Optimized rod length of polyplex micelles for maximizing transfection efficiency and their performance in systemic gene therapy against stroma-rich pancreatic tumors

Biomaterials

Volumn 35, Issue 20, 2014, Pages 5359-5368

  Dirisala, Anjaneyulu ^a   Osada, Kensuke ^a,d   Chen, Qixian ^a   Tockary, Theofilus A ^a   Machitani, Kaori ^a   Osawa, Shigehito ^a   Liu, Xueying ^b   Ishii, Takehiko ^a   Miyata, Kanjiro ^b   Oba, Makoto ^c   Uchida, Satoshi ^b   Itaka, Keiji ^b   Kataoka, Kazunori ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NAGASAKI UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

DNA; Gene transfer; In vitro test; In vivo test; Micelle; Nanoparticle

Indexed keywords

AMINO ACIDS; BLOCK COPOLYMERS; BLOOD; DNA; ECONOMIC AND SOCIAL EFFECTS; EFFICIENCY; GENE THERAPY; GENE TRANSFER; LIPOSOMES; MICELLES; MOLECULAR BIOLOGY; NANOPARTICLES; POLYETHYLENE OXIDES;

ANTI-TUMOR EFFICACY; CRITICAL THRESHOLD; IN-VITRO TESTS; IN-VIVO TESTS; PANCREATIC ADENOCARCINOMA; POLYPLEX MICELLES; STRUCTURAL FEATURE; TRANSFECTION EFFICIENCY;

POLYETHYLENE GLYCOLS;

COPOLYMER; LIPOFECTAMINE; MACROGOL; VASCULOTROPIN RECEPTOR 1; CYCLIC ARGININE-GLYCINE-ASPARTIC ACID PEPTIDE; CYCLOPEPTIDE; MACROGOL DERIVATIVE; MICELLE; POLYMER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CIRCULATION; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; GENE TARGETING; GENE THERAPY; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IN VITRO GENE TRANSFER; MICELLE; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; POLYPLEX MICELLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; SYSTEMIC THERAPY; TUMOR GROWTH; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; FLOW CYTOMETRY; GENE TRANSFER; HELA CELL LINE; METABOLISM; PANCREATIC NEOPLASMS; PROCEDURES; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HELA CELLS; HUMANS; MICE; MICE, INBRED BALB C; MICELLES; MICROSCOPY, ELECTRON, TRANSMISSION; PANCREATIC NEOPLASMS; PEPTIDES, CYCLIC; POLYETHYLENE GLYCOLS; POLYMERS; TRANSFECTION;

EID: 84899488301     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.03.037     Document Type: Article

References (55)

