Skin dendritic cell targeting via microneedle arrays laden with antigen-encapsulated poly- D, l -Lactide- Co -Glycolide nanoparticles induces efficient antitumor and antiviral immune responses

ACS Nano

Volumn 7, Issue 3, 2013, Pages 2042-2055

  Zaric, Marija ^a   Lyubomska, Oksana ^a   Touzelet, Olivier ^a   Poux, Candice ^a   Al Zahrani, Sharifah ^b   Fay, Francois ^b   Wallace, Leah ^a   Terhorst, Dorothea ^c,d   Malissen, Bernard ^c,d   Henri, Sandrine ^c,d   Power, Ultan F ^a   Scott, Christopher J ^b   Donnelly, Ryan F ^b   Kissenpfennig, Adrien ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d INSERM   (France)

Author keywords

dissolvable microneedles; immunotherapy; PLGA nanoparticles; skin dendritic cells; vaccines

Indexed keywords

ANTIGEN PRESENTING CELLS; BIODEGRADABLE POLYMERIC NANOPARTICLES; DENDRITIC CELLS; DENDRITIC CELLS (DCS); IMMUNOTHERAPY; MICRONEEDLE ARRAYS; MICRONEEDLES; PLGA NANOPARTICLES;

CELLS; IMMUNE SYSTEM; NANOPARTICLES; NEEDLES; VACCINES; VIRUSES;

ANTIGENS;

ANTIGEN; ANTIMICROBIAL CATIONIC PEPTIDE; NANOCAPSULE; OVALBUMIN; PEPTIDE GLY LEU AMIDE; PEPTIDE-GLY-LEU-AMIDE; VACCINE;

ADAPTIVE IMMUNITY; ANIMAL; ARTICLE; CHEMISTRY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG DELIVERY SYSTEM; EXPERIMENTAL MELANOMA; FEMALE; IMMUNOLOGY; INTRADERMAL DRUG ADMINISTRATION; MALE; MOUSE; NANOTECHNOLOGY; NEEDLE; RESPIROVIRUS INFECTION; SENDAI VIRUS; SKIN; TRANSGENIC MOUSE;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS; ANTIMICROBIAL CATIONIC PEPTIDES; DENDRITIC CELLS; DRUG DELIVERY SYSTEMS; FEMALE; INJECTIONS, INTRADERMAL; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, TRANSGENIC; NANOCAPSULES; NANOTECHNOLOGY; NEEDLES; OVALBUMIN; RESPIROVIRUS INFECTIONS; SENDAI VIRUS; SKIN; T-LYMPHOCYTES, CYTOTOXIC; VACCINES;

EID: 84875674290     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn304235j     Document Type: Article

References (54)

