Nanoparticle surface charge impacts distribution, uptake and lymph node trafficking by pulmonary antigen-presenting cells

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 12, Issue 3, 2016, Pages 677-687

  Fromen, Catherine A ^a   Rahhal, Tojan B ^b   Robbins, Gregory R ^c,d   Kai, Marc P ^a   Shen, Tammy W ^b   Luft, J Christopher ^b,d   DeSimone, Joseph M ^a,b,d,e  

^a North Carolina State University   (United States)

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

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

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

Author keywords

Dendritic cell; Lung; Nanoparticle; Pulmonary drug delivery; Vaccine

Indexed keywords

BIOLOGICAL ORGANS; BODY FLUIDS; CELLS; VACCINES;

ANTIGEN PRESENTING CELLS; CATIONIC NANOPARTICLES; CHARGED NANOPARTICLES; DENDRITIC CELLS; ENGINEERED NANOPARTICLES; LUNG; NANOPARTICLE SURFACE CHARGE; PULMONARY DRUG DELIVERY;

NANOPARTICLES;

CD103 ANTIGEN; CD11B ANTIGEN; DRUG CARRIER; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NANOPARTICLE; TUMOR NECROSIS FACTOR ALPHA; VACCINE; ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG FORMULATION; DRUG TRANSPORT; DRUG UPTAKE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNE RESPONSE; INTERNALIZATION; LUNG ALVEOLUS MACROPHAGE; MEDIASTINUM LYMPH NODE; MOUSE; NONHUMAN; PULMONARY ANTIGEN PRESENTING CELL; SURFACE CHARGE; UPREGULATION; ANIMAL; C57BL MOUSE; CHEMISTRY; HUMAN; LUNG; LYMPH NODE; METABOLISM; SURFACE PROPERTY;

ANIMALS; DENDRITIC CELLS; DRUG CARRIERS; FEMALE; HUMANS; IONS; LUNG; LYMPH NODES; MACROPHAGES, ALVEOLAR; MICE, INBRED C57BL; NANOPARTICLES; SURFACE PROPERTIES; VACCINES;

EID: 84959419429     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2015.11.002     Document Type: Article

References (48)

