Polyplex gene delivery modulated by redox potential gradients

Journal of Drug Targeting

Volumn 14, Issue 8, 2006, Pages 519-526

  Soundara Manickam, Devika ^a   Oupický, David ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Gene delivery; Glutathione; Polycations; Polyplexes

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; COPOLYMER; DISULFIDE; GLUTATHIONE; MACROGOL; MESSENGER RNA; NUCLEIC ACID; PLASMID DNA; POLYCATION; POLYETHYLENEIMINE; POLYMER; POLYPEPTIDE; SMALL INTERFERING RNA; THIOL GROUP;

CROSS LINKING; CYTOTOXICITY; DISULFIDE BOND; DNA REPAIR; DNA SYNTHESIS; DRUG FORMULATION; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSFECTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONVIRAL GENE DELIVERY SYSTEM; OXIDATION REDUCTION POTENTIAL; POLYMERIZATION; PRIORITY JOURNAL; REVIEW;

ANIMALS; DNA; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; OLIGONUCLEOTIDES, ANTISENSE; OXIDATION-REDUCTION; PLASMIDS; POLYAMINES; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 33750098007     PISSN: 1061186X     EISSN: 10292330     Source Type: Journal    
DOI: 10.1080/10611860600834409     Document Type: Review

References (68)

