Google Scholar 

  110. K.B. Mullis, F.A. Faloona, Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 155, 335–350 (1987)

    Article  Google Scholar 

  111. N. Murray, The challenge of using biomarkers and molecularly targeted drugs to improve cure rate in early stage non-small cell lung cancer. J. Thorac. Dis. 7, 230–234 (2015)

    Google Scholar 

  112. N. Nandagopal, M.B. Elowitz, Synthetic biology: integrated gene circuits. Science 333, 1244–1248 (2011)

    ADS  Article  Google Scholar 

  113. E. Nedanovska, G. Nersisyan, T.J. Morgan, L. Hüwel, C.L.S. Lewis, D. Riley, W.G. Graham, Comparison of the electron density measurements using Thomson scattering and emission spectroscopy for laser induced breakdown in one atmosphere of helium. Appl. Phys. Lett. 99, 261504 (2011)

    ADS  Article  Google Scholar 

  114. S. Okazaki, M. Kogoma, M. Uehara, Y. Kimura, Appearance of stable glow-discharge in air, argon, oxygen and nitrogen at atmospheric-pressure using a 50-Hz source. J. Phys. D Appl. Phys. 26, 889–892 (1993)

    ADS  Article  Google Scholar 

  115. Y. Okazaki, Y. Wang, H. Tanaka, M. Mizuno, K. Nakamura, H. Kajiyama, H. Kano, K. Uchida, F. Kikkawa, M. Hori et al., Direct exposure of non-equilibrium atmospheric pressure plasma confers simultaneous oxidative and ultraviolet modifications in biomolecules. J. Clin. Biochem. Nutr. 55, 207–215 (2014)

    Article  Google Scholar 

  116. A. Pagano, F. Auxilia, S. Passarella, M.P. Casati, R. Pozzato, Low-temperature sterilization: evaluation of a method based on hydrogen peroxide gas plasma. Annali di igiene: medicina preventiva e di comunita 9, 153–164 (1997)

    Google Scholar 

  117. J. Park, I. Henins, H.W. Herrmann, G.S. Selwyn, R.F. Hicks, Discharge phenomena of an atmospheric pressure radio-frequency capacitive plasma source. J. Appl. Phys. 89, 20–28 (2001)

    ADS  Article  Google Scholar 

  118. A.V. Pipa, Y.Z. Ionikh, V.M. Chekishev, M. Dunnbier, S. Reuter, Resonance broadening of argon lines in a micro-scaled atmospheric pressure plasma jet (argon mu APPJ). Appl. Phys. Lett. 106, 244104 (2015)

    ADS  Article  Google Scholar 

  119. S.G. Priglinger, C. Haritoglou, D. Palanker, D. Kook, M. Grueterich, A. Mueller, C.S. Alge, A. Kampik, Pulsed electron avalanche knife for capsulotomy in congenital and mature cataract. J. Cataract Refr. Surg. 32, 1085–1088 (2006)

    Article  Google Scholar 

  120. B.J. Raphael, J.R. Dobson, L. Oesper, F. Vandin, Identifying driver mutations in sequenced cancer genomes: computational approaches to enable precision medicine. Genome Med. 6, 5 (2014)

    Article  Google Scholar 

  121. S. Reuter, H. Tresp, K. Wende, M.U. Hammer, J. Winter, K. Masur, A. Schmidt-Bleker, K.D. Weltmann, From RONS to ROS: tailoring plasma jet treatment of skin cells. IEEE Trans. Plasma Sci. 40, 2986–2993 (2012)

    ADS  Article  Google Scholar 

  122. A. Roettgen, I. Shkurenkov, M.S. Simeni, V. Petrishchev, I.V. Adamovich, W.R. Lempert, Time-resolved electron density and electron temperature measurements in nanosecond pulse discharges in helium. Plasma Sources Sci. Technol. 25, 055009 (2016)

