A review of RGD-functionalized nonviral gene delivery vectors for cancer therapy

Cancer Gene Therapy

Volumn 19, Issue 11, 2012, Pages 741-748

  Park, J ^a   Singha, K ^a   Son, S ^a   Kim, J ^a   Namgung, R ^a   Yun, C O ^b   Kim, W J ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b Hanyang University   (South Korea)

Author keywords

angiogenesis; integrin; nonviral vectors; RGD peptide

Indexed keywords

ACRYLAMIDE DERIVATIVE; ALPHA5 INTEGRIN; ARGINYLGLYCYLASPARTIC ACID; BETA3 INTEGRIN; INTEGRIN RECEPTOR; POLYCATION; POLYMER; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; BREAST CANCER; CANCER CELL CULTURE; CANCER GENE THERAPY; CELL ADHESION; CHEMICAL STRUCTURE; COLON CANCER; DISULFIDE BOND; ELECTRON MICROSCOPY; GENE CONTROL; GENE EXPRESSION; GENE VECTOR; HUMAN; INTRACELLULAR SIGNALING; MICELLE; MOLECULAR RECOGNITION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; REVIEW;

AMINO ACID SEQUENCE; ANGIOGENESIS INHIBITORS; ANIMALS; ENDOTHELIUM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS; INTEGRINS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OLIGOPEPTIDES; PEPTIDES, CYCLIC; POLYETHYLENE GLYCOLS;

EID: 84867746099     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2012.64     Document Type: Review

References (96)

1. Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2007\an update. J Gene Med 9: 833-842.
2. Sheridan C. Gene therapy finds its niche. Nat Biotechnol 2011; 29: 121-128.
3. El-Aneed A. Current strategies in cancer gene therapy. Eur J Pharmacol 2004; 498: 1-8.
4. Guinn BA, Mulherkar R. International progress in cancer gene therapy. Cancer Gene Ther 2008; 15: 765-775.
5. Folkman J, Shing Y. Angiogenesis. J Biol Chem 1992; 267: 10931-10934.
6. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-1186.
7. Tonini T, Rossi F, Claudio PP. Molecular basis of angiogenesis and cancer. Onco-gene 2003; 22: 6549-6556.
8. Folkman J. Angiogenesis. Annu Rev Med 2006; 57: 1-18.
9. Feldman AL, Libutti SK. Progress in antiangiogenic gene therapy of cancer. Cancer 2000; 89: 1181-1194.
10. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 1996; 12: 697-715.
11. Kasono K, Blackwell JL, Douglas JT, Dmitriev I, Strong TV, Reynolds P et al. Selective gene delivery to head and neck cancer cells via an integrin targeted adenoviral vector. Clin Cancer Res 1999; 5: 2571-2579.
12. Matilainen H, Mäkelä AR, Riikonen R, Saloniemi T, Korhonen E, Hyypiä T et al. RGD motifs on the surface of baculovirus enhance transduction of human lung carcinoma cells. J Biotechnol 2006; 125: 114-126.
13. Temming K, Schiffelers RM, Molema G, Kok RJ. RGD-based strategies for selective delivery of therapeutics and imaging agents to the tumor vasculature. Drug Resist Update 2005; 8: 381-402.
14. Eldar-Boock A, Miller K, Sanchis J, Lupu R, Vicent MJ, Satchi-Fainaro R. Integrin-assisted drug delivery of nano-scaled polymer therapeutics bearing paclitaxel. Biomaterials 2011; 32: 3862-3874.
15. Mulligan RC. The basic science of gene therapy. Science 1993; 260: 926-932.
16. Liekens S, De Clercq E, Neyts J. Angiogenesis: regulators and clinical applications. Biochem Pharmacol 2001; 61: 253-270.
17. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995; 1: 27-31.
18. Pierschbacher MD, Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 1984; 309: 30-33.
19. Akiyama SK, Yamada KM. Synthetic peptides competitively inhibit both direct binding to fibroblasts and functional biological assays for the purified cell-binding domain of fibronectin. J Biol Chem 1985; 260: 10402-10405.
20. Cheresh DA, Spiro RC. Biosynthetic and functional properties of an Arg-Gly-Asp-directed receptor involved in human melanoma cell attachment to vitronectin, fibrinogen, and von Willebrand factor. J Biol Chem 1987; 262: 17703-17711.
21. Koivunen E, Wang B, Ruoslahti E. Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Nat Bio-technol 1995; 13: 265-270.
22. Bogdanowich-Knipp SJ, Chakrabarti S, Williams TD, Dillman RK, Siahaan TJ. Solution stability of linear vs. cyclic RGD peptides. J Pept Res 1999; 53: 530-541.
23. Geiger T, Clarke S. Deamidation isomerization, and racemization at asparaginyl and aspartyl residues in peptides. J Biol Chem 1987; 262: 785-794.
24. Wakankar AA, Borchardt RT. Formulation consideration for proteins susceptible to asparagine deamidation and aspartate isomerization. J Pharm Sci 2006; 95: 2321-2336.
25. Pack DW, Hoffman AS, Pun S, Stayton PS. Design and development of polymers for gene delivery. Nat Rev Drug Discovery 2005; 4: 581-593.
26. Lee D, Singha K, Park J, Jo S, Kim WJ. Enhanced gene delivery by palmitic acid-conjugated low molecular weight polyethylenimine. Macromol Res 2012; 20: 244-249.
27. Singha K, Namgung R, Kim WJ. Polymers in small-interfering RNA delivery. Nucleic Acid Ther 2011; 21: 133-147.
28. Morille M, Passirani C, Vonarbourg A, Clavreul A, Benoit JP. Progress in developing cationic vectors for non-viral systemic gene therapy against cancer. Biomaterials 2008; 29: 3477-3496.
29. Park J, Kim WJ. Current status of gene delivery: spotlight on nanomaterial-poly-mer hybrids. J Drug Targeting 2012; 20: 648-666.
