Incorporation of CpG into a liposomal vaccine formulation increases the maturation of antigen-loaded dendritic cells and monocytes to improve local and systemic immunity

Journal of Immunology

Volumn 192, Issue 8, 2014, Pages 3666-3675

  Neeland, Melanie R ^a   Elhay, Martin J ^b   Nathanielsz, Jackie ^b   Meeusen, Els N T ^a   De Veer, Michael J ^a  

^a MONASH UNIVERSITY   (Australia)

^b ZOETIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DENDRITIC CELLS; IMMUNITY, INNATE; IMMUNIZATION; INTERFERON-GAMMA; LIPOSOMES; LYMPH; LYMPHOCYTES; MONOCYTES; OLIGODEOXYRIBONUCLEOTIDES; PHENOTYPE; RECEPTORS, IMMUNOLOGIC; SHEEP; TIME FACTORS; VACCINES;

EID: 84898670711     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303014     Document Type: Article

References (54)

1. Coffman, R. L., A. Sher, and R. A. Seder. 2010. Vaccine adjuvants: putting innate immunity to work. Immunity 33: 492-503.
2. de Veer, M., and E. Meeusen. 2011. New developments in vaccine research -unveiling the secret of vaccine adjuvants. Discov. Med. 12: 195-204.
3. Bode, C., G. Zhao, F. Steinhagen, T. Kinjo, and D. M. Klinman. 2011. CpG DNA as a vaccine adjuvant. Expert Rev. Vaccines 10: 499-511.
4. Overstreet, M. G., H. Freyberger, I. A. Cockburn, Y. C. Chen, S. W. Tse, and F. Zavala. 2010. CpG-enhanced CD8+ T-cell responses to peptide immunization are severely inhibited by B cells. Eur. J. Immunol. 40: 124-133.
5. Jung, J., A. K. Yi, X. Zhang, J. Choe, L. Li, and Y. S. Choi. 2002. Distinct response of human B cell subpopulations in recognition of an innate immune signal, CpG DNA. J. Immunol. 169: 2368-2373.
6. Davis, H. L., R. Weeratna, T. J. Waldschmidt, L. Tygrett, J. Schorr, and A. M. Krieg. 1998. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. [Published erratum appears in 1999 J. Immunol. 162: 3103.] J. Immunol. 160: 870-876.
7. Lipford, G. B., M. Bauer, C. Blank, R. Reiter, H. Wagner, and K. Heeg. 1997. CpG-containing synthetic oligonucleotides promote B and cytotoxic T cell responses to protein antigen: a new class of vaccine adjuvants. Eur. J. Immunol. 27: 2340-2344.
8. Chu, R. S., O. S. Targoni, A. M. Krieg, P. V. Lehmann, and C. V. Harding. 1997. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J. Exp. Med. 186: 1623-1631.
9. Tross, D., and D. M. Klinman. 2008. Effect of CpG oligonucleotides on vaccineinduced B cell memory. J. Immunol. 181: 5785-5790.
10. Mapletoft, J. W., M. Oumouna, H. G. Townsend, S. Gomis, L. A. Babiuk, and S. van Drunen Littel-van den Hurk. 2006. Formulation with CpG oligodeoxynucleotides increases cellular immunity and protection induced by vaccination of calves with formalin-inactivated bovine respiratory syncytial virus. Virology 353: 316-323.
11. Linghua, Z., T. Xingshan, and Z. Fengzhen. 2008. In vivo oral administration effects of various oligodeoxynucleotides containing synthetic immunostimulatory motifs in the immune response to pseudorabies attenuated virus vaccine in newborn piglets. Vaccine 26: 224-233.
12. Klinman, D. M., H. Xie, S. F. Little, D. Currie, and B. E. Ivins. 2004. CpG oligonucleotides improve the protective immune response induced by the anthrax vaccination of rhesus macaques. Vaccine 22: 2881-2886.