    ADS  Article  Google Scholar 

  123. W.A. Rutala, M.F. Gergen, D.J. Weber, Comparative evaluation of the sporicidal activity of new low-temperature sterilization technologies: ethylene oxide, 2 plasma sterilization systems, and liquid peracetic acid. Am. J. Infect. Control 26, 393–398 (1998)

    Article  Google Scholar 

  124. H. Sakakita, S. Ikehara, Irradiation experiments on a mouse using a mild-plasma generator for medical applications. Plasma Fusion Res. 5, S2117–S2117 (2010)

    ADS  Article  Google Scholar 

  125. S. Sasaki, M. Kanzaki, T. Kaneko, Highly efficient and minimally invasive transfection using time-controlled irradiation of atmospheric-pressure plasma. Appl. Phys. Express 7, 026202 (2014)

    ADS  Article  Google Scholar 

  126. M. Schena, D. Shalon, R.W. Davis, P.O. Brown, Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270, 467–470 (1995)

    ADS  Article  Google Scholar 

  127. A. Schmidt-Bleker, J. Winter, A. Bosel, S. Reuter, K.D. Weltmann, On the plasma chemistry of a cold atmospheric argon plasma jet with shielding gas device. Plasma Sources Sci. Technol. 25, 015005 (2016)

    ADS  Article  Google Scholar 

  128. A. Schmidt, K. Wende, S. Bekeschus, L. Bundscherer, A. Barton, K. Ottmuller, K.D. Weltmann, K. Masur, Non-thermal plasma treatment is associated with changes in transcriptome of human epithelial skin cells. Free Radic. Res. 47, 577–592 (2013)

    Article  Google Scholar 

  129. C.G. Schregel, E.A.D. Carbone, D. Luggenholscher, U. Czarnetzki, Ignition and afterglow dynamics of a high pressure nanosecond pulsed helium micro-discharge: I. Electron, Rydberg molecules and He (2(3)S) densities. Plasma Sources Sci. Technol. 25, 054004 (2016)

    ADS  Article  Google Scholar 

  130. A. Schutze, J.Y. Jeong, S.E. Babayan, J. Park, G.S. Selwyn, R.F. Hicks, The atmospheric-pressure plasma jet: a review and comparison to other plasma sources. IEEE Trans. Plasma Sci. 26, 1685–1694 (1998)

    ADS  Article  Google Scholar 

  131. E. Seidler, The tetrazolium-formazan system: design and histochemistry. Prog. Histochem. Cytochem. 24, 1–86 (1991)

    Article  Google Scholar 

  132. R. Sensenig, S. Kalghatgi, E. Cerchar, G. Fridman, A. Shereshevsky, B. Torabi, K.P. Arjunan, E. Podolsky, A. Fridman, G. Friedman et al., Non-thermal plasma induces apoptosis in melanoma cells via production of intracellular reactive oxygen species (retracted article. see vol. 41, pg. 656, 2013). Ann. Biomed. Eng. 39, 674–687 (2011)

    Article  Google Scholar 

  133. K. Setsukinai, Y. Urano, K. Kakinuma, H.J. Majima, T. Nagano, Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278, 3170–3175 (2003)

    Article  Google Scholar 

  134. L. Shi, Y. Wang, F. Ito, Y. Okazaki, H. Tanaka, M. Mizuno, M. Hori, D.R. Richardson, S. Toyokuni, Biphasic effects of l-ascorbate on the tumoricidal activity of non-thermal plasma against malignant mesothelioma cells. Arch. Biochem. Biophys. 605, 109–116 (2016)

    Article  Google Scholar 

  135. O. Shimomura, F.H. Johnson, Y. Saiga, Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J. Cell. Comp. Physiol. 59, 223–239 (1962)

    Article  Google Scholar 

  136. C. Siemens, On the electrical tests employed during the construction of the malta and alexandria telegraph, and on insulating and protecting submarine cables. J. Frankl. Inst. 74, 166–170 (1862)

