Low-temperature plasma treatment induces DNA damage leading to necrotic cell death in primary prostate epithelial cells

British Journal of Cancer

Volumn 112, Issue 9, 2015, Pages 1536-1545

  Hirst, A M ^a   Simms, M S ^b,c   Mann, V M ^b,c   Maitland, N J ^a   O'connell, D ^a   Frame, F M ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b CASTLE HILL HOSPITAL   (United Kingdom)

^c UNIVERSITY OF HULL   (United Kingdom)

Author keywords

low temperature plasma; necrosis; primary epithelial cells; prostate cancer; reactive species

Indexed keywords

HYDROGEN PEROXIDE; STAUROSPORINE; PLASMA GAS;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER THERAPY; CELL DEATH; CELL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DNA DAMAGE; HUMAN; HUMAN CELL; HUMAN TISSUE; LOW TEMPERATURE PLASMA; PLASMA GAS; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE EPITHELIUM CELL; CELL CULTURE; COLD; DRUG EFFECTS; EPITHELIUM CELL; MALE; METABOLISM; NECROSIS; PATHOLOGY; PHARMACOLOGY; PROSTATE; PROSTATIC NEOPLASMS; WESTERN BLOTTING;

APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; CELLS, CULTURED; COLD TEMPERATURE; DNA DAMAGE; EPITHELIAL CELLS; HUMANS; HYDROGEN PEROXIDE; MALE; NECROSIS; PLASMA GASES; PROSTATE; PROSTATIC NEOPLASMS;

EID: 84928769128     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2015.113     Document Type: Article

References (54)

