Neutral polymer micelle carriers with pH-responsive, endosome-releasing activity modulate antigen trafficking to enhance CD8+ T cell responses

Journal of Controlled Release

Volumn 191, Issue , 2014, Pages 24-33

  Keller, Salka ^a   T wilson, John ^a   Patilea, Gabriela I ^a   Kern, Hanna B ^a   Convertine, Anthony J ^a   Stayton, Patrick S ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Nanoparticles; Ph responsive; Polymer micelles; Subunit vaccine

Indexed keywords

ANTIGENS; CELL CULTURE; CELLS; CYTOLOGY; IMMUNIZATION; MICELLES; MIXTURES; NANOPARTICLES; POLYMERS; PROTEINS; VACCINES;

ANTIGEN PRESENTING CELLS; DIMETHYLAMINOETHYL METHACRYLATES; HUMORAL IMMUNE RESPONSE; INTRACELLULAR PATHOGENS; MURINE DENDRITIC CELLS; PH-RESPONSIVE; POLYMER MICELLES; SUBUNIT VACCINE;

T-CELLS;

ACRYLIC ACID DERIVATIVE; ANTIGEN; DISULFIDE; DRUG CARRIER; GAMMA INTERFERON; IMMUNOGLOBULIN G1 ANTIBODY; N (2 HYDROXYPROPYL)METHACRYLAMIDE; NANOPARTICLE; OVALBUMIN; POLYMER; PROPYLACRYLIC ACID; UNCLASSIFIED DRUG; VACCINE; DELAYED RELEASE FORMULATION; MICELLE; SUBUNIT VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN PRESENTING CELL; ARTICLE; BIOCOMPATIBILITY; CD8+ T LYMPHOCYTE; CONFORMATIONAL TRANSITION; CONJUGATION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENDOSOME; EXOCYTOSIS; FEMALE; IMMUNIZATION; IN VITRO STUDY; MACROPHAGE; MICELLE; MOUSE; NONHUMAN; PARTICLE SIZE; PH; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CELL LINE; CHEMISTRY; DELAYED RELEASE FORMULATION; DRUG EFFECTS; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; MEDICINAL CHEMISTRY; METABOLISM; PHARMACEUTICS; PROCEDURES; PROTEIN TRANSPORT; TIME;

ANIMALS; ANTIGENS; CELL LINE; CHEMISTRY, PHARMACEUTICAL; DELAYED-ACTION PREPARATIONS; DENDRITIC CELLS; DRUG CARRIERS; ENDOSOMES; FEMALE; HYDROGEN-ION CONCENTRATION; IMMUNIZATION; LYMPH NODES; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE, INBRED C57BL; MICELLES; NANOPARTICLES; OVALBUMIN; PARTICLE SIZE; POLYMERS; PROTEIN TRANSPORT; T-LYMPHOCYTES, CYTOTOXIC; TECHNOLOGY, PHARMACEUTICAL; TIME FACTORS; VACCINES, SUBUNIT;

EID: 84906950999     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.03.041     Document Type: Article

References (48)

