Tuning the immune response of dendritic cells to surface-assembled poly(I:C) on microspheres through synergistic interactions between phagocytic and TLR3 signaling

Biomaterials

Volumn 32, Issue 10, 2011, Pages 2651-2661

  Hafner, Annina M ^a   Corthésy, Blaise ^b   Textor, Marcus ^a   Merkle, Hans P ^a  

^a ETH ZURICH   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Immunostimulation; Microspheres; PEGylation; Phagocytosis; Poly(I:C); Surface assembly

Indexed keywords

IMMUNOSTIMULATION; PEGYLATION; PHAGOCYTOSIS; POLY(I:C); SURFACE ASSEMBLY;

AMINO ACIDS; ANTIGEN-ANTIBODY REACTIONS; CELL PROLIFERATION; ETHYLENE; ETHYLENE GLYCOL; MICROSPHERES; POLYETHYLENE OXIDES; POLYSTYRENES; SIGNALING;

POLYETHYLENE GLYCOLS;

B7 ANTIGEN; CD86 ANTIGEN; COPOLYMER; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; MACROGOL; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MICROSPHERE; POLYINOSINIC POLYCYTIDYLIC ACID; POLYLYSINE; POLYSTYRENE; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA;

AQUEOUS SOLUTION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG FORMULATION; HELPER CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; MOLECULAR STABILITY; MONOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; SURFACE PROPERTY; T LYMPHOCYTE; ZETA POTENTIAL;

CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNITY; IMMUNIZATION; LYMPHOCYTE ACTIVATION; MICROSPHERES; MONOCYTES; PHAGOCYTES; POLY I-C; POLYETHYLENE GLYCOLS; POLYLYSINE; SIGNAL TRANSDUCTION; SURFACE PROPERTIES; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER; TOLL-LIKE RECEPTOR 3;

EID: 79251594583     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.12.021     Document Type: Article

References (65)

