'Smart' non-viral delivery systems for targeted delivery of RNAi to the lungs

Therapeutic Delivery

Volumn 4, Issue 1, 2013, Pages 59-76

  Ramsey, Joanne M ^a   Hibbitts, Alan ^a   Barlow, James ^a   Kelly, Ciara ^a,b   Sivadas, Neeraj ^a,c   Cryan, Sally Ann ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c Freund Pharmatec Ltd   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CATIONIC LIPOSOME; CELL PENETRATING PEPTIDE; CHITOSAN; CHOLESTEROL; COPOLYMER; CYCLODEXTRIN; DRUG CARRIER; EXCIPIENT; HIGH MOLECULAR WEIGHT CHITOSAN; LIPID; LIPOSOME; LOW MOLECULAR WEIGHT CHITOSAN; MACROGOL; NANOPARTICLE; NUCLEIC ACID; PEPTIDE DERIVATIVE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PLACEBO; POLYETHYLENEIMINE; POLYGLACTIN; POLYLACTIC ACID; POLYMER; PROTEIN DERIVATIVE; SALBUTAMOL; SEBACIC ACID; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AEROSOL; BIOCOMPATIBILITY; BIODEGRADABILITY; BIOENGINEERING; CELL SPECIFICITY; CELL TYPE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYSTIC FIBROSIS; DRUG EFFICACY; DRUG HALF LIFE; DRUG SAFETY; DRUG STABILITY; DRUG TOLERABILITY; EPITHELIUM CELL; FREEZE DRYING; HUMAN; IMMUNOGENICITY; INHALER; LUNG ALVEOLUS MACROPHAGE; LUNG CANCER; LUNG FIBROSIS; METERED DOSE INHALER; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PARAINFLUENZA VIRUS INFECTION; PATIENT COMPLIANCE; PHYSICAL CHEMISTRY; PNEUMONIA; POWDER INHALER; PRIORITY JOURNAL; PROCEDURES; RESPIRATORY EPITHELIUM; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RESPIRATORY TRACT DISEASE; RESPIRATORY TRACT INFECTION; REVIEW; RNA INTERFERENCE; SUPERCRITICAL FLUID; TARGET CELL; VIRAL RESPIRATORY TRACT INFECTION;

EID: 84871561844     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.12.133     Document Type: Review

References (133)

1. Courrier HM, Butz N, Vandamme TF. Pulmonary drug delivery systems: recent developments and prospects. Crit. Rev. Ther. Drug Carrier Syst. 19(4-5), 425-498 (2002).
2. Shan G. RNA interference as a gene knockdown technique. Int. J. Biochem. Cell Biol. 42(8), 1243-1251 (2010).
3. Kong Y, Ruan L, Ma L et al. RNA interference as a novel and powerful tool in immunopharmacological research. Int. Immunopharmacol. 7(4), 417-426 (2007).
4. Kim DH, Rossi JJ. RNAi mechanisms and applications. Biotechniques 44(5), 613-616 (2008).
5. Kaiser PK, Symons RC, Shah SM et al. RNAi-based treatment for neovascular age-related macular degeneration by siRNA-027. Am. J. Ophthalmol. 150(1), 33-39 (2010).
6. Cotrim AP and Baum BJ. Gene therapy: some history, applications, problems, and prospects. Toxicol. Pathol 36(1), 97-103. (2008).
7. Patton JS, Byron PR. Inhaling medicines: delivering drugs to the body through the lungs. Nat. Rev. Drug Discov. 6(1), 67-74 (2007).
8. Akhtar S, Benter IF. Non-viral delivery of synthetic siRNAs in vivo. J. Clin. Investig. 117(12), 3623 (2007).
9. Merkel OM, Zheng M, H Debus H, Kissel T. Pulmonary gene delivery using polymeric non-viral vectors. Bioconjug. Chem. 23(1), 3-20 (2012).