1. Kabanov A.V. Polymer genomics: an insight into pharmacology and toxicology of nanomedicines. Adv Drug Deliv Rev 2006, 58:1597-1621.
2. Cabral H., Nishiyama N., Kataoka K. Supramolecular nanodevices: from design validation to theranostic nanomedicine. Acc Chem Res 2011, 44:999-1008.
3. Hubbell J.A., Chilkoti A. Nanomaterials for drug delivery. Science 2012, 37:303-305.
4. Kopecek J. Polymer-drug conjugates: origins, progress to date and future directions. Adv Drug Deliv Rev 2013, 65:49-59.
5. Mulligan R.C. The basic science of gene therapy. Science 1993, 260:926-932.
6. Kay M.A. State-of-the-art gene-based therapies: the road ahead. Nat Rev Genet 2011, 12:316-328.
7. Osada K., Christie J.R., Kataoka K. Polymeric micelles from poly(ethylene glycol)-poly(amino acid) block copolymer for drug and gene delivery. J R Soc Interface 2009, 6:S325-S339.
8. Miyata K., Nishiyama N., Kataoka K. Rational design of smart supramolecular assemblies for gene delivery: chemical challenges in the creation of artificial viruses. Chem Soc Rev 2012, 41:2562-2574.
9. Ogris M., Brunner S., Schuller S., Kircheis R., Wagner E. PEGylated DNA/transferrin-PEI complexes: reduced interaction with blood components, extended circulation in blood and potential for systemic gene delivery. Gene Ther 1999, 4:595-605.
10. Katayose S., Kataoka K. Water-soluble polyion complex associates of DNA and poly(ethylene glycol)-poly(L-lysine) block copolymer. Bioconjug Chem 1997, 8:702-707.
11. Kakizawa Y., Kataoka K. Block copolymer micelles for delivery of gene and related compounds. Adv Drug Deliv Rev 2002, 54:203-222.
12. Osada K., Oshima H., Kobayashi D., Doi M., Enoki M., Yamasaki Y., et al. Quantized folding of plasmid DNA condensed with block catiomer into characteristic rod structures promoting transgene efficacy. J Am Chem Soc 2010, 132:12343-12348.
13. Akagi D., Oba M., Koyama H., Nishiyama N., Fukushima S., Miyata T., et al. Biocompatible micellar nanovectors achieve efficient gene transfer to vascular lesions without cytotoxicity and thrombus formation. Gene Ther 2007, 14:1029-1038.
14. Miyata K., Kakizawa Y., Nishiyama N., Harada A., Yamasaki Y., Koyama H., et al. Block catiomer polyplexes with regulated densities of charge and disulfide cross-linking directed to enhance gene expression. J Am Chem Soc 2004, 126:2355-2361.
15. Oba M., Vachutinsky Y., Miyata K., Kano M.R., Ikeda S., Nishiyama N., et al. Antiangiogenic gene therapy of solid tumor by systemic injection of polyplex micelles loading plasmid DNA encoding soluble Flt-1. Mol Pharm 2010, 7:501-509.
16. Vachutinsky Y., Oba M., Miyata K., Hiki S., Kano M.R., Nishiyama N., et al. Antiangiogenic gene therapy of experimental pancreatic tumor by sFlt-1 plasmid DNA carried by RGD-modified crosslinked polyplex micelles. J Control Release 2011, 149:51-57.
17. Tockary T.A., Osada K., Chen Q., Machitani K., Dirisala A., Uchida S., et al. Tethered PEG crowdedness determining shape and blood circulation profile of polyplex micelle gene carriers. Macromolecules 2013, 46:6585-6592.
18. Osada K., Shiotani T., Tockary T.A., Kobayashi D., Oshima H., Ikeda S., et al. Enhanced gene expression promoted by the quantized folding of pDNA within polyplex micelles. Biomaterials 2012, 33:325-332.
19. Lu F., Wu S.H., Hung Y., Mou C.Y. Size effect on cell uptake in well-suspended, uniform mesoporous silica nanoparticles. Small 2009, 5:1408-1413.
20. Katayose S., Kataoka K. Remarkable increase in nuclease resistance of plasmid DNA through supramolecular assembly with poly(ethylene glycol)-poly(L-lysine)block copolymer. J Pharm Sci 1998, 87:160-163.
21. 5 integrins. Bioconjug Chem 2007, 18:1415-1423.
22. Oba M., Aoyagi K., Miyata K., Matsumoto Y., Itaka K., Nishiyama N., et al. Polyplex micelles with cyclic RGD peptide ligands and disulfide cross-links directing to the enhanced transfection via controlled intracellular trafficking. Mol Pharm 2008, 5:1080-1092.
23. Mickler F.M., Vachutinsky Y., Oba M., Miyata K., Nishiyama N., Kataoka K., et al. Effect of integrin targeting and PEG shielding on polyplex micelle internalization studied by live-cell imaging. J Control Release 2011, 156:364-373.
24. Ge Z., Chen Q., Osada K., Liu X., Tockary T.A., Uchida S., et al. Targeted gene delivery by polyplex micelles with crowded PEG palisade and cRGD moiety for systemic treatment of pancreatic tumors. Biomaterials 2014, 35:3416-3426.
25. Daly W.H., Poché D. The preparation of N-carboxyanhydrides of α-amino acids using bis(trichloromethyl)carbonate. Tetrahedron Lett 1998, 29:5859-5862.
26. Tam J.P., Wu C.R., Liu W., Zhang J.W. Disulfide bond formation in peptides by dimethyl sulfoxide. Scope and applications. J Am Chem Soc 1991, 113:6657-6662.
27. Itaka K., Yamauchi K., Harada A., Nakamura K., Kawaguchi H., Kataoka K. Polyion complex micelles from plasmid DNA and poly(ethylene glycol)-poly(L-lysine) block copolymer as serum-tolerable polyplex system: physicochemical properties of micelles relevant to gene transfection efficiency. Biomaterials 2003, 24:4495-4506.
