Effect of integrin targeting and PEG shielding on polyplex micelle internalization studied by live-cell imaging

Journal of Controlled Release

Volumn 156, Issue 3, 2011, Pages 364-373

  Mickler, F M ^a,b   Vachutinsky, Y ^c,e   Oba, M ^d   Miyata, K ^d   Nishiyama, N ^d   Kataoka, K ^c,d   Brauchle C ^a,b   Ruthardt, N ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b Munich Center for Integrated Protein Science   (Germany)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e INSIGHTEC LTD   (Israel)

Author keywords

Gene therapy; Integrin targeting; Live cell imaging; Polyplex micelles; Shielding

Indexed keywords

CANCER THERAPY; CLATHRINS; CLINICAL THERAPY; GENE VECTORS; HELA CELL; HIGHLY SENSITIVE; HOST CELLS; INTEGRINS; LIVE-CELL IMAGING; LOW DOSE; PLASMID DNA; POLYPLEXES; REPORTER-GENE EXPRESSION; RGD PEPTIDE; SHELL LAYERS; SURFACE SHIELDING; TARGET STRUCTURE; TRANSGENE EXPRESSION; TUMOR GROWTH;

AMINO ACIDS; CELLS; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE THERAPY; GLYCOPROTEINS; LIGANDS; MOLECULAR BIOLOGY; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; SHIELDING; TUMORS;

MICELLES;

ARGINYLGLYCYLASPARTIC ACID; CLATHRIN; COPOLYMER; INTEGRIN; LUCIFERASE; MACROGOL; NANOCARRIER; PLASMID DNA; POLYLYSINE;

ARTICLE; CANCER GENE THERAPY; DRUG TARGETING; DRUG TUMOR LEVEL; ENDOCYTOSIS; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE VECTOR; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMAGING; INTERNALIZATION; LIVE CELL IMAGING; POLYPLEX MICELLE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; GENES, REPORTER; HELA CELLS; HUMANS; INTEGRINS; LUCIFERASES; MICELLES; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; OLIGOPEPTIDES; POLYETHYLENE GLYCOLS;

EID: 82755160663     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.08.003     Document Type: Article

References (52)

