Bacteriophages as vehicles for gene delivery into mammalian cells: Prospects and problems

Expert Opinion on Drug Delivery

Volumn 11, Issue 10, 2014, Pages 1561-1574

  Bakhshinejad, Babak ^a   Sadeghizadeh, Majid ^a  

^a TARBIAT MODARES UNIVERSITY   (Iran)

Author keywords

Bacteriophage; Gene delivery; Gene therapy; Intracellular barriers; Phage display; Targeting

Indexed keywords

PROTEASOME;

BACTERIOPHAGE; CELL MIGRATION; CELL NUCLEUS MEMBRANE; ENDOCYTOSIS; ENDOSOME; GENE EXPRESSION; GENE LOCATION; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSDUCTION; INTERNALIZATION; INTRANUCLEAR SPACE; LYSOSOME; MAMMAL CELL; NONHUMAN; PHAGE DISPLAY; REVIEW; TROPISM; ANIMAL; GENE THERAPY; GENE TRANSFER; GENE VECTOR; GENETICS; HUMAN; PROCEDURES;

ANIMALS; BACTERIOPHAGES; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS;

EID: 84905575652     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2014.927437     Document Type: Review

References (104)

1. Ibraheem D, Elaissari A, Fessi H. Gene therapy and DNA delivery systems. Int J Pharm 2014;459(1-2):70-83
2. Seow Y, Wood MJ. Biological gene delivery vehicles: Beyond viral vectors. Mol Ther 2009;17(5):767-77
3. Michael SI, Curiel DT. Strategies to achieve targeted gene delivery via the receptor-mediated endocytosis pathway. Gene Ther 1994;1(4):223-32
4. Nayerossadat N, Maedeh T, Ali PA. Viral and nonviral delivery systems for gene delivery. Adv Biomed Res 2012;1:27
5. Alba R, Baker AH, Nicklin SA. Vector systems for prenatal gene therapy: Principles of adenovirus design and production. Methods Mol Biol 2012;891:55-84
6. nnenmacher M, Weber T. Intracellular transport of recombinant adenoassociated virus vectors. Gene Ther 2012;19(6):649-58
7. Maetzig T, Galla M, Baum C, et al. Gammaretroviral vectors: Biology, technology and application. Viruses 2011;3(6):677-713
8. Cooray S, Howe SJ, Thrasher AJ. Retrovirus and lentivirus vector design and methods of cell conditioning. Methods Enzymol 2012;507:29-57
9. Cockrell AS, Kafri T. Gene delivery by lentivirus vectors. Mol Biotechnol 2007;36(3):184-204
10. Bhavsar MD, Amiji MM. Polymeric nano-And microparticle technologies for oral gene delivery. Expert Opin Drug Del 2007;4(3):197-213
11. Duzgunes N, de Ilarduya CT. Genetic nanomedicine: Gene delivery by targeted lipoplexes. Methods Enzymol 2012;509:355-67
12. Schmidt-Wolf GD, Schmidt-Wolf IG. Non-viral and hybrid vectors in human gene therapy: An update. Trends Mol Med 2003;9(2):67-72
13. Lowenstein PR, Mandel RJ, Xiong WD, et al. Immune responses to adenovirus and adeno-Associated vectors used for gene therapy of brain diseases: The role of immunological synapses in understanding the cell biology of neuroimmune interactions. Curr Gene Ther 2007;7(5):347-6
14. Nayak S, Herzog RW. Progress and prospects: Immune responses to viral vectors. Gene Ther 2010;17(3):295-304
15. Daniel R, Smith JA. Integration site selection by retroviral vectors: Molecular mechanism and clinical consequences. Hum Gene Ther 2008;19(6):557-68
16. Clark JR, March JB. Bacteriophages and biotechnology: Vaccines, gene therapy and antibacterials. Trends Biotechnol 2006;24(5):212-18
17. Dabrowska K, Switala-Jelen K, Opolski A, et al. Bacteriophage penetration in vertebrates. J Appl Microbiol 2005;98(1):7-13
18. Gorski A, Dabrowska K, Switala-Jelen K, et al. New insights into the possible role of bacteriophages in host defense and disease. Med Immunol 2003;2(1):2
