Cold atmospheric plasma treatment inhibits growth in colorectal cancer cells

References

Abbas, T. and Dutta, A. (2009). p21 in cancer: intricate networks and multiple activities. Nat. Rev. Cancer 9, 400–414.10.1038/nrc2657Search in Google Scholar PubMed PubMed Central

Al-Ahwal, M., Gomaa, W., Emam, E., Qari, Y., Buhmeida, A., Radwi, S., Al-Maghrabi, B., Al-Qahtani, M., and Al-Maghrabi, J. (2016). p16 protein is upregulated in a stepwise fashion in colorectal adenoma and colorectal carcinoma. Saudi J. Gastroenterol. 22, 435–440.10.4103/1319-3767.195560Search in Google Scholar PubMed PubMed Central

Arndt, S. and Bosserhoff, A.K. (2006). TANGO is a tumor suppressor of malignant melanoma. Int. J. Cancer 119, 2812–2820.10.1002/ijc.22242Search in Google Scholar PubMed

Arndt, S., Maegdefrau, U., Dorn, C., Schardt, K., Hellerbrand, C., and Bosserhoff, A.K. (2010). Iron-induced expression of bone morphogenic protein 6 in intestinal cells is the main regulator of hepatic hepcidin expression in vivo. Gastroenterology 138, 372–382.10.1053/j.gastro.2009.09.048Search in Google Scholar PubMed

Arndt, S., Wacker, E., Li, Y.F., Shimizu, T., Thomas, H.M., Morfill, G.E., Karrer, S., Zimmermann, J.L., and Bosserhoff, A.K. (2013). Cold atmospheric plasma, a new strategy to induce senescence in melanoma cells. Exp. Dermatol. 22, 284–289.10.1111/exd.12127Search in Google Scholar PubMed

Arndt, S., Landthaler, M., Zimmermann, J.L., Unger, P., Wacker, E., Shimizu, T., Li, Y.F., Morfill, G.E., Bosserhoff, A.K., and Karrer, S. (2015). Effects of cold atmospheric plasma (CAP) on ss-defensins, inflammatory cytokines, and apoptosis-related molecules in keratinocytes in vitro and in vivo. PLoS One 10, e0120041.10.1371/journal.pone.0120041Search in Google Scholar PubMed PubMed Central

Barnouin, K., Dubuisson, M.L., Child, E.S., Fernandez de Mattos, S., Glassford, J., Medema, R.H., Mann, D.J., and Lam, E.W. (2002). H2O2 induces a transient multi-phase cell cycle arrest in mouse fibroblasts through modulating cyclin D and p21Cip1 expression. J. Biol. Chem. 277, 13761–13770.10.1074/jbc.M111123200Search in Google Scholar PubMed

Bekeschus, S., Rodder, K., Fregin, B., Otto, O., Lippert, M., Weltmann, K.D., Wende, K., Schmidt, A., and Gandhirajan, R.K. (2017a). Toxicity and immunogenicity in murine melanoma following exposure to physical plasma-derived oxidants. Oxid. Med. Cell Longev. 2017, 4396467.10.1155/2017/4396467Search in Google Scholar PubMed PubMed Central

Bekeschus, S., Wende, K., Hefny, M.M., Rodder, K., Jablonowski, H., Schmidt, A., Woedtke, T.V., Weltmann, K.D., and Benedikt, J. (2017b). Oxygen atoms are critical in rendering THP-1 leukaemia cells susceptible to cold physical plasma-induced apoptosis. Sci. Rep. 7, 2791.10.1038/s41598-017-03131-ySearch in Google Scholar PubMed PubMed Central

Binenbaum, Y., Ben-David, G., Gil, Z., Slutsker, Y.Z., Ryzhkov, M.A., Felsteiner, J., Krasik, Y.E., and Cohen, J.T. (2017). Cold atmospheric plasma, created at the tip of an elongated flexible capillary using low electric current, can slow the progression of melanoma. PLoS One 12, e0169457.10.1371/journal.pone.0169457Search in Google Scholar PubMed PubMed Central

