Synergistic effects of nanosecond pulsed electric fields combined with low concentration of gemcitabine on human oral squamous cell carcinoma in vitro

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Wang, Jing ^a   Guo, Jinsong ^a,b   Wu, Shan ^b   Feng, Hongqing ^b   Sun, Shujun ^b   Pan, Jie ^c   Zhang, Jue ^b   Beebe, Stephen J ^d  

^a LANZHOU UNIVERSITY   (China)

^b PEKING UNIVERSITY   (China)

^c PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^d OLD DOMINION UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; GEMCITABINE;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CELL ASSAY; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CLONOGENIC ASSAY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ELECTROCHEMOTHERAPY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUTH SQUAMOUS CELL CARCINOMA; NANOSECOND PULSED ELECTRIC FIELD; PULSED ELECTRIC FIELD; TRANSMISSION ELECTRON MICROSCOPY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DEOXYCYTIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION THERAPY; HUMANS; MOUTH NEOPLASMS; NECROSIS; NEOPLASM INVASIVENESS; TIME FACTORS;

EID: 84865304520     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043213     Document Type: Article

References (56)

1. Boyl P, Levin B (Eds) (2008) World Cancer Report. Lyon, France: IARC Press.
2. Jemal A, Siegel R, Xu JQ, Ward E, (2010) Cancer statistics, CA. Can J for Clin 60: 277-300.
3. Rhodus N, (2007) Oral Cancer: Early Detection and Prevention. Inside Dent 3: 1-9.
4. Petersen P, (2009) Oral cancer prevention and control - the approach of the World Health Organization. Oral Oncol 45: 454-460.
5. Chen YW, Liu JY, Lin ST, Li JM, Huang SH, et al. (2001) Proteomic analysis of gemcitabine-induced drug resistance in pancreatic cancer cells. Mol Biosyst 7: 3065-3074.
6. Galmarini C, Clarke M, Jordheim L, Santos C, Cros E, et al. (2004) Resistance to gemcitabine in a human follicular lymphoma cell line is due to partial deletion of the deoxycytidine kinase gene. BMC Pharm 4: 8.
7. Galmarini C, Mackey JR, Dumontet C, (2001) Nucleoside analogues: mechanisms of drug resistance and reversal strategies. Leukemia 15: 875-890.
8. Panesar K, (2011) Typical Drug Interactions in Oncology. US Pharmacist 36: 7-9.
9. Heller LC, Heller R (2011) Gene Electrotransfer to Tumor In Clinical Aspects of Electroporation. In Kee ST, Gehl J, Lee EW, editors. Clinical Aspects of Electroporation. Springer. pp. 159-164.
10. Davalos RV, Mir IL, Rubinsky B, (2005) Tissue ablation with irreversible electroporation. Ann Biomed Eng 33: 223-231.
11. Okino M, Mohri H, (1987) Effects of a high-voltage electrical impulse and an anticancer drug on in vivo growing tumors. Jpn J Cancer Res 78: 1319-1321.
12. Prausnitz MR, Bose VG, Langer R, Weaver JC, (1993) Electroporation of mammalian skin: A mechanism to enhance transdermal drug delivery. Proc Natl Acad Sci U S A 90: 10504-10508.
13. Mir LM, Orlowski S, (1999) Mechanisms of electrochemotherapy. Adv Drug Deliv Rev 35: 107-118.
14. Mir LM, (2008) Application of electroporation gene therapy: past, current, and future. Methods in Molec Biol 423: 3-17.
15. Hofmann GA, Dev SB, Dimmer S, Nanda GS, (1999) Electroporation therapy: a new approach for the treatment of head and neck cancer. IEEE Trans Biomed Eng 46: 752-759.
16. Dev SB, Rabussay DP, Widera G, Hofmann GA, (2000) Medical applications of electroporation. IEEE Trans on Plasma Sci 28: 206-223.
17. Burian M, Formanek M, Regele H, (2003) Electroporation therapy in head and neck cancer. Acta Otolaryngol 123: 264-268.
