The Effect of Millisecond Pulsed Electric Fields (msPEF) on Intracellular Drug Transport with Negatively Charged Large Nanocarriers Made of Solid Lipid Nanoparticles (SLN): In Vitro Study

Journal of Membrane Biology

Volumn 249, Issue 5, 2016, Pages 645-661

  Kulbacka, Julita ^a   Pucek, Agata ^b   Wilk, Kazimiera Anna ^b   Dubińska Magiera, Magda ^c   Rossowska, Joanna ^d   Kulbacki, Marek ^e   Kotulska, Małgorzata ^b  

^a WROCLAW MEDICAL UNIVERSITY   (Poland)

^b WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^c UNIVERSITY OF WROC AW   (Poland)

^d INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^e POLISH JAPANESE INSTITUTE OF INFORMATION TECHNOLOGY   (Poland)

Author keywords

Coumarin 6; Drug delivery; Electroporation; Millisecond pulsed electric field; Solid lipid nanocarriers

Indexed keywords

ALPHA ACTIN; BETA TUBULIN; COUMARIN 6; COUMARIN DERIVATIVE; CYTOSKELETON PROTEIN; FLUORESCENT DYE; NANOCARRIER; SOLID LIPID NANOPARTICLE; UNCLASSIFIED DRUG; DRUG CARRIER; LIPID; NANOPARTICLE; THIAZOLE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; COLORECTAL CANCER CELL LINE; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; DRUG TRANSPORT; ELECTROPORATION; FEMALE; FLUORESCENCE MICROSCOPY; HAMSTER OVARIAN FIBROBLASTOID CHO K1 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR TRANSPORT; LOVO CANCER CELL LINE; MILLISECOND PULSED ELECTRIC FIELD; NANOENCAPSULATION; NANOPHARMACEUTICS; NONHUMAN; OVARY CELL; PULSED ELECTRIC FIELD; ANIMAL; CELL LINE; CELL SURVIVAL; CHEMICAL STRUCTURE; CHEMISTRY; DIFFERENTIAL SCANNING CALORIMETRY; DRUG DELIVERY SYSTEM; FLOW CYTOMETRY; METABOLISM; PARTICLE SIZE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CALORIMETRY, DIFFERENTIAL SCANNING; CELL LINE; CELL SURVIVAL; COUMARINS; CYTOSKELETON; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; ELECTROPORATION; FLOW CYTOMETRY; HUMANS; LIPIDS; MICROSCOPY, FLUORESCENCE; MOLECULAR STRUCTURE; NANOPARTICLES; PARTICLE SIZE; THIAZOLES;

EID: 84966712916     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-016-9906-1     Document Type: Article

References (80)

