Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions

Journal of Leukocyte Biology

Volumn 73, Issue 6, 2003, Pages 781-792

  Marshall, Jason D ^a   Fearon, Karen ^a   Abbate, Christi ^a   Subramanian, Sandhya ^a   Yee, Priscilla ^a   Gregorio, Josh ^a   Coffman, Robert L ^a   Van Nest, Gary ^a  

^a Dynavax Technologies Corporation   (United States)

Author keywords

Cytokines; Human

Indexed keywords

ALPHA INTERFERON; ANTIGEN; C 274; C 405; C 582; C 583; C 593; C 594; C 595; C 630; C 631; C 633; C 637; C 640; C 642; C 644; C 646; C 661; CYTOKINE; D 19; DNA; GAMMA INTERFERON; GUANOSINE DERIVATIVE; IMMUNOSTIMULATING AGENT; OLIGODEOXYRIBONUCLEOTIDE; C274 OLIGONUCLEOTIDE; CHEMOKINE; CPG OLIGONUCLEOTIDE; CPG-OLIGONUCLEOTIDE; IMMUNOLOGICAL ADJUVANT; LEUKOCYTE ANTIGEN; MESSENGER RNA; OLIGONUCLEOTIDE;

ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL STIMULATION; CHIMERA; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DNA SEQUENCE; DRUG ACTIVITY; DRUG IDENTIFICATION; DRUG POTENCY; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; KINETICS; LYMPHOCYTE PROLIFERATION; MOLECULAR RECOGNITION; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN INDUCTION; PROTEIN MOTIF; STRUCTURE ACTIVITY RELATION; B LYMPHOCYTE; BIOSYNTHESIS; CELL CULTURE; CHEMISTRY; CLASSIFICATION; DRUG EFFECT; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MONONUCLEAR CELL; NUCLEOTIDE SEQUENCE;

ADJUVANTS, IMMUNOLOGIC; ANTIGENS, CD; B-LYMPHOCYTES; BASE SEQUENCE; CELLS, CULTURED; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION; INTERFERON TYPE II; INTERFERON-ALPHA; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; OLIGODEOXYRIBONUCLEOTIDES; OLIGONUCLEOTIDES; RNA, MESSENGER;

EID: 0038341916     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1202630     Document Type: Article

References (62)