1. Gupta R.K., Singh M., O'Hagan D.T. Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv Drug Deliv Rev 1998, 32(3):225-246.
2. Alving C.R., Alan D.T.B., Lawrence R.S. Vaccine adjuvants. Vaccines for biodefense and emerging and neglected diseases 2009, 115. Academic Press, London.
3. Johansen P., Men Y., Merkle H.P., Gander B. Revisiting PLA/PLGA microspheres: an analysis of their potential in parenteral vaccination. Eur J Pharm Biopharm 2000, 50(1):129-146.
4. Langer R., Cleland J.L., Hanes J. New advances in microsphere-based single-dose vaccines. Adv Drug Deliv Rev 1997, 28(1):97-119.
5. Waeckerle-Men Y., Groettrup M. PLGA microspheres for improved antigen delivery to dendritic cells as cellular vaccines. Adv Drug Deliv Rev 2005, 57(3):475-482.
6. Audran R., Peter K., Dannull J., Men Y., Scandella E., Groettrup M., et al. Encapsulation of peptides in biodegradable microspheres prolongs their MHC class-I presentation by dendritic cells and macrophages in vitro. Vaccine 2003, 21(11-12):1250-1255.
7. Men Y., Tamber H., Audran R., Gander B., Corradin G. Induction of a cytotoxic T lymphocyte response by immunization with a malaria specific CTL peptide entrapped in biodegradable polymer microspheres. Vaccine 1997, 15(12-13):1405-1412.
8. Evans J.T., Ward J.R., Kern J., Johnson M.E. A single vaccination with protein-microspheres elicits a strong CD8 T-cell-mediated immune response against mycobacterium tuberculosis antigen Mtb8.4. Vaccine 2004, 22(15-16):1964-1972.
9. Men Y., Thomasin C., Merkle H.P., Gander B., Corradin G. A single administration of tetanus toxoid in biodegradable microspheres elicits T cell and antibody responses similar or superior to those obtained with aluminum hydroxide. Vaccine 1995, 13(7):683-689.
10. Men Y., Gander B., Merkle H.P., Corradin G. Induction of sustained and elevated immune responses to weakly immunogenic synthetic malarial peptides by encapsulation in biodegradable polymer microspheres. Vaccine 1996, 14(15):1442-1450.
11. Sharp F.A., Ruane D., Claass B., Creagh E., Harris J., Malyala P., et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc Natl Acad Sci U S A 2009, 106(3):870-875.
12. Wischke C., Zimmermann J., Wessinger B., Schendler A., Borchert H.H., Peters J.H., et al. Poly(I: C) coated PLGA microparticles induce dendritic cell maturation. Int J Pharm 2009, 365(1-2):61-68.
13. Fischer S., Uetz-von Allmen E., Waeckerle-Men Y., Groettrup M., Merkle H.P., Gander B. The preservation of phenotype and functionality of dendritic cells upon phagocytosis of polyelectrolyte-coated PLGA microparticles. Biomaterials 2007, 28(6):994-1004.
14. Wattendorf U., Coullerez G., Voros J., Textor M., Merkle H.P. Mannose-based molecular patterns on stealth microspheres for receptor-specific targeting of human antigen-presenting cells. Langmuir 2008, 24(20):11790-11802.
15. Medzhitov R., Janeway C.A. Innate immune recognition and control of adaptive immune responses. Semin Immunol 1998, 10(5):351-353.
16. Takeda K., Akira S. Toll-like receptors in innate immunity. Int Immunol 2005, 17(1):1-14.
17. Kumar H., Kawai T., Akira S. Toll-like receptors and innate immunity. Biochem Biophys Res Commun 2009, 388(4):621-625.
18. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000, 18:767-811.
19. Granucci F., Foti M., Ricciardi-Castagnoli P. Dendritic cell biology. Adv Immunol 2005, 88:193-233.
20. van Duin D., Medzhitov R., Shaw A.C. Triggering TLR signaling in vaccination. Trends Immunol 2006, 27(1):49-55.
21. Klinman D.M. Adjuvant activity of CpG oligodeoxynucleotides. Int Rev Immunol 2006, 25(3-4):135-154.
22. Jin B., Sun T., Yu X.-H., Liu C.-Q., Yang Y.-X., Lu P., et al. Immunomodulatory effects of dsRNA and its potential as vaccine adjuvant. J Biomed Biotechnol 2010.
23. Matsumoto M., Seya T. TLR3: interferon induction by double-stranded RNA including poly(I: C). Adv Drug Deliv Rev 2008, 60(7):805-812.
24. Alexopoulou L., Holt A.C., Medzhitov R., Flavell R.A. Recognition of double-stranded RNA and activation of NF-kappaB by toll-like receptor 3. Nature 2001, 413(6857):732-738.
25. Verdijk R.M., Mutis T., Esendam B., Kamp J., Melief C.J.M., Brand A., et al. Polyriboinosinic polyribocytidylic acid (poly(I: C)) induces stable maturation of functionally active human dendritic cells. J Immunol 1999, 163(1):57-61.
26. Cella M., Salio M., Sakakibara Y., Langen H., Julkunen I., Lanzavecchia A. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 1999, 189(5):821-829.
27. Suzuki K., Mori A., Ishii K.J., Saito J., Singer D.S., Klinman D.M., et al. Activation of target-tissue immune-recognition molecules by double-stranded polynucleotides. Proc Natl Acad Sci U S A 1999, 96(5):2285-2290.
28. Anders H.J., Zecher D., Pawar R.D., Patole P.S. Molecular mechanisms of autoimmunity triggered by microbial infection. Arthritis Res Ther 2005, 7(5):215-224.
29. Lang K.S., Recher M., Junt T., Navarini A.A., Harris N.L., Freigang S., et al. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat Med 2005, 11(2):138-145.
30. Wattendorf U., Koch M.C., Walter E., Voeroes J., Textor M., Merkle H.P. Phagocytosis of poly(L-lysine)-graft-poly(ethylene glycol) coated microspheres by antigen presenting cells: impact of grafting ratio and poly(ethylene glycol) chain length on cellular recognition. Biointerphases 2006, 1(4):123-133.
31. Wattendorf U., Kreft O., Textor M., Sukhorukov G.B., Merkle H.P. Stable stealth function for hollow polyelectrolyte microcapsules through a poly(ethylene glycol) grafted polyelectrolyte adlayer. Biomacromolecules 2008, 9(1):100-108.
