Open Access

Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells

  • Authors:
    • Rafael Guerrero-Preston
    • Takenori Ogawa
    • Mamoru Uemura
    • Gary Shumulinsky
    • Blanca L. Valle
    • Francesca Pirini
    • Rajani Ravi
    • David Sidransky
    • Michael Keidar
    • Barry Trink
  • View Affiliations

  • Published online on: July 11, 2014     https://doi.org/10.3892/ijmm.2014.1849
  • Pages: 941-946
  • Copyright: © Guerrero-Preston et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

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Abstract

The treatment of locoregional recurrence (LRR) of head and neck squamous cell carcinoma (HNSCC) often requires a combination of surgery, radiation therapy and/or chemotherapy. Survival outcomes are poor and the treatment outcomes are morbid. Cold atmospheric plasma (CAP) is an ionized gas produced at room temperature under laboratory conditions. We have previously demonstrated that treatment with a CAP jet device selectively targets cancer cells using in vitro melanoma and in vivo bladder cancer models. In the present study, we wished to examine CAP selectivity in HNSCC in vitro models, and to explore its potential for use as a minimally invasive surgical approach that allows for specific cancer cell or tumor tissue ablation without affecting the surrounding healthy cells and tissues. Four HNSCC cell lines (JHU-022, JHU-028, JHU-029, SCC25) and 2 normal oral cavity epithelial cell lines (OKF6 and NOKsi) were subjected to cold plasma treatment for durations of 10, 30 and 45 sec, and a helium flow of 20 l/min-1 for 10 sec was used as a positive treatment control. We showed that cold plasma selectively diminished HNSCC cell viability in a dose-response manner, as evidenced by MTT assays; the viability of the OKF6 cells was not affected by the cold plasma. The results of colony formation assays also revealed a cell-specific response to cold plasma application. Western blot analysis did not provide evidence that the cleavage of PARP occurred following cold plasma treatment. In conclusion, our results suggest that cold plasma application selectively impairs HNSCC cell lines through non-apoptotic mechanisms, while having a minimal effect on normal oral cavity epithelial cell lines.

References

1 

Agrawal N, Frederick MJ, Pickering CR, et al: Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science. 333:1154–1157. 2011. View Article : Google Scholar : PubMed/NCBI

2 

Jemal A, Siegel R, Ward E, et al: Cancer statistics, 2007. CA Cancer J Clin. 57:43–66. 2007. View Article : Google Scholar

3 

Fletcher EV: Epidermal growth factor receptor inhibitor induces interleukin-6 via NADPH oxidase enzymes in head and neck cancer cells. Master’s thesis. University of Iowa; 2012

4 

Forastiere AA, Goepfert H, Maor M, et al: Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N Engl J Med. 349:2091–2098. 2003. View Article : Google Scholar : PubMed/NCBI

5 

Hardisson D: Molecular pathogenesis of head and neck squamous cell carcinoma. Eur Arch Otorhinolaryngol. 260:502–508. 2003. View Article : Google Scholar : PubMed/NCBI

6 

Wang M, Holmes B, Cheng X, et al: Cold atmospheric plasma for selectively ablating metastatic breast cancer cells. PLoS One. 8:e737412013. View Article : Google Scholar : PubMed/NCBI

7 

Shimizu T, Steffes B, Pompl R, et al: Characterization of microwave plasma torch for decontamination. Plasma Process Polym. 5:577–582. 2008. View Article : Google Scholar

8 

Yonson S, Coulombe S, Léveillé V and Leask RL: Cell treatment and surface functionalization using a miniature atmospheric pressure glow discharge plasma torch. J Phys D Appl Phys. 39:3508–3513. 2008. View Article : Google Scholar

9 

Kim JY, Ballato J, Foy P, et al: Single-cell-level cancer therapy using a hollow optical fiber-based microplasma. Small. 6:1474–1478. 2010. View Article : Google Scholar : PubMed/NCBI

10 

Lupu AR, Georgescu N, Călugăru A, et al: The effects of cold atmospheric plasma jets on B16 and COLO320 tumoral cells. Roum Arch Microbiol Immunol. 68:136–144. 2009.PubMed/NCBI

