Delivery of therapeutic nucleic acids via transferrin and transferrin receptors: Lipoplexes and other carriers

Expert Opinion on Drug Delivery

Volumn 10, Issue 11, 2013, Pages 1583-1591

  Tros De Ilarduya, Conchita ^a   Düzgüneş, Nejat ^b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF THE PACIFIC   (United States)

Author keywords

Cationic liposomes; IL 12; P53; Receptor recycling; SiRNA; Suicide gene therapy; Transferrin lipoplexes

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; ANTISENSE OLIGONUCLEOTIDE; APOTRANSFERRIN; BETA 2 MICROGLOBULIN; CASPASE 3; CISPLATIN; CYTOSINE DEAMINASE; DIOLEOYLPHOSPHATIDYLETHANOLAMINE; FLUCYTOSINE; FLUOROURACIL; GANCICLOVIR; GEMCITABINE; HLA B7 ANTIGEN; IMATINIB; IMMUNOLIPOSOME; INTERLEUKIN 12; LIPOFECTAMINE; LIPOPLEX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEIC ACID; POLYAMIDOAMINE; POLYETHYLENEIMINE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; SMALL INTERFERING RNA; THYMIDINE KINASE; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNINDEXED DRUG;

ACIDIFICATION; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER REGRESSION; CANCER SURVIVAL; CELL DEATH; CELL PROLIFERATION; COLORECTAL CARCINOMA; COMPLEX FORMATION; CONJUGATE; CYTOTOXICITY; DISSOCIATION; DNA SYNTHESIS INHIBITION; DRUG CONJUGATION; DRUG EFFICACY; ENDOSOME; GENE DIRECTED ENZYME PRODRUG THERAPY; GENE EXPRESSION; GENE THERAPY; GENETIC TRANSFECTION; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; IMMUNOTHERAPY; IN VITRO GENE TRANSFER; IN VITRO STUDY; IN VIVO GENE TRANSFER; IN VIVO STUDY; LIPOSOMAL GENE DELIVERY SYSTEM; LIVER METASTASIS; LUNG CANCER; LUNG METASTASIS; MELANOMA; MEMBRANE FUSION; MYELOID LEUKEMIA; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PANCREAS CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; PROTON TRANSPORT; RECTUM CANCER; REVIEW; SURFACE PROPERTY; TUMOR SUPPRESSOR GENE; TUMOR VOLUME;

ANIMALS; CHEMISTRY, PHARMACEUTICAL; DRUG DELIVERY SYSTEMS; GENES, TRANSGENIC, SUICIDE; GENETIC THERAPY; HUMANS; LIPOSOMES; MOLECULAR TARGETED THERAPY; RECEPTORS, TRANSFERRIN; RNA, SMALL INTERFERING; TRANSFERRIN;

EID: 84886633919     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2013.837447     Document Type: Review

References (72)