Bossi, G., Lapi, E., Strano, S., Rinaldo, C., Blandino, G., and Sacchi, A. (2006). Mutant p53 gain of function: reduction of tumor malignancy of human cancer cell lines through abrogation of mutant p53 expression. Oncogene 25, 304–309.10.1038/sj.onc.1209026Search in Google Scholar

Boxhammer, V., Li, Y.F., Koritzer, J., Shimizu, T., Maisch, T., Thomas, H.M., Schlegel, J., Morfill, G.E., and Zimmermann, J.L. (2013). Investigation of the mutagenic potential of cold atmospheric plasma at bactericidal dosages. Mutat. Res. 753, 23–28.10.1016/j.mrgentox.2012.12.015Search in Google Scholar

Brehmer, F., Haenssle, H.A., Daeschlein, G., Ahmed, R., Pfeiffer, S., Gorlitz, A., Simon, D., Schon, M.P., Wandke, D., and Emmert, S. (2015). Alleviation of chronic venous leg ulcers with a hand-held dielectric barrier discharge plasma generator (PlasmaDerm((R)) VU-2010): results of a monocentric, two-armed, open, prospective, randomized and controlled trial (NCT01415622). J. Eur. Acad. Dermatol. Venereol. 29, 148–155.10.1111/jdv.12490Search in Google Scholar

Brugarolas, J., Chandrasekaran, C., Gordon, J.I., Beach, D., Jacks, T., and Hannon, G.J. (1995). Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377, 552–557.10.1038/377552a0Search in Google Scholar

Brulle, L., Vandamme, M., Ries, D., Martel, E., Robert, E., Lerondel, S., Trichet, V., Richard, S., Pouvesle, J.M., and Le Pape, A. (2012). Effects of a non thermal plasma treatment alone or in combination with gemcitabine in a MIA PaCa2-luc orthotopic pancreatic carcinoma model. PLoS One 7, e52653.10.1371/journal.pone.0052653Search in Google Scholar

Chen, Z., Lin, L., Cheng, X., Gjika, E., and Keidar, M. (2016). Treatment of gastric cancer cells with nonthermal atmospheric plasma generated in water. Biointerphases 11, 031010.10.1116/1.4962130Search in Google Scholar

Chen, Z., Simonyan, H., Cheng, X., Gjika, E., Lin, L., Canady, J., Sherman, J.H., Young, C., and Keidar, M. (2017). A novel micro cold atmospheric plasma device for glioblastoma both in vitro and in vivo. Cancers (Basel) 9. doi: 10.3390/cancers9060061.10.3390/cancers9060061Search in Google Scholar

Cheng, X., Sherman, J., Murphy, W., Ratovitski, E., Canady, J., and Keidar, M. (2014). The effect of tuning cold plasma composition on glioblastoma cell viability. PLoS One 9, e98652.10.1371/journal.pone.0098652Search in Google Scholar

Chernets, N., Kurpad, D., Alexeev, V., Rodrigues, D., and Freeman, T. (2015). Reaction chemistry generated by nanosecond pulsed dielectric barrier discharge treatment is responsible for the tumor eradication in the B16 melanoma mouse model. Plasma Process. Polym. 12, 1400–1409.10.1002/ppap.201500140Search in Google Scholar

Deng, C., Zhang, P., Harper, J.W., Elledge, S.J., and Leder, P. (1995). Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82, 675–684.10.1016/0092-8674(95)90039-XSearch in Google Scholar

Dy, G.K., Hobday, T.J., Nelson, G., Windschitl, H.E., O’Connell, M.J., Alberts, S.R., Goldberg, R.M., Nikcevic, D.A., and Sargent, D.J. (2009). Long-term survivors of metastatic colorectal cancer treated with systemic chemotherapy alone: a north central cancer treatment group review of 3811 patients, n0144. Clin. Colorectal. Cancer 8, 88–93.10.3816/CCC.2009.n.014Search in Google Scholar PubMed

