"programmed packaging" for gene delivery

Journal of Controlled Release

Volumn 193, Issue , 2014, Pages 316-323

  Hyodo, M ^a   Sakurai, Y ^a   Akita, H ^a   Harashima, H ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Active targeting; Drug delivery system; Gene therapy; MEND; pDNA; siRNA

Indexed keywords

ACTIVE TARGETING; DRUG DELIVERY SYSTEM; MEND; PDNA; SIRNA;

GENE THERAPY;

APTAMER; CELL NUCLEUS DNA; DNA VACCINE; EXTRACHROMOSOMAL DNA; LIPID; LIPOFECTAMINE; LIPOPLEX; LIPOSOME; NANOPARTICLE; NUCLEIC ACID; PHOSPHORAMIDOUS ACID; PLASMID DNA; POLYMER; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; SURFACTANT; DRUG CARRIER;

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; ARTICLE; AUTOIMMUNITY; CELL ORGANELLE; COMBINATORIAL CHEMISTRY; CYTOTOXICITY; DENDRITIC CELL; DNA LIBRARY; DRUG DELIVERY SYSTEM; ENDOTHELIUM CELL; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; IMMUNOGENICITY; LIPOSOMAL GENE DELIVERY SYSTEM; MITOCHONDRION; NANOENCAPSULATION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PH; RNA INTERFERENCE; STATIC ELECTRICITY; THERMOSTABILITY; TUMOR GROWTH; TUMOR VASCULARIZATION; CHEMISTRY; GENE TRANSFER; GENETICS; INTRACELLULAR SPACE; METABOLISM; NEOPLASMS; PROCEDURES;

DRUG CARRIERS; DRUG DELIVERY SYSTEMS; GENE TRANSFER TECHNIQUES; HUMANS; INTRACELLULAR SPACE; LIPIDS; NANOPARTICLES; NEOPLASMS; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84908268652     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.04.023     Document Type: Article

References (83)

