Therapeutic ultrasound promotes plasmid DNA uptake by clathrin-mediated endocytosis

Journal of Gene Medicine

Volumn 13, Issue 7-8, 2011, Pages 392-401

  de Paula, Daisy Maria Bentes ^a   Valero Lapchik, Valderez Bastos ^a   Paredes Gamero, Edgar Julian ^a   Han, Sang Won ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Calcium influx; Clathrin; Endocytosis; Plasmid uptake; ROS generation; Ultrasound

Indexed keywords

CALCIUM; CAVEOLIN 1; CLATHRIN; FLUORESCENT DYE; PLASMID DNA; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE POTENTIAL; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ECHOGRAPHY; ENDOCYTOSIS; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; NONVIRAL GENE THERAPY; PRIORITY JOURNAL;

ANIMALS; CALCIUM; CLATHRIN; DNA; ENDOCYTOSIS; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MEMBRANE POTENTIALS; MICE; NIH 3T3 CELLS; PLASMIDS; PROTEIN BINDING; REACTIVE OXYGEN SPECIES; ULTRASONIC THERAPY;

EID: 79960858872     PISSN: 1099498X     EISSN: 15212254     Source Type: Journal    
DOI: 10.1002/jgm.1586     Document Type: Article

References (40)

1. Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 2003; 4: 346-358.
2. Kootstra NA, Verma IM. Gene therapy with viral vectors. Annu Rev Pharmacol Toxicol 2003; 43: 413-439.
3. Nayak S, Herzog RW. Progress and prospects: immune responses to viral vectors. Gene Ther 2010; 17: 295-304.
4. Mintzer MA, Simanek EE. Nonviral vectors for gene delivery. Chem Rev 2009; 109: 259-302.
5. Li SD, Huang L. Gene therapy progress and prospects: non-viral gene therapy by systemic delivery. Gene Ther 2006; 13: 1313-1319.
6. Fechheimer M, Boylan J, Parker S, Sisken J, Patel G, Zimmer S. Transfection of mammalian cells with plasmid DNA by scrape loading and sonication loading. Proc Natl Acad Sci USA 1987; 84: 8463-8467.
7. Joersbo M, Brunstedt J. Protein synthesis stimulated in sonicated sugar beet cells and protoplasts. Ultrasound Med Biol 1990; 16: 719-724.
8. Huber PE, Pfisterer P. In vitro and in vivo transfection of plasmid DNA in the Dunning prostate tumor R3327-AT1 is enhanced by focused ultrasound. Gene Ther 2000; 7: 1516-1525.
9. Lawrie A, Brisken AF, Francis SE, et al. Ultrasound enhances reporter gene expression after transfection of vascular cells in vitro. Circulation 1999; 99: 2617-2620.
10. Larina LV, Evers BM, Esenaliev RO. Optimal drug and gene delivery in cancer cells by ultrasound-induced cavitation. Anticancer Res 2005; 25: 149-156.
11. Liang HD, Lu QL, Xue SA, et al. Optimization of ultrasound-mediated gene transfer (sonoporation) in skeletal muscle cells. Ultrasound Med Biol 2004; 30: 1523-1529.
12. Baker KG, Robertson VJ, Duck FA. A review of therapeutic ultrasound: biophysical effects. Phys Ther 2001; 81: 1351-1358.
13. Schlicher RK, Radhakrishna H, Tolentino TP, Apkarian RP, Zarnitsyn V, Prausnitz MR. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med Biol 2006; 32: 915-924.
14. Tachibana K, Uchida T, Ogawa K, Yamashita N, Tamura K. Induction of cell-membrane porosity by ultrasound. Lancet 1999; 353: 1409.
15. Mehier-Humbert S, Bettinger T, Yan F, Guy RH. Ultrasound-mediated gene delivery: kinetics of plasmid internalization and gene expression. J Control Release 2005; 104: 203-211.
16. Duvshani-Eshet M, Baruch L, Kesselman E, Shimoni E, Machluf M. Therapeutic ultrasound-mediated DNA to cell and nucleus: bioeffects revealed by confocal and atomic force microscopy. Gene Ther 2006; 13: 163-172.
