Preclinical Cold Atmospheric Plasma Cancer Treatment
Abstract
:Simple Summary
Abstract
1. CAP and Plasma Sources
2. General Picture of In Vitro Studies
3. Direct CAP Treatment In Vivo
4. CAP-Activated Solutions (PAS) and In Vivo Application
5. Abscopal Effect
6. Sensitization of Tumor to Drugs
7. Clinical Anti-Tumor Trials
8. Mechanism Discussion
9. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
AC | Alternating Current |
APPJ | Atmospheric Pressure Plasma Jet |
ATP | Adenosine Triphosphate |
CAP | Cold Atmospheric Plasma |
CHCP | Canady Helios Cold Atmospheric Plasma |
CRT | Calreticulin |
DAMP | Damage-Associated Molecular Patterns |
DBD | Dielectric Barrier Discharge |
DPI | Diphenylenyleneiodonium |
EM | Electromagnetic |
ICD | Immunogenic Cell Death |
IFN | Inflammatory Cytokines |
IL | Interleukin |
nsP | Nanosecond Pulsed |
PAS | CAP-Activated Solutions |
PAPB | PLEL Biogel |
PBS | Phosphate-Buffered Saline |
PDT | Cold Plasma Discharge Tube |
PLEL | (Poly-DL-Lactide)-(Poly-Ethylene-Glycol)-(Poly-DL-Lactide) |
RF | Radiofrequency |
ROS | Reactive Oxygen Species |
RNS | Reactive Nitrogen Species |
TMZ | Temozolomide |
USMI | US Medical Innovation |
References
- Von Woedtke, T.; Schmidt, A.; Bekeschus, S.; Wende, K.; Weltmann, K.D. Plasma medicine: A field of applied redox biology. In Vivo 2019, 33, 1011–1026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fridman, G.; Friedman, G.; Gutsol, A.; Shekhter, A.B.; Vasilets, V.N.; Fridman, A. Applied plasma medicine. Plasma Processes Polym. 2008, 5, 503–533. [Google Scholar] [CrossRef]
- Keidar, M. Plasma for cancer treatment. Plasma Sources Sci. Technol. 2015, 24, 033001. [Google Scholar] [CrossRef]
- Keidar, M. A prospectus on innovations in the plasma treatment of cancer. Phys. Plasmas 2018, 25, 083504. [Google Scholar] [CrossRef]
- Graves, D.B. Reactive species from cold atmospheric plasma: Implications for cancer therapy. Plasma Processes Polym. 2014, 11, 1120–1127. [Google Scholar] [CrossRef]
- Tendero, C.; Tixier, C.; Tristant, P.; Desmaison, J.; Leprince, P. Atmospheric pressure plasmas: A review. Spectrochim. Acta B At. Spectrosc. 2006, 61, 2–30. [Google Scholar] [CrossRef]
- Yan, D.; Sherman, J.H.; Keidar, M. Cold atmospheric plasma, a novel promising anti-cancer treatment modality. Oncotarget 2017, 8, 15977. [Google Scholar] [CrossRef] [Green Version]
- Lu, X.; Naidis, G.V.; Laroussi, M.; Ostrikov, K. Guided ionization waves: Theory and experiments. Phys. Rep. 2014, 540, 123–166. [Google Scholar] [CrossRef]
- Lu, X.P.; Ostrikov, K.K. Guided ionization waves: The physics of repeatability. Appl. Phys. Rev. 2018, 5, 031102. [Google Scholar] [CrossRef]
- Lin, L.; Yan, D.; Lee, T.; Keidar, M. Self-adaptive plasma chemistry and intelligent plasma medicine. Adv. Intell. Syst. 2022, 4, 2100112. [Google Scholar] [CrossRef]
- Keidar, M. A map of control for cold atmospheric plasma jets: From physical mechanisms to optimizations. Appl. Phys. Rev. 2021, 8.1, 011306. [Google Scholar]
- Kogelschatz, U. Atmospheric-pressure plasma technology. Plasma Phys. Control. Fusion 2004, 46, B63–B75. [Google Scholar] [CrossRef]
- Park, G.Y.; Park, S.J.; Choi, M.Y.; Koo, I.G.; Byun, J.H.; Hong, J.W.; Sim, J.Y.; Collins, G.J.; Lee, J.K. Atmospheric-pressure plasma sources for biomedical applications. Plasma Sources Sci. Technol. 2012, 21, 043001. [Google Scholar] [CrossRef]
- Yan, D.; Lin, L.; Xu, W.; Nourmohammadi, N. Cold plasma-based control of the activation of pancreatic adenocarcinoma cells. J. Phys. D Appl. Phys. 2019, 52.44, 445202. [Google Scholar] [CrossRef]
- Laroussi, M. Low temperature plasma-based sterilization: Overview and state-of-the-art. Plasma Processes Polym. 2005, 2, 391–400. [Google Scholar] [CrossRef]
- Feil, L.; Koch, A.; Utz, R.; Ackermann, M.; Barz, J.; Stope, M.; Krämer, B.; Wallwiener, D.; Brucker, S.Y.; Weiss, M. Cancer-selective treatment of cancerous and non-cancerous human cervical cell models by a non-thermally operated electrosurgical argon plasma device. Cancers 2020, 12, 1037. [Google Scholar] [CrossRef] [Green Version]
- Wenzel, T.; Berrio, D.A.C.; Reisenauer, C.; Layland, S.; Koch, A.; Wallwiener, D.; Brucker, S.Y.; Schenke-Layland, K.; Brauchle, E.M.; Weiss, M. Trans-mucosal efficacy of non-thermal plasma treatment on cervical cancer tissue and human cervix uteri by a next generation electrosurgical argon plasma device. Cancers 2020, 12, 267. [Google Scholar] [CrossRef] [Green Version]