Gay-Mimbrera, J., Garcia, M.C., Isla-Tejera, B., Rodero-Serrano, A., Garcia-Nieto, A.V., and Ruano, J. (2016). Clinical and biological principles of cold atmospheric plasma application in skin cancer. Adv. Ther. 33, 894–909.10.1007/s12325-016-0338-1Search in Google Scholar PubMed PubMed Central

Guerrero-Preston, R., Ogawa, T., Uemura, M., Shumulinsky, G., Valle, B.L., Pirini, F., Ravi, R., Sidransky, D., Keidar, M., and Trink, B. (2014). Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells. Int. J. Mol. Med. 34, 941–946.10.3892/ijmm.2014.1849Search in Google Scholar PubMed PubMed Central

Guo, G.E., Ma, L.W., Jiang, B., Yi, J., Tong, T.J., and Wang, W.G. (2010). Hydrogen peroxide induces p16(INK4a) through an AUF1-dependent manner. J. Cell Biochem. 109, 1000–1005.10.1002/jcb.22474Search in Google Scholar

Haggar, F.A. and Boushey, R.P. (2009). Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clinics Colon. Rectal. Surg. 22, 191–197.10.1055/s-0029-1242458Search in Google Scholar PubMed PubMed Central

Heinlin, J., Zimmermann, J.L., Zeman, F., Bunk, W., Isbary, G., Landthaler, M., Maisch, T., Monetti, R., Morfill, G., Shimizu, T., et al. (2013). Randomized placebo-controlled human pilot study of cold atmospheric argon plasma on skin graft donor sites. Wound Repair. Regen. 21, 800–807.10.1111/wrr.12078Search in Google Scholar PubMed

Hirst, A.M., Frame, F.M., Maitland, N.J., and O’Connell, D. (2014). Low temperature plasma: a novel focal therapy for localized prostate cancer? Biomed. Res. Int. 2014, 878319.10.1155/2014/878319Search in Google Scholar PubMed PubMed Central

Hirst, A.M., Simms, M.S., Mann, V.M., Maitland, N.J., O’Connell, D., and Frame, F.M. (2015). Low-temperature plasma treatment induces DNA damage leading to necrotic cell death in primary prostate epithelial cells. Br. J. Cancer 112, 1536–1545.10.1038/bjc.2015.113Search in Google Scholar PubMed PubMed Central

Hou, J., Ma, J., Yu, K.N., Li, W., Cheng, C., Bao, L., and Han, W. (2015). Non-thermal plasma treatment altered gene expression profiling in non-small-cell lung cancer A549 cells. BMC Genomics 16, 435.10.1186/s12864-015-1644-8Search in Google Scholar PubMed PubMed Central

Irani, S., Shahmirani, Z., Atyabi, S.M., and Mirpoor, S. (2015). Induction of growth arrest in colorectal cancer cells by cold plasma and gold nanoparticles. Arch. Med. Sci. 11, 1286–1295.10.5114/aoms.2015.48221Search in Google Scholar PubMed PubMed Central

Isbary, G., Morfill, G., Schmidt, H.U., Georgi, M., Ramrath, K., Heinlin, J., Karrer, S., Landthaler, M., Shimizu, T., Steffes, B., et al. (2010). A first prospective randomized controlled trial to decrease bacterial load using cold atmospheric argon plasma on chronic wounds in patients. Br. J. Dermatol. 163, 78–82.10.1111/j.1365-2133.2010.09744.xSearch in Google Scholar PubMed

