Dendrimer nanocarriers for transport modulation across models of the pulmonary epithelium

Molecular Pharmaceutics

Volumn 12, Issue 3, 2015, Pages 826-838

  Bharatwaj, Balaji ^a   Mohammad, Abdul Khader ^b   Dimovski, Radovan ^a   Cassio, Fernando L ^c   Bazito, Reinaldo C ^c   Conti, Denise ^a   Fu, Qiang ^b   Reineke, Joshua ^b   Da Rocha, Sandro R P ^a  

^a Wayne State University   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Calu 3; in vitro transport; in vivo pharmacokinetics; modulation; PEGylation; poly(amido amine) dendrimers; respiratory drug delivery

Indexed keywords

ALCIAN BLUE; DENDRIMER; FLUORESCEIN ISOTHIOCYANATE; FLUORESCENT DYE; NANOCARRIER; POLYAMIDOAMINE; PROTEIN ZO1; DRUG CARRIER; MACROGOL DERIVATIVE; NANOMATERIAL; PAMAM STARBURST;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; CELL LYSATE; CELL SURFACE; CELL VIABILITY; CIRCULATION TIME; CYTOTOXICITY; DRUG ABSORPTION; DRUG BIOAVAILABILITY; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG HALF LIFE; DRUG SYNTHESIS; ELIMINATION RATE CONSTANT; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYDRODYNAMICS; HYDROPHILICITY; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; KIDNEY CLEARANCE; LIGHT SCATTERING; LIMIT OF DETECTION; LUNG ALVEOLUS EPITHELIUM; MALE; MAXIMUM PLASMA CONCENTRATION; MICROVILLUS; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; ONE POT SYNTHESIS; OPSONIZATION; PHARMACOKINETIC ASSAY; PLASMA CLEARANCE; PLASMA CONCENTRATION-TIME CURVE; POLARIZATION; PORE SIZE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCANNING ELECTRON MICROSCOPY; SURFACE CHARGE; SURFACE PROPERTY; TIGHT JUNCTION; ZETA POTENTIAL; ACTIVE TRANSPORT; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; LUNG; METABOLISM; PHARMACEUTICS; RESPIRATORY MUCOSA;

ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; BIOPHARMACEUTICS; CELL LINE; DENDRIMERS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; HUMANS; LUNG; MALE; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; NANOSTRUCTURES; POLYETHYLENE GLYCOLS; RESPIRATORY MUCOSA; SURFACE PROPERTIES;

EID: 84923931083     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp500662z     Document Type: Article

References (70)

