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Original Research

Gas plasma irradiation of breast cancers promotes immunogenicity, tumor reduction, and an abscopal effect in vivo

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Article: 1859731 | Received 24 Jun 2020, Accepted 01 Dec 2020, Published online: 29 Dec 2020

References

  • Li, N.; Deng, Y.; Zhou, L.; Tian, T.; Yang, S.; Wu, Y.; Zheng, Y.; Zhai, Z.; Hao, Q.; Song, D.; Zhang, D.; Kang, H.; Dai, Z. Global burden of breast cancer and attributable risk factors in 195 countries and territories, from 1990 to 2017: Results from the global burden of disease study 2017. J Hematol Oncol. 2019;12:140. doi:10.1186/s13045-019-0828-0..
  • Curado MP. Breast cancer in the world: incidence and mortality. Salud Publica Mex. 2011;53:372–14.
  • Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90. doi:10.3322/caac.20107.
  • Chakraborty S, Rahman T. The difficulties in cancer treatment. Ecancermedicalscience. 2012;6:ed16. doi:10.3332/ecancer.2012.ed16.
  • Guan X. Cancer metastases: challenges and opportunities. Acta Pharm Sin B. 2015;5(5):402–418. doi:10.1016/j.apsb.2015.07.005.
  • Coleman RE, Lipton A, Roodman GD, Guise TA, Boyce BF, Brufsky AM, Clezardin P, Croucher PI, Gralow JR, Hadji P, et al. Metastasis and bone loss: advancing treatment and prevention. Cancer Treat Rev. 2010;36:615–620. doi:10.1016/j.ctrv.2010.04.003.
  • Falzone L, Salomone S, Libra M. Evolution of cancer pharmacological treatments at the turn of the third millennium. Front Pharmacol. 2018;9:1300. doi:10.3389/fphar.2018.01300.
  • Mokhtari RB, Homayouni TS, Baluch N, Morgatskaya E, Kumar S, Das B, Yeger H. Combination therapy in combating cancer. Oncotarget. 2017;8(23):38022. doi:10.18632/oncotarget.16723.
  • Pucci C, Martinelli C, Ciofani G. Innovative approaches for cancer treatment: current perspectives and new challenges. Ecancermedicalscience. 2019;13:961. doi:10.3332/ecancer.2019.961.
  • Vanneman M, Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer. 2012;12:237–251. doi:10.1038/nrc3237.
  • Sudhakar A. History of cancer, ancient and modern treatment methods. J Cancer Sci Ther. 2009;1:1–4. doi:10.4172/1948-5956.100000e2.
  • Tokumaru Y, Joyce D, Takabe K. Current status and limitations of immunotherapy for breast cancer. Surgery. 2020;167(3):628–630. doi:10.1016/j.surg.2019.09.018.
  • Woodward WA. Building momentum for subsets of patients with advanced triple-negative breast cancer. Lancet Oncol. 2020;21(1):3–5. doi:10.1016/S1470-2045(19)30737-5.
  • Schmid P, Rugo HS, Adams S, Schneeweiss A, Barrios CH, Iwata H, Dieras V, Henschel V, Molinero L, Chui SY, et al. Atezolizumab plus nab-paclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (impassion130): updated efficacy results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2020;21(1):44–59. doi:10.1016/S1470-2045(19)30689-8.
  • Bhandaru M, Rotte A. Monoclonal antibodies for the treatment of melanoma: present and future strategies. Methods Mol Biol. 2019;1904:83–108. doi:10.1007/978-1-4939-8958-4_4.
  • Berner F, Bomze D, Diem S, Ali OH, Fassler M, Ring S, Niederer R, Ackermann CJ, Baumgaertner P, Pikor N, et al. Association of checkpoint inhibitor-induced toxic effects with shared cancer and tissue antigens in non-small cell lung cancer. JAMA Oncol. 2019;5:1043–1047. doi:10.1001/jamaoncol.2019.0402.