- Marzi, J.; Stope, M.B.; Henes, M.; Koch, A.; Wenzel, T.; Holl, M.; Layland, S.L.; Neis, F.; Bösmüller, H.; Ruoff, F. Noninvasive physical plasma as innovative and tissue-preserving therapy for women positive for cervical intraepithelial neoplasia. Cancers 2022, 14, 1933. [Google Scholar] [CrossRef]
- Yan, D.; Talbot, A.; Nourmohammadi, N.; Sherman, J.H.; Cheng, X.; Keidar, M. Toward understanding the selective anticancer capacity of cold atmospheric plasma—A model based on aquaporins. Biointerphases 2015, 10, 040801. [Google Scholar] [CrossRef]
- Hirst, A.M.; Frame, F.M.; Arya, M.; Maitland, N.J.; O’Connell, D. Low temperature plasmas as emerging cancer therapeutics: The state of play and thoughts for the future. Tumor Biol. 2016, 37, 7021–7031. [Google Scholar] [CrossRef] [Green Version]
- Laroussi, M.; Lu, X.; Keidar, M. Perspective: The Physics, diagnostics, and applications of atmospheric pressure low temperature plasma sources used in plasma medicine. J. Appl. Phys. 2017, 122, 020901. [Google Scholar] [CrossRef]
- Kieft, I.E.; Dvinskikh, N.A.; Broers, J.L.v.; Slaaf, D.W.; Stoffels, E. Effect of plasma needle on cultured cells. Proc. SPIE 2004, 5483, 247–251. [Google Scholar]
- Fridman, G.; Shereshevsky, A.; Jost, M.M.; Brooks, A.D.; Fridman, A.; Gutsol, A.; Vasilets, V.; Friedman, G. Floating electrode dielectric barrier discharge plasma in air promoting apoptotic behavior in melanoma skin cancer cell lines. Plasma Chem. Plasma Process. 2007, 27, 163–176. [Google Scholar] [CrossRef]
- Lee, H.J.; Shon, C.H.; Kim, Y.S.; Kim, S.; Kim, G.C.; Kong, M.G. Degradation of adhesion molecules of g361 melanoma cells by a non-thermal atmospheric pressure microplasma. New J. Phys. 2009, 11, 115026. [Google Scholar] [CrossRef]
- Georgescu, N.; Lupu, A.R. Tumoral and normal cells treatment with high-voltage pulsed cold atmospheric plasma jets. IEEE Trans. Plasma Sci. 2010, 38.8, 1949–1955. [Google Scholar] [CrossRef]
- Kim, C.-H.; Bahn, J.H.; Lee, S.-H.; Kim, G.-Y.; Jun, S.-I.; Lee, K.; Baek, S.J. Induction of cell growth arrest by atmospheric non-thermal plasma in colorectal cancer cells. J. Biotechnol. 2010, 150, 530–538. [Google Scholar] [CrossRef]
- Kim, G.J.; Kim, W.; Kim, K.T.; Lee, J.K. DNA damage and mitochondria dysfunction in cell apoptosis induced by nonthermal air plasma. Appl. Phys. Lett. 2010, 96, 021502. [Google Scholar] [CrossRef] [Green Version]
- Ahn, H.J.; Kim, K.I.; Kim, G.; Moon, E.; Yang, S.S.; Lee, J.S. Atmospheric-pressure plasma jet induces apoptosis involving mitochondria via generation of free radicals. PLoS ONE 2011, 6, e28154. [Google Scholar] [CrossRef] [Green Version]
- Köritzer, J.; Boxhammer, V.; Schäfer, A.; Shimizu, T.; Klämpfl, T.G.; Li, Y.F.; Welz, C.; Schwenk-Zieger, S.; Morfill, G.E.; Zimmermann, J.L.; et al. Restoration of sensitivity in chemo-resistant glioma cells by cold atmospheric plasma. PLoS ONE 2013, 8, e64498. [Google Scholar] [CrossRef] [Green Version]
- Ja Kim, S.; Min Joh, H.; Chung, T.H. Production of intracellular reactive oxygen species and change of cell viability induced by atmospheric pressure plasma in normal and cancer cells. Appl. Phys. Lett. 2013, 103, 153705. [Google Scholar] [CrossRef]
- Arndt, S.; Wacker, E.; Li, Y.F.; Shimizu, T.; Thomas, H.M.; Morfill, G.E.; Karrer, S.; Zimmermann, J.L.; Bosserhoff, A.K. Cold atmospheric plasma, a new strategy to induce senescence in melanoma cells. Exp. Dermatol. 2013, 22, 284–289. [Google Scholar] [CrossRef] [PubMed]
- Lin, A.; Truong, B.; Pappas, A.; Kirifides, L.; Oubarri, A.; Chen, S.; Lin, S.; Dobrynin, D.; Fridman, G.; Fridman, A.; 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 Processes Polym. 2015, 12, 1392–1399. [Google Scholar] [CrossRef]
- Yan, D.; Cui, H.; Zhu, W.; Talbot, A.; Zhang, L.G.; Sherman, J.H.; Keidar, M. The strong cell-based hydrogen peroxide generation triggered by cold atmospheric plasma. Sci. Rep. 2017, 7, 10831. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.; Ito, F.; Wang, Y.; Okazaki, Y.; Tanaka, H.; Mizuno, M.; Hori, M.; Hirayama, T.; Nagasawa, H.; Richardson, D.R.; et al. Non-thermal plasma induces a stress response in mesothelioma cells resulting in increased endocytosis, lysosome biogenesis and autophagy. Free Radic. Biol. Med. 2017, 108, 904–917. [Google Scholar] [CrossRef]