1. MacGillivray RT, Mendez E, Shewale JG, et al. The primary structure of human serum transferrin. The structures of seven cyanogen bromide fragments and the assembly of the complete structure. J Biol Chem 1983;258:3543-53
2. Klausner RD, Harford J, van Renswoude J. Rapid internalization of the transferrin receptor in K562 cells is triggered by ligand binding or treatment with a phorbol ester. Proc Natl Acad Sci USA 1984;81:3005-9
3. van Renswoude J, Bridges KR, Harford JB, et al. Receptor-mediated endocytosis of transferrin and the uptake of Fe in K562 cells: identification of a nonlysosomal acidic compartment. Proc Natl Acad Sci USA 1982;79:6186-90
4. Mayle KM, Le AM, Kamei DT. The intracellular trafficking pathway of transferrin. Biochim Biophys Acta 2012;1820:264-81
5. Klausner RD, Ashwell G, van Renswoude J, et al. Binding of apotransferrin to K562 cells: explanation of the transferrin cycle. Proc Natl Acad Sci USA 1983;80:2263-6
6. Daniels TR, Bernabeu E, Rodŕguez JA, et al. The transferrin receptor and the targeted delivery of therapeutic agents against cancer. Biochim Biophys Acta 2012;1820:291-317
7. Wagner E, Zenke M, Cotten M, et al. Transferrin-polycation conjugates as carriers for DNA uptake into cells. Proc Natl Acad Sci USA 1990;87:3410-14
8. Cotten M, Längle-Rouault F, Kirlappos H, et al. Transferrin- polycation-mediated introduction of DNA into human leukemic cells: stimulation by agents that affect the survival of transfected DNA or modulate transferrin receptor levels. Proc Natl Acad Sci USA 1990;87:4033-7
9. Cheng PW. Receptor ligand-facilitated gene transfer: enhancement of liposome-mediated gene transfer and expression by transferrin. Hum Gene Ther 1996;7:275-82
10. Xu L, Pirollo KF, Chang EH. Transferrin-liposome-mediated p53 sensitization of squamous cell carcinoma of the head and neck to radiation in vitro. Hum Gene Ther 1997;8:467-75
11. Simões S, Slepushkin V, Gaspar R, et al. Gene delivery by negatively charged ternary complexes of DNA, cationic liposomes and transferrin or fusigenic peptides. Gene Ther 1998;5:955-64
12. Simões S, Slepushkin V, Gaspar R, et al. Successful transfection of lymphocytes by ternary lipoplexes. Biosci Rep 1999;19:601-9
13. Simões S, Slepushkin V, Pretzer E, et al. Transfection of human macrophages by lipoplexes via the combined use of transferrin and pH-sensitive peptides. J Leukoc Biol 1999;65:270-9
14. Simões S, Slepushkin V, Pires P, et al. Mechanisms of gene transfer mediated by lipoplexes associated with targeting ligands or pH-sensitive peptides. Gene Ther 1999;6:1798-807
15. Xu Y, Szoka FC Jr. Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry 1996;35:5616-23
16. Singh M, Hawtrey A, Ariatti M. Lipoplexes with biotinylated transferrin accessories: novel, targeted, serum-tolerant gene carriers. Int J Pharm 2006;321:124-37
17. Nomura T, Nakajima S, Kawabata K, et al. Intratumoral pharmacokinetics and in vivo gene expression of naked plasmid DNA and its cationic liposome complexes after direct gene transfer. Cancer Res 1997;57:2681-6
18. Blezinger P, Freimark BD, Matar M, et al. Intratracheal administration of interleukin 12 plasmid-cationic lipid complexes inhibits murine lung metastases. Hum Gene Ther 1999;10:723-31
19. Nabel GJ, Gordon D, Bishop DK, et al. Immune response in human melanoma after transfer of an allogenic class I major histocompatibility complex gene with DNA-liposome complexes. Proc Natl Acad Sci USA 1996;93:15388-93
20. Voges J, Reszka R, Gossmann C, et al. Imaging-guided convection-enhanced delivery and gene therapy of glioblastoma. Ann Neurol 2003;54:479-87
21. Li S, Yu B, An P, et al. Combined liposome-mediated cytosine deaminase gene therapy with radiation in killing rectal cancer cells and xenografts in athymic mice. Clin Cancer Res 2005;11:3574-8
22. Sher YP, Tzeng TF, Kan J, et al. Cancer targeted gene therapy of BikDD inhibits orthotopic lung cancer growth and improves long-term survival. Oncogene 2009;28:2123-30
23. Koldehoff M, Steckel NK, Beelen DW, et al. Therapeutic application of small interfering RNA directed against bcr-abl transcripts to a patient with imatinib-resistant chronic myeloid leukaemia. Clin Exp Med 2007;7:47-55
24. Okumura K, Nakase M, Inui M, et al. Bax mRNA therapy using cationic liposomes for human malignant melanoma. J Gene Med 2008;10:910-17