  • Samstein RM, Lee CH, Shoushtari AN, Hellmann MD, Shen R, Janjigian YY, Barron DA, Zehir A, Jordan EJ, Omuro A, et al. Tumor mutational load predicts survival after immunotherapy across multiple cancer types. Nat Genet. 2019;51:202–206. doi:10.1038/s41588-018-0312-8.
  • Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348(6230):69–74. doi:10.1126/science.aaa4971.
  • Ruckert M, Deloch L, Fietkau R, Frey B, Hecht M, Gaipl US. Immune modulatory effects of radiotherapy as basis for well-reasoned radioimmunotherapies. Strahlenther Onkol. 2018;194:509–519. doi:10.1007/s00066-018-1287-1.
  • Arina A, Gutiontov SI, Weichselbaum RR. Radiotherapy and immunotherapy for cancer: from “systemic” to “multisite. Clin Cancer Res. 2020. doi:10.1158/1078-0432.CCR-19-2034.
  • Zhang D, Zhou T, He F, Rong Y, Lee SH, Wu S, Zuo L. Reactive oxygen species formation and bystander effects in gradient irradiation on human breast cancer cells. Oncotarget. 2016;7:41622–41636. doi:10.18632/oncotarget.9517.
  • Pasqual-Melo G, Sagwal SK, Freund E, Gandhirajan RK, Frey B, von Woedtke T, Gaipl U, Bekeschus S. Combination of gas plasma and radiotherapy has immunostimulatory potential and additive toxicity in murine melanoma cells in vitro. Int J Mol Sci. 2020;21:1379. doi:10.3390/ijms21041379.
  • Perillo B, Di Donato M, Pezone A, Di Zazzo E, Giovannelli P, Galasso G, Castoria G, Migliaccio A. Ros in cancer therapy: the bright side of the moon. Exp Mol Med. 2020;52:192–203. doi:10.1038/s12276-020-0384-2.
  • Dai X, Bazaka K, Richard DJ, Thompson ERW, Ostrikov KK. The emerging role of gas plasma in oncotherapy. Trends Biotechnol. 2018;36:1183–1198. doi:10.1016/j.tibtech.2018.06.010.
  • Privat-Maldonado A, Schmidt A, Lin A, Weltmann KD, Wende K, Bogaerts A, Bekeschus S. Ros from physical plasmas: redox chemistry for biomedical therapy. Oxid Med Cell Longev. 2019;2019:9062098. doi:10.1155/2019/9062098.
  • Reuter S, von Woedtke T, Weltmann KD. The kinpen-a review on physics and chemistry of the atmospheric pressure plasma jet and its applications. J Phys D: Appl Phys. 2018:51. doi:10.1088/1361-6463/aab3ad.
  • Semmler ML, Bekeschus S, Schafer M, Bernhardt T, Fischer T, Witzke K, Seebauer C, Rebl H, Grambow E, Vollmar B, et al. Molecular mechanisms of the efficacy of cold atmospheric pressure plasma (cap) in cancer treatment. Cancers (Basel). 2020;12(2):269. doi:10.3390/cancers12020269.
  • Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13:54–61. doi:10.1038/nm1523.
  • Garg AD, Agostinis P. Cell death and immunity in cancer: from danger signals to mimicry of pathogen defense responses. Immunol Rev. 2017;280:126–148. doi:10.1111/imr.12574.
  • Hasse S, Meder T, Freund E, von Woedtke T, Bekeschus S. Plasma treatment limits human melanoma spheroid growth and metastasis independent of the ambient gas composition. Cancers (Basel). 2020;12(9):2570. doi:10.3390/cancers12092570.
  • Bekeschus S, Clemen R, Niessner F, Sagwal SK, Freund E, Schmidt A. Medical gas plasma jet technology targets murine melanoma in an immunogenic fashion. Adv Sci (Weinh). 2020;7:1903438. doi:10.1002/advs.201903438.
  • Fucikova J, Moserova I, Truxova I, Hermanova I, Vancurova I, Partlova S, Fialova A, Sojka L, Cartron PF, Houska M, et al. High hydrostatic pressure induces immunogenic cell death in human tumor cells. Int J Cancer. 2014;135:1165–1177. doi:10.1002/ijc.28766.