1. Aihara H, Miyazaki J (1998) Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 16(9):867–870
2. Bazylińska U, Pietkiewicz J, Saczko J, Nattich-Rak M, Rossowska J, Garbiec A, Wilk KA (2012) Nanoemulsion-templated multilayer nanocapsules for cyanine-type photosensitizer delivery to human breast carcinoma cells. Eur J Pharm Sci 47:406–420
3. Bazylińska U, Kulbacka J, Wilk KA (2014a) Dicephalic ionic surfactants in fabrication of biocompatible nanoemulsions: factors influencing droplet size and stability. Colloids Surf A: Physicochem Eng Asp 460:312–320
4. Bazylińska U, Pucek A, Sowa M, Matczak-Jon E, Wilk KA (2014b) Engineering of phosphatidylcholine-based solid lipid nanocarriers for flavonoids delivery. Colloids Surf A: Physicochem Eng Asp 460:483–493
5. Born SL, Hu JK, Lehman-McKeeman LD (2000) o-hydroxyphenylacetaldehyde is a hepatotoxic metabolite of coumarin. Drug Metab Dispos 28(2):218–223
6. Cadossi R, Ronchetti M, Cadossi M (2014) Locally enhanced chemotherapy by electroporation: clinical experiences and perspective of use of electrochemotherapy. Future Oncol 10(5):877–890
7. Calderón-Colón X, Raimondi G, Benkoski JJ, Patrone JB (2015) Solid lipid nanoparticles (SLNs) for intracellular targeting applications. J Vis Exp. doi:10.3791/53102
8. Campana LG, Galuppo S, Valpione S, Brunello A, Ghiotto C, Ongaro A, Rossi CR (2014) Bleomycin electrochemotherapy in elderly metastatic breast cancer patients: clinical outcome and management considerations. J Cancer Res Clin Oncol 140(9):1557–1565
9. Casadei MA, Cerreto F, Cesa S, Giannuzzo M, Feeney M, Marianecci C, Paolicelli P (2006) Solid lipid nanoparticles incorporated in dextran hydrogels: a new drug delivery system for oral formulations. Int J Pharm 325:140–146
10. Čemažar M, Miklavcic D, Sersa G (1998a) Intrinsic sensitivity of tumor cells to bleomycin as an indicator of tumor response to electrochemotherapy. Jpn J Cancer Res 89(3):328–333
11. Čemažar M, Sersa G, Miklavcic D (1998b) Electrochemotherapy with cisplatin in the treatment of tumor cells resistant to cisplatin. Anticancer Res 18(6A):4463–4466
12. Čemažar M, Sersa G, Wilson J, Tozer GM, Hart SL, Grosel A, Dachs GU (2002) Effective gene transfer to solid tumors using different nonviral gene delivery techniques: electroporation, liposomes, and integrin-targeted vector. Cancer Gene Ther 9(4):399–406
13. Chuang JY, Huang YF, Lu HF, Ho HC, Yang JS, Li TM, Chang NW, Chung JG (2007) Coumarin induces cell cycle arrest and apoptosis in human cervical cancer HeLa cells through a mitochondria- and caspase-3 dependent mechanism and NF-kappaB down-regulation. In Vivo 21(6):1003–1009
14. Colacino KR, Arena CB, Dong S, Roman M, Davalos RV, Lee YW (2014) Folate conjugated cellulose nanocrystals potentiate irreversible electroporation-induced cytotoxicity for the selective treatment of cancer cells. Technol Cancer Res Treat (Epub ahead of print; PubMed PMID: 24750004)
15. Davalos RV, Mir IL, Rubinsky B (2005) Tissue ablation with irreversible electroporation. Ann Biomed Eng 33(2):223–231
16. Delemotte L, Tarek M (2012) Molecular dynamics simulations of lipid membrane electroporation. J Membr Biol 245(9):531–543
17. Dimitrov DS (1995) Electroporation and electrofusion of membranes, Chap. 18. In: Sackmann E, Lipowsky R (eds) Handbook of physics of biological systems, structure and dynamics of membranes, vol 1b. Elsevier, Amsterdam, pp 852–901
18. Emr BM, Roy S, Kollisch-Singule M, Gatto LA, Barravecchia M, Lin X, Young JL, Wang G, Liu J, Satalin J, Snyder K, Nieman GF, Dean DA (2014) Electroporation Mediated Gene Delivery of Na+, K+-ATPase and ENaC subunits to the lung attenuates acute respiratory distress syndrome in a two-hit porcine model. Shock (Epub ahead of print; PubMed PMID: 25004064)