- Yan, D.; Xu, W.; Yao, X.; Lin, L.; Sherman, J.H.; Keidar, M. The cell activation phenomena in the cold atmospheric plasma cancer treatment. Sci. Rep. 2018, 8, 15418. [Google Scholar] [CrossRef] [Green Version]
- Yan, D.; Wang, Q.; Adhikari, M.; Malyavko, A.; Lin, L.; Zolotukhin, D.B.; Yao, X.; Kirschner, M.; Sherman, J.H.; Keidar, M. A physically triggered cell death via transbarrier cold atmospheric plasma cancer treatment. ACS Appl. Mater. Interfaces 2020, 12, 34548–34563. [Google Scholar] [CrossRef]
- Yang, X.; Chen, G.; Yu, K.N.; Yang, M.; Peng, S.; Ma, J.; Qin, F.; Cao, W.; Cui, S.; Nie, L.; et al. Cold atmospheric plasma induces GSDME-dependent pyroptotic signaling pathway via ROS generation in tumor cells. Cell Death Dis. 2020, 11, 295. [Google Scholar] [CrossRef]
- Yao, X.; Lin, L.; Soni, V.; Gjika, E.; Sherman, J.H.; Yan, D.; Keidar, M. Sensitization of glioblastoma cells to temozolomide by a helium gas discharge tube. Phys. Plasmas 2020, 27, 114502. [Google Scholar] [CrossRef]
- Yan, D.; Talbot, A.; Nourmohammadi, N.; Cheng, X.; Canady, J.; Sherman, J.; Keidar, M. Principles of using cold atmospheric plasma stimulated media for cancer treatment. Sci. Rep. 2015, 5, 18339. [Google Scholar] [CrossRef] [Green Version]
- Yan, D.; Malyavko, A.; Wang, Q.; Ostrikov, K.K.; Sherman, J.H.; Keidar, M. Multi-modal biological destruction by cold atmospheric plasma: Capability and mechanism. Biomedicines 2021, 9, 1259. [Google Scholar] [CrossRef]
- Wang, Q.; Malyavko, A.; Yan, D.; Lamanna, O.K.; Hsieh, M.H.; Sherman, J.; Keidar, M. A Comparative study of cold atmospheric plasma treatment, chemical versus physical strategy. J. Phys. D Appl. Phys. 2020, 54, 095207. [Google Scholar] [CrossRef]
- Dezest, M.; Chavatte, L.; Bourdens, M.; Quinton, D.; Camus, M.; Garrigues, L.; Descargues, P.; Arbault, S.; Burlet-Schiltz, O.; Casteilla, L. Mechanistic insights into the impact of cold atmospheric pressure plasma on human epithelial cell lines. Sci. Rep. 2017, 7.1, 41163. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gorbanev, Y.; O’Connell, D.; Chechik, V. Non-thermal plasma in contact with water: The origin of species. J. Chem. 2016, 22, 3496–3505. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, R.; Zhou, R.; Wang, P.; Xian, Y.; Mai-prochnow, A. Plasma-activated water: Generation, origin of reactive species and biological applications. J. Phys. D Appl. Phys. 2020, 53, 303001. [Google Scholar] [CrossRef]
- Brisset, J.L.; Pawlat, J. 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. 2016, 36, 355–381. [Google Scholar] [CrossRef]
- Tanaka, H.; Bekeschus, S.; Yan, D.; Hori, M.; Keidar, M.; Laroussi, M. Plasma-Treated Solutions (PTS) in cancer therapy. Cancers 2021, 13, 1737. [Google Scholar] [CrossRef]
- Yan, D.; Horkowitz, A.; Wang, Q.; Keidar, M. On the selective killing of cold atmospheric plasma cancer treatment: Status and beyond. Plasma Processes Polym. 2021, 18, 202100020. [Google Scholar] [CrossRef]
- Chernets, N.; Kurpad, D.S.; Alexeev, V.; Rodrigues, D.B.; Freeman, T.A. Reaction chemistry generated by nanosecond pulsed dielectric barrier discharge treatment is responsible for the tumor eradication in the B16 melanoma mouse model. Plasma Processes Polym. 2015, 12, 1400–1409. [Google Scholar] [CrossRef]
- Keidar, M.; Walk, R.; Shashurin, A.; Srinivasan, P.; Sandler, A.; Dasgupta, S.; Ravi, R.; Guerrero-Preston, R.; Trink, B. Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br. J. Cancer 2011, 105, 1295–1301. [Google Scholar] [CrossRef]
- Binenbaum, Y.; Ben-David, G.; Gil, Z.; Slutsker, Y.Z.; Ryzhkov, M.A.; Felsteiner, J.; Krasik, Y.E.; Cohen, J.T. Cold atmospheric plasma, created at the tip of an elongated flexible capillary using low electric current, can slow the progression of melanoma. PLoS ONE 2017, 12, e0169457. [Google Scholar] [CrossRef] [Green Version]
- Boehm, D.; Heslin, C.; Cullen, P.J.; Bourke, P. Cytotoxic and mutagenic potential of solutions exposed to cold atmospheric plasma. Sci. Rep. 2016, 6, 21464. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yan, D.; Malyavko, A.; Wang, Q.; Lin, L.; Sherman, J.H. Applied sciences cold atmospheric plasma cancer treatment, a critical review. Appl. Sci. 2021, 11, 7757. [Google Scholar] [CrossRef]
