Low-temperature plasma-activated medium inhibited invasion and metastasis of melanoma cells via suppressing the Wnt/β-catenin pathway
Jin-Ren Liu
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorLing-Ge Gao
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorYue-Ming Wu
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorGui-Min Xu
School of Electronics and Control Engineering, Chang'an University, Xi'an, Shaanxi, China
State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorYan Ma
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorYue Hao
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorCorresponding Author
Xing-Min Shi
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Correspondence Xing-Min Shi, Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, 710061 Shaanxi, China.
Email: [email protected]
Guan-Jun Zhang, State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, 710049 Shaanxi, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Guan-Jun Zhang
State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Correspondence Xing-Min Shi, Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, 710061 Shaanxi, China.
Email: [email protected]
Guan-Jun Zhang, State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, 710049 Shaanxi, China.
Email: [email protected]
Search for more papers by this authorJin-Ren Liu
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorLing-Ge Gao
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorYue-Ming Wu
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorGui-Min Xu
School of Electronics and Control Engineering, Chang'an University, Xi'an, Shaanxi, China
State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorYan Ma
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorYue Hao
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Search for more papers by this authorCorresponding Author
Xing-Min Shi
Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Correspondence Xing-Min Shi, Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, 710061 Shaanxi, China.
Email: [email protected]
Guan-Jun Zhang, State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, 710049 Shaanxi, China.
Email: [email protected]
Search for more papers by this authorCorresponding Author
Guan-Jun Zhang
State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, Shaanxi, China
Correspondence Xing-Min Shi, Medical Science Center, School of Public Health, Xi'an Jiaotong University, Xi'an, 710061 Shaanxi, China.
Email: [email protected]
Guan-Jun Zhang, State Key Laboratory of Electrical Insulation and Power Equipment, Xi'an Jiaotong University, Xi'an, 710049 Shaanxi, China.
Email: [email protected]
Search for more papers by this authorAbstract
Low-temperature plasma (LTP) has shown promising and potential applications in the field of biomedicine. The effects of the plasma-activated medium (PAM) inhibiting tumor cell invasion and metastasis have been verified, but the associated molecular mechanisms are poorly understood. The aim of this study was to identify the anti-invasion and antimetastasis effects and mechanism induced by PAM on B16 melanoma cells cultured in vitro. For this purpose, an atmospheric pressure plasma jet in helium was applied to generate PAM to treat B16 cells. Cell invasion and migration assays showed that PAM exerted an inhibitory effect on B16 cell invasion and migration in a time-dependent manner. Then, detection of the invasion- and metastasis-related proteins, including matrix metalloproteinase (MMP)-2, MMP-9, CD44, and E-cadherin, showed that their changes accorded with the invasion and metastasis of the PAM-treated B16 cells. Furthermore, the Wnt/β-catenin pathway-related proteins in PAM-treated cells were measured, and the pathway was found to be suppressed by PAM. Finally, numerous specific reactive oxygen species (ROS) scavengers were applied to eliminate LTP-induced ROS in PAM, and it was revealed that H2O2 played a critical role in these processes. These findings demonstrated that PAM exerted anti-invasion and antimetastasis effects on B16 cells mainly by suppressing the Wnt/β-catenin pathway, which consequently decreased the expressions of MMP-9, MMP-2, and CD44 via H2O2.
REFERENCES
- 1A. Bogaerts, E. Neyts, R. Gijbels, J. van der Mullen, Spectrochim. Acta. Part B 2002, 57, 609.
- 2M. Laroussi, IEEE Trans. Plasma Sci. 2009, 37, 714.
- 3M. Laroussi, Plasma Process. Polym. 2005, 2, 391.
- 4M. Miletić, S. Mojsilović, I. Okić đorđević, D. Maletić, N. Puač, S. Lazović, G. Malović, P. Milenković, Z. Lj petrović, D. Bugarski, J. Phys. D: Appl. Phys. 2013, 46, 1.