1. T. Nakamura, H. Akita, Y. Yamada, H. Hatakeyama, and H. Harashima A multifunctional envelope-type nanodevice for use in nanomedicine: concept and applications Acc. Chem. Res. 45 2012 1113 1121
2. H. Hatakeyama, H. Akita, and H. Harashima A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma Adv. Drug Deliv. Rev. 63 2011 152-60
3. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs Cancer Res. 46 1986 6387 6392
4. Z. Cheng, A. Al Zaki, J.Z. Hui, V.R. Muzykantov, and A. Tsourkas Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities Science 338 2012 903 910
5. Y.J. Yu, Y. Zhang, M. Kenrick, K. Hoyte, W. Luk, Y. Lu, J. Atwal, J.M. Elliott, S. Prabhu, R.J. Watts, and M.S. Dennis Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target Sci. Transl. Med. 3 2011 (84ra44)
6. A.D. Keefe, S. Pai, and A. Ellington Aptamers as therapeutics Nat. Rev. Drug Discov. 9 2010 537 550
7. A.D. Ellington, and J.W. Szostak In vitro selection of RNA molecules that bind specific ligands Nature 346 1990 818 822
8. C. Tuerk, and L. Gold Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase Science 249 1990 505 510
9. D. Shangguan, Y. Li, Z. Tang, Z.C. Cao, H.W. Chen, P. Mallikaratchy, K. Sefah, C.J. Yang, and W. Tan Aptamers evolved from live cells as effective molecular probes for cancer study Proc. Natl. Acad. Sci. U. S. A. 103 2006 11838 11843
10. J. Folkman Tumor angiogenesis: therapeutic implications N. Engl. J. Med. 285 1971 1182 1186
11. U.B. Gyllensten, and H.A. Erlich Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus Proc. Natl. Acad. Sci. U. S. A. 85 1988 7652 7656
12. M.N. Ara, M. Hyodo, N. Ohga, K. Hida, and H. Harashima Development of a novel DNA aptamer ligand targeting to primary cultured tumor endothelial cells by a cell-based SELEX method PLoS One 7 2012 e50174
13. Y. Yamada, and H. Harashima Mitochondrial drug delivery systems for macromolecule and their therapeutic application to mitochondrial diseases Adv. Drug Deliv. Rev. 60 2008 1439 1462
14. Y. Yamada, H. Akita, H. Kamiya, K. Kogure, T. Yamamoto, Y. Shinohara, K. Yamashita, H. Kobayashi, H. Kikuchi, and H. Harashima Mitoporter: a liposome-based carrier system for delivery of macromolecules into mitochondria via membrane fusion Biochim. Biophys. Acta 1778 2008 423 432
15. S.M. Elbashir, J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells Nature 411 2001 494 498
16. D.V. Morrissey, J.A. Lockridge, L. Shaw, K. Blanchard, K. Jensen, W. Breen, K. Hartsough, L. Machemer, S. Radka, V. Jadhav, N. Vaish, S. Zinnen, C. Vargeese, K. Bowman, C.S. Shaffer, L.B. Jeffs, A. Judge, I. MacLachlan, and B. Polisky Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs Nat. Biotechnol. 23 2005 1002 1007
17. K.A. Whitehead, R. Langer, and D.G. Anderson Knocking down barriers: advances in siRNA delivery Nat. Rev. Drug Discov. 8 2009 129 138
18. R.L. Kanasty, K.A. Whitehead, A.J. Vegas, and D.G. Anderson Action and reaction: the biological response to siRNA and its delivery vehicles Mol. Ther. 20 2012 513 524
19. G. Meister, and T. Tuschl Mechanisms of gene silencing by double-stranded RNA Nature 431 2004 343 349
20. G.R. Rettig, and M.A. Behlke Progress toward in vivo use of siRNAs-II Mol. Ther. 20 2012 483 512
21. R. Kanasty, J.R. Dorkin, A. Vegas, and D. Anderson Delivery materials for siRNA therapeutics Nat. Mater. 12 2013 967 977
22. C. Dohmen, D. Edinger, T. Frohlich, L. Schreiner, U. Lachelt, C. Troiber, J. Radler, P. Hadwiger, H.P. Vornlocher, and E. Wagner Nanosized multifunctional polyplexes for receptor-mediated siRNA delivery ACS Nano 6 2012 5198 5208