- Vandamme, M.; Robert, E.; Pesnel, S.; Barbosa, E.; Dozias, S.; Sobilo, J.; Lerondel, S.; le Pape, A.; Pouvesle, J.M. Antitumor effect of plasma treatment on U87 glioma xenografts: Preliminary results. Plasma Processes Polym. 2010, 7, 264–273. [Google Scholar] [CrossRef]
- Vandamme, M.; Robert, E.; Dozias, S.; Sobilo, J.; Lerondel, S.; le Pape, A.; Pouvesle, J.-M. Response of human glioma U87 xenografted on mice to non thermal plasma treatment. Plasma Med. 2011, 1, 27–43. [Google Scholar] [CrossRef] [Green Version]
- Brullé, L.; Vandamme, M.; Riès, D.; Martel, E.; Robert, E.; Lerondel, S.; Trichet, V.; Richard, S.; Pouvesle, J.M.; le Pape, A. Effects of a non thermal plasma treatment alone or in combination with gemcitabine in a MIA PaCa2-luc orthotopic pancreatic carcinoma model. PLoS ONE 2012, 7, e52653. [Google Scholar] [CrossRef] [PubMed]
- Vandamme, M.; Robert, E.; Lerondel, S.; Sarron, V.; Ries, D.; Dozias, S.; Sobilo, J.; Gosset, D.; Kieda, C.; Legrain, B.; et al. ROS implication in a new antitumor strategy based on non-thermal plasma. Int. J. Cancer. 2012, 130, 2185–2194. [Google Scholar] [CrossRef] [PubMed]
- Walk, R.M.; Snyder, J.A.; Srinivasan, P.; Kirsch, J.; Diaz, S.O.; Blanco, F.C.; Shashurin, A.; Keidar, M.; Sandler, A.D. Cold atmospheric plasma for the ablative treatment of neuroblastoma. J. Pediatr. Surg. 2013, 48, 67–73. [Google Scholar] [CrossRef]
- Yajima, I.; Iida, M.; Kumasaka, M.Y.; Omata, Y.; Ohgami, N.; Chang, J.; Ichihara, S.; Hori, M.; Kato, M. Non-equilibrium atmospheric pressure plasmas modulate cell cycle-related gene expressions in melanocytic tumors of RET-transgenic mice. Exp. Dermatol. 2014, 23, 424–425. [Google Scholar] [CrossRef] [Green Version]
- Kang, S.U.; Cho, J.-H.; Chang, J.W.; Shin, Y.S.; Kim, K.I.; Park, J.K.; Yang, S.S.; Lee, J.-S.; Moon, E.; Lee, K.; et al. Nonthermal plasma induces head and neck cancer cell death: The potential involvement of mitogen-activated protein kinase-dependent mitochondrial reactive oxygen species. Cell Death Dis. 2014, 5, e1056. [Google Scholar] [CrossRef]
- Ikeda, J.I.; Tsuruta, Y.; Nojima, S.; Sakakita, H.; Hori, M.; Ikehara, Y. Anti-cancer effects of nonequilibrium atmospheric pressure plasma on cancer-initiating cells in human endometrioid adenocarcinoma cells. Plasma Processes Polym. 2015, 12, 1370–1376. [Google Scholar] [CrossRef]
- Kaushik, N.K.; Kaushik, N.; Yoo, K.C.; Uddin, N.; Kim, J.S.; Lee, S.J.; Choi, E.H. Low doses of PEG-coated gold nanoparticles sensitize solid tumors to cold plasma by blocking the PI3K/AKT-driven signaling axis to suppress cellular transformation by inhibiting growth and EMT. Biomaterials 2016, 87, 118–130. [Google Scholar] [CrossRef] [PubMed]
- Mirpour, S.; Piroozmand, S.; Soleimani, N.; Jalali Faharani, N.; Ghomi, H.; Fotovat Eskandari, H.; Sharifi, A.M.; 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. [Google Scholar] [CrossRef] [PubMed]
- Lin, A.G.; Xiang, B.; Merlino, D.J.; Baybutt, T.R.; Sahu, J.; Fridman, A.; Snook, A.E.; Miller, V. Non-thermal plasma induces immunogenic cell death in vivo in murine CT26 colorectal tumors. Oncoimmunology 2018, 7, e1484978. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yan, D.; Nourmohammadi, N.; Bian, K.; Murad, F.; Sherman, J.H.; Keidar, M. Stabilizing the cold plasma-stimulated medium by regulating medium’s composition. Sci. Rep. 2016, 6, 26016. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, H.; Mizuno, M.; Ishikawa, K.; Nakamura, K.; Kajiyama, H.; Kano, H.; Kikkawa, F.; Hori, M. Plasma-activated medium selectively kills glioblastoma brain tumor cells by down-regulating a survival signaling molecule, AKT kinase. Plasma Med. 2011, 1, 265–277. [Google Scholar] [CrossRef] [Green Version]
- Yan, D.; Sherman, J.H.; Keidar, M. The application of the cold atmospheric plasma-activated solutions in cancer treatment. Anti-Cancer Agents Med. Chem. 2018, 18, 769–775. [Google Scholar] [CrossRef]
- Takeda, S.; Yamada, S.; Hattori, N.; Nakamura, K.; Tanaka, H.; Kajiyama, H.; Kanda, M.; Kobayashi, D.; Tanaka, C.; Fujii, T.; et al. Intraperitoneal administration of plasma-activated medium: Proposal of a novel treatment option for peritoneal metastasis from gastric cancer. Ann. Surg. Oncol. 2017, 24, 1188–1194. [Google Scholar] [CrossRef]
- Harley, J.C.; Suchowerska, N.; Mckenzie, D.R. Cancer treatment with gas plasma and with gas plasma-activated liquid: Positives, potentials and problems of clinical translation. Biophys. Rev. 2020, 12, 989–1006. [Google Scholar] [CrossRef]
