Antitumor drug delivery in multicellular spheroids by electropermeabilization

Journal of Controlled Release

Volumn 167, Issue 2, 2013, Pages 138-147

  Gibot, Laure ^b   Wasungu, Luc ^b   Teissié, Justin ^b   Rols, Marie Pierre ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

3D; Bleomycin; Cisplatin; Doxorubicin; Electrochemotherapy; Electroporation

Indexed keywords

3D; BLEOMYCINS; CIS-PLATIN; DOXORUBICIN; ELECTROCHEMOTHERAPY; ELECTROPORATION;

CELL ADHESION; CELL DEATH; CELL MEMBRANES; DRUG DELIVERY; DRUG PRODUCTS; PEPTIDES; PLATINUM COMPOUNDS; THREE DIMENSIONAL COMPUTER GRAPHICS;

TUMORS;

BLEOMYCIN; CISPLATIN; DOXORUBICIN;

APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL ADHESION; CELL PERMEABILIZATION; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG POTENCY; DRUG SCREENING; ELECTROCHEMOTHERAPY; ELECTROPORATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MULTICELLULAR SPHEROID; PRIORITY JOURNAL; PROCESS OPTIMIZATION; TUMOR MODEL; TUMOR SPHEROID;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLEOMYCIN; CISPLATIN; COLORING AGENTS; DOXORUBICIN; DRUG DELIVERY SYSTEMS; ELECTROPORATION; HCT116 CELLS; HUMANS; PERMEABILITY; PROPIDIUM; SPHEROIDS, CELLULAR;

EID: 84874398633     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.01.021     Document Type: Article

References (56)