30. Namgung R, Singha K, Yu MK, Jon S, Kim YS, Ahn Y et al. Hybrid super-paramagnetic iron oxide nanoparticle-branched polyethylenimine magneto-plexes for gene transfection of vascular endothelial cells. Biomaterials 2010; 31: 4204-4213.
31. Namgung R, Zhang Y, Fang QL, Singha K, Lee HJ, Kwon IK et al. Multifunctional silica nanotubes for dual-modality gene delivery and MR imaging. Biomaterials 2011; 32: 3042-3052.
32. Zhao XB, Lee RJ. Tumor-selective targeted delivery of genes and antisense oligodeoxyribonucleotides via the folate receptor. Adv Drug Deliver Rev 2004; 56: 1193-1204.
33. Son S, Singha K, Kim WJ. Bioreducible BPEI-SS-PEG-cNGR polymer as a tumor targeted nonviral gene carrier. Biomaterials 2010; 31: 6344-6354.
34. Bellocq NC, Pun SH, Jensen GS, Transferrin-containing Davis ME. cyclodextrin polymer-based particles for tumor-targeted gene delivery. Bioconjugate Chem 2003; 14: 1122-1132.
35. Pan X, Guan J, Yoo J-W, Epstein AJ, Lee LJ, Lee RJ. Cationic lipid-coated magnetic nanoparticles associated with transferring for gene delivery. Int J Pharm 2008; 358: 263-270.
36. Suh W, Chung JK, Park SH, Kim SW. Anti-JL1 antibody-conjugated poly(L-lysine) for targeted gene delivery to leukemia T cells. J Control Release 2001; 72: 171-178.
37. Lee CH, Hsiao M, Tseng YL, Chang FH. Enhanced gene delivery to HER-2-over-expressing breast cancer cells by modified immunolipoplexes conjugated with the anti-HER-2 antibody. J Biomed Sci 2003; 10: 337-344.
38. Lungwitz U, Breunig M, Blunk T, Göpferich A. Polyethylenimine-based non-viral gene delivery systems. Eur J Pharm Biopharm 2005; 60: 247-266.
39. Suh W, Han SO, Yu L, Kim SW. An angiogenic, endothelial-cell-targeted polymeric gene carrier. Mol Ther 2002; 6: 664-672.
40. Kim WJ, Yockman JW, Lee M, Jeong JH, Kim YH, Kim SW. Soluble Flt-1 gene delivery using PEI-g-PEG-RGD conjugate for anti-angiogenesis. J Control Release 2005; 106: 224-234.
41. Kim WJ, Yockman JW, Jeong JH, Christensen LV, Lee M, Kim YH et al. Anti-angio-genic inhibition of tumor growth by systemic delivery of PEI-g-PEG-RGD/pCMV-sFlt-1 complexes in tumor-bearing mice. J Control Release 2006; 114: 381-388.
42. Fenske DB, MacLachlan I, Cullis PR. Long-circulating vectors for the systemic delivery of genes. Curr Opin Mol Ther 2001; 3: 153-158.
43. Dash PR, Read ML, Barrett LB, Wolfert MA, Seymour LW. Factors affecting blood clearance and in vivo distribution of polyelectrolyte complexes for gene delivery. Gene Ther 1999; 6: 643-650.
44. Yockman JW, Kim WJ, Chang C-W, Kim SW. Non-viral delivery of interleukin-2 and soluble Flk-1 inhibits metastatic and primary tumor growth in renal cell carcinoma. Gene Ther 2007; 14: 1399-1405.
45. Kim J, Kim SW, Kim WJ. PEI-g-PEG-RGD/small interference RNA polyplex-mediated silencing of vascular endothelial growth factor receptor and its potential as an anti-angiogenic tumor therapeutic strategy. Oligonucleotides 2011; 21: 101-107.
46. Schiffelers RM, Ansari A, Xu J, Zhou Q, Tang Q, Storm G et al. Cancer siRNA therapy by tumor selective delivery with ligand-targeted sterically stabilized nanoparticle. Nucleic Acids Res 2004; 32: e149.
47. Erbacher P, Remy J-S, Behr J-P. Gene transfer with synthetic virus-like particles via the integrin-mediated endocytosis pathway. Gene Ther 1999; 6: 138-145.
48. Bai J, Acan B, Ghahary A, Ritchie B, Somayaji V, Uludag H. Poly(ethyleneimine)/arginine-glycine-aspartic acid conjugates prepared with N-succinimidyl 3-(2-pyr-idyldithio)propionate: an investigation of peptide coupling and conjugate stability. J Polym Sci Pol Chem 2004; 42: 6143-6156.
49. Namgung R, Nam S, Kim SK, Son S, Singha K, Kwon J-S et al. An acid-labile temperature-responsive sol-gel reversible polymer for enhanced gene delivery to the myocardium and skeletal muscle cells. Biomaterials 2009; 30: 5225-5233.
50. Park I-K, Singha K, Arote RB, Choi Y-J, Kim WJ, Cho C-S. pH-responsive polymers as gene carriers. Macromol Rapid Commun 2010; 31: 1122-1133.