1. M.A. Swartz, S. Hirosue, J.A. Hubbell, Engineering approaches to immunotherapy, Sci. Transl. Med. 4 (2012) 148rv9.
2. J.A. Hubbell, S.N. Thomas, M.A. Swartz, Materials engineering for immunomodulation, Nature 462 (2009) 449-460.
3. M.-L. De Temmerman, J. Rejman, J. Demeester, D.J. Irvine, B. Gander, S.C. De Smedt, Particulate vaccines: on the quest for optimal delivery and immune response, Drug Discov. Today 16 (2011) 569-582.
4. S. Flanary, A.S. Hoffman, P.S. Stayton, Antigen delivery with poly (propylacrylic acid) conjugation enhances MHC-1 presentation and T-Cell activation, Bioconjug. Chem. 20 (2009) 241-248.
5. H. Shen, A.L. Ackerman, V. Cody, A. Giodini, E.R. Hinson, P. Cresswell, et al., Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles, Immunology 117 (2006) 78-88.
6. D.M. Smith, J.K. Simon, J.R. Baker, Applications of nanotechnology for immunology, Nat. Rev. Immunol. 13 (2013) 592-605.
7. I.C. Kourtis, S. Hirosue, A. De Titta, S. Kontos, T. Stegmann, J.A. Hubbell, et al., Peripherally administered nanoparticles target monocytic myeloid cells, secondary lymphoid organs and tumors in mice, PLoS One 8 (2013) e61646.
8. T. Akagi, F. Shima, M. Akashi, Intracellular degradation and distribution of proteinencapsulated amphiphilic poly(amino acid) nanoparticles, Biomaterials 32 (2011) 4959-4967.
9. J.T.Wilson, S. Keller, M.J.Manganiello, C.Cheng, C.-C. Lee, C. Opara, et al., pH-responsive nanoparticle vaccines for dual-delivery of antigens and immunostimulatory oligonucleotides, ACS Nano 7 (2013) 3912-3925.
10. J.K. Eby, K.Y. Dane, C.P. O'Neil, S. Hirosue, M.A. Swartz, J.A. Hubbell, Polymermicelles with pyridyl disulfide-coupled antigen travel through lymphatics and show enhanced cellular responses following immunization, Acta Biomater. 8 (2012) 3210-3217.
11. Y. Jik, E. James, N. Shastri, J.M.J. Fréchet, Y.J. Kwon, E. Jamest, et al., In vivo targeting of dendritic cells for activation of cellular immunity using vaccine carriers based on pH-responsive microparticles, Proc. Natl. Acad. Sci. U. S. A. 102 (2012) 18264-18268.
12. J.J. Moon, H. Suh, A. Bershteyn, M.T. Stephan, H. Liu, B. Huang, et al., Interbilayercrosslinked multilamellar vesicles as synthetic vaccines for potent humoral and cellular immune responses, Nat. Med. 10 (2011) 243-251.
13. E. Yuba, C. Kojima, A. Harada, Tana, S. Watarai, K. Kono, pH-sensitive fusogenic polymer-modified liposomes as a carrier of antigenic proteins for activation of cellular immunity, Biomaterials 31 (2010) 943-951.
14. J. Zhang, L. Wu, F. Meng, Z. Wang, C. Deng, H. Liu, et al., pH and reduction dualbioresponsive polymersomes for efficient intracellular protein delivery, Langmuir 28 (2012) 2056-2065.
15. A. Stano, E.A. Scott, K.Y. Dane, M.A. Swartz, J.A. Hubbell, Tunable T cell immunity towards a protein antigen using polymersomes vs. solid-core nanoparticles, Biomaterials (2013) 2-9.
16. L.M. Kaminskas, C.J.H. Porter, Targeting the lymphatics using dendritic polymers (dendrimers), Adv. Drug Deliv. Rev. 63 (2011) 890-900.
17. S. Foster, C.L. Duvall, E.F. Crownover, A.S. Hoffman, P.S. Stayton, Intracellular delivery of a protein antigen with an endosomal-releasing polymer enhances CD8 T-cell production and prophylactic vaccine efficacy, Bioconjug. Chem. 21 (2010) 2205-2212.
18. B.B. Lundy, A. Convertine, M. Miteva, P.S. Stayton, Neutral polymeric micelles for RNA delivery, Bioconjug. Chem. 24 (2013) 398-407.
19. A.J. Convertine, C. Diab, M. Prieve, A. Paschal, A.S. Hoffman, P.H. Johnson, et al., pH-responsive polymeric micelle carriers for siRNA drugs, Biomacromolecules 11 (2010) 2904-2911.
20. J.J. Skehel, D.C.Wiley, Receptor binding and membrane fusion in virus entry: The influenza hemagglutinin, Annu. Rev. Biochem. 12 (2000) 531-569.
21. C.W. Scales, Y.A. Vasilieva, A.J. Convertine, A.B. Lowe, C.L. McCormick, Direct, controlled synthesis of the nonimmunogenic, hydrophilic polymer, poly(N-(2-hydroxypropyl) methacrylamide) via RAFT in aqueous media, Biomacromolecules 6 (2005) 1846-1850.
22. A.J. Convertine, D.S.W. Benoit, C.L. Duvall, A.S. Hoffman, P.S. Stayton, Development of a novel endosomolytic diblock copolymer for siRNA delivery, J. Control. Release 133 (2009) 221-229.
23. C. Nembrini, A. Stano, K.Y. Dane, M. Ballester, A.J. van der Vlies, B.J. Marsland, et al., Nanoparticle conjugation of antigen enhances cytotoxic T-cell responses in pulmonary vaccination, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) E989-E997.
24. S. Hirosue, I.C. Kourtis, A.J. van der Vlies, J.A. Hubbell, M.A. Swartz, Antigen delivery to dendritic cells by poly(propylene sulfide) nanoparticles with disulfide conjugated peptides: cross-presentation and T cell activation, Vaccine 28 (2010) 7897-7906.
