Polyamine–DNA interactions and development of gene delivery vehicles

Amino Acids

Volumn 48, Issue 10, 2016, Pages 2423-2431

  Thomas, T J ^a,b   Tajmir Riahi, H A ^c   Thomas, Thresia ^a  

^a RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

Author keywords

Biodegradable polymers; DNA condensation; DNA transfection; Gene delivery vehicles; Polyamines; Polyamine DNA interactions; Tetraplex DNA; Triplex DNA

Indexed keywords

CATION; DNA; DNA Z; NANOPARTICLE; POLYAMINE; SPERMIDINE; SPERMINE; TETRAPLEX DNA; TRIPLEX DNA; UNCLASSIFIED DRUG;

ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; DNA AGGREGATION; DNA BINDING; DNA CONDENSATION; DNA RESOLUBILITY; DNA STABILIZATION; DNA STRUCTURE; DNA TRANSFECTION; ELECTRON MICROSCOPY; GENE AND NUCLEIC ACID PARAMETERS; GENE DELIVERY SYSTEM; GENE THERAPY; HUMAN; IN VIVO GENE TRANSFER; INTERACTIONS WITH DNA; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; CHEMISTRY; GENE TRANSFER; PROCEDURES;

ANIMALS; BIOGENIC POLYAMINES; DNA; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUMANS; NANOPARTICLES;

EID: 84966709547     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-016-2246-8     Document Type: Review

References (119)