Ishaq, M., Kumar, S., Varinli, H., Han, Z.J., Rider, A.E., Evans, M.D., Murphy, A.B., and Ostrikov, K. (2014). Atmospheric gas plasma-induced ROS production activates TNF-ASK1 pathway for the induction of melanoma cancer cell apoptosis. Mol. Biol. Cell 25, 1523–1531.10.1091/mbc.e13-10-0590Search in Google Scholar PubMed PubMed Central

Joh, H.M., Choi, J.Y., Kim, S.J., Chung, T.H., and Kang, T.H. (2014). Effect of additive oxygen gas on cellular response of lung cancer cells induced by atmospheric pressure helium plasma jet. Sci. Rep. 4, 6638.10.1038/srep06638Search in Google Scholar PubMed PubMed Central

Kastan, M.B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R.W. (1991). Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51, 6304–6311.10.1158/0008-5472.CAN-16-1560Search in Google Scholar PubMed

Keidar, M., Walk, R., Shashurin, A., Srinivasan, P., Sandler, A., Dasgupta, S., Ravi, R., Guerrero-Preston, R., and Trink, B. (2011). Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br. J. Cancer 105, 1295–1301.10.1038/bjc.2011.386Search in Google Scholar PubMed PubMed Central

Kim, C.H., Bahn, J.H., Lee, S.H., Kim, G.Y., Jun, S.I., Lee, K., and Baek, S.J. (2010a). Induction of cell growth arrest by atmospheric non-thermal plasma in colorectal cancer cells. J. Biotechnol. 150, 530–538.10.1016/j.jbiotec.2010.10.003Search in Google Scholar PubMed

Kim, C.H., Kwon, S., Bahn, J.H., Lee, K., Jun, S.I., Rack, P.D., and Baek, S.J. (2010b). Effects of atmospheric nonthermal plasma on invasion of colorectal cancer cells. Appl. Phys. Lett. 96, 243701.10.1063/1.3449575Search in Google Scholar PubMed PubMed Central

Kim, J.Y., Ballato, J., Foy, P., Hawkins, T., Wei, Y., Li, J., and Kim, S.O. (2011). Apoptosis of lung carcinoma cells induced by a flexible optical fiber-based cold microplasma. Biosens. Bioelectron. 28, 333–338.10.1016/j.bios.2011.07.039Search in Google Scholar PubMed

Klimczak, A., Kempinska-Miroslawska, B., Mik, M., Dziki, L., and Dziki, A. (2011). Incidence of colorectal cancer in Poland in 1999–2008. Arch. Med. Sci. 7, 673–678.10.5114/aoms.2011.24138Search in Google Scholar PubMed PubMed Central

Kluge, S., Bekeschus, S., Bender, C., Benkhai, H., Sckell, A., Below, H., Stope, M.B., and Kramer, A. (2016). Investigating the mutagenicity of a cold argon-plasma jet in an HET-MN model. PLoS One 11, e0160667.10.1371/journal.pone.0160667Search in Google Scholar PubMed PubMed Central

Koensgen, D., Besic, I., Gumbel, D., Kaul, A., Weiss, M., Diesing, K., Kramer, A., Bekeschus, S., Mustea, A., and Stope, M.B. (2017). Cold atmospheric plasma (CAP) and CAP-stimulated cell culture media suppress ovarian cancer cell growth – a putative treatment option in ovarian cancer therapy. Anticancer Res. 37, 6739–6744.10.21873/anticanres.12133Search in Google Scholar

Koritzer, J., Boxhammer, V., Schafer, A., Shimizu, T., Klampfl, T.G., Li, Y.F., Welz, C., Schwenk-Zieger, S., Morfill, G.E., Zimmermann, J.L., et al. (2013). Restoration of sensitivity in chemo-resistant glioma cells by cold atmospheric plasma. PLoS One 8, e64498.10.1371/journal.pone.0064498Search in Google Scholar PubMed PubMed Central