1. Steinman, R. M. Lasker Basic Medical Research Award. Dendritic Cells: Versatile Controllers of the Immune System Nat. Med. 2007, 13, 1155-1159
2. Steinman, R. M. Dendritic Cells in Vivo: A Key Target for a New Vaccine Science Immunity 2008, 29, 319-324
3. Hegde, N. R.; Kaveri, S. V.; Bayry, J. Recent Advances in the Administration of Vaccines for Infectious Diseases: Microneedles as a Painless Delivery Devices for Mass Vaccination Drug Discovery Today 2011, 16, 1061-1068
4. Koutsonanos, D. G.; del Pilar Martin, M.; Zarnitsyn, V. G.; Sullivan, S. P.; Compans, R. W.; Prausnitz, M. R.; Skountzou, I. Transdermal Influenza Immunization with Vaccine-Coated Microneedle Arrays PLoS One 2009, 4, e4773
5. Miller, M. A.; Pisani, E. The Cost of Unsafe Injections Bull. World Health Org. 1999, 77, 808-811
6. Prausnitz, M. R.; Langer, R. Transdermal Drug Delivery Nat. Biotechnol. 2008, 26, 1261-1268
7. Combadiere, B.; Vogt, A.; Mahe, B.; Costagliola, D.; Hadam, S.; Bonduelle, O.; Sterry, W.; Staszewski, S.; Schaefer, H.; van der Werf, S. et al. Preferential Amplification of CD8 Effector-T Cells after Transcutaneous Application of an Inactivated Influenza Vaccine: A Randomized Phase I Trial PLoS One 2010, 5, e10818
8. Belshe, R. B.; Newman, F. K.; Cannon, J.; Duane, C.; Treanor, J.; Van Hoecke, C.; Howe, B. J.; Dubin, G. Serum Antibody Responses after Intradermal Vaccination Against Influenza N. Engl. J. Med. 2004, 351, 2286-2294
9. Kenney, R. T.; Frech, S. A.; Muenz, L. R.; Villar, C. P.; Glenn, G. M. Dose Sparing with Intradermal Injection of Influenza Vaccine N. Engl. J. Med. 2004, 351, 2295-2301
10. Prausnitz, M. R. Microneedles for Transdermal Drug Delivery Adv. Drug Delivery Rev. 2004, 56, 581-587
11. Al-Zahrani, S.; Zaric, M.; McCrudden, C.; Scott, C.; Kissenpfennig, A.; Donnelly, R. F. Microneedle-Mediated Vaccine Delivery: Harnessing Cutaneous Immunobiology To Improve Efficacy Expert Opin. Drug Delivery 2012, 9, 541-550
12. Kim, Y. C.; Park, J. H.; Prausnitz, M. R. Microneedles for Drug and Vaccine Delivery Adv. Drug Delivery Rev. 2012, 64, 1547-1568
13. Donnelly, R. F.; Majithiya, R.; Singh, T. R.; Morrow, D. I.; Garland, M. J.; Demir, Y. K.; Migalska, K.; Ryan, E.; Gillen, D.; Scott, C. J. et al. Design, Optimization and Characterisation of Polymeric Microneedle Arrays Prepared by a Novel Laser-Based Micromoulding Technique Pharm. Res. 2011, 28, 41-57
14. Storni, T.; Kundig, T. M.; Senti, G.; Johansen, P. Immunity in Response to Particulate Antigen-Delivery Systems Adv. Drug Delivery Rev. 2005, 57, 333-355
15. Gutierro, I.; Hernandez, R. M.; Igartua, M.; Gascon, A. R.; Pedraz, J. L. Size Dependent Immune Response after Subcutaneous, Oral and Intranasal Administration of BSA Loaded Nanospheres Vaccine 2002, 21, 67-77
16. Jaganathan, K. S.; Vyas, S. P. Strong Systemic and Mucosal Immune Responses to Surface-Modified PLGA Microspheres Containing Recombinant Hepatitis B Antigen Administered Intranasally Vaccine 2006, 24, 4201-4211
17. Mahapatro, A.; Singh, D. K. Biodegradable Nanoparticles Are Excellent Vehicle for Site Directed In Vivo Delivery of Drugs and Vaccines J. Nanobiotechnol. 2011, 9, 55
18. Panyam, J.; Labhasetwar, V. Biodegradable Nanoparticles for Drug and Gene Delivery to Cells and Tissue Adv. Drug Delivery Rev. 2003, 55, 329-347
19. Kumari, A.; Yadav, S. K.; Yadav, S. C. Biodegradable Polymeric Nanoparticles Based Drug Delivery Systems Colloids Surf., B 2010, 75, 1-18
20. Hunter, S. K.; Andracki, M. E.; Krieg, A. M. Biodegradable Microspheres Containing Group B Streptococcus Vaccine: Immune Response in Mice Am. J. Obstet. Gynecol. 2001, 185, 1174-1179