10. Roy I, Vij N. Nano-delivery in airway diseases: challenges and therapeutic applications. Nanomedicine 6(2), 237-244 (2009).
11. Hornung V, Guenthner-Biller M, Bourquin C et al. Sequence-specific potent induction of IFN-alpha by short interfering RNA in plasmacytoid dendritic cells through TLR7. Nat. Med. 11(3), 263-270 (2005).
12. Judge AD, Sood V, Shaw JR, Fang D, McClintock K, MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23(4), 457-462 (2005).
13. Chiu YL, Ali A, Chu CY, Cao H, Rana TM. Visualizing a correlation between siRNA localization, cellular uptake and RNAi in living cells. Chem. Biol. 11(8), 1165-1175 (2004).
14. Kim SH, Mok H, Jeong JH, Kim SW, Park TG. Comparative evaluation of target-specific GFP gene silencing efficiencies for antisense ODN, synthetic siRNA, and siRNA plasmid complexed with PEI632 PEG-FOL conjugate. Bioconjug. Chem. 17(1), 241-244 (2006).
15. Li CX, Parker A, Menocal E, Xiang S, Borodyansky L, Fruehauf JH et al. Delivery of RNA interference. Cell Cycle 5(18), 2103-2109 (2006).
16. Bitko V, Musiyenko A, Shulyayeva O, Barik S. Inhibition of respiratory viruses by nasally administered siRNA. Nat. Med. 11(1), 50-55 (2005).
17. Edwards DA, Dunbar C. Bioengineering of therapeutic aerosols. Ann. Rev. Biomed. Engin. 4(1), 93-107 (2002).
18. Frijlink HW, de Boer AH. Trends in the technology-driven development of new inhalation devices. Drug Discov. Today 2(1), 47-57 (2005).
19. Chow AH, Tong HH, Chattopadhyay P, Shekunov BY. Particle engineering for pulmonary drug delivery. Pharm. Res. 24(3), 411-437 (2007).
20. Swarbrick J, Boylan JC. Encyclopedia of Pharmaceutical Technology. Informa Health Care, New York, NY, USA. (2002).
21. Sivadas N, O'Rourke D, Tobin A et al. A comparative study of a range of polymeric microspheres as potential carriers for the inhalation of proteins. Int. J. Pharm. 358(1), 159-167 (2008).
22. Santel A, Giese K, Kaufmann J. The AtuPLEX technology for therapeutic siRNA delivery in oncology. Drug Delivery Technology 10(2), 54-57 (2010).
23. Semple SC, Akinc A, Chen J et al. Rational design of cationic lipids for siRNA delivery. Nat. Biotech. 28(2), 172-176 (2010).
24. Haussecker D. The Business of RNAi Therapeutics in 2012. Molecular Therapy Nucleic Acids 1(2), e8 (2012).
25. Garbuzenko OB, Saad M, Betigeri S et al. Intratracheal versus intravenous liposomal delivery of siRNA, antisense oligonucleotides and anticancer drug. Pharm. Res. 26(2), 382-394 (2009).
26. Lomas-Neira JL, Chung CS, Wesche DE, Perl M, Ayala A et al. In vivo gene silencing (with siRNA) of pulmonary expression of MIP-2 versus KC results in divergent effects on hemorrhage-induced, neutrophil-mediated septic acute lung injury. J. Leukocyte Biol. 77(6), 846-853 (2005).
27. Adjei AL, Gupta PK. Inhalation Delivery of Therapeutic Peptides and Proteins. Informa Health Care, New York, NY, USA (1997).
28. Sakagami M, Byron PR. Respirable microspheres for inhalation: the potential of manipulating pulmonary disposition for improved therapeutic efficacy. Clin. Pharmaco. 44(3), 263 (2005).
29. Edwards DA, Ben-Jebria A, Langer R. Large porous particles for pulmonary drug delivery. Science 276(5320), 1868-1871 (1997).