  • Fucikova J, Kralikova P, Fialova A, Brtnicky T, Rob L, Bartunkova J, Spisek R. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res. 2011;71(14):4821–4833. doi:10.1158/0008-5472.CAN-11-0950.
  • Cirone M, Di Renzo L, Lotti LV, Conte V, Trivedi P, Santarelli R, Gonnella R, Frati L, Faggioni A. Primary effusion lymphoma cell death induced by bortezomib and ag 490 activates dendritic cells through cd91. PLoS One. 2012;7:e31732. doi:10.1371/journal.pone.0031732.
  • Galluzzi L, Buque A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017;17:97–111. doi:10.1038/nri.2016.107.
  • Ledford H, Else H, Warren M. Cancer immunologists scoop medicine nobel prize. Nature. 2018;562(7725):20–21. doi:10.1038/d41586-018-06751-0.
  • Mole RH. Whole body irradiation; radiobiology or medicine? Br J Radiol. 1953;26:234–241. doi:10.1259/0007-1285-26-305-234.
  • Ehlers G, Fridman M. Abscopal effect of radiation in papillary adenocarcinoma. Br J Radiol. 1973;46:220–222. doi:10.1259/0007-1285-46-543-220.
  • Topalian SL, Taube JM, Pardoll DM. Neoadjuvant checkpoint blockade for cancer immunotherapy. Science. 2020:367. doi:10.1126/science.aax0182.
  • Frey B, Rubner Y, Wunderlich R, Weiss EM, Pockley AG, Fietkau R, Gaipl US. Induction of Abscopal Anti-tumor Immunity and Immunogenic Tumor Cell Death by Ionizing Irradiation - Implications for Cancer Therapies. Curr Med Chem. 1751-1764;2012(19). doi:10.2174/092986712800099811.
  • Schroter P, Hartmann L, Osen W, Baumann D, Offringa R, Eisel D, Debus J, Eichmuller SB, Rieken S. Radiation-induced alterations in immunogenicity of a murine pancreatic ductal adenocarcinoma cell line. Sci Rep. 2020;10:686. doi:10.1038/s41598-020-57456-2.
  • Park SS, Dong H, Liu X, Harrington SM, Krco CJ, Grams MP, Mansfield AS, Furutani KM, Olivier KR, Kwon ED. Pd-1 restrains radiotherapy-induced abscopal effect. Cancer Immunol Res. 2015;3(6):610–619. doi:10.1158/2326-6066.CIR-14-0138.
  • Shiraishi K, Ishiwata Y, Nakagawa K, Yokochi S, Taruki C, Akuta T, Ohtomo K, Matsushima K, Tamatani T, Kanegasaki S. Enhancement of antitumor radiation efficacy and consistent induction of the abscopal effect in mice by eci301, an active variant of macrophage inflammatory protein-1alpha. Clin Cancer Res. 2008;14(4):1159–1166. doi:10.1158/1078-0432.CCR-07-4485.
  • Yin L, Xue J, Li R, Zhou L, Deng L, Chen L, Zhang Y, Li Y, Zhang X, Xiu W, et al. Effect of low-dose radiotherapy on abscopal responses to hypofractionated radiotherapy and anti-pd1 in mice and nsclc patients. Int J Radiat Oncol Biol Phys. 2020. doi:10.1016/j.ijrobp.2020.05.002.
  • Hu ZI, McArthur HL, Ho AY. The abscopal effect of radiation therapy: what is it and how can we use it in breast cancer? Curr Breast Cancer Rep. 2017;9:45–51. doi:10.1007/s12609-017-0234-y.
  • Grass GD, Krishna N, Kim S. The immune mechanisms of abscopal effect in radiation therapy. Curr Probl Cancer. 2016;40:10–24. doi:10.1016/j.currproblcancer.2015.10.003.