51. Son S, Kim WJ. Biodegradable nanoparticles modified by branced poly-ethylenimine for plasmid DNA delivery. Biomaterials 2010; 31: 133-143.
52. Breunig M, Lungwitz U, Liebl R, Fontanari C, Klar J, Kurtz A et al. Gene delivery with low molecular weight linear polyethylenimines. J Gene Med 2005; 7: 1287-1298.
53. Namgung R, Kim J, Singha K, Kim C-H, Kim WJ. Synergistic effect of low cytotoxic linear polyethylenimine and multiarm polyethylene glycol: study of physico-chemical properties and in vitro gene transfection. Mol Pharm 2009; 6: 1826-1835.
54. Kim T, Kim SW. Bioreducible polymers for gene delivery. React Funct Polym 2011; 71: 344-349.
55. Christensen LV, Chang CW, Kim WJ, Kim SW, Zhong Z, Lin C et al. Reducible poly(amido ethylenimine)s designed for triggered intracellular gene delivery. Bioconjugate Chem 2006; 17: 1233-1240.
56. Son S, Namgung R, Kim J, Singha K, Kim WJ. Bioreducible polymers for gene silencing and delivery. Acc Chem Res 2012; 45: 1100-1112.
57. Sun YX, Zeng X, Meng QF, Zhang XZ, Cheng SX, Zhuo RX. The influence of RGD addition on the gene transfer characteristics of disulfide-containing poly-ethyleneimine/DNA complexes. Biomaterials 2008; 29: 4356-4365.
58. Kabanov AV, Kabanov VA. DNA complexes with polycations for the delivery of genetic material into cells. Bioconjugate Chem 1995; 6: 7-20.
59. Maruyama K, Iwasaki F, Takizawa T, Yanagie H, Niidome T, Yamada E et al. Novel receptor-mediated gene delivery system comprising plasmid/protamine/sugar- containing polyanion ternary complex. Biomaterials 2004; 25: 3267-3273.
60. Plank C, Mechtler K, Szoka Jr FC, Wagner E. Activation of the complement system by synthetic DNA complexes: a potential barrier for intravenous gene delivery. Hum Gene Ther 1996; 7: 1437-1446.
61. 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.
62. Trubetskoy VS, Wong SC, Subbotin V, Budker VG, Loomis A, Hagstrom JE et al. Recharging cationic DNA complexes with highly charged polyanions for in vitro and in vivo gene delivery. Gene Ther 2003; 10: 261-271.
63. Koyama Y, Yamada E, Ito T, Mizutani Y, Yamaoka T. Sugar-containing polyanions as a self-assembled coating of plasmid/polycation complexes for receptor-mediated gene delivery. Macromol Biosci 2002; 2: 251-256.
64. Arigita C, Zuidam NJ, Crommelin DJ, Hennink WE. Association and dissociation characteristics of polymer/DNA complexes used for gene delivery. Pharm Res 1999; 16: 1534-1541.
65. Koyama Y, Ito T, Matsumoto H, Tanioka A, Okuda T, Yamaura N et al. Novel poly(ethylene glycol) derivatives with carboxylic acid pendant groups: synthesis and their protection and enhancing effect on non-viral gene transfection systems. J Biomater Sci Polym Ed 2003; 14: 515-531.
66. Sakae M, Ito T, Yoshihara C, Iida-Tanaka N, Yanagie H, Eriguchi M et al. Highly efficient in vivo gene transfection by plasmid/PEI complexes coated by anionic PEG derivatives bearing carboxyl groups and RGD peptide. Biomed Pharmacother 2008; 62: 448-453.
67. Oishi J, Ijuin M, Sonoda T, Kang J-H, Kawamura K, Mori T et al. A protein kinase signal-responsive gene carrier modified RGD peptide. Bioorg Med Chem Lett 2006; 16: 5740-5743.
68. Carlson CC, Smithers SL, Yeh KA, Burnham LL, Dransfield DT. Protein kinase A regulatory subunits in colon cancer. Neoplasia 1999; 4: 373-378.
69. Kenneth WL, Barbara L, Richard MN. Retinoic acid increases cyclic AMP-dependent protein kinase activity in murine melanoma cells. J Biol Chem 1980; 255: 5999-6002.
70. Katayama Y, Fujii K, Ito E, Sakakihara S, Sonoda T, Murata M et al. Intracellular signal-responsive artificial gene regulation for novel gene delivery. Biomacro-molecules 2002; 3: 905-909.
71. Oishi J, Kawamura K, Kang J-H, Kodama K, Sonoda T, Murata M et al. An intra-cellular kinase signal-responsive gene carrier for disordered cell-specific gene therapy. J Control Release 2006; 110: 431-436.
72. Kakizawa Y, Kataoka K. Block copolymer micelles for delivery of gene and related compounds. Adv Drug Deliv Rev 2002; 54: 203-222.