1. Arrigo, AP. (1999) Gene expression and the thiol redox state Free Radic Biol Med, 27, pp. 936-944.
2. Austin, CD and Wen, X and Gazzard, L and Nelson, C and Scheller, RH and Scales, SJ. (2005) Oxidizing potential of endosomes and lysosomes limits intracellular cleavage of disulfide-based antibody-drug conjugates Proc Natl Acad Sci USA, 102, pp. 17987-17992.
3. Balakirev, M and Schoehn, G and Chroboczek, J. (2000) Lipoic acid-derived amphiphiles for redox-controlled DNA delivery Chem Biol, 7, pp. 813-819.
4. Bellomo, G and Vairetti, M and Stivala, L and Mirabelli, F and Richelmi, P and Orrenius, S. (1992) Demonstration of nuclear compartmentalization of glutathione in hepatocytes Proc Natl Acad Sci USA, 89, pp. 4412-4416.
5. Bettinger, T and Carlisle, RC and Read, ML and Ogris, M and Seymour, LW. (2001) Peptide-mediated RNA delivery: A novel approach for enhanced transfection of primary and post-mitotic cells Nucleic Acids Res, 29, pp. 3882-3891.
6. Braakman, I and Helenius, J and Helenius, A. (1992) Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum EMBO J, 11, pp. 1717-1722.
7. Byk, G and Wetzer, B and Frederic, M and Dubertret, C and Pitard, B and Jaslin, G and Scherman, D. (2000) Reduction-sensitive lipopolyamines as a novel nonviral gene delivery system for modulated release of DNA with improved transgene expression J Med Chem, 43, pp. 4377-4387.
8. Carlisle, RC and Etrych, T and Briggs, SS and Preece, JA and Ulbrich, K and Seymour, LW. (2004) Polymer-coated polyethylenimine/DNA complexes designed for triggered activation by intracellular reduction J Gene Med, 6, pp. 337-344.
9. Chittimalla, C and Zammut-Italiano, L and Zuber, G and Behr, JP. (2005) Monomolecular DNA nanoparticles for intravenous delivery of genes. J Am Chem Soc, 127, pp. 11436-11441.
10. Collins, DS and Unanue, ER and Harding, CV. (1991) Reduction of disulfide bonds within lysosomes is a key step in antigen processing J Immunol, 147, pp. 4054-4059.
11. Dauty, E and Behr, JP and Remy, JS. (2002) Development of plasmid and oligonucleotide nanometric particles Gene Ther, 9, pp. 743-748.
12. Donoghue, N and Hogg, PJ. (2002) Characterization of redox-active proteins on cell surface Methods Enzymol, 348, pp. 76-86.
13. Donoghue, N and Yam, PTW and Jiang, XM and Hogg, PJ. (2000) Presence of closely spaced protein thiols on the surface of mammalian cells protein Sci, 9, pp. 2436-2445.
14. Essex, DW and Chen, K and Swiatkowska, M. (1995) Localization of protein disulfide isomerase to the external surface of the platelet plasma membrane Blood, 86, pp. 2168-2173.
15. Feener, EP and Shen, WC and Ryser, HJP. (1990) Cleavage of disulfide bonds in endocytosed macromolecules - a processing not associated with lysosomes or endosomes J Biol Chem, 265, pp. 18780-18785.
16. Fivaz, M and Vilbois, F and Thurnheer, S and Pasquali, C and Abrami, L and Bickel, PE and Parton, RG and van der Goot, FG. (2002) Differential sorting and fate of endocytosed GPI-anchored proteins EMBO J, 21, pp. 3989-4000.
17. Gilbert, HF. (1990) Molecular and cellular aspects of thiol-disulfide exchange Adv Enzymol Relat Areas Mol Biol, 63, pp. 69-172.
18. Gilbert, HF. (1997) Protein disulfide isomerase and assisted protein folding J Biol Chem, 272, pp. 29399-29402.
19. Godbey, WT and Wu, KK and Mikos, AG. (2001) Poly(ethylenimine)-mediated gene delivery affects endothelial cell function and viability Biomaterials, 22, pp. 471-480.
20. Gosselin, MA and Guo, WJ and Lee, RJ. (2001) Efficient gene transfer using reversibly cross-linked low molecular weight polyethylenimine Bioconjugate Chem, 12, pp. 989-994.
21. Gosselin, MA and Guo, WJ and Lee, RJ. (2002) Incorporation of reversibly cross-linked polyplexes into LPDII vectors for gene delivery Bioconjugate Chem, 13, pp. 1044-1053.
22. Hwang, C and Sinskey, AJ and Lodish, HF. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum Science, 257, pp. 1496-1502.
23. Hwang, C and Lodish, HF and Sinskey, AJ. (1995) Measurement of glutathione redox state in cytosol and secretory pathway of cultured cells Methods Enzymol, 251, pp. 212-221.
24. Jiang, XM and Fitzgerald, M and Grant, CM and Hogg, PJ. (1999) Redox control of exofacial protein thiols/disulfides by protein disulfide isomerase J Biol Chem, 274, pp. 2416-2423.
25. Jones, DP and Carlson, JL and Samiec, PS and Sternberg, P, Jr and Mody, VC, Jr and Reed, RL and Brown, LA. (1998) Glutathione measurement in human plasma. Evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC Clin Chim Acta, 275, pp. 175-184.
26. Kakizawa, Y and Harada, A and Kataoka, K. (1999) Environment-sensitive stabilization of core-shell structured polyion complex micelle by reversible cross-linking of the core through disulfide bond J Am Chem Soc, 121, pp. 11247-11248.
