Coadministration of antigen-conjugated and free CpG: Effects of in vitro and in vivo interactions in a murine model

Immunology Letters

Volumn 160, Issue 2, 2014, Pages 178-185

  Herbáth, Melinda ^a   Szekeres, Zsuzsanna ^b   Kövesdi, Dorottya ^a   Papp, Krisztián ^b   Erdei, Anna ^a,b   Prechl, József ^b  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b MTA ELTE Immunology Research Group Eötvös University   (Hungary)

Author keywords

Adjuvant; Antigen presentation; Cell activation; CpG; TLR9; Vaccination

Indexed keywords

ANTIBODY; ANTIGEN; CPG OLIGODEOXYNUCLEOTIDE; STREPTAVIDIN; TOLL LIKE RECEPTOR 9; ANTIBODY CONJUGATE; BIOTIN; CPG-OLIGONUCLEOTIDE; IMMUNOLOGICAL ADJUVANT; MYC PROTEIN; MYC PROTEIN, MOUSE; OLIGODEOXYRIBONUCLEOTIDE; PEPTIDE; RECOMBINANT VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; BIOTINYLATION; CELL ACTIVATION; CONJUGATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; T LYMPHOCYTE; VACCINATION; ANIMAL; C57BL MOUSE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LYMPH NODE; TRANSPORT AT THE CELLULAR LEVEL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS; B-LYMPHOCYTES; BIOLOGICAL TRANSPORT; BIOTIN; BIOTINYLATION; DENDRITIC CELLS; FEMALE; IMMUNOCONJUGATES; LYMPH NODES; MICE; MICE, INBRED C57BL; OLIGODEOXYRIBONUCLEOTIDES; PEPTIDES; PROTO-ONCOGENE PROTEINS C-MYC; STREPTAVIDIN; T-LYMPHOCYTES; VACCINATION; VACCINES, SYNTHETIC;

EID: 84902539513     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2014.02.007     Document Type: Article

References (33)

