PEGylated composite nanoparticles of PLGA and polyethylenimine for safe and efficient delivery of pDNA to lungs

International Journal of Pharmaceutics

Volumn 524, Issue 1-2, 2017, Pages 382-396

  Kolte, Atul ^a,b   Patil, Sushilkumar ^a   Lesimple, Pierre ^b   Hanrahan, John W ^b   Misra, Ambikanandan ^a  

^a M S UNIVERSITY OF BARODA   (India)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cystic fibrosis; Dry powder inhaler; Gene therapy; Nanoparticles; PEI; PLGA

Indexed keywords

LACTOSE PERMEASE; NANOPARTICLE; PLASMID DNA; POLYETHYLENEIMINE; POLYGLACTIN; DNA; LACTIC ACID; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER;

AEROSOL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG RELEASE; DRUG SAFETY; DRY POWDER; DRY POWDER INHALER; FREEZE DRYING; IN VITRO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; LUNG PARENCHYMA; MALE; MUCUS; NANOENCAPSULATION; NANOPHARMACEUTICS; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PARTICLE SIZE; PRIORITY JOURNAL; RAT; ZETA POTENTIAL; CELL LINE; CHEMISTRY; DRUG EFFECTS; GENETIC TRANSFECTION; HUMAN; LUNG;

CELL LINE; DNA; HUMANS; LACTIC ACID; LUNG; NANOPARTICLES; PARTICLE SIZE; POLYETHYLENEIMINE; POLYGLYCOLIC ACID; TRANSFECTION;

EID: 85017475832     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2017.03.094     Document Type: Article

References (54)