19. Fathi M, Varshosaz J, Mohebbi M, Shahidi F (2013) Hesperetin-loaded solid lipid nanoparticles and nanostructure lipid carriers for food fortification: preparation, characterization, and modeling. Food Bioproc Technol 6:1464–1475
20. Faurie C, Golzio M, Moller P, Teissié J, Rols MP (2003) Cell and animal imaging of electrically mediated gene transfer. DNA Cell Biol 22(12):777–783
21. Forde PF, Sadadcharam M, Hall LJ, O’ Donovan TR, de Kruijf M, Byrne WL, O’ Sullivan GC, Soden DM (2014) Enhancement of electroporation facilitated immunogene therapy via T-reg depletion. Cancer Gene Ther 21(8):349–354
22. Gamper N, Stockand JD, Shapiro MS (2005) The use of Chinese hamster ovary (CHO) cells in the study of ion channels. J Pharmacol Toxicol Meth 51(3):177–185
23. Gehl J (2014) Gene electrotransfer in clinical trials. Methods Mol Biol 1121:241–246
24. Gibot L, Rols MP (2015) Gene transfer by pulsed electric field is highly promising in cutaneous wound healing. Expert Opin Biol Ther. 29:1–11
25. Gilbert R, Jaroszeski MJ, Heller L, Heller R (2002) Electric field enhanced plasmid delivery to liver hepatocellular carcinomas. Technol Cancer Res Treat 1(5):355–364
26. Heller R (2002) Overview of electroporation. Technol Cancer Res Treat 1(5):317–318
27. Heller LC, Heller R (2010) Electroporation gene therapy preclinical and clinical trials for melanoma. Curr Gene Ther 10(4):312–317
28. Heller R, Jaroszeski M, Atkin A, Moradpour D, Gilbert R, Wands J, Nicolau C (1996) In vivo gene electroinjection and expression in rat liver. FEBS Lett 389(3):225–228
29. Heller R, Schultz J, Lucas ML, Jaroszeski MJ, Heller LC, Gilbert RA, Moelling K, Nicolau C (2001) Intradermal delivery of interleukin-12 plasmid DNA by in vivo electroporation. DNA Cell Biol 20(1):21–26
30. (Erratum in: DNA Cell Biol; 20(6): 381)
31. Heller LC, Ugen K, Heller R (2005) Electroporation for targeted gene transfer. Expert Opin Drug Deliv 2(2):255–268
32. Henri P, Ospital R, Teissié J (2015) Content delivery of lipidic nanovesicles in electropermeabilized cells. J Membr Biol 248(5):849–855
33. Hu J, Li S (2014) Electroporation formulation for cell therapy. Methods Mol Biol 1121:55–60
34. Huang S, Deshmukh H, Rajagopalan KK, Wang S (2014) Gold nanoparticles electroporation enhanced polyplex delivery to mammalian cells. Electrophoresis 35(12–13):1837–1845
35. Interactive 3D Surface Plot. http://rsb.info.nih.gov/ij/plugins/surface-plot-3d.html, 2004/11/19 (V1.0): first version; 2015/10/19 (V2.4): last version
36. Jaroszeski MJ, Gilbert R, Heller R (1995) Cytometric detection and quantitation of cell-cell electrofusion products. Methods Mol Biol 48:355–363
37. Jaroszeski MJ, Gilbert R, Nicolau C, Heller R (1999) In vivo gene delivery by electroporation. Adv Drug Deliv Rev 35(1):131–137
38. Jaroszeski MJ, Gilbert R, Nicolau C, Heller R (2000) Delivery of genes in vivo using pulsed electric fields. Methods Mol Med 37:173–186
39. Jaroszeski MJ, Heller LC, Gilbert R, Heller R (2004) Electrically mediated plasmid DNA delivery to solid tumors in vivo. Methods Mol Biol 245:237–244
40. Kalli C, Teoh WC, Leen E (2014) Introduction of genes via sonoporation and electroporation. Adv Exp Med Biol 818:231–254
41. Kee ST, Gehl J, Lee EW (2011) Clinical aspects of electroporation, 1st edn. Springer, New York
42. Kim JA, Lee WG (2011) Role of weakly polarized nanoparticles in electroporation. Nanoscale 3(4):1526–1532