    Article  Google Scholar 

  137. M.S. Simeni, A. Roettgen, V. Petrishchev, K. Frederickson, I.V. Adamovich, Electron density and electron temperature measurements in nanosecond pulse discharges over liquid water surface. Plasma Sources Sci. Technol. 25, 064005 (2016)

    ADS  Article  Google Scholar 

  138. C. Spry, Low-temperature hydrogen peroxide gas plasma–atomic age sterilization technology. Today’s Surg. Nurse 20, 25–28 (1998)

    Google Scholar 

  139. E. Stoffels, A.J. Flikweert, W.W. Stoffels, G.M.W. Kroesen, Plasma needle: a non-destructive atmospheric plasma source for fine surface treatment of (bio)materials. Plasma Sources Sci. Technol. 11, 383–388 (2002)

    ADS  Article  Google Scholar 

  140. W. Strober, Trypan blue exclusion test of cell viability. Curr. Protoc. Immunol. 3, Appendix 3B (2001)

    Google Scholar 

  141. J. Su, M. Cai, W. Li, B. Hou, H. He, C. Ling, T. Huang, H. Liu, Y. Guo, Molecularly targeted drugs plus radiotherapy and temozolomide treatment for newly diagnosed glioblastoma: a meta-analysis and systematic review. Oncol. Res. 24, 117–128 (2016)

    Article  Google Scholar 

  142. Z. Su, D. Dias-Santagata, M. Duke, K. Hutchinson, Y.L. Lin, D.R. Borger, C.H. Chung, P.P. Massion, C.L. Vnencak-Jones, A.J. Iafrate et al., A platform for rapid detection of multiple oncogenic mutations with relevance to targeted therapy in non-small-cell lung cancer. J. Mol. Diagn. JMD 13, 74–84 (2011)

    Article  Google Scholar 

  143. Y. Tabuchi, H. Uchiyama, Q.L. Zhao, T. Yunoki, G. Andocs, N. Nojima, K. Takeda, K. Ishikawa, M. Hori, T. Kondo, Effects of nitrogen on the apoptosis of and changes in gene expression in human lymphoma U937 cells exposed to argon-based cold atmospheric pressure plasma. Int. J. Mol. Med. 37, 1706–1714 (2016)

    Article  Google Scholar 

  144. M. Tajadini, M. Panjehpour, S.H. Javanmard, Comparison of SYBR Green and TaqMan methods in quantitative real-time polymerase chain reaction analysis of four adenosine receptor subtypes. Adv. Biomed. Res. 3, 85 (2014)

    Article  Google Scholar 

  145. Takeda Keigo, Ishikawa Kenji, Tanaka Hiromasa, Sekine Makoto, H. Masaru, Spatial distributions of O, N, NO, OH and vacuum ultraviolet light along gas flow direction in an AC-excited atmospheric pressure Ar plasma jet generated in open air. J. Phys. D Appl. Phys. 50, 195202 (2017)

    Article  Google Scholar 

  146. S. Takeda, S. Yamada, N. Hattori, K. Nakamura, H. Tanaka, H. Kajiyama, M. Kanda, D. Kobayashi, C. Tanaka, T. Fujii et al., Intraperitoneal administration of plasma-activated medium: proposal of a novel treatment option for peritoneal metastasis from gastric cancer. Ann. Surg. Oncol. 24, 1188–1194 (2017)

    Article  Google Scholar 

  147. H. Tanaka, M. Mizuno, K. Ishikawa, H. Kondo, K. Takeda, H. Hashizume, K. Nakamura, F. Utsumi, H. Kajiyama, H. Kano et al., Plasma with high electron density and plasma-activated medium for cancer treatment. Clin. Plasma Med. 3, 72–76 (2015a)

    Article  Google Scholar 

  148. H. Tanaka, M. Mizuno, K. Ishikawa, K. Nakamura, H. Kajiyama, H. Kano, F. Kikkawa, M. Hori, Plasma-activated medium selectively kills glioblastoma brain tumor cells by down-regulating a survival signaling molecule, AKT kinase. Plasma Med. 1, 265–277 (2013)