1. Agostinelli E, Vianello F, Magliulo G, Thomas T, Thomas TJ (2015) Nanoparticle strategies for cancer therapeutics: nucleic acids, polyamines, bovine serum amine oxidase and iron oxide nanoparticles (review). Int J Oncol 46:5–16
2. Albuquerque LJ, Annes K, Milazzotto MP, Mattei B, Riske KA, Jäger E, Pánek J, Štěpánek P, Kapusta P, Muraro PI, De Freitas AG, Schmidt V, Giacomelli C, Bonvent JJ, Giacomelli FC, Albuquerque LJC, Annes K, Milazzotto MP et al (2016) Efficient condensation of DNA into environmentally responsive polyplexes produced from block catiomers carrying amine or diamine groups. Langmuir 32:577–586
3. Amir RJ, Pessah N, Shamis M, Shabat D (2003) Self-immolative dendrimers. Angew Chem Int Ed Eng 42:4494–4499
4. Antony T, Thomas T, Shirahata A, Thomas TJ (1999a) Selectivity of polyamines on the stability of RNA-DNA hybrids containing phosphodiester and phosphorothioate oligodeoxyribonucleotides. Biochemistry 38:10775–10784
5. Antony T, Thomas T, Shirahata A, Sigal LH, Thomas TJ (1999b) Selectivity of spermine homologs on triplex DNA stabilization. Antisense Nucleic Acid Drug Dev 9:221–231
6. Antony T, Thomas T, Sigal LH, Shirahata A, Thomas TJ (2001) A molecular beacon strategy for the thermodynamic characterization of triplex DNA: triplex formation at the promoter region of cyclin D1. Biochemistry 40:9387–9395
7. Bancroft D, Williams LD, Rich A, Egli M (1994) The low-temperature crystal structure of the pure-spermine form of Z-DNA reveals binding of a spermine molecule in the minor groove. Biochemistry 33:1073–1086
8. Barnard A, Posocco P, Pricl S, Calderon M, Haag R, Hwang ME, Shum VWT, Pack DW, Smith DK (2011) Degradable self-assembling dendrons for gene delivery: experimental and theoretical insights into the barriers to cellular uptake. J Am Chem Soc 133:20288–20300
9. Bazzicalupi C, Chioccioli M, Sissi C, Porcù E, Bonaccini C, Pivetta C, Bencini A, Giorgi C, Valtancoli B, Melani F, Gratteri P (2010) Modeling and biological investigations of an unusual behavior of novel synthesized acridine-based polyamine ligands in the binding of double helix and G-quadruplex DNA. ChemMedChem 5:1995–2005
10. Beck A, Vijayanathan V, Thomas T, Thomas TJ (2013) Ionic microenvironmental effects on triplex DNA stabilization: cationic counterion effects on poly(dT).poly(dA).poly(dT). Biochimie 95:1310–1318
11. Behe M, Felsenfeld G (1981) Effects of methylation on a synthetic polynucleotide: the B-Z transition in poly(dG-m5dC)poly(dG-m5dC). Proc Natl Acad Sci USA 78:1619–1623
12. Blessing T, Remy JS, Behr JP (1998) Template oligomerization of DNA-bound cations produces calibrated nanometric particles. J Am Chem Soc 120:8519–8520
13. Bloomfield VA (1996) DNA condensation. Curr Opin Struct Biol 6:334–341
14. Boussif O, Lezoualc’h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA 92:7297–7301
15. Braunlin WH, Strick TJ, Record MT Jr (1982) Equilibrium dialysis studies of polyamine binding to DNA. Biopolymers 21:1301–1314
16. Burak Y, Ariel G, Andelman D (2003) Onset of DNA aggregation in presence of monovalent and multivalent counterions. Biophys J 85:2100–2110
17. Cai X, Dong C, Dong H, Wang G, Pauletti GM, Pan X, Wen H, Mehl I, Li Y, Shi D (2012) Effective gene delivery using stimulus-responsive catiomer designed with redox-sensitive disulfide and acid-labile imine linkers. Biomacromolecules 13:1024–1034
18. Cooney M, Czernuszewicz G, Postel EH, Flint SJ, Hogan ME (1988) Site-specific oligonucleotide binding represses transcription of the human c-myc gene in vitro. Science 241:456–459
19. Costa D, Valente AJ, Queiroz J (2015) Stimuli-responsive polyamine-DNA blend nanogels for co-delivery in cancer therapy. Colloids Surf B Biointerfaces 132:194–201
20. Cowman MK, Fasman GD (1978) Circular dichroism analysis of mononucleosome DNA conformation. Proc Natl Acad Sci USA 75:4759–4763
21. Demeneix B, Behr JP (2005) Polyethyleneimine (PEI). Adv Genet 53:215–230
22. Demeneix B, Hassani Z, Behr JP (2004) Towards multifunctional synthetic vectors. Curr Gene Ther 4:445–455