27. Kakizawa, Y and Harada, A and Kataoka, K. (2001) Glutathione-sensitive stabilization of block copolymer micelles composed of antisense DNA and thiolated poly(ethylene glycol)-block-poly(l-lysine): A potential carrier for systemic delivery of antisense DNA Biomacromolecules, 2, pp. 491-497.
28. Kichler, A and Remy, JS and Boussif, O and Frisch, B and Boeckler, C and Behr, JP and Schuber, F. (1995) Efficient gene delivery with neutral complexes of lipospermine and thiol-reactive phospholipids Biochem Biophys Res Com, 209, pp. 444-450.
29. Kosower, NS and Kosower, EM. (1978) The glutathione status of cells Int Rev Cytol, 54, pp. 109-160.
30. Kwok, KY and Park, Y and Yang, Y and McKenzie, DL and Liu, Y and Rice, KG. (2003) In vivo gene transfer using sulfhydryl cross-linked PEG-peptide/glycopeptide DNA co-condensates J Pharm Sci, 92, pp. 1174-1185.
31. Lahav, J and Jurk, K and Hess, O and Barnes, MJ and Farndale, RW and Luboshitz, J and Kehrel, BE. (2002) Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange Blood, 100, pp. 2472-2478.
32. Laragione, T and Bonetto, V and Casoni, F and Massignan, T and Bianchi, G and Gianazza, E and Ghezzi, P. (2003) Redox regulation of surface protein thiols: Identification of integrin alpha-4 as a molecular target by using redox proteomics Proc Natl Acad Sci USA, 100, pp. 14737-14741.
33. Lash, LH and Putt, DA and Matherly, LH. (2002) Overexpression of a mitochondrial glutathione transporter protects NRK-52E cells from chemically induced apoptosis J Am Soc Nephrol, 13, pp. 292A-292A.
34. McKenzie, DL and Kwok, KY and Rice, KG. (2000a) A potent new class of reductively activated peptide gene delivery agents J Biol Chem, 275, pp. 9970-9977.
35. McKenzie, DL and Smiley, E and Kwok, KY and Rice, KG. (2000b) Low molecular weight disulfide cross-linking peptides as nonviral gene delivery carriers Bioconjugate Chem, 11, pp. 901-909.
36. Meister, A and Anderson, ME. (1983) Glutathione Annu Rev Biochem, 52, pp. 711-760.
37. Miyata, K and Kakizawa, Y and Nishiyama, N and Harada, A and Yamasaki, Y and Koyama, H and Kataoka, K. (2004) Block catiomer polyplexes with regulated densities of charge and disulfide cross-linking directed to enhance gene expression J Am Chem Soc, 126, pp. 2355-2361.
38. Miyata, K and Kakizawa, Y and Nishiyama, N and Yamasaki, Y and Watanabe, T and Kohara, M and Kataoka, K. (2005) Freeze-dried formulations for in vivo gene delivery of PEGylated polyplex micelles with disulfide crosslinked cores to the liver J Control Release, 109, pp. 15-23.
39. Moghimi, SM and Symonds, P and Murray, JC and Hunter, AC and Debska, G and Szewczyk, A. (2005) A two-stage poly(ethylenimine)-mediated cytotoxicity: Implications for gene transfer/therapy Mol Ther, 11, pp. 990-995.
40. Muratovska, A and Eccles, MR. (2004) Conjugate for efficient delivery of short interfering RNA (siRNA) into mammalian cells FEBS Lett, 558, pp. 63-68.
41. Oishi, M and Hayama, T and Akiyama, Y and Takae, S and Harada, A and Yamasaki, Y and Nagatsugi, F and Sasaki, S and Nagasaki, Y and Kataoka, K. (2005) Supramolecular assemblies for the cytoplasmic delivery of antisense oligodeoxynucleotide: Polyion complex (PIC) micelles based on poly(ethylene glycol)-SS-oligodeoxynucleotide conjugate Biomacromolecules, 6, pp. 2449-2454.
42. Oupicky, D and Carlisle, RC and Seymour, LW. (2001) Triggered intracellular activation of disulfide crosslinked polyelectrolyte gene delivery complexes with extended systemic circulation in vivo Gene Ther, 8, pp. 713-724.
43. Oupicky, D and Parker, AL and Seymour, LW. (2002) Laterally stabilized complexes of DNA with linear reducible polycations: Strategy for triggered intracellular activation of DNA delivery vectors J Am Chem Soc, 124, pp. 8-9.
44. Park, Y and Kwok, KY and Boukarim, C and Rice, KG. (2002) Synthesis of sulfhydryl cross-linking poly(ethylene glycol)-peptides and glycopeptides as carriers for gene delivery Bioconjugate Chem, 13, pp. 232-239.
45. Phan, UT and Arunachalam, B and Cresswell, P. (2000) Gamma-interferon-inducible lysosomal thiol reductase (GILT) - maturation, activity, and mechanism of action J Biol Chem, 275, pp. 25907-25914.
46. Pichon, C and LeCam, E and Guerin, B and Coulaud, D and Delain, E and Midoux, P. (2002) Poly[Lys-(AEDTP)]: A cationic polymer that allows dissociation of pDNA/cationic polymer complexes in a reductive medium and enhances polyfection Bioconjugate Chem, 13, pp. 76-82.
47. Ramachandran, N and Root, P and Jiang, XM and Hogg, PJ and Mutus, B. (2001) Mechanism of transfer of NO from extracellular S-nitrosothiols into the cytosol by cell-surface protein disulfide isomerase Proc Natl Acad Sci USA, 98, pp. 9539-9544.