- Yan, D.; Sherman, J.H.; Cheng, X.; Ratovitski, E.; Canady, J.; Keidar, M. Controlling plasma stimulated media in cancer treatment application. Appl. Phys. Lett. 2014, 105, 224101. [Google Scholar] [CrossRef] [Green Version]
- Girard, P.-M.; Arbabian, A.; Fleury, M.; Bauville, G.; Puech, V.; Dutreix, M.; Sousa, J.S. Synergistic effect of H2O2 and NO2 in cell death induced by cold atmospheric He plasma. Sci. Rep. 2016, 6, 29098. [Google Scholar] [CrossRef] [Green Version]
- Yan, D.; Cui, H.; Zhu, W.; Nourmohammadi, N.; Milberg, J.; Zhang, L.G.; Sherman, J.H.; Keidar, M. The specific vulnerabilities of cancer cells to the cold atmospheric plasma-stimulated solutions. Sci. Rep. 2017, 7, 4479. [Google Scholar] [CrossRef] [PubMed]
- Kumar, N.; Park, J.H.; Jeon, S.N.; Park, B.S.; Choi, E.H.; Attri, P. The Action of microsecond-pulsed plasma-activated media on the inactivation of human lung cancer cells. J. Phys. D Appl. Phys. 2016, 49, 115401. [Google Scholar] [CrossRef]
- Chen, C.Y.; Cheng, Y.C.; Cheng, Y.J. Synergistic effects of plasma-activated medium and chemotherapeutic drugs in cancer treatment. J. Phys. D Appl. Phys. 2018, 51, 13LT01. [Google Scholar] [CrossRef]
- Yan, D.; Nourmohammadi, N.; Talbot, A.; Sherman, J.H.; Keidar, M. The strong anti-glioblastoma capacity of the plasma-stimulated lysine-rich medium. J. Phys. D Appl. Phys. 2016, 49, 274001. [Google Scholar] [CrossRef]
- Kaushik, N.; Lee, S.J.; Choi, T.G.; Baik, K.Y.; Uhm, H.S.; Kim, C.H.; Kaushik, N.K.; Choi, E.H. Non-thermal plasma with 2-deoxy-D-glucose synergistically induces cell death by targeting glycolysis in blood cancer cells. Sci. Rep. 2015, 5, 8726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adachi, T.; Nonomura, S.; Horiba, M.; Hirayama, T.; Kamiya, T.; Nagasawa, H.; Hara, H. Iron stimulates plasma-activated medium-induced A549 cell injury. Sci. Rep. 2016, 6, 20928. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, N.H.; Park, H.J.; Yang, S.S.; Choi, K.S.; Lee, J.S. Anti-cancer efficacy of nonthermal plasma dissolved in a liquid, liquid plasma in heterogeneous cancer cells. Sci. Rep. 2016, 6, 29020. [Google Scholar] [CrossRef]
- Saito, K.; Asai, T.; Fujiwara, K.; Sahara, J.; Koguchi, H.; Fukuda, N.; Suzuki-Karasaki, M.; Soma, M.; Suzuki-Karasaki, Y. Tumor-selective mitochondrial network collapse induced by atmospheric gas plasma-activated medium. Oncotarget 2016, 7, 19910. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.; Zhou, R.; Thomas, P.; Zhao, L.; Zhou, R.; Mandal, S.; Jolly, M.K.; Richard, D.J.; Rehm, B.H.A.; Ostrikov, K.; et al. Epithelial-to-Mesenchymal transition enhances cancer cell sensitivity to cytotoxic effects of zcold atmospheric plasmas in breast and bladder cancer systems. Cancers 2021, 13, 2889. [Google Scholar] [CrossRef]
- Liedtke, K.R.; Bekeschus, S.; Kaeding, A.; Hackbarth, C.; Kuehn, J.-P.; Heidecke, C.-D.; von Bernstorff, W.; von Woedtke, T.; Partecke, L.I. Non-thermal plasma-treated solution demonstrates antitumor activity against pancreatic cancer cells in vitro and in vivo. Sci. Rep. 2017, 7, 8319. [Google Scholar] [CrossRef]
- Xu, D.; Cui, Q.; Xu, Y.; Wang, B.; Tian, M.; Li, Q.; Liu, Z.; Liu, D.; Chen, H.; Kong, M.G. Systemic study on the safety of immuno- deficient nude mice treated by atmospheric plasma-activated water. Plasma Sci. Technol. 2018, 20, 44003. [Google Scholar] [CrossRef] [Green Version]
- Nastasa, V.; Pasca, A.S.; Malancus, R.N.; Bostanaru, A.C.; Ailincai, L.I.; Ursu, E.L.; Vasiliu, A.L.; Minea, B.; Hnatiuc, E.; Mares, M. Toxicity assessment of long-term exposure to non-thermal plasma activated water in mice. Int. J. Mol. Sci. 2021, 22, 11534. [Google Scholar] [CrossRef] [PubMed]
- Utsumi, F.; Kajiyama, H.; Nakamura, K.; Tanaka, H.; Mizuno, M.; Ishikawa, K.; Kondo, H.; Kano, H.; Hori, M.; Kikkawa, F. 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 2013, 8, e81576. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liedtke, K.R.; Freund, E.; Hermes, M.; Oswald, S.; Heidecke, C.D.; Partecke, L.I.; Bekeschus, S. Gas plasma-conditioned ringer’s lactate enhances the cytotoxic activity of cisplatin and gemcitabine in pancreatic cancer in vitro and in ovo. Cancers 2020, 12, 123. [Google Scholar] [CrossRef] [Green Version]