25. Goplan B, Ito I, Branch CD, et al. Nanoparticle based systemic gene therapy for lung cancer: molecular mechanisms and strategies to suppress nanoparticle-mediated inflammatory response. Tech Cancer Res Treat 2004;3:647-57
26. Rubin J, Galanis E, Pitot HC, et al. Phase I study of immunotherapy of hepatic metastases of colorectal carcinoma by direct gene transfer of an allogenic histocompatibility antigen HLA-B7. Gene Ther 1997;4:419-25
27. Hallaj-Nezhadi S, Lotfipour F, Dass C. Nanoparticle-mediated interleukin-12 cancer gene therapy. J Pharm Pharm Sci 2010;13:472-85
28. Rodrigo-Garzón M, Berraondo P, Ochoa L, et al. Antitumoral efficacy of DNA nanoparticles in murine models of lung cancer and pulmonary metastasis. Cancer Gene Ther 2010;17:20-7
29. Ndoye A, Dolivet G, Hogset A, et al. Eradication of p53-mutated head and neck squamous cell carcinoma xenografts using nonviral p53 gene therapy and photochemical internalization. Mol Ther 2006;13:1156-62
30. Wang M, Thanou M. Targeting nanoparticles to cancer. Pharm Res 2010;62:90-9
31. Mei M, Ren Y, Zhou X, et al. Downregulation of miR-21 enhances chemotherapeutic effect of taxol in breast carcinoma cells. Tech Cancer Res 2010;9:77-86
32. Tros de Ilarduya C, Garcia L, Düzgüneş N. Liposomes and lipopolymeric carriers for gene delivery. J Microencapsul 2010;27:602-8
33. Kircheis R, Ostermann E, Wolschek MF, et al. Tumor-targeted gene delivery of tumor necrosis factor-alpha induces tumor necrosis and tumor regression without systemic toxicity. Cancer Gene Ther 2002;9:673-80
34. Ogris M, Walker G, Blesing T, et al. Tumor-targeted gene therapy. Strategies for the preparation of ligand-polyethylene glycol-polyethylenimine/ DNA complexes. J Control Release 2003;91:173-81
35. Sakaguchi N, Kojima C, Harada A, et al. Effect of transferrin as a ligand of pH-sensitive fusogenic liposome-lipoplex hybrid complexes. Bioconjug Chem 2008;19:1588-95
36. Abela RA, Qian J, Xu L, et al. Radiation improves gene delivery by a novel transferrin-lipoplex nanoparticle selectively in cancer cells. Cancer Gene Ther 2008;15:496-507
37. Sing M, Atwall H, Micetich R, et al. Transferrin directed delivery of adriamycin to human cells. Anticancer Res 1998;18:1423-7
38. Kratz F, Beyer U, Roth T, et al. Transferrin conjugates of doxorubicin: synthesis, characterization, cellular uptake, and in vitro efficacy. J Pharm Sci 1998;87:338-46
39. Elliott RL, Stjernholm R, Elliott MC. Preliminary evaluation of platinum transferrin (MPTC-63) as a potential nontoxic treatment for breast cancer. Cancer Detect Prev 1998;12:469-80
40. Beyer U, Roth T, Shumacher P, et al. Synthesis and in vitro efficacy of transferrin conjugates of the anticancer drug chlorambucil. J Med Chem 1998;41:2701-8
41. Tanaka T, Shiramoto S, Miyashita M, et al. Tumor targeting based on the effect of enhanced permeability and retention (EPR) and the mechanism of receptor-mediated endocytosis (RME). Int J Pharm 2004;277:39-61
42. Bejaoui N, Page M, Noel C. Cytotoxicity of transferrin-daunorubicin conjugates on small cell carcinoma of the lung (SCCL) cell line NCl-H69. Anticancer Res 1991;11:2211-13
43. Mayers GL, Raghavan D, Hitt S, et al. Transferrin-gemcitabine conjugate: application to chemotherapy. Proc Am Assoc Cancer Res 1998;89:63
44. Ishida O, Marayuma K, Tanahashi H, et al. Liposomes bearing polyethyleneglycol-coupled transferrin with intra-cellular targeting property to the solid tumors in vivo. Pharm Res 2001;18:1042-8
45. Li X, Ding L, Xu Y, et al. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int J Pharm 2009;373:116-23
46. Iinuma H, Maruyama K, Okinaga K, et al. Intracellular targeting therapy of cisplatin-encapsulated transferrinpolyethylene glycol liposome on peritoneal dissemination of gastric cancer. Int J Cancer 2002;99:130-7
47. Sahoo SK, Ma W, Labhasetwar V. Efficacy of transferrin-conjugated paclitaxel-loaded nanoparticles in a murine model of prostate cancer. Int J Cancer 2004;112:335-40
48. Xu L, Frederik P, Pirollo KF, et al. Self-assembly of a virus-mimicking nanostructure system for efficient tumor-targeted gene delivery. Hum Gene Ther 2002;13:469-81
