Lung gene therapy with highly compacted DNA nanoparticles that overcome the mucus barrier

Journal of Controlled Release

Volumn 178, Issue 1, 2014, Pages 8-17

  Suk, Jung Soo ^a   Kim, Anthony J ^a,d   Trehan, Kanika ^a,c   Schneider, Craig S ^a,b   Cebotaru, Liudmila ^a   Woodward, Owen M ^a   Boylan, Nicholas J ^b   Boyle, Michael P ^a   Lai, Samuel K ^a,b,e   Guggino, William B ^a   Hanes, Justin ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e UNC Hamner Institute for Drug Safety Sciences   (United States)

Author keywords

Airway gene therapy; DNA nanoparticle; Mucus barrier; Multiple particle tracking

Indexed keywords

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATORS; DNA NANOPARTICLES; MUCOCILIARY CLEARANCE; MUCUS BARRIER; MULTIPLE PARTICLE TRACKING; PARTICLE DISTRIBUTIONS; POLYETHYLENE GLYCOL (PEG); POLYMERIC GENE CARRIERS;

BIOLOGICAL ORGANS; DNA; DRUG PRODUCTS; GENE THERAPY; GENE TRANSFER; MAMMALS; NANOPARTICLES;

BODY FLUIDS;

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA NANOPARTICLE; MACROGOL; NANOCARRIER; PLASMID DNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRONCHUS MUCUS; CYSTIC FIBROSIS; EX VIVO GENE TRANSFER; GENE THERAPY; IN VITRO STUDY; LUNG; MOUSE; MUCOCILIARY CLEARANCE; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; TRACHEA;

AIRWAY GENE THERAPY; DNA NANOPARTICLE; MUCUS BARRIER; MULTIPLE PARTICLE TRACKING;

ADMINISTRATION, INTRANASAL; ADULT; ANIMALS; CHO CELLS; CRICETULUS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA; ESOPHAGUS; FEMALE; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUMANS; LUNG; MICE, INBRED BALB C; MUCUS; NANOPARTICLES; POLYETHYLENE GLYCOLS; POLYETHYLENEIMINE; POLYLYSINE; STOMACH; YOUNG ADULT;

EID: 84893359543     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.01.007     Document Type: Article

References (56)