1. Alton, E., The UK gene therapy trial. Pediatr. Pulmonol. 49 (2014), 153–154.
2. Anjos, S.M., Robert, R., Waller, D., Zhang, D.L., Balghi, H., Sampson, H.M., Ciciriello, F., Lesimple, P., Carlile, G.W., Goepp, J., Liao, J., Ferraro, P., Phillipe, R., Dantzer, F., Hanrahan, J.W., Thomas, D.Y., Decreasing poly(ADP-ribose) polymerase activity restores DeltaF508 CFTR trafficking. Front. Pharmacol., 3, 2012, 165.
3. Arnold, M.M., Gorman, E.M., Schieber, L.J., Munson, E.J., Berkland, C., NanoCipro encapsulation in monodisperse large porous PLGA microparticles. J. Control. Release 121 (2007), 100–109.
4. Bivas-Benita, M., Romeijn, S., Junginger, H.E., Borchard, G., PLGA-PEI nanoparticles for gene delivery to pulmonary epithelium. Eur. J. Pharm. Biopharm. 58 (2004), 1–6.
5. Broughton-Head, V.J., Smith, J.R., Shur, J., Shute, J.K., Actin limits enhancement of nanoparticle diffusion through cystic fibrosis sputum by mucolytics. Pulm. Pharmacol. Ther. 20 (2007), 708–717.
6. Cheng, C.J., Saltzman, W.M., Enhanced siRNA delivery into cells by exploiting the synergy between targeting ligands and cell-penetrating peptides. Biomaterials 32 (2011), 6194–6203.
7. Croll, T.I., O'Connor, A.J., Stevens, G.W., Cooper-White, J.J., Controllable surface modification of poly(lactic-co-glycolic acid) (PLGA) by hydrolysis or aminolysis I: physical, chemical, and theoretical aspects. Biomacromolecules 5 (2004), 463–473.
8. Cu, Y., LeMoellic, C., Caplan, M.J., Saltzman, W.M., Ligand-modified gene carriers increased uptake in target cells but reduced DNA release and transfection efficiency. Nanomedicine 6 (2010), 334–343.
9. Drake, D.M., Pack, D.W., Biochemical investigation of active intracellular transport of polymeric gene-delivery vectors. J. Pharm. Sci. 97 (2008), 1399–1413.
10. Efremova, N.V., Huang, Y., Peppas, N.A., Leckband, D.E., Direct measurement of interactions between tethered poly(ethylene glycol) chains and adsorbed mucin layers. Langmuir 18 (2002), 836–845.
11. Forier, K., Messiaen, A.S., Raemdonck, K., Deschout, H., Rejman, J., De Baets, F., Nelis, H., De Smedt, S.C., Demeester, J., Coenye, T., Braeckmans, K., Transport of nanoparticles in cystic fibrosis sputum and bacterial biofilms by single-particle tracking microscopy. Nanomedicine 8 (2013), 935–949.
12. Forrest, M.L., Meister, G.E., Koerber, J.T., Pack, D.W., Partial acetylation of polyethylenimine enhances in vitro gene delivery. Pharm. Res. 21 (2004), 365–371.
13. Giri, J., Diallo, M.S., Simpson, A.J., Liu, Y., Goddard, W.A., Kumar, R., Woods, G.C., Interactions of poly(amidoamine) dendrimers with human serum albumin: binding constants and mechanisms. ACS Nano 5 (2011), 3456–3468.
14. Grabowski, N., Hillaireau, H., Vergnaud, J., Santiago, L.A., Kerdine-Romer, S., Pallardy, M., Tsapis, N., Fattal, E., Toxicity of surface-modified PLGA nanoparticles toward lung alveolar epithelial cells. Int. J. Pharm. 454 (2013), 686–694.
15. Griesenbach, U., Alton, E.W., Current status and future directions of gene and cell therapy for cystic fibrosis. BioDrugs 25 (2011), 77–88.
16. Guan, X.P., Quan, D.P., Liao, K.R., Tao, W., Peng, X., Mai, K.C., Preparation and characterization of cationic chitosan-modified poly(D,L-lactide-co-glycolide) copolymer nanospheres as DNA carriers. J. Biomater. Appl. 22 (2008), 353–371.
17. Gupta, V., Rawat, A., Ahsan, F., Feasibility study of aerosolized prostaglandin E1 microspheres as a noninvasive therapy for pulmonary arterial hypertension. J. Pharm. Sci. 99 (2010), 1774–1789.
18. Hunter, A.C., Moghimi, S.M., Cationic carriers of genetic material and cell death: a mitochondrial tale. Biochim. Biophys. Acta 1797 (2010), 1203–1209.