18. Landstrom FJ, Nilsson COS, Crafoord S, Reizenstein JA, Adamsson GBM, et al. (2010) Electroporation Therapy of Skin Cancer in the Head and Neck Area. Dermatol Surg 36: 1245-1250.
19. Sun C, Yao CG, Mi Y, Xiong L, Liao RJ, et al. (2004) Experimental study on irreversible electrical breakdown of tumor cell under steep pulsed electric fields. Conf Proc IEEE Eng Med Biol Soc 7: 5005-5008.
20. Schoenbach KH, Joshi RP, Kolb JF, Chen N, Stacey M, et al. (2004) Ultrashort electrical pulses open a new gateway into biological cells. Proc of the IEEE 92: 1122-1137.
21. Frey W, White JA, Price RO, Blackmore PF, Joshi RP, et al. (2006) Plasma membrane voltage changes during Nanosecond Pulsed Electric Field exposure. Biophys J 90: 8-15.
22. Gowrishankar TR, Weaver JC, (2006) Electrical behavior and pore accumulation in a multicellular model for conventional and supra-electroporation. Biochem Biophys Res Comm 394: 643-653.
23. Hu Q, Joshi RP, Schoenbach KH, (2005) Simulations of nanopore formation and phosphatidylserine externalization in lipid membranes subjected to a high-intensity, ultrashort electric pulse. Phys Rev E Stat Nonlin Soft Matter Phys 71: 031902.
24. Vernier PT, Ziegler MJ, Sun Y, Gundersen MA, Tieleman DP, (2006) Nanopore-facilitated, voltage-driven phosphatidylserine translocation in lipid bilayers-in cells and in silico. Phys Biol 3: 233-247.
25. Pakhomov AG, Bowman AM, Ibey BL, Andre FM, Pakhomova ON, et al. (2009) Lipid nanopores can form a stable, ion channel-like conduction pathway in cell membrane. Biochem Biophys Res Commun 385: 181-186.
26. Beebe SJ, Fox PM, Rec LJ, Willis EL, Schoenbach KH, (2003) Nanosecond, High intensity Pulsed Electric Fields induce apoptosis in human cells. FASEB J 17: 1493-1495.
27. Ren W, Beebe SJ, (2011) An apoptosis targeted stimulus with nanosecond pulsed electric fields (nsPEFs) in E4 squamous cell carcinoma. Apoptosis 16: 359-369.
28. Hall EH, Schoenbach KH, Beebe SJ, (2007) Nanosecond pulsed electric fields induce apoptosis in p53-wildtype and p53-null HCT116 colon carcinoma cells. Apoptosis 12: 1721-1731.
29. Beebe SJ, Fox PM, Rec LJ, Somers K, Stark RK, et al. (2002) Nanosecond Pulsed Electric Field (nsPEF) effects on cells and tissues: apoptosis induction and tumor growth inhibition. IEEE Trans Plasma Sci 30: 286-292.
30. Vernier PT, Li AM, Marcu L, Craft CM, Gundersen MA, (2003) Ultrashort pulsed electric fields induce membrane phospholipid translocation and caspase activation: differential sensitivities of Jurkat T lymphoblasts and rat glioma C6 cells. IEEE Trans on Dielect Elect Ins 10: 795-809.
31. Nuccitelli R, Pliquett U, Chen X, Ford F, Swanson JR, et al. (2006) Nanosecond pulsed electric fields cause melanomas to self-destruct. Biochem Biophys Res Commun 343: 351-360.
32. Chen X, Kolb JF, Swanson RJ, Schoenbach KH, Beebe SJ, (2010) Apoptosis initiation and angiogenesis inhibition: melanoma targets for nanosecond pulsed electric fields. Pigment Cell Melanoma Res 23: 554-556.
33. Chen X, Zhuang J, Kolb JF, Schoenbach KH, Beebe SJ, (2012) Long Term Survival of mice with Hepatocellular Carcinoma after Pulse Power Ablation with Nanosecond Pulsed Electric Fields. Technol Cancer Res Treat 11: 83-93.
34. Beebe SJ, White J, Blackmore PF, Deng YP, Somers K, et al. (2003) Diverse effects of nanosecond pulsed electric fields on cells and tissues. DNA Cell Biol 22: 785-796.
35. Vernier PT, Sun Y, Marcu L, Salemi S, Craft CM, et al. (2003) Calcium bursts induced by nanosecond electric pulses. Biochem Biophys Res Com 310: 286-295.
