Emerging significance of plasmid DNA nuclear import in gene therapy

Advanced Drug Delivery Reviews

Volumn 55, Issue 6, 2003, Pages 749-760

  Munkonge, Felix M ^a,b   Dean, David A ^c   Hillery, Elizabeth ^a,b   Griesenbach, Uta ^a,b   Alton, Eric W F W ^a,b  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b UK Cystic Fibrosis Gene Therapy Consortium   (United Kingdom)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cyto nucleoplasmic transport; Gene therapy; Nonviral gene transfer; Nuclear import; Nuclear localising signals; Nuclear localising signals (NLS); Peptide nucleic acid (PNA); Plasmid DNA (pDNA)

Indexed keywords

BIOASSAY; CELLS; DETERGENTS; GENETIC ENGINEERING;

GENE TRANSFER;

DNA;

ARGINYLGLUTAMYLALANYLARGINYLARGINYLASPARAGINYLARGINYLARGINYLARGINYLARGIN YLT RYPTOPHYLARGINYLGLUTAMYLARGINYLGLUTAMYLARGINYLGLUTAMINE; GLYCYLARGINYLLYSYLLYSYLARGINYLARGINYLGLUTAMYLARGINYLARGINYLARGINYLALANYL PRO LINE; LYSYLARGINYLPROLYLALANYLALANYLTHREONYLLYSYLLYSYLALANYLGLYCYLGLUTAMINYLAL ANY LLYSYLLYSYLLYSYLLYSINE; AMINO ACID; ASIALOFETUIN; ASIALOGLYCOPROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN BETA; NUCLEOPORIN; PLASMID DNA; REV PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; CELL ASSAY; DNA BINDING; DNA HELIX; DNA TRANSFECTION; GENE ACTIVATION; GENE REPLACEMENT THERAPY; HUMAN IMMUNODEFICIENCY VIRUS 1; MACROMOLECULE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; NUCLEIC ACID SYNTHESIS; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REPORTER GENE; REVIEW;

EID: 0038360771     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(03)00050-4     Document Type: Review

References (84)