49. Xu L, Pirollo KF, Tang WH, et al. Transferrin-liposome-mediated systemic p53 gene therapy in combination with radiation results in regression of human head and neck cancer xenografts. Hum Gene Ther 1999;10:2941-52
50. Xu L, Pirollo KF, Chang EH. Transferrin-liposome-mediated p53 sensitization of squamous cell carcinoma of the head and neck to radiation in vitro. Hum Gene Ther 1997;8:467-75
51. Seki M, Iwakawa J, Cheng H, et al. p53 and PTEN/MMAC1/TEP1 gene therapy of human prostate PC-3 carcinoma xenograft, using transferrin-facilitated lipofection gene delivery strategy. Hum Gene Ther 2002;6:761-3
52. Xu L, Tang WH, Huang CC, et al. Systemic p53 gene therapy of cancer with immunolipoplexes targeted by anti-transferrin receptor scFv. Mol Med 2001;7:723-34
53. Xu L, Huang CC, Huang W, et al. Systemic tumor-targeted gene delivery by anti-transferrin receptor scFv-immunoliposomes. Mol Cancer Ther 2002;1:337-46
54. Camp ER, Wang C, Little EC, et al. Transferrin receptor targeting nanomedicine delivering wild-type p53 gene sensitizes pancreatic cancer to gemcitabine therapy. Cancer Gene Ther 2013;20:222-8
55. Yu W, Pirollo KF, Rait A, et al. A sterically stabilized immunolipoplex for systemic administration of a therapeutic gene. Gene Ther 2004;1:1434-40
56. Mendonça LS, Firmino F, Moreira JN, et al. Transferrin receptor-targeted liposomes encapsulating anti-BCR-ABL siRNA or asODN for chronic myeloid leukemia treatment. Bioconjug Chem 2010;21:157-68
57. Davis ME, Zuckerman JE, Choi CH, et al. Evidence of RNAi in humans from systemically administered siRNA via targeted nanoparticles. Nature 2010;464:1067-70
58. Cardoso AL, Simões S, de Almeida LP, et al. siRNA delivery by a transferrin-associated lipid-based vector: a non-viral strategy to mediate gene silencing. J Gene Med 2007;9:170-83
59. Cardoso AL, Simões S, de Almeida LP, et al. Tf-lipoplexes for neuronal siRNA delivery: a promising system to mediate gene silencing in the CNS. J Control Release 2008;2:113-23
60. Cardoso A, Trabulo S, Moreira JN, et al. Targeted lipoplexes for siRNA delivery. Methods Enzymol 2009;465:267-87
61. Cardoso AL, Costa P, de Almeida LP, et al. Tf-lipoplex-mediated c-Jun silencing improves neuronal survival following excitotoxic damage in vivo. J Control Release 2010;142:392-403
62. Tros de Ilarduya C, Buñuales M, Qiang C, et al. Antitumoral activity of transferrin-lipoplexes carrying the IL-12 gene in the treatment of colon cancer. J Drug Target 2006;14:527-35
63. Jin Y, Liu S, Yu B, et al. Targeted delivery of antisense oligodeoxynucleotide by transferrin conjugated pH-sensitive lipopolyplex nanoparticles: a novel oligonucleotide-based therapeutic strategy in acute myeloid leukemia. Mol Pharm 2010;7:196-206
64. Ko YT, Bhattacharya R, Bickel U. Liposome encapsulated polyethylenimine/ODN polyplexes for brain targeting. J Control Release 2009;133:203-7
65. Chiu SJ, Liu S, Perrotti D, et al. Efficient delivery of a Bcl-2-specific antisense oligodeoxyribonucleotide (G3139) via transferrin receptor-targeted liposomes. J Control Release 2006;112:199-207
66. Zhang X, Koh CG, Yu B, et al. Transferrin receptor targeted lipopolyplexes for delivery of antisense oligonucleotide G3139 in a murine K562 xenograft model. Pharm Res 2009;26:1516-24
67. Neves SS, Sarmento-Ribeiro AB, Simoes SP, et al. Transfection of oral cancer cells mediated by transferrin-associated lipoplexes: mechanisms of cell death induced by herpes simplex virus thymidine kinase/ganciclovir therapy. Biochim Biophys Acta 2006;11:1703-12
68. Neves S, Faneca H, Bertin S, et al. Transferrin lipoplex-mediated suicide gene therapy of oral squamous cell carcinoma in an immunocompetent murine model and mechanisms involved in the antitumoral response. Cancer Gene Ther 2009;16:91-101
69. da Cruz MT, Cardoso AL, de Almeida LP, et al. Tf-lipoplex-mediated NGF gene transfer to the CNS:neuronal protection and recovery in an excitotoxic model of brain injury. Gene Ther 2005;16:1242-52
70. Ponka P, Lok CN. The transferrin receptor: role in health and disease. Int J Biochem Cell Biol 1999;31:1111-37
71. Yamada Y, Akita H, Harashima H. Multifunctional envelope-type nano device (MEND) for organelle targeting via a stepwise membrane fusion process. Methods Enzymol 2012;509:301-26
72. Düzgüneş N. A new paradigm for NIH grants. The Scientist 2007;21:24