1. S. Papiris, A. Kotanidou, K. Malagari, and C. Roussos Clinical review: severe asthma Crit. Care 6 2002 30 44 (Pubitemid 34162856)
2. P.A. Flume Pulmonary complications of cystic fibrosis Respir. Care 54 2009 618 627
3. U. Griesenbach, and E.W. Alton Gene transfer to the lung: lessons learned from more than 2 decades of CF gene therapy Adv. Drug Deliv. Rev. 61 2009 128 139
4. K. Podolska, A. Stachurska, K. Hajdukiewicz, and M. Malecki Gene therapy prospects - intranasal delivery of therapeutic genes Adv. Clin. Exp. Med. 21 2012 525 534
5. P.L. Sinn, E.R. Burnight, and P.B. McCray Jr. Progress and prospects: prospects of repeated pulmonary administration of viral vectors Gene Ther. 16 2009 1059 1065
6. M.W. Konstan, P.B. Davis, J.S. Wagener, K.A. Hilliard, R.C. Stern, L.J. Milgram, T.H. Kowalczyk, S.L. Hyatt, T.L. Fink, C.R. Gedeon, S.M. Oette, J.M. Payne, O. Muhammad, A.G. Ziady, R.C. Moen, and M.J. Cooper Compacted DNA nanoparticles administered to the nasal mucosa of cystic fibrosis subjects are safe and demonstrate partial to complete cystic fibrosis transmembrane regulator reconstitution Hum. Gene Ther. 15 2004 1255 1269 (Pubitemid 40052437)
7. R.A. Cone Barrier properties of mucus Adv. Drug Deliv. Rev. 61 2009 75 85
8. S.K. Lai, Y.Y. Wang, and J. Hanes Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues Adv. Drug Deliv. Rev. 61 2009 158 171
9. N.N. Sanders, S.C. De Smedt, E. Van Rompaey, P. Simoens, F. De Baets, and J. Demeester Cystic fibrosis sputum: a barrier to the transport of nanospheres Am. J. Respir. Crit. Care Med. 162 2000 1905 1911
10. C.A. Sheils, J. Kas, W. Travassos, P.G. Allen, P.A. Janmey, M.E. Wohl, and T.P. Stossel Actin filaments mediate DNA fiber formation in chronic inflammatory airway disease Am. J. Pathol. 148 1996 919 927 (Pubitemid 126660683)
11. J.S. Suk, S.K. Lai, Y.Y. Wang, L.M. Ensign, P.L. Zeitlin, M.P. Boyle, and J. Hanes The penetration of fresh undiluted sputum expectorated by cystic fibrosis patients by non-adhesive polymer nanoparticles Biomaterials 30 2009 2591 2597
12. S.K. Lai, Y.Y. Wang, K. Hida, R. Cone, and J. Hanes Nanoparticles reveal that human cervicovaginal mucus is riddled with pores larger than viruses Proc. Natl. Acad. Sci. U. S. A. 107 2010 598 603
13. K. Hida, S.K. Lai, J.S. Suk, S.Y. Won, M.P. Boyle, and J. Hanes Common gene therapy viral vectors do not efficiently penetrate sputum from cystic fibrosis patients PLoS One 6 2011 e19919
14. N.J. Boylan, J.S. Suk, S.K. Lai, R. Jelinek, M.P. Boyle, M.J. Cooper, and J. Hanes Highly compacted DNA nanoparticles with low MW PEG coatings: In vitro, ex vivo and in vivo evaluation J. Control. Release 157 2011 72 79
15. J.S. Suk, N.J. Boylan, K. Trehan, B.C. Tang, C.S. Schneider, J.M. Lin, M.P. Boyle, P.L. Zeitlin, S.K. Lai, M.J. Cooper, and J. Hanes N-acetylcysteine enhances cystic fibrosis sputum penetration and airway gene transfer by highly compacted DNA nanoparticles Mol. Ther. 19 2011 1981 1989
16. X. Sun, and N. Zhang Cationic polymer optimization for efficient gene delivery Mini Rev. Med. Chem. 10 2010 108 125
17. D.D. Dunlap, A. Maggi, M.R. Soria, and L. Monaco Nanoscopic structure of DNA condensed for gene delivery Nucleic Acids Res. 25 1997 3095 3101 (Pubitemid 27331404)
18. J.F. Kukowska-Latallo, E. Raczka, A. Quintana, C. Chen, M. Rymaszewski, and J.R. Baker Jr. Intravascular and endobronchial DNA delivery to murine lung tissue using a novel, nonviral vector Hum. Gene Ther. 11 2000 1385 1395 (Pubitemid 30451019)
19. S. Ferrari, A. Pettenazzo, N. Garbati, F. Zacchello, J.P. Behr, and M. Scarpa Polyethylenimine shows properties of interest for cystic fibrosis gene therapy Biochim. Biophys. Acta 1447 1999 219 225 (Pubitemid 29494993)
20. A. Akinc, M. Thomas, A.M. Klibanov, and R. Langer Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis J. Gene Med. 7 2005 657 663 (Pubitemid 40744532)