19. Ibricevic, A., Guntsen, S.P., Zhang, K., Shrestha, R., Liu, Y., Sun, J.Y., Welch, M.J., Wooley, K.L., Brody, S.L., PEGylation of cationic, shell-crosslinked-knedel-like nanoparticles modulates inflammation and enhances cellular uptake in the lung. Nanomedicine 9 (2013), 912–922.
20. Kim, I.S., Lee, S.K., Park, Y.M., Lee, Y.B., Shin, S.C., Lee, K.C., Oh, I.J., Physicochemical characterization of poly(L-lactic acid) and poly(D,L-lactide-co-glycolide) nanoparticles with polyethylenimine as gene delivery carrier. Int. J. Pharm. 298 (2005), 255–262.
21. Kircheis, R., Wightman, L., Wagner, E., Design and gene delivery activity of modified polyethylenimines. Adv. Drug Deliv. Rev. 53 (2001), 341–358.
22. Kolate, A., Baradia, D., Patil, S., Vhora, I., Kore, G., Misra, A., PEG − a versatile conjugating ligand for drugs and drug delivery systems. J. Control. Release 192 (2014), 67–81.
23. Kolate, A., Kore, G., Lesimple, P., Baradia, D., Patil, S., Hanrahan, J.W., Misra, A., Polymer assisted entrapment of netilmicin in PLGA nanoparticles for sustained antibacterial activity. J. Microencapsul. 32 (2015), 61–74.
24. Kunath, K., von Harpe, A., Fischer, D., Petersen, 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. Control. Release 89 (2003), 113–125.
25. Menon, J.U., Ravikumar, P., Pise, A., Gyawali, D., Hsia, C.C., Nguyen, K.T., Polymeric nanoparticles for pulmonary protein and DNA delivery. Acta Biomater. 10 (2014), 2643–2652.
26. Messai, I., Munier, S., Ataman-Önal, Y., Verrier, B., Delair, T., Elaboration of poly(ethyleneimine) coated poly(d,l-lactic acid) particles: effect of ionic strength on the surface properties and DNA binding capabilities. Colloids Surf. B: Biointerfaces 32 (2003), 293–305.
27. Mornon, J.P., Lehn, P., Callebaut, I., Molecular models of the open and closed states of the whole human CFTR protein. Cell. Mol. Life Sci. 66 (2009), 3469–3486.
28. Mura, S., Hillaireau, H., Nicolas, J., Le Droumaguet, B., Gueutin, C., Zanna, S., Tsapis, N., Fattal, E., Influence of surface charge on the potential toxicity of PLGA nanoparticles towards Calu-3 cells. Int. J. Nanomed. 6 (2011), 2591–2605.
29. Okamoto, H., Aoki, M., Danjo, K., A novel apparatus for rat in vivo evaluation of dry powder formulations for pulmonary administration. J. Pharm. Sci. 89 (2000), 1028–1035.
30. Oster, C.G., Kim, N., Grode, L., Barbu-Tudoran, L., Schaper, A.K., Kaufmann, S.H., Kissel, T., Cationic microparticles consisting of poly(lactide-co-glycolide) and polyethylenimine as carriers systems for parental DNA vaccination. J. Control. Release 104 (2005), 359–377.
31. Patil, Y., Panyam, J., Polymeric nanoparticles for siRNA delivery and gene silencing. Int. J. Pharm. 367 (2009), 195–203.
32. Peppas, N.A., Analysis of Fickian and non-Fickian drug release from polymers. Pharm. Acta Helv. 60 (1985), 110–111.
33. Pfeifer, C., Hasenpusch, G., Uezguen, S., Aneja, M.K., Reinhardt, D., Kirch, J., Schneider, M., Claus, S., Friess, W., Rudolph, C., Dry powder aerosols of polyethylenimine (PEI)-based gene vectors mediate efficient gene delivery to the lung. J. Control. Release 154 (2011), 69–76.
34. Pierrat, P., Creusat, G., Laverny, G., Pons, F., Zuber, G., Lebeau, L., A cationic phospholipid-detergent conjugate as a new efficient carrier for siRNA delivery. Chemistry 18 (2012), 3835–3839.
35. Ravi Kumar, M.N., Bakowsky, U., Lehr, C.M., Preparation and characterization of cationic PLGA nanospheres as DNA carriers. Biomaterials 25 (2004), 1771–1777.
36. Robert, R., Carlile, G.W., Liao, J., Balghi, H., Lesimple, P., Liu, N., Kus, B., Rotin, D., Wilke, M., de Jonge, H.R., Scholte, B.J., Thomas, D.Y., Hanrahan, J.W., Correction of the Delta phe508 cystic fibrosis transmembrane conductance regulator trafficking defect by the bioavailable compound glafenine. Mol. Pharmacol. 77 (2010), 922–930.