  • Durgeau A, Virk Y, Corgnac S, Mami-Chouaib F. Recent advances in targeting cd8 t-cell immunity for more effective cancer immunotherapy. Front Immunol. 2018;9:14. doi:10.3389/fimmu.2018.00014.
  • Bekeschus S, Masur K, Kolata J, Wende K, Schmidt A, Bundscherer L, Barton A, Kramer A, Broker B, Weltmann KD. Human mononuclear cell survival and proliferation is modulated by cold atmospheric plasma jet. Plasma Process Polym. 2013;10:706–713. doi:10.1002/ppap.201300008.
  • Bekeschus S, von Woedtke T, Kramer A, Weltmann K-D, Masur K. Cold physical plasma treatment alters redox balance in human immune cells. Plasma Med. 2013;3:267–278. doi:10.1615/PlasmaMed.2014011972.
  • Bekeschus S, Kolata J, Winterbourn C, Kramer A, Turner R, Weltmann KD, Broker B, Masur K. Hydrogen peroxide: A central player in physical plasma-induced oxidative stress in human blood cells. Free Radic Res. 2014;48:542–549. doi:10.3109/10715762.2014.892937.
  • Bekeschus S, Rödder K, Schmidt A, Stope MB, von Woedtke T, Miller V, Fridman A, Weltmann K-D, Masur K, Metelmann H-R, et al. Cold physical plasma selects for specific t helper cell subsets with distinct cells surface markers in a caspase-dependent and nf-κb-independent manner. Plasma Process Polym. 2016;13:1144–1150. doi:10.1002/ppap.201600080.
  • Zanetti M. Tapping cd4 t cells for cancer immunotherapy: the choice of personalized genomics. J Immunol. 2015;194:2049–2056. doi:10.4049/jimmunol.1402669.
  • Badoual C, Hans S, Rodriguez J, Peyrard S, Klein C, Agueznay Nel H, Mosseri V, Laccourreye O, Bruneval P, Fridman WH, et al. Prognostic value of tumor-infiltrating cd4+ t-cell subpopulations in head and neck cancers. Clin Cancer Res. 2006;12:465–472. doi:10.1158/1078-0432.CCR-05-1886.
  • de Ruiter EJ, Ooft ML, Devriese LA, Willems SM. The prognostic role of tumor infiltrating t-lymphocytes in squamous cell carcinoma of the head and neck: A systematic review and meta-analysis. Oncoimmunology. 2017;6:e1356148. doi:10.1080/2162402X.2017.1356148.
  • Geng Y, Shao Y, He W, Hu W, Xu Y, Chen J, Wu C, Jiang J. Prognostic role of tumor-infiltrating lymphocytes in lung cancer: A meta-analysis. Cell Physiol Biochem. 2015;37(4):1560–1571. doi:10.1159/000438523.
  • Matsumoto H, Thike AA, Li H, Yeong J, Koo SL, Dent RA, Tan PH, Iqbal J. Increased cd4 and cd8-positive t cell infiltrate signifies good prognosis in a subset of triple-negative breast cancer. Breast Cancer Res Treat. 2016;156:237–247. doi:10.1007/s10549-016-3743-x.
  • Antony PA, Piccirillo CA, Akpinarli A, Finkelstein SE, Speiss PJ, Surman DR, Palmer DC, Chan CC, Klebanoff CA, Overwijk WW, et al. Cd8+ t cell immunity against a tumor/self-antigen is augmented by cd4+ t helper cells and hindered by naturally occurring t regulatory cells. J Immunol. 2005;174:2591–2601. doi:10.4049/jimmunol.174.5.2591.
  • Bos R, Sherman LA. Cd4+ t-cell help in the tumor milieu is required for recruitment and cytolytic function of cd8+ t lymphocytes. Cancer Res. 2010;70:8368–8377. doi:10.1158/0008-5472.CAN-10-1322.
  • Tay RE, Richardson EK, Toh HC. Revisiting the role of cd4(+) t cells in cancer immunotherapy-new insights into old paradigms. Cancer Gene Ther. 2020. doi:10.1038/s41417-020-0183-x.