36. Buescher ES, Smith RR, Schoenbach KH, (2004) Submicrosecond intense pulsed electric field effects on intracellular free calcium: mechanisms and effects. IEEE Trans Plasma Sci 32: 1563-1572.
37. White JA, Blackmore PF, Schoenbach KH, Beebe SJ, (2004) Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields. J Biol Chem 79: 22964-22972.
38. Beebe SJ, Blackmore PF, White J, Joshi RP, Schoenbach KH, (2004) Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms. Physiol Meas 25: 1077-1093.
39. Spielmann M, Llombart CA, Kalla S, Espie M, Namer M, et al. (2001) Single agent gemcitabine is active in previously treated metastatic breast cancer. Oncology 60: 303-307.
40. Braakhuis BJ, van Dongen JA, Vermorken JB, Gordon BS, (1991) Preclinical in vivo activity of 2′, 2′-difluorodeoxycytidine (gemcitabine) against human head and neck cancer. Cancer Res 51: 211-214.
41. Carmichael J, (1995) The role of gemcitabine in the treatment of other tumours. Br J Cancer 8: 21-25.
42. Plunkett SW, Huang P, Xu YZ, Heinemann V, Grunewald R, et al. (1995) Gemcitabine: metabolism, mechanisms of action, and self-potentiation. Semin Oncol 2: 3-10.
43. Ueno H, Kiyosawa K, Kaniwa N, (2007) Pharmacogenomics of gemcitabine: can genetic studies lead to tailor-made therapy? Br J Cancer 7: 145-151.
44. Pauwels B, Korst AE, Lardon F, Vermorken JB, (2005) Combined Modality Therapy of Gemcitabine and Radiation. The Oncologist 10: 34-51.
45. Huang P, Plunkett PW, (1995) Induction of apoptosis by gemcitabine. Semin Oncol 22: 19-25.
46. LeBlanc AK, LaDue TA, Turrel KM, Klein MK, (2004) Unexpected toxicity following use of gemcitabine as a radiosensitizer in head and neck carcinomas: a veterinary radiation therapy oncology group pilot study. Vet Radiol Ultrasound 45: 466-470.
47. Wu Y, Aravind S, Ranganathan G, Martin A, Nalysnyk L, (2009) Anemia and thrombocytopenia in patients undergoing chemotherapy for solid tumors: a descriptive study of a large outpatient oncology practice database, 2000-2007. Clin Ther 31: 2416-2432.
48. Beebe SJ, Schoenbach KH, Heller R, (2010) Bioelectric Applications for Treatment of Melanoma. Cancers 2: 1731-1770.
49. Ford We, Ren W, Blackmore PF, Schoenbach KH, Beebe SJ, (2010) Nanosecond pulsed electric fields stimulate apoptosis without release of pro-apoptotic factors from mitochondria in B16f10 melanoma. Arch Biochem Biophys 497: 82-89.
50. Vernier PT, (2011) Mitochondrial membrane permeabilization with nanosecond electric pulses. Conf Proc IEEE Eng Med Biol Soc 2011: 743-745.
51. Stacey M, Stickley J, Fox P, Statler V, Schoenbach K, et al. (2003) Differential effects in cells exposed to ultra-short, high intensity electric fields: cell survival, DNA damage, and cell cycle analysis. Mutat Res 542: 65-75.
52. Ren W, Sain NM, Beebe SJ, (2012) Nanosecond Pulsed Electric Fields (nsPEFs) Activate Intrinsic Caspase-Dependent and Caspase-Independent Cell Death in Jurkat Cells. Biochem. Biophys Res Commun 421: 808-812.
53. Orrenius S, Zhivotovsky B, Nicotera P, (2003) Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4 (7):: 552-65.
54. Eguchi Y, Shimizu S, Tsujimoto Y, (1997) Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57 (10):: 1835-1840.
55. Lawrence TS, Davis MA, Hough A, Rehemtulla A, (2001) The Role of Apoptosis in 2′,2′-Difluoro-2′-deoxycytidine (Gemcitabine)-mediated Radiosensitization. Clin Cancer Res 7: 314-319.
56. Pauwels B, Korst AE, Lardon F, Vermorken JB, (2005) Combined modality therapy of gemcitabine and radiation. Oncologist 10 (1):: 34-51.