Structure, dynamics, and energetics of siRNA-Cationic vector complexation: A molecular dynamics study

Journal of Physical Chemistry B

Volumn 114, Issue 28, 2010, Pages 9220-9230

  Ouyang, Defang ^a   Zhang, Hong ^a   Herten, Dirk Peter ^b   Parekh, Harendra S ^a   Smith, Sean C ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; DYES; DYNAMICS; FREE ENERGY; GENE TRANSFER; MOLECULAR DYNAMICS; NUCLEIC ACIDS; POLYMERS; RNA; VAN DER WAALS FORCES;

ATOMISTIC MOLECULAR DYNAMICS SIMULATIONS; BINDING FREE ENERGY; CARRIER SYSTEMS; CYTOSOLS; EFFECTIVE INDEX; ELECTROSTATIC CONTRIBUTIONS; GENE DELIVERY; MECHANISTIC ASPECTS; MOLECULAR LEVELS; NON-VIRAL GENE DELIVERY; NONVIRAL VECTORS; POLYCATION COMPLEXES; POLYCATIONS; RATIONAL DESIGN; SURFACE TOPOLOGY; VAN DER WAALS INTERACTIONS;

BINDING ENERGY;

EID: 77954694522     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp911906e     Document Type: Article

References (84)

1. Niidome, T.; Huang, L. Gene therapy progress and prospects: nonviral vectors Gene Ther. 2002, 9 (24) 1647-1652
2. Pouton, C. W.; Seymour, L. W. Key issues in non-viral gene delivery Adv. Drug Delivery Rev. 2001, 46 (1-3) 187-203
3. Roth, C. M.; Sundaram, S. Engineering synthetic vectors for improved DNA delivery: Insights from intracellular pathways Annu. Rev. Biomed. Eng. 2004, 6, 397-426
4. Gersting, S. W.; Schillinger, U.; Lausier, J.; Nicklaus, P.; Rudolph, C.; Plank, C.; Reinhardt, D.; Rosenecker, J. Gene delivery to respiratory epithelial cells by magnetofection J. Gene Med. 2004, 6 (8) 913-922
5. Ruponen, M.; Honkakoski, P.; Ronkko, S.; Pelkonen, J.; Tammi, M.; Urtti, A. Extracellular and intracellular barriers in non-viral gene delivery J. Controlled Release 2003, 93 (2) 213-217
6. Zabner, J.; Fasbender, A. J.; Moninger, T.; Poellinger, K. A.; Welsh, M. J. Cellular and molecular barriers to gene transfer by a cationic lipid J. Biol. Chem. 1995, 270 (32) 18997-19007
7. Schaffer, D. V.; Fidelman, N. A.; Dan, N.; Lauffenburger, D. A. Vector unpacking as a potential barrier for receptor-mediated polyplex gene delivery Biotechnol. Bioeng. 2000, 67 (5) 598-606
8. Yamagata, M.; Kawano, T.; Shiba, K.; Mori, T.; Katayama, Y.; Niidome, T. Structural advantage of dendritic poly(L-lysine) for gene delivery into cells Bioorg. Med. Chem. 2007, 15 (1) 526-532
9. Mannisto, M.; Vanderkerken, S.; Toncheva, V.; Elomaa, M.; Ruponen, M.; Schacht, E.; Urtti, A. Structure-activity relationships of poly(L-lysines): Effects of pegylation and molecular shape on physicochemical and biological properties in gene delivery J. Controlled Release 2002, 83 (1) 169-182
10. Bertschinger, M.; Backliwal, G.; Schertenleib, A.; Jordan, M.; Hacker, D. L.; Wurm, F. M. Disassembly of polyethylenimine-DNA particles in vitro: Implications for polyethylenimine-mediated DNA delivery J. Controlled Release 2006, 116 (1) 96-104
11. Jeong, G. J.; Byun, H. M.; Kim, J. M.; Yoon, H.; Choi, H. G.; Kim, W. K.; Kim, S. J.; Oh, Y. K. Biodistribution and tissue expression kinetics of plasmid DNA complexed with polyethylenimines of different molecular weight and structure J. Controlled Release 2007, 118 (1) 118-125
12. Kunath, K.; von Harpe, A.; Fischer, D.; Peterson, H.; Bickel, U.; Voigt, K.; Kissel, T. Low-molecular-weight polyethylenimine as a non-viral vector for DNA delivery: Comparison of physicochemical properties, transfection efficiency and in vivo distribution with high-molecular-weight polyethylenimine J. Controlled Release 2003, 89 (1) 113-125