1. Cipolla, D. C.; Gonda, I. Formulation technology to repurpose drugs for inhalation delivery Drug Discovery Today 2011, 8, 123-130
2. Patton, J. S.; Byron, P. R. Inhaling medicines: delivering drugs to the body through lungs Nat. Rev. Drug Discovery 2007, 6, 67-74
3. Aurora, S. K.; Silberstein, S. D.; Kori, S. H.; Tepper, S. J.; Borland, S. W.; Wang, M.; Dodick, D. W. MAP0004, orally inhaled DHE: a randomized, controlled study in the acute treatment of migraine Headache 2011, 51 (4) 507-17
4. Dolovich, M. B.; Dhand, R. Aerosol drug delivery: developments in device design and clinical use Lancet 2011, 377 (9770) 1032-45
5. Merkel, O. M.; Kissel, T. Nonviral pulmonary delivery of siRNA Acc. Chem. Res. 2011, 10.1021/ar200110p
6. Agu, R. U. In vitro and in vivo testing methods for respiratory drug delivery Expert Opin. Drug Delivery 2011, 8 (1) 57-69
7. Azarmi, S.; Roa, W. H.; Lobenberg, R. Targeted delivery of nanoparticles for the treatment of lung diseases Adv. Drug Delivery Rev. 2008, 60, 863-875
8. Inapagolla, R.; Guru, B. R.; Kurtoglu, Y. E.; Gao, X.; Lieh-Lai, M.; Bassett, D. J.; Kannan, R. M. In vivo efficacy of dendrimer-methylprednisolone conjugate formulation for the treatment of lung inflammation Int. J. Pharm. 2010, 399 (1-2) 140-7
9. Menjoge, A. R.; Kannan, R. M.; Tomalia, D. A. Dendrimer-based drug and imaging conjugates: design considerations for nanomedical applications Drug Discovery Today 2010, 15 (5-6) 171-85
10. Misra, A.; Hickey, A. J.; Rossi, C.; Borchard, G.; Terada, H.; Makino, K.; Fourie, P. B.; Colombo, P. Inhaled drug therapy for treatment of tuberculosis Tuberculosis 2011, 91 (1) 71-81
11. Roy, I.; Vij, N. Nanodelivery in airway diseases: challenges and therapeutic applications Nanomed. Nanotechnol. 2010, 6 (2) 237-44
12. Rytting, E.; Nguyen, J.; Wang, X.; Kissel, T. Biodegradable polymeric nanocarriers for pulmonary drug delivery Expert Opin Drug Delivery 2008, 5, 629-639
13. Davis, M. E.; Chen, Z.; Shin, D. M. Nanoparticle therapeutics: an emerging treatment modality for cancer Nat. Rev. Drug Discovery 2008, 7, 771-782
14. Lai, S. K.; Wang, Y. Y.; Hanes, J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues Adv. Drug Delivery Rev. 2009, 61 (2) 158-71
15. Pison, U.; Welte, T.; Giersig, M.; Groneberg, D. A. Nanomedicine for respiratory diseases Eur. J. Pharmacol. 2006, 533, 341-350
16. Svenson, S. Dendrimers as versatile platform in drug delivery applications Eur. J. Pharm. Biopharm. 2009, 71 (3) 445-62
17. D'Emanuele, A.; Attwood, D. Dendrimer-drug interactions Adv. Drug Delivery Rev. 2005, 57 (15) 2147-62
18. Sadekar, S.; Ghandehari, H. Transepithelial transport and toxicity of PAMAM dendrimers: Implications for oral drug delivery Adv. Drug Delivery Rev. 2011, 64, 571-588
19. Grainger, C. I.; Greenwell, L. L.; Lockley, D. J.; Martin, G. P.; Forbes, B. Culture of Calu-3 cells at the air interface provides a representative model of the airway epithelial barrier Pharm. Res. 2006, 23 (7) 1482-90
20. Zhang, X. Q.; Intra, J.; Salem, A. K. Conjugation of polyamidoamine dendrimers on biodegradable microparticles for nonviral gene delivery Bioconjugate Chem. 2007, 18 (6) 2068-76
21. Guillaudeu, S. J.; Fox, M. E.; Haidar, Y. M.; Dy, E. E.; Szoka, F. C.; Frechet, J. M. PEGylated dendrimers with core functionality for biological applications Bioconjugate Chem. 2008, 19 (2) 461-9