23. Donkuru M, Badea I, Wettig S, Verrall R, Elsabahy M, Foldvari M (2010) Advancing nonviral gene delivery: lipid- and surfactant-based nanoparticle design strategies. Nanomedicine 5:1103–1127
24. Durland RH, Kessler DJ, Gunnell S, Duvic M, Pettitt BM, Hogan ME (1991) Binding of triple helix forming oligonucleotides to sites in gene promoters. Biochemistry 30:9246–9255
25. Elsabahy M, Wooley KL (2012) Design of polymeric nanoparticles for biomedical delivery applications. Chem Soc Rev 41:2545
26. Felsenfeld G, Davies DR, Rich A (1957) Formation of a three stranded polynucleotide molecule. J Am Chem Soc 79:2023–2024
27. Feuerstein BG, Pattabiraman N, Marton LJ (1986) Spermine-DNA interactions: a theoretical study. Proc Natl Acad Sci USA 83:5948–5952
28. Fischer W, Quadir MA, Barnard A, Smith DK, Haag R (2011) Controlled release of DNA from photoresponsive hyperbranched polyglycerols with oligoamine shells. Macromol Biosci 11:1736–1747
29. Fox KR, Brown T (2011) Formation of stable DNA triplexes. Biochem Soc Trans 39:629–634
30. Frassineti C, Ghelli S, Gans P, Sabatini A, Moruzzi MS, Vacca A (1995) Nuclear magnetic resonance as a tool for determining protonation constants of natural polyprotic bases in solution. Anal Biochem 231:374–382
31. Gosselin MA, Guo W, Lee RJ (2001) Efficient gene transfer using reversibly cross-linked low molecular weight polyethylenimine. Bioconjugate Chem 12:989–994
32. Hardin CC, Perry AG, White K (2001) Thermodynamic and kinetic characterization of the dissociation and assembly of quadruplex nucleic acids. Biopolymers 56:147–194
33. He C, Zhuang X, Tang Z, Tian H, Chen X (2012) Stimuli-sensitive synthetic polypeptide-based materials for drug and gene delivery. Adv Healthc Mater 1:48–78
34. Heerschap A, Walters JA, Hilbers CW (1985) Interactions of some naturally occurring cations with phenylalanine and initiator tRNA from yeast as reflected by their thermal stability. Biophys Chem 22:205–217
35. Igarashi K, Aoki Y, Hirose S (1977) Base specificity of polyamine binding to synthetic polynucleotides. J Biochem 81:1091–1096
36. Jain A, Wang G, Vasquez KM (2008) DNA triple helices: biological consequences and therapeutic potential. Biochimie 90:1117–1130
37. Jiang X, Qu W, Pan D, Ren Y, Williford JM, Cui H, Luijten E, Mao HQ (2013) Plasmid-templated shape control of condensed DNA-block copolymer nanoparticles. Adv Mater 25:227–232
38. Jovin TM, McIntosh LP, Arndt-Jovin DJ, Zarling DA, Robert-Nicoud M, van de Sande JH, Jorgenson KF, Eckstein F (1983) Left-handed DNA: from synthetic polymers to chromosomes. J Biomol Struct Dyn 1:21–57
39. Joyeux M (2015) Compaction of bacterial genomic DNA: clarifying the concepts. J Phys Condens Matter 27:383001
40. Kabir A, Suresh Kumar G (2013) Binding of the biogenic polyamines to deoxyribonucleic acids of varying base composition: base specificity and the associated energetics of the interaction. PLoS One 8:e70510
41. Kabir A, Suresh Kumar G (2014) Targeting double-stranded RNA with spermine, 1-naphthylacetyl spermine and spermidine: a comparative biophysical investigation. J Phys Chem B 118:11050–11064
42. Keniry MA, Owen EA (2007) An investigation of the dynamics of spermine bound to duplex and quadruplex DNA by (13)C NMR spectroscopy. Eur Biophys J 36:637–646
43. Kornyshev AA, Leikin S (2013) Helical structure determines different susceptibilities of dsDNA, dsRNA, and tsDNA to counterion-induced condensation. Biophys J 104:2031–2041
44. Korolev N, Lyubartsev AP, Nordenskiöld L (2010) Cation-induced polyelectrolyte-polyelectrolyte attraction in solutions of DNA and nucleosome core particles. Adv Colloid Interface Sci 158:32–47
45. Kostiainen MA, Rosilo H (2009) Low-molecular-weight dendrons for DNA binding and release by reduction-triggered degradation of multivalent interactions. Chemistry 15:5656–5660
46. Kostiainen MA, Smith DK, Ikkala O (2007) Optically triggered release of DNA from multivalent dendrons by degrading and charge-switching multivalency. Angew Chem Int Ed Engl 46:7600–7604
47. Lee YS, Kim SW (2014) Bioreducible polymers for therapeutic gene delivery. J Control Release 190:424–439