30. Fu J, Fiegel J, Krauland E, Hanes J. New polymeric carriers for controlled drug delivery following inhalation or injection. Biomaterials 23(22), 4425-4433 (2002).
31. Uchegbu IF, Schätzlein AG. Polymers in drug delivery. CRC Press, Taylor and Francis, Boca Raton, FL, USA (2006).
32. Puente XS, Ordonez GR, López-Otín C et al. The Cancer Degradome (Proteases and Cancer Biology). Edwards D, Hoyer-Hansen G, Blasi F, Sloane BF (Eds). Springer Publishers, NY, USA. (2008).
33. Sivadas N, Cryan SA. Inhalable, bioresponsive microparticles for targeted drug delivery in the lungs. J. Pharm. Pharmacol. 63(3), 369-375 (2011).
34. Knowles MR, Boucher RC. Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109(5), 571-577 (2002).
35. Antunes MB, Cohen NA. Mucociliary clearance-a critical upper airway host defense mechanism and methods of assessment. Curr. Opin. Allergy Clin. Immunol. 7(1), 5-10 (2007).
36. Sanders N, Rudolph C, Braeckmans K, De Smedt SC, Demeester J. Extracellular barriers in respiratory gene therapy. Adv. Drug Deliv. Rev. 61(2), 115-127 (2009).
37. Maina JN, West JB, Orgeig S et al. Recent advances into understanding some aspects of the structure and function of mammalian and avian lungs. Physiol. Biochem. Zool. 83(5), 792-807 (2010).
38. Goerke J. Pulmonary surfactant: functions and molecular composition. Biochim. Biophys. Acta 1408(2-3), 79-89 (1998).
39. Sutinen S, Riska H, Backman R, Sutinen SH, Fröseth B. Alveolar lavage fluid (ALF) of normal volunteer subjects: cytologic, immunocytochemical, and biochemical reference values. Respir. Med. 89(2), 85-92 (1995).
40. Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4(2), 145-160 (2005).
41. Felgner PL, Gadek TR, Holm M et al. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl Acad. Sci. USA 84(21), 7413-7417 (1987).
42. Malone RW, Felgner PL, Verma IM. Cationic liposome-mediated RNA transfection. Proc. Natl Acad. Sci. USA 86(16) 6077-6081 (1989).
43. Dokka S, Toledo D, Shi X, Castranova V, Rojanasakul Y. Oxygen radical-mediated pulmonary toxicity induced by some cationic liposomes. Pharm. Res. 17(5), 521-525 (2000).
44. Hobel S, Aigner A. Nonviral delivery platform for therapeutic RNAi: pegylated siRNA/cationic liposome complexes for targeting of the proto-oncogene bcl-2. Future Oncol. 5(1), 13-17 (2009).
45. Mishra S, Webster P, Davis ME. PEGylation significantly affects cellular uptake and intracellular trafficking of non-viral gene delivery particles. Eur. J. Cell Biol. 83(3), 97-111 (2004).
46. Shi F, Wasungu L, Nomden A et al. Interference of poly(ethylene glycol)-lipid analogues with cationic-lipid mediated delivery of oligonucleotides; role of lipid exchangeability and non-lamellar transitions. Biochem. J. 366(Pt 1), 333-341 (2002).
47. Cryan SA, Devocelle M, Moran PJ, Hickey AJ, Kelly JG. Increased intracellular targeting to airway cells using octaarginine coated liposomes: in vitro assessment of their suitability for inhalation. Mol. Pharm. 3(2), 104-112 (2006).
48. Baker SM, Kim N, Gumpert AM, Segretain D, Falk MM. Acute internalization of gap junctions in vascular endothelial cells in response to inflammatory mediator-induced G-protein coupled receptor activation. FEBS Lett. 582(29), 4039-4046 (2008).