Lee, S., Lee, H., Bae, H., Choi, E.H., and Kim, S.J. (2016). Epigenetic silencing of miR-19a-3p by cold atmospheric plasma contributes to proliferation inhibition of the MCF-7 breast cancer cell. Sci. Rep. 6, 30005.10.1038/srep30005Search in Google Scholar PubMed PubMed Central

Lee, S., Lee, H., Jeong, D., Ham, J., Park, S., Choi, E.H., and Kim, S.J. (2017). Cold atmospheric plasma restores tamoxifen sensitivity in resistant MCF-7 breast cancer cell. Free Radic. Biol. Med. 110, 280–290.10.1016/j.freeradbiomed.2017.06.017Search in Google Scholar PubMed

Li, X.L., Zhou, J., Chen, Z.R., and Chng, W.J. (2015). P53 mutations in colorectal cancer – molecular pathogenesis and pharmacological reactivation. World J. Gastroenterol. 21, 84–93.10.3748/wjg.v21.i1.84Search in Google Scholar PubMed PubMed Central

Liang, S.H. and Clarke, M.F. (1999a). The nuclear import of p53 is determined by the presence of a basic domain and its relative position to the nuclear localization signal. Oncogene 18, 2163–2166.10.1038/sj.onc.1202350Search in Google Scholar PubMed

Liang, S.H. and Clarke, M.F. (1999b). A bipartite nuclear localization signal is required for p53 nuclear import regulated by a carboxyl-terminal domain. J. Biol. Chem. 274, 32699–32703.10.1074/jbc.274.46.32699Search in Google Scholar PubMed

Lupu, A.R., Georgescu, N., Calugaru, A., Cremer, L., Szegli, G., and Kerek, F. (2009). The effects of cold atmospheric plasma jets on B16 and COLO320 tumoral cells. Roum Arch. Microbiol. Immunol. 68, 136–144.Search in Google Scholar

Ma, Y., Ha, C.S., Hwang, S.W., Lee, H.J., Kim, G.C., Lee, K.W., and Song, K. (2014). Non-thermal atmospheric pressure plasma preferentially induces apoptosis in p53-mutated cancer cells by activating ROS stress-response pathways. PLoS One 9, e91947.10.1371/journal.pone.0091947Search in Google Scholar PubMed PubMed Central

Macleod, K.F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B., and Jacks, T. (1995). p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 9, 935–944.10.1101/gad.9.8.935Search in Google Scholar PubMed

Maisch, T., Bosserhoff, A.K., Unger, P., Heider, J., Shimizu, T., Zimmermann, J.L., Morfill, G.E., Landthaler, M., and Karrer, S. (2017). Investigation of toxicity and mutagenicity of cold atmospheric argon plasma. Environ. Mol. Mutagen 58, 172–177.10.1002/em.22086Search in Google Scholar PubMed

Metelmann, H.-R., Nedrelow, D.S., Seebauer, C., Schuster, M., von Woedtke, T., Weltmann, K.-D., Kindler, S., Metelmann, P.H., Finkelstein, S.E., Von Hoff, D.D., et al. (2015). Head and neck cancer treatment and physical plasma. Clin. Plasma Med. 3, 17–23.10.1016/j.cpme.2015.02.001Search in Google Scholar

Metelmann, H.-R., Seebauer, C., Miller, V., Fridman, A., Bauer, G., Graves, D.B., Pouvesle, J.-M., Rutkowski, R., Schuster, M., Bekeschus, S., et al. (2018). Clinical experience with cold plasma in the treatment of locally advanced head and neck cancer. Clin. Plasma Med. 9, 6–13.10.1016/j.cpme.2017.09.001Search in Google Scholar

Mirpour, S., Piroozmand, S., Soleimani, N., Jalali Faharani, N., Ghomi, H., Fotovat Eskandari, H., Sharifi, A.M., Eftekhari, M., and Nikkhah, M. (2016). Utilizing the micron sized non-thermal atmospheric pressure plasma inside the animal body for the tumor treatment application. Sci. Rep. 6, 29048.10.1038/srep29048Search in Google Scholar PubMed PubMed Central