48. Lee Y, Mo H, Koo H, Park JY, Cho MY, Jin GW, Park JS (2007) Visualization of the degradation of a disulfide polymer, linear poly(ethylenimine sulfide), for gene delivery. Bioconjugate Chem 18:13–18
49. Lewis JS, Thomas TJ, Shirahata A, Thomas T (2000) Self-assembly of an oligodeoxyribonucleotide harboring the estrogen response element in the presence of polyamines: ionic, structural, and DNA sequence specificity effects. Biomacromolecules 1:339–349
50. Lungwitz U, Breunig M, Blunk T, Göpferich A (2005) Polyethylenimine-based non-viral gene delivery systems. Eur J Pharm Biopharm 60:247–266
51. Mamasakhlisov YSh, Todd BA, Badasyan AV, Mkrtchyan AV, Morozov VF, Parsegian VA (2009) DNA stretching and multivalent-cation-induced condensation. Phys Rev E Stat Nonlin Soft Matter Phys 80:031915-1-9
52. Manning GS (1978) The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys 11:179–246
53. Marquet R, Houssier C (1991) Thermodynamics of cation-induced DNA condensation. J Biomol Struct Dyn 9:159–167
54. Mastorakos P, da Silva AL, Chisholm J (2015) Highly compacted biodegradable DNA nanoparticles capable of overcoming the mucus barrier for inhaled lung gene therapy. Proc Natl Acad Sci USA 112:8720–8725
55. Matulis D, Rouzina I, Bloomfield VA (2000) Thermodynamics of DNA binding and condensation: isothermal titration calorimetry and electrostatic mechanism. J Mol Biol 296:1053–1063
56. McCutchan JH, Pagano JS (1968) Enchancement of the infectivity of simian virus 40 deoxyribonucleic acid with diethylaminoethyl-dextran. J Nat Cancer Inst 41:351–357
57. Midoux P, Pichon C, Yaouanc JJ, Jaffrès PA (2009) Chemical vectors for gene delivery: a current review on polymers, peptides and lipids containing histidine or imidazole as nucleic acids carriers. Br J Pharmacol 157:166–178
58. Miyata K, Nishiyama N, Kataoka K (2012) Rational design of smart supramolecular assemblies for gene delivery: chemical challenges in the creation of artificial viruses. Chem Soc Rev 41:2562–2574
59. Müller S, Rodriguez R (2014) G-quadruplex interacting small molecules and drugs: from bench toward bedside. Expert Rev Clin Pharmacol 7:663–679
60. N’soukpoé-Kossi CN, Ouameur AA, Thomas T, Shirahata A, Thomas TJ, Tajmir-Riahi HA (2008) DNA interaction with antitumor polyamine analogues: a comparison with biogenic polyamines. Biomacromolecules 9:2712–2718
61. N’soukpoé-Kossi CN, Ahmed Ouameur A, Thomas T, Thomas TJ, Tajmir-Riahi HA (2009) Interaction of tRNA with antitumor polyamine analogues. Biochem Cell Biol 87:621–630
62. Nayvelt I, Thomas T, Thomas TJ (2007) Mechanistic differences in DNA nanoparticle formation in the presence of oligolysines and poly-l-lysine. Biomacromolecules 8:477–484
63. Nayvelt I, Hyvönen MT, Alhonen L, Pandya I, Thomas T, Khomutov AR, Vepsäläinen J, Patel R, Keinänen TA, Thomas TJ (2010) DNA condensation by chiral alpha-methylated polyamine analogues and protection of cellular DNA from oxidative damage. Biomacromolecules 11:97–105
64. Neidle S, Parkinson GN (2008) Quadruplex DNA crystal structures and drug design. Biochimie 90:1184–1196
65. Ouameur AA, Tajmir-Riahi HA (2004) Structural analysis of DNA interactions with biogenic polyamines and cobalt(III)hexamine studied by Fourier transform infrared and capillary electrophoresis. J Biol Chem 279:42041–42054
66. Parkinson GN, Lee MP, Neidle S (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417:876–880
67. Pasternack RF (2003) Circular dichroism and the interactions of water soluble porphyrins with DNA. Chirality 15:329–332
68. Pelta J Jr, Durand D, Doucet J, Livolant F (1996a) DNA mesophases induced by spermidine: structural properties and biological implications. Biophys J 71:48–63
69. Pelta J, Livolant F, Sikorav JL (1996b) DNA aggregation induced by polyamines and cobalthexamine. J Biol Chem 271:5656–5662
70. Pensado A, Seijo B, Sanchez A (2014) Current strategies for DNA therapy based on lipid nanocarriers. Expert Opin Drug Deliv 11:1721–1731
71. Pichon C, LeCam E, Guérin B, Coulaud D, Delain E, 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 13:76–82