22. Jain, N. K.; Nahar, M. PEGylated Nanocarriers for Systemic Delivery. In Cancer Nanotechnology: Methods in Molecular Biology; Springer: New York, 2009; Vol. 624, pp 221-234.
23. Perumal, O. P.; Inapagolla, R.; Kannan, S.; Kannan, R. M. The effect of surface functionality on cellular trafficking of dendrimers Biomaterials 2008, 29 (24-25) 3469-76
24. ueous Non-Radioactive Cell Proliferation Assay; Promega: Madison, WI, 2009.
25. Probes, M. ZO-1, Mouse Monoclonal Antibody-Alexa Fluor 546; Invitrogen: Grand Island, NY, 2010.
26. Biotechnology, P. Pierce BCA Protein Assay; Thermo Scientific: Rockford, IL, 2011.
27. 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. 2007, 20 (6) 708-717
28. Sanders, N.; Rudolph, C.; Braeckmans, K.; De Smedt, S. C.; Demeester, J. Extracellular barriers in respiratory gene therapy Adv. Drug Delivery Rev. 2009, 61 (2) 115-127
29. Bhat, P. G.; Flanagan, D. R.; Donovan, M. D. Drug diffusion through cystic fibrotic mucus: Steady-state permeation, rheologic properties, and glycoprotein morphology J. Pharm. Sci. 1996, 85 (6) 624-630
30. Sanders, N. N.; Van Rompaey, E.; De Smedt, S. C.; Demeester, J. Structural alterations of gene complexes by cystic fibrosis sputum Am. J. Respir. Crit. Care Med. 2001, 164 (3) 486-493
31. Sarlo, K.; Blackburn, K. L.; Clark, E. D.; Grothaus, J.; Chaney, J.; Neu, S.; Flood, J.; Abbott, D.; Bohne, C.; Casey, K.; Fryer, C.; Kuhn, M. Tissue distribution of 20 nm, 100 and 1000 nm fluorescent polystyrene latex nanospheres following acute systemic or acute and repeat airway exposure in the rat Toxicology 2009, 263 (2-3) 117-26
32. Gajbhiye, A.; Kumar, V. P.; Tekade, R. K.; Jain, N. K. Pharmaceutical and biomedical potential of PEGylated dendrimers Curr. Pharm. Des. 2007, 13, 415-429
33. Kaminskas, L. M.; Boyd, B. J.; Karellas, P.; Krippner, G. Y.; Lessene, R.; Kelly, B.; Porter, C. J. The impact of molecular weight and PEG chain length on the systemic pharmacokinetics of PEGylated poly l -lysine dendrimers Mol. Pharmaceutics 2008, 5 (3) 449-63
34. Kim, Y.; Klutz, A. M.; Jacobson, K. A. Systematic investigation of polyamidoamine dendrimers surface-modified with poly(ethylene glycol) for drug delivery applications: synthesis, characterization, and evaluation of cytotoxicity Bioconjugate Chem. 2008, 19 (8) 1660-72
35. Kim, Y.; Hechler, B.; Klutz, A. M.; Gachet, C.; Jacobson, K. A. Toward multivalent signaling across G protein-coupled receptors from poly(amidoamine) dendrimers Bioconjugate Chem. 2008, 19 (2) 406-11
36. Jevprasesphant, R.; Penny, J.; Attwood, D.; McKeown, N. B.; D'Emanuele, A. Engineering of dendrimer surfaces to enhance transepithelial transport and reduce cytotoxicity Pharm. Res. 2003, 20 (10) 1543-50
37. Sweet, D. M.; Kolhatkar, R. B.; Ray, A.; Swaan, P.; Ghandehari, H. Transepithelial transport of PEGylated anionic poly(amidoamine) dendrimers: implications for oral drug delivery J. Controlled Release 2009, 138 (1) 78-85
38. Zhu, S.; Hong, M.; Tang, G.; Qian, L.; Lin, J.; Jiang, Y.; Pei, Y. Partly PEGylated polyamidoamine dendrimer for tumor-selective targeting of doxorubicin: the effects of PEGylation degree and drug conjugation style Biomaterials 2010, 31 (6) 1360-71
