A novel class of immune-stimulatory cpg oligodeoxynucleotides unifies high potency in type i interferon induction with preferred structural properties

Oligonucleotides

Volumn 20, Issue 2, 2010, Pages 93-101

  Samulowitz, Ulrike ^a   Weber, Markus ^a   Weeratna, Risini ^a   Uhlmann, Eugen ^a   Noll, Bernhard ^a,b   Krieg, Arthur M ^a   Vollmer, Jörg ^a  

^a PFIZER INC   (United States)

^b Roche Kulmbach GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; DIMER; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 6; MONOMER; PLACEBO; TOLL LIKE RECEPTOR 9;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG DOSE COMPARISON; HUMAN; HUMAN CELL; IMMUNOMODULATION; INTERFERON INDUCTION; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; BASE SEQUENCE; CELL LINE; CHROMATOGRAPHY, GEL; CPG ISLANDS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNE SYSTEM; INTERFERON TYPE I; MICE; MICE, INBRED BALB C; OLIGODEOXYRIBONUCLEOTIDES;

EID: 77951969254     PISSN: 15454576     EISSN: None     Source Type: Journal    
DOI: 10.1089/oli.2009.0210     Document Type: Article

References (36)

1. ABEL, K., WANG, Y., FRITTS, L., SANCHEZ, E., CHUNG, E., FITZGERALD-BOCARSLY, P., KRIEG, A.M., and MILLER, C.J. (2005). Deoxycytidyl-deoxyguanosine oligonucleotide classes A, B, and C induce distinct cytokine gene expression patterns in rhesus monkey peripheral blood mononuclear cells and distinct alpha interferon responses in TLR9-expressing rhesus monkey plasmacytoid dendritic cells. Clin. Diagn. Lab. Immunol. 12, 606-621.
2. BAUER, S., KIRSCHNING, C.J., HACKER, H., REDECKE, V., HAUSMANN, S., AKIRA, S., WAGNER, H., and LIPFORD, G.B. (2001). Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U. S. A. 98, 9237-9242.
3. COOPER, C.L., AHLUWALIA, N.K., EFLER, S.M., VOLLMER, J., KRIEG, A.M., and DAVIS, H.L. (2008). Immuno-stimulatory effects of three classes of CpG oligodeoxy-nucleotides on PBMC from HCV chronic carriers. J. Immune Based Ther. Vaccines 6, 3-11.
4. COSTA, L.T., KERKMANN, M., HARTMANN, G., ENDRES, S., BISCH, P.M., HECKL, W.M., and THALHAMMER, S. (2004). Structural studies of oligonucleotides containing G-quadruplex motifs using AFM. Biochem. Biophys. Res. Commun. 313, 1065-1072.
5. DONHAUSER, N., HELM, M., PRITSCHET, K., SCHUSTER, P., RIES, M., KORN, K., VOLLMER, J., and SCHMIDT, B. (2010). Differential effects of P-class versus other CpG oligodeoxy-nucleotide classes on the impaired innate immunity of plas-macytoid dentritic cells in HIV type 1 infection. AIDS Res. Hum. Retroviruses 26, 161-171
6. FORSBACH, A., NEMORIN, J., VOLP, K., SAMULOWITZ, U., MONTINO, C., MULLER, C., TLUK, S., HAMM, S., BAUER, S., LIPFORD, G., and VOLLMER, J. (2007). Characterization of conserved viral leader RNA sequences that stimulate innate immunity through TLRs. Oligonucleotides 17, 405-417.
7. GURSEL, M., VERTHELYI, D., GURSEL, I., ISHII, K.J., and KLINMAN, D.M. (2002). Differential and competitive activation of human immune cells by distinct classes of CpG oligodeoxynucleotide. J. Leukoc. Biol. 71, 813-820.
8. HARTMANN, G., BATTIANY, J., POECK, H., WAGNER, M., KERKMANN, M., LUBENOW, N., ROTHENFUSSER, S., and ENDRES, S. (2003). Rational design of new CpG oligonucle-otides that combine B cell activation with high IFN-A induction in plasmacytoid dendritic cells. Eur. J. Immunol. 33, 1633-1641.
