Enhancement of airway gene transfer by DNA nanoparticles using a pH-responsive block copolymer of polyethylene glycol and poly-l-lysine

Biomaterials

Volumn 33, Issue 7, 2012, Pages 2361-2371

  Boylan, Nicholas J ^a,b   Kim, Anthony J ^a,b,c   Suk, Jung Soo ^a,c   Adstamongkonkul, Pichet ^a   Simons, Brian W ^a   Lai, Samuel K ^b,e   Cooper, Mark J ^d   Hanes, Justin ^a,b,c  

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

^b Johns Hopkins University   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d University of North Carolina at Chapel Hill ^*  (United States)

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

Author keywords

Cystic fibrosis; Gene therapy; Non viral; PH buffering

Indexed keywords

BALB/C MICE; BUFFERING CAPACITIES; CLINICAL TRIAL; COLLOIDAL STABILITY; CYSTIC FIBROSIS; GENE DELIVERY; HUMAN BRONCHIAL EPITHELIAL CELLS; HUMAN GENE THERAPY; IN-VITRO; IN-VIVO; LUNG AIRWAYS; NONVIRAL; NUCLEOLIN; PH BUFFERING; PH-RESPONSIVE; PLASMID DNA; POLY-L-HISTIDINE; POLY-L-LYSINE; POLYETHYLENEIMINE; ROD-SHAPED; SINGLE MOLECULE; TRIBLOCK COPOLYMER SYSTEMS;

AMINO ACIDS; BLOCK COPOLYMERS; DNA; GENE THERAPY; GENE TRANSFER; GLYCOLS; NANOPARTICLES; POLYETHYLENE OXIDES; POLYETHYLENES; THERMOPLASTICS;

POLYETHYLENE GLYCOLS;

COPOLYMER; DNA NANOPARTICLE; INTERCELLULAR ADHESION MOLECULE 1; NANOPARTICLE; NUCLEOLIN; PLASMID DNA; POLY(ETHYLENE GLYCOL)BLOCK POLY(HISTIDINE)BLOCK POLY(LYSINE)COPOLYMER; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRONCHUS MUCOSA; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA BINDING; DNA STRUCTURE; DRUG SCREENING; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO GENE TRANSFER; IN VIVO GENE TRANSFER; LYSOSOME; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON TRANSPORT; ZETA POTENTIAL;

ANIMALS; CELL LINE; DNA; DRUG CARRIERS; EPITHELIAL CELLS; FEMALE; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; HYDROGEN-ION CONCENTRATION; MATERIALS TESTING; MICE; MICE, INBRED BALB C; MOLECULAR STRUCTURE; NANOPARTICLES; POLYETHYLENE GLYCOLS; POLYLYSINE; POLYMERS; RESPIRATORY MUCOSA;

MUS;

EID: 84855721343     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.11.080     Document Type: Article

References (48)