49. Dong C, Filipeanu CM, Duvernay MT, Wu G. Regulation of G protein-coupled receptor export trafficking. Biochim. Biophys. Acta 1768(4), 853-870 (2007).
50. Allon N, Saxena A, Chambers C, Doctor BP. A new liposome-based gene delivery system targeting lung epithelial cells using endothelin antagonist. J. Control. Release 160(2), 217-224 (2012).
51. Davidson TJ, Harel S, Arboleda VA et al. Highly efficient small interfering RNA delivery to primary mammalian neurons induces MicroRNA-like effects before mRNA degradation. J. Neurosci. 24(45), 10040-10046 (2004).
52. Muratovska A, Eccles MR. Conjugate for efficient delivery of short interfering RNA (siRNA) into mammalian cells. FEBS Lett. 558(1-3), 63-68 (2004).
53. Wang YH, Hou YW, Lee HJ. An intracellular delivery method for siRNA by an arginine-rich peptide. J. Biochem. Biophys. Methods 70(4), 579-586 (2007).
54. Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55(6), 1189-1193 (1988).
55. Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus TAT trans-activator protein. Cell 55(6), 1179-1188 (1988).
56. Moschos SA, Jones SW, Perry MM et al. Lung delivery studies using siRNA conjugated to TAT (48-60) and penetration reveal peptide induced reduction in gene expression and induction of innate immunity. Bioconjug. Chem. 18(5), 1450-1459 (2007).
57. Baoum A, Ovcharenko D, Berkland C. Calcium condensed cell penetrating peptide complexes offer highly efficient, low toxicity gene silencing. Int. J. Pharm. 427(1), 134-142 (2012).
58. Mitchell DJ, Kim DT, Steinman L, Fathman CG, Rothbard JB. Polyarginine enters cells more efficiently than other polycationic homopolymers. J. Pept. Res. 56(5), 318-325 (2000).
59. Derossi D, Joliot AH, Chassaing G, Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269(14), 10444-10450 (1994).
60. Meyer M, Dohmen C, Philipp A et al. Synthesis and biological evaluation of a bioresponsive and endosomolytic siRNA-polymer conjugate. Mol. Pharm. 6(3), 752-762 (2009).
61. Meade BR, Dowdy SF. Enhancing the cellular uptake of siRNA duplexes following noncovalent packaging with protein transduction domain peptides. Adv. Drug Deliv. Rev. 60(4-5) 530-536 (2008).
62. Eguchi A, Dowdy SF. siRNA delivery using peptide transduction domains. Trends Pharmacol. Sci. 30(7), 341-345 (2009).
63. Wu M, Pasula R, Smith PA, Martin WJ 2nd. Mapping alveolar binding sites in vivo using phage peptide libraries. Gene Ther. 10(17), 1429-1436 (2003).
64. Beyerle A, Braun A, Merkel O, Koch F, Kissel T, Stoeger T. Comparative in vivo study of poly(ethylene imine)/siRNA complexes for pulmonary delivery in mice. J. Control. Release 151(1), 51-56 (2011).
65. Günther M, Lipka J, Malek A, Gutsch D, Kreyling W, Aigner A. Polyethylenimines for RNAi-mediated gene targeting in vivo and siRNA delivery to the lung. Eur. J. Pharm. Biopharm. 77(3), 438-449 (2011).
66. Boussif O, Lezoualc'h F, Zanta MA et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl Acad. Sci. USA 92(16) 7297-301 (1995).
67. Goula D, Remy JS, Erbacher P et al. Size, diffusibility and transfection performance of linear PEI/DNA complexes in the mouse central nervous system. Gene Ther. 5(5), 712-717 (1998).
68. Kren BT, Parashar B, Bandyopadhyay P, Chowdhury NR, Chowdhury JR, Steer CJ. Correction of the UDP-glucuronosyltransferase gene defect in the gunn rat model of crigler-najjar syndrome type I with a chimeric oligonucleotide. Proc. Natl Acad. Sci. USA 96(18), 10349-10354 (1999).