1. Griesenbach U., Alton E.W.F.W. Recent progress in gene therapy for cystic fibrosis. Curr. Opin. Mol. Ther. 3:2001;385-389.
2. Richardson P.D., Augustin L.B., Kren B.T., Steer C.J. Gene repair and transposon-mediated gene therapy. Stem Cells. 20:2002;105-118.
3. Brown M.D., Schatzlein A.G., Uchegbu I.F. Gene delivery with synthetic (non viral) carriers. Int. J. Pharm. 229:2001;1-21.
4. Alesci S., Ramsey W.J., Bornstein S.R., Chrousos G.P., Hornsby P.J., Benvenga S., Trimarchi F., Ehrhart-Bornstein M. Adenoviral vectors can impair adrenocortical steroidogenesis: Clinical implications for natural infections and gene therapy. Proc. Natl. Acad. Sci. USA. 99:2002;7484-7489.
5. Capecchi M.R. High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell. 22:1980;479-488.
6. Zabner J., Fasbender A.J., Moninger T., Poellinger K., Welsh M. Cellular and molecular barriers to gene transfer by a cationic lipid. J. Biol. Chem. 270:1995;18997-19007.
7. Salina D., Bodoor K., Eckley D.M., Schroer T.A., Rattner J.B., Burke B. Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell. 108:2002;97-107.
8. Beaudouin J., Gerlich D., Daigle N., Eils R., Ellenberg J. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell. 108:2002;83-96.
9. Terasaki M., Campagnola P., Rolls M.M., Stein P.A., Ellenberg J., Hinkle B., Slepchenko B. A new model for nuclear envelope breakdown. Mol. Biol. Cell. 12:2001;503-510.
10. Bennett C.F., Chiang M.-Y., Chan H., Shoemaker J.E., Mirabelli C.K. Cationic lipids enhance cellular uptake and activity of phosphorothioate antisense oligonucleotides. Mol. Pharmacol. 41:1992;1023-1033.
11. Chin D.J., Green G.A., Zon G., Szoka F.C. Jr., Straubinger R.M. Rapid nuclear accumulation of injected oligodeoxyribonucleotides. New Biol. 2:1990;1091-1100.
12. Ludtke J.J., Zhang G., Sebestyen M.G., Wolff J.A. A nuclear localization signal can enhance both the nuclear transport and expression of 1 kb DNA. J. Cell Sci. 112:1999;2033-2041.
13. Lang I., Scholz M., Peters R.F. Molecular mobility and nucleocytoplasmic flux in hepatoma cells. J. Cell Biol. 102:1986;1183-1190.
14. Mattaj I.W., Englmeier L. Nucleocytoplasmic transport the soluble phase. Annu. Rev. Biochem. 67:1998;265-306.
15. Nakielny S., Dreyfuss G. Transport of proteins and RNAs in and out of the nucleus. Cell. 23:1999;677-690.
16. Cullen B.R. Journey to the center of the cell. Cell. 105:2001;697-700.
17. Wente S.R. Gatekeepers of the nucleus. Science. 288:2000;1374-1377.
18. Vasu S.K., Forbes D.J. Nuclear pores and nuclear assembly. Curr. Opin. Cell Biol. 13:2001;363-375.
19. Hinshaw J.E., Carragher B.O., Miligan R.A. Architecture and design of the nuclear pore complex. Cell. 69:1992;1133-1141.
20. Akey C.W., Radermacher M. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol. 122:1993;1-19.
21. Bastos R., Pante N., Burke B. Nuclear pore complex proteins. Int. Rev. Cytol. 162B:1995;257-302.
22. Goldberg M.W., Allen T.D. The nuclear pore complex and lamina: three-dimensional structures and interactions determined by field emission in-lens scanning electron microscopy. J. Mol. Biol. 257:1996;848-865.
23. Cordes V.C., Reidenbach S., Rackwitz H.R., Franke W.W. Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments. J. Cell Biol. 136:1997;515-529.
24. Bonner W.M. Protein migration and accumulation in nuclei. Busch H. The Cell Nucleus. Vol. 6:1978;97-148 Academic Press, New York.
25. Feldherr C.M., Kallenbach E., Schultz N. Movement of a karyophilic protein through the nuclear pores of oocytes. J. Cell Biol. 99:1984;2216-2222.
26. Dworetzky S.I., Lanford R.E., Feldherr C.M. The effects of variations in the number and sequence of targeting signals on nuclear uptake. J. Cell Biol. 107:1988;1279-1287.
27. Pante N., Kann M. Nuclear pore complex is able to transport macromolecules with diameters of ∼39 nm. Mol. Cell. Biol. 13:2002;425-434.
28. Daigle N., Beaudouin J., Hartnell L., Imreh G., Hallberg E., Lippincott-Schwartz J., Ellenberg J. Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J. Cell Biol. 154:2001;71-84.
29. Ribbeck K., Gorlich D. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 20:2001;1320-1330.