21. Alonso, M. J.; Gupta, R. K.; Min, C.; Siber, G. R.; Langer, R. Biodegradable Microspheres as Controlled-Release Tetanus Toxoid Delivery Systems Vaccine 1994, 12, 299-306
22. Newman, K. D.; Elamanchili, P.; Kwon, G. S.; Samuel, J. Uptake of Poly(d, l -lactic- co -Glycolic Acid) Microspheres by Antigen-Presenting Cells in Vivo J. Biomed. Mater. Res. 2002, 60, 480-486
23. Putney, S. D.; Burke, P. A. Improving Protein Therapeutics with Sustained-Release Formulations Nat. Biotechnol. 1998, 16, 153-157
24. Uchida, T.; Goto, S. Oral Delivery of Poly(lactide- co -Glycolide) Microspheres Containing Ovalbumin as Vaccine Formulation: Particle Size Study Biol. Pharm. Bull. 1994, 17, 1272-1276
25. Kumar, A.; Wonganan, P.; Sandoval, M. A.; Li, X.; Zhu, S.; Cui, Z. Microneedle-Mediated Transcutaneous Immunization with Plasmid DNA Coated on Cationic PLGA Nanoparticles J. Controlled Release 2012, 163, 230-239
26. Audran, R.; Peter, K.; Dannull, J.; Men, Y.; Scandella, E.; Groettrup, M.; Gander, B.; Corradin, G. Encapsulation of Peptides in Biodegradable Microspheres Prolongs Their MHC Class-I Presentation by Dendritic Cells and Macrophages in Vitro Vaccine 2003, 21, 1250-1255
27. De Geest, B. G.; Willart, M. A.; Hammad, H.; Lambrecht, B. N.; Pollard, C.; Bogaert, P.; De Filette, M.; Saelens, X.; Vervaet, C.; Remon, J. P. et al. Polymeric Multilayer Capsule-Mediated Vaccination Induces Protective Immunity Against Cancer and Viral infection ACS Nano 2012, 6, 2136-2149
28. Burgdorf, S.; Kurts, C. Endocytosis Mechanisms and the Cell Biology of Antigen Presentation Curr. Opin. Immunol. 2008, 20, 89-95
29. Abdelghany, S. M.; Quinn, D. J.; Ingram, R. J.; Gilmore, B. F.; Donnelly, R. F.; Taggart, C. C.; Scott, C. J. Gentamicin-Loaded Nanoparticles Show Improved Antimicrobial Effects towards Pseudomonas aeruginosa Infection Int. J. Nanomed. 2012, 7, 4053-4063
30. Lutsiak, M. E.; Robinson, D. R.; Coester, C.; Kwon, G. S.; Samuel, J. Analysis of Poly(d, l -lactic- co -Glycolic Acid) Nanosphere Uptake by Human Dendritic Cells and Macrophages in Vitro Pharm. Res. 2002, 19, 1480-1487
31. Elamanchili, P.; Diwan, M.; Cao, M.; Samuel, J. Characterization of Poly(d, l -lactic- co -Glycolic Acid) Based Nanoparticulate System for Enhanced Delivery of Antigens to Dendritic Cells Vaccine 2004, 22, 2406-2412
32. Vallhov, H.; Qin, J.; Johansson, S. M.; Ahlborg, N.; Muhammed, M. A.; Scheynius, A.; Gabrielsson, S. The Importance of an Endotoxin-Free Environment during the Production of Nanoparticles Used in Medical Applications Nano Lett. 2006, 6, 1682-1686
33. Uto, T.; Wang, X.; Sato, K.; Haraguchi, M.; Akagi, T.; Akashi, M.; Baba, M. Targeting of Antigen to Dendritic Cells with Poly(γ-glutamic acid) Nanoparticles Induces Antigen-Specific Humoral and Cellular Immunity J. Immunol. 2007, 178, 2979-2986
34. Donnelly, R. F.; Garland, M. J.; Morrow, D. I.; Migalska, K.; Singh, T. R.; Majithiya, R.; Woolfson, A. D. Optical Coherence Tomography Is a Valuable Tool in the Study of the Effects of Microneedle Geometry on Skin Penetration Characteristics and In-Skin Dissolution J. Controlled Release 2010, 147, 333-341
35. del Pilar Martin, M.; Weldon, W. C.; Zarnitsyn, V. G.; Koutsonanos, D. G.; Akbari, H.; Skountzou, I.; Jacob, J.; Prausnitz, M. R.; Compans, R. W. Local Response to Microneedle-Based Influenza Immunization in the Skin MBio 2012, 3, e00012-12
36. Henri, S.; Poulin, L. F.; Tamoutounour, S.; Ardouin, L.; Guilliams, M.; de Bovis, B.; Devilard, E.; Viret, C.; Azukizawa, H.; Kissenpfennig, A. et al. CD207+ CD103+ Dermal Dendritic Cells Cross-Present Keratinocyte-Derived Antigens Irrespective of the Presence of Langerhans Cells J. Exp. Med. 2010, 207, 189-206