32. Pasche S., De Paul S.M., Voeroes J., Spencer N.D., Textor M. Poly(L-lysine)-graft-poly(ethylene glycol) assembled monolayers on niobium oxide surfaces: a quantitative study of the influence of polymer interfacial architecture on resistance to protein adsorption by ToF-SIMS and in situ OWLSu OWLS. Langmuir 2003, 19(22):9216-9225.
33. O'Garra A. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 1998, 8(3):275-283.
34. Constant S.L., Bottomly K. Induction of Th1 and Th2 CD4+T cell responses: the alternative approaches. Annu Rev Immunol 1997, 15:297-322.
35. Sokolova V, Knuschke T, Kovtun A, Buer J, Epple M, Westendorf AM. The use of calcium phosphate nanoparticles encapsulating toll-like receptor ligands and the antigen hemagglutinin to induce dendritic cell maturation and T cell activation. Biomaterials;31(21):5627.
36. Schlosser E., Mueller M., Fischer S., Basta S., Busch D.H., Gander B., et al. TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses. Vaccine 2008, 26(13):1626-1637.
37. De Paul S.M., Falconnet D., Pasche S., Textor M., Abel A.P., Kauffmann E., et al. Tuned graft copolymers as controlled coatings for DNA microarrays. Anal Chem 2005, 77(18):5831-5838.
38. Kohase M., Vilcek J. Regulation of human interferon production stimulated with poly(I)-poly(C): correlation between shutoff and hyporesponsiveness to reinduction. Virology 1977, 76(1):47-54.
39. Sehgal P.B., Dobberstein B., Tamm I. Interferon messenger RNA content of human fibroblasts during induction, shutoff, and superinduction of interferon production. Proc Natl Acad Sci U S A 1977, 74(8):3409-3413.
40. Guillot L., Le Goffic R., Bloch S., Escriou N., Akira S., Chignard M., et al. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza a virus. J Biol Chem 2005, 280(7):5571-5580.
41. King N.J., Kesson A.M. Interferon-independent increases in class I major histocompatibility complex antigen expression follow flavivirus infection. J Gen Virol 1988, 69:2535-2543.
42. Samuel C.E. Antiviral actions of interferons. Clin Microbiol Rev 2001, 14(4):778-809.
43. Kocic G., Bjelakovic G., Saranac L., Kocic R., Jevtovic T., Sokolovic D., et al. Altered degradation of circulating nucleic acids and oligonucleotides in diabetic patients. Diabetes Res Clin Pract 2008, 79(2):204-213.
44. Sobel D.O., Newsome J., Ewel C.H., Bellanti J.A., Abbassi V., Creswell K., et al. Poly I: C induces development of diabetes mellitus in BB rat. Diabetes 1992, 41(4):515-520.
45. Moore K.W., de Waal Malefyt R., Coffman R.L., O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001, 19:683-765.
46. Ma X., Trinchieri G. Regulation of interleukin-12 production in antigen-presenting cells. Adv Immunol 2001, 79:55-92.
47. Caspi R.R. IL-12 in autoimmunity. Clin Immunol Immunopathol 1998, 88(1):4-13.
48. Shi F.D., Ljunggren H.G., Sarvetnick N. Innate immunity and autoimmunity: from self-protection to self-destruction. Trends Immunol 2001, 22(2):97-101.
49. de Bouteiller O., Merck E., Hasan U.A., Hubac S., Benguigui B., Trinchieri G., et al. Recognition of double-stranded RNA by human toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH. J Biol Chem 2005, 280(46):38133-38145.
50. Kung M.P., Ho Y.K., Lalka D., Bardos T.J. Plasma clearance and tissue distribution of partially thiolated polycytidylic acid and its degradation products in rodents. Cancer Res 1984, 44(10):4602-4606.
51. Kol'tsov V.D., Krasnova L.V., Balandin I.G., Meshkova E.N. Interferon-inducing activity of poly(I)-poly(C) and its complexes with polycations and their resistance to enzymatic degradation. Biull Eksp Biol Med 1983, 96(9):74-77.
52. Underhill D.M., Gantner B. Integration of toll-like receptor and phagocytic signaling for tailored immunity. Microbes Infect 2004, 6(15):1368-1373.
53. Sallusto F., Cella M., Danieli C., Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 1995, 182(2):389-400.
54. Blander J.M., Medzhitov R. Regulation of phagosome maturation by signals from toll-like receptors. Science 2004, 304(5673):1014-1018.
55. Yates R.M., Russell D.G. Phagosome maturation proceeds independently of stimulation of toll-like receptors 2 and 4. Immunity 2005, 23(4):409-417.
56. Russell D.G., Yates R.M. Toll-like receptors and phagosome maturation. Nat Immunol 2007, 8(3):217-218.
57. Blander J.M., Medzhitov R. Reply to: toll-like receptors and phagosome maturation. Nat Immunol 2007, 8(3):217.
58. Blander J.M. Coupling toll-like receptor signaling with phagocytosis: potentiation of antigen presentation. Trends Immunol 2007, 28(1):19-25.
59. Hume D.A., Ross I.L., Himes S.R., Sasmono R.T., Wells C.A., Ravasi T. The mononuclear phagocyte system revisited. J Leukoc Biol 2002, 72(4):621-627.
60. Chieppa M., Bianchi G., Doni A., Del Prete A., Sironi M., Laskarin G., et al. Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J Immunol 2003, 171(9):4552-4560.
61. Rittirsch D., Flierl M.A., Day D.E., Nadeau B.A., Zetoune F.S., Sarma J.V., et al. Cross-talk between TLR4 and Fc gamma receptor III (CD16) pathways. PLoS Pathog 2009, 5(6):e1000464.
62. Sutterwala F.S., Noel G.J., Salgame P., Mosser D.M. Reversal of proinflammatory responses by ligating the macrophage Fc gamma receptor type I. J Exp Med 1998, 188(1):217-222.
63. Sutterwala F.S., Noel G.J., Clynes R., Mosser D.M. Selective suppression of interleukin-12 induction after macrophage receptor ligation. J Exp Med 1997, 185(11):1977-1985.
64. Anderson C.F., Mosser D.M. Cutting edge: biasing immune responses by directing antigen to macrophage Fc gamma receptors. J Immunol 2002, 168(8):3697-3701.
65. de Jong E.C., Vieira P.L., Kalinski P., Schuitemaker J.H., Tanaka Y., Wierenga E.A., et al. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse Th cell-polarizing signals. J Immunol 2002, 168(4):1704-1709.