73. Osada K, Kataoka K. Drug and gene delivery based on supramolecular assembly of PEG-polypeptide hybrid block copolymers. Adv Polym Sci 2006; 202: 113-153.
74. Akagi D, Oba M, Koyama H, Nishiyama N, Fukushima S, Miyata T et al. Bio-compatible micellar nanovectors achieve efficient gene transfer to vascular lesions without cytotoxicity and thrombus formation. Gene Ther 2007; 14: 1029-1038.
75. 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.
76. Miyata K, Kakizawa Y, Nishiyama N, Yamasaki Y, Watanabe T, Kohara M et al. Freeze-dried formulations for in vivo gene delivery of PEGylated polyplex micelles with disulfide crosslinked cores to the liver. J Control Release 2005; 109: 15-23.
77. 5 integrins. Bioconjugate Chem 2007; 18: 1415-1423.
78. Kagaya H, Oba M, Miura Y, Koyama H, Ishii T, Shimada T et al. Impact of polyplex micelles installed with cyclic RGD peptides as ligand on gene delivery to vascular lesions. Gene Ther 2012; 19: 61-69.
79. 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.
80. Mickler FM, 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.
81. Vachutinsky Y, Oba M, Miyata K, Hiki S, Kano MR, Nishiyama N et al. Anti-angiogenic 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.
82. Kaneda Y, Saeki Y, Morishita R. Gene therapy using HVJ-liposomes: the best of both worlds? Mol Med Today 1999; 5: 298-303.
83. Chander R, Schreier H. Artificial viral envelopes containing recombinant human immunodeficiency virus (HIV) gp 160. Life Sci 1992; 50: 481-489.
84. Müller K, Nahde T, Fahr A, Müller R, Brüsselbach S. Highly efficient transduction of endothelial cells by targeted artificial virus-like particles. Cancer Gene Ther 2001; 8: 107-117.
85. Anwer K, Kao G, Rolland A, Driessen WH, Sullivan SM. Peptide-mediated gene transfer of cationic lipid/plasmid DNA complexes to endothelial cells. J Drug Target 2004; 12: 215-221.
86. Thompson B, Mignet N, Hofland H, Lamons D, Seguin J, Nicolazzi C et al. Neutral postgrafted colloidal particles for gene delivery. Bioconjugate Chem 2005; 16: 608-614.
87. Harvie P, Dutzar B, Galbraith T, Cudmore S, O'Mahony D, Anklesaria P et al. Targeting of lipid-protamine-DNA (LPD) lipopolyplexes using RGD motifs. J Liposome Res 2003; 13: 231-247.
88. Kibria G, Hatakeyama H, Ohga N, Hida K, Harashima H. Dual-ligand modification of PEGylated liposomes shows better cell selectivity and efficient gene delivery. J Control Release 2011; 153: 141-148.
89. Jiang J, Yang S-J, Wang J-C, Yang L-J, Xu Z-Z, Yang T et al. Sequential treatment of drug-resistant tumors with RGD-modified liposomes containing siRNA or doxor-ubicin. Eur J Pharm Biopharm 2010; 76: 170-178.
90. Smith LC, Duguid J, Wadhwa MS, Logan MJ, Tung C-H, Edwards V et al. Synthetic peptide-based DNA complexes for nonviral gene delivery. Adv Drug Deliv Rev 1998; 30: 115-131.
91. Parker AL, Collins L, Zhang X, Fabre JW. Exploration of peptide motifs for potent non-viral gene delivery highly selective for dividing cells. J Gene Med 2005; 7: 1545-1554.
92. Aoki Y, Hosaka S, Kawa S, Kiyosawa K. Potential tumor-targeting peptide vector of histidylated oligolysine conjugated to a tumor-homing RGD motif. Cancer Gene Ther 2001; 8: 783-787.
93. Moore NM, Barbour TR, Sakiyama-Elbert SE. Synthesis and characterization of four-arm poly(ethylene glycol)-based gene delivery vehicles coupled to integrin and DNA-binding peptides. Mol Pharm 2007; 5: 140-150.
94. Moore NM, Sakiyama-Elbert SE. Analysis of cell binding and internalization of mul-tivalent PEG-based gene delivery vehicles. IEEE Trans Nanobiosci 2012; 11: 54-61.
95. Isberg RR. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science 1991; 252: 934-938.
96. Kornberg LJ, Earp HS, Turner CE, Prockop C, Juliano RL. Signal transduction by integrins: increased protein tyrosine phosphorylation caused by clustering of beta 1 integrins. Proc Natl Acad Sci USA 1991; 88: 8392-8396.