The immunostimulatory activity of phosphorothioate CpG oligonucleotides is affected by distal sequence changes

Molecular Immunology

Volumn 48, Issue 8, 2011, Pages 1027-1034

  Roberts, Tara L ^a,b   Dunn, Jasmyn A ^a   Sweet, Matthew J ^a   Hume, David A ^c   Stacey, Katryn J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

CpG; Innate immunity; Phosphorothioate oligonucleotides; TLR9

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ARTICLE; CPG ISLAND; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IMMUNOSTIMULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MOTIF; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; CPG ISLANDS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOROTHIOATE OLIGONUCLEOTIDES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME FACTORS;

BACTERIA (MICROORGANISMS);

EID: 79952449379     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.01.011     Document Type: Article

References (39)

1. Ashman R.F., Goeken J.A., Drahos J., Lenert P. Sequence requirements for oligodeoxyribonucleotide inhibitory activity. Int. Immunol. 2005, 17(4):411-420.
2. Bauer S., Kirschning C.J., Hacker H., Redecke V., Hausmann S., Akira S., Wagner H., Lipford G.B. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U.S.A. 2001, 98(16):9237-9242.
3. Brown D.A., Kang S.H., Gryaznov S.M., DeDionisio L., Heidenreich O., Sullivan S., Xu X., Nerenberg M.I. Effect of phosphorothioate modification of oligodeoxynucleotides on specific protein binding. J. Biol. Chem. 1994, 269(43):26801-26805.
4. Costelloe E.O., Stacey K.J., Antalis T.M., Hume D.A. Regulation of the plasminogen activator inhibitor-2 (PAI-2) gene in murine macrophages. Demonstration of a novel pattern of responsiveness to bacterial endotoxin. J. Leukocyte Biol. 1999, 66(1):172-182.
5. Davis H.L., Weeratna R., Waldschmidt T.J., Tygrett L., Schorr J., Krieg A.M. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J. Immunol. 1998, 160(2):870-876.
6. de Jong S.D., Basha G., Wilson K.D., Kazem M., Cullis P., Jefferies W., Tam Y. The immunostimulatory activity of unmethylated and methylated CpG oligodeoxynucleotide is dependent on their ability to colocalize with TLR9 in late endosomes. J. Immunol. 2010, 184(11):6092-6102.
7. 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(4):595-600.
8. Hartmann B., Bertrand H., Fermandjian S. Sequence effects on energetic and structural properties of phosphorothioate DNA: a molecular modelling study. Nucleic Acids Res. 1999, 27(16):3342-3347.
9. Hartmann G., Krieg A.M. Mechanism and function of a newly identified CpG DNA motif in human primary B cells. J. Immunol. 2000, 164(2):944-953.
10. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., Akira S. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408(6813):740-745.
11. Jurk M., Vollmer J. Therapeutic applications of synthetic CpG oligodeoxynucleotides as TLR9 agonists for immune modulation. Biodrugs 2007, 21(6):387-401.
12. Krieg A.M. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 2002, 20:709-760.
13. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., Koretzky G.A., Klinman D.M. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374(6522):546-549.
14. Latz E., Schoenemeyer A., Visintin A., Fitzgerald K.A., Monks B.G., Knetter C.F., Lien E., Nilsen N.J., Espevik T., Golenbock D.T. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 2004, 5(2):190-198.
15. Latz E., Verma A., Visintin A., Gong M., Sirois C.M., Klein D.C., Monks B.G., McKnight C.J., Lamphier M.S., Duprex W.P., Espevik T., Golenbock D.T. Ligand-induced conformational changes allosterically activate Toll-like receptor 9. Nat. Immunol. 2007, 8(7):772-779.
16. Lenert P., Goeken A.J., Ashman R.F. Extended sequence preferences for oligodeoxyribonucleotide activity. Immunology 2006, 117(4):474-481.
17. Manzel L., Macfarlane D.E. Lack of immune stimulation by immobilized CpG-oligodeoxynucleotide. Antisense Nucleic Acid Drug Dev. 1999, 9(5):459-464.
18. Park Y., Lee S.W., Sung Y.C. Cutting Edge: CpG DNA inhibits dendritic cell apoptosis by up-regulating cellular inhibitor of apoptosis proteins through the phosphatidylinositide-3'-OH kinase pathway. J. Immunol. 2002, 168(1):5-8.
19. Roberts T.L., Dunn J.A., Terry T.D., Jennings M.P., Hume D.A., Sweet M.J., Stacey K.J. Differences in macrophage activation by bacterial DNA and CpG-containing oligonucleotides. J. Immunol. 2005, 175(6):3569-3576.