43. Kulbacka J, Daczewska M, Dubińska-Magiera M, Choromańska A, Rembiałkowska N, Surowiak P, Kulbacki M, Kotulska M, Saczko J (2014) Doxorubicin delivery enhanced by electroporation to gastrointestinal adenocarcinoma cells with P-gp overexpression. Bioelectrochemistry 100:96–104
44. Lai SK, O’Hanlon DE, Harrold S, Man ST, Wang YY, Cone R, Hanes J (2007) Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proc Natl Acad Sci USA 104(5):1482–1487. doi:10.1073/pnas.0608611104
45. ® Delivery. Cytotoxicity and Pro-apoptotic Activity in Human Breast and Ovarian Cancer Cells, Photodiag Photodyn Ther 11(4):570–585
46. Lima AM, Pizzol CD, Monteiro Fabíola BF, Creczynski-Pasa Tânia B, Andrade Gislaine P, Ribeiro Anderson O, Perussi Janice R (2013) Hypericin encapsulated in solid lipid nanoparticles: phototoxicity and photodynamic efficiency. J Photochem Photobiol B: Biology 125:146–154
47. Liu Y-C, Wu P-C, Shieh D-B, Wu S-N (2012) The effects of magnetite (Fe3O4) nanoparticles on electroporation-induced inward currents in pituitary tumor (GH3) cells and in RAW 264.7 macrophages. Int J Nanomed 7:1687–1696
48. Ma YM, Zhou YB, Xie CM, Chen DM, Li J (2012) Novel microtubule-targeted agent 6-chloro-4-(methoxyphenyl) coumarin induces G2-M arrest and apoptosis in HeLa cells. Acta Pharmacol Sin 33(3):407–417
49. Makhlof A, Werle M, Tozuka Y, Takeuchi H (2011) A mucoadhesive nanoparticulate system for the simultaneous delivery of macromolecules and permeation enhancers to the intestinal mucosa. J Control Release 149:81–88
50. McGregor DB, Edwards I, Wolf CR, Forrester LM, Caspary WJ (1991) Endogenous xenobiotic enzyme levels in mammalian cells. Mutat Res 261(1):29–39
51. Mehnert W, Mader K (2001) Solid lipid nanoparticles—production, characterization and application. Adv Drug Deliv Rev 47:165–196
52. Miklavčič D, Mali B, Kos B, Heller R, Serša G (2014) Electrochemotherapy: from the drawing board into medical practice. Biomed Eng Online 13(1):29
53. Mir LM (2014) Electroporation-based gene therapy: recent evolution in the mechanism description and technology developments. Methods Mol Biol 1121:3–23
54. Mir LM, Orlowski S, Poddevin B, Belehradek J Jr (1992) Electrochemotherapy tumor treatment is improved by interleukin-2 stimulation of the host’s defenses. Eur Cytokine Netw 3(3):331–334
55. Mir LM, Morsli N, Garbay JR, Billard V, Robert C, Marty M (2003) Electrochemotherapy: a new treatment of solid tumors. J Exp Clin Cancer Res 22(4 Suppl):145–148
56. Miyazaki J, Aihara H (2002) Gene transfer into muscle by electroporation in vivo. Methods Mol Med 69:49–62
57. de Morais MG, Martins VG, Steffens D, Pranke P, da Costa JA (2014) Biological applications of nanobiotechnology. J Nanosci Nanotechnol 14(1):1007–1017
58. Müller RH, Mäder K, Gohla S (2000) Solid lipid nanoparticles (SLN) for controlled drug delivery—a review of the state of the art. Eur J Pharma Biopharma 50(1):161–177
59. Müller RH, Jacobs C, Kayser O (2001) Nanosuspensions as particulate drug formulations in therapy. Rationale for development and what we can expect for the future. Adv Drug Deliv Rev 47(1):3–19
60. Orio J, Bellard E, Baaziz H, Pichon C, Mouritzen P, Rols MP, Teissié J, Golzio M, Chabot S (2013) Sub-cellular temporal and spatial distribution of electrotransferred LNA/DNA oligomer. J RNAi Gene Silenc 9:479–485 (eCollection 2013)
61. Paliwal R, Babu RJ, Palakurthi S (2014) Nanomedicine scale-up technologies: feasibilities and challenges. AAPS PharmSciTech 15(6):1527–1534