72. Plum GE, Bloomfield VA (1990) Structural and electrostatic effects on binding of trivalent cations to double-stranded and single-stranded poly[d (AT)]. Biopolymers 29:13–27
73. Rajeev KG, Jadhav VR, Ganesh KN (1997) Triplex formation at physiological pH: comparative studies on DNA triplexes containing 5-Me-dC tethered at N4 with spermine and tetraethyleneoxyamine. Nucleic Acids Res 25:4187–4193
74. Raspaud E, Chaperon I, Leforestier A, Livolant F (1999) Spermine-induced aggregation of DNA, nucleosome, and chromatin. Biophys J 77:1547–1555
75. Raspaud E, Durand D, Livolant F (2005) Interhelical spacing in liquid crystalline spermine and spermidine-DNA precipitates. Biophys J 88:392–403
76. Rau DC, Parsegian VA (1992) Direct measurement of the intermolecular forces between counterion-condensed DNA double helices. Evidence for long range attractive hydration forces. Biophys J 61:246–259
77. Remy S, Sirlin C, Vierling P, Behr JP (1994) Gene transfer with a series of lipophilic DNA-binding molecules. Bioconjugate Chem 5:647–654
78. Rubin RL (1977) Spermidine-deoxyribonucleic acid interaction in vitro and in Escherichia coli. J Bacteriol 129:916–925
79. Safinya Cyrus R (2001) Structures of lipid–DNA complexes: supramolecular assembly and gene delivery. Curr Opin Struct Biol 11:440–448
80. Saminathan M, Antony T, Shirahata A, Sigal LH, Thomas T, Thomas TJ (1999) Ionic and structural specificity effects of natural and synthetic polyamines on the aggregation and resolubilization of single-, double-, and triple-stranded DNA. Biochemistry 38:3821–3830
81. Saminathan M, Thomas T, Shirahata A, Pillai CK, Thomas TJ (2002) Polyamine structural effects on the induction and stabilization of liquid crystalline DNA: potential applications to DNA packaging, gene therapy and polyamine therapeutics. Nucleic Acids Res 30:3722–3731
82. Santhakumaran LM, Thomas T, Thomas TJ (2004) Enhanced cellular uptake of a triplex-forming oligonucleotide by nanoparticle formation in the presence of polypropylenimine dendrimers. Nucleic Acids Res 32:2102–2112
83. Schellman JA, Parthasarathy N (1984) X-ray diffraction studies on cation-collapsed DNA. J Mol Biol 175:313–329
84. Shafer RH (1998) Stability and structure of model DNA triplexes and quadruplexes and their interactions with small ligands. Prog Nucleic Acid Res Mol Biol 59:55–94
85. Shim MS, Kwon YJ (2012) Stimuli-responsive polymers and nanomaterials for gene delivery and imaging applications. Adv Drug Deliv Rev 64:1046–1059
86. Son S, Namgung R, Kim J, Singha K, Kim WJ (2012) Bioreducible polymers for gene silencing and delivery. Acc Chem Res 45:1100–1112
87. Strekas TC, Engel R, Locknauth K, Cohen J, Fabian J (1999) Polycations. 5. Inducement of psi-DNA circular dichroism signals for duplex deoxyribonucleotide homopolymers by polycationic strings. Arch Biochem Biophys 364:129–131
88. Sun H, Xiang J, Liu Y, Li L, Li Q, Xu G, Tang Y (2011) A stabilizing and denaturing dual-effect for natural polyamines interacting with G-quadruplexes depending on concentration. Biochimie 93:1351–1356
89. Sundaresan N, Suresh CH, Thomas T, Thomas TJ, Pillai CK (2008) Liquid crystalline phase behavior of high molecular weight DNA: a comparative study of the influence of metal ions of different size, charge and binding mode. Biomacromolecules 9:1860–1869
90. Tabor H (1962) The protective effect of spermine and other polyamines against heat denaturation of deoxyribonucleic acid. Biochemistry 1:496–501
91. Thomas TJ, Bloomfield VA (1983) Collapse of DNA caused by trivalent cations: pH and ionic specificity effects. Biopolymers 22:1097–1106
92. Thomas TJ, Bloomfield VA (1984) Ionic and structural effects on the thermal helix-coil transition of DNA complexed with natural and synthetic polyamines. Biopolymers 23:1295–1306
93. Thomas TJ, Messner RP (1986) A left-handed (Z) conformation of poly(dA-dC).poly(dG-dT) induced by polyamines. Nucleic Acids Res 14:6721–6733