69. Kim SH, Jeong JH, Lee SH, Kim SW, Park TG et al. Local and systemic delivery of VEGF siRNA using polyelectrolyte complex micelles for effective treatment of cancer. J. Control. Release 129(2), 107-116 (2008).
70. Ogris M, Brunner S, Schüller S, Kircheis R, Wagner E. PEGylated DNA/transferrin-PEI complexes: reduced interaction with blood components, extended circulation in blood and potential for systemic gene delivery. Gene Ther. 6(4), 595-605 (1999).
71. Godbey WT, Mikos AG. Recent progress in gene delivery using non-viral transfer complexes. J. Control. Release 72(1-3), 115-125 (2001).
72. Hsu CY, Uludag H. Cellular uptake pathways of lipid-modified cationic polymers in gene delivery to primary cells. Biomaterials 33(31), 7834-7848 (2012).
73. Merkel OM, Beyerle A, Librizzi D et al. Nonviral siRNA delivery to the lung: investigation of PEG-PEI polyplexes and their in vivo performance. Mol. Pharm. 6(4), 1246-1260 (2009).
74. Petersen H, Fechner PM, Martin AL et al. Polyethylenimine-graft- poly(ethylene glycol) copolymers: influence of copolymer block structure on DNA complexation and biological activities as gene delivery system. Bioconjug. Chem. 13(4), 845-854 (2002).
75. Mao S, Neu M, Germershaus O et al. Influence of polyethylene glycol chain length on the physicochemical and biological properties of poly(ethylene imine)-graft-poly(ethylene glycol) block copolymer/siRNA polyplexes. Bioconjug. Chem. 17(5), 1209-1218 (2006).
76. Beyerle A, Merkel O, Stoeger T, Kissel T. PEGylation affects cytotoxicity and cell-compatibility of poly(ethylene imine) for lung application: structure-function relationships. Toxicol. Appl. Pharmacol. 242(2), 146-154 (2010).
77. Beyerle A, Long AS, White PA, Kissel T, Stoeger T. Poly(ethylene imine) nanocarriers do not induce mutations noroxidative DNA damage in vitro in MutaMouse FE1 cells. Mol. Pharm. 8(3), 976-981 (2011).
78. Hibbitts A, Lieggi N, McCabe O et al. Screening of siRNA nanoparticles for delivery to airway epithelial cells using high-content analysis. Therap. Deliv. 2(8), 987-999 (2011).
79. Florea BI, Meaney C, Junginger HE, Borchard G. Transfection efficiency and toxicity of polyethylenimine in differentiated Calu-3 and nondifferentiated COS-1 cell cultures. AAPS PharmSci. 4(3), E12 (2002).
80. Suh J, Choy KL, Lai SK et al. PEGylation of nanoparticles improves their cytoplasmic transport. Int. J. Nanomedicine 2(4), 735-741 (2007).
81. Tang BC, Dawson M, Lai SK et al. Biodegradable polymer nanoparticles that rapidly penetrate the human mucus barrier. Proc. Natl Acad. Sci. USA 106(46), 19268-19273 (2009).
82. Kunath K, Merdan T, Hegener O, Häberlein H, Kissel T. Integrin targeting using RGD-PEI conjugates for in vitro gene transfer. J. Gene Med. 5(7), 588-599 (2003).
83. Köping-Höggård M, Vårum KM, Issa M et al. Improved chitosan-mediated gene delivery based on easily dissociated chitosan polyplexes of highly defined chitosan oligomers. Gene Ther. 11(19), 1441-1452 (2004).
84. Lee MK, Chun SK, Choi WJ et al. The use of chitosan as a condensing agent to enhance emulsion mediated gene transfer. Biomaterials 26(14), 2147-2156 (2005).