- Jiang, L.; Zheng, H.; Lyu, Q.; Hayashi, S.; Sato, K.; Sekido, Y. Redox biology lysosomal nitric oxide determines transition from autophagy to ferroptosis after exposure to plasma-activated ringer’s lactate. Redox Biol. 2021, 43, 101989. [Google Scholar] [CrossRef]
- Ishikawa, K.; Hosoi, Y.; Tanaka, H.; Jiang, L.; Toyokuni, S.; Nakamura, K.; Kajiyama, H.; Kikkawa, F.; Mizuno, M.; Hori, M. Non-thermal plasma–activated lactate solution kills U251SP glioblastoma cells in an innate reductive manner with altered metabolism. Arch. Biochem. Biophys. 2020, 688, 108414. [Google Scholar] [CrossRef]
- Rouven, K.; Freund, E.; Hackbarth, C.; Heidecke, C. A myeloid and lymphoid infiltrate in murine pancreatic tumors exposed to plasma-treated medium. Clin. Plasma Med. 2020, 11, 10–17. [Google Scholar]
- Zhang, H.; Xu, S.; Zhang, J.; Wang, Z.; Liu, D.; Guo, L.; Cheng, C.; Cheng, Y.; Xu, D.; Kong, M.G.; et al. Plasma-activated thermosensitive biogel as an exogenous ROS carrier for post-surgical treatment of cancer. Biomaterials 2021, 276, 121057. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Jinno, R.; Komuro, A.; Yanai, H.; Ono, R. Antitumor abscopal effects in mice induced by normal tissue irradiation using pulsed streamer discharge plasma. J. Phys. D Appl. Phys. 2022, 55, 17LT01. [Google Scholar] [CrossRef]
- Yan, D.; Wang, Q.; Yao, X.; Malyavko, A. Anti-melanoma capability of contactless cold atmospheric plasma treatment. Int. J. Mol. Sci. 2021, 22, 11728. [Google Scholar] [CrossRef] [PubMed]
- Mitra, S.; Nguyen, L.N.; Akter, M.; Park, G.; Choi, E.H.; Kaushik, N.K. Impact of ROS generated by chemical, physical, and plasma techniques on cancer attenuation. Cancers 2019, 11, 1030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eramo, A.; Ricci-Vitiani, L.; Zeuner, A.; Pallini, R.; Lotti, F.; Sette, G.; Pilozzi, E.; Larocca, L.M.; Peschle, C.; de Maria, R. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ. 2006, 13, 1238–1241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.Y. Temozolomide Resistance in Glioblastoma Multiforme. Genes Dis. 2016, 3, 198–210. [Google Scholar] [CrossRef] [Green Version]
- Soni, V.; Adhikari, M.; Simonyan, H.; Lin, L.; Sherman, J.H.; Young, C.N.; Keidar, M. In vitro and in vivo enhancement of temozolomide effect in human glioblastoma by non-invasive application of cold atmospheric plasma. Cancers 2021, 13, 4485. [Google Scholar] [CrossRef] [PubMed]
- Yao, X.; Yan, D.; Lin, L.; Sherman, J.H.; Peters, K.B.; Keir, S.T.; Keidar, M. Cold plasma discharge tube enhances antitumoral efficacy of temozolomide. ACS Appl. Bio Mater. 2022, 5.4, 1610–1623. [Google Scholar] [CrossRef]
- Canady, J.; Gordon, S.; Zhuang, T.; Wigh, S.; Rowe, W.; Shashurin, A.; Chiu, D.; Jones, S.; Wiley, K.; Cohen, E.; et al. Cold atmospheric plasma (cap) combined with chemo-radiation and cytoreductive surgery: The first clinical experience for stage iv metastatic colon cancer. In Comprehensive Clinical Plasma Medicine: Cold Physical Plasma for Medical Application; Metelmann, H.R., Von Woedtke, T., Weltmann, K.D., Eds.; Springer-Nature: Cham, Switzerland, 2018; pp. 163–183. [Google Scholar]
- 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. Head and neck cancer treatment and physical plasma. Clin. Plasma Med. 2015, 3, 17–23. [Google Scholar] [CrossRef]
- 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. Clinical experience with cold plasma in the treatment of locally advanced head and neck cancer. Clin. Plasma Med. 2018, 9, 6–13. [Google Scholar] [CrossRef]
- Bekeschus, S.; von Woedtke, T.; Emmert, S.; Schmidt, A. Medical gas plasma-stimulated wound healing: Evidence and mechanisms: Mechanisms of gas plasma-assisted wound healing. Redox Biol. 2021, 46, 102116. [Google Scholar] [CrossRef]
- Canady, J. Phase I Clinical Trial of Canady Helios Cold Atmospheric Plasma (CHCP) Treatment for Patients with Advanced Stage IV Metastatic and Recurrent Solid Tumors: A Novel Potential 4th Treatment Arm for Cancer. In Proceedings of the Bi-annual Conference of the Israeli Society of Surgical Oncology (ISSO), Haifa, Israel, 13 May 2022. [Google Scholar]
- Graves, D.B. Oxy-nitroso shielding burst model of cold atmospheric plasma therapeutics. Clin. Plasma Med. 2014, 2, 38–49. [Google Scholar] [CrossRef] [Green Version]