13. Cooper, C. L., H. L. Davis, J. B. Angel, M. L. Morris, S. M. Elfer, I. Seguin, A. M. Krieg, and D. W. Cameron. 2005. CPG 7909 adjuvant improves hepatitis B virus vaccine seroprotection in antiretroviral-treated HIV-infected adults. AIDS 19: 1473-1479.
14. Cooper, C. L., H. L. Davis, M. L. Morris, S. M. Efler, M. A. Adhami, A. M. Krieg, D. W. Cameron, and J. Heathcote. 2004. CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B HBV vaccine in healthy adults: a double-blind phase I/II study. J. Clin. Immunol. 24: 693-701.
15. Halperin, S. A., G. Van Nest, B. Smith, S. Abtahi, H. Whiley, and J. J. Eiden. 2003. A phase I study of the safety and immunogenicity of recombinant hepatitis B surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide adjuvant. Vaccine 21: 2461-2467.
16. Gursel, I., M. Gursel, K. J. Ishii, and D. M. Klinman. 2001. Sterically stabilized cationic liposomes improve the uptake and immunostimulatory activity of CpG oligonucleotides. J. Immunol. 167: 3324-3328.
17. Shargh, V. H., M. R. Jaafari, A. Khamesipour, I. Jaafari, S. A. Jalali, A. Abbasi, and A. Badiee. 2012. Liposomal SLA co-incorporated with PO CpG ODNs or PS CpG ODNs induce the same protection against the murine model of leishmaniasis. Vaccine 30: 3957-3964.
18. Zaks, K., M. Jordan, A. Guth, K. Sellins, R. Kedl, A. Izzo, C. Bosio, and S. Dow. 2006. Efficient immunization and cross-priming by vaccine adjuvants containing TLR3 or TLR9 agonists complexed to cationic liposomes. J. Immunol. 176: 7335-7345.
19. Jaafari, M. R., A. Badiee, A. Khamesipour, A. Samiei, D. Soroush, M. T. Kheiri, F. Barkhordari, W. R. McMaster, and F. Mahboudi. 2007. The role of CpG ODN in enhancement of immune response and protection in BALB/c mice immunized with recombinant major surface glycoprotein of Leishmania (rgp63) encapsulated in cationic liposome. Vaccine 25: 6107-6117.
20. Lonez, C., M. Vandenbranden, and J. M. Ruysschaert. 2008. Cationic liposomal lipids: from gene carriers to cell signaling. Prog. Lipid Res. 47: 340-347.
21. Ma, Y. F., Y. Zhuang, X. F. Xie, C. Wang, F. Wang, D. M. Zhou, J. Q. Zeng, and L. T. Cai. 2011. The role of surface charge density in cationic liposomepromoted dendritic cell maturation and vaccine-induced immune responses. Nanoscale 3: 2307-2314.
22. Zhang, Y. M., M. Rusckowski, N. Liu, C. Liu, and D. J. Hnatowich. 2001. Cationic liposomes enhance cellular/nuclear localization of 99mTc-antisense oligonucleotides in target tumor cells. Cancer Biother. Radiopharm. 16: 411-419.
23. De Oliveira, M. C., V. Boutet, E. Fattal, D. Boquet, J. M. Grognet, P. Couvreur, and J. R. Deverre. 2000. Improvement of in vivo stability of phosphodiester oligonucleotide using anionic liposomes in mice. Life Sci. 67: 1625-1637.
24. Nordly, P., H. B. Madsen, H. M. Nielsen, and C. Foged. 2009. Status and future prospects of lipid-based particulate delivery systems as vaccine adjuvants and their combination with immunostimulators. Expert Opin. Drug Deliv. 6: 657-672.
25. Neeland, M. R., E. N. Meeusen, and M. J. de Veer. 2013. Afferent lymphatic cannulation as a model system to study innate immune responses to infection and vaccination. Vet. Immunol. Immunopathol. 158: 86-97.
26. de Veer, M., J. Kemp, J. Chatelier, M. J. Elhay, and E. N. Meeusen. 2010. The kinetics of soluble and particulate antigen trafficking in the afferent lymph, and its modulation by aluminum-based adjuvant. Vaccine 28: 6597-6602.