  • Mucida D, Husain MM, Muroi S, van Wijk F, Shinnakasu R, Naoe Y, Reis BS, Huang Y, Lambolez F, Docherty M, et al. Transcriptional reprogramming of mature cd4(+) helper t cells generates distinct mhc class ii-restricted cytotoxic t lymphocytes. Nat Immunol. 2013;14:281–289. doi:10.1038/ni.2523.
  • Aarntzen EH, De Vries IJ, Lesterhuis WJ, Schuurhuis D, Jacobs JF, Bol K, Schreibelt G, Mus R, De Wilt JH, Haanen JB, et al. Targeting cd4(+) t-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res. 2013;73:19–29. doi:10.1158/0008-5472.CAN-12-1127.
  • Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and damps in cancer therapy. Nat Rev Cancer. 2012;12:860–875. doi:10.1038/nrc3380.
  • Garg AD, Dudek AM, Agostinis P. Cancer immunogenicity, danger signals, and damps: what, when, and how? BioFactors. 2013;39(4):355–367. doi:10.1002/biof.1125.
  • Schulz D, Stancev I, Sorrentino A, Menevse AN, Beckhove P, Brockhoff G, Hautmann MG, Reichert TE, Bauer RJ, Ettl T. Increased pd-l1 expression in radioresistant hnscc cell lines after irradiation affects cell proliferation due to inactivation of gsk-3beta. Oncotarget. 2019;10:573–583. doi:10.18632/oncotarget.26542.
  • Wu CT, Chen WC, Chang YH, Lin WY, Chen MF. The role of pd-l1 in the radiation response and clinical outcome for bladder cancer. Sci Rep. 2016;6:19740. doi:10.1038/srep19740.
  • Golden EB, Frances D, Pellicciotta I, Demaria S, Helen Barcellos-Hoff M, Formenti SC. Radiation fosters dose-dependent and chemotherapy-induced immunogenic cell death. Oncoimmunology. 2014;3(4):e28518. doi:10.4161/onci.28518.
  • Golden EB, Apetoh L. Radiotherapy and immunogenic cell death. Semin Radiat Oncol. 2015;25:11–17. doi:10.1016/j.semradonc.2014.07.005.
  • Panzarini E, Inguscio V, Dini L. Immunogenic cell death: can it be exploited in photodynamic therapy for cancer? Biomed Res Int. 2013, 2013:482160. doi:10.1155/2013/482160.
  • Tanaka M, Kataoka H, Yano S, Sawada T, Akashi H, Inoue M, Suzuki S, Inagaki Y, Hayashi N, Nishie H, et al. Immunogenic cell death due to a new photodynamic therapy (pdt) with glycoconjugated chlorin (g-chlorin). Oncotarget. 2016;7(30):47242–47251. doi:10.18632/oncotarget.9725.
  • Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer. 2003;3:380–387. doi:10.1038/nrc1071.
  • Sonveaux P. Ros and radiotherapy: more we care. Oncotarget. 2017;8(22):35482–35483. doi:10.18632/oncotarget.16613.
  • Chen HHW, Kuo MT. Improving radiotherapy in cancer treatment: promises and challenges. Oncotarget. 2017;8(37):62742–62758. doi:10.18632/oncotarget.18409.
  • Carta S, Castellani P, Delfino L, Tassi S, Vene R, Rubartelli A. Damps and inflammatory processes: the role of redox in the different outcomes. J Leukoc Biol. 2009;86:549–555. doi:10.1189/jlb.1008598.
  • Castellani P, Balza E, Rubartelli A. Inflammation, damps, tumor development, and progression: A vicious circle orchestrated by redox signaling. Antioxid Redox Signal. 2014;20:1086–1097. doi:10.1089/ars.2012.5164.
  • Li G, Tang D, Lotze MT. Menage a trois in stress: damps, redox and autophagy. Semin Cancer Biol. 2013;23:380–390. doi:10.1016/j.semcancer.2013.08.002.