23. A.D. Judge, M. Robbins, I. Tavakoli, J. Levi, L. Hu, A. Fronda, E. Ambegia, K. McClintock, and I. MacLachlan Confirming the RNAi-mediated mechanism of action of siRNA-based cancer therapeutics in mice J. Clin. Invest. 119 2009 661 673
24. Y. Yang, J. Li, F. Liu, and L. Huang Systemic delivery of siRNA via LCP nanoparticle efficiently inhibits lung metastasis Mol. Ther. 20 2012 609 615
25. T.S. Zimmermann, A.C. Lee, A. Akinc, B. Bramlage, D. Bumcrot, M.N. Fedoruk, J. Harborth, J.A. Heyes, L.B. Jeffs, M. John, A.D. Judge, K. Lam, K. McClintock, L.V. Nechev, L.R. Palmer, T. Racie, I. Rohl, S. Seiffert, S. Shanmugam, V. Sood, J. Soutschek, I. Toudjarska, A.J. Wheat, E. Yaworski, W. Zedalis, V. Koteliansky, M. Manoharan, H.P. Vornlocher, and I. MacLachlan RNAi-mediated gene silencing in non-human primates Nature 441 2006 111 114
26. R.J. Christie, Y. Matsumoto, K. Miyata, T. Nomoto, S. Fukushima, K. Osada, J. Halnaut, F. Pittella, H.J. Kim, N. Nishiyama, and K. Kataoka Targeted polymeric micelles for siRNA treatment of experimental cancer by intravenous injection ACS Nano 6 2012 5174 5189
27. Y.W. Won, S.M. Yoon, K.M. Lee, and Y.H. Kim Poly(oligo-d-arginine) with internal disulfide linkages as a cytoplasm-sensitive carrier for siRNA delivery Mol. Ther. 19 2011 372 380
28. E. Song, P. Zhu, S.K. Lee, D. Chowdhury, S. Kussman, D.M. Dykxhoorn, Y. Feng, D. Palliser, D.B. Weiner, P. Shankar, W.A. Marasco, and J. Lieberman Antibody mediated in vivo delivery of small interfering RNAs via cell-surface receptors Nat. Biotechnol. 23 2005 709 717
29. C.I. Wooddell, D.B. Rozema, M. Hossbach, M. John, H.L. Hamilton, Q. Chu, J.O. Hegge, J.J. Klein, D.H. Wakefield, C.E. Oropeza, J. Deckert, I. Roehl, K. Jahn-Hofmann, P. Hadwiger, H.P. Vornlocher, A. McLachlan, and D.L. Lewis Hepatocyte-targeted RNAi therapeutics for the treatment of chronic hepatitis B virus infection Mol. Ther. 21 2013 973 985
30. J. Liu, Y. Huang, A. Kumar, A. Tan, S. Jin, A. Mozhi, and X.J. Liang pH-sensitive nano-systems for drug delivery in cancer therapy Biotechnol. Adv. 2013 (in press)
31. K.T. Love, K.P. Mahon, C.G. Levins, K.A. Whitehead, W. Querbes, J.R. Dorkin, J. Qin, W. Cantley, L.L. Qin, T. Racie, M. Frank-Kamenetsky, K.N. Yip, R. Alvarez, D.W. Sah, A. de Fougerolles, K. Fitzgerald, V. Koteliansky, A. Akinc, R. Langer, and D.G. Anderson Lipid-like materials for low-dose, in vivo gene silencing Proc. Natl. Acad. Sci. U. S. A. 107 2010 1864 1869
32. S.K. Kim, M.B. Foote, and L. Huang Targeted delivery of EV peptide to tumor cell cytoplasm using lipid coated calcium carbonate nanoparticles Cancer Lett. 334 2013 311 318
33. M. Jayaraman, S.M. Ansell, B.L. Mui, Y.K. Tam, J. Chen, X. Du, D. Butler, L. Eltepu, S. Matsuda, J.K. Narayanannair, K.G. Rajeev, I.M. Hafez, A. Akinc, M.A. Maier, M.A. Tracy, P.R. Cullis, T.D. Madden, M. Manoharan, and M.J. Hope Maximizing the potency of siRNA lipid nanoparticles for hepatic gene silencing in vivo Angew. Chem. Int. Ed. 51 2012 8529 8533
34. S.C. Semple, A. Akinc, J. Chen, A.P. Sandhu, B.L. Mui, C.K. Cho, D.W. Sah, D. Stebbing, E.J. Crosley, E. Yaworski, I.M. Hafez, J.R. Dorkin, J. Qin, K. Lam, K.G. Rajeev, K.F. Wong, L.B. Jeffs, L. Nechev, M.L. Eisenhardt, M. Jayaraman, M. Kazem, M.A. Maier, M. Srinivasulu, M.J. Weinstein, Q. Chen, R. Alvarez, S.A. Barros, S. De, S.K. Klimuk, T. Borland, V. Kosovrasti, W.L. Cantley, Y.K. Tam, M. Manoharan, M.A. Ciufolini, M.A. Tracy, A. de Fougerolles, I. MacLachlan, P.R. Cullis, T.D. Madden, and M.J. Hope Rational design of cationic lipids for siRNA delivery Nat. Biotechnol. 28 2010 172 176