1. Ahmad-Nejad P., Hacker H., Rutz M., Bauer S., Vabulas R.M., Wagner H. Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur J Immunol 2002, 32:1958-1968.
2. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374:546-549.
3. Stacey K.J., Sweet M.J., Hume D.A. Macrophages ingest and are activated by bacterial DNA. J Immunol 1996, 157:2116-2122.
4. Ballas Z.K., Rasmussen W.L., Krieg A.M. Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J Immunol 1996, 157:1840-1845.
5. Krieg A.M. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 2002, 20:709-760.
6. Zhao Q., Matson S., Herrera C.J., Fisher E., Yu H., Krieg A.M. Comparison of cellular binding and uptake of antisense phosphodiester, phosphorothioate, and mixed phosphorothioate and methylphosphonate oligonucleotides. Antisense Res Dev 1993, 3:53-66.
7. Brown D.A., Kang S.H., Gryaznov S.M., DeDionisio L., Heidenreich O., Sullivan S., et al. Effect of phosphorothioate modification of oligodeoxynucleotides on specific protein binding. J Biol Chem 1994, 269:26801-26805.
8. Eckl-Dorna J., Batista F.D. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood 2009, 113:3969-3977.
9. Utaisincharoen P., Kespichayawattana W., Anuntagool N., Chaisuriya P., Pichyangkul S., Krieg A.M., et al. CpG ODN enhances uptake of bacteria by mouse macrophages. Clin Exp Immunol 2003, 132:70-75.
10. Iribarren P., Chen K., Hu J., Gong W., Cho E.H., Lockett S., et al. CpG-containing oligodeoxynucleotide promotes microglial cell uptake of amyloid beta 1-42 peptide by up-regulating the expression of the G-protein-coupled receptor mFPR2. FASEB J 2005, 19:2032-2034.
11. Prechl J., Molnar E., Szekeres Z., Isaak A., Papp K., Balogh P., et al. Murine CR1/2 targeted antigenized single-chain antibody fragments induce transient low affinity antibodies and negatively influence an ongoing immune response. Adv Exp Med Biol 2007, 598:214-225.
12. Szekeres Z., Herbath M., Angyal A., Szittner Z., Virag V., Balogh P., et al. Modulation of immune response by combined targeting of complement receptors and low-affinity Fcgamma receptors. Immunol Lett 2010, 130:66-73.
13. Szekeres Z., Herbath M., Szittner Z., Papp K., Erdei A., Prechl J. Modulation of the humoral immune response by targeting CD40 and FcgammaRII/III; delivery of soluble but not particulate antigen to CD40 enhances antibody responses with a Th1 bias. Mol Immunol 2011, 49:155-162.
14. Inaba K., Inaba M., Romani N., Aya H., Deguchi M., Ikehara S., et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992, 176:1693-1702.
15. Janas M.L., Groves P., Kienzle N., Kelso A. IL-2 regulates perforin and granzyme gene expression in CD8+ T cells independently of its effects on survival and proliferation. J Immunol 2005, 175:8003-8010.
16. Hacker H., Mischak H., Miethke T., Liptay S., Schmid R., Sparwasser T., et al. CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J 1998, 17:6230-6240.
17. Baumann C.L., Aspalter I.M., Sharif O., Pichlmair A., Bluml S., Grebien F., et al. CD14 is a coreceptor of Toll-like receptors 7 and 9. J Exp Med 2010, 207:2689-2701.
18. Gursel M., Gursel I., Mostowski H.S., Klinman D.M. CXCL16 influences the nature and specificity of CpG-induced immune activation. J Immunol 2006, 177:1575-1580.
19. Jozefowski S., Sulahian T.H., Arredouani M., Kobzik L. Role of scavenger receptor MARCO in macrophage responses to CpG oligodeoxynucleotides. J Leukoc Biol 2006, 80:870-879.
20. Lahoud M.H., Ahmet F., Zhang J.G., Meuter S., Policheni A.N., Kitsoulis S., et al. DEC-205 is a cell surface receptor for CpG oligonucleotides. Proc Natl Acad Sci U S A 2012, 109:16270-16275.
21. Asokan R., Banda N.K., Szakonyi G., Chen X.S., Holers V.M. Human complement receptor 2 (CR2/CD21) as a receptor for DNA: implications for its roles in the immune response and the pathogenesis of systemic lupus erythematosus (SLE). Mol Immunol 2012, 53:99-110.
22. Sivori S., Falco M., Carlomagno S., Romeo E., Soldani C., Bensussan A., et al. A novel KIR-associated function: evidence that CpG DNA uptake and shuttling to early endosomes is mediated by KIR3DL2. Blood 2010, 116:1637-1647.
23. Anderson R.B., Cianciolo G.J., Kennedy M.N., Pizzo S.V. Alpha 2-macroglobulin binds CpG oligodeoxynucleotides and enhances their immunostimulatory properties by a receptor-dependent mechanism. J Leukoc Biol 2008, 83:381-392.
24. Heeg K., Dalpke A., Peter M., Zimmermann S. Structural requirements for uptake and recognition of CpG oligonucleotides. Int J Med Microbiol 2008, 298:33-38.
25. Landrigan A., Wong M.T., Utz P.J. CpG and non-CpG oligodeoxynucleotides directly costimulate mouse and human CD4+ T cells through a TLR9- and MyD88-independent mechanism. J Immunol 2011, 187:3033-3043.
26. Avalos A.M., Ploegh H.L. Competition by inhibitory oligonucleotides prevents binding of CpG to C-terminal TLR9. Eur J Immunol 2011, 41:2820-2827.
27. Hacker H., Vabulas R.M., Takeuchi O., Hoshino K., Akira S., Wagner H. Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF)6. J Exp Med 2000, 192:595-600.
28. Kulkarni R., Behboudi S., Sharif S. Insights into the role of Toll-like receptors in modulation of T cell responses. Cell Tissue Res 2011, 343:141-152.
29. Oxenius A., Martinic M.M., Hengartner H., Klenerman P. CpG-containing oligonucleotides are efficient adjuvants for induction of protective antiviral immune responses with T-cell peptide vaccines. J Virol 1999, 73:4120-4126.
30. Vabulas R.M., Pircher H., Lipford G.B., Hacker H., Wagner H. CpG-DNA activates in vivo T cell epitope presenting dendritic cells to trigger protective antiviral cytotoxic T cell responses. J Immunol 2000, 164:2372-2378.
31. Dalpke A.H., Zimmermann S., Albrecht I., Heeg K. Phosphodiester CpG oligonucleotides as adjuvants: polyguanosine runs enhance cellular uptake and improve immunostimulative activity of phosphodiester CpG oligonucleotides in vitro and in vivo. Immunology 2002, 106:102-112.
32. Sparwasser T., Miethke T., Lipford G., Borschert K., Hacker H., Heeg K., et al. Bacterial DNA causes septic shock. Nature 1997, 386:336-337.
33. Heikenwalder M., Polymenidou M., Junt T., Sigurdson C., Wagner H., Akira S., et al. Lymphoid follicle destruction and immunosuppression after repeated CpG oligodeoxynucleotide administration. Nat Med 2004, 10:187-192.