1. K. Kinosita Jr., and T.Y. Tsong Formation and resealing of pores of controlled sizes in human erythrocyte membrane Nature 268 1977 438 441
2. E. Neumann, and K. Rosenheck Permeability changes induced by electric impulses in vesicular membranes J. Membr. Biol. 10 1972 279 290
3. L.M. Mir, L.F. Glass, G. Sersa, J. Teissie, C. Domenge, D. Miklavcic, M.J. Jaroszeski, S. Orlowski, D.S. Reintgen, Z. Rudolf, M. Belehradek, R. Gilbert, M.P. Rols, J. Belehradek Jr., J.M. Bachaud, R. DeConti, B. Stabuc, M. Cemazar, P. Coninx, and R. Heller Effective treatment of cutaneous and subcutaneous malignant tumours by electrochemotherapy Br. J. Cancer 77 1998 2336 2342
4. G. Sersa, M. Cemazar, and M. Snoj Electrochemotherapy of solid tumors-preclinical and clinical experience 2011 IEEE Engineering in Medicine and Biology Society Conference pp. 728-731
5. M. Marty, G. Sersa, J.R. Garbay, J. Gehl, C.G. Collins, M. Snoj, V. Billard, P.F. Geertsen, J.O. Larkin, D. Miklavcic, I. Pavlovic, S.M. Paulin-Kosir, M. Cemazar, N. Morsli, D.M. Soden, Z. Rudolf, C. Robert, G.C. O'Sullivan, and L.M. Mir Electrochemotherapy - an easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study EJC Suppl. 4 2006 3 13
6. J. Gehl Electroporation for drug and gene delivery in the clinic: doctors go electric Methods Mol. Biol. 423 2008 351 359
7. T. Jarm, M. Cemazar, D. Miklavcic, and G. Sersa Antivascular effects of electrochemotherapy: implications in treatment of bleeding metastases Expert Rev. Anticancer Ther. 10 2010 729 746
8. L.W. Matthiessen, R.L. Chalmers, D.C. Sainsbury, S. Veeramani, G. Kessell, A.C. Humphreys, J.E. Bond, T. Muir, and J. Gehl Management of cutaneous metastases using electrochemotherapy Acta Oncol. 50 2011 621 629
9. Y. Tamzali, L. Borde, M.P. Rols, M. Golzio, F. Lyazrhi, and J. Teissie Successful treatment of equine sarcoids with cisplatin electrochemotherapy: a retrospective study of 48 cases Equine Vet. J. 44 2012 214 220
10. A.I. Daud, R.C. DeConti, S. Andrews, P. Urbas, A.I. Riker, V.K. Sondak, P.N. Munster, D.M. Sullivan, K.E. Ugen, J.L. Messina, and R. Heller Phase I trial of interleukin-12 plasmid electroporation in patients with metastatic melanoma J. Clin. Oncol. 26 2008 5896 5903
11. L. Low, A. Mander, K. McCann, D. Dearnaley, T. Tjelle, I. Mathiesen, F. Stevenson, and C.H. Ottensmeier DNA vaccination with electroporation induces increased antibody responses in patients with prostate cancer Hum. Gene Ther. 20 2009 1269 1278
12. S. Vasan, A. Hurley, S.J. Schlesinger, D. Hannaman, D.F. Gardiner, D.P. Dugin, M. Boente-Carrera, R. Vittorino, M. Caskey, J. Andersen, Y. Huang, J.H. Cox, T. Tarragona-Fiol, D.K. Gill, H. Cheeseman, L. Clark, L. Dally, C. Smith, C. Schmidt, H.H. Park, J.T. Kopycinski, J. Gilmour, P. Fast, R. Bernard, and D.D. Ho In vivo electroporation enhances the immunogenicity of an HIV-1 DNA vaccine candidate in healthy volunteers PLoS One 6 2011 e19252
13. M. Golzio, J.M. Escoffre, T. Portet, C. Mauroy, J. Teissie, D.S. Dean, and M.P. Rols Observations of the mechanisms of electromediated DNA uptake - from vesicles to tissues Curr. Gene Ther. 10 2010 256 266
14. J.M. Escoffre, T. Portet, C. Favard, J. Teissie, D.S. Dean, and M.P. Rols Electromediated formation of DNA complexes with cell membranes and its consequences for gene delivery Biochim. Biophys. Acta 1808 2011 1538 1543
15. G. Mazzoleni, D. Di Lorenzo, and N. Steimberg Modelling tissues in 3D: the next future of pharmaco-toxicology and food research? Genes Nutr. 4 2009 13 22
16. F. Pampaloni, E.G. Reynaud, and E.H. Stelzer The third dimension bridges the gap between cell culture and live tissue Nat. Rev. Mol. Cell Biol. 8 2007 839 845
17. T.T. Goodman, C.P. Ng, and S.H. Pun 3-D tissue culture systems for the evaluation and optimization of nanoparticle-based drug carriers Bioconjug. Chem. 19 2008 1951 1959
18. R.M. Sutherland Cell and environment interactions in tumor microregions: the multicell spheroid model Science 240 1988 177 184
19. I. Truchet, S. Jozan, S. Baron, C. Frongia, P. Balaguer, H. Richard-Foy, and A. Valette Estrogen and antiestrogen-dependent regulation of breast cancer cell proliferation in multicellular spheroids: influence of cell microenvironment Int. J. Oncol. 32 2008 1033 1039
20. L.A. Kunz-Schughart, J.A. Schroeder, M. Wondrak, F. van Rey, K. Lehle, F. Hofstaedter, and D.N. Wheatley Potential of fibroblasts to regulate the formation of three-dimensional vessel-like structures from endothelial cells in vitro Am. J. Physiol. Cell Physiol. 290 2006 C1385 C1398
21. T. Nederman, B. Norling, B. Glimelius, J. Carlsson, and U. Brunk Demonstration of an extracellular matrix in multicellular tumor spheroids Cancer Res. 44 1984 3090 3097
22. K.R. Stevens, K.L. Kreutziger, S.K. Dupras, F.S. Korte, M. Regnier, V. Muskheli, M.B. Nourse, K. Bendixen, H. Reinecke, and C.E. Murry Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue Proc. Natl. Acad. Sci. U. S. A. 106 2009 16568 16573
23. M. Vinci, S. Gowan, F. Boxall, L. Patterson, M. Zimmermann, W. Court, C. Lomas, M. Mendiola, D. Hardisson, and S.A. Eccles Advances in establishment and analysis of 3D tumour spheroid-based functional assays for target validation and drug evaluation BMC Biol. 10 2012 29
24. L. Wasungu, J.M. Escoffre, A. Valette, J. Teissie, and M.P. Rols A 3D in vitro spheroid model as a way to study the mechanisms of electroporation Int. J. Pharm. 379 2009 278 284
25. B. Marrero, and R. Heller The use of an in vitro 3D melanoma model to predict in vivo plasmid transfection using electroporation Biomaterials 33 2012 3036 3046