37. Ruiz, F.E., Clancy, J.P., Perricone, M.A., Bebok, Z., Hong, J.S., Cheng, S.H., Meeker, D.P., Young, K.R., Schoumacher, R.A., Weatherly, M.R., Wing, L., Morris, J.E., Sindel, L., Rosenberg, M., van Ginkel, F.W., McGhee, J.R., Kelly, D., Lyrene, R.K., Sorscher, E.J., A clinical inflammatory syndrome attributable to aerosolized lipid-DNA administration in cystic fibrosis. Hum. Gene Ther. 12 (2001), 751–761.
38. Rytting, E., Nguyen, J., Wang, X., Kissel, T., Biodegradable polymeric nanocarriers for pulmonary drug delivery. Expert Opin. Drug Deliv. 5 (2008), 629–639.
39. Sampson, H.M., Robert, R., Liao, J., Matthes, E., Carlile, G.W., Hanrahan, J.W., Thomas, D.Y., Identification of a NBD1-binding pharmacological chaperone that corrects the trafficking defect of F508del-CFTR. Chem. Biol. 18 (2011), 231–242.
40. Sanders, N.N., De Smedt, S.C., Van Rompaey, E., Simoens, P., De Baets, F., Demeester, J., Cystic fibrosis sputum: a barrier to the transport of nanospheres. Am. J. Respir. Crit. Care Med. 162 (2000), 1905–1911.
41. Suh, J., Choy, K.L., Lai, S.K., Suk, J.S., Tang, B.C., Prabhu, S., Hanes, J., PEGylation of nanoparticles improves their cytoplasmic transport. Int. J. Nanomed. 2 (2007), 735–741.
42. Suk, J., Hanes, J.S., Mucus Penetrating Gene Carrier. 2016, The Johns Hopkins University.
43. Suk, J.S., Lai, S.K., Wang, Y.Y., Ensign, L.M., Zeitlin, P.L., Boyle, M.P., Hanes, J., The penetration of fresh undiluted sputum expectorated by cystic fibrosis patients by non-adhesive polymer nanoparticles. Biomaterials 30 (2009), 2591–2597.
44. Suk, J.S., Lai, S.K., Boylan, N.J., Dawson, M.R., Boyle, M.P., Hanes, J., Rapid transport of muco-inert nanoparticles in cystic fibrosis sputum treated with N-acetyl cysteine. Nanomedicine 6 (2011), 365–375.
45. Tang, B.C., Dawson, M., Lai, S.K., Wang, Y.-Y., Suk, J.S., Yang, M., Zeitlin, P., Boyle, M.P., Fu, J., Hanes, J., Biodegradable polymer nanoparticles that rapidly penetrate the human mucus barrier. Proc. Natl. Acad. Sci. 106 (2009), 19268–19273.
46. Thomas, C.E., Ehrhardt, A., Kay, M.A., Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet. 4 (2003), 346–358.
47. Tse, M.T., Blatchford, C., Oya Alpar, H., Evaluation of different buffers on plasmid DNA encapsulation into PLGA microparticles. Int. J. Pharm. 370 (2009), 33–40.
48. The United States Pharmacopeia (USP), Chapter 601: Aerosols, Nasal Sprays, Metered-Dose Inhalers, and Dry Powder Inhalers. 2012, USP 35-NF30, Rockville, MD.
49. Ungaro, F., d'Angelo, I., Coletta, C., d'Emmanuele di Villa Bianca, R., Sorrentino, R., Perfetto, B., Tufano, M.A., Miro, A., La Rotonda, M.I., Quaglia, F., Dry powders based on PLGA nanoparticles for pulmonary delivery of antibiotics: modulation of encapsulation efficiency, release rate and lung deposition pattern by hydrophilic polymers. J. Control. Release 157 (2012), 149–159.
50. Wang, C., Ge, Q., Ting, D., Nguyen, D., Shen, H.R., Chen, J., Eisen, H.N., Heller, J., Langer, R., Putnam, D., Molecularly engineered poly(ortho ester) microspheres for enhanced delivery of DNA vaccines. Nat. Mater. 3 (2004), 190–196.
51. Woodrow, K.A., Cu, Y., Booth, C.J., Saucier-Sawyer, J.K., Wood, M.J., Saltzman, W.M., Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nat. Mater. 8 (2009), 526–533.
52. Xu, Q., Ensign, L.M., Boylan, N.J., Schon, A., Gong, X., Yang, J.C., Lamb, N.W., Cai, S., Yu, T., Freire, E., Hanes, J., Impact of surface polyethylene glycol (PEG) density on biodegradable nanoparticle transport in mucus ex vivo and distribution in vivo. ACS Nano 9 (2015), 9217–9227.
53. Yang, Y., Tsifansky, M.D., Shin, S., Lin, Q., Yeo, Y., Mannitol-guided delivery of Ciprofloxacin in artificial cystic fibrosis mucus model. Biotechnol. Bioeng. 108 (2011), 1441–1449.
54. Zolnik, B.S., Burgess, D.J., Effect of acidic pH on PLGA microsphere degradation and release. J. Control. Release 122 (2007), 338–344.