- 5S. U. Kalghatgi, G. Fridman, M. Cooper, G. Nagaraj, M. Peddinghaus, M. Balasubramanian, V. N. Vasilets, A. F. Gutsol, A. Fridman, G. Friedman, IEEE Trans. Plasma Sci. 2007, 35, 1559.
- 6G. M. Xu, X. M. Shi, J. F. Cai, S. L. Chen, P. Li, C. W. Yao, Z. S. Chang, G. J. Zhang, Wound Repair Regen. 2015, 23, 878.
- 7D. Y. Yan, J. H. Sherman, M. Keidar, Oncotarget 2016, 8, 15977.
- 8M. Keidar, Plasma Sources Sci. Technol. 2015, 24.
- 9O. Volotskova, T. S. Hawley, M. A. Stepp, M. Keidar, Sci. Rep. 2012, 2, 636.
- 10N. Barekzi, M. Laroussi, Plasma Process. Polym. 2013, 10, 1039.
- 11M. Laroussi, Plasma Process. Polym. 2015, 11, 1138.
- 12C. H. Kim, J. H. Bahn, S. H. Lee, G. Y. Kim, S. I. Jun, K. Lee, S. J. Baek, J. Biotechnol. 2010, 150, 530.
- 13J. Y. Kim, Y. Wei, J. Li, S. O. Kim, Biosens. Bioelectron. 2011, 26, 555.
- 14J. W. Chang, S. U. Kang, Y. S. Shin, K. I. Kim, S. J. Seo, S. S. Yang, J. S. Lee, E. Moon, K. Lee, C. H. Kim, PLOS One 2014, 9, e92198.
- 15W. Li, K. N. Yu, L. Bao, J. Shen, C. Cheng, W. Han, Sci. Rep. 2016, 6, 19720.
- 16H. Tanaka, M. Mizuno, K. Ishikawa, K. Nakamura, H. Kajiyama, H. Kano, F. Kikkawa, Plasma Med. 2011, 1, 265.
10.1615/PlasmaMed.2012006275 Google Scholar
- 17T. Sato, M. Yokoyama, K. Johkura, J. Phys. D: Appl. Phys. 2011, 44, 372001.
- 18A. Azzariti, R. M. Iacobazzi, R. Di fonte, L. Porcelli, R. Gristina, P. Favia, F. Fracassi, I. trizio, N. Silvestris, G. Guida, S. Tommasi, E. Sardella, Sci. Rep. UK 2019, 9, 4099.
- 19J. R. Liu, Y. M. Wu, G. M. Xu, L. G. Gao, Y. Ma, X. M. Shi, G. J. Zhang, J. Phys. D: Appl. Phys. 2019, 52, 315204.
- 20T. Adachi, S. Nonomura, M. Horiba, T. Hirayama, T. Kamiya, H. Nagasawa, H. Hara, Sci. Rep. UK 2016, 6, 20928.
- 21N. Kumar, J. H. Park, S. N. Jeon, B. S. Park, E. H. Choi, P. Attri, J. Phys. D: Appl. Phys. 2016, 49, 115401.
- 22H. Yang, R. Lu, Y. Xian, L. Gan, X. Lu, X. Yang, Phys. Plasmas 2015, 22, 122006.
- 23F. Utsumi, H. Kajiyama, K. Nakamura, H. Tanaka, M. Mizuno, K. Ishikawa, H. Kondo, H. Kano, M. Hori, F. Kikkawa, PLOS One 2013, 8, e81576.
- 24J. Chauvin, F. Judee, N. Merbahi, P. Vicendo, Anti-Cancer Agent Med. Chem. 2018, 18, 776.
- 25J. Duan, X. Lu, G. He, J. Appl. Phys. 2017, 121, 13302.
- 26K. R. Liedtke, S. Bekeschus, A. Kaeding, C. Hackbarth, J. P. Kuehn, C. D. Heidecke, W. von Bernstorff, T. von Woedtke, L. I. Partecke, Sci. Rep. 2017, 7, 8319.
- 27D. Yan, J. H. Sherman, X. Cheng, E. Ratovitski, J. Canady, M. Keidar, Appl. Phys. Lett. 2014, 105, 224101.