11 

Lupu AR and Georgescu N: Cold atmospheric plasma jet effects on V79-4 cells. Roum Arch Microbiol Immunol. 69:67–74. 2010.PubMed/NCBI

12 

Moisan M, Barbeau J, Moreau S, et al: Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. Int J Pharm. 226:1–21. 2001. View Article : Google Scholar : PubMed/NCBI

13 

Kim JY, Ballato J, Foy P, et al: Apoptosis of lung carcinoma cells induced by a flexible optical fiber-based cold microplasma. Biosens Bioelectron. 28:333–338. 2011. View Article : Google Scholar : PubMed/NCBI

14 

Panngom K, Baik KY, Nam MK, et al: Preferential killing of human lung cancer cell lines with mitochondrial dysfunction by nonthermal dielectric barrier discharge plasma. Cell Death Dis. 4:e6422013. View Article : Google Scholar : PubMed/NCBI

15 

Keidar M, Walk R, Shashurin A, et al: Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br J Cancer. 105:1295–1301. 2011. View Article : Google Scholar : PubMed/NCBI

16 

Hoffmann M, Bruch HP, Kujath P and Limmer S: Cold-plasma coagulation in the treatment of malignant pleural mesothelioma: results of a combined approach. Interact Cardiovasc Thorac Surg. 10:502–505. 2010. View Article : Google Scholar : PubMed/NCBI

17 

Walk RM, Snyder JA, Srinivasan P, et al: Cold atmospheric plasma for the ablative treatment of neuroblastoma. J Pediatr Surg. 48:67–73. 2013. View Article : Google Scholar : PubMed/NCBI

18 

Volotskova O, Hawley TS, Stepp MA and Keidar M: Targeting the cancer cell cycle by cold atmospheric plasma. Sci Rep. 2:6362012. View Article : Google Scholar : PubMed/NCBI

19 

Sensenig R, Kalghatgi S, Cerchar E, et al: Non-thermal plasma induces apoptosis in melanoma cells via production of intracellular reactive oxygen species. Ann Biomed Eng. 39:674–687. 2011. View Article : Google Scholar : PubMed/NCBI

20 

Vandamme M, Robert E, Lerondel S, et al: ROS implication in a new antitumor strategy based on non-thermal plasma. Int J Cancer. 130:2185–2194. 2012. View Article : Google Scholar : PubMed/NCBI

21 

Arndt S, Wacker E, Li YF, et al: Cold atmospheric plasma, a new strategy to induce senescence in melanoma cells. Exp Dermatol. 22:284–289. 2013. View Article : Google Scholar : PubMed/NCBI

22 

Sandulache VC, Ow TJ, Daram SP, et al: Residual nodal disease in patients with advanced-stage oropharyngeal squamous cell carcinoma treated with definitive radiation therapy and posttreatment neck dissection: association with locoregional recurrence, distant metastasis, and decreased survival. Head Neck. 35:1454–1460. 2013.

23 

Kieft IE, Kurdi M and Stoffels E: Reattachment and apoptosis after plasma-needle treatment of cultured cells. IEEE T Plasma Sci. 34:1331–1336. 2006. View Article : Google Scholar

24 

Lee HJ, Shon CH, Kim YS, et al: Degradation of adhesion molecules of G361 melanoma cells by a non-thermal atmospheric pressure microplasma. New J Phys. 11:1150262009. View Article : Google Scholar

25 

Shashurin A, Stepp MA, Hawley TS, et al: Influence of cold plasma atmospheric jet on surface integrin expression of living cells. Plasma Process Polym. 7:294–300. 2010. View Article : Google Scholar

26 

Keidar M, Shashurin A, Volotskova O, et al: Cold atmospheric plasma in cancer therapy. Physics of Plasmas. 20:0571012013. View Article : Google Scholar

27 

Vandamme M, Robert E, Pesnel S, et al: Antitumor effect of plasma treatment on U87 glioma xenografts: preliminary results. Plasma Process Polym. 7:264–273. 2010. View Article : Google Scholar

28 

Skinner HD, Sandulache VC, Ow TJ, et al: TP53 disruptive mutations lead to head and neck cancer treatment failure through inhibition of radiation-induced senescence. Clin Cancer Res. 18:290–300. 2012. View Article : Google Scholar : PubMed/NCBI