39. He, H.; Li, Y.; Jia, X.-R.; Du, J.; Ying, X.; Lu, W.-L.; Lou, J.-N.; Wei, Y. PEGylated poly(amidoamine) dendrimer-based dual-targeting carrier for treating brain tumors Biomaterials 2010, 32, 478-487
40. Kannan, S.; Kolhe, P.; Raykova, V.; Glibatec, M.; Kannan, R. M.; Lieh-Lai, M.; Bassett, D. Dynamics of cellular entry and drug delivery by dendritic polymers into human lung epithelial carcinoma cells J. Biomate.r Sci. Polym. Ed. 2004, 15, 311-330
41. Kitchens, K. M.; Ghandehari, H. PAMAM Dendrimers as Nanoscale Oral Drug Delivery Systems. In Nanotechnology in Drug Delivery; de Villiers, M. M.; Aramwit, P.; Kwon, G. S., Eds.; Springer Science: New York, 2009; Vol. X, pp 423-459.
42. Saovapakhiran, A.; D'Emanuele, A.; Attwood, D.; Penny, J. Surface modification of PAMAM dendrimers modulates the mechanism of cellular internalization Bioconjugate Chem. 2009, 20 (4) 693-701
43. Mathias, N. R.; Timoszyk, J.; Stetsko, P. I.; Megill, J. R.; Smith, R. L.; Wall, D. A. Permeability characteristics of Calu-3 human bronchial epithelial cells: in vitro-in vivo correlation to predict lung absorption in rats J. Drug Target. 2002, 10, 31-40
44. Linnankoski, J.; Makela, J.; Palmgren, J.; Mauriala, T.; Vedin, C.; Ungell, A. L.; Lazorova, L.; Artursson, P.; Urtti, A.; Yliperttula, M. Paracellular porosity and pore size of the human intestinal epithelium in tissue and cell culture models J. Pharm. Sci. 2010, 99 (4) 2166-75
45. Tajarobi, F.; El-Sayed, M.; Rege, B. D.; Polli, J. E.; Ghandehari, H. Transport of poly amidoamine dendrimers across Madin-Darby canine kidney cells Int. J. Pharm. 2001, 215 (1-2) 263-7
46. Buckley, S. T.; Kim, K.-J.; Ehrhardt, C. In Vitro Cell Culture Models for Evaluating Controlled Release Pulmonary Drug Delivery. In Controlled Pulmonary Drug Delivery; Smyth, H. D. C.; Hickey, A. J., Eds.; Springer: New York, 2011; pp 417-442.
47. Jain, K.; Kesharwani, P.; Gupta, U.; Jain, N. K. Dendrimer toxicity: let's meet the challenge Int. J. Pharm. 2010, 394, 122-142
48. Wang, W.; Xiong, W.; Wan, J.; Xu, H.; Yang, X. The decrease of PAMAM dendrimer-induced cytotoxicity by PEGylation via attenuation of oxidative stress Nanotechnology 2009, 20, 105-113
49. Qi, R.; Y, G.; Tang, Y.; He, R.-R.; Liu, T.-L.; He, Y.; Sun, S.; Li, B.-Y.; Li, Y.-B.; Liu, G. PEG-conjugated PAMAM dendrimers mediate efficient intramuscular gene expression AAPS J. 2009, 11, 395-405
50. Forbes, B.; Ehrhardt, C. Human respiratory epithelial cell culture for drug delivery applications Eur. J. Pharm. Biopharm. 2005, 60 (2) 193-205
51. Haghi, M.; Young, P. M.; Traini, D.; Jaiswal, R.; Gong, J.; Bebawy, M. Time- and passage- dependent characteristics of a Calu-3 respiratory cell model Drug Dev. Ind. Pharm. 2010, 36, 1207-1214
52. Vllasaliu, D.; Fowler, R.; Garnett, M.; Eaton, M.; Stolnik, S. Barrier characteristics of epithelial cultures modelling the airway and intestinal mucosa: a comparison Biochem. Biophys. Res. Commun. 2011, 415 (4) 579-85
53. Ong, H. X.; Traini, D.; Bebawy, M.; Young, P. M. Ciprofloxacin is actively transported across bronchial lung epithelial cells using a Calu-3 air interface cell model Antimicrob. Agents Chemother. 2013, 57 (6) 2535-40
54. Bi, X.; Shi, X.; Baker, J. R., Jr. Synthesis, characterization and stability of a luteinizing hormone-releasing hormone (LHRH)-functionalized poly(amidoamine) dendrimer conjugate J. Biomater. Sci. Polym. Ed. 2008, 19 (1) 131-42
