Addition of ascorbic acid to the extracellular environment activates lipoplexes of a ferrocenyl lipid and promotes cell transfection

Journal of Controlled Release

Volumn 157, Issue 2, 2012, Pages 249-259

  Aytar, Burcu S ^a   Muller, John P E ^a   Golan, Sharon ^b   Hata, Shinichi ^c   Takahashi, Hiro ^c   Kondo, Yukishige ^c   Talmon, Yeshayahu ^b   Abbott, Nicholas L ^a   Lynn, David M ^a  

^a University of Wisconsin Madison   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Ascorbic acid; External stimulus; Ferrocenyl lipid; Lipoplexes; Nanostructure; Transfection

Indexed keywords

ASCORBIC ACIDS; EXTERNAL STIMULUS; FERROCENYL; LIPOPLEXES; TRANSFECTION;

BROMINE COMPOUNDS; CELL CULTURE; CELLS; CONFOCAL MICROSCOPY; KETONES; LIPOSOMES; NANOSTRUCTURES; NEUTRON SCATTERING; ORGANIC ACIDS; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL;

MOLECULAR BIOLOGY;

ASCORBIC ACID; BROMIDE; FERROCENYL LIPID BIS(11 FERROCENYLUNDECYL)DIMETHYLAMMONIUM BROMIDE; LIPOPLEX; NANOMATERIAL; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL GROWTH; CELL STRAIN COS7; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CULTURE MEDIUM; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; NEUTRON SCATTERING; NONVIRAL GENE DELIVERY SYSTEM; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; SPECTROPHOTOMETRY; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROSCOPY; ZETA POTENTIAL;

ANIMALS; ASCORBIC ACID; CELL LINE; CERCOPITHECUS AETHIOPS; FERROUS COMPOUNDS; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; HUMANS; LUCIFERASES; LUMINESCENT AGENTS; MICE; OXIDATION-REDUCTION; TRANSGENES;

EID: 84855814635     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.09.074     Document Type: Article

References (59)