85. Shu XZ, Zhu KJ. The influence of multivalent phosphate structure on the properties of ionically cross-linked chitosan films for controlled drug release. Eur. J. Pharm. Biopharm. 54(2), 235-243 (2002).
86. Liu X, Howard KA, Dong M et al. The influence of polymeric properties on chitosan/siRNA nanoparticle formulation and gene silencing. Biomaterials 28(6), 1280-1288 (2007).
87. Cai G, Jiang H, Tu K, Wang L, Zhu K. A facile route for regioselective conjugation of organo-soluble polymers onto chitosan. Macromol. Biosci. 9(3), 256-261 (2009).
88. Jiang HL, Park IK, Shin NR et al. In vitro study of the immune stimulating activity of an atrophic [correction of athrophic] rhinitis vaccine associated to chitosan microspheres. Eur. J. Pharm. Biopharm. 58(3), 471-476 (2004).
89. Noh SM, Park MO, Shim G et al. Pegylated poly-l-arginine derivatives of chitosan for effective delivery of siRNA. J. Control. Release 145(2), 159-64 (2010).
90. Luo Y, Zhai X, Ma C et al. An inhalable beta(2)-adrenoceptor ligand-directed guanidinylated chitosan carrier for targeted delivery of siRNA to lung. J. Control. Release 162(1), 28-36 (2012).
91. Chan P, Kurisawa M, Chung JE, Yang YY. Synthesis and characterization of chitosan-g-poly(ethylene glycol)-folate as a non-viral carrier for tumor-targeted gene delivery. Biomaterials 28(3), 540-549 (2007).
92. Gao S, Chen J, Xu X. Galactosylated low molecular weight chitosan as DNA carrier for hepatocyte-targeting. Int. J. Pharm. 255(1-2), 57-68 (2003).
93. Mao HQ, Roy K, Troung-Le VL et al. Chitosan-DNA nanoparticles as gene carriers: synthesis, characterization and transfection efficiency. J. Control. Release 70(3), 399-421 (2001).
94. Li J, Loh XJ. Cyclodextrin-based supramolecular architectures: syntheses, structures, and applications for drug and gene delivery. Adv. Drug Deliv. Rev. 60(9), 1000-1017 (2008).
95. Frank DW, Gray JE, Weaver RN. Cyclodextrin nephrosis in the rat. Am. J. Pathol. 83(2), 367-382 (1976).
96. O'Mahony AM, Ogier J, Desgranges S, Cryan JF, Darcy R, O'Driscoll CM. A click chemistry route to 2-functionalised PEGylated and cationic beta-cyclodextrins: co-formulation opportunities for siRNA delivery. Org. Biomol. Chem. 10(25), 4954-4960 (2012).
97. Ping Y, Liu C, Zhang Z, Liu KL, Chen J, Li J. Chitosan-graft-(PEI-beta- cyclodextrin) copolymers and their supramolecular PEGylation for DNA and siRNA delivery. Biomaterials 32(32), 8328-8341 (2011).
98. Paul SM, Mytelka DS, Dunwiddie CT et al. How to improve R&D productivity: the pharmaceutical industry's grand challenge. Nat. Rev. Drug Discov. 9(3), 203-214 (2010).
99. Pammolli F, Magazzini L, Riccaboni M. The productivity crisis in pharmaceutical R&D. Nat. Rev. Drug Discov. 10(6), 428-438 (2011).
100. Lee H, Jeong JH, Lee JH, Park TG. Enhancing transfection efficiency using polyethylene glycol grafted polyethylenimine and fusogenic peptide. Biotechnol. Bioprocess. Engin. 6(4), 269-273 (2001).
101. Brus C, Petersen H, Aigner A, Czubayko F, Kissel T et al. Synthesis, characterization, and biocompatibility of polyethylenimine-graft-poly(ethylene glycol) block copolymers. Macromolecules 35(18), 6867-6874 (2002).