35. K. Kusumoto, H. Akita, T. Ishitsuka, Y. Matsumoto, T. Nomoto, R. Furukawa, A. El-Sayed, H. Hatakeyama, K. Kajimoto, Y. Yamada, K. Kataoka, and H. Harashima Lipid envelope-type nanoparticle incorporating a multifunctional peptide for systemic siRNA delivery to the pulmonary endothelium ACS Nano 7 2013 7534 7541
36. Y. Sakurai, H. Hatakeyama, H. Akita, M. Oishi, Y. Nagasaki, S. Futaki, and H. Harashima Efficient short interference RNA delivery to tumor cells using a combination of octaarginine, GALA and tumor-specific, cleavable polyethylene glycol system Biol. Pharm. Bull. 32 2009 928 932
37. Y. Sakurai, H. Hatakeyama, Y. Sato, H. Akita, K. Takayama, S. Kobayashi, S. Futaki, and H. Harashima Endosomal escape and the knockdown efficiency of liposomal-siRNA by the fusogenic peptide shGALA Biomaterials 32 2011 5733 5742
38. Y. Sato, H. Hatakeyama, Y. Sakurai, M. Hyodo, H. Akita, and H. Harashima A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo J. Control. Release 163 2012 267 276
39. Y. Sakurai, H. Hatakeyama, Y. Sato, M. Hyodo, H. Akita, and H. Harashima Gene silencing via RNAi and siRNA quantification in tumor tissue using MEND, a liposomal siRNA delivery system Mol. Ther. 21 2013 1195 1203
40. A. Akinc, W. Querbes, S. De, J. Qin, M. Frank-Kamenetsky, K.N. Jayaprakash, M. Jayaraman, K.G. Rajeev, W.L. Cantley, J.R. Dorkin, J.S. Butler, L. Qin, T. Racie, A. Sprague, E. Fava, A. Zeigerer, M.J. Hope, M. Zerial, D.W. Sah, K. Fitzgerald, M.A. Tracy, M. Manoharan, V. Koteliansky, A. Fougerolles, and M.A. Maier Targeted delivery of RNAi therapeutics with endogenous and exogenous ligand-based mechanisms Mol. Ther. 18 2010 1357 1364
41. C. Murdoch, M. Muthana, S.B. Coffelt, and C.E. Lewis The role of myeloid cells in the promotion of tumour angiogenesis Nat. Rev. Cancer 8 2008 618 631
42. N. Ferrara, K.J. Hillan, H.P. Gerber, and W. Novotny Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer Nat. Rev. Drug Discov. 3 2004 391 400
43. A. Grothey, and E. Galanis Targeting angiogenesis: progress with anti-VEGF treatment with large molecules Nat. Rev. Clin. Oncol. 6 2009 507 518
44. Y. Sakurai, H. Hatakeyama, Y. Sato, M. Hyodo, H. Akita, N. Ohga, K. Hida, and H. Harashima RNAi-mediated gene knockdown and anti-angiogenic therapy of RCCs using a cyclic RGD-modified liposomal-siRNA system J. Control. Release 173C 2013 110 118
45. F. Danhier, A. Le Breton, and V. Preat RGD-based strategies to target alpha(v) beta(3) integrin in cancer therapy and diagnosis Mol. Pharm. 9 2012 2961 2973
46. L. Witte, D.J. Hicklin, Z. Zhu, B. Pytowski, H. Kotanides, P. Rockwell, and P. Bohlen Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy Cancer Metastasis Rev. 17 1998 155 161
47. G. Kibria, H. Hatakeyama, N. Ohga, K. Hida, and H. Harashima The effect of liposomal size on the targeted delivery of doxorubicin to integrin alphavbeta3-expressing tumor endothelial cells Biomaterials 34 2013 5617 5627
48. Y.M. Chook, and K.E. Suel Nuclear import by karyopherin-betas: recognition and inhibition Biochim. Biophys. Acta 1813 2011 1593 1606
49. M. Marfori, A. Mynott, J.J. Ellis, A.M. Mehdi, N.F. Saunders, P.M. Curmi, J.K. Forwood, M. Boden, and B. Kobe Molecular basis for specificity of nuclear import and prediction of nuclear localization Biochim. Biophys. Acta 1813 2011 1562 1577
50. S. Kose, M. Furuta, and N. Imamoto Hikeshi, a nuclear import carrier for Hsp70s, protects cells from heat shock-induced nuclear damage Cell 149 2012 578 589
51. M. Raices, and M.A. D'Angelo Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions Nat. Rev. Mol. Cell Biol. 13 2012 687 699