13. Kawakami, S.; Ito, Y.; Charoensit, P.; Yamashita, F.; Hashida, M. Evaluation of proinflammatory cytokine production induced by linear and branched polyethylenimine/plasmid DNA complexes in mice J. Pharmacol. Exp. Ther. 2006, 317 (3) 1382-1390
14. Brissault, B.; Leborgne, C.; Guis, C.; Danos, O.; Cheradame, H.; Kichler, A. Linear topology confers in vivo gene transfer activity to polyethylenimines Bioconjugate Chem. 2006, 17 (3) 759-765
15. Wightman, L.; Kircheis, R.; Rossler, V.; Carotta, S.; Ruzicka, R.; Kursa, M.; Wagner, E. Different behavior of branched and linear polyethylenimine for gene delivery in vitro and in vivo J. Gene Med. 2001, 3 (4) 362-372
16. Jones, N. A.; Hill, I. R. C.; Stolnik, S.; Bignotti, F.; Davis, S. S.; Garnett, M. C. Polymer chemical structure is a key determinant of physicochemical and colloidal properties of polymer-DNA complexes for gene delivery Biochim. Biophys. Acta, Gene Struct. Express. 2000, 1517 (1) 1-18
17. Lee, C. C.; Liu, Y.; Reineke, T. M. General structure-activity relationship for poly(glycoamidoamine)s: The effect of amine density on cytotoxicity and DNA delivery efficiency Bioconjugate Chem. 2008, 19 (2) 428-440
18. Hsu, C. Y. M.; Uludag, H. Effects of size and topology of DNA molecules on intracellular delivery with non-viral gene carriers BMC Biotechnol. 2008, 8
19. Parekh, H. S.; Marano, R. J.; Rakoczy, E. P.; Blanchfield, J.; Toth, I. Synthesis of a library of polycationic lipid core dendrimers and their evaluation in the delivery of an oligonucleotide with hVEGF inhibition Bioorg. Med. Chem. 2006, 14 (14) 4775-4780
20. Parekh, H. S. The advance of dendrimers - A versatile targeting platform for gene/drug delivery Curr. Pharm. Des. 2007, 13 (27) 2837-2850
21. Mann, A.; Richa, R.; Ganguli, M. DNA condensation by poly-L-lysine at the single molecule level: Role of DNA concentration and polymer length J. Controlled Release 2008, 125 (3) 252-262
22. Shen, X. C.; Zhou, J.; Liu, X.; Wu, J.; Qu, F.; Zhang, Z. L.; Pang, D. W.; Quelever, G.; Zhang, C. C.; Peng, L. Importance of size-to-charge ratio in construction of stable and uniform nanoscale RNA/dendrimer complexes Org. Biomol. Chem. 2007, 5 (22) 3674-3681
23. Van Rompaey, E.; Chen, Y.; Muller, J. D.; Gratton, E.; Van Craenenbroeck, E.; Engelborghs, Y.; De Smedt, S.; Demeester, J. Fluorescence fluctuation analysis for the study of interactions between oligonucleotides and polycationic polymers Biol. Chem. 2001, 382 (3) 379-386 (Pubitemid 32372480)
24. Margineanu, A.; De Feyter, S.; Melnikov, S.; Marchand, D.; van Aerschot, A.; Herdewijn, P.; Habuchi, S.; De Schryver, F. C.; Hofkens, J. Complexation of lipofectarnine and cholesterol-modified DNA sequences-studied by single-molecule fluorescence techniques Biomacromolecules 2007, 8 (11) 3382-3392
25. Lucas, B.; Van Rompaey, E.; De Smedt, S. C.; Demeester, J.; Van Oostveldt, P. Dual-color fluorescence fluctuation spectroscopy to study the complexation between poly-l-lysine and oligonucleotides Macromolecules 2002, 35 (21) 8152-8160
26. Lyulin, S. V.; Darinskii, A. A.; Lyulin, A. V. computer simulation of complexes of dendrimers with linear polyelectrolytes Macromolecules 2005, 38 (9) 3990-3998
27. Lyulin, S. V.; Vattulainen, I.; Gurtovenko, A. A. Complexes comprised of charged dendrimers, linear polyelectrolytes, and counterions: Insight through coarse-grained molecular dynamics simulations Macromolecules 2008, 41 (13) 4961-4968
28. Farago, O.; Gronbech-Jensen, N. Computational and analytical modeling of cationic lipid-DNA complexes Biophys. J. 2007, 92 (9) 3228-3240