  • Rubartelli A, Lotze MT. Inside, outside, upside down: damage-associated molecular-pattern molecules (damps) and redox. Trends Immunol. 2007;28(10):429–436. doi:10.1016/j.it.2007.08.004.
  • Bekeschus S, Eisenmann S, Sagwal SK, Bodnar Y, Moritz J, Poschkamp B, Stoffels I, Emmert S, Madesh M, Weltmann KD, et al. Xct (slc7a11) expression confers intrinsic resistance to physical plasma treatment in tumor cells. Redox Biol. 2020;30:101423. doi:10.1016/j.redox.2019.101423.
  • Ninomiya K, Ishijima T, Imamura M, Yamahara T, Enomoto H, Takahashi K, Tanaka Y, Uesugi Y, Shimizu N. Evaluation of extra- and intracellular oh radical generation, cancer cell injury, and apoptosis induced by a non-thermal atmospheric-pressure plasma jet. J Phys D: Appl Phys. 2013;46:425401. doi:10.1088/0022-3727/46/42/425401.
  • Bekeschus S, Lippert M, Diepold K, Chiosis G, Seufferlein T, Azoitei N. Physical plasma-triggered ros induces tumor cell death upon cleavage of hsp90 chaperone. Sci Rep. 2019;9:4112. doi:10.1038/s41598-019-38580-0.
  • Mirpour S, Piroozmand S, Soleimani N, Jalali Faharani N, Ghomi H, Fotovat Eskandari H, Sharifi AM, Mirpour S, Eftekhari M, Nikkhah M. Utilizing the micron sized non-thermal atmospheric pressure plasma inside the animal body for the tumor treatment application. Sci Rep. 2016;6:29048. doi:10.1038/srep29048.
  • Lin A, Gorbanev Y, De Backer J, Van Loenhout J, Van Boxem W, Lemiere F, Cos P, Dewilde S, Smits E, Bogaerts A. Non-thermal plasma as a unique delivery system of short-lived reactive oxygen and nitrogen species for immunogenic cell death in melanoma cells. Adv Sci (Weinh). 2019;6:1802062. doi:10.1002/advs.201802062.
  • Bekeschus S, Rodder K, Fregin B, Otto O, Lippert M, Weltmann KD, Wende K, Schmidt A, Gandhirajan RK. Toxicity and immunogenicity in murine melanoma following exposure to physical plasma-derived oxidants. Oxid Med Cell Longev. 2017;2017:4396467. doi:10.1155/2017/4396467.
  • Lin A, Truong B, Patel S, Kaushik N, Choi EH, Fridman G, Fridman A, Miller V. Nanosecond-pulsed dbd plasma-generated reactive oxygen species trigger immunogenic cell death in a549 lung carcinoma cells through intracellular oxidative stress. Int J Mol Sci. 2017;18:966. doi:10.3390/ijms18050966.
  • Bekeschus S, Mueller A, Miller V, Gaipl U, Weltmann K-D. Physical plasma elicits immunogenic cancer cell death and mitochondrial singlet oxygen. IEEE Transactions on Radiation and Plasma Medical Sciences. 2018;2(2):138–146. doi:10.1109/trpms.2017.2766027.
  • Lin AG, Xiang B, Merlino DJ, Baybutt TR, Sahu J, Fridman A, Snook AE, Miller V. Non-thermal plasma induces immunogenic cell death in vivo in murine CT26 colorectal tumors. Oncoimmunology. 2018;7(9):e1484978. doi:10.1080/2162402X.2018.1484978.
  • Azzariti A, Iacobazzi RM, Di Fonte R, Porcelli L, Gristina R, Favia P, Fracassi F, Trizio I, Silvestris N, Guida G, et al. Plasma-activated medium triggers cell death and the presentation of immune activating danger signals in melanoma and pancreatic cancer cells. Sci Rep. 2019;9:4099. doi:10.1038/s41598-019-40637-z.
  • Freund E, Liedtke KR, van der Linde J, Metelmann HR, Heidecke CD, Partecke LI, Bekeschus S. Physical plasma-treated saline promotes an immunogenic phenotype in ct26 colon cancer cells in vitro and in vivo. Sci Rep. 2019;9:634. doi:10.1038/s41598-018-37169-3.