    Article  Google Scholar 

  149. H. Tanaka, M. Mizuno, K. Ishikawa, K. Nakamura, F. Utsumi, H. Kajiyama, H. Kano, S. Maruyama, F. Kikkawa, M. Hori, Cell survival and proliferation signaling pathways are downregulated by plasma-activated medium in glioblastoma brain tumor cells. Plasma Med. 2, 207–220 (2014a)

    Article  Google Scholar 

  150. H. Tanaka, M. Mizuno, K. Ishikawa, K. Takeda, K. Nakamura, F. Utsumi, H. Kajiyama, H. Kano, Y. Okazaki, S. Toyokuni et al., Plasma medical science for cancer therapy: toward cancer therapy using nonthermal atmospheric pressure plasma. IEEE Trans. Plasma Sci. 42, 3760–3764 (2014b)

    ADS  Article  Google Scholar 

  151. H. Tanaka, M. Mizuno, F. Kikkawa, M. Hori, Interactions between a plasma-activated medium and cancer cells. Plasma Med. 6, 101–106 (2016a)

    Article  Google Scholar 

  152. H. Tanaka, M. Mizuno, S. Toyokuni, S. Maruyama, Y. Kodera, H. Terasaki, T. Adachi, M. Kato, F. Kikkawa, M. Hori, Cancer therapy using non-thermal atmospheric pressure plasma with ultra-high electron density. Phys. Plasmas 22, 122003 (2015b)

    ADS  Article  Google Scholar 

  153. H. Tanaka, K. Nakamura, M. Mizuno, K. Ishikawa, K. Takeda, H. Kajiyama, F. Utsumi, F. Kikkawa, M. Hori, Non-thermal atmospheric pressure plasma activates lactate in Ringer’s solution for anti-tumor effects. Sci. Rep. 6, 36282 (2016b)

    ADS  Article  Google Scholar 

  154. H. Tanaka, E. Takasu, T. Aigaki, K. Kato, S. Hayashi, A. Nose, Formin3 is required for assembly of the F-actin structure that mediates tracheal fusion in Drosophila. Dev. Biol. 274, 413–425 (2004)

    Article  Google Scholar 

  155. H. Tanaka, M. Mizuno, K. Ishikawa, K. Takeda, H. Hashizume, K. Nakamura, F. Utsumi, H. Kajiyama, H. Kano, Y. Okazaki, S. Toyokuni, S. Maruyama, T. Adachi, H. Kaneko, H. Terasaki, F. Kikkawa, M. Hori, Dynamic behaviour of glioblastoma cells in plasma-activated medium. in Proceedings of the 22nd International Symposium on Plasma Chemistry O7-1 (2015)

  156. K. Torii, S. Yamada, K. Nakamura, H. Tanaka, H. Kajiyama, K. Tanahashi, N. Iwata, M. Kanda, D. Kobayashi, C. Tanaka et al., Effectiveness of plasma treatment on gastric cancer cells. Gastric Cancer 18, 635–643 (2014)

    Article  Google Scholar 

  157. H. Towbin, T. Staehelin, J. Gordon, Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets—procedure and some applications. Proc. Natl. Acad. Sci. USA. 76, 4350–4354 (1979)

    ADS  Article  Google Scholar 

  158. S. Toyokuni, The origin and future of oxidative stress pathology: from the recognition of carcinogenesis as an iron addiction with ferroptosis-resistance to non-thermal plasma therapy. Pathol. Int. 66, 245–259 (2016)

    Article  Google Scholar 

  159. S. Trispel, Costs of low temperature plasma sterilization. J. Hosp. Infect. 42, 247–248 (1999)

    Article  Google Scholar 

  160. M. Ueda, D. Yamagami, K. Watanabe, A. Mori, H. Kimura, K. Sano, H. Saji, K. Ishikawa, M. Hori, H. Sakakita et al., Histological and nuclear medical comparison of inflammation after hemostasis with non-thermal plasma and thermal coagulation. Plasma Process. Polym. 12, 1338–1342 (2015)