- Szili, E.J.; Oh, J.S.; Fukuhara, H.; Bhatia, R.; Gaur, N.; Nguyen, C.K.; Hong, S.H.; Ito, S.; Ogawa, K.; Kawada, C.; et al. Modelling the helium plasma jet delivery of reactive species into a 3D cancer tumour. Plasma Sources Sci. Technol. 2017, 27, 014001. [Google Scholar] [CrossRef] [Green Version]
- Szili, E.J.; Hong, S.; Oh, J.; Gaur, N.; Short, R.D. Tracking the penetration of plasma reactive species in tissue models. Trends Biotechnol. 2018, 36, 594–602. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh, J.S.; Szili, E.J.; Gaur, N.; Hong, S.H.; Furuta, H.; Kurita, H.; Mizuno, A.; Hatta, A.; Short, R.D. How to assess the plasma delivery of RONS into tissue fluid and tissue. J. Phys. D Appl. Phys. 2016, 49, 304005. [Google Scholar] [CrossRef]
- Oh, J.S.; Szili, E.J.; Ito, S.; Hong, S.H.; Gaur, N.; Furuta, H.; Short, R.D.; Hatta, A. Slow molecular transport of plasma generated reactive oxygen and nitrogen species. Plasma Med. 2015, 5, 2–4. [Google Scholar] [CrossRef]
- Szili, E.J.; Oh, J.S.; Hong, S.H.; Hatta, A.; Short, R.D. Probing the transport of plasma-generated RONS in an agarose target as surrogate for real tissue: Dependency on time, distance and material composition. J. Phys. D Appl. Phys. 2015, 48, 202001. [Google Scholar] [CrossRef]
- Wenzel, T.; Carvajal Berrio, D.A.; Daum, R.; Reisenauer, C.; Weltmann, K.D.; Wallwiener, D.; Brucker, S.Y.; Schenke-Layland, K.; Brauchle, E.M.; Weiss, M. Molecular Effects and tissue penetration depth of physical plasma in human mucosa analyzed by contact- and marker-independent raman microspectroscopy. ACS Appl. Mater. Interfaces 2019, 11, 42885. [Google Scholar] [CrossRef]
- Lu, X.; Keidar, M.; Laroussi, M.; Choi, E.; Szili, E.J.; Ostrikov, K. Transcutaneous plasma stress: From soft-matter models to living tissues. Mater. Sci. Eng. R Rep. 2019, 138, 36–59. [Google Scholar] [CrossRef]
- Kimura, K.; Tsuchida, A.; Kimura, K.; Tsuchida, A. Drying dissipative patterns of the colloidal crystals of silica spheres in an DC-electric field. Colloids Surf. B Biointerfaces. 2007, 56, 201–209. [Google Scholar]
- Omran, A.V.; Busco, G.; Ridou, L.; Dozias, S.; Grillon, C.; Pouvesle, J.-M.; Robert, E. Cold atmospheric single plasma jet for RONS delivery on large biological surfaces-IOPscience cold atmospheric single plasma jet for RONS delivery on large biological surfaces. Plasma Sources Sci. Technol. 2020, 29, 105002. [Google Scholar] [CrossRef]
- Ki, S.H.; Masur, K.; Baik, K.Y.; Choi, E.H. UV absorption spectroscopy for the diffusion of plasma-generated reactive species through a skin model. Appl. Sci. 2021, 11, 7958. [Google Scholar] [CrossRef]
- Jiang, C.; Oshin, E.A.; Guo, S.; Scott, M.; Li, X.; Mangiamele, C.; Heller, R. Synergistic effects of an atmospheric-pressure plasma jet and pulsed electric field on cells and skin. IEEE Trans. Plasma Sci. 2021, 49, 3317–3324. [Google Scholar] [CrossRef] [PubMed]
- Miller, V.; Lin, A.; Fridman, A. Why target immune cells for plasma treatment of cancer. Plasma Chem. Plasma Process 2016, 36, 259–268. [Google Scholar] [CrossRef]
- Cheng, F.; Yan, D.; Chen, J.; Wang, Z.; Horkowitz, A.; Keidar, M.; Sotomayor, E.M. Enhancing innate and adaptive immune systems by cold atmospheric plasma (CAP) and its antitumor immunity. arXiv 2022, 2201, 12737. [Google Scholar]
- Miller, V.; Lin, A.; Fridman, G.; Dobrynin, D.; Fridman, A. Plasma stimulation of migration of macrophages. Plasma Processes Polym. 2014, 11, 1193–1197. [Google Scholar] [CrossRef]
- Lin, A.; Truong, B.; Patel, S.; Kaushik, N.; Choi, E.H.; 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. [Google Scholar] [CrossRef] [Green Version]
- Lin, A.; Gorbanev, Y.; Cos, P.; Smits, E.; Bogaerts, A. Plasma elicits immunogenic death in melanoma cells regulation of antigen-presenting machinery in melanoma after plasma treatment. Clin. Plasma Med. 2018, 9, 9. [Google Scholar] [CrossRef]
- Khalili, M.; Daniels, L.; Lin, A.; Krebs, F.C.; Snook, A.E.; Bekeschus, S.; Bowne, W.B.; Miller, V. Non-thermal plasma-induced immunogenic cell death in cancer. J. Phys. D Appl. Phys. 2019, 52, 423001. [Google Scholar] [CrossRef] [PubMed]
- Bekeschus, S.; Mueller, A.; Miller, V.; Gaipl, U.; Weltmann, K. Physical plasma elicits immunogenic cancer cell death and mitochondrial singlet oxygen. IEEE Trans. Radiat. Plasma Med. Sci. 2018, 2, 138–146. [Google Scholar] [CrossRef]