1. Imler, J., Hoffmann, J. A. (2001) Toll receptors in innate immunity. Trends Cell Biol. 11, 304-311.
2. Medzhitov, R. (2001) Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135-145.
3. Medzhitov, R., Janeway, C. (2000) The toll receptor family and microbial recognition. Trends Microbiol. 8, 452-456.
4. Schnare, M., Barton, G. M., Holt, A. C., Takeda, K., Akira, S., Medzhitov, R. (2001) Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2, 917-950.
5. Akira, S., Takeda, K., Kaisho, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680.
6. Gilliet, M., Boonstra, A., Paturel, C., Antonenko, S., Xu, X. L., Trinchieri, G., O'Garra, A., Liu, Y. J. (2002) The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 195, 953-958.
7. Asselin-Paturel, C., Boonstra, A., Dalod, M., Durand, I., Yessaad, N., Dezutter-Dambuyant, C., Vicari, A., O'Garra, A., Biron, C., Briere, F., Trinchieri, G. (2001) Mouse type 1 IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2, 1144-1150.
8. Krug, A., Towarowski, A., Britsch, S., Rothenfusser, S., Hornung, V., Bals, R., Giese, T., Engelmann, H., Endres, S., Krieg, A. M., Hartmann, G. (2001) Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur. J. Immunol. 31, 3026-3037.
9. Zarember, K. A., Godowski, P. J. (2002) Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukoeytes in response to microbes, their products, and cytokines. J. Immunol. 168, 554-561.
10. Bauer, M., Redecke, V., Ellwart, J. W., Scherer, B., Kremer, J. P., Wagner, H., Lipford, G. B. (2001) Bacterial CpG-DNA triggers activation and maturation of human CD11c(-), CD123(+) dendritic cells. J. Immunol. 166, 5000-5007.
11. Klinman, D. M., Barnhart, K. M., Conover, J. (1999) CpG motifs as immune adjuvants. Vaccine, 17, 19-25.
12. Jahn-Schmid, B., Wiedennann, U., Bohle, B., Repa, A., Kraft, D., Ebner, C. (1999) Oligodeoxynucleotides containing CpG motifs modulate the allergic TH2 response of BALB/c mice to Bet v 1, the major birch pollen allergen. J. Allergy Clin. Immunol. 104, 1015-1023.
13. Tighe, H., Takabayashi, K., Schwartz, D., Marsden, R., Beck, L., Corbeil, J., Richman, D. D., Eiden Jr., J. J., Spiegelberg, H. L., Raz, E. (2000) Conjugation of protein to immunoslimulatory DNA results in a rapid, long-lasting and potent induction of cell-mediated and humoral immunity. Eur. J. Immunol. 30, 1939-1947.
14. Cho, H. J., Takabayashi, K., Cheng, P. M., Nguyen, M. D., Corr, M., Tuck, S., Raz, E. (2000) Immunostimulatory DNA-based vaccine induce cytotoxic lymphocyte activity by a T-helper cell-independent mechanism. Nat. Biotechnol. 18, 509-514.
15. Shirola, H., Sano, K., Kikuchi, T., Tamura, G., Shirato, K. (2000) Regulation of murine airway eosinophilia and Th2 cells by antigen-conjugated CpG oligodeoxynucleotides as a novel antigen-specific immunomodulator. J. Immunol. 164, 5575-5582.
16. Klinman, D. M., Conover, J., Coban, C. (1999) Repeated administration of synthetic oligodeoxynucleotides expressing CpG motifs provides long-term protection against bacterial infection. Infect. Immun. 67, 5658-5663.
17. Sur, S., Wild, J. S., Choudhury, B. K., Sur, N., Alam, R., Klinman, D. M. (1999) Long term prevention of allergic lung inflammation in a mouse model of asthma by CpG oligodeoxynucleotides. J. Immunol. 162, 6284-6293.
18. Magone, M. T., Chan, C. C., Beck, L., Whitcup, S. M., Raz, E. (2000) Systemic or mucosal administration of immunostimulatory DNA inhibits early and late phases of murine allergic conjunctivitis. Eur. J. Immunol. 30, 1841-1850.
19. Kawarada, Y., Ganss, R., Garbi, N., Sacher, T., Arnold, B., Hammerling, G. J. (2001) NK- and CD8(+) T cell-mediated cradication of established tumors by peritumoral injection of CpG-containing oligodeoxynucleotides. J. Immunol. 167, 5247-5253.
20. Kranzer, K., Bauer, M., Lipford, G. B., Heeg, K., Wagner, H., Lang, R. (2000) CpG-oligodeoxynucleotides enhance T-cell receptor-triggered intefferon-gamma production and up-regulation of CD69 via induction of antigen-presenting cell-derived interferon type 1 and interleukin-12. Immunology 99, 170-178.
21. Krug, A., Rothenfusser, S., Hornung, V., Jahrsdorfer, B., Blackwell, S., Ballas, Z. K., Endres, S., Krieg, A. M., Hartmann, G. (2001) Identification of CpG oligonucleolide sequences with high induction of IFN-alpha/beta in plasmacytoid dendritic cells. Eur. J. Immunol. 31, 2154-2163.
22. Hartmann, G., Krieg, A. M. (2000) Mechanism and function of a newly identified CpG DNA motif in human primary B cells. J. Immunol. 164, 944-953.
23. Ballas, Z. K., Rasmussen, W. L., Krieg, A. M. (1996) Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleolides and bacterial DNA. J. Immunol. 157, 1840-1845.
24. Hartmann, G., Weiner, G. J., Krieg, A. M. (1999) CpG DNA: a potent signal for growth, activation, and maturation of human dendritic cells. Proc. Natl. Acad. Sci. USA 96, 9305-9310.
25. Bauer, M., Heeg, K., Wagner, H., Lipford, G. B. (1999) DNA activates human immune cells through a CpG sequence-dependent manner. Immunology 97, 699-705.
26. Fujieda, S., Iho, S., Kimura, Y., Yamamoto, H., Igawa, H., Saito, H. (2000) Synthetic oligodeoxynucleotides inhibit IgE induction in human lymphocytes. Am. J. Respir. Crit. Care Med. 162, 232-239.
27. Krieg, A. M. (2002) CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20, 709-760.
28. Verthelyi, D., Ishii, K. J., Gursel, M., Takeshita, F., Klinman, D. M. (2001) Human peripheral blood cells differentially recognize and respond to two distinct CpG motifs. J. Immunol. 166, 2372-2377.
29. Verthelyi, D., Kenney, R. T., Seder, R. A., Gam, A. A., Friedag, B., Klinman, D. M. (2002) CpG oligodeoxynucleotides as vaccine adjuvants in primates. J. Immunol. 168, 1659-1663.
30. Hornung, V., Rothenfusser, S., Britsch, S., Krug, A., Jahrsdorfer, B., Giese, T., Endres, S., Hartmann, G. (2002) Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleolides. J. Immunol. 168, 4531-4537.
31. Yamamoto, S., Yamamoto, T., Iho, S., Tokunaga, T. (2000) Activation of NK cell (human and mouse) by immunostimulatory DNA sequence. Springer Semin. Immunopathol. 22, 35-43.
32. Williamson, J. R., Raghuraman, M. K., Cech, T. R. (1989) Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell 59, 871-880.
33. Lee, S. W., Song, M. K., Baek, K. H., Park, Y., Kim, J. K., Lee, C. H., Cheong, H. K., Cheong, C., Sung, Y. C. (2000) Effects of a hexameric deoxyriboguanosine run conjugation into CpG oligodeoxynucleotides on their immunostimulatory potentials. J. Immunol. 165, 3631-3639.
34. Gursel, M., Verthelyi, D., Gursel, I., Ishii, K. J., Klinman, D. M. (2002) Differential and competitive activation of human immune cells by distinct classes of CpG oligodeoxynucleotide. J. Leukoc. Biol. 71, 813-820.
35. Gursel, M., Verthelyi, D., Klinman, D. M. (2002) CpG oligodeoxynucleotides induce human monocytes to mature into functional dendritic cells. Eur. J. Immunol. 32, 2617-2622.
36. Tang, J. Y., Han, Y., Tang, J. X., Zhang, Z. (2000) Large-scale synthesis of oligonucleotide phosphorothioates using 3-amino-1,2,4-dithiazole-5-thione as an efficient sulfur-transfer reagent. Org. Proc. Res. Dev. 4, 194-198.
37. Zon, G. (1993) Oligonucleoside phosphorothioates. In Protocols for Oligonucleotides and Analogs (S. Agrawal, ed.), Totowa, NJ, Humana, 172-174.
38. Preneta, A. Z. (1989) Separation on the basis of size: gel permeation chromatography. In Protein Purification Methods, a Practical Approach (E. L. V. Harris, S. Angal, eds.), New York, NY, Oxford University Press, 293-306.
39. Broide, D. H., Stachnick, G., Castaneda, D., Nayar, J., Miller, M., Cho, J. Y., Roman, M., Zubeldia