1. R. Duncan The dawning era of polymer therapeutics Nat. Rev. Drug. Discov. 2 5 2003 347 360 (Pubitemid 37361705)
2. D. Schaffert, and E. Wagner Gene therapy progress and prospects: synthetic polymer-based systems Gene Ther. 15 16 2008 1131 1138
3. K. Itaka, and K. Kataoka Recent development of nonviral gene delivery systems with virus-like structures and mechanisms Eur. J. Pharm. Biopharm. 71 3 2009 475 483
4. Y. Lu, and C.O. Madu Viral-based gene delivery and regulated gene expression for targeted cancer therapy Expert Opin. Drug Deliv. 7 1 2010 19 35
5. F. Danhier, O. Feron, and V. Préat To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery J. Control. Release 148 2 2010 135 146
6. M. Günther, E. Wagner, and M. Ogris Specific targets in tumor tissue for the delivery of therapeutic genes Curr. Med. Chem. Anticancer Agents 5 2005 157 171 (Pubitemid 40347989)
7. K.L. Douglas Toward development of artificial viruses for gene therapy: a comparative evaluation of viral and non-viral transfection Biotechnol. Progr. 24 4 2008 871 883
8. K. Miyata, Y. Kakizawa, N. Nishiyama, A. Harada, Y. Yamasaki, H. Koyama, and K. Kataoka Block catiomer polyplexes with regulated densities of charge and disulfide cross-linking directed to enhance gene expression J. Am. Chem. Soc. 126 8 2004 2355 2361 (Pubitemid 38295715)
9. K. Miyata, M. Oba, M. Kano, S. Fukushima, Y. Vachutinsky, M. Han, H. Koyama, K. Miyazono, N. Nishiyama, and K. Kataoka Polyplex micelles from triblock copolymers composed of tandemly aligned segments with biocompatible, endosomal escaping, and DNA-condensing functions for systemic gene delivery to pancreatic tumor tissue Pharm. Res. 25 12 2008 2924 2936
10. S. Mishra, P. Webster, and M.E. Davis PEGylation significantly affects cellular uptake and intracellular trafficking of non-viral gene delivery particles Eur. J. Cell Biol. 83 3 2004 97 111 (Pubitemid 38765217)
11. X. Zhang, S.R. Pan, H.M. Hu, G.F. Wu, M. Feng, W. Zhang, and X. Luo Poly(ethylene glycol)-block-polyethylenimine copolymers as carriers for gene delivery: effects of PEG molecular weight and PEGylation degree J. Biomed. Mater. Res. A 84A 3 2008 795 804 (Pubitemid 351237797)
12. M. Oba, K. Aoyagi, K. Miyata, Y. Matsumoto, K. Itaka, N. Nishiyama, Y. Yamasaki, H. Koyama, and K. Kataoka Polyplex micelles with cyclic RGD peptide ligands and disulfide cross-links directing to the enhanced transfection via controlled intracellular trafficking Mol. Pharm. 5 6 2008 1080 1092
13. M. Oba, S. Fukushima, N. Kanayama, K. Aoyagi, N. Nishiyama, H. Koyama, and K. Kataoka Cyclic RGD peptide-conjugated polyplex micelles as a targetable gene delivery system directed to cells possessing alphavbeta3 and alphavbeta5 integrins Bioconjug. Chem. 18 5 2007 1415 1423 (Pubitemid 47464048)
14. W. Arap, R. Pasqualini, and E. Ruoslahti Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model Science 279 5349 1998 377 380 (Pubitemid 28063372)
15. C. Rader, M. Popkov, J.A. Neves, and C.F. Barbas Integrin avb3-targeted therapy for Kaposi's sarcoma with an in vitro-evolved antibody FASEB J. 16 14 2002 2000 2002
16. O.M. Merkel, O. Germershaus, C.K. Wada, P.J. Tarcha, T. Merdan, and T. Kissel Integrin [alpha]v[beta]3 targeted gene delivery using RGD peptidomimetic conjugates with copolymers of PEGylated poly(ethylene imine) Bioconjug. Chem. 20 6 2009 1270 1280
17. J.S. Desgrosellier, and D.A. Cheresh Integrins in cancer: biological implications and therapeutic opportunities Nat. Rev. Cancer 10 1 2010 9 22
18. S. Meng, B. Su, W. Li, Y. Ding, L. Tang, W. Zhou, Y. Song, and Z. Caicun Integrin-targeted paclitaxel nanoliposomes for tumor therapy Med. Oncol. 2010 1 8
19. K. Temming, R.M. Schiffelers, G. Molema, and R.J. Kok RGD-based strategies for selective delivery of therapeutics and imaging agents to the tumour vasculature Drug Resist. Updat. 8 6 2005 381 402 (Pubitemid 43358061)
20. G. Zuber, M. Dontenwill, and J.-P. Behr Synthetic viruslike particles for targeted gene delivery to [alpha]v[beta]3 integrin-presenting endothelial cells Mol. Pharm. 6 5 2009 1544 1552
21. Y. Vachutinsky, M. Oba, K. Miyata, S. Hiki, M.R. Kano, N. Nishiyama, H. Koyama, K. Miyazono, and K. Kataoka Antiangiogenic gene therapy of experimental pancreatic tumor by sFlt-1 plasmid DNA carried by RGD-modified crosslinked polyplex micelles J. Control. Release 149 1 2011 51 57
22. M. Oba, Y. Vachutinsky, K. Miyata, M.R. Kano, S. Ikeda, N. Nishiyama, K. Itaka, K. Miyazono, H. Koyama, and K. Kataoka Antiangiogenic gene therapy of solid tumor by systemic injection of polyplex micelles loading plasmid DNA encoding soluble Flt-1 Mol. Pharm. 7 2 2010 501 509
23. K. de Bruin, N. Ruthardt, K. von Gersdorff, R. Bausinger, E. Wagner, M. Ogris, and C. Brauchle Cellular dynamics of EGF receptor-targeted synthetic viruses Mol. Ther. 15 7 2007 1297 1305 (Pubitemid 46965326)
24. A.M. Sauer, K.G. de Bruin, N. Ruthardt, O. Mykhaylyk, C. Plank, and C. Bräuchle Dynamics of magnetic lipoplexes studied by single particle tracking in living cells J. Control. Release 137 2 2009 136 145
25. K.G. de Bruin, C. Fella, M. Ogris, E. Wagner, N. Ruthardt, and C. Bräuchle Dynamics of photoinduced endosomal release of polyplexes J. Control. Release 130 2 2008 175 182