- Mohamed, H.; Esposito, R.A.; Kutzler, M.A.; Wigdahl, B.; Krebs, F.C.; Miller, V. Nonthermal plasma as part of a novel strategy for vaccination. Plasma Processes Polym. 2020, 17, 2000051. [Google Scholar] [CrossRef]
- Nasri, Z.; Bruno, G.; Bekeschus, S.; Weltmann, K.D.; von Woedtke, T.; Wende, K. Development of an electrochemical sensor for in-situ monitoring of reactive species produced by cold physical plasma. Sens. Actuators B Chem. 2021, 326, 129007. [Google Scholar] [CrossRef]
- Yan, D.; Lin, L.; Xu, W.; Nourmohammadi, N.; Jonathan, H.; Keidar, M. Universality of micromolar-level cell-based hydrogen peroxide generation during direct cold atmospheric plasma treatment. Plasma Med. 2018, 8, 335–343. [Google Scholar] [CrossRef] [Green Version]
- Los, M.; Dröge, W.; Stricker, K.; Baeuerle, P.A.; Schulze-Osthoff, K. Hydrogen peroxide as a potent activator of t-lymphocyte functions. Eur. J. Immunol. 1995, 25, 159–165. [Google Scholar] [CrossRef] [PubMed]
- Reth, M. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 2002, 3, 1129–1134. [Google Scholar] [CrossRef] [PubMed]
- Graves, D.B. Lessons from tesla for plasma medicine. IEEE Trans. Radiat. Plasma Med. Sci. 2018, 2, 594–607. [Google Scholar] [CrossRef]
- Yan, D.; Wang, Q.; Malyavko, A.; Zolotukhin, D.B.; Adhikari, M.; Sherman, J.H.; Keidar, M. The anti-glioblastoma effect of cold atmospheric plasma treatment: Physical pathway v.s. chemical pathway. Sci. Rep. 2020, 10, 11788. [Google Scholar] [CrossRef]
- Chen, Z.; Xu, R.G.; Chen, P.; Wang, Q. Potential agricultural and biomedical applications of cold atmospheric plasma-activated liquids with self-organized patterns formed at the interface. IEEE Trans. Plasma Sci. 2020, 48, 3455–3471. [Google Scholar] [CrossRef]
Ref | Cancer Cellular Response | Years |
---|---|---|
[22] | Apoptosis | 2004 |
[23] | Growth Inhibition | 2007 |
[24] | Cytoskeletal Damage | 2009 |
[25] | Selective Cell Death | 2010 |
[26] | Cell Cycle Arrest | 2010 |
[27] | Nuclear and DNA Damage | 2010 |
[27] | Mitochondrial Damage | 2010 |
[28] | Rise of Intracellular ROS | 2011 |
[29] | Chemically-based Sensitization to Drugs | 2013 |
[30] | Selective Rise of Intracellular ROS | 2013 |
[31] | Senescence | 2013 |
[32] | Immunogenic Cell Death | 2015 |
[33] | Cell-based H2O2 Generation | 2017 |
[34] | Autophagy-associated Cell Death | 2017 |
[35] | Activation Phenomena | 2018 |
[36] | Physically-triggered Necrosis | 2020 |
[37] | Pyroptosis | 2020 |
[38] | Physically-based Sensitization to Drugs | 2021 |
Ref | Years | Tumor Types | Tumor Size | Survival Rate | Tumor Diagnostics |
---|---|---|---|---|---|
[53] | 2010 | Glioblastoma | Decreased | N/A | Bioluminescence imaging |
[49] | 2010 | Bladder cancer | Decreased | Increased | Tissue size measurement |
[54] | 2011 | Glioblastoma | Decreased | Increased | Bioluminescence imaging |
[55] | 2012 | Pancreatic carcinoma | Decreased | N/A | Bioluminescence imaging |
[56] | 2012 | Glioblastoma | Decreased | N/A | Bioluminescence imaging |
[57] | 2013 | Neuroblastoma | Decreased | Increased | Tissue size measurement |
[58] | 2014 | Melanoma | Decreased | N/A | Tissue size measurement |
[59] | 2014 | Head and neck cancer | Decreased | N/A | Tissue size measurement |
[48] | 2015 | Melanoma | Decreased | Increased | Tissue size measurement |
[60] | 2015 | Endometrioid adenocarcinoma | Decreased | N/A | Tissue size measurement |
[61] | 2016 | Glioblastoma | Decreased | N/A | Tissue size measurement |
[62] | 2016 | Breast cancer | Decreased | N/A | Tissue size measurement |
[50] | 2017 | Melanoma | Decreased | N/A | Bioluminescence imaging |
[63] | 2018 | Colorectal tumor | Decreased | N/A | Tissue size measurement |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Limanowski, R.; Yan, D.; Li, L.; Keidar, M. Preclinical Cold Atmospheric Plasma Cancer Treatment. Cancers 2022, 14, 3461. https://doi.org/10.3390/cancers14143461
Limanowski R, Yan D, Li L, Keidar M. Preclinical Cold Atmospheric Plasma Cancer Treatment. Cancers. 2022; 14(14):3461. https://doi.org/10.3390/cancers14143461
Chicago/Turabian StyleLimanowski, Ruby, Dayun Yan, Lin Li, and Michael Keidar. 2022. "Preclinical Cold Atmospheric Plasma Cancer Treatment" Cancers 14, no. 14: 3461. https://doi.org/10.3390/cancers14143461
APA StyleLimanowski, R., Yan, D., Li, L., & Keidar, M. (2022). Preclinical Cold Atmospheric Plasma Cancer Treatment. Cancers, 14(14), 3461. https://doi.org/10.3390/cancers14143461