Nofel, M., Chauvin, J., Vicendo, P., and Judee, F. (2017). Effects of Plasma Activated Medium on Head and Neck FaDu Cancerous Cells: comparison of 3D and 2D response. Anticancer Agents Med. Chem. pii: ACAMC-EPUB-85101. Doi: 10.2174/1871520617666170801111055.10.2174/1871520617666170801111055Search in Google Scholar PubMed

O’Keefe, K., Li, H., and Zhang, Y. (2003). Nucleocytoplasmic shuttling of p53 is essential for MDM2-mediated cytoplasmic degradation but not ubiquitination. Mol. Cell Biol. 23, 6396–6405.10.1128/MCB.23.18.6396-6405.2003Search in Google Scholar PubMed PubMed Central

Parrales, A. and Iwakuma, T. (2015). Targeting oncogenic mutant p53 for cancer therapy. Front Oncol. 5, 288.10.3389/fonc.2015.00288Search in Google Scholar PubMed PubMed Central

Partecke, L.I., Evert, K., Haugk, J., Doering, F., Normann, L., Diedrich, S., Weiss, F.U., Evert, M., Huebner, N.O., Guenther, C., et al. (2012). Tissue tolerable plasma (TTP) induces apoptosis in pancreatic cancer cells in vitro and in vivo. BMC Cancer 12, 473.10.1186/1471-2407-12-473Search in Google Scholar PubMed PubMed Central

Rochette, P.J., Bastien, N., Lavoie, J., Guerin, S.L., and Drouin, R. (2005). SW480, a p53 double-mutant cell line retains proficiency for some p53 functions. J. Mol. Biol. 352, 44–57.10.1016/j.jmb.2005.06.033Search in Google Scholar PubMed

Ruwan Kumara, M.H., Piao, M.J., Kang, K.A., Ryu, Y.S., Park, J.E., Shilnikova, K., Jo, J.O., Mok, Y.S., Shin, J.H., Park, Y., et al. (2016). Non-thermal gas plasma-induced endoplasmic reticulum stress mediates apoptosis in human colon cancer cells. Oncol. Rep. 36, 2268–2274.10.3892/or.2016.5038Search in Google Scholar PubMed

Schuster, M., Seebauer, C., Rutkowski, R., Hauschild, A., Podmelle, F., Metelmann, C., Metelmann, B., von Woedtke, T., Hasse, S., Weltmann, K.D., et al. (2016). Visible tumor surface response to physical plasma and apoptotic cell kill in head and neck cancer. J. Craniomaxillofac. Surg. 44, 1445–1452.10.1016/j.jcms.2016.07.001Search in Google Scholar PubMed

Shaulsky, G., Goldfinger, N., Peled, A., and Rotter, V. (1991a). Involvement of wild-type p53 protein in the cell cycle requires nuclear localization. Cell Growth Differ. 2, 661–667.Search in Google Scholar

Shaulsky, G., Goldfinger, N., Tosky, M.S., Levine, A.J., and Rotter, V. (1991b). Nuclear localization is essential for the activity of p53 protein. Oncogene 6, 2055–2065.Search in Google Scholar

Smolinska, K. and Paluszkiewicz, P. (2010). Risk of colorectal cancer in relation to frequency and total amount of red meat consumption. Systematic review and meta-analysis. Arch. Med. Sci. 6, 605–610.10.5114/aoms.2010.14475Search in Google Scholar PubMed PubMed Central

Takayama, T., Miyanishi, K., Hayashi, T., Sato, Y., and Niitsu, Y. (2006). Colorectal cancer: genetics of development and metastasis. J. Gastroenterol. 41, 185–192.10.1007/s00535-006-1801-6Search in Google Scholar PubMed