1. P.L. Felgner, T.R. Gadek, M. Holm, R. Roman, H.W. Chan, M. Wenz, J.P. Northrop, G.M. Ringold, and M. Danielsen Lipofection - a highly efficient, lipid-mediated DNA-transfection procedure Proc. Natl. Acad. Sci. U.S.A. 84 1987 7413 7417
2. J. Zabner Cationic lipids used in gene transfer Adv. Drug Deliv. Rev. 27 1997 17 28 (Pubitemid 27301394)
3. A.V. Kabanov, P.L. Felgner, and L.W. Seymour Self-assembling complexes for gene delivery: from laboratory to clinical trial 1998 John Wiley and Sons New York
4. M.C.P. de Lima, S. Neves, A. Filipe, N. Duzgunes, and S. Simoes Cationic liposomes for gene delivery: from biophysics to biological applications Curr. Med. Chem. 10 2003 1221 1231 (Pubitemid 36763932)
5. L. Wasungu, and D. Hoekstra Cationic lipids, lipoplexes and intracellular delivery of genes J. Control. Release 116 2006 255 264 (Pubitemid 44854274)
6. C.T. de Ilarduya, Y. Sun, and N. Duzgunes Gene delivery by lipoplexes and polyplexes Eur. J. Pharm. Sci. 40 2010 159 170
7. D.D. Lasic, and N.S. Templeton Liposomes in gene therapy Adv. Drug Deliv. Rev. 20 1996 221 266 (Pubitemid 26284164)
8. S.B. Zhang, Y.M. Xu, B. Wang, W.H. Qiao, D.L. Liu, and Z.S. Li Cationic compounds used in lipoplexes and polyplexes for gene delivery J. Control. Release 100 2004 165 180 (Pubitemid 39491269)
9. J.G. Lewis, K.Y. Lin, A. Kothavale, W.M. Flanagan, M.D. Matteucci, R.B. DePrince, R.A. Mook, R.W. Hendren, and R.W. Wagner A serum-resistant cytofectin for cellular delivery of antisense oligodeoxynucleotides and plasmid DNA Proc. Natl. Acad. Sci. U.S.A. 93 1996 3176 3181 (Pubitemid 26127586)
10. J.J. Wheeler, L. Palmer, M. Ossanlou, I. MacLachlan, R.W. Graham, Y.P. Zhang, M.J. Hope, P. Scherrer, and P.R. Cullis Stabilized plasmid-lipid particles: construction and characterization Gene Ther. 6 1999 271 281 (Pubitemid 29089926)
11. M.F.M. Mustapa, S.M. Grosse, L. Kudsiova, M. Elbs, E.A. Raiber, J.B. Wong, A.P.R. Brain, H.E.J. Armer, A. Warley, M. Keppler, T. Ng, M.J. Lawrence, S.L. Hart, H.C. Hailes, and A.B. Tabor Stabilized integrin-targeting ternary lpd (lipopolyplex) vectors for gene delivery designed to disassemble within the target cell Bioconjug. Chem. 20 2009 518 532
12. B. Wetzer, G. Byk, M. Frederic, M. Airiau, F. Blanche, B. Pitard, and D. Scherman Reducible cationic lipids for gene transfer Biochem. J. 356 2001 747 756 (Pubitemid 32588446)
13. F.X. Tang, and J.A. Hughes Introduction of a disulfide bond into a cationic lipid enhances transgene expression of plasmid DNA Biochem. Biophys. Res. Commun. 242 1998 141 145 (Pubitemid 28412392)
14. F.X. Tang, and J.A. Hughes Use of dithiodiglycolic acid as a tether for cationic lipids decreases the cytotoxicity and increases transgene expression of plasmid DNA in vitro Bioconjug. Chem. 10 1999 791 796 (Pubitemid 29456365)
15. X. Guo, and F.C. Szoka Chemical approaches to triggerable lipid vesicles for drug and gene delivery Acc. Chem. Res. 36 2003 335 341
16. Z.H. Huang, W.J. Li, J.A. MacKay, and F.C. Szoka Thiocholesterol-based lipids for ordered assembly of bioresponsive gene carriers Mol. Ther. 11 2005 409 417 (Pubitemid 40277317)
17. V. Budker, V. Gurevich, J.E. Hagstrom, F. Bortzov, and J.A. Wolff pH-sensitive, cationic liposomes: a new synthetic virus-like vector Nat. Biotechnol. 14 1996 760 764 (Pubitemid 26157549)
18. O.V. Gerasimov, J.A. Boomer, M.M. Qualls, and D.H. Thompson Cytosolic drug delivery using pH- and light-sensitive liposomes Adv. Drug Deliv. Rev. 38 1999 317 338 (Pubitemid 29376580)
19. J. Zhu, R.J. Munn, and M.H. Nantz Self-cleaving ortho ester lipids: a new class of pH-vulnerable amphiphiles J. Am. Chem. Soc. 122 2000 2645 2646 (Pubitemid 30211978)
20. P. Meers Enzyme-activated targeting of liposomes Adv. Drug Deliv. Rev. 53 2001 265 272 (Pubitemid 34026337)