9. HEMMI, H., TAKEUCHI, O., KAWAI, T., KAISHO, T., SATO, S., SANJO, H., MATSUMOTO, M., HOSHINO, K., WAGNER, H., TAKEDA, K., and AKIRA, S. (2000). A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
10. HONDA, K., OHBA, Y., YANAI, H., NEGISHI, H., MIZUTA-NI, T., TAKAOKA, A., TAYA, C., and TANIGUCHI, T. (2005). Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434, 1035-1040.
11. HONDA, K., YANAI, H., MIZUTANI, T., NEGISHI, H., SHIMA-DA, N., SUZUKI, N., OHBA, Y., TAKAOKA, A., YEH, W.C., and TANIGUCHI, T. (2004). Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. U. S. A. 101, 15416-15421.
12. JURK, M., KRITZLER, A., DEBELAK, H., VOLLMER, J., KRIEG, A.M., and UHLMANN, E. (2006). Structure-activity relationship studies on the immune stimulatory effects of base-modified CpG toll-like receptor 9 agonists. Chem. Med. Chem. 1, 1007-1014.
13. JURK, M., SCHULTE, B., KRITZLER, A., NOLL, B., UHL-MANN, E., WADER, T., SCHETTER, C., KRIEG, A.M., and VOLLMER, J. (2004). C-Class CpG ODN: sequence requirements and characterization of immunostimulatory activities on mRNA level. Immunobiology 209, 141-154.
14. KERKMANN, M., COSTA, L.T., RICHTER, C., ROTHEN-FUSSER, S., BATTIANY, J., HORNUNG, V., JOHNSON, J., ENGLERT, S., KETTERER, T., HECKL, W., THALHAM-MER, S., ENDRES, S., and HARTMANN, G. (2005). Spontaneous formation of nucleic acid-based nanoparticles is responsible for high interferon-alpha induction by CpG-A in plasmacytoid dendritic cells. J. Biol. Chem. 280, 8086-8093.
15. KERKMANN, M., LOCHMANN, D., WEYERMANN, J., MARSCHNER, A., POECK, H., WAGNER, M., BATTIANY, J., ZIMMER, A., ENDRES, S., and HARTMANN, G. (2006). Immunostimulatory properties of CpG-oligonucleotides are enhanced by the use of protamine nanoparticles. Oligonu-cleotides 16, 313-322.
16. KLASCHIK, S., TROSS, D., and KLINMAN, D.M. (2009). Inductive and suppressive networks regulate TLR9-dependent gene expression in vivo. J. Leukoc. Biol. 85, 788-795.
17. KLINMAN, D.M., and CURRIE, D. (2003). Hierarchical recognition of CpG motifs expressed by immunostimulatory oli-godeoxynucleotides. Clin. Exp. Immunol. 133, 227-232.
18. KRIEG, A.M. (2002). CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20, 709-760.
19. KRIEG, A.M. (2003). CpG DNA: trigger of sepsis, mediator of protection, or both? Scand. J. Infect. Dis. 35, 653-659.
20. KRIEG, A.M., GUGA, P., and STEC, W. (2003). P-chirality-dependent immune activation by phosphorothioate CpG oligodeoxynucleotides. Oligonucleotides 13, 491-499.
21. KRIEG, A.M., YI, A.K., MATSON, S., WALDSCHMIDT, T.J., BISHOP, G.A., TEASDALE, R., KORETZKY, G.A., and KLINMAN, D.M. (1995). CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374, 546-549.
22. KRUG, A., ROTHENFUSSER, S., HORNUNG, V., JAHRSDOR-FER, B., BLACKWELL, S., BALLAS, Z.K., ENDRES, S., KRIEG, A.M., and HARTMANN, G. (2001). Identification of CpG oligonucleotide sequences with high induction of IFN-alpha=beta in plasmacytoid dendritic cells. Eur. J. Immunol. 31, 2154-2163.
23. LEVIN, A.A., MONTEITH, J.M., LEEDS, J.M., NICKLIN, P.L., GEARY, R.S., BUTLER, M., TEMPLIN, M.V., and HENRY, S.P. (1998). Toxicity of oligodeoxynucleotide therapeutics. In: CROOKE, S.T. (ed.). Antisense Research and Application, Berlin: Springer, pp. 169-216.