1. Garcia A., Mack P., Williams S., Fromen C., Shen T., Tully J., et al. Microfabricated engineered particle systems for respiratory drug delivery and other pharmaceutical applications. J Drug Deliv 2012, 2012:941243. 10.1155/2012/941243.
2. Blank F., Stumbles P., von Garnier C. Opportunities and challenges of the pulmonary route for vaccination. Expert Opin Drug Deliv 2011, 8:547-563.
3. Moon J.J., Huang B., Irvine D.J. Engineering nano- and microparticles to tune immunity. Adv Mater 2012, 24:3724-3746.
4. Li A.V., Moon J.J., Abraham W., Suh H., Elkhader J., Seidman M.A., et al. Generation of effector memory T cell-based mucosal and systemic immunity with pulmonary nanoparticle vaccination. Sci Transl Med 2013, 5:204ra130. 10.1126/scitranslmed.3006516.
5. Nembrini C., Stano A., Dane K.Y., Ballester M., van der Vlies A.J., Marsland B.J., et al. Nanoparticle conjugation of antigen enhances cytotoxic T-cell responses in pulmonary vaccination. Proc Natl Acad Sci U S A 2011, 108:E989-E997.
6. Smith D.M., Simon J.K., Baker J.R. Applications of nanotechnology for immunology. Nat Rev Immunol 2013, 13:592-605.
7. Pulliam B., Sung J.C., Edwards D.A. Design of nanoparticle-based dry powder pulmonary vaccines. Expert Opin Drug Deliv 2007, 4:651-663.
8. Fromen C.A., Robbins G.R., Shen T.W., Kai M.P., Ting J.P.Y., DeSimone J.M. Controlled analysis of nanoparticle charge on mucosal and systemic antibody responses following pulmonary immunization. Proc Natl Acad Sci 2014, 10.1073/pnas.1422923112.
9. Fromen C.A., Shen T.W., Larus A.E., Mack P., Maynor B.W., Luft J.C., et al. Synthesis and characterization of monodisperse uniformly shaped respirable aerosols. AIChE J 2013, 59:3184-3194.
10. Kunda N.K., Somavarapu S., Gordon S.B., Hutcheon G.A., Saleem I.Y. Nanocarriers targeting dendritic cells for pulmonary vaccine delivery. Pharm Res 2013, 30:325-341.
11. Sakagami M. In vivo, in vitro and ex vivo models to assess pulmonary absorption and disposition of inhaled therapeutics for systemic delivery. Adv Drug Deliv Rev 2006, 58:1030-1060.
12. Guilliams M., Lambrecht B.N., Hammad H. Division of labor between lung dendritic cells and macrophages in the defense against pulmonary infections. Mucosal Immunol 2013, 6:464-473.
13. Azarmi S., Roa W.H., Lobenberg R. Targeted delivery of nanoparticles for the treatment of lung diseases. Adv Drug Deliv Rev 2008, 60:863-875.
14. Hassan M.S., Lau R.W. Effect of particle shape on dry particle inhalation: Study of flowability, aerosolization, and deposition properties. AAPS PharmSciTech 2009, 10:1252-1262.
15. Kleinstreuer C., Zhang Z., Li Z., Roberts W.L., Rojas C. A new methodology for targeting drug-aerosols in the human respiratory system. Int J Heat Mass Transf 2008, 51:5578-5589.
16. Hardy C.L., Lemasurier J.S., Mohamud R., Yao J., Xiang S.D., Rolland J.M., et al. Differential uptake of nanoparticles and microparticles by pulmonary APC subsets induces discrete immunological imprints. J Immunol 2013, 191:5278-5290.
17. Fernandes C.A., Vanbever R. Preclinical models for pulmonary drug delivery. Expert Opin Drug Deliv 2009, 6:1231-1245.
18. Thiel C.G. Can in vitro particle size measurements be used to predict pulmonary deposition of aerosol from inhalers?. J Aerosol Med 1998, 11:S43-S52.
19. Inaba K., Steinman R.M., Van Voorhis W.C., Muramatsu S. Dendritic cells are critical accessory cells for thymus-dependent antibody responses in mouse and in man. Proc Natl Acad Sci U S A 1983, 80:6041-6045.
20. Naito T., Suda T., Suzuki K., Nakamura Y., Inui N., Sato J., et al. Lung dendritic cells have a potent capability to induce production of immunoglobulin a. Am J Respir Cell Mol Biol 2008, 38:161-167.
21. Xie Y., Zeng P., Wiedmann T.S. Disease guided optimization of the respiratory delivery of microparticulate formulations. Expert Opin Drug Deliv 2008, 5:269-289.
22. Abdelwahed W., Degobert G., Stainmesse S., Fessi H. Freeze-drying of nanoparticles: Formulation, process and storage considerations. Adv Drug Deliv Rev 2006, 58:1688-1713.
23. Furuhashi K., Suda T., Hasegawa H., Suzuki Y., Hashimoto D., Enomoto N., et al. Mouse lung Cd103+ and Cd11b high dendritic cells preferentially induce distinct Cd4+ T-cell responses. Am J Respir Cell Mol Biol 2012, 46:165-172.
24. Suzuki Y., Suda T., Furuhashi K., Shibata K., Hashimoto D., Enomto N., et al. Mouse Cd11b high lung dendritic cells have more potent capability to induce IgA than Cd103+ lung dendritic cells in vitro. Am J Respir Cell Mol Biol 2012, 46:773-780.