19. Petty NK, Evans TJ, Fineran PC, et al. Biotechnological exploitation of bacteriophage research. Trends Biotechnol 2007;25(1):7-15
20. Hambly E, Suttle CA. The viriosphere, diversity, and genetic exchange within phage communities. Curr Opin Microbiol 2005;8(4):444-50
21. Yacoby I, Benhar I. Targeted filamentous bacteriophages as therapeutic agents. Expert Opin Drug Del 2008;5(3):321-9
22. Lederberg J. Smaller fleas. ad infinitum: Therapeutic bacteriophage redux. Proc Natl Acad Sci USA 1996;93(8):3167-8
23. Larocca D, Burg MA, Jensen-Pergakes K, et al. Evolving phage vectors for cell targeted gene delivery. Curr Pharm Biotechnol 2002;3(1):45-57
24. Jepson CD, March JB. Bacteriophage lambda is a highly stable DNA vaccine delivery vehicle. Vaccine 2004;22(19):2413-19
25. Reynaud A, Cloastre L, Bernard J, et al. Characteristics and diffusion in the rabbit of a phage for Escherichia coli 0103. Attempts to use this phage for therapy. Vet Microbiol 1992;30(2-3):203-12
26. Hildebrand GJ, Wolochow H. Translocation of bacteriophage across the intestinal wall of the rat. Proc Soc Exp Biol Med 1962;109:183-5
27. Weber-Dabrowska B, Dabrowski M, Slopek S. Studies on bacteriophage penetration in patients subjected to phage therapy. Arch Immunol Ther Exp 1987;35(5):563-8
28. Maruyama IN, Brenner S. A selective lambda phage cloning vector with automatic excision of the insert in a plasmid. Gene 1992;120(2):135-41
29. Merril CR, Biswas B, Carlton R, et al. Long-circulating bacteriophage as antibacterial agents. Proc Natl Acad Sci USA 1996;93(8):3188-92
30. Baker ML, Jiang W, Rixon FJ, et al. Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 2005;79(23):14967-70
31. Benson SD, Bamford JK, Bamford DH, et al. Does common architecture reveal a viral lineage spanning all three domains of life? Mol Cell 2004;16(5):673-85
32. Thomas CE, Ehrhardt A, Kay MA. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 2003;4(5):346-58
33. Paillard F. Bacteriophage: Tools toward a cell-Targeted delivery. Hum Gene Ther 1998;9(16):2307-8
34. Larocca D, Kassner PD, Witte A, et al. Gene transfer to mammalian cells using genetically targeted filamentous bacteriophage. FASEB J 1999;13(6):727-34
35. Larocca D, Baird A. Receptor-mediated gene transfer by phage-display vectors: Applications in functional genomics and gene therapy. Drug Discov Today 2001;6(15):793-801
36. Lankes HA, Zanghi CN, Santos K, et al. In vivo gene delivery and expression by bacteriophage lambda vectors. J Appl Microbiol 2007;102(5):1337-49
37. Merril CR, Geier MR, Petricciani JC. Bacterial virus gene expression in human cells. Nature 1971;233(5319):398-400
38. Geier MR, Merril CR. Lambda phage transcription in human fibroblasts. Virology 1972;47(3):638-43
39. Ishiura M, Hirose S, Uchida T, et al. Phage particle-mediated gene transfer to cultured mammalian cells. Mol Cell Biol 1982;2(6):607-16
40. Okayama H, Berg P. Bacteriophage lambda vector for transducing a cDNA clone library into mammalian cells. Mol Cell Biol 1985;5(5):1136-42
41. Yokoyama-Kobayashi M, Kato S. Recombinant f1 phage particles can transfect monkey COS-7 cells by DEAE dextran method. Biochem Biophys Res Commun 1993;192(2):935-9
42. Yokoyama-Kobayashi M, Kato S. Recombinant f1 phage-mediated transfection of mammalian cells using lipopolyamine technique. Anal Biochem 1994;223(1):130-4