1. Griesenbach U., Alton E.W. Gene transfer to the lung: lessons learned from more than 2 decades of CF gene therapy. Adv Drug Deliv Rev 2009, 61(2):128-139.
2. Ziady A.G., Davis P.B., Konstan M.W. Non-viral gene transfer therapy for cystic fibrosis. Expert Opin Biol Ther 2003, 3(3):449-458.
3. Fasbender A., Zabner J., Zeiher B.G., Welsh M.J. Alow rate of cell proliferation and reduced DNA uptake limit cationic lipid-mediated gene transfer to primary cultures of ciliated human airway epithelia. Gene Ther 1997, 4(11):1173-1180.
4. Suh J., Wirtz D., Hanes J. Efficient active transport of gene nanocarriers to the cell nucleus. Proc Natl Acad Sci U S A 2003, 100(7):3878-3882.
5. 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.
6. Liu G., Li D., Pasumarthy M.K., Kowalczyk T.H., Gedeon C.R., Hyatt S.L., et al. Nanoparticles of compacted DNA transfect postmitotic cells. JBiol Chem 2003, 278(35):32578-32586.
7. Ziady A.G., Gedeon C.R., Miller T., Quan W., Payne J.M., Hyatt S.L., et al. Transfection of airway epithelium by stable PEGylated poly-l-lysine DNA nanoparticles invivo. Mol Ther 2003, 8(6):936-947.
8. Yurek D.M., Fletcher A.M., Smith G.M., Seroogy K.B., Ziady A.G., Molter J., et al. Long-term transgene expression in the central nervous system using DNA nanoparticles. Mol Ther 2009, 17(4):641-650.
9. Farjo R., Skaggs J., Quiambao A.B., Cooper M.J., Naash M.I. Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PLoS ONE 2006, 1. e38.
10. Ziady A.G., Gedeon C.R., Muhammad O., Stillwell V., Oette S.M., Fink T.L., et al. Minimal toxicity of stabilized compacted DNA nanoparticles in the murine lung. Mol Ther 2003, 8(6):948-956.
11. Ding X.Q., Quiambao A.B., Fitzgerald J.B., Cooper M.J., Conley S.M., Naash M.I. Ocular delivery of compacted DNA-nanoparticles does not elicit toxicity in the mouse retina. PLoS ONE 2009, 4(10). e7410.
12. Chen X., Kube D.M., Cooper M.J., Davis P.B. Cell surface nucleolin serves as receptor for DNA nanoparticles composed of pegylated polylysine and DNA. Mol Ther 2007, 16(2):333-342.
13. Chen X., Shank S., Davis P.B., Ziady A.G. Nucleolin-mediated cellular trafficking of DNA nanoparticle is lipid raft and microtubule dependent and can be modulated by glucocorticoid. Mol Ther 2011, 19(1):93-102.
14. Rejman J., Bragonzi A., Conese M. Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes. Mol Ther 2005, 12(3):468-474.
15. Nguyen D.N., Green J.J., Chan J.M., Langer R., Anderson D.G. Polymeric materials for gene delivery and DNA vaccination. Adv Mater 2009, 21(8):847-867.
16. Pack D.W., Hoffman A.S., Pun S., Stayton P.S. Design and development of polymers for gene delivery. Nat Rev Drug Discov 2005, 4(7):581-593.
17. Wong S.Y., Pelet J.M., Putnam D. Polymer systems for gene delivery-past, present, and future. Prog Polym Sci. 2007, 32(8-9):799-837.
18. Behr J.-P. The proton sponge: a trick to enter cells the viruses did not exploit. Chimia 1997, 51:34-36.
19. Sonawane N.D., Szoka F.C., Verkman A.S. Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes. JBiol Chem 2003, 278(45):44826-44831.
20. Wong S.Y., Sood N., Putnam D. Combinatorial evaluation of cations, pH-sensitive and hydrophobic moieties for polymeric vector design. Mol Ther 2009, 17(3):480-490.
21. Midoux P., Monsigny M. Efficient gene transfer by histidylated polylysine/pDNA complexes. Bioconjug Chem 1999, 10(3):406-411.
22. Zhong Z., Feijen J., Lok M.C., Hennink W.E., Christensen L.V., Yockman J.W., et al. Low molecular weight linear polyethylenimine-b-poly(ethylene glycol)-b-polyethylenimine triblock copolymers: synthesis, characterization, and invitro gene transfer properties. Biomacromolecules 2005, 6(6):3440-3448.
23. Rao G.V., Tinkle S., Weissman D.N., Antonini J.M., Kashon M.L., Salmen R., et al. Efficacy of a technique for exposing the mouse lung to particles aspirated from the pharynx. JToxicol Environ Health A 2003, 66(15):1441-1452.
24. Rennard S.I., Basset G., Lecossier D., O'Donnell K.M., Pinkston P., Martin P.G., et al. Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. JAppl Physiol 1986, 60(2):532-538.
25. Boylan N.J., Suk J.S., Lai S.K., Jelinek R., Boyle M.P., Cooper M.J., et al. Highly compacted DNA nanoparticles with low MW PEG coatings: invitro, exvivo and invivo evaluation. JControl Release 2011, 10.1016/j.jconrel.2011.08.031.
26. Atsuta J., Sterbinsky S.A., Plitt J., Schwiebert L.M., Bochner B.S., Schleimer R.P. Phenotyping and cytokine regulation of the BEAS-2B human bronchial epithelial cell: demonstration of inducible expression of the adhesion molecules VCAM-1 and ICAM-1. Am J Respir Cell Mol Biol 1997, 17(5):571-582.