29. Farago, O.; Ewert, K.; Ahmad, A.; Evans, H. M.; Gronbech-Jensen, N.; Safinya, C. R. Transitions between distinct compaction regimes in complexes of multivalent cationic lipids and DNA Biophys. J. 2008, 95 (2) 836-846
30. Thyveetil, M. A.; Coveney, P. V.; Greenwell, H. C.; Suter, J. L. Role of host layer flexibility in DNA guest intercalation revealed by computer simulation of layered nanomaterials J. Am. Chem. Soc. 2008, 130 (37) 12485-12495
31. Thyveetil, M. A.; Coveney, P. V.; Greenwell, H. C.; Suter, J. L. Computer simulation study of the structural stability and materials properties of DNA-intercalated layered double hydroxides J. Am. Chem. Soc. 2008, 130 (14) 4742-4756
32. Maiti, P. K.; Bagchi, B. Structure and dynamics of DNA-dendrimer complexation: Role of counterions, water, and base pair sequence Nano Lett. 2006, 6 (11) 2478-2485
33. Nikakhtar, A.; Nasehzadeh, A.; Mansoori, G. A. Formation and stability conditions of DNA-dendrimer nano-clusters J. Comput. Theor. Nanosci. 2007, 4 (3) 521-528
34. Bandyopadhyay, S.; Tarek, M.; Klein, M. L. Molecular dynamics study of a lipid-DNA complex J. Phys. Chem. B 1999, 103 (46) 10075-10080
35. Molas, M.; Bartrons, R.; Perales, J. C., Single-stranded DNA condensed with poly-L-lysine results in nanometric particles that are significantly smaller, more stable in physiological ionic strength fluids and afford higher efficiency of gene delivery than their double-stranded counterparts Biochim. Biophys. Acta, Gen. Subj. 2002, 1572 (1) 37-44
36. Pavan, G. M.; Danani, A.; Pricl, S.; Smith, D. K. Modeling the multivalent recognition between dendritic molecules and DNA: Understanding how ligand "sacrifice" and screening can enhance binding J. Am. Chem. Soc. 2009, 131 (28) 9686-9694
37. Srinivasan, J.; Cheatham, T. E.; Cieplak, P.; Kollman, P. A.; Case, D. A. Continuum solvent studies of the stability of DNA, RNA, and phosphoramidate-DNA helices J. Am. Chem. Soc. 1998, 120 (37) 9401-9409 (Pubitemid 28452628)
38. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S. H.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A.; Cheatham, T. E. Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models Acc. Chem. Res. 2000, 33 (12) 889-897
39. Kuhn, B.; Kollman, P. A. Binding of a diverse set of ligands to avidin and streptavidin: An accurate quantitative prediction of their relative affinities by a combination of molecular mechanics and continuum solvent models J. Med. Chem. 2000, 43 (20) 3786-3791
40. Lee, M. R.; Duan, Y.; Kollman, P. A. Use of MM-PB/SA in estimating the free energies of proteins: Application to native, intermediates, and unfolded villin headpiece Proteins: Struct., Funct., Genet. 2000, 39 (4) 309-316
41. Massova, I.; Kollman, P. A. Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding Perspect. Drug Discovery Des. 2000, 18, 113-135
42. Reyes, C. M.; Kollman, P. A. Structure and thermodynamics of RNA-protein binding: Using molecular dynamics and free energy analyses to calculate the free energies of binding and conformational change J. Mol. Biol. 2000, 297 (5) 1145-1-58
43. Case, D. A.; Darden, T. A.; Cheatham, I. T. E.; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Merz, K. M.; Pearlman, D. A.; Crowley, M.; Walker, R. C.; Zhang, W.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Wong, K. F.; Paesani, F.; Wu, X.; Brozell, S.; Tsui, V.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Beroza, P.; Mathews, D. H.; Schafmeister, C.; Ross, W. S.; Kollman, P. A. AMBER 9; University of California: San Francisco, 2006.