48. Read, ML and Bremner, KH and Oupicky, D and Green, NK and Searle, PF and Seymour, LW. (2003) Vectors based on reducible polycations facilitate intracellular release of nucleic acids J Gene Med, 5, pp. 232-245.
49. Read, ML and Singh, S and Ahmed, Z and Stevenson, M and Briggs, SS and Oupicky, D and Barrett, LB and Spice, R and Kendall, M and Berry, M and Preece, JA and Logan, A and Seymour, LW. (2005) A versatile reducible polycation-based system for efficient delivery of a broad range of nucleic acids Nucleic Acids Res, 33, pp. e86.
50. Ryser, HJ and Mandel, R and Ghani, F. (1991) Cell surface sulfhydryls are required for the cytotoxicity of diphtheria toxin but not of ricin in Chinese hamster ovary cells J Biol Chem, 266, pp. 18439-18442.
51. Sahaf, B and Heydari, K and Herzenberg, LA and Herzenberg, LA. (2005) The extracellular microenvironment plays a key role in regulating the redox status of cell surface proteins in HIV-infected subjects Arch Biochem Biophys, 434, pp. 26-32.
52. Saito, G and Amidon, GL and Lee, KD. (2003) Enhanced cytosolic delivery of plasmid DNA by a sulfhydryl-activatable listeriolysin O/protamine conjugate utilizing cellular reducing potential Gene Ther, 10, pp. 72-83.
53. Schafer, FQ and Buettner, GR. (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic Biol Med, 30, pp. 1191-1212.
54. Shen, WC and Ryser, HJ and LaManna, L. (1985) Disulfide spacer between methotrexate and poly(d-lysine). A probe for exploring the reductive process in endocytosis J Biol Chem, 260, pp. 10905-10908.
55. Smith, CV and Jones, DP and Guenthner, TM and Lash, LH and Lauterburg, BH. (1996) Compartmentation of glutathione: Implications for the study of toxicity and disease Toxicol Appl Pharmacol, 140, pp. 1-12.
56. Soboll, S and Grundel, S and Harris, J and Kolb-Bachofen, V and Ketterer, B and Sies, H. (1995) The content of glutathione and glutathione S-transferases and the glutathione peroxidase activity in rat liver nuclei determined by a non-aqueous technique of cell fractionation Biochem J, 311(Pt 3), pp. 889-894.
57. Soundara Manickam, D and Bisht, HS and Wan, L and Mao, G and Oupicky, D. (2005) Influence of TAT-peptide polymerization on properties and transfection activity of TAT/DNA polyplexes J Control Release, 102, pp. 293-306.
58. Symonds, P and Murray, JC and Hunter, AC and Debska, G and Szewczyk, A and Moghimi, SM. (2005) Low and high molecular weight poly(l-lysine)s/ poly(l-lysine)-DNA complexes initiate mitochondrial-mediated apoptosis differently FEBS Lett, 579, pp. 6191-6198.
59. Tang, FX and Hughes, JA. (1998) Introduction of a disulfide bond into a cationic lipid enhances transgene expression of plasmid DNA Biochem Biophys Res Com, 242, pp. 141-145.
60. Tang, FX and Hughes, JA. (1999) Use of dithiodiglycolic acid as a tether for cationic lipids decreases the cytotoxicity and increases transgene expression of plasmid DNA in vitro Bioconjugate Chem, 10, pp. 791-796.
61. Trentin, D and Hall, H and Wechsler, S and Hubbell, JA. (2006) Peptide-matrix-mediated gene transfer of an oxygen-insensitive hypoxia-inducible factor-1alpha variant for local induction of angiogenesis Proc Natl Acad Sci USA, 103, pp. 2506-2511.
62. Trentin, D and Hubbell, J and Hall, H. (2005) Non-viral gene delivery for local and controlled DNA release J Control Release, 102, pp. 263-275.
63. Trubetskoy, VS and Budker, VG and Hanson, LJ and Slattum, PM and Wolff, JA and Hagstrom, JE. (1998) Self-assembly of DNA-polymer complexes using template polymerization Nucleic Acids Res, 26, pp. 4178-4185.
64. Trubetskoy, VS and Loomis, A and Slattum, PM and Hagstrom, JE and Budker, VG and Wolff, JA. (1999) Caged DNA does not aggregate in high ionic strength solutions Bioconjugate Chem, 10, pp. 624-628.
65. Wahllander, A and Soboll, S and Sies, H and Linke, I and Muller, M. (1979) Hepatic mitochondrial and cytosolic glutathione content and the subcellular distribution of GSH-S-transferases FEBS Lett, 97, pp. 138-140.
66. Wu, X and Bishopric, NH and Discher, DJ and Murphy, BJ and Webster, KA. (1996) Physical and functional sensitivity of zinc finger transcription factors to redox change Mol Cell Biol, 16, pp. 1035-1046.
67. Zhang, JX and Zalipsky, S and Mullah, N and Pechar, M and Allen, TM. (2004) Pharmaco attributes of dioleoylphosphatidylethanolamine/ cholesterylhemisuccinate liposomes containing different types of cleavable lipopolymers Pharmacol Res, 49, pp. 185-198.
68. Zhou, QH and Miller, DL and Carlisle, RC and Seymour, LW and Oupicky, D. (2005) Ultrasound-enhanced transfection activity of HPMA-stabilized DNA polyplexes with prolonged plasma circulation J Control Release, 106, pp. 416-427.