102. Lawlor C, O'Sullivan MP, Rice B et al. Therapeutic aerosol bioengineering of targeted, inhalable microparticle formulations to treat Mycobacterium tuberculosis (MTb). J. Mater. Sci. Mater. Med. 23, 89-98 (2012).
103. Rosas-Taracoa AG, Higginsa DM, Sánchez-Campilloa J et al. Local pulmonary immunotherapy with siRNA targeting TGFb1 enhances antimicrobial capacity in Mycobacterium tuberculosis infected mice. Tuberculosis 91(1), 98-106 (2011).
104. Kapoor M, Burgess DJ, Patil SD. Physicochemical characterization techniques for lipid based delivery systems for siRNA. Int. J. Pharm. 427 (1), 35-57 (2012).
105. Immordino ML, Dosio F, Cattel L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int. J. Nanomed. 1(3), 297-315 (2006).
106. Ahsan F, Rivas IP, Khan MA, Torres Suarez AI. Targeting to macrophages: role of physicochemical properties of particulate carriers-liposomes and microspheres-on the phagocytosis by macrophages. J. Control. Release 79(1-3), 29-40 (2002).
107. Chono S, Tanino T, Seki T, Morimoto K. Influence of particle size on drug delivery to rat alveolar macrophages following pulmonary administration of ciprofloxacin incorporated into liposomes. J. Drug Target. 14(8), 557-566 (2006).
108. Chono S, Tanino T, Seki T, Morimoto K. Uptake characteristics of liposomes by rat alveolar macrophages: influence of particle size and surface mannose modification. J. Pharm. Pharmacol. 59(1), 75-80 (2007).
109. Fidler IJ, Raz A, Fogler WE, Kirsh R, Bugelski P, Poste G. Design of liposomes to improve delivery of macrophage-augmenting agents to alveolar macrophages. Cancer Res. 40(12), 4460-4466 (1980).
110. Moghimi SM, Hunter AC. Recognition by macrophages and liver cells of opsonized phospholipid vesicles and phospholipid headgroups. Pharm. Res. 18(1), 1-8 (2001).
111. Vyas SP, Kannan ME, Jain S, Mishra V, Singh P. Design of liposomal aerosols for improved delivery of rifampicin to alveolar macrophages. Int. J. Pharm. 269(1), 37-49 (2004).
112. Gibbons A, Padilla-Carlin D, Kelly C. The effect of liposome encapsulation on the pharmacokinetics of recombinant secretory leukocyte protease inhibitor (rSLPI) therapy after local delivery to a guinea pig asthma model. Pharm. Res. 28(9), 2233-2245 (2011).
113. Koning GA, Kamps JA, Scherphof GL. Interference of macrophages with immunotargeting of liposomes. J. Liposome Res. 12(1-2), 107-119 (2002).
114. Ishii M, Kojima N. Mucosal adjuvant activity of oligomannose-coated liposomes for nasal immunization. Glycoconj. J. 27(1), 115-123 (2010).
115. Wijagkanalan W, Kawakami S, Takenaga M, Igarashi R, Yamashita F, Hashida M. Targeted delivery of oligomannose-coated liposome to the omental micrometastasis by peritoneal macrophages from patients with gastric cancer. Cancer Sci. 101(7), 1670-1677 (2010).
116. Wijagkanalan W et al. Efficient targeting to alveolar macrophages by intratracheal administration of mannosylated liposomes in rats. J. Control. Release 125(2), 121-130 (2008).
117. Jain S, Mishra V, Singh P, Dubey PK, Saraf DK, Vyas SP. RGD-anchored magnetic liposomes for monocytes/neutrophils-mediated brain targeting. Int. J. Pharm. 261(1-2), 43-55 (2003).
118. Wijagkanalan W, Higuchi Y, Kawakami S, Teshima M, Sasaki H, Hashida M. Enhanced anti-inflammation of inhaled dexamethasone palmitate using mannosylated liposomes in an endotoxin-induced lung inflammation model. Mol. Pharmacol. 74(5), 1183-1192 (2008).