21. S. Ferrari, C. Kitson, R. Farley, R. Steel, C. Marriott, D.A. Parkins, M. Scarpa, B. Wainwright, M.J. Evans, W.H. Colledge, D.M. Geddes, and E.W. Alton Mucus altering agents as adjuncts for nonviral gene transfer to airway epithelium Gene Ther. 8 2001 1380 1386 (Pubitemid 32895668)
22. Y.Y. Wang, S.K. Lai, J.S. Suk, A. Pace, R. Cone, and J. Hanes Addressing the PEG mucoadhesivity paradox to engineer nanoparticles that "slip" through the human mucus barrier Angew. Chem. Int. Ed. Engl. 47 2008 9726 9729
23. S.K. Lai, D.E. O'Hanlon, S. Harrold, S.T. Man, Y.Y. Wang, R. Cone, and J. Hanes Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus Proc. Natl. Acad. Sci. U. S. A. 104 2007 1482 1487 (Pubitemid 46214616)
24. S.K. Lai, J.S. Suk, A. Pace, Y.Y. Wang, M. Yang, O. Mert, J. Chen, J. Kim, and J. Hanes Drug carrier nanoparticles that penetrate human chronic rhinosinusitis mucus Biomaterials 32 2011 6285 6290
25. A. Beyerle, A. Braun, A. Banerjee, N. Ercal, O. Eickelberg, T.H. Kissel, and T. Stoeger Inflammatory responses to pulmonary application of PEI-based siRNA nanocarriers in mice Biomaterials 32 2011 8694 8701
26. H. Petersen, P.M. Fechner, A.L. Martin, K. Kunath, S. Stolnik, C.J. Roberts, D. Fischer, M.C. Davies, and T. Kissel Polyethylenimine-graft- poly(ethylene glycol) copolymers: influence of copolymer block structure on DNA complexation and biological activities as gene delivery system Bioconjug. Chem. 13 2002 845 854 (Pubitemid 34801128)
27. A. Kichler, M. Chillon, C. Leborgne, O. Danos, and B. Frisch Intranasal gene delivery with a polyethylenimine-PEG conjugate J. Control. Release 81 2002 379 388 (Pubitemid 34607157)
28. Y. Hu, J. Xie, Y.W. Tong, and C.H. Wang Effect of PEG conformation and particle size on the cellular uptake efficiency of nanoparticles with the HepG2 cells J. Control. Release 118 2007 7 17 (Pubitemid 46283099)
29. S. Pamujula, S. Hazari, G. Bolden, R.A. Graves, D.D. Chinta, S. Dash, V. Kishore, and T.K. Mandal Cellular delivery of PEGylated PLGA nanoparticles J. Pharm. Pharmacol. 64 2012 61 67
30. M. Amblard, J.A. Fehrentz, J. Martinez, and G. Subra Methods and protocols of modern solid phase peptide synthesis Mol. Biotechnol. 33 2006 239 254 (Pubitemid 44337228)
31. A.G. Ziady, C.R. Gedeon, T. Miller, W. Quan, J.M. Payne, S.L. Hyatt, T.L. Fink, O. Muhammad, S. Oette, T. Kowalczyk, M.K. Pasumarthy, R.C. Moen, M.J. Cooper, and P.B. Davis Transfection of airway epithelium by stable PEGylated poly-L-lysine DNA nanoparticles in vivo Mol. Ther. 8 2003 936 947 (Pubitemid 38072306)
32. J. Suh, M. Dawson, and J. Hanes Real-time multiple-particle tracking: applications to drug and gene delivery Adv. Drug Deliv. Rev. 57 2005 63 78 (Pubitemid 39424064)
33. T. Savin, and P.S. Doyle Static and dynamic errors in particle tracking microrheology Biophys. J. 88 2005 623 638 (Pubitemid 40070706)
34. N. Ruthardt, D.C. Lamb, and C. Brauchle Single-particle tracking as a quantitative microscopy-based approach to unravel cell entry mechanisms of viruses and pharmaceutical nanoparticles Mol. Ther. 19 2011 1199 1211
35. X. Michalet, and A.J. Berglund Optimal diffusion coefficient estimation in single-particle tracking Phys. Rev. E. Stat. Nonlin. Soft Matter Phys. 85 2012 061916
36. J.C. Crocker, and B.D. Hoffman Multiple-particle tracking and two-point microrheology in cells Methods Cell Biol. 83 2007 141 178
37. L.H. Liang, O.M. Woodward, Z.H. Chen, R. Cotter, and W.B. Guggino A novel role of protein tyrosine kinase2 in mediating chloride secretion in human airway epithelial cells PLoS One 6 2011
38. A. Malek, F. Czubayko, and A. Aigner PEG grafting of polyethylenimine (PEI) exerts different effects on DNA transfection and siRNA-induced gene targeting efficacy J. Drug Target. 16 2008 124 139 (Pubitemid 351266549)