26. L.M. Mir, O. Tounekti, and S. Orlowski Bleomycin: revival of an old drug Gen. Pharmacol. 27 1996 745 748
27. O. Tounekti, A. Kenani, N. Foray, S. Orlowski, and L.M. Mir The ratio of single- to double-strand DNA breaks and their absolute values determine cell death pathway Br. J. Cancer 84 2001 1272 1279
28. Z.H. Siddik Cisplatin: mode of cytotoxic action and molecular basis of resistance Oncogene 22 2003 7265 7279
29. A. Gothelf, L.M. Mir, and J. Gehl Electrochemotherapy: results of cancer treatment using enhanced delivery of bleomycin by electroporation Cancer Treat. Rev. 29 2003 371 387
30. G. Sersa, M. Cemazar, and M. Snoj Electrochemotherapy of solid tumors - preclinical and clinical experience Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011 2011 728 731
31. A. Testori, G. Tosti, C. Martinoli, G. Spadola, F. Cataldo, F. Verrecchia, F. Baldini, M. Mosconi, J. Soteldo, I. Tedeschi, C. Passoni, C. Pari, A. Di Pietro, and P.F. Ferrucci Electrochemotherapy for cutaneous and subcutaneous tumor lesions: a novel therapeutic approach Dermatol. Ther. 23 2010 651 661
32. S. Kee, J. Gehl, and E. Lee Clinical Aspects of Electroporation 1st ed. 2011 Springer New-York
33. J.M. Kelm, N.E. Timmins, C.J. Brown, M. Fussenegger, and L.K. Nielsen Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types Biotechnol. Bioeng. 83 2003 173 180
34. L.W. Matthiessen, H.H. Johannesen, H.W. Hendel, T. Moss, C. Kamby, and J. Gehl Electrochemotherapy for large cutaneous recurrence of breast cancer: a phase II clinical trial Acta Oncol. 51 2012 713 721
35. A. Abbott Cell culture: biology's new dimension Nature 424 2003 870 872
36. E. Burdett, F.K. Kasper, A.G. Mikos, and J.A. Ludwig Engineering tumors: a tissue engineering perspective in cancer biology Tissue Eng. Part B Rev. 16 2010 351 359
37. P.J. Canatella, M.M. Black, D.M. Bonnichsen, C. McKenna, and M.R. Prausnitz Tissue electroporation: quantification and analysis of heterogeneous transport in multicellular environments Biophys. J. 86 2004 3260 3268
38. G. Pucihar, T. Kotnik, J. Teissie, and D. Miklavcic Electropermeabilization of dense cell suspensions Eur. Biophys. J. 36 2007 173 185
39. G. Pron, J. Belehradek Jr., and L.M. Mir Identification of a plasma membrane protein that specifically binds bleomycin Biochem. Biophys. Res. Commun. 194 1993 333 337
40. O. Tounekti, G. Pron, J. Belehradek Jr., and L.M. Mir Bleomycin, an apoptosis-mimetic drug that induces two types of cell death depending on the number of molecules internalized Cancer Res. 53 1993 5462 5469
41. M. Cemazar, M. Golzio, J.M. Escoffre, B. Couderc, G. Sersa, and J. Teissie In vivo imaging of tumor growth after electrochemotherapy with cisplatin Biochem. Biophys. Res. Commun. 348 2006 997 1002
42. H. Mekid, O. Tounekti, A. Spatz, M. Cemazar, F.Z. El Kebir, and L.M. Mir In vivo evolution of tumour cells after the generation of double-strand DNA breaks Br. J. Cancer 88 2003 1763 1771
43. S. Huerta, E.J. Goulet, S. Huerta-Yepez, and E.H. Livingston Screening and detection of apoptosis J. Surg. Res. 139 2007 143 156
44. L. Galluzzi, L. Senovilla, I. Vitale, J. Michels, I. Martins, O. Kepp, M. Castedo, and G. Kroemer Molecular mechanisms of cisplatin resistance Oncogene 31 2012 1869 1883
45. J.S. Lazo, S.M. Sebti, and J.H. Schellens Bleomycin Cancer Chemother. Biol. Response Modif. 16 1996 39 47
46. D.D. Von Hoff, M.W. Layard, P. Basa, H.L. Davis Jr., A.L. Von Hoff, M. Rozencweig, and F.M. Muggia Risk factors for doxorubicin-induced congestive heart failure Ann. Intern. Med. 91 1979 710 717
47. K. Chitcholtan, P.H. Sykes, and J.J. Evans The resistance of intracellular mediators to doxorubicin and cisplatin are distinct in 3D and 2D endometrial cancer J. Transl. Med. 10 2012 38
48. J. Gehl, T. Skovsgaard, and L.M. Mir Enhancement of cytotoxicity by electropermeabilization: an improved method for screening drugs Anticancer Drugs 9 1998 319 325
49. S. Orlowski, J. Belehradek Jr., C. Paoletti, and L.M. Mir Transient electropermeabilization of cells in culture. Increase of the cytotoxicity of anticancer drugs Biochem. Pharmacol. 37 1988 4727 4733
50. S. Meschini, M. Condello, P. Lista, B. Vincenzi, A. Baldi, G. Citro, G. Arancia, and E.P. Spugnini Electroporation adopting trains of biphasic pulses enhances in vitro and in vivo the cytotoxic effect of doxorubicin on multidrug resistant colon adenocarcinoma cells (LoVo) Eur. J. Cancer 48 2012 2236 2243
51. S.K. Frandsen, H. Gissel, P. Hojman, T. Tramm, J. Eriksen, and J. Gehl Direct therapeutic applications of calcium electroporation to effectively induce tumor necrosis Cancer Res. 72 2012 1336 1341
52. H.R. Mellor, L.A. Davies, H. Caspar, C.R. Pringle, S.C. Hyde, D.R. Gill, and R. Callaghan Optimising non-viral gene delivery in a tumour spheroid model J. Gene Med. 8 2006 1160 1170
53. L. Chopinet, L. Wasungu, and M.P. Rols First explanations for differences in electrotransfection efficiency in vitro and in vivo using spheroid model Int. J. Pharm. 423 2012 7 15
54. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
55. S. Zhu, D.A. Lee, and S. Li IL-12 and IL-27 sequential gene therapy via intramuscular electroporation delivery for eliminating distal aggressive tumors J. Immunol. 184 2010 2348 2354
56. B. Marrero, J.L. Messina, and R. Heller Generation of a tumor spheroid in a microgravity environment as a 3D model of melanoma, in vitro cellular & developmental biology Animal 45 2009 523 534