    Article  Google Scholar 

  161. F. Utsumi, H. Kajiyama, K. Nakamura, H. Tanaka, M. Hori, F. Kikkawa, Selective cytotoxicity of indirect nonequilibrium atmospheric pressure plasma against ovarian clear-cell carcinoma. SpringerPlus 3, 398 (2014)

    Article  Google Scholar 

  162. F. Utsumi, H. Kajiyama, K. Nakamura, H. Tanaka, M. Mizuno, K. Ishikawa, H. Kondo, H. Kano, M. Hori, F. Kikkawa, Effect of indirect nonequilibrium atmospheric pressure plasma on anti-proliferative activity against chronic chemo-resistant ovarian cancer cells in vitro and in vivo. PLoS One 8, e81576 (2013)

    ADS  Article  Google Scholar 

  163. F. Utsumi, H. Kajiyama, K. Nakamura, H. Tanaka, M. Mizuno, S. Toyokuni, M. Hori, F. Kikkawa, Variable susceptibility of ovarian cancer cells to non-thermal plasma-activated medium. Oncol. Rep. 35, 3169–3177 (2016)

    Article  Google Scholar 

  164. J.J.A.M. van der Mullen, M.J. van de Sande, N. de Vries, B. Broks, E. Iordanova, A. Gamero, J. Torres, A. Sola, Single-shot Thomson scattering on argon plasmas created by the Microwave Plasma Torch; evidence for a new plasma class. Spectrochim. Acta B 62, 1135–1146 (2007)

    ADS  Article  Google Scholar 

  165. A.F.H. van Gessel, E.A.D. Carbone, P.J. Bruggeman, J.J.A.M. van der Mullen, Laser scattering on an atmospheric pressure plasma jet: disentangling Rayleigh, Raman and Thomson scattering. Plasma Sources Sci. Technol. 21, 015003 (2012)

    ADS  Article  Google Scholar 

  166. B. van Gessel, R. Brandenburg, P. Bruggeman, Electron properties and air mixing in radio frequency driven argon plasma jets at atmospheric pressure. Appl. Phys. Lett. 103, 064103 (2013)

    ADS  Article  Google Scholar 

  167. M. Vandamme, E. Robert, S. Pesnel, E. Barbosa, S. Dozias, J. Sobilo, S. Lerondel, A. Le Pape, J.M. Pouvesle, Antitumor effect of plasma treatment on U87 glioma xenografts: preliminary results. Plasma Process. Polym. 7, 264–273 (2010)

    Article  Google Scholar 

  168. D.T. Vistica, P. Skehan, D. Scudiero, A. Monks, A. Pittman, M.R. Boyd, Tetrazolium-based assays for cellular viability: a critical examination of selected parameters affecting formazan production. Can. Res. 51, 2515–2520 (1991)

    Google Scholar 

  169. T. von Woedtke, S. Reuter, K. Masur, K.D. Weltmann, Plasmas for medicine. Phys. Rep. 530, 291–320 (2013)

    ADS  Article  Google Scholar 

  170. K.D. Weltmann, E. Kindel, R. Brandenburg, C. Meyer, R. Bussiahn, C. Wilke, T. von Woedtke, Atmospheric pressure plasma jet for medical therapy: plasma parameters and risk estimation. Contrib. Plasma Phys. 49, 631–640 (2009)

    ADS  Article  Google Scholar 

  171. K.D. Weltmann, E. Kindel, T. von Woedtke, M. Hahnel, M. Stieber, R. Brandenburg, Atmospheric-pressure plasma sources: prospective tools for plasma medicine. Pure Appl. Chem. 82, 1223–1237 (2010)