30. Iovine M.K., Watkins J.L., Wente S.R. The GLFG repetitive region of the nucleoporin Nup116p interacts with Kap95p, an essential yeast nuclear import factor. J. Cell Biol. 131:1995;1699-1713.
31. Rexach M., Blobel G. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell. 83:1995;683-692.
32. Hu T., Guan T., Gerace L. Molecular and functional characterization of the p62 complex, an assembly of nuclear pore complex glycoproteins. J. Cell Biol. 134:1996;589-601.
33. Moore M.S. Ran and nuclear transport. J. Biol. Chem. 273:1998;22857-22860.
34. Ribbeck K., Gorlich D. The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J. 21:2002;2664-2671.
35. L Wilson G., Dean B.S., Wang G., Dean D.A. Nuclear import of plasmid DNA in digitonin-permeabilised cells requires both cytoplasmic factors and specific DNA sequences. J. Biol. Chem. 274:1999;22025-22032.
36. Smith A.E., Slepchenko B.M., Schaff J.C., Loew L.M., Macara I.G. Systems analysis of Ran transport. Science. 295:2002;488-491.
37. Dean D.A. Import of plasmid DNA into the nucleus is sequence specific. Exp. Cell Res. 230:2001;293-302.
38. Salman H., Zbaida D., Rabin Y., Chatenay D., Elbaum M. Kinetics and mechanism of DNA uptake into the cell nucleus. Proc. Natl. Acad. Sci. USA. 98:2001;7247-7252.
39. Wilson R.W., Bloomfield V.A. Counterion-induced condensation of deoxyribonucleic acid. A light-scattering study. Biochemistry. 18:1979;2192-2196.
40. Gao X., Huang L. Potentiation of cationic liposome-mediated gene delivery by polycations. Biochemistry. 35:1996;1027-1036.
41. Blobel G. Protein targeting (Nobel lecture). Chembiochemistry. 1:2002;86-102.
42. Kalderon D., Roberts B.L., Richardson W.D., Smith A.E. A short amino acid sequence able to specify nuclear location. Cell. 39:1984;499-509.
43. Kalderon D., Richardson W.D., Markham A.F., Smith A.E. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature. 311:1984;33-38.
44. Robbins J., Dilworth S.M., Laskey R.A., Dingwall C. Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell. 64:1991;615-623.
45. Boulikas T. Nuclear localization signals (NLS). Crit. Rev. Eukaryot. Gene Expr. 3:1993;193-227.
46. Henderson B.R., Percipalle P. Interactions between HIV Rev and nuclear import and export factors: the Rev nuclear localisation signal mediates specific binding to human importin-β J. Mol. Biol. 274:1997;693-707.
47. Siomi H., Dreyfuss G.A. Nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129:1995;551-560.
48. Nakielny S., Mikkio S.C., Haruhiko S., Michael W.M., Pollard V., Dreyfuss G. Transportin: nuclear import receptor of a novel nuclear protein import pathway. Exp. Cell Res. 229:1996;261-266.
49. Cokol M., Nair R., Rost B. Finding nuclear localization signals. EMBO Rep. 1:2000;411-415.
50. Hodel M.R., Corbett A.H., E Hodel A. Dissection of a nuclear localization signal. J. Biol. Chem. 276:2001;1317-1325.
51. Vives E., Brodin P., Lebleu B. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272:1997;16010-16017.
52. Duverger E., Roche A.C., Monsigny M. N-acetylglucosamine-dependent nuclear import of neoglycoproteins. Glycobiology. 6:1996;381-386.
53. Duverger E., Pellerin-Mendes C., Mayer R., Roche A.C., Monsigny M. Nuclear import of glycoconjugates is distinct from the classical NLS pathway. J. Cell Sci. 108:1995;1325-1332.
54. Collas P., Husebye H., Alestrom P. The nuclear localization sequence of the SV40 T antigen promotes transgene uptake and expression in zebrafish embryo nuclei. Transgenic Res. 5:1996;451-458.
55. Collas P., Alestrom P. Rapid targeting of plasmid DNA to zebrafish embryo nuclei by the nuclear localization signal of SV40 T antigen. Mol. Mar. Biol. Biotechnol. 6:1997;48-58.
56. Subramanian A., Ranganathan P., Diamond S.L. Nuclear targeting peptide scaffolds for lipofection of nondividing mammalian cells. Nature Biotechnol. 17:1999;873-877.
57. Chan C.K., Jans D.A. Enhancement of polylysine-mediated transferrinfection by nuclear localization sequences: polylysine does not function as a nuclear localization sequence. Hum. Gene Ther. 10:1999;1695-1702.
58. Chan C.K., Jans D.A. Enhancement of MSH receptor- and GAL4-mediated gene transfer by switching the nuclear import pathway. Gene Ther. 8:2001;166-171.
59. Tung C.-H., Stein S. Preparation and applications of peptide oligonucleotide conjugates. Bioconj. Chem. 11:2000;605-618.