37. Sullivan, S. P.; Koutsonanos, D. G.; Del Pilar Martin, M.; Lee, J. W.; Zarnitsyn, V.; Choi, S. O.; Murthy, N.; Compans, R. W.; Skountzou, I.; Prausnitz, M. R. Dissolving Polymer Microneedle Patches for Influenza Vaccination Nat. Med. 2010, 16, 915-920
38. Nishioka, Y.; Yoshino, H. Lymphatic Targeting with Nanoparticulate System Adv. Drug Delivery Rev. 2001, 47, 55-64
39. Reddy, S. T.; Rehor, A.; Schmoekel, H. G.; Hubbell, J. A.; Swartz, M. A. In Vivo Targeting of Dendritic Cells in Lymph Nodes with Poly(propylene sulfide) Nanoparticles J. Controlled Release 2006, 112, 26-34
40. Torchilin, V. P. Multifunctional Nanocarriers Adv. Drug Delivery Rev. 2006, 58, 1532-1555
41. Vasir, J. K.; Labhasetwar, V. Biodegradable Nanoparticles for Cytosolic Delivery of Therapeutics Adv. Drug Delivery Rev. 2007, 59, 718-728
42. Banchereau, J.; Steinman, R. M. Dendritic Cells and the Control of Immunity Nature 1998, 392, 245-252
43. Gamvrellis, A.; Leong, D.; Hanley, J. C.; Xiang, S. D.; Mottram, P.; Plebanski, M. Vaccines That Facilitate Antigen Entry into Dendritic Cells Immunol. Cell Biol. 2004, 82, 506-516
44. Waeckerle-Men, Y.; Allmen, E. U.; Gander, B.; Scandella, E.; Schlosser, E.; Schmidtke, G.; Merkle, H. P.; Groettrup, M. Encapsulation of Proteins and Peptides into Biodegradable Poly(d, l -lactide- co -Glycolide) Microspheres Prolongs and Enhances Antigen Presentation by Human Dendritic Cells Vaccine 2006, 24, 1847-1857
45. Partidos, C. D.; Beignon, A. S.; Mawas, F.; Belliard, G.; Briand, J. P.; Muller, S. Immunity under the Skin: Potential Application for Topical Delivery of Vaccines Vaccine 2003, 21, 776-780
46. Stoitzner, P.; Green, L. K.; Jung, J. Y.; Price, K. M.; Tripp, C. H.; Malissen, B.; Kissenpfennig, A.; Hermans, I. F.; Ronchese, F. Tumor Immunotherapy by Epicutaneous Immunization Requires Langerhans Cells J. Immunol. 2008, 180, 1991-1998
47. Seo, N.; Tokura, Y.; Nishijima, T.; Hashizume, H.; Furukawa, F.; Takigawa, M. Percutaneous Peptide Immunization via Corneum Barrier-Disrupted Murine Skin for Experimental Tumor Immunoprophylaxis Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 371-376
48. Kissenpfennig, A.; Henri, S.; Dubois, B.; Laplace-Builhe, C.; Perrin, P.; Romani, N.; Tripp, C. H.; Douillard, P.; Leserman, L.; Kaiserlian, D. et al. Dynamics and Function of Langerhans Cells in Vivo: Dermal Dendritic Cells Colonize Lymph Node Areas Distinct from Slower Migrating Langerhans Cells Immunity 2005, 22, 643-654
49. Hogquist, K. A.; Jameson, S. C.; Heath, W. R.; Howard, J. L.; Bevan, M. J.; Carbone, F. R. T Cell Receptor Antagonist Peptides Induce Positive Selection Cell 1994, 76, 17-27
50. Barnden, M. J.; Allison, J.; Heath, W. R.; Carbone, F. R. Defective TCR Expression in Transgenic Mice Constructed Using cDNA-Based α- and β-Chain Genes under the Control of Heterologous Regulatory Elements Immunol. Cell Biol. 1998, 76, 34-40
51. Tamoutounour, S.; Henri, S.; Lelouard, H.; de Bovis, B.; de Haar, C.; van der Woude, C. J.; Woltman, A. M.; Reyal, Y.; Bonnet, D.; Sichien, D. et al. CD64 Distinguishes Macrophages from Dendritic Cells in the Gut and Reveals the Th1-Inducing Role of Mesenteric Lymph Node Macrophages During Colitis Eur. J. Immunol. 2012, 42, 3150-3156
52. Vremec, D.; Pooley, J.; Hochrein, H.; Wu, L.; Shortman, K. CD4 and CD8 Expression by Dendritic Cell Subtypes in Mouse Thymus and Spleen J. Immunol. 2000, 164, 2978-2986
53. Brown, D. M.; Fisher, T. L.; Wei, C.; Frelinger, J. G.; Lord, E. M. Tumours Can Act as Adjuvants for Humoral Immunity Immunology 2001, 102, 486-497
54. Touzelet, O.; Loukili, N.; Pelet, T.; Fairley, D.; Curran, J.; Power, U. F. De Novo Generation of a Non-segmented Negative Strand RNA Virus with a Bicistronic Gene Virus Res. 2009, 140, 40-48