  • Bekeschus S, Schmidt A, Niessner F, Gerling T, Weltmann KD, Wende K. Basic research in plasma medicine - a throughput approach from liquids to cells. J Vis Exp. 2017:e56331. doi:10.3791/56331.
  • Liedtke KR, Freund E, Hackbarth C, Heidecke C-D, Partecke L-I, Bekeschus S. A myeloid and lymphoid infiltrate in murine pancreatic tumors exposed to plasma-treated medium. Clin Plas Med. 2018;11:10–17. doi:10.1016/j.cpme.2018.07.001.
  • Mizuno K, Yonetamari K, Shirakawa Y, Akiyama T, Ono R. Anti-tumor immune response induced by nanosecond pulsed streamer discharge in mice. J Phys D: Appl Phys. 2017;50:12LT01. doi:10.1088/1361-6463/aa5dbb.
  • Mizuno K, Shirakawa Y, Sakamoto T, Ishizaki H, Nishijima Y, Ono R. Plasma-induced suppression of recurrent and reinoculated melanoma tumors in mice. Ieee Trpms. 2018;2:353–359. doi:10.1109/trpms.2018.2809673.
  • Tresp H, Hammer MU, Winter J, Weltmann KD, Reuter S. Quantitative detection of plasma-generated radicals in liquids by electron paramagnetic resonance spectroscopy. J Phys D: Appl Phys. 2013;46:435401. doi:10.1088/0022-3727/46/43/435401.
  • Bekeschus S, Wende K, Hefny MM, Rodder K, Jablonowski H, Schmidt A, Woedtke TV, Weltmann KD, Benedikt J. Oxygen atoms are critical in rendering thp-1 leukaemia cells susceptible to cold physical plasma-induced apoptosis. Sci Rep. 2017;7:2791. doi:10.1038/s41598-017-03131-y.
  • Jablonowski H, von Woedtke T. Research on plasma medicine-relevant plasma–liquid interaction: what happened in the past five years? Clin Plas Med. 2015;3:42–52. doi:10.1016/j.cpme.2015.11.003.
  • Winter J, Sousa JS, Sadeghi N, Schmidt-Bleker A, Reuter S, Puech V. The spatio-temporal distribution of he (23s1) metastable atoms in a mhz-driven helium plasma jet is influenced by the oxygen/nitrogen ratio of the surrounding atmosphere. Plasma Sources Sci T. 2015;24:25015–25025. doi:10.1088/0963-0252/24/2/025015.
  • Bekeschus S, Winterbourn CC, Kolata J, Masur K, Hasse S, Broker BM, Parker HA. Neutrophil extracellular trap formation is elicited in response to cold physical plasma. J Leukoc Biol. 2016;100:791–799. doi:10.1189/jlb.3A0415-165RR.
  • Chiang CL, Kandalaft LE, Tanyi J, Hagemann AR, Motz GT, Svoronos N, Montone K, Mantia-Smaldone GM, Smith L, Nisenbaum HL, et al. A dendritic cell vaccine pulsed with autologous hypochlorous acid-oxidized ovarian cancer lysate primes effective broad antitumor immunity: from bench to bedside. Clin Cancer Res. 2013;19(17):4801–4815. doi:10.1158/1078-0432.CCR-13-1185.
  • Tanyi JL, Bobisse S, Ophir E, Tuyaerts S, Roberti A, Genolet R, Baumgartner P, Stevenson BJ, Iseli C, Dangaj D, et al. Personalized cancer vaccine effectively mobilizes antitumor t cell immunity in ovarian cancer. Sci Transl Med. 2018;10. doi:10.1126/scitranslmed.aao5931.
  • Bekeschus S, Schmidt A, Weltmann K-D, von Woedtke T. The plasma jet kinpen – a powerful tool for wound healing. Clin Plas Med. 2016;4:19–28. doi:10.1016/j.cpme.2016.01.001.