52. Y. Yoneda, T. Arioka, N. Imamoto-Sonobe, H. Sugawa, Y. Shimonishi, and T. Uchida Synthetic peptides containing a region of SV 40 large T-antigen involved in nuclear localization direct the transport of proteins into the nucleus Exp. Cell Res. 170 1987 439 452
53. T. Nagasaki, T. Myohoji, T. Tachibana, S. Futaki, and S. Tamagaki Can nuclear localization signals enhance nuclear localization of plasmid DNA? Bioconjug. Chem. 14 2003 282 286
54. M. Tanimoto, H. Kamiya, N. Minakawa, A. Matsuda, and H. Harashima No enhancement of nuclear entry by direct conjugation of a nuclear localization signal peptide to linearized DNA Bioconjug. Chem. 14 2003 1197 1202
55. J.J. Ludtke, G. Zhang, M.G. Sebestyen, and J.A. Wolff A nuclear localization signal can enhance both the nuclear transport and expression of 1 kb DNA J. Cell Sci. 112 Pt 12 1999 2033 2041
56. T. Nagasaki, T. Kawazu, T. Tachibana, S. Tamagaki, and S. Shinkai Enhanced nuclear import and transfection efficiency of plasmid DNA using streptavidin-fused importin-beta J. Control. Release 103 2005 199 207
57. C.K. Chan, and D.A. Jans Enhancement of polylysine-mediated transferrinfection by nuclear localization sequences: polylysine does not function as a nuclear localization sequence Hum. Gene Ther. 10 1999 1695 1702
58. C.K. Chan, T. Senden, and D.A. Jans Supramolecular structure and nuclear targeting efficiency determine the enhancement of transfection by modified polylysines Gene Ther. 7 2000 1690 1697
59. W. Ritter, C. Plank, J. Lausier, C. Rudolph, D. Zink, D. Reinhardt, and J. Rosenecker A novel transfecting peptide comprising a tetrameric nuclear localization sequence J. Mol. Med. 81 2003 708 717
60. C. Rudolph, C. Plank, J. Lausier, U. Schillinger, R.H. Muller, and J. Rosenecker Oligomers of the arginine-rich motif of the HIV-1 TAT protein are capable of transferring plasmid DNA into cells J. Biol. Chem. 278 2003 11411 11418
61. H. Akita, M. Tanimoto, T. Masuda, K. Kogure, S. Hama, K. Ninomiya, S. Futaki, and H. Harashima Evaluation of the nuclear delivery and intra-nuclear transcription of plasmid DNA condensed with micro (mu) and NLS-micro by cytoplasmic and nuclear microinjection: a comparative study with poly-l-lysine J. Gene Med. 8 2006 198 206
62. M. Keller, R.P. Harbottle, E. Perouzel, M. Colin, I. Shah, A. Rahim, L. Vaysse, A. Bergau, S. Moritz, C. Brahimi-Horn, C. Coutelle, and A.D. Miller Nuclear localisation sequence templated nonviral gene delivery vectors: investigation of intracellular trafficking events of LMD and LD vector systems Chembiochem 4 2003 286 298
63. T. Masuda, H. Akita, and H. Harashima Evaluation of nuclear transfer and transcription of plasmid DNA condensed with protamine by microinjection: the use of a nuclear transfer score FEBS Lett. 579 2005 2143 2148
64. H. Akita, T. Masuda, T. Nishio, K. Niikura, K. Ijiro, and H. Harashima Improving in vivo hepatic transfection activity by controlling intracellular trafficking: the function of GALA and maltotriose Mol. Pharm. 8 2011 1436 1442
65. T. Nakamura, R. Moriguchi, K. Kogure, A. Minoura, T. Masuda, H. Akita, K. Kato, H. Hamada, M. Ueno, S. Futaki, and H. Harashima Delivery of condensed DNA by liposomal non-viral gene delivery system into nucleus of dendritic cells Biol. Pharm. Bull. 29 2006 1290 1293
66. I.A. Khalil, S. Futaki, M. Niwa, Y. Baba, N. Kaji, H. Kamiya, and H. Harashima Mechanism of improved gene transfer by the N-terminal stearylation of octaarginine: enhanced cellular association by hydrophobic core formation Gene Ther. 11 2004 636 644