24. MARSHALL, J.D., FEARON, K., ABBATE, C., SUB-RAMANIAN, S., YEE, P., GREGORIO, J., COFFMAN, R.L., and VAN NEST, G. (2003). Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J. Leukoc. Biol. 73, 781-792.
25. MARSHALL, J.D., FEARON, K.L., HIGGINS, D., HESSEL, E.M., KANZLER, H., ABBATE, C., YEE, P., GREGORIO, J., CRUZ, T.D., LIZCANO, J.O., ZOLOTOREV, A., MCCLURE, H.M., BRASKY, K.M., MURTHY, K.K., COFFMAN, R.L., and NEST, G.V. (2005). Superior activity of the type C class of ISS in vitro and in vivo across multiple species. DNA Cell. Biol. 24, 63-72.
26. MARTINSON, J.A., TENORIO, A.R., MONTOYA, C.J., AL HARTHI, L., GICHINGA, C.N., KRIEG, A.M., BAUM, L.L., and LANDAY, A.L. (2007). Impact of class A, B and C CpG-oligodeoxynucleotides on in vitro activation of innate immune cells in human immunodeficiency virus-1 infected individuals. Immunology 120, 526-535.
27. SACHDEVA, N., ASTHANA, V., BREWER, T.H., GARCIA, D., and ASTHANA, D. (2008). Impaired restoration of plasma-cytoid dendritic cells in HIV-1-infected patients with poor CD4 T cell reconstitution is associated with decrease in capacity to produce IFN-alpha but not proinflammatory cyto-kines. J. Immunol. 181, 2887-2897.
28. VERTHELYI, D., ISHII, K.J., GURSEL, M., TAKESHITA, F., and KLINMAN, D.M. (2001). Human peripheral blood cells differentially recognize and respond to two distinct CPG motifs. J. Immunol. 166, 2372-2377.
29. VICARI, A.P., SCHMALBACH, T., LEKSTROM-HIMES, J., MORRIS, M.L., AL ADHAMI, M.J., LAFRAMBOISE, C., LEESE, P., KRIEG, A.M., EFLER, S.M., and DAVIS, H.L. (2007). Safety, pharmacokinetics and immune effects in normal volunteers of CPG 10101 (ACTILON), an investigational synthetic Toll-like receptor 9 agonist. Antivir. Ther. 12, 741-751.
30. VOLLMER, J. (2006a). CpG motifs to modulate innate and adaptive immune responses. Int. Rev. Immunol. 25, 125-134.
31. VOLLMER, J. (2006b). TLR9 in health and disease. Int. Rev. Immunol. 25, 155-181.
32. VOLLMER, J., and KRIEG, A. (2007). Mechanisms and therapeutic applications of immune modulatory oligodeox-ynucleotide and oligoribonucleotide ligands for toll-like receptors. In: CROOKE, S.T. (ed.). Antisense Drug Technology, Taylor & Francis Group, LLC, Boca Raton, pp. 747-772.
33. VOLLMER, J., and KRIEG, A.M. (2009). Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists. Adv. Drug Deliv. Rev. 61, 195-204.
34. VOLLMER, J., WEERATNA, R., PAYETTE, P., JURK, M., SCHETTER, C., LAUCHT, M., WADER, T., TLUK, S., LIU, M., DAVIS, H.L., and KRIEG, A.M. (2004). Characterization of three CpG oligodeoxynucleotide classes with distinct im-munostimulatory activities. Eur. J. Immunol. 34, 251-262.
35. YASUDA, K., YU, P., KIRSCHNING, C.J., SCHLATTER, B., SCHMITZ, F., HEIT, A., BAUER, S., HOCHREIN, H., and WAGNER, H. (2005). Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and-independent pathways. J. Immunol. 174, 6129-6136.
36. ZWIOREK, K., BOURQUIN, C., BATTIANY, J., WINTER, G., ENDRES, S., HARTMANN, G., and COESTER, C. (2008). Delivery by cationic gelatin nanoparticles strongly increases the immunostimulatory effects of CpG oligonucleotides. Pharm. Res. 25, 551-562.