20. Roberts T.L., Idris A., Dunn J.A., Kelly G.M., Burnton C.M., Hodgson S., Hardy L.L., Garceau V., Sweet M.J., Ross I.L., Hume D.A., Stacey K.J. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009, 323(5917):1057-1060.
21. Roberts T.L., Sweet M.J., Hume D.A., Stacey K.J. Cutting edge: species-specific TLR9-mediated recognition of CpG and non-CpG phosphorothioate-modified oligonucleotides. J. Immunol. 2005, 174(2):605-608.
22. Rutz M., Metzger J., Gellert T., Luppa P., Lipford G.B., Wagner H., Bauer S. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 2004, 34(9):2541-2550.
23. Sanjuan M.A., Rao N., Lai K.T., Gu Y., Sun S., Fuchs A., Fung-Leung W.P., Colonna M., Karlsson L. CpG-induced tyrosine phosphorylation occurs via a TLR9-independent mechanism and is required for cytokine secretion. J. Cell. Biol. 2006, 172(7):1057-1068.
24. Sester D.P., Beasley S.J., Sweet M.J., Fowles L.F., Cronau S.L., Stacey K.J., Hume D.A. Bacterial/CpG DNA down-modulates colony stimulating factor-1 receptor surface expression on murine bone marrow-derived macrophages with concomitant growth arrest and factor-independent survival. J. Immunol. 1999, 163(12):6541-6550.
25. Sester D.P., Brion K., Trieu A., Goodridge H.S., Roberts T.L., Dunn J., Hume D.A., Stacey K.J., Sweet M.J. CpG DNA activates survival in murine macrophages through TLR9 and the phosphatidylinositol 3-kinase-Akt pathway. J. Immunol. 2006, 177(7):4473-4480.
26. Sester D.P., Naik S., Beasley S.J., Hume D.A., Stacey K.J. Phosphorothioate backbone modification modulates macrophage activation by CpG DNA. J. Immunol. 2000, 165(8):4165-4173.
27. Stacey K.J., Sester D.P., Sweet M.J., Hume D.A. Macrophage activation by immunostimulatory DNA. Curr. Top. Microbiol. Immunol. 2000, 247:41-58.
28. Stacey K.J., Young G.R., Clark F., Sester D.P., Roberts T.L., Naik S., Sweet M.J., Hume D.A. The molecular basis for the lack of immunostimulatory activity of vertebrate DNA. J. Immunol. 2003, 170(7):3614-3620.
29. Sweet M.J., Campbell C.C., Sester D.P., Xu D., McDonald R.C., Stacey K.J., Hume D.A., Liew F.Y. Colony-stimulating factor-1 suppresses responses to CpG DNA and expression of toll-like receptor 9 but enhances responses to lipopolysaccharide in murine macrophages. J. Immunol. 2002, 168(1):392-399.
30. Sweet M.J., Stacey K.J., Kakuda D.K., Markovich D., Hume D.A. IFN-gamma primes macrophage responses to bacterial DNA. J. Interferon Cytokine Res. 1998, 18(4):263-271.
31. Trieu A., Roberts T.L., Dunn J.A., Sweet M.J., Stacey K.J. DNA motifs suppressing TLR9 responses. Crit. Rev. Immunol. 2006, 26(6):527-544.
32. Tsujimura H., Tamura T., Kong H.J., Nishiyama A., Ishii K.J., Klinman D.M., Ozato K. Toll-like receptor 9 signaling activates NF-kappaB through IFN regulatory factor-8/IFN consensus sequence binding protein in dendritic cells. J. Immunol. 2004, 172(11):6820-6827.
33. Vollmer J., Weeratna R., Payette P., Jurk M., Schetter C., Laucht M., Wader T., Tluk S., Liu M., Davis H.L., Krieg A.M. Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities. Eur. J. Immunol. 2004, 34(1):251-262.
34. Vollmer J., Weeratna R.D., Jurk M., Samulowitz U., McCluskie M.J., Payette P., Davis H.L., Schetter C., Krieg A.M. Oligodeoxynucleotides lacking CpG dinucleotides mediate Toll-like receptor 9 dependent T helper type 2 biased immune stimulation. Immunology 2004, 113(2):212-223.
35. Yamada H., Gursel I., Takeshita F., Conover J., Ishii K.J., Gursel M., Takeshita S., Klinman D.M. Effect of suppressive DNA on CpG-induced immune activation. J. Immunol. 2002, 169(10):5590-5594.
36. Yasuda K., Yu P., Kirschning C.J., Schlatter B., Schmitz F., Heit A., Bauer S., Hochrein H., Wagner H. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 2005, 174(10):6129-6136.
37. Yi A.K., Chace J.H., Cowdery J.S., Krieg A.M. IFN-gamma promotes IL-6 and IgM secretion in response to CpG motifs in bacterial DNA and oligodeoxynucleotides. J. Immunol. 1996, 156(2):558-564.
38. Yi A.K., Krieg A.M. CpG DNA rescue from anti-IgM-induced WEHI-231 B lymphoma apoptosis via modulation of I kappa B alpha and I kappa B beta and sustained activation of nuclear factor-kappa B/c-Rel. J. Immunol. 1998, 160(3):1240-1245.
39. Zhang Z., Weinschenk T., Schluesener H.J. Uptake, cellular distribution and novel cellular binding proteins of immunostimulatory CpG oligodeoxynucleotides in glioblastoma cells. Mol. Cell. Biochem. 2005, 272(1-2):35-46.