21. C.A.H. Prata, Y.X. Zhao, P. Barthelemy, Y.G. Li, D. Luo, T.J. McIntosh, S.J. Lee, and M.W. Grinstaff Charge-reversal amphiphiles for gene delivery J. Am. Chem. Soc. 126 2004 12196 12197 (Pubitemid 39304865)
22. T. Nagasaki, A. Taniguchi, and S. Tamagaki Photoenhancement of transfection efficiency using novel cationic lipids having a photocleavable spacer Bioconjug. Chem. 14 2003 513 516 (Pubitemid 36597359)
23. J.A. Wolff, and D.B. Rozema Breaking the bonds: non-viral vectors become chemically dynamic Mol. Ther. 16 2008 8 15
24. Y.C. Liu, A.L.M. Le Ny, J. Schmidt, Y. Talmon, B.F. Chmelka, and C.T. Lee Photo-assisted gene delivery using light-responsive catanionic vesicles Langmuir 25 2009 5713 5724
25. J. Ziauddin, and D.M. Sabatini Microarrays of cells expressing defined cDNAs Nature 411 2001 107 110 (Pubitemid 32428199)
26. F. Yamauchi, K. Kato, and H. Iwata Micropatterned, self-assembled monolayers for fabrication of transfected cell microarrays Biochim. Biophys. Acta, Gen. Subj. 1672 2004 138 147 (Pubitemid 38746502)
27. F.H. Chang, C.H. Lee, M.T. Chen, C.C. Kuo, Y.L. Chiang, C.Y. Hang, and S. Roffler Surfection: a new platform for transfected cell arrays Nucleic Acids Res. 32 2004 e33
28. M. Isalan, M.I. Santori, C. Gonzalez, and L. Serrano Localized transfection on arrays of magnetic beads coated with PCR products Nat. Methods 2 2005 113 118 (Pubitemid 41131032)
29. A.L. Hook, H. Thissen, and N.H. Voelcker Advanced substrate fabrication for cell microarrays Biomacromolecules 10 2009 573 579
30. W.M. Saltzman Delivering tissue regeneration Nat. Biotechnol. 17 1999 534 535 (Pubitemid 29262911)
31. L.D. Shea, E. Smiley, J. Bonadio, and D.J. Mooney DNA delivery from polymer matrices for tissue engineering Nat. Biotechnol. 17 1999 551 554 (Pubitemid 29262917)
32. J.A. Shepard, A. Huang, A. Shikanov, and L.D. Shea Balancing cell migration with matrix degradation enhances gene delivery to cells cultured three-dimensionally within hydrogels J. Control. Release 146 2010 128 135
33. F. Yang, S.W. Cho, S.M. Son, S.R. Bogatyrev, D. Singh, J.J. Green, Y. Mei, S. Park, S.H. Bhang, B.S. Kim, R. Langer, and D.G. Anderson Genetic engineering of human stem cells for enhanced angiogenesis using biodegradable polymeric nanoparticles Proc. Natl. Acad. Sci. U.S.A. 107 2010 3317 3322
34. Y. Kakizawa, H. Sakai, K. Nishiyama, M. Abe, H. Shoji, Y. Kondo, and N. Yoshino Solution properties of double-tailed cationic surfactants having ferrocenyl groups in their hydrophobic moieties Langmuir 12 1996 921 924 (Pubitemid 126568086)
35. N. Yoshino, H. Shoji, Y. Kondo, Y. Kakizawa, H. Sakai, and M. Abe Syntheses of cationic surfactants having two ferrocenylalkyl chains J. Jpn. Oil Chem. Soc. 45 1996 769 775
36. Y. Kakizawa, H. Sakai, A. Yamaguchi, Y. Kondo, N. Yoshino, and M. Abe Electrochemical control of vesicle formation with a double-tailed cationic surfactant bearing ferrocenyl moieties Langmuir 17 2001 8044 8048 (Pubitemid 35330878)
37. N.L. Abbott, C.M. Jewell, M.E. Hays, Y. Kondo, and D.M. Lynn Ferrocene-containing cationic lipids: Influence of redox state on cell transfection J. Am. Chem. Soc. 127 2005 11576 11577 (Pubitemid 41208726)
38. C.M. Jewell, M.E. Hays, Y. Kondo, N.L. Abbott, and D.M. Lynn Ferrocene-containing cationic lipids for the delivery of DNA: oxidation state determines transfection activity J. Control. Release 112 2006 129 138
39. M.E. Hays, C.M. Jewell, Y. Kondo, D.M. Lynn, and N.L. Abbott Lipoplexes formed by DNA and ferrocenyl lipids: effect of lipid oxidation state on size, internal dynamics, and zeta-potential Biophys. J. 93 2007 4414 4424 (Pubitemid 350294487)
40. C.L. Pizzey, C.M. Jewell, M.E. Hays, D.M. Lynn, N.L. Abbott, Y. Kondo, S. Golan, and Y. Talmon Characterization of the nanostructure of complexes formed by a redox-active cationic lipid and DNA J. Phys. Chem. B 112 2008 5849 5857 (Pubitemid 351704601)