43. Smith GP. Filamentous fusion phage: Novel expression vectors that display cloned antigens on the virion surface. Science 1985;228(4705):1315-17
44. Larocca D, Witte A, Johnson W, et al. Targeting bacteriophage to mammalian cell surface receptors for gene delivery. Hum Gene Ther 1998;9(16):2393-9
45. Eguchi A, Akuta T, Okuyama H, et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J Biol Chem 2001;276(28):26204-10
46. Zanghi CN, Sapinoro R, Bradel-Tretheway B, et al. A tractable method for simultaneous modifications to the head and tail of bacteriophage lambda and its application to enhancing phage-mediated gene delivery. Nucleic Acids Res 2007;35(8):e59
47. Clark JR, March JB. Bacteriophage-mediated nucleic acid immunisation. FEMS Immunol Med Microbiol 2004;40(1):21-6
48. March JB, Clark JR, Jepson CD. Genetic immunisation against hepatitis B using whole bacteriophage lambda particles. Vaccine 2004;22(13-14):1666-71
49. Khalaj-Kondori M, Sadeghizadeh M, Behmanesh M, et al. Chemical coupling as a potent strategy for preparation of targeted bacteriophage-derived gene nanocarriers into eukaryotic cells. J Gene Med 2011;13(11):622-31
50. Rakover IS, Zabavnik N, Kopel R, et al. Antigen-specific therapy of EAE via intranasal delivery of filamentous phage displaying a myelin immunodominant epitope. J Neuroimmunol 2010;225(1-2):68-76
51. Kassner PD, Burg MA, Baird A, et al. Genetic selection of phage engineered for receptor-mediated gene transfer to mammalian cells. Biochem Biophys Res Commun 1999;264(3):921-8
52. Piersanti S, Cherubini G, Martina Y, et al. Mammalian cell transduction and internalization properties of lambda phages displaying the full-length adenoviral penton base or its central domain. J Mol Med (Berl) 2004;82(7):467-76
53. Di Giovine M, Salone B, Martina Y, et al. Binding properties, cell delivery, and gene transfer of adenoviral penton base displaying bacteriophage. Virology 2001;282(1):102-12
54. Poul MA, Marks JD. Targeted gene delivery to mammalian cells by filamentous bacteriophage. J Mol Biol 1999;288(2):203-11
55. Kato Y, Sugiyama Y. Targeted delivery of peptides, proteins, and genes by receptormediated endocytosis. Crit Rev Ther Drug Carrier Syst 1997;14(3):287-331
56. Sapinoro R, Volcy K, Rodrigo WW, et al. Fc receptor-mediated, antibodydependent enhancement of bacteriophage lambda-mediated gene transfer in mammalian cells. Virology 2008;373(2):274-86
57. Ivanenkov VV, Felici F, Menon AG. Targeted delivery of multivalent phage display vectors into mammalian cells. Biochim Biophys Acta 1999;1448(3):463-72
58. Wang J, Tian S, Petros RA, et al. The complex role of multivalency in nanoparticles targeting the transferrin receptor for cancer therapies. J Am Chem Soc 2010;132(32):11306-13
59. Ghaemi A, Soleimanjahi H, Gill P, et al. Recombinant lambda-phage nanobioparticles for tumor therapy in mice models. Genet Vaccines Ther 2010;8:3
60. Uppala A, Koivunen E. Targeting of phage display vectors to mammalian cells. Comb Chem High Throughput Screen 2000;3(5):373-92
61. Lakadamyali M, Rust MJ, Zhuang X. Endocytosis of influenza viruses. Microbes Infect 2004;6(10):929-36
62. Sanchez A. Analysis of filovirus entry into vero e6 cells, using inhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. J Infect Dis 2007;196(Suppl 2):S251-8
63. Hong SS, Gay B, Karayan L, et al. Cellular uptake and nuclear delivery of recombinant adenovirus penton base. Virology 1999;262(1):163-77