27. Hall, J. G. 1967. A method for collecting lymph from the prefemoral lymph node of unanaesthetised sheep. Q. J. Exp. Physiol. Cogn. Med. Sci. 52: 200-205.
28. de Veer, M., J. Kemp, J. Chatelier, M. J. Elhay, and E. N. Meeusen. 2012. Modulation of soluble and particulate antigen transport in afferent lymph by monophosphoryl lipid A. Immunol. Cell Biol. 90: 404-410.
29. Wee, J. L., D. L. Greenwood, X. Han, and J. P. Scheerlinck. 2011. Inflammatory cytokines IL-6 and TNF-a regulate lymphocyte trafficking through the local lymph node. Vet. Immunol. Immunopathol. 144: 95-103.
30. Jiang, Z. H., and R. R. Koganty. 2003. Synthetic vaccines: the role of adjuvants in immune targeting. Curr. Med. Chem. 10: 1423-1439.
31. Egan, P. J.,W. Kimpton, H. F. Seow, V.M. Bowles, M. R. Brandon, and A. D. Nash. 1996. Inflammation-induced changes in the phenotype and cytokine profile of cells migrating through skin and afferent lymph. Immunology 89: 539-546.
32. Caskey, M., F. Lefebvre, A. Filali-Mouhim, M. J. Cameron, J. P. Goulet, E. K. Haddad, G. Breton, C. Trumpfheller, S. Pollak, I. Shimeliovich, et al. 2011. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J. Exp. Med. 208: 2357-2366.
33. de Veer, M., M. Neeland, M. Burke, J. Pleasance, J. Nathanielsz, M. Elhay, and E. Meeusen. 2013. Cell recruitment and antigen trafficking in afferent lymph after injection of antigen and poly(I:C) containing liposomes, in aqueous or oilbased formulations. Vaccine 31: 1012-1018.
34. Yang, G. X., Z. X. Lian, K. Kikuchi, Y. J. Liu, A. A. Ansari, S. Ikehara, and M. E. Gershwin. 2005. CD4-plasmacytoid dendritic cells (pDCs) migrate in lymph nodes by CpG inoculation and represent a potent functional subset of pDCs. J. Immunol. 174: 3197-3203.
35. Sparwasser, T., E. S. Koch, R. M. Vabulas, K. Heeg, G. B. Lipford, J. W. Ellwart, and H. Wagner. 1998. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 28: 2045-2054.
36. Carrasco, C. P., R. C. Rigden, I. E. Vincent, C. Balmelli, M. Ceppi, O. Bauhofer, V. Tâche, B. Hjertner, F. McNeilly, H. G. van Gennip, et al. 2004. Interaction of classical swine fever virus with dendritic cells. J. Gen. Virol. 85: 1633-1641.
37. Behboudi, S., D. Chao, P. Klenerman, and J. Austyn. 2000. The effects of DNA containing CpG motif on dendritic cells. Immunology 99: 361-366.
38. Hackstein, H., A. Knoche, A. Nockher, J. Poeling, T. Kubin, M. Jurk, J. Vollmer, and G. Bein. 2011. The TLR7/8 ligand resiquimod targets monocyte-derived dendritic cell differentiation via TLR8 and augments functional dendritic cell generation. Cell. Immunol. 271: 401-412.
39. Bertho, N., F. Marquet, F. Pascale, C. Kang, M. Bonneau, and I. Schwartz-Cornil. 2011. Steady state pig dendritic cells migrating in skin draining pseudo-afferent lymph are semi-mature. Vet. Immunol. Immunopathol. 144: 430-436.
40. Gursel, M., D. Verthelyi, and D. M. Klinman. 2002. CpG oligodeoxynucleotides induce human monocytes to mature into functional dendritic cells. Eur. J. Immunol. 32: 2617-2622.
41. Ziegler-Heitbrock, L., P. Ancuta, S. Crowe, M. Dalod, V. Grau, D. N. Hart, P. J. Leenen, Y. J. Liu, G. MacPherson, G. J. Randolph, et al. 2010. Nomenclature of monocytes and dendritic cells in blood. Blood 116: e74-e80.