25. C.L.Duvall, A.J. Convertine, D.S.W. Benoit, A.S. Hoffman, P.S. Stayton, Intracellulardelivery of a proapoptotic peptide via conjugation to a RAFT synthesized endosomolytic polymer, Mol. Pharm. 7 (2010) 468-476.
26. J. Kim, D.A. Tirrell, Synthesis of well-defined poly (2-ethylacrylic acid), Macromolecules 32 (1999) 945-948.
27. N. Murthy, J.R. Robichaud, D.A. Tirrell, P.S. Stayton, A.S. Hoffman, The design and synthesis of polymers for eukaryotic membrane disruption, J. Control. Release 61 (1999) 137-143.
28. J. Karttunen, S. Sanderson, N. Shastri, Detection of rare antigen-presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens, Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 6020-6024.
29. J. Shi, B. Chou, J.L. Choi, A. Ta, S.H. Pun, Investigation of polyethylenimine/DNA polyplex transfection to cultured cells using radiolabeling and subcellular fractionation methods, Mol. Pharm. 10 (2013) 2145-2156.
30. L.A. Brito, M. Singh, Acceptable levels of endotoxin in vaccine formulations during preclinical research, J. Pharm. Sci. 100 (2011) 34-37.
31. J. Chiefari, Y.K.B. Chong, F. Ercole, J. Kristina, J. Jeffery, T.P.T. Le, et al., Living freeradical polymerization by reversible addition-fragmentation chain transfer: The RAFT process, Macromolecules 9297 (1998) 5559-5562.
32. G. Moad, E. Rizzardo, S.H. Thang, Living radical polymerization by the RAFT process, Aust. J. Chem. 58 (2005) 379.
33. Z. Szablan, A.A.H. Toy, A. Terrenoire, T.P. Davis, C. Barner-Kowollik, Living free-radical polymerization of sterically hindered monomers: improving the understanding of 1, 1-disubstituted monomer systems, J. Polym. Sci. A Polym. Chem. 44 (2006) 3692-3710.
34. Z. Szablan, A.A. Toy, T.P. Davis, X. Hao, M.H. Stenzel, C. Barner-Kowollik, Reversible addition fragmentation chain transfer polymerization of sterically hindered monomers: Toward well-defined rod/coil architectures, J. Polym. Sci. A Polym. Chem. 42 (2004) 2432-2443.
35. F.P. Seib, A.T. Jones, R. Duncan, Establishment of subcellular fractionation techniques to monitor the intracellular fate of polymer therapeutics I. Differential centrifugation fractionation B16F10 cells and use to study the intracellular fate of HPMA copolymer-doxorubicin, J. Drug Target. 14 (2006) 375-390.
36. M. Wendeler, K. Sandhoff, Hexosaminidase assays, Glycoconj. J. 26 (2009) 945-952.
37. J.-P. Gorvel, P. Chavrier, M. Zerial, J. Gruenberg, Rab5 controls early endosome fusion in vitro, Cell 64 (1991) 915-925.
38. E. Eskelinen, A.L. Illert, Y. Tanaka, J. Blanz, K. Von Figura, P. Saftig, et al., Role of LAMP-2 in lysosome biogenesis and autophagy, Mol. Biol. Cell 13 (2002) 3355-3368.
39. S.T. Reddy, A.J. van der Vlies, E. Simeoni, V. Angeli, G.J. Randolph, C.P. O'Neil, et al., Exploiting lymphatic transport and complement activation in nanoparticle vaccines, Nat. Biotechnol. 25 (2007) 1159-1164.
40. S.T. Reddy, A. Rehor, H.G. Schmoekel, J.A. Hubbell, M.A. Swartz, In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles, J. Control. Release 112 (2006) 26-34.
41. B. Salomon, J.L. Cohen, C. Masurier, D. Klatzmann, Three populations of mouse lymph node dendritic cells with different origins and dynamics, J. Immunol. 160 (1998) 708-717.
42. S.E. Macatonia, S.C. Knight, A.J. Edwards, S. Griffiths, P. Fryer, Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate, J. Exp. Med. 166 (1987) 1654-1667.
43. S.C.W. Richardson, N.G. Pattrick, N. Lavignac, P. Ferruti, R. Duncan, Intracellular fate of bioresponsive poly(amidoamine)s in vitro and in vivo, J. Control. Release 142 (2010) 78-88.
44. L.S. Johnson, K.W. Dunn, B. Pytowski, T.E. McGraw, Endosome acidification and receptor trafficking: bafilomycin A1 slows receptor externalization by a mechanism involving the receptor's internalization motif, Mol. Biol. Cell 4 (1993) 1251-1266.
45. M.I. Crespo, E.R. Zacca, N.G. Núñez, R.P. Ranocchia, M. Maccioni, B.A. Maletto, et al., TLR7 triggering with polyuridylic acid promotes cross-presentation in CD8α+ conventional dendritic cells by enhancing antigen preservation and MHC class I antigen permanence on the dendritic cell surface, J. Immunol. 190 (2013) 948-960.
46. V. Manolova, A. Flace, M. Bauer, K. Schwarz, P. Saudan, M.F. Bachmann, Nanoparticles target distinct dendritic cell populations according to their size, Eur. J. Immunol. 38 (2008) 1404-1413.
47. F. Wegmann, K.H. Gartlan, A.M. Harandi, S.A. Brinckmann, M. Coccia, W.R. Hillson, et al., Polyethyleneimine is a potent mucosal adjuvant for viral glycoprotein antigens, Nat. Biotechnol. (2012) 1-8.
48. T. Akagi, M. Baba, M. Akashi, Biodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccines, Adv. Polym. Sci. 247 (2012) 31-64.