55. Jevprasesphant, R.; Penny, J.; Attwood, D.; D'Emanuele, A. Transport of dendrimer nanocarriers through epithelial cells via the transcellular route J. Controlled Release 2004, 97 (2) 259-67
56. Navath, R. S.; Wang, B.; Kannan, S.; Romero, R.; Kannan, R. M. Stimuli-responsive star poly(ethylene glycol) drug conjugates for improved intracellular delivery of the drug in neuroinflammation J. Controlled Release 2010, 142 (3) 447-56
57. Yellepeddi, V. K.; Kumar, A.; Palakurthi, S. Biotinylated poly(amido)amine (PAMAM) dendrimers as carriers for drug delivery to ovarian cancer cells in vitro Anticancer Res. 2009, 29 (8) 2933-43
58. Mitragotri, S.; Lahann, J. Materials for drug delivery: innovative solutions to address complex biological hurdles Adv. Mater. 2012, 24 (28) 3717-3723
59. Kitchens, K. M.; Kolhatkar, R. B.; Swaan, P. W.; Eddington, N. D.; Ghandehari, H. Transport of poly(amidoamine) dendrimers across Caco-2 cell monolayers: Influence of size, charge and fluorescent labeling Pharm. Res. 2006, 23 (12) 2818-26
60. Pisal, D. S.; Yellepeddi, V. K.; Kumar, A.; Palakurthi, S. Transport of surface engineered polyamidoamine (PAMAM) dendrimers across IPEC-J2 cell monolayers Drug Delivery 2008, 15 (8) 515-22
61. Pisal, D. S.; Yellepeddi, V. K.; Kumar, A.; Kaushik, R. S.; Hildreth, M. B.; Guan, X.; Palakurthi, S. Permeability of surface-modified polyamidoamine (PAMAM) dendrimers across Caco-2 cell monolayers Int. J. Pharm. 2008, 350 (1-2) 113-21
62. Anderson, J. M. Molecular structure of tight junctions and their role in epithelial transport Physiology 2001, 16, 126-130
63. Casettari, L.; Vllasaliu, D.; Mantovani, G.; Howdle, S. M.; Stolnik, S.; Illum, L. Effect of PEGylation on the toxicity and permeability enhancement of chitosan Biomacromolecules 2010, 11, 2854-2865
64. Lai, S. K.; O'Hanlon, D. E.; Harrold, S.; Man, S. T.; Wang, Y. Y.; Cone, R.; Hanes, J. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (5) 1482-7
65. Wang, Y. Y.; Lai, S. K.; Suk, J. S.; Pace, A.; Cone, R.; Hanes, J. Addressing the PEG mucoadhesivity paradox to engineer nanoparticles that "slip" through the human mucus barrier Angew. Chem., Int. Ed. 2008, 47 (50) 9726-9
66. Bucior, I.; Mostov, K.; Engel, J. N. Pseudomonas aeruginosa -mediated damage requires distinct receptors at the apical and basolateral surfaces of the polarized epithelium Infect. Immun. 2010, 78 (3) 939-53
67. Goldberg, D. S.; Ghandehari, H.; Swaan, P. W. Cellular entry of G3.5 poly (amido amine) dendrimers by clathrin- and dynamin-dependent endocytosis promotes tight junctional opening in intestinal epithelia Pharm. Res. 2010, 27 (8) 1547-57
68. Plotkowski, M. C.; Costa, A. O.; Morandi, V.; Barbosa, H. S.; Nader, H. B.; de Bentzmann, S.; Puchelle, E. Role of heparan sulphate proteoglycans as potential receptors for non-piliated Pseudomonas aeruginosa adherence to non-polarised airway epithelial cells J. Med. Microbiol. 2001, 50 (2) 183-90
69. Longmire, M.; Choyke, P. L.; Kobayashi, H. Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats Nanomedicine 2008, 3 (5) 703-17
70. Ryan, G. M.; Kaminskas, L. M.; Kelly, B. D.; Owen, D. J.; McIntosh, M. P.; Porter, C. J. Pulmonary administration of PEGylated polylysine dendrimers: absorption from the lung versus retention within the lung is highly size-dependent Mol. Pharmaceutics 2013, 10 (8) 2986-95