- 28D. Yan, A. Talbot, N. Nourmohammadi, X. Cheng, J. Canady, J. Sherman, M. Keidar, Sci. Rep. 2015, 5, 18339.
- 29S. Mohades, N. Barekzi, H. Razavi, V. Maruthamuthu, M. Laroussi, Plasma Process. Polym. 2016, 13, 1206.
- 30D. Yan, N. Nourmohammadi, K. Bian, F. Murad, J. H. Sherman, M. Keidar, Sci. Rep. 2016, 6, 26016.
- 31T. Adachi, H. Tanaka, S. Nonomura, H. Hara, S. Kondo, M. Hori, Free Radic. Biol. Med. 2015, 79, 28.
- 32F. Judée, C. Fongia, B. Ducommun, M. Yousfi, V. Lobjois, N. Merbahi, Sci. Rep. 2016, 6, 21421.
- 33P. M. Girard, A. Arbabian, M. Fleury, G. Bauville, V. Puech, M. Dutreix, J. S. Sousa, Sci. Rep. 2016, 6, 29098.
- 34N. Kurake, H. Tanaka, K. Ishikawa, T. Kondo, M. Sekine, K. Nakamura, H. Kajiyama, F. Kikkawa, M. Mizuno, M. Hori, Arch. Biochem. Biophys. 2016, 605, 102.
- 35D. Boehm, C. Heslin, P. J. Cullen, P. Bourke, Sci. Rep. 2016, 6, 21464.
- 36P. Polakis, Curr. Opin. Genet. Dev. 2007, 17, 45.
- 37A. Klaus, W. Birchmeier, Nat. Rev. Cancer 2008, 8, 387.
- 38P. J. Morin, BioEssays 2015, 21, 1021.
- 39B. Wu, S. P. Crampton, C. C. W. Hughes, Immunity 2007, 26, 227.
- 40E. C. McGary, D. C. Lev, M. Bareli, Cancer Biol. Ther. 2002, 1, 459.
- 41V. J. M. Wielenga, R. Smits, V. Korinek, L. Smit, M. Kielman, R. Fodde, H. Clevers, S. T. Pals, Am. J. Pathol. 1999, 154, 515.
- 42M. A. Huber, N. Kraut, H. Beug, Curr. Opin. Cell Biol. 2005, 17, 548.
- 43E. I. Deryugina, J. P. Quigley, Cancer Metastat. Rev. 2006, 25, 9.
- 44R. Marhaba, M. Zöller, J. Mol. Histol. 2004, 35, 211.
- 45N. Pećina-Šlaus, Cancer Cell. Int. 2003, 3, 17.
- 46E. Sysolyatina, M. Vasiliev, M. Kurnaeva, I. Kornienko, O. Petrov, V. Fortov, A. Gintsburg, E. Petersen, S. Ermolaeva, J. Phys. D: Appl. Phys. 2016, 49, 294002.
- 47J. R. Liu, G. M. Xu, X. M. Shi, G. J. Zhang, Sci. Rep. 2017, 7, 11698.
- 48P. Brun, S. Pathak, I. Castagliuolo, G. Palù, P. Brun, M. Zuin, R. Cavazzana, E. Martines, PLOS One 2014, 15, 9.
- 49A. Schmidt, K. Wende, S. Bekeschus, L. Bundscherer, A. Barton, K. Ottmüller, K. D. Weltmann, K. Masur, Free Radic. Res. 2013, 47, 577.
- 50W. Song, E. Wang, Y. Gao, Q. Wu, S. Rao, H. Wang, L. Bao, Plasma Process. Polym. 2018, 15, e1600249.
- 51T. Adachi, H. Tanaka, S. Nonomura, H. Hara, S. Kondo, M. Hori, Free Radic. Bio. Med. 2015, 79, 28.
- 52J. W. Chang, S. U. Kang, Y. S. Shin, K. I. Kim, S. J. Seo, S. S. Yang, J. S. Lee, E. Moon, S. J. Baek, K. Lee, C. H. Kim, Arch. Biochem. Biophys. 2014, 545, 133.