60. Sebestyen M.G., Ludtke J.J., Bassik M.C., Zhang G., Budker V., Lukhtanov E.A., Hagstrom J.E., Wolff J.A. DNA vector chemistry: the covalent attachment of signal peptides to plasmid DNA. Nature Biotechnol. 16:1998;80-85.
61. Zanta M.A., Belguise-Valladier P., Behr J.P. Gene delivery: a single nuclear localization signal peptide is sufficient to carry DNA to the cell nucleus. Proc. Natl. Acad. Sci. USA. 96:1999;91-96.
62. Ciolina C., Byk G., Blanche F., Thuillier V., Scherman D., Wils P. Coupling of nuclear localization signals to plasmid DNA and specific interaction of the conjugates with importin-α Bioconj. Chem. 10:1999;49-55.
63. Zelphati O., Liang X., Hobart P., Felgner P.L. Gene chemistry: functionally and conformationally intact fluorescent plasmid DNA. Hum. Gene Ther. 10:1999;15-24.
64. Dean D.A. Peptide nucleic acids: versatile tools for gene therapy strategies. Adv. Drug Deliv. Rev. 44:2000;81-95.
65. Demidov V.V., Potaman V.N., Frank-Kamenetskii M.D., Egholm M., Buchard O., Sonnichsen S.H., Nielsen P.E. Stability of peptide nucleic acids in human serum and cellular extracts. Biochem. Pharmacol. 48:1994;1310-1313.
66. Nielsen P.E., Haaima G. Peptide nucleic acid. A DNA mimic with a pseudopeptide backbone. Chem. Soc. Rev. 96:1997;73-78.
67. Branden L.J., I Smith C. Bioplex technology: novel synthetic gene delivery system based on peptides anchored to nucleic acids. Methods Enzymol. 346:2002;106-124.
68. Awasthi S.K., Nielsen P.E. Parallel synthesis of PNA-peptide conjugate libraries. Comb. Chem. High Throughput Screen. 5:2002;253-259.
69. Adam S.A., Marr R.S., Gerace L. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111:1990;807-816.
70. Branden L.J., Mohamed A.J., I Smith C. A peptide nucleic acid-nuclear localization signal fusion that mediates nuclear transport of DNA. Nature Biotechnol. 17:1999;784-787.
71. Branden L.J., Christensson B., Smith C.I. In vivo nuclear delivery of oligonucleotides via hybridizing bifunctional peptides. Gene Ther. 8:2001;84-87.
72. Schirmbeck R., Konig-Merediz S.A., Riedl P., Kwissa M., Sack F., Schroff M., Junghans C., Reimann J., Wittig B. Priming of immune responses to hepatitis B surface antigen with minimal DNA expression constructs modified with a nuclear localization signal peptide. J. Mol. Med. 79:2001;343-350.
73. 1-antitrypsin gene transfer in vivo results in stationary long-term gene expression. J. Mol. Med. 79:2001;205-212.
74. Neves C., Escriou V., Byk G., Scherman D., Wils P. Intracellular fate and nuclear targeting of plasmid DNA. Cell Biol. Toxicol. 15:1999;193-202.
75. Conti E., Uy M., Leighton L., Blobel G., Kuriyan J. Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherins-α Cell. 94:1998;193-204.
76. Conti E., Kuriyan J. Crystallographic analysis of the specific yet versatile recognition of distinct nuclear localization signals by karyopherin-α Struct. Fold Des. 8:2000;329-338.
77. Fontes M.R., The T., Kobe B. Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-α J. Mol. Biol. 297:2000;1183-1194.
78. Hagstrom J.E., Sebestyen M.G., Budker V., Ludtke J.J., Fritz J.D., Wolff J.A. Complexes of non-cationic liposomes and histone H1 mediate efficient transfection of DNA without encapsulation. Biochim. Biophys. Acta. 1284:1996;47-55.
79. Fritz J.D., Herweijer H., Zhang G., Wolff J.A. Gene transfer into mammalian cells using histone-condensed plasmid DNA. Hum. Gene Ther. 7:1996;1395-1404.
80. Dean D.A., Dean B.S., Muller S., Smith L.C. Sequence requirements for DNA plasmid nuclear import. Exp. Cell Res. 253:1999;713-722.
81. Vacik J., Dean B.S., Zimmer W.E., Dean D.A. Cell-specific nuclear import of plasmid DNA. Gene Ther. 6:1999;1006-1014.
82. Mesika A., Grigoreva I., Zohar M., Reich Z. A regulated, NFκB-assisted import of plasmid DNA into mammalian cell nuclei. Mol. Ther. 3:2001;653-657.
83. Li S., MacLaughlin F.C., Fewell J.G., Gondo M., Wang J., Nicol F., Dean D.A., Smith L.C. Muscle-specific enhancement of gene expression by incorporation of SV40 enhancer in the expression plasmid. Gene Ther. 8:2001;494-497.
84. Cartier R., Reszka R. Utilization of synthetic peptides containing nuclear localization signals for nonviral gene transfer systems. Gene Ther. 9:2002;157-167.