Takeda, S., Yamada, S., Hattori, N., Nakamura, K., Tanaka, H., Kajiyama, H., Kanda, M., Kobayashi, D., Tanaka, C., Fujii, T., et al. (2017). Intraperitoneal administration of plasma-activated medium: proposal of a novel treatment option for peritoneal metastasis from gastric cancer. Ann. Surg. Oncol. 24, 1188–1194.10.1245/s10434-016-5759-1Search in Google Scholar PubMed

Thiyagarajan, M., Gonzales, X.F., and Anderson, H. (2013). Regulated cellular exposure to non-thermal plasma allows preferentially directed apoptosis in acute monocytic leukemia cells. Stud. Health Technol. Inform. 184, 436–442.Search in Google Scholar

Thiyagarajan, M., Anderson, H., and Gonzales, X.F. (2014). Induction of apoptosis in human myeloid leukemia cells by remote exposure of resistive barrier cold plasma. Biotechnol. Bioeng. 111, 565–574.10.1109/PLASMA.2014.7012621Search in Google Scholar

Torii, K., Yamada, S., Nakamura, K., Tanaka, H., Kajiyama, H., Tanahashi, K., Iwata, N., Kanda, M., Kobayashi, D., Tanaka, C., et al. (2015). Effectiveness of plasma treatment on gastric cancer cells. Gastric Cancer 18, 635–643.10.1007/s10120-014-0395-6Search in Google Scholar PubMed

Tuhvatulin, A.I., Sysolyatina, E.V., Scheblyakov, D.V., Logunov, D.Y., Vasiliev, M.M., Yurova, M.A., Danilova, M.A., Petrov, O.F., Naroditsky, B.S., Morfill, G.E., et al. (2012). Non-thermal plasma causes p53-dependent apoptosis in human colon carcinoma cells. Acta Naturae 4, 82–87.10.32607/20758251-2012-4-3-82-87Search in Google Scholar

Turrini, E., Laurita, R., Stancampiano, A., Catanzaro, E., Calcabrini, C., Maffei, F., Gherardi, M., Colombo, V., and Fimognari, C. (2017). Cold atmospheric plasma induces apoptosis and oxidative stress pathway regulation in T-lymphoblastoid leukemia cells. Oxid. Med. Cell Longev. 2017, 4271065.10.1155/2017/4271065Search in Google Scholar PubMed PubMed Central

Utsumi, F., Kajiyama, H., Nakamura, K., Tanaka, H., Mizuno, M., Ishikawa, K., Kondo, H., Kano, H., Hori, M., and Kikkawa, F. (2013). 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, e81576.10.1371/journal.pone.0081576Search in Google Scholar PubMed PubMed Central

Utsumi, F., Kajiyama, H., Nakamura, K., Tanaka, H., Mizuno, M., Toyokuni, S., Hori, M., and Kikkawa, F. (2016). Variable susceptibility of ovarian cancer cells to non-thermal plasma-activated medium. Oncol. Rep. 35, 3169–3177.10.3892/or.2016.4726Search in Google Scholar PubMed PubMed Central

Vandamme, M., Robert, E., Dozias, S., Sobilo, J., Lerondel, S., Le Pape, A., and Pouvesle, J.-M. (2011). Response of human glioma U87 xenografted on mice to non thermal plasma treatment. Plasma Med. 31, 27–43.10.1615/PlasmaMed.v1.i1.30Search in Google Scholar

Vandamme, M., Robert, E., Lerondel, S., Sarron, V., Ries, D., Dozias, S., Sobilo, J., Gosset, D., Kieda, C., Legrain, B., et al. (2012). ROS implication in a new antitumor strategy based on non-thermal plasma. Int. J. Cancer 130, 2185–2194.10.1002/ijc.26252Search in Google Scholar PubMed

Volotskova, O., Hawley, T.S., Stepp, M.A., and Keidar, M. (2012). Targeting the cancer cell cycle by cold atmospheric plasma. Sci. Rep. 2, 636.10.1038/srep00636Search in Google Scholar PubMed PubMed Central