- 53G. M. Xu, J. R. Liu, Y. M. Wu, X. M. Shi, G. J. Zhang, IEEE Trans. Plasma Sci. 2018, 46, 2805.
- 54D. B. Graves, J. Phys. D: Appl. Phys. 2012, 45, 263001.
- 55S. Curran, G. I. Murray, J. Pathol. 1999, 189, 300.
10.1002/(SICI)1096-9896(199911)189:3<300::AID-PATH456>3.0.CO;2-C CAS PubMed Web of Science® Google Scholar
- 56W. Kim, K. C. Woo, G. C. Kim, K. T. Kim, J. Phys. D: Appl. Phys. 2011, 44, 013001.
- 57A. R. Nelson, B. Fingleton, M. L. Rothenberg, L. M. Matrisian, J. Clin. Oncol. 2000, 18, 1135.
- 58U. B. Hofmann, J. R. Westphal, G. N. P. van Muijen, D. J. Ruiter, J. Invest. Dermatol. 2000, 115, 337.
- 59U. B. Hofmann, J. R. Westphal, A. A. van Kraats, D. J. Ruiter, G. N. van Muijen, Int. J. Cancer 2000, 87, 12.
- 60U. B. Hofmann, J. R. Westphal, E. T. Waas, A. J. W. Zendman, I. M. H. A. Cornelissen, D. J. Ruiter, G. N. P. Muijen, Br. J. Cancer 1999, 81, 774.
- 61P. Redondo, P. Lloret, M. Idoate, Clin. Exp. Dermatol. 2005, 30, 541.
- 62N. S. Penneys, S. Shapiro, J. Cutan. Pathol. 1994, 21, 22.
- 63E. Manten-Horst, E. H. J. Danen, L. Smit, M. Snoek, I. L. Caroline poole, G. N. P. van Muijen, S. T. Pals, D. J. Ruiter, Int. J. Cancer 1995, 64, 182.
- 64W. Birchmeier, J. Behrens, Biochim. Biophys. Acta 1994, 1198, 11.
- 65J. Behrens, M. M. Mareel, F. M. van Roy, W. Birchmeier, J. Cell Bio. 1989, 108, 2435.
- 66J. N. Anastas, R. T. Moon, Nat. Rev. Cancer 2013, 13, 11.
- 67J. D. Brown-Clay, D. N. Shenoy, O. Timofeeva, B. V. Kallakury, A. K. Nandi, P. P. Banerjee, Oncotarget 2015, 6, 15594.
- 68N. Kumar, P. Attri, D. K. Yadav, J. Choi, E. H. Choi, H. S. Uhm, Sci. Rep. 2014, 4, 7589.
- 69R. Li, S. Erdamar, H. Dai, M. Sayeeduddin, A. Frolov, T. M. Wheeler, G. E. Ayala, Anticancer Res. 2009, 29, 2077.
- 70M. Nishikawa, Cancer Lett. 2008, 266, 53.
- 71D. Hoogeboom, M. A. G. Essers, P. E. Polderman, E. Voets, L. M. M. Smits, B. M. T. Burgering, J. Biol. Chem. 2008, 283, 9224.
- 72S. Y. Shin, B. R. Chin, Y. H. Lee, J. H. Kim, Cell Signal. 2006, 18, 601.
- 73Y. Funato, T. Michiue, M. Asashima, H. Miki, Nat. Cell Biol. 2006, 8, 501.
- 74M. Almeida, L. Han, M. Martin-Millan, C. A. O'Brien, S. C. Manolagas, J. Biol. Chem. 2007, 282, 27298.
- 75S. Y. Shin, C. G. Kim, E. H. Jho, M. S. Rho, Y. S. Kim, Y. H. Kim, Y. H. Lee, Cancer Lett. 2004, 212, 225.
- 76Y. J. Lee, H. J. Han, Am. J. Physiol. Renal. Physiol. 2010, 298.