26. G. Seisenberger, M.U. Ried, T. Endre, H. Buning, M. Hallek, and C. Braeuchle Real-time single-molecule imaging of the infection pathway of an adeno-associated virus Science 294 5548 2001 1929 1932 (Pubitemid 33101590)
27. R.D. Singh, V. Puri, J.T. Valiyaveettil, D.L. Marks, R. Bittman, and R.E. Pagano Selective caveolin-1-dependent endocytosis of glycosphingolipids Mol. Biol. Cell 14 8 2003 3254 3265 (Pubitemid 37013125)
28. A. Dautry-Varsat Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor Biochimie 68 1986 375 381 (Pubitemid 16075046)
29. D. Vercauteren, R.E. Vandenbroucke, A.T. Jones, J. Rejman, J. Demeester, S.C. De Smedt, N.N. Sanders, and K. Braeckmans The Use of Inhibitors to Study Endocytic Pathways of Gene Carriers: Optimization and Pitfalls Mol Ther 18 3 2010 561 569
30. M. Ogris, G. Walker, T. Blessing, R. Kircheis, M. Wolschek, and E. Wagner Tumor-targeted gene therapy: strategies for the preparation of ligand-polyethylene glycol-polyethylenimine/DNA complexes J. Control. Release 91 1-2 2003 173 181 (Pubitemid 37288888)
31. O. Veiseh, F.M. Kievit, J.W. Gunn, B.D. Ratner, and M. Zhang A ligand-mediated nanovector for targeted gene delivery and transfection in cancer cells Biomaterials 30 4 2009 649 657
32. L.M. Kaminskas, B.J. Boyd, P. Karellas, G.Y. Krippner, R. Lessene, B. Kelly, and C.J.H. Porter The impact of molecular weight and PEG chain length on the systemic pharmacokinetics of PEGylated poly l-lysine dendrimers Mol. Pharm. 5 3 2008 449 463 (Pubitemid 351929829)
33. L. van Vlerken, T. Vyas, and M. Amiji Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery Pharm. Res. 24 8 2007 1405 1414 (Pubitemid 46988224)
34. R.B. Cheyne, and M.G. Moffitt Self-assembly of polystyrene-block- poly(ethylene oxide) copolymers at the Air water interface: is dewetting the genesis of surface aggregate formation? Langmuir 22 20 2006 8387 8396 (Pubitemid 44547062)
35. D. Hoenig, J. DeRouchey, R. Jungmann, C. Koch, C. Plank, and J.O. Raedler Biophysical Characterization of Copolymer-Protected Gene Vectors Biomacromolecules 11 7 2010 1802 1809
36. Y. Kim, J. Pyun, J.M.J. Frechet, C.J. Hawker, and C.W. Frank The dramatic effect of architecture on the self-assembly of block copolymers at interfaces Langmuir 21 23 2005 10444 10458 (Pubitemid 41692118)
37. A. Kichler Gene transfer with modified polyethylenimines J. Genet Med. 6 S1 2004 S3 S10
38. M. Piest, and J.F.J. Engbersen Effects of charge density and hydrophobicity of poly(amido amine)s for non-viral gene delivery J. Control. Release 148 1 2010 83 90
39. L. Sancey, E. Garanger, S. Foillard, G. Schoehn, A. Hurbin, C. Albiges-Rizo, D. Boturyn, C. Souchier, A. Grichine, P. Dumy, and J.-L. Coll Clustering and internalization of integrin [alpha]v[beta]3 with a tetrameric RGD-synthetic peptide Mol. Ther. 17 5 2009 837 843
40. P.T. Caswell, S. Vadrevu, and J.C. Norman Integrins: masters and slaves of endocytic transport Nat. Rev. Mol. Cell Biol. 10 12 2009 843 853
41. M.S. Roberts, A.J. Woods, T.C. Dale, P. van der Sluijs, and J.C. Norman Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of {alpha}v{beta}3 and {alpha}5{beta}1 integrins Mol. Cell. Biol. 24 4 2004 1505 1515 (Pubitemid 38167074)
42. A.J. Woods, D.P. White, P.T. Caswell, and J.C. Norman PKD1/PKC promotes [alpha]v[beta]3 integrin recycling and delivery to nascent focal adhesions EMBO J. 23 13 2004 2531 2543 (Pubitemid 38988225)
43. E.J. Ezratty, C. Bertaux, E.E. Marcantonio, and G.G. Gundersen Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells J. Cell Biol. 187 5 2009 733 747
44. T. Nishimura, and K. Kaibuchi Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3 Dev. Cell 13 1 2007 15 28 (Pubitemid 46972036)
45. B.G. Galvez, S. Matias-Roman, M. Yanez-Mo, M. Vicente-Manzanares, F. Sanchez-Madrid, and A.G. Arroyo Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells Mol. Biol. Cell 15 2 2004 678 687 (Pubitemid 38146484)
46. F. Shi, and J. Sottile Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover J. Cell Sci. 121 14 2008 2360 2371
47. Z. Gu, E.H. Noss, V.W. Hsu, and M.B. Brenner Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration J.Cell Biol. 193 1 2011 61 70
48. M. Lakadamyali, M.J. Rust, and X. Zhuang Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes Cell 124 5 2006 997 1009 (Pubitemid 43344239)
49. R.N. Cohen, M.A.E.M. 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 2 2009 166 174
50. G. Schwake, S. Youssef, J.-T. Kuhr, S. Gude, M.P. David, E. Mendoza, E. Frey, and J.O. Rädler Predictive modeling of non-viral gene transfer Biotechnol. Bioeng. 105 4 2010 805 813
51. D.M. Shayakhmetov, A.M. Eberly, Z.-Y. Li, and A. Lieber Deletion of penton RGD motifs affects the efficiency of both the internalization and the endosome escape of viral particles containing adenovirus serotype 5 or 35 fiber knobs J. Virol. 79 2 2005 1053 1061 (Pubitemid 40053889)
52. A. Chávez, M. Pujol, I. Haro, M.A. Alsina, and Y. Cajal Membrane fusion by an RGD-containing sequence from the core protein VP3 of hepatitis A virus and the RGA-analogue: implications for viral infection Biopolymers 58 1 2001 63 77 (Pubitemid 32064068)