1. Ahn HJ, Kim KI, Hoan NN, Kim CH, Moon E, Choi KS, Yang SS, Lee JS. (2014). Targeting cancer cells with reactive oxygen and nitrogen species generated by atmospheric-pressure air plasma. PLoS One 9: e86173
2. Bandyopadhyay U, Das D, Banerjee RK. (1999). Reactive oxygen species: oxidative damage and pathogenesis. Curr Sci 77: 658-666
3. Casiano CA, Ochs RL, Tan EM. (1998). Distinct cleavage products of nuclear proteins in apoptosis and necrosis revealed by autoantibody probes. Cell Death Differ 5: 183-190
4. Chang JW, Kang SU, Shin YS, Kim KI, Seo SJ, Yang SS, Lee JS, Moon E, Baek SJ, Lee K, Kim CH. (2014). Non-Thermal atmospheric pressure plasma induces apoptosis in oral cavity squamous cell carcinoma: Involvement of DNA-damage-Triggering sub-G(1) arrest via the ATM/p53 pathway Arch Biochem Biophys 545: 133-140
5. Chen MJ, Weltman E, Hanriot RM, Luz FP, Cecilio PJ, Da Cruz JC, Moreira FR, Santos AS, Martins LC, Nadalin W. (2007). Intensity modulated radiotherapy for localized prostate cancer: rigid compliance to dose-volume constraints as a warranty of acceptable toxicity? Radiat Oncol 2: 6
6. Cheng X, Sherman J, Murphy W, Ratovitski E, Canady J, Keidar M. (2014). The effect of tuning cold plasma composition on glioblastoma cell viability. PLoS One 9: e98652
7. Chu KF, Dupuy DE. (2014). Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer 14: 199-208
8. Cohen GM. (1997). Caspases: the executioners of apoptosis. Biochem J 326(Pt 1): 1-16
9. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951
10. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, Clarke MF. (2009). Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783
11. Donaldson IA, Alonzi R, Barratt D, Barret E, Berge V, Bott S, Bottomley D, Eggener S, Ehdaie B, Emberton M, Hindley R, Leslie T, Miners A, Mccartan N, Moore CM, Pinto P, Polascik TJ, Simmons L, Van Der Meulen J, Villers A, Willis S, Ahmed HU. (2014). Focal therapy: patients, interventions, and outcomes-A report from a consensus meeting. Eur Urol 67(4): 771-777
12. Frame FM, Pellacani D, Collins AT, Simms MS, Mann VM, Jones GD, Meuth M, Bristow RG, Maitland NJ. (2013). HDAC inhibitor confers radiosensitivity to prostate stem-like cells. Br J Cancer 109: 3023-3033
13. Francipane MG, Alea MP, Lombardo Y, Todaro M, Medema JP, Stassi G. (2008). Crucial role of interleukin-4 in the survival of colon cancer stem cells. Cancer Res 68: 4022-4025
14. Gibson AR, Mccarthy HO, Ali AA, Oconnell D, Graham WG. (2014). Interactions of a non-Thermal atmospheric pressure plasma effluent with PC-3 prostate cancer cells. Plasma Process Polym 11(12): 1142-1149
15. Gorrini C, Harris IS, Mak TW. (2013). Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov 12: 931-947
16. Graves DB. (2012). The emerging role of reactive oxygen and nitrogen species in redox biology and some implications for plasma applications to medicine and biology. J Phys D Appl Phys 45: 263001
17. Graves DB. (2014). Low temperature plasma biomedicine: a tutorial reviewa. Phys Plasmas 21: 080901
18. Gregory CD, Pound JD. (2010). Microenvironmental influences of apoptosis in vivo and in vitro. Apoptosis 15: 1029-1049
19. Guerrero-Preston R, Ogawa T, Uemura M, Shumulinsky G, Valle BL, Pirini F, Ravi R, Sidransky D, Keidar M, Trink B. (2014). Cold atmospheric plasma treatment selectively targets head and neck squamous cell carcinoma cells. Int J Mol Med 34: 941-946
20. Gulden M, Jess A, Kammann J, Maser E, Seibert H. (2010). Cytotoxic potency of H2O2 in cell cultures: impact of cell concentration and exposure time. Free Radic Biol Med 49: 1298-1305
21. Hirst AM, Frame FM, Maitland NJ, Oconnell D (2014) Low temperature plasma causes double-strand break DNA damage in primary epithelial cells cultured from a human prostate tumor. Plasma Sci IEEE Trans 42(10): 2740-2741
22. Hirst AM, Frame FM, Maitland NJ, Oconnell D (2014) Low temperature plasma: a novel focal therapy for localized prostate cancer? Biomed Res Int 2014: 878319
23. Ishaq M, Kumar S, Varinli H, Han ZJ, Rider AE, Evans MD, Murphy AB, 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
24. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. (2011). Global cancer statistics. CA Cancer J Clin 61: 69-90
25. Jones JS. (2011). Radiorecurrent prostate cancer: an emerging and largely mismanaged epidemic. Eur Urol 60: 411-412
26. Kang SU, Cho JH, Chang JW, Shin YS, Kim KI, Park JK, Yang SS, Lee JS, Moon E, Lee K, Kim CH. (2014). 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 5: e1056
27. Kasivisvanathan V, Emberton M, Ahmed HU. (2013). Focal therapy for prostate cancer: rationale and treatment opportunities. Clin Oncol (R Coll Radiol) 25: 461-473
28. Keidar M, Walk R, Shashurin A, Srinivasan P, Sandler A, Dasgupta S, Ravi R, Guerrero-Preston R, Trink B. (2011). Cold plasma selectivity and the possibility of a paradigm shift in cancer therapy. Br J Cancer 105: 1295-1301
29. Kepp O, Galluzzi L, Lipinski M, Yuan J, Kroemer G. (2011). Cell death assays for drug discovery. Nat Rev Drug Discov 10: 221-237