    Article  Google Scholar 

  172. K.D. Weltmann, T. von Woedtke, Plasma medicine-current state of research and medical application. Plasma Phys. Control. Fusion 59, 014031 (2017)

    ADS  Article  Google Scholar 

  173. M.L. Wong, J.F. Medrano, Real-time PCR for mRNA quantitation. Biotechniques 39, 75–85 (2005)

    Article  Google Scholar 

  174. Y.I. Wu, D. Frey, O.I. Lungu, A. Jaehrig, I. Schlichting, B. Kuhlman, K.M. Hahn, A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104–108 (2009)

    ADS  Article  Google Scholar 

  175. A.J. Wu, X.D. Li, L. Chen, C.M. Du, J.H. Yan, Investigation of the physical properties in rotating gliding arc discharge with rapeseed oil. IEEE Trans. Plasma Sci. 43, 3219–3223 (2015)

    ADS  Article  Google Scholar 

  176. E. Wulf, A. Deboben, F.A. Bautz, H. Faulstich, T. Wieland, Fluorescent phallotoxin, a tool for the visualization of cellular actin. Proc. Natl. Acad. Sci. USA. 76, 4498–4502 (1979)

    ADS  Article  Google Scholar 

  177. D. Yan, A. Talbot, N. Nourmohammadi, X. Cheng, J. Canady, J. Sherman, M. Keidar, Principles of using cold atmospheric plasma stimulated media for cancer treatment. Sci. Rep. UK 5, 18339 (2015)

    ADS  Article  Google Scholar 

  178. D.Y. Yan, N. Nourmohammadi, K. Bian, F. Murad, J.H. Sherman, M. Keidar, Stabilizing the cold plasma-stimulated medium by regulating medium’s composition. Sci. Rep. UK 6, 26016 (2016)

    ADS  Article  Google Scholar 

  179. D.Y. Yan, J.H. Sherman, X.Q. Cheng, E. Ratovitski, J. Canady, M. Keidar, Controlling plasma stimulated media in cancer treatment application. Appl. Phys. Lett. 105, 224101 (2014)

    ADS  Article  Google Scholar 

  180. F. Ye, H. Kaneko, Y. Nagasaka, R. Ijima, K. Nakamura, M. Nagaya, K. Takayama, H. Kajiyama, T. Senga, H. Tanaka et al., Plasma-activated medium suppresses choroidal neovascularization in mice: a new therapeutic concept for age-related macular degeneration. Sci. Rep. 5, 7705 (2015)

    Article  Google Scholar 

  181. M. Yokoyama, K. Johkura, T. Sato, Gene expression responses of HeLa cells to chemical species generated by an atmospheric plasma flow. Biochem. Biophys. Res. Commun. 450, 1266–1271 (2014)

    Article  Google Scholar 

  182. T.L. Yuan, L.C. Cantley, PI3K pathway alterations in cancer: variations on a theme. Oncogene 27, 5497–5510 (2008)

    Article  Google Scholar 

  183. W. Zhang, E.K. Flemington, K. Zhang, Mutant TP53 disrupts age-related accumulation patterns of somatic mutations in multiple cancer types. Cancer Genet. 209, 376–380 (2016)

    Article  Google Scholar 

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Acknowledgements

This work was partly supported by Grants-in-Aid for Scientific Research on Innovative Areas “Plasma Medical Innovation” (Grant Nos. 24108002 and 24108008), a Grant-in-Aid for Young Scientists (A) (Grant No. 15H05430), and a Grant-in-Aid for Challenging Exploratory Research Grant (No. 15K13390) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Tanaka, H., Ishikawa, K., Mizuno, M. et al. State of the art in medical applications using non-thermal atmospheric pressure plasma. Rev. Mod. Plasma Phys. 1, 3 (2017). https://doi.org/10.1007/s41614-017-0004-3

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Keywords

  • Plasma medical science
  • Plasma cancer therapy
  • Plasma-activated medium (PAM)
  • Reactive oxygen species (ROS)