42. Joseph, A., I. Louria-Hayon, A. Plis-Finarov, E. Zeira, Z. Zakay-Rones, E. Raz, T. Hayashi, K. Takabayashi, Y. Barenholz, and E. Kedar. 2002. Liposomal immunostimulatory DNA sequence (ISS-ODN): an efficient parenteral and mucosal adjuvant for influenza and hepatitis B vaccines. Vaccine 20: 3342-3354.
43. Contreras, V., C. Urien, R. Guiton, Y. Alexandre, T. P. Vu Manh, T. Andrieu, K. Crozat, L. Jouneau, N. Bertho, M. Epardaud, et al. 2010. Existence of CD8a-like dendritic cells with a conserved functional specialization and a common molecular signature in distant mammalian species. J. Immunol. 185: 3313-3325.
44. Hope, J. C., E. Guzman, C. Cubillos-Zapata, S. A. Stephens, S. C. Gilbert, H. Prentice, P. Sopp, C. J. Howard, and B. Charleston. 2012. Migratory subpopulations of afferent lymphatic dendritic cells differ in their interactions with Mycobacterium bovis Bacille Calmette Guerin. Vaccine 30: 2357-2367.
45. Stephens, S. A., J. Brownlie, B. Charleston, and C. J. Howard. 2003. Differences in cytokine synthesis by the sub-populations of dendritic cells from afferent lymph. Immunology 110: 48-57.
46. Milling, S. W. F., C. D. Jenkins, U. Yrlid, V. Cerovic, H. Edmond, V. McDonald, M. Nassar, and G. Macpherson. 2009. Steady-state migrating intestinal dendritic cells induce potent inflammatory responses in naive CD4+ T cells. Mucosal Immunol. 2: 156-165.
47. Bedoui, S., P. G. Whitney, J. Waithman, L. Eidsmo, L. Wakim, I. Caminschi, R. S. Allan, M. Wojtasiak, K. Shortman, F. R. Carbone, et al. 2009. Crosspresentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10: 488-495.
48. Cobb, D., S. Guo, and R. B. Smeltz. 2013. CpG and interleukin-15 synergize to enhance IFN-gamma production by activated CD8+ T cells. BioMed Res. Int. 2013: 924023.
49. Zhao, K., H. Wang, and C. Y. Wu. 2011. The immune responses of HLAA0201 restricted SARS-CoV S peptide-specific CD8? T cells are augmented in varying degrees by CpG ODN, PolyI:C and R848. Vaccine 29: 6670-6678.
50. Andrews, C. D., M. S. Huh, K. Patton, D. Higgins, G. Van Nest, G. Ott, and K. D. Lee. 2012. Encapsulating immunostimulatory CpG oligonucleotides in listeriolysin O-liposomes promotes a Th1-type response and CTL activity. Mol. Pharm. 9: 1118-1125.
51. Ferrick, D. A., M. D. Schrenzel, T. Mulvania, B. Hsieh, W. G. Ferlin, and H. Lepper. 1995. Differential production of interferon-gamma and interleukin-4 in response to Th1-and Th2-stimulating pathogens by gamma delta T cells in vivo. Nature 373: 255-257.
52. Pinheiro, M. B., L. R. Antonelli, R. Sathler-Avelar, D. M. Vitelli-Avelar, S. Spindola-de-Miranda, T. M. P. D. Guimaraes, A. Teixeira-Carvalho, O. A. Martins, and V. P. C. P. Toledo. 2012. CD4-CD8-alpha beta and gamma delta T Cells Display Inflammatory and Regulatory Potentials during Human Tuberculosis. PLoS ONE 7: e50923.
53. Windon, R. G., P. J. Chaplin, P. McWaters, M. Tavarnesi, M. Tzatzaris, W. G. Kimpton, R. N. Cahill, L. Beezum, A. Coulter, D. Drane, et al. 2001. Local immune responses to influenza antigen are synergistically enhanced by the adjuvant ISCOMATRIX. Vaccine 20: 490-497.
54. Young, A. J., T. J. Seabrook, W. L. Marston, L. Dudler, and J. B. Hay. 2000. A role for lymphatic endothelium in the sequestration of recirculating gamma delta T cells in TNF-alpha-stimulated lymph nodes. Eur. J. Immunol. 30: 327-334.