29 

Tokumaru Y, Yamashita K, Osada M, et al: Inverse correlation between cyclin A1 hypermethylation and p53 mutation in head and neck cancer identified by reversal of epigenetic silencing. Cancer Res. 64:5982–5987. 2004. View Article : Google Scholar : PubMed/NCBI

30 

Gu X, Song X, Dong Y, et al: Vitamin E succinate induces ceramide-mediated apoptosis in head and neck squamous cell carcinoma in vitro and in vivo. Clin Cancer Res. 14:1840–1848. 2008. View Article : Google Scholar : PubMed/NCBI

31 

Burns JE, Baird MC, Clark LJ, et al: Gene mutations and increased levels of p53 protein in human squamous cell carcinomas and their cell lines. Br J Cancer. 67:1274–1284. 1993. View Article : Google Scholar : PubMed/NCBI

32 

Ho AS, Kraus DH, Ganly I, et al: Decision making in the management of recurrent head and neck cancer. Head Neck. 36:144–151. 2014. View Article : Google Scholar : PubMed/NCBI

33 

Strojan P, Corry J, Eisbruch A, et al: Recurrent and second primary squamous cell carcinoma of the head and neck: when and how to reirradiate. Head Neck. Nov 7–2013.(Epub ahead of print).

34 

Mehanna HM and Ang KK: Head and Neck Cancer Recurrence: Evidence-based Multidisciplinary Management. 1st edition. Thieme Medical Publishers, Inc; New York, NY: pp. 3162012

35 

Hoffmann TK: Systemic therapy strategies for head-neck carcinomas: current status. GMS Curr Top Otorhinolaryngol Head Neck Surg. 11:Doc032012.PubMed/NCBI

36 

Bonner JA, Harari PM, Giralt J, et al: Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med. 354:567–578. 2006. View Article : Google Scholar : PubMed/NCBI

37 

Ang KK, Harris J, Wheeler R, et al: Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med. 363:24–35. 2010. View Article : Google Scholar : PubMed/NCBI

38 

Kelloff GJ, Lippman SM, Dannenberg AJ, et al: Progress in chemoprevention drug development: the promise of molecular biomarkers for prevention of intraepithelial neoplasia and cancer-a plan to move forward. Clin Cancer Res. 12:3661–3697. 2006. View Article : Google Scholar : PubMed/NCBI

39 

Myers MF, Chang MH, Jorgensen C, et al: Genetic testing for susceptibility to breast and ovarian cancer: evaluating the impact of a direct-to-consumer marketing campaign on physicians’ knowledge and practices. Genet Med. 8:361–370. 2006.PubMed/NCBI

40 

Whitworth A: New research suggests access, genetic differences play role in high minority cancer death rate. J Natl Cancer Inst. 98:6692006. View Article : Google Scholar : PubMed/NCBI

41 

Svatek RS, Lee JJ, Roehrborn CG, Lippman SM and Lotan Y: The cost of prostate cancer chemoprevention: a decision analysis model. Cancer Epidemiol Biomarkers Prev. 15:1485–1489. 2006. View Article : Google Scholar : PubMed/NCBI

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October 2014
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Copy and paste a formatted citation
APA
Guerrero-Preston, R., Ogawa, T., Uemura, M., Shumulinsky, G., Valle, B.L., Pirini, F. ... Trink, B. (2014). Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells. International Journal of Molecular Medicine, 34, 941-946. https://doi.org/10.3892/ijmm.2014.1849
MLA
Guerrero-Preston, R., Ogawa, T., Uemura, M., Shumulinsky, G., Valle, B. L., Pirini, F., Ravi, R., Sidransky, D., Keidar, M., Trink, B."Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells". International Journal of Molecular Medicine 34.4 (2014): 941-946.
Chicago
Guerrero-Preston, R., Ogawa, T., Uemura, M., Shumulinsky, G., Valle, B. L., Pirini, F., Ravi, R., Sidransky, D., Keidar, M., Trink, B."Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells". International Journal of Molecular Medicine 34, no. 4 (2014): 941-946. https://doi.org/10.3892/ijmm.2014.1849