64. Plank C, Oberhauser B, Mechtler K, et al. The influence of endosomedisruptive peptides on gene transfer using synthetic virus-like gene transfer systems. J Biol Chem 1994;269(17):12918-24
65. Cotten M, Wagner E, Zatloukal K, et al. High-efficiency receptor-mediated delivery of small and large (48 kilobase gene constructs using the endosomedisruption activity of defective or chemically inactivated adenovirus particles. Proc Natl Acad Sci USA 1992;89(13):6094-8
66. Wagner E, Plank C, Zatloukal K, et al. Influenza virus hemagglutinin HA-2 N-Terminal fusogenic peptides augment gene transfer by transferrin-polylysine-DNA complexes: Toward a synthetic virus-like gene-Transfer vehicle. Proc Natl Acad Sci USA 1992;89(17):7934-8
67. Akache B, Grimm D, Shen X, et al. A two-hybrid screen identifies cathepsins B and L as uncoating factors for adenoassociated virus 2 and 8. Mol Ther 2007;15(2):330-9
68. Qiu Z, Hingley ST, Simmons G, et al. Endosomal proteolysis by cathepsins is necessary for murine coronavirus mouse hepatitis virus type 2 spike-mediated entry. J Virol 2006;80(12):5768-76
69. Chandran K, Sullivan NJ, Felbor U, et al. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 2005;308(5728):1643-5
70. Schornberg K, Matsuyama S, Kabsch K, et al. Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J Virol 2006;80(8):4174-8
71. Ebert DH, Deussing J, Peters C, et al. Cathepsin L and cathepsin B mediate reovirus disassembly in murine fibroblast cells. J Biol Chem 2002;277(27):24609-17
72. Golden JW, Bahe JA, Lucas WT, et al. Cathepsin S supports acid-independent infection by some reoviruses. J Biol Chem 2004;279(10):8547-57
73. Moriuchi H, Moriuchi M, Fauci AS. Cathepsin G, a neutrophil-derived serine protease, increases susceptibility of macrophages to acute human immunodeficiency virus type 1 infection. J Virol 2000;74(15):6849-55
74. Volcy K, Dewhurst S. Proteasome inhibitors enhance bacteriophage lambda (lambda) mediated gene transfer in mammalian cells. Virology 2009;384(1):77-87
75. Uddin S, Ahmed M, Bavi P, et al. Bortezomib (Velcade) induces p27Kip1 expression through Sphasekinase protein 2 degradation in colorectal cancer. Cancer Res 2008;68(9):3379-88
76. Saeki Y, Tanaka K. Assembly and function of the proteasome. Methods Mol Biol 2012;832:315-37
77. Rastogi N, Mishra DP. Therapeutic targeting of cancer cell cycle using proteasome inhibitors. Cell Div 2012;7(1):26
78. Ros C, Burckhardt CJ, Kempf C. Cytoplasmic trafficking of minute virus of mice: Low-pH requirement, routing to late endosomes, and proteasome interaction. J Virol 2002;76(24):12634-45
79. Ros C, Kempf C. The ubiquitinproteasome machinery is essential for nuclear translocation of incoming minute virus of mice. Virology 2004;324(2):350-60
80. Chen YT, Lin CH, Ji WT, et al. Proteasome inhibition reduces avian reovirus replication and apoptosis induction in cultured cells. J Virol Methods 2008;151(1):95-100
81. Douar AM, Poulard K, Stockholm D, et al. Intracellular trafficking of adenoassociated virus vectors: Routing to the late endosomal compartment and proteasome degradation. J Virol 2001;75(4):1824-33
82. Jennings K, Miyamae T, Traister R, et al. Proteasome inhibition enhances AAV-mediated transgene expression in human synoviocytes in vitro and in vivo. Mol Ther 2005;11(4):600-7
83. Schwartz O, Marechal V, Friguet B, et al. Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J Virol 1998;72(5):3845-50