44. Case, D. A.; Cheatham, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The Amber biomolecular simulation programs J. Comput. Chem. 2005, 26 (16) 1668-1688
45. Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E.; Debolt, S.; Ferguson, D.; Seibel, G.; Kollman, P. AMBER, a package of computer-programs for applying molecular mechanics, normal-mode analysis, molecular-dynamics and free-energy calculations to simulate the structural and energetic properties of molecules Comput. Phys. Commun. 1995, 91 (1-3) 1-41
46. Putral, L. N.; Bywater, M. J.; Gu, W.; Saunders, N. A.; Gabrielli, B. G.; Leggatt, G. R.; McMillan, N. A. RNA interference against human papillomavirus oncogenes in cervical cancer cells results in increased sensitivity to cisplatin Mol. Pharmacol. 2005, 68 (5) 1311-1319
47. Wang, J. M.; Cieplak, P.; Kollman, P. A. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules J. Comput. Chem. 2000, 21 (12) 1049-1074
48. Wang, J. M.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field (vol 25, pg 1157, 2004) J. Comput. Chem. 2005, 26 (1) 114-114
49. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald - An N.Log(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98 (12) 10089-10092
50. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A smooth particle mesh Ewald method J. Chem. Phys. 1995, 103 (19) 8577-8593
51. Crowley, M. F.; Darden, T. A.; Cheatham, T. E.; Deerfield, D. W. Adventures in improving the scaling and accuracy of a parallel molecular dynamics program J. Supercomputing 1997, 11 (3) 255-278
52. Sagui, C.; Darden, T. A. In P3M and PME: a Comparison of the Two Methods, Workshop on Treatment of Electrostatic Interactions in Computer Simulations of Condensed Media, Santa Fe, NM, Jun 23-25; Pratt, L. R.; Hummer, G., Eds.; Amer. Inst. Physics: Melville, NY, 1999; pp 104 - 113.
53. Toukmaji, A.; Sagui, C.; Board, J.; Darden, T. Efficient particle-mesh Ewald based approach to fixed and induced dipolar interactions J. Chem. Phys. 2000, 113 (24) 10913-10927
54. Sagui, C.; Pedersen, L. G.; Darden, T. A. Towards an accurate representation of electrostatics in classical force fields: Efficient implementation of multipolar interactions in biomolecular simulations J. Chem. Phys. 2004, 120 (1) 73-87
55. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79 (2) 926-935
56. Leach, A. R. Molecular Modelling: Principles and Applications, 2 nd ed.; Prentice Hall: New York, 2001.
57. Höltje, H.-D.; Sippl, W.; Rognan, D.; Folkers, G. Molecular Modeling: Basic Principles and Applications, 3 rd ed.; Wiley-VCH: Weinheim, 2008.