30. Kim H, Park BK, Kim CK. (2008). Spontaneous regression of pulmonary and adrenal metastases following percutaneous radiofrequency ablation of a recurrent renal cell carcinoma. Korean J Radiol 9: 470-472
31. Kim JY, Ballato J, Foy P, Hawkins T, Wei Y, Li J, Kim SO. (2011). Apoptosis of lung carcinoma cells induced by a flexible optical fiber-based cold microplasma. Biosens Bioelectron 28: 333-338
32. Knake N, Niemi K, Reuter S, Schulz-Von Der Gathen V, Winter J. (2008). Absolute atomic oxygen density profiles in the discharge core of a microscale atmospheric pressure plasma jet. Appl Phys Lett 93: 131503-131503
33. Krzykawska-Serda M, Dabrowski JM, Arnaut LG, Szczygiel M, Urbanska K, Stochel G, Elas M. (2014). The role of strong hypoxia in tumors after treatment in the outcome of bacteriochlorin-based photodynamic therapy. Free Radic Biol Med 73C: 239-251
34. Lips IM, Dehnad H, Van Gils CH, Boeken Kruger AE, Van Der Heide UA, Van Vulpen M. (2008). High-dose intensity-modulated radiotherapy for prostate cancer using daily fiducial marker-based position verification: acute and late toxicity in 331 patients. Radiat Oncol 3: 15
35. Ma Y, Ha CS, Hwang SW, Lee HJ, Kim GC, Lee KW, Song K. (2014). Nonthermal atmospheric pressure plasma preferentially induces apoptosis in p53-mutated cancer cells by activating ROS stress-response pathways. PLoS One 9: e91947
36. Melcher A, Gough M, Todryk S, Vile R. (1999). Apoptosis or necrosis for tumor immunotherapy: whats in a name? J Mol Med (Berl) 77: 824-833
37. Murakami T, Niemi K, Gans T, Oconnell D, Graham WG. (2013). Chemical kinetics and reactive species in atmospheric pressure helium-oxygen plasmas with humid-Air impurities. Plasma Sources Sci Technol 22: 015003
38. Niemi K, Oconnell D, Oliveira DE, Joyeux N, Nahon D, Booth L, Gans, T. JP. (2013). Absolute atomic oxygen and nitrogen densities in radio-frequency driven atmospheric pressure cold plasmas: synchrotron vacuum ultraviolet high-resolution Fourier-Transform absorption measurements. Appl Phys Lett 103: 034102
39. Ninomiya K, Ishijima T, Imamura M, Yamahara T, Enomoto H, Takahashi K, Tanaka Y, Uesugi Y, Shimizu N. (2013). 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 46: 425401
40. Palacios DA, Miyake M, Rosser CJ. (2013). Radiosensitization in prostate cancer: mechanisms and targets. BMC Urol 13: 4
41. Plewa JM, Yousfi M, Frongia C, Eichwald O, Ducommun B, Merbahi N, Lobjois V. (2014). Low-Temperature plasma-induced antiproliferative effects on multi-cellular tumor spheroids. N J Phys 16: 043027
42. Robert E, Vandamme M, Brullé L, Lerondel S, Le Pape A, Sarron V, Riés D, Darny T, Dozias S, Collet G, Kieda C, Pouvesle JM. (2013). Perspectives of endoscopic plasma applications. Clin Plasma Med 1: 8-16
43. Sanchez-Ortiz RF, Tannir N, Ahrar K, Wood CG. (2003). Spontaneous regression of pulmonary metastases from renal cell carcinoma after radio frequency ablation of primary tumor: an in situ tumor vaccine? J Urol 170: 178-179
44. Sharman WM, Allen CM, Van Lier JE. (1999). Photodynamic therapeutics: basic principles and clinical applications. Drug Discov Today 4: 507-517
45. Sousa JS, Niemi K, Cox LJ, Algwari QT, Gans T, Oconnell D. (2011). Cold atmospheric pressure plasma jets as sources of singlet delta oxygen for biomedical applications. J Appl Phys 109: 123302
46. Sturmey RG, Hawkhead JA, Barker EA, Leese HJ. (2009). DNA damage and metabolic activity in the preimplantation embryo. Hum Reprod 24: 81-91
47. Sullivan KF, Crawford ED. (2009). Targeted focal therapy for prostate cancer: a review of the literature. Ther Adv Urol 1: 149-159
48. Vandamme M, Robert E, Lerondel S, Sarron V, Ries D, Dozias S, Sobilo J, Gosset D, Kieda C, Legrain B, Pouvesle JM, Pape AL. (2012). ROS implication in a new antitumor strategy based on non-Thermal plasma. Int J Cancer 130: 2185-2194
49. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. (1997). Immunosuppressive effects of apoptotic cells. Nature 390: 350-351
50. Wagenaars E, Gans T, Oconnell D, Niemi K. (2012). Two-photon absorption laser-induced fluorescence measurements of atomic nitrogen in a radio-frequency atmospheric-pressure plasma jet. Plasma Sources Sci Technol 21: 042002
51. Wang M, Holmes B, Cheng X, Zhu W, Keidar M, Zhang LG. (2013). Cold atmospheric plasma for selectively ablating metastatic breast cancer cells. PLoS One 8: e73741
52. Waskoenig J, Niemi K, Knake N, Graham LM, Reuter S, Schulz-Von Der Gathen V, Gans T. (2010). Atomic oxygen formation in a radio-frequency driven micro-Atmospheric pressure plasma jet. Plasma Sources Sci Technol 19: 045018
53. Wiseman H, Halliwell B. (1996). Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J 313(Pt 1): 17-29
54. Woo JA, Chen LN, Bhagat A, Oermann EK, Kim JS, Moures R, Yung T, Lei S, Collins BT, Kumar D, Suy S, Dritschilo A, Lynch JH, Collins SP. (2014). Clinical characteristics and management of late urinary symptom flare following stereotactic body radiation therapy for prostate cancer. Front Oncol 4: 122