39. O.M. Merkel, R. Urbanics, P. Bedocs, Z. Rozsnyay, L. Rosivall, M. Toth, T. Kissel, and J. Szebeni In vitro and in vivo complement activation and related anaphylactic effects associated with polyethylenimine and polyethylenimine- graft-poly(ethylene glycol) block copolymers Biomaterials 32 2011 4936 4942
40. L. Cebotaru, N. Vij, I. Ciobanu, J. Wright, T. Flotte, and W.B. Guggino Cystic fibrosis transmembrane regulator missing the first four transmembrane segments increases wild type and DeltaF508 processing J. Biol. Chem. 283 2008 21926 21933
41. C.M. Fuller, and D.J. Benos CFTR! Am. J. Physiol. 263 1992 C267 C286
42. A.S. Verkman, G.L. Lukacs, and L.J. Galietta CFTR chloride channel drug discovery - inhibitors as antidiarrheals and activators for therapy of cystic fibrosis Curr. Pharm. Des. 12 2006 2235 2247 (Pubitemid 43891397)
43. A.C. Hunter, and S.M. Moghimi Cationic carriers of genetic material and cell death: a mitochondrial tale Biochim. Biophys. Acta 1797 2010 1203 1209
44. I.A. Pringle, S.C. Hyde, and D.R. Gill Non-viral vectors in cystic fibrosis gene therapy: recent developments and future prospects Expert. Opin. Biol. Ther. 9 2009 991 1003
45. N. Sanders, C. Rudolph, K. Braeckmans, S.C. De Smedt, and J. Demeester Extracellular barriers in respiratory gene therapy Adv. Drug Deliv. Rev. 61 2009 115 127
46. A. Beyerle, O. Merkel, T. Stoeger, and T. Kissel PEGylation affects cytotoxicity and cell-compatibility of poly(ethylene imine) for lung application: structure-function relationships Toxicol. Appl. Pharmacol. 242 2010 146 154
47. A.G. Ziady, C.R. Gedeon, O. Muhammad, V. Stillwell, S.M. Oette, T.L. Fink, W. Quan, T.H. Kowalczyk, S.L. Hyatt, J. Payne, A. Peischl, J.E. Seng, R.C. Moen, M.J. Cooper, and P.B. Davis Minimal toxicity of stabilized compacted DNA nanoparticles in the murine lung Mol. Ther. 8 2003 948 956 (Pubitemid 38072307)
48. P. Erbacher, T. Bettinger, E. Brion, J.L. Coll, C. Plank, J.P. Behr, and J.S. Remy Genuine DNA/polyethylenimine (PEI) complexes improve transfection properties and cell survival J. Drug Target. 12 2004 223 236 (Pubitemid 39140069)
49. L.A. Davies, G. McLachlan, S.G. Sumner-Jones, D. Ferguson, A. Baker, P. Tennant, C. Gordon, C. Vrettou, E. Baker, J. Zhu, E.W. Alton, D.D. Collie, D.J. Porteous, S.C. Hyde, and D.R. Gill Enhanced lung gene expression after aerosol delivery of concentrated pDNA/PEI complexes Mol. Ther. 16 2008 1283 1290 (Pubitemid 351866060)
50. S. Boeckle, K. von Gersdorff, S. van der Piepen, C. Culmsee, E. Wagner, and M. Ogris Purification of polyethylenimine polyplexes highlights the role of free polycations in gene transfer J. Gene Med. 6 2004 1102 1111 (Pubitemid 40228122)
51. D. Jere, H.L. Jiang, R. Arote, Y.K. Kim, Y.J. Choi, M.H. Cho, T. Akaike, and C.S. Cho Degradable polyethylenimines as DNA and small interfering RNA carriers Expert Opin. Drug Deliv. 6 2009 827 834
52. J.C. Davies, and E.W. Alton Gene therapy for cystic fibrosis Proc. Am. Thorac. Soc. 7 2010 408 414
53. S.C. Hyde, I.A. Pringle, S. Abdullah, A.E. Lawton, L.A. Davies, A. Varathalingam, G. Nunez-Alonso, A.M. Green, R.P. Bazzani, S.G. Sumner-Jones, M. Chan, H. Li, N.S. Yew, S.H. Cheng, A.C. Boyd, J.C. Davies, U. Griesenbach, D.J. Porteous, D.N. Sheppard, F.M. Munkonge, E.W. Alton, and D.R. Gill CpG-free plasmids confer reduced inflammation and sustained pulmonary gene expression Nat. Biotechnol. 26 2008 549 551 (Pubitemid 351668040)
54. P.L. Sinn, R.M. Anthony, and P.B. McCray Jr. Genetic therapies for cystic fibrosis lung disease Hum. Mol. Genet. 20 2011 R79 R86
55. U. Griesenbach, and E.W. Alton Current status and future directions of gene and cell therapy for cystic fibrosis BioDrugs 25 2011 77 88
56. L.A. Davies, S.C. Hyde, G. Nunez-Alonso, R.P. Bazzani, R. Harding-Smith, I.A. Pringle, A.E. Lawton, S. Abdullah, T.C. Roberts, D. McCormick, S.G. Sumner-Jones, and D.R. Gill The use of CpG-free plasmids to mediate persistent gene expression following repeated aerosol delivery of pDNA/PEI complexes Biomaterials 33 2012 5618 5627