17. Schweizer FE, Ryan TA. The synaptic vesicle: Cycle of exocytosis and endocytosis. Curr Opin Neurobiol 2006; 16: 298-304.
18. Henkel AW, Almers W. Fast steps in exocytosis and endocytosis studied by capacitance measurements in endocrine cells. Curr Opin Neurobiol 1996; 6: 350-357.
19. MacDonald PE, Eliasson L, Rorsman P. Calcium increases endocytotic vesicle size and accelerates membrane fission in insulin-secreting INS-1 cells. J Cell Sci 2005; 118: 5911-5920.
20. Meijering BDM, Juffermans LJM, Van Wamel A, et al. Ultrasound and Microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ Res 2009; 104: 679-687.
21. Carvalho LP, Takeshita D, Carillo B, et al. Hydrodynamics- and ultrasound-based transfection of heart with naked plasmid DNA. Hum Gene Ther 2007; 18: 1233-1243.
22. Montana V, Farkas DL, Loew LM. Dual-wavelength ratiometric fluorescence measurements of membrane potencial. Biochemistry 1989; 28: 4536-4539.
23. McGahren ED, Beach JM, Duling BR. Capillaries demonstrate changes in membrane potential in response to pharmacological stimuli. Am J Physiol 1998; 274: 60-65.
24. Deng CX, Sieling F, Pan H, Cui J. Ultrasound-induced cell membrane porosity. Ultrasound Med Biol 2004; 30: 519-526.
25. Lionetti V, Fittipaldi A, Agostini S, Giacca M, Recchia FA, Picano E. Enhanced caveolae-mediated endocytosis by diagnostic ultrasound in vitro. Ultrasound Med Biol 2009; 35: 136-143.
26. Hauser J, Ellisman M, Steinau H, Stefan E, Dudda M, Hauser M. Ultrasound enhanced endocytotic activity of human fibroblasts. Ultrasound Med Biol 2009; 12: 2089-2092.
27. Tsai K, Fang S, Yang S, Shieh M, Lin W, Chen W. Time dependency of ultrasound-facilitated gene transfection. J Gene Med 2009; 11: 729-736.
28. Zhou Y, Shi J, Cui J, Deng CX. Effects of extracellular calcium on cell membrane resealing in sonoporation. J Control Release 2008; 126: 34-43.
29. Perrais D, Merrifield C. Dynamics of endocytotic vesicles creation. Developmental Cell 2005; 9: 581-592.
30. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytotic regulation of cell signaling. Nat Rev Mol Cell Biol 2005; 6: 112-126.
31. Takakura Y, Takagi T, Hashiguchi M, et al. Characterization of plasmid DNA binding and uptake by peritoneal macrophages from class A scavenger receptor knockout mice. Pharm Res 1999; 16: 503-508.
32. Rejman J, Bragonzi A, Conese M. Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes. Mol Ther 2005; 12: 468-74.
33. Budker V, Budker T, Zhang G, Subbotin V, Loomis A, Wolff JA. Hypothesis: naked plasmid DNA is taken up by cells in vivo by a receptor-mediated process. J Gene Med 2000; 2: 76-88.
34. Han B, Bai XH, Lodyga M, et al. Conversion of mechanical force into biochemical signaling. J Biol Chem 2004; 279: 54793-54801.
35. Apodaca G. Modulation of membrane traffic by mechanical stimuli. Am J Physiol Renal Physiol 2002; 282: F179-F190.
36. Sundqvist T, Liu SM. Hydrogen peroxide stimulates endocytosis in cultured bovine aortic endothelial cells. Acta Physiol Scand 1993; 149: 127-131.
37. Ca channels. Ultrasound Med Biol 2008; 34: 502-508.
38. Zupancic G, Ogden D, Magnus CJ, Wheeler-Jones C, Carter D. Differential exocytosis from human endothelial cells evoked by high intracellular Ca(2++) concentration. J Physiol 2002; 544: 741-755.
39. Fan Z, Kumon RE, Park J, Deng CX. Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J Control Release 2010; 142: 31-39.
40. Lee JH, Welsh MJ. Enhancement of calcium phosphate-mediated transfection by inclusion of adenovirus in coprecipitates. Gene Ther 1999; 6: 676-682.