62. Puglia C, Damiani E, Offerta A, Rizza L, Tirendi GG, Tarico MS, Curreri S, Bonina F, Perrotta RE (2014) Evaluation of nanostructured lipid carriers (NLC) and nanoemulsions as carriers for UV-filters: characterization, in vitro penetration and photostability studies. Eur J Pharm Sci 51:211–217
63. Ramos C, Bonato D, Winterhalter M, Stegmann T, Teissie J (2002) Spontaneous lipid vesicle fusion with electropermeabilized cells. FEBS Lett 518(1–3):135–138
64. Rols MP, Delteil C, Golzio M, Dumond P, Cros S, Teissie J (1998) In vivo electrically mediated protein and gene transfer in murine melanoma. Nat Biotechnol 16(2):168–171
65. Saadeh Y, Leung T, Vyas A, Chaturvedi LS, Perumal O, Vyas D (2014) Applications of nanomedicine in breast cancer detection, imaging, and therapy. J Nanosci Nanotechnol 14(1):913–923
66. Saczko J, Kamińska I, Kotulska M, Bar J, Choromańska A, Rembiałkowska N, Bieżuńska-Kusiak K, Rossowska J, Nowakowska D, Kulbacka J (2014) Combination of therapy with 5-fluorouracil and cisplatin with electroporation in human ovarian carcinoma model in vitro. Biomed Pharmacother 68(5):573–580
67. Sersa G, Stabuc B, Cemazar M, Jancar B, Miklavcic D, Rudolf Z (1998) Electrochemotherapy with cisplatin: potentiation of local cisplatin antitumour effectiveness by application of electric pulses in cancer patients. Eur J Cancer 34(8):1213–1218
68. Sersa G, Miklavcic D, Cemazar M, Rudolf Z, Pucihar G, Snoj M (2008) Electrochemotherapy in treatment of tumours. Eur J Surg Oncol 34(2):232–240
69. Sersa G, Cemazar M, Snoj M (2009) Electrochemotherapy of tumours. Curr Oncol. 16(2):34–35
70. Szczepanowicz K, Bazylińska U, Pietkiewicz J, Szyk-Warszyńska L, Wilk KA, Warszyński P (2014) Biocompatible long-sustained release oil-core polyelectrolyte nanocarriers: from controlling physical state and stability to biological impact, Adv Colloid Interface Sci (pii: S0001-8686(14)00278-4)
71. Takei Y (2014) Electroporation-mediated siRNA delivery into tumors. Methods Mol Biol 1121:131–138
72. Tran TH, Ramasamy T, Truong DH, Choi HG, Yong CS, Kim JO (2014) Preparation and characterization of fenofibrate-loaded nanostructured lipid carriers for oral bioavailability enhancement. AAPS PharmSciTech 15(6):1509–1515
73. Ugen KE, Heller R (2003) Electroporation as a method for the efficient in vivo delivery of therapeutic genes. DNA Cell Biol 22(12):753
74. Vásquez JL, Ibsen P, Lindberg H, Gehl J (2014) In vitro and in vivo experiments on electrochemotherapy for bladder cancer. J Urol (pii: S0022-5347(14)04435-8)
75. Wezgowiec J, Derylo MB, Teissie J, Orio J, Rols MP, Kulbacka J, Saczko J, Kotulska M (2013) Electric field-assisted delivery of photofrin to human breast carcinoma cells. J Memb Biol 246(10):725–735
76. Wissing SA, Kayser O, Müller RH (2004) Solid lipid nanoparticles for parenteral drug delivery. Adv Drug Del Rev 56:1257–1272
77. Yarmush ML, Golberg A, Serša G, Kotnik T, Miklavčič D (2014) Electroporation-based technologies for medicine: principles, applications, and challenges. Annu Rev Biomed Eng 16:295–320
78. Yu Y, Lin J, Huang Z, Xi G, Lin D, Chen Y, Chen R, Zeng H (2011) Improved electroporation parameters of delivering silver nanoparticles into living C666 cells for surface-enhanced Raman scattering. J Phys: Conf Ser 277:012045
79. Zou M, De Koninck P, Neve RL, Friedrich RW (2014) Fast gene transfer into the adult zebrafish brain by herpes simplex virus 1 (HSV-1) and electroporation: methods and optogenetic applications. Front Neural Circuits 8:41. doi:10.3389/fncir.2014.00041
80. Zu Y, Huang S, Liao WC, Lu Y, Wang S (2014) Gold nanoparticles enhanced electroporation for mammalian cell transfection. J Biomed Nanotechnol 10(6):982–992