28. von Köckritz-Blickwede M., Chow O.A., Nizet V. Fetal calf serum contains heat-stable nucleases that degrade neutrophil extracellular traps. Blood 2009, 114:5245-5246.
29. Bernfield M., Götte M., Park P. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999, 68:729-777.
30. Tumova S., Woods A., Couchman J.R. Heparan sulfate proteoglycans on the cell surface: versatile coordinators of cellular functions. Int J Biochem Cell Biol 2000, 32:269-288.
31. Burke R.S., Pun S.H. Extracellular barriers to in vivo PEI and PEGylated PEI polyplex-mediated gene delivery to the liver. Bioconjug Chem 2008, 19:693-704.
32. Ruponen M., Ylä-Herttuala S., Urtti A. Interactions of polymeric and liposomal gene delivery systems with extracellular glycosaminoglycans: physicochemical and transfection studies. Biochim Biophys Acta 1999, 1415:331-341.
33. Yanagishita M., Hascall V.C. Characterization of heparan sulfate proteoglycans synthesized by rat ovarian granulosa cells in culture. J Biol Chem 1983, 8:12857-12864.
34. Pikas D.S., Li J.-P., Vlodavsky I., Lindahl U. Substrate specificity of heparanases from human hepatoma and platelets. J Biol Chem 1998, 273:18770-18777.
35. Kakizawa Y., Harada A., Kataoka K. Environment-sensitive stabilization of core-shell structured polyion complex micelle by reversible cross-linking of the core through disulfide bond. J Am Chem Soc 1999, 121:11247-11248.
36. Kursa M., Walker G.F., Roessler V., Ogris M., Roedl W., Kircheis R., et al. Novel shielded transferrin-polyethylene glycol-polyethylenimine/DNA complexes for systemic tumor-targeted gene transfer. Bioconjug Chem 2003, 14:222-231.
37. Mishra S., Webster P., Davis M.E. PEGylation significantly affects cellular uptake and intracellular trafficking of non-viral gene delivery particles. Eur J Cell Biol 2004, 83:97-111.
38. Conner S.D., Schimd S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
39. Kobayahi M., Hoshino T. Phagocytic activity of HeLa cells after thymidine treatment. Arch Histol Jpn 1983, 46:479-489.
40. Lim J.P., Gleeson P.A. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol 2011, 89:836-843.
41. McMahon H.T., Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2011, 12:517-533.
42. Rejman J., Oberle V., Zuhorn I.S., Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 2004, 377:159-169.
43. Pelkmans L., Helenius A. Endocytosis via caveolae. Traffic 2002, 3:311-320.
44. Geng Y., Dalhaimer P., Cai S.S., Tsai R., Tewari M., Minko T., et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol 2007, 2:249-255.
45. Ji S., Xu J., Zhang B., Yao W., Xu W., Wu W., et al. RGD-conjugated albumin nanoparticles as a novel delivery vehicle in pancreatic cancer therapy. Cancer Biol Ther 2012, 13:206-215.
46. Kagaya H., Oba M., Miura Y., Koyama H., Ishii T., Shimada T., et al. Impact of polyplex micelles installed with cyclic RGD peptide as ligand on gene delivery to vascular lesions. Gene Ther 2012, 19:61-69.
47. Boussif O., Lezoualch F., Zanta M.A., Mergny M.D., Scherman D., Demeneix B., et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci U S A 1995, 92:7297-7301.
48. Zhou X., Huang L. DNA transfection mediated by cationic liposomes containing lipopolylysine: characterization and mechanism of action. Biochim Biophys Acta 1994, 1189:195-203.
49. Kano M.R., Komuta Y., Iwata C., Oka M., Shirai Y., Morishita Y., et al. Comparison of the effects of the kinase inhibitors imatinib, sorafenib, and transforming growth factor-beta receptor inhibitor on extravasation of nanoparticles from neovasculature. Cancer Sci 2009, 100:173-180.
50. Kano M.R., Bae Y., Iwata C., Morishita Y., Yashiro M., Oka M., et al. Improvement of cancer-targeting therapy, using nanocarriers for intractable solid tumors by inhibition of TGF-beta signaling. Proc Natl Acad Sci U S A 2007, 104:3460-3465.
51. Sofuni A., Iijima H., Moriyasu F., Nakayama D., Shimizu M., Nakamura K., et al. Differential diagnosis of pancreatic tumors using ultrasound contrast imaging. J Gastroenterol 2005, 40:518-525.
52. Takahashi Y., Cleary K.R., Mai M., Kitadai Y., Bucana C.D., Ellis L.M. Significance of vessel count and vascular endothelial growth factor and its receptor (KDR) in intestinal-type gastric cancer. Clin Cancer Res 1996, 2:1679-1684.
53. 5 are expressed by endothelium of high-risk neuroblastoma and their inhibition is associated with increased endogenous ceramide. Cancer Res 2000, 60:712-721.
54. Kendall R.L., Thomas K.A. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 1993, 90:10705-10709.
55. Yamaguchi S., Iwata K., Shibuya M. Soluble Flt-1 (soluble VEGFR-1), a potent natural antiangiogenic molecule in mammals, is phylogenetically conserved in avians. Biochem Biophys Res Commun 2002, 291:554-559.