27. Kim A.J., Boylan N.J., Suk J.S., Lai S.K., Hanes J. Non-degradative intracellular trafficking of highly compacted polymeric DNA nanoparticles. JControl Release 2011, 10.1016/j.jconrel.2011.10.031.
28. Lai S.K., Hida K., Man S.T., Chen C., Machamer C., Schroer T.A., et al. Privileged delivery of polymer nanoparticles to the perinuclear region of live cells via a non-clathrin, non-degradative pathway. Biomaterials 2007, 28(18):2876-2884.
29. Rejman J., Oberle V., Zuhorn I.S., Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 2004, 377(Pt 1):159-169.
30. Zuhorn I.S., Kalicharan R., Hoekstra D. Lipoplex-mediated transfection of mammalian cells occurs through the cholesterol-dependent clathrin-mediated pathway of endocytosis. JBiol Chem. 2002, 277(20):18021-18028.
31. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci U S A 1999, 96(12):6775-6780.
32. Rodal S.K., Skretting G., Garred Ø, Vilhardt F., van Deurs B., Sandvig K. Extraction of cholesterol with methyl-β-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 1999, 10(4):961-974.
33. Zhang L., Button B., Gabriel S.E., Burkett S., Yan Y., Skiadopoulos M.H., et al. CFTR delivery to 25% of surface epithelial cells restores normal rates of mucus transport to human cystic fibrosis airway epithelium. PLoS Biol 2009, 7(7). e1000155.
34. Konstan M.W., Davis P.B., Wagener J.S., Hilliard K.A., Stern R.C., Milgram L.J., et al. 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 2004, 15(12):1255-1269.
35. Suk J.S., Boylan N.J., Trehan K., Tang B.C., Schneider C.S., Lin J.-M.G., et al. N-acetylcysteine enhances cystic fibrosis sputum penetration and airway gene transfer by highly compacted DNA nanoparticles. Mol Ther 2011, 10.1038/mt.2011.160.
36. Gratton S., Napier M., Ropp P., Tian S., DeSimone J. Microfabricated particles for engineered drug therapies: elucidation into the mechanisms of cellular internalization of PRINT particles. Pharm Res 2008, 25(12):2845-2852.
37. Harush-Frenkel O., Debotton N., Benita S., Altschuler Y. Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochem Biophys Res Commun 2007, 353(1):26-32.
38. Cho E.C., Xie J., Wurm P.A., Xia Y. Understanding the role of surface charges in cellular adsorption versus internalization by selectively removing gold nanoparticles on the cell surface with a I2/KI etchant. Nano Lett 2009, 9(3):1080-1084.
39. Villanueva A., Canete M., Roca A.G., Calero M., Veintemillas-Verdaguer S., Serna C.J., et al. The influence of surface functionalization on the enhanced internalization of magnetic nanoparticles in cancer cells. Nanotechnology 2009, 20(11). 115103.
40. Verma A., Stellacci F. Effect of surface properties on nanoparticle-cell interactions. Small 2010, 6(1):12-21.
41. Moghimi S.M., Symonds P., Murray J.C., Hunter A.C., Debska G., Szewczyk A. Atwo-stage poly(ethylenimine)-mediated cytotoxicity: implications for gene transfer/therapy. Mol Ther 2005, 11(6):990-995.
42. Beyerle A., Irmler M., Beckers J., Kissel T., Stoeger T. Toxicity pathway focused gene expression profiling of PEI-based polymers for pulmonary applications. Mol Pharm 2010, 7(3):727-737.
43. Merkel O.M., Urbanics R., Bedocs P., Rozsnyay Z., Rosivall L., Toth M., et al. Invitro and invivo complement activation and related anaphylactic effects associated with polyethylenimine and polyethylenimine-graft-poly(ethylene glycol) block copolymers. Biomaterials 2011, 32(21):4936-4942.
44. Plank C., Mechtler K., Szoka F.C., Wagner E. Activation of the complement system by synthetic DNA complexes: a potential barrier for intravenous gene delivery. Hum Gene Ther 1996, 7(12):1437-1446.
45. Hyde S.C., Pringle I.A., Abdullah S., Lawton A.E., Davies L.A., Varathalingam A., et al. CpG-free plasmids confer reduced inflammation and sustained pulmonary gene expression. Nat Biotechnol 2008, 26(5):549-551.
46. Ziady A.G., Kotlarchyk M., Bryant L., McShane M., Lee Z. Bioluminescent imaging of reporter gene expression in the lungs of wildtype and model mice following the administration of PEG-stabilized DNA nanoparticles. Microsc Res Tech 2010, 73(9):918-928.
47. Gill D.R., Smyth S.E., Goddard C.A., Pringle I.A., Higgins C.F., Colledge W.H., et al. Increased persistence of lung gene expression using plasmids containing the ubiquitin C or elongation factor 1alpha promoter. Gene Ther 2001, 8(20):1539-1546.
48. Yew N.S., Przybylska M., Ziegler R.J., Liu D., Cheng S.H. High and sustained transgene expression invivo from plasmid vectors containing a hybrid ubiquitin promoter. Mol Ther 2001, 4(1):75-82.