67. I.A. Khalil, K. Kogure, S. Futaki, S. Hama, H. Akita, M. Ueno, H. Kishida, M. Kudoh, Y. Mishina, K. Kataoka, M. Yamada, and H. Harashima Octaarginine-modified multifunctional envelope-type nanoparticles for gene delivery Gene Ther. 14 2007 682 689
68. H. Akita, A. Kudo, A. Minoura, M. Yamaguti, I.A. Khalil, R. Moriguchi, T. Masuda, R. Danev, K. Nagayama, K. Kogure, and H. Harashima Multi-layered nanoparticles for penetrating the endosome and nuclear membrane via a step-wise membrane fusion process Biomaterials 30 2009 2940 2949
69. S.M. Shaheen, H. Akita, A. Yamashita, R. Katoono, N. Yui, V. Biju, M. Ishikawa, and H. Harashima Quantitative analysis of condensation/decondensation status of pDNA in the nuclear sub-domains by QD-FRET Nucleic Acids Res. 39 2011 e48
70. T.B. Wyman, F. Nicol, O. Zelphati, P.V. Scaria, C. Plank, and F.C. Szoka Jr. Design, synthesis, and characterization of a cationic peptide that binds to nucleic acids and permeabilizes bilayers Biochemistry 36 1997 3008 3017
71. S.M. Shaheen, H. Akita, T. Nakamura, S. Takayama, S. Futaki, A. Yamashita, R. Katoono, N. Yui, and H. Harashima KALA-modified multi-layered nanoparticles as gene carriers for MHC class-I mediated antigen presentation for a DNA vaccine Biomaterials 32 2011 6342 6350
72. H. Akita, S. Ishii, N. Miura, S.M. Shaheen, Y. Hayashi, T. Nakamura, N. Kaji, Y. Baba, and H. Harashima A DNA microarray-based analysis of immune-stimulatory and transcriptional responses of dendritic cells to KALA-modified nanoparticles Biomaterials 34 2013 8979 8990
73. K.J. Ishii, T. Kawagoe, S. Koyama, K. Matsui, H. Kumar, T. Kawai, S. Uematsu, O. Takeuchi, F. Takeshita, C. Coban, and S. Akira TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines Nature 451 2008 725 729
74. H. Ishikawa, and G.N. Barber STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling Nature 455 2008 674 678
75. H. Ishikawa, Z. Ma, and G.N. Barber STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity Nature 461 2009 788 792
76. K.A. Mislick, and J.D. Baldeschwieler Evidence for the role of proteoglycans in cation-mediated gene transfer Proc. Natl. Acad. Sci. U. S. A. 93 1996 12349 12354
77. S.L. Ginn, I.E. Alexander, M.L. Edelstein, M.R. Abedi, and J. Wixon Gene therapy clinical trials worldwide to 2012 - an update J. Gene Med. 15 2013 65 77
78. S. Hama, H. Akita, S. Iida, H. Mizuguchi, and H. Harashima Quantitative and mechanism-based investigation of post-nuclear delivery events between adenovirus and lipoplex Nucleic Acids Res. 35 2007 1533 1543
79. S. Hama, H. Akita, R. Ito, H. Mizuguchi, T. Hayakawa, and H. Harashima Quantitative comparison of intracellular trafficking and nuclear transcription between adenoviral and lipoplex systems Mol. Ther. 13 2006 786 794
80. R.N. Cohen, M.A. van der Aa, N. Macaraeg, A.P. Lee, and F.C. Szoka Jr. Quantification of plasmid DNA copies in the nucleus after lipoplex and polyplex transfection J. Control. Release 135 2009 166 174
81. C.M. Varga, N.C. Tedford, M. Thomas, A.M. Klibanov, L.G. Griffith, and D.A. Lauffenburger Quantitative comparison of polyethylenimine formulations and adenoviral vectors in terms of intracellular gene delivery processes Gene Ther. 12 2005 1023 1032
82. H. Akita, R. Ishiba, H. Hatakeyama, H. Tanaka, Y. Sato, K. Tange, M. Arai, K. Kubo, and H. Harashima A neutral envelope-type nanoparticle containing pH-responsive and SS-cleavable lipid-like material as a carrier for plasmid DNA Adv. Healthc. Mater. 2 2013 1120 1125
83. H. Tanaka, H. Akita, R. Ishiba, K. Tange, M. Arai, K. Kubo, and H. Harashima Neutral biodegradable lipid-envelope-type nanoparticle using vitamin A-scaffold for nuclear targeting of plasmid DNA Biomaterials 35 2014 1755 1761]