25. Zhao L., Seth A., Wibowo N., Zhao C.X., Mitter N., Yu C., et al. Nanoparticle vaccines. Vaccine 2014, 32:327-337.
26. Michen B., Graule T. Isoelectric points of viruses. J Appl Microbiol 2010, 109:388-397.
27. van der Mei H.C., Busscher H.J. Bacterial cell surface heterogeneity: A pathogen's disguise. PLoS Pathog 2012, 10.1371/journal.ppat.1002821.
28. Perry J.L., Reuter K.G., Kai M.P., Herlihy K.P., Jones S.W., Luft J.C., et al. Pegylated print nanoparticles: The impact of peg density on protein binding, macrophage association, biodistribution, and pharmacokinetics. Nano Lett 2012, 12:5304-5310.
29. Shen T.W., Fromen C.A., Kai M.P., Luft J.C., Rahhal T.B., Robbins G.R., et al. Distribution and cellular uptake of pegylated polymeric particles in the lung towards cell-specific targeted delivery. Pharm Res 2015, 32:3248-3260.
30. Robbins G.R., Truax A.D., Davis B.K., Zhang L., Brickey W.J., Ting J.P. Regulation of class i major histocompatibility complex (MHC) by nucleotide-binding domain, leucine-rich repeat-containing (NLR) proteins. J Biol Chem 2012, 287:24294-24303.
31. Mitchell J.P., Nagel M.W. Cascade impactors for the size characterization of aerosols from medical inhalers. J Aerosol Med 2003, 16:341-377.
32. Roberts R.A., Shen T., Allen I.C., Hasan W., DeSimone J.M., Ting J.P. Analysis of the murine immune response to pulmonary delivery of precisely fabricated nano- and microscale particles. PLoS One 2013, 8:e62115. 10.1371/journal.pone.0062115.
33. Johnston C.J., Finkelstein J.N., Gelein R., Oberdorster G. Pulmonary cytokine and chemokine mRNA levels after inhalation of lipopolysaccharide in C57bl/6 mice. Toxicol Sci 1998, 46:300-307.
34. Pesce I., Monaci E., Muzzi A., Tritto E., Tavarini S., Nuti S., et al. Intranasal administration of CpG induces a rapid and transient cytokine response followed by dendritic and natural killer cell activation and recruitment in the mouse lung. J Innate Immun 2010, 2:144-159.
35. Rose C.E., Sung S.S., Fu S.M. Significant involvement of Ccl2 (Mcp-1) in inflammatory disorders of the lung. Microcirculation 2003, 10:273-288.
36. Deshmane S.L., Kremlev S., Amini S., Sawaya B.E. Monocyte chemoattractant protein-1 (Mcp-1): An overview. J Interferon Cytokine Res 2009, 29:313-326.
37. Larhrib H., Martin G.P., Marriott C., Prime D. The influence of carrier and drug morphology on drug delivery from dry powder formulations. Int J Pharm 2003, 257:283-296.
38. Dong S., Zhang X., He Y., Xu F., Li D., Xu W., et al. Synergy of Il-27 and Tnf-alpha in regulating Cxcl10 expression in lung fibroblasts. Am J Respir Cell Mol Biol 2013, 48:518-530.
39. Cook D.N., Bottomly K. Innate immune control of pulmonary dendritic cell trafficking. Proc Am Thorac Soc 2007, 4:234-239.
40. Smarr C.B., Hsu C.L., Byrne A.J., Miller S.D., Bryce P.J. Antigen-fixed leukocytes tolerize Th2 responses in mouse models of allergy. J Immunol 2011, 187:5090-5098.
41. Choi H.S., Ashitate Y., Lee J.H., Kim S.H., Matsui A., Insin N., et al. Rapid translocation of nanoparticles from the lung airspaces to the body. Nat Biotechnol 2010, 28:1300-1303.
42. Pal I., Ramsey J.D. The role of the lymphatic system in vaccine trafficking and immune response. Adv Drug Deliv Rev 2011, 63:909-922.
43. Blank F., Stumbles P.A., Seydoux E., Holt P.G., Fink A., Rothen-Rutishauser B., et al. Size-dependent uptake of particles by pulmonary antigen-presenting cell populations and trafficking to regional lymph nodes. Am J Respir Cell Mol Biol 2013, 49:67-77.
44. Mueller S.N., Tian S., DeSimone J.M. Rapid and persistent delivery of antigen by lymph node targeting print nanoparticle vaccine carrier to promote humoral immunity. Mol Pharm 2015, 12:1356-1365.
45. Tonnis W.F., Kersten G.F., Frijlink H.W., Hinrichs W.L.J., de Boer A.H., Amorij J. Pulmonary vaccine delivery: A realistic approach?. J Aerosol Med Pulm Drug Deliv 2012, 25:249-260.
46. Sou T., Meeusen E.N., de Veer M., Morton D.A., Kaminskas L.M., McIntosh M.P. New developments in dry powder pulmonary vaccine delivery. Trends Biotechnol 2011, 29:191-198.
47. Neutra M.R., Kozlowski P.A. Mucosal vaccines: The promise and the challenge. Nat Rev Immunol 2006, 6:148-158.
48. Galloway A.L., Murphy A., DeSimone J.M., Di J., Herrmann J.P., Hunter M.E., et al. Development of a nanoparticle-based influenza vaccine using the print technology. Nanomedicine 2013, 9:523-531.