94. Thomas TJ, Messner RP (1988) Structural specificity of polyamines in left-handed Z-DNA formation. Immunological and spectroscopic studies. J Mol Biol 201:463–467
95. Thomas T, Thomas TJ (1993) Selectivity of polyamines in triplex DNA stabilization. Biochemistry 32:14068–14074
96. 8-acetyl spermidine. Biopolymers 24:725–729
97. Thomas TJ, Faaland CA, Gallo MA, Thomas T (1995) Suppression of c-myc oncogene expression by a polyamine-complexed triplex forming oligonucleotide in MCF-7 breast cancer cells. Nucleic Acids Res 23:3594–3599
98. Thomas TJ, Kulkarni GD, Greenfield NJ, Shirahata A, Thomas T (1996) Structural specificity effects of trivalent polyamine analogues on the stabilization and conformational plasticity of triplex DNA. Biochem J 319:591–599
99. Thomas RM, Thomas T, Wada M, Sigal LH, Shirahata A, Thomas TJ (1999) Facilitation of the cellular uptake of a triplex-forming oligonucleotide by novel polyamine analogues: structure-activity relationships. Biochemistry 38:13328–13337
100. Todd BA, Parsegian VA, Shirahata A, Thomas TJ, Rau DC (2008) Attractive forces between cation condensed DNA double helices. Biophys J 94:4775–4782
101. Travers A, Muskhelishvili G (2015) DNA structure and function. FEBS J 282:2279–2295
102. Veis A (2011) A review of the early development of the thermodynamics of the complex coacervation phase separation. Adv Colloid Interface Sci 167:2–11
103. Venkiteswaran S, Vijayanathan V, Shirahata A, Thomas T, Thomas TJ (2005) Antisense recognition of the HER-2 mRNA: effects of phosphorothioate substitution and polyamines on DNA.RNA, RNA.RNA, and DNA.DNA duplex stability. Biochemistry 44:303–312
104. Vijayanathan V, Thomas T, Shirahata A, Thomas TJ (2001) DNA condensation by polyamines: a laser light scattering study of structural effects. Biochemistry 40:13644–13651
105. Vijayanathan V, Thomas T, Thomas TJ (2002) DNA nanoparticles and development of DNA delivery vehicles for gene therapy. Biochemistry 48:14085–14094
106. Vijayanathan V, Thomas T, Antony T, Shirahata A, Thomas TJ (2004) Formation of DNA nanoparticles in the presence of novel polyamine analogues: a laser light scattering and atomic force microscopic study. Nucleic Acids Res 32:127–134
107. Vijayanathan V, Lyall J, Thomas T, Shirahata A, Thomas TJ (2005) Ionic, structural, and temperature effects on DNA nanoparticles formed by natural and synthetic polyamines. Biomacromolecules 6:1097–1103
108. Vijayanathan V, Agostinelli E, Thomas T, Thomas TJ (2014) Innovative approaches to the use of polyamines for DNA nanoparticle preparation for gene therapy. Amino Acids 46:499–509
109. Wagner E (2007) Programmed drug delivery: nanosystems for tumor targeting. Expert Opin Biol Ther 7:587–593
110. Wagner E (2008) Converging path of viral and non-viral vector engineering. Mol Ther 16:1–2
111. Wagner E (2014) Polymers for nucleic acid transfer-an overview. Adv Genet 88:231–261
112. Watson JD, Crick FH (1953) Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 171:737–738
113. Wen LN, Xie MX (2013) Evidence of different G-quadruplex DNA binding with biogenic polyamines probed by electrospray ionization-quadrupole time of flight mass spectrometry, circular dichroism and atomic force microscopy. Biochimie 95:1185–1195
114. Wen Y, Pan S, Luo X, Zhang W, Shen Y, Feng M (2010) PEG- and PDMAEG-graft-modified branched PEI as novel gene vector: synthesis, characterization and gene transfection. J Biomater Sci Polym Ed 21:1103–1126
115. Wilson RW, Bloomfield VA (1979) Counterion-induced condensation of deoxyribonucleic acid. A light-scattering study. Biochemistry 18:2192–2196
116. Wilson RW, Rau DC, Bloomfield VA (1980) Comparison of polyelectrolyte theories of the binding of cations to DNA. Biophys J 30:317–325
117. Wolff JA, Rozema DB (2008) Breaking the bonds: non-viral vectors become chemically dynamic. Mol Ther 16:16–29
118. Wu GY, Wu CH (1987) Receptor-mediated in vitro gene transformation by a soluble DNA carrier system. J Biol Chem 262:4429–4432
119. Zhang C, Jin R, Zhao P, Lin C (2014) A family of cationic polyamides for in vitro and in vivo gene transfection. Acta Biomater 22:120–130