41. C.M. Jewell, M.E. Hays, Y. Kondo, N.L. Abbott, and D.M. Lynn Chemical activation of lipoplexes formed from DNA and a redox-active, ferrocene-containing cationic lipid Bioconjug. Chem. 19 2008 2120 2128
42. T. Saji, K. Hoshino, and S. Aoyagui Reversible formation and disruption of micelles by control of the redox state of the head group J. Am. Chem. Soc. 107 1985 6865 6868
43. B.S. Gallardo, M.J. Hwa, and N.L. Abbott In-situ and reversible control of the surface-activity of ferrocenyl surfactants in aqueous-solutions Langmuir 11 1995 4209 4212
44. D.E. Bennett, B.S. Gallardo, and N.L. Abbott Dispensing surfactants from electrodes: Marangoni phenomenon at the surface of aqueous solutions of (11-ferrocenylundecyl)trimethylammonium bromide J. Am. Chem. Soc. 118 1996 6499 6505 (Pubitemid 26247704)
45. B.S. Gallardo, V.K. Gupta, F.D. Eagerton, L.I. Jong, V.S. Craig, R.R. Shah, and N.L. Abbott Electrochemical principles for active control of liquids on submillimeter scales Science 283 1999 57 60 (Pubitemid 29044844)
46. C.A. Rosslee, C. Khripin, T.M.D. Foley, and N.L. Abbott Using "prosurfactants" to enhance rates of delivery of surfactants AlChE J. 50 2004 708 714 (Pubitemid 38387776)
47. A. Meister, and M.E. Anderson Glutathione Annu. Rev. Biochem. 52 1983 711 760 (Pubitemid 13030692)
48. F.Q. Schafer, and G.R. Buettner Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic. Biol. Med. 30 2001 1191 1212 (Pubitemid 32463931)
49. G. Banhegyi, L. Braun, M. Csala, F. Puskas, and J. Mandl Ascorbate metabolism and its regulation in animals Free Radic. Biol. Med. 23 1997 793 803 (Pubitemid 27364874)
50. A. Guinier, and G. Fournet Small Angle X-Ray Scattering 1955 John Wiley & Sons New York
51. J.R. Bellare, H.T. Davis, L.E. Scriven, and Y. Talmon Controlled environment vitrification system - an improved sample preparation technique J. Electron Microsc. Tech. 10 1988 87 111
52. D. Danino, A. Bernheim-Groswasser, and Y. Talmon Digital cryogenic transmission electron microscopy: an advanced tool for direct imaging of complex fluids Colloids Surf. A: Physicochem. Eng. Asp. 183 2001 113 122 (Pubitemid 32396881)
53. E.V.B. van Gaal, R. van Eijk, R.S. Oosting, R.J. Kok, W.E. Hennink, D.J.A. Crommelin, and E. Mastrobattista How to screen non-viral gene delivery systems in vitro? J. Control. Release 154 2011 218 232
54. J.P. Vigneron, N. Oudrhiri, M. Fauquet, L. Vergely, J.C. Bradley, M. Basseville, P. Lehn, and J.M. Lehn Guanidinium-cholesterol cationic lipids: efficient vectors for the transfection of eukaryotic cells Proc. Natl. Acad. Sci. U.S.A. 93 1996 9682 9686 (Pubitemid 26296669)
55. Y. Gluzman SV40-transformed simian cells support the replication of early SV40 mutants Cell 23 1981 175 182 (Pubitemid 11173621)
56. W.S. Pear, G.P. Nolan, M.L. Scott, and D. Baltimore Production of high-titer helper-free retroviruses by transient transfection Proc. Natl. Acad. Sci. U.S.A. 90 1993 8392 8396 (Pubitemid 23277674)
57. E. Tomlinson, and A.P. Rolland Controllable gene therapy - pharmaceutics of non-viral gene delivery systems J. Control. Release 39 1996 357 372 (Pubitemid 26194229)
58. F. Sakurai, R. Inoue, Y. Nishino, A. Okuda, O. Matsumoto, T. Taga, F. Yamashita, Y. Takakura, and M. Hashida Effect of DNA/liposome mixing ratio on the physicochemical characteristics, cellular uptake and intracellular trafficking of plasmid DNA/cationic liposome complexes and subsequent gene expression J. Control. Release 66 2000 255 269 (Pubitemid 30160862)
59. M. Cardenas, C.A. Dreiss, T. Nylander, C.P. Chan, T. Cosgrove, and B. Lindman SANS study of the interactions among DNA, a cationic surfactant, and polystyrene latex particles Langmuir 21 2005 3578 3583 (Pubitemid 40538369)