119. Kuramoto Y, Kawakami S, Zhou S. Use of mannosylated cationic liposomes/immunostimulatory CpG DNA complex for effective inhibition of peritoneal dissemination in mice. J. Gene Med. 10(4), 392-399 (2008).
120. Un K, Kawakami S, Suzuki R. Enhanced transfection efficiency into macrophages and dendritic cells by a combination method using mannosylated lipoplexes and bubble liposomes with ultrasound exposure. Hum. Gene Ther. 21(1), 65-74 (2010).
121. Mundargi RC, Babu VR, Rangaswamy V, Patel P, Aminabhavi TM. Nano/micro technologies for delivering macromolecular therapeutics using poly(d, l-lactide-co-glycolide) and its derivatives. J. Control. Release 125(3), 193-209 (2008).
122. Lawlor C, O'Sullivan MP, Sivadas N et al. The application of high-content analysis in the study of targeted particulate delivery systems for intracellular drug delivery to alveolar macrophages. Mol. Pharm. 8(4), 1100-1112 (2011).
123. Nguyen J, Steele TW, Merkel O, Reul R, Kissel T. Fast degrading polyesters as siRNA nano-carriers for pulmonary gene therapy. J. Control. Release 132(3), 243-251 (2008).
124. Mountziaris PM, Sing DC, Chew SA et al. Controlled release of anti-inflammatory siRNA from biodegradable polymeric microparticles intended for intra-articular delivery to the temporomandibular joint. Pharm. Res. 28(6) 1370-1384 (2011).
125. Lam JK, Liang W, Chan HK. Pulmonary delivery of therapeutic siRNA. Adv. Drug Deliv. Rev. 64(1), 1-15 (2012).
126. Gutbier B, Kube SM, Reppe K et al. RNAi-mediated suppression of constitutive pulmonary gene expression by small interfering RNA in mice. Pulm. Pharmacol. Therap. 23(4), 334-344 (2010).
127. Kim TH, Kim SH, Seo JY et al. Blockade of the Wnt/B-catenin pathway attenuates bleomycin-induced pulmonary fibrosis. Tohoku J. Exp. Med. 223(1), 45-54 (2011).
128. Rosas-Taraco AG, Higgins DM, Sánchez-Campillo J, Lee EJ, Orme IM, González-Juarrero M. Intrapulmonary delivery of XCL1-targeting small interfering RNA in mice chronically infected with Mycobacterium tuberculosis. Am. J. Respir. Cell Mol. Biol. 41(2), 136-145 (2009).
129. Perl M, Chung CS, Lomas-Neira J et al. Silencing of Fas, but not caspase-8, in lung epithelial cells ameliorates pulmonary apoptosis, inflammation, and neutrophil influx after hemorrhagic shock and sepsis. Am. J. Pathol. 167(6), 1545-1559 (2005).
130. Quesada Calvo F, Fillet M, Renaut J et al. Potential therapeutic target discovery by 2D-DIGE proteomic analysis in mouse models of asthma. J. Proteome Res. 10(9), 4291-4301 (2011).
131. Wang JC, Lai S, Guo X et al. Attenuation of fibrosis in vitro and in vivo with SPARC siRNA. Arthritis Res. Ther. 12(2), R60 (2010).
132. Dong M, Mürdter TE, Philippi C et al. Pulmonary delivery and tissue distribution of aerosolized antisense 2́-O-methyl RNA containing nanoplexes in the isolated perfused and ventilated rat lung. Eur. J. Pharm. Biopharmaceutics 81(3), 478-485 (2012).
133. Nielsen EJ, Nielsen JM, Becker D et al. Pulmonary gene silencing in transgenic EGFP mice using aerosolised chitosan/siRNA nanoparticles. Pharm. Res. 27(12), 2520-2527 (2010).