58. Ryckaert, J. P.; Ciccotti, G.; Berendsen, H. J. C. Numerical-integration of Cartesian equations of motion of a system with constraints - Molecular-dynamics of n -alkanes J. Comput. Phys. 1977, 23 (3) 327-341
59. Cerutti, D. S.; Duke, R.; Freddolino, P. L.; Fan, H.; Lybrand, T. P. A vulnerability in popular molecular dynamics packages concerning Langevin and Andersen dynamics J. Chem. Theory Comput. 2008, 4 (10) 1669-1680
60. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-dynamics with coupling to an external bath J. Chem. Phys. 1984, 81 (8) 3684-3690
61. Wu, X. W.; Brooks, B. R. Self-guided Langevin dynamics simulation method Chem. Phys. Lett. 2003, 381 (3-4) 512-518
62. Luo, R.; David, L.; Gilson, M. K. Accelerated Poisson-Boltzmann calculations for static and dynamic systems J. Comput. Chem. 2002, 23 (13) 1244-1253
63. Lu, Q.; Luo, R. A Poisson-Boltzmann dynamics method with nonperiodic boundary condition J. Chem. Phys. 2003, 119 (21) 11035-11047
64. Honig, B.; Nicholls, A. Classical electrostatics in biology and chemistry Science 1995, 268 (5214) 1144-1149
65. Still, W. C.; Tempczyk, A.; Hawley, R. C.; Hendrickson, T. Semianalytical treatment of solvation for molecular mechanics and dynamics J. Am. Chem. Soc. 1990, 112 (16) 6127-6129
66. Jayaram, B.; Sprous, D.; Beveridge, D. L. Solvation free energy of biomacromolecules: Parameters for a modified generalized born model consistent with the AMBER force field J. Phys. Chem. B 1998, 102 (47) 9571-9576
67. Cramer, C. J.; Truhlar, D. G. Implicit solvation models: Equilibria, structure, spectra, and dynamics Chem. Rev. 1999, 99 (8) 2161-2200
68. Bashford, D.; Case, D. A. Generalized born models of macromolecular solvation effects Annu. Rev. Phys. Chem. 2000, 51, 129-152
69. Onufriev, A.; Bashford, D.; Case, D. A. Modification of the generalized Born model suitable for macromolecules J. Phys. Chem. B 2000, 104 (15) 3712-3720
70. Lee, M.S.; Salsbury, F. R.; Brooks, C. L. Novel generalized Born methods J. Chem. Phys. 2002, 116 (24) 10606-10614
71. AMBER. AMBER 9 Users' Manual; http://ambermd.org/doc9/, 2007.
72. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules J. Am. Chem. Soc. 1995, 117 (19) 5179-5197
73. Sitkoff, D.; Sharp, K. A.; Honig, B. Accurate calculation of hydration free-energies using macroscopic solvent models J. Phys. Chem US 1994, 98 (7) 1978-1988
74. Connolly, M. L. Analytical molecular-surface calculation J. Appl. Crystallogr. 1983, 16, 548-558
75. Ouyang, D. F.; Zhang, H.; Herten, D. P.; Parekh, H. S.; Smith, S. C. Flexibility of short-strand RNA in aqueous solution as revealed by molecular dynamics simulation: Are A-RNA and A'-RNA distinct conformational structures Aust. J. Chem. 2009, 62 (9) 1054-1061
76. Lu, X. J.; Olson, W. K. 3DNA: A software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures Nucleic Acids Res. 2003, 31 (17) 5108-5121
77. Goodsell, D. S. Inside a living cell Trends Biochem. Sci. 1991, 16 (6)) 203-206
78. Ellis, R. J. Macromolecular crowding: Obvious but underappreciated Trends Biochem. Sci. 2001, 26 (10) 597-604
79. Zhou, H. X.; Rivas, G. N.; Minton, A. P. Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys. 2008, 37, 375-397
80. Okuda, T.; Niidome, T.; Aoyagi, H. Cytosolic soluble proteins induce DNA release from DNA-gene carrier complexes J. Controlled Release 2004, 98 (2) 325-332
81. Iida, T.; Mori, T.; Katayama, Y.; Niidome, T. Overall interaction of cytosolic proteins with the PEI/DNA complex J. Controlled Release 2007, 118 (3) 364-369
82. Bertschinger, M.; Backliwal, G.; Schertenleib, A.; Jordan, M.; Hacker, D. L.; Wurm, F. M. Disassembly of polyethylenimine-DNA particles in vitro: Implications for polyethylenimine-mediated DNA delivery J. Controlled Release 2006, 116 (1) 96-104
83. Huth, S.; Hoffmann, F.; von Gersdorff, K.; Laner, A.; Reinhardt, D.; Rosenecker, J.; Rudolph, C. Interaction of polyamine gene vectors with RNA leads to the dissociation of plasmid DNA-carrier complexes J. Gene Med. 2006, 8 (12) 1416-1424
84. Ward, C. M.; Read, M. L.; Seymour, L. W. Systemic circulation of poly(L-lysine)/DNA vectors is influenced by polycation molecular weight and type of DNA: Differential circulation in mice and rats and the implications for human gene therapy Blood 2001, 97 (8) 2221-2229