  • Wende K, Bekeschus S, Schmidt A, Jatsch L, Hasse S, Weltmann KD, Masur K, von Woedtke T. Risk assessment of a cold argon plasma jet in respect to its mutagenicity. Mutat Res Genet Toxicol Environ Mutagen. 2016;798-799:48–54. doi:10.1016/j.mrgentox.2016.02.003.
  • Bekeschus S, Schmidt A, Kramer A, Metelmann HR, Adler F, von Woedtke T, Niessner F, Weltmann KD, Wende K. High throughput image cytometry micronucleus assay to investigate the presence or absence of mutagenic effects of cold physical plasma. Environ Mol Mutagen. 2018;59:268–277. doi:10.1002/em.22172.
  • Kluge S, Bekeschus S, Bender C, Benkhai H, Sckell A, Below H, Stope MB, Kramer A. Investigating the mutagenicity of a cold argon-plasma jet in an het-mn model. PLoS One. 2016;11:e0160667. doi:10.1371/journal.pone.0160667.
  • Schmidt A, Woedtke TV, Stenzel J, Lindner T, Polei S, Vollmar B, Bekeschus S. One year follow-up risk assessment in skh-1 mice and wounds treated with an argon plasma jet. Int J Mol Sci. 2017:18. doi:10.3390/ijms18040868.
  • Metelmann H-R, Vu TT, Do HT, Le TNB, Hoang THA, Phi TTT, Luong TML, Doan VT, Nguyen TTH, Nguyen THM, et al. Scar formation of laser skin lesions after cold atmospheric pressure plasma (cap) treatment: A clinical long term observation. Clin Plas Med. 2013;1:30–35. doi:10.1016/j.cpme.2012.12.001.
  • Biscop E, Lin A, Boxem WV, Loenhout JV, Backer J, Deben C, Dewilde S, Smits E, Bogaerts AA. Influence of cell type and culture medium on determining cancer selectivity of cold atmospheric plasma treatment. Cancers. 2019;11 Basel. doi:10.3390/cancers11091287.
  • Wang M, Holmes B, Cheng X, Zhu W, Keidar M, Zhang LG. Cold atmospheric plasma for selectively ablating metastatic breast cancer cells. PLoS One. 2013;8:e73741. doi:10.1371/journal.pone.0073741.
  • Van der Paal J, Neyts EC, Verlackt CCW, Bogaerts A. Effect of lipid peroxidation on membrane permeability of cancer and normal cells subjected to oxidative stress. Chem Sci. 2016;7:489–498. doi:10.1039/c5sc02311d.
  • Van Boxem W, Van der Paal J, Gorbanev Y, Vanuytsel S, Smits E, Dewilde S, Bogaerts A. Anti-cancer capacity of plasma-treated pbs: effect of chemical composition on cancer cell cytotoxicity. Sci Rep. 2017;7:16478. doi:10.1038/s41598-017-16758-8.
  • Acharya A, Das I, Chandhok D, Saha T. Redox regulation in cancer: A double-edged sword with therapeutic potential. Oxid Med Cell Longev. 2010;3:23–34. doi:10.4161/oxim.3.1.10095.
  • Saadati F, Mahdikia H, Abbaszadeh HA, Abdollahifar MA, Khoramgah MS, Shokri B. Comparison of direct and indirect cold atmospheric-pressure plasma methods in the b16f10 melanoma cancer cells treatment. Sci Rep. 2018;8:7689. doi:10.1038/s41598-018-25990-9.
  • Zhou D, Shao L, Spitz DR. Reactive oxygen species in normal and tumor stem cells. In Adv. Cancer res., Elsevier:. 2014; Vol. 122. 1–67. https://www.sciencedirect.com/science/article/pii/B9780124201170000013
  • Xiang L, Xu X, Zhang S, Cai D, Dai X. Cold atmospheric plasma conveys selectivity on triple negative breast cancer cells both in vitro and in vivo. Free Radic Biol Med. 2018;124:205–213. doi:10.1016/j.freeradbiomed.2018.06.001.