84. Tang SC, Sambanis A, Sibley E. Proteasome modulating agents induce rAAV2-mediated transgene expression in human intestinal epithelial cells. Biochem Biophys Res Commun 2005;331(4):1392-400
85. Wu X, Anderson JL, Campbell EM, et al. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc Natl Acad Sci U S A 2006;103(19):7465-70
86. Yan Z, Zak R, Luxton GW, et al. Ubiquitination of both adeno-Associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J Virol 2002;76(5):2043-53
87. Yan Z, Zak R, Zhang Y, et al. Distinct classes of proteasome-modulating agents cooperatively augment recombinant adeno-Associated virus type 2 and type 5-mediated transduction from the apical surfaces of human airway epithelia. J Virol 2004;78(6):2863-74
88. Dean DA, Strong DD, Zimmer WE. Nuclear entry of nonviral vectors. Gene Ther 2005;12(11):881-90
89. Conti E, Izaurralde E. Nucleocytoplasmic transport enters the atomic age. Curr Opin Cell Biol 2001;13(3):310-19
90. McLane LM, Corbett AH. Nuclear localization signals and human disease. IUBMB Life 2009;61(7):697-706
91. Imamoto N, Kamei Y, Yoneda Y. Nuclear transport factors: Function, behavior and interaction. Eur J Histochem 1998;42(1):9-20
92. Zanta MA, Belguise-Valladier P, Behr JP. Gene delivery: A single nuclear localization signal peptide is sufficient to carry DNA to the cell nucleus. Proc Natl Acad Sci USA 1999;96(1):91-6
93. Ludtke JJ, Zhang G, Sebestyen MG, et al. A nuclear localization signal can enhance both the nuclear transport and expression of 1 kb DNA. J Cell Sci 1999;112(Pt 12):2033-41
94. Cohen S, Au S, Pante N. How viruses access the nucleus. Biochim Biophys Acta 2011;1813(9):1634-45
95. Whittaker GR, Kann M, Helenius A. Viral entry into the nucleus. Ann Rev Cell Dev Biol 2000;16:627-51
96. Akuta T, Eguchi A, Okuyama H, et al. Enhancement of phage-mediated gene transfer by nuclear localization signal. Biochem Biophys Res Commun 2002;297(4):779-86
97. Nakanishi M, Eguchi A, Akuta T, et al. Basic peptides as functional components of non-viral gene transfer vehicles. Curr Protein Pep Sci 2003;4(2):141-50
98. Redrejo-Rodriguez M, Munoz-Espin D, Holguera I, et al. Functional eukaryotic nuclear localization signals are widespread in terminal proteins of bacteriophages. Proc Natl Acad Sci USA 2012;109(45):18482-7
99. Mencia M, Gella P, Camacho A, et al. Terminal protein-primed amplification of heterologous DNA with a minimal replication system based on phage Phi29. Proc Natl Acad Sci U S A 2011;108(46):18655-60
100. Redrejo-Rodriguez M, Munoz-Espin D, Holguera I, et al. Nuclear localization signals in phage terminal proteins provide a novel gene delivery tool in mammalian cells. Commun Integr Biol 2013;6(2):e22829
101. Le Y, Gagneten S, Tombaccini D, et al. Nuclear targeting determinants of the phage P1 cre DNA recombinase. Nucleic Acids Res 1999;27(24):4703-9
102. Glover DJ, Leyton DL, Moseley GW, et al. The efficiency of nuclear plasmid DNA delivery is a critical determinant of transgene expression at the single cell level. J Gene Med 2010;12(1):77-85
103. Hama S, Akita H, Ito R, et al. Quantitative comparison of intracellular trafficking and nuclear transcription between adenoviral and lipoplex systems. Mol Ther 2006;13(4):786-94
104. Moisy D, Avilov SV, Jacob Y, et al. HMGB1 protein binds to influenza virus nucleoprotein and promotes viral replication. J Virol 2012;86(17):9122-33