Walk, R.M., Snyder, J.A., Srinivasan, P., Kirsch, J., Diaz, S.O., Blanco, F.C., Shashurin, A., Keidar, M., and Sandler, A.D. (2013). Cold atmospheric plasma for the ablative treatment of neuroblastoma. J. Pediatr. Surg. 48, 67–73.10.1016/j.jpedsurg.2012.10.020Search in Google Scholar PubMed

Wang, M., Holmes, B., Cheng, X., Zhu, W., Keidar, M., and Zhang, L.G. (2013). Cold atmospheric plasma for selectively ablating metastatic breast cancer cells. PLoS One 8, e73741.10.1371/journal.pone.0073741Search in Google Scholar PubMed PubMed Central

Wang, M., Geilich, B.M., Keidar, M., and Webster, T.J. (2017). Killing malignant melanoma cells with protoporphyrin IX-loaded polymersome-mediated photodynamic therapy and cold atmospheric plasma. Int. J. Nanomed. 12, 4117–4127.10.2147/IJN.S129266Search in Google Scholar PubMed PubMed Central

Weiss, M., Gumbel, D., Hanschmann, E.M., Mandelkow, R., Gelbrich, N., Zimmermann, U., Walther, R., Ekkernkamp, A., Sckell, A., Kramer, A., et al. (2015a). Cold atmospheric plasma treatment induces anti-proliferative effects in prostate cancer cells by redox and apoptotic signaling pathways. PLoS One 10, e0130350.10.1371/journal.pone.0130350Search in Google Scholar PubMed PubMed Central

Weiss, M., Gumbel, D., Gelbrich, N., Brandenburg, L.O., Mandelkow, R., Zimmermann, U., Ziegler, P., Burchardt, M., and Stope, M.B. (2015b). Inhibition of cell growth of the prostate cancer cell model LNCaP by cold atmospheric plasma. In Vivo 29, 611–616.Search in Google Scholar

Welz, C., Emmert, S., Canis, M., Becker, S., Baumeister, P., Shimizu, T., Morfill, G.E., Harreus, U., and Zimmermann, J.L. (2015). Cold Atmospheric plasma: a promising complementary therapy for squamous head and neck cancer. PLoS One 10, e0141827.10.1371/journal.pone.0141827Search in Google Scholar PubMed PubMed Central

Wende, K., Reuter, S., von Woedtke, T., Weltmann, K., and Masur, K. (2014). Redox-based assay for assessment of biological impact of plasma treatment. Plasma Process. Polym. 11, 655–663.10.1002/ppap.201300172Search in Google Scholar

Wende, K., Bekeschus, S., Schmidt, A., Jatsch, L., Hasse, S., Weltmann, K., Masur, K., and von Woedtke, T. (2016). Risk assessment of a cold argon plasma jet in respect to its mutagenicity. Mutat. Res-Gen. Tox. En. 798, 48–54.10.1016/j.mrgentox.2016.02.003Search in Google Scholar PubMed

Yajima, I., Iida, M., Kumasaka, M.Y., Omata, Y., Ohgami, N., Chang, J., Ichihara, S., Hori, M., and Kato, M. (2014). Non-equilibrium atmospheric pressure plasmas modulate cell cycle-related gene expressions in melanocytic tumors of RET-transgenic mice. Exp. Dermatol. 23, 424–425.10.1111/exd.12415Search in Google Scholar PubMed

Yan, X., Zou, F., Zhao, S., Lu, X., He, G., Xiong, Z., Xiong, Q., Zhao, Q., Deng, P., Huang, J., et al. (2010). On the mechanism of plasma inducing cell apoptosis. IEEE Transact. Plasma Sci. 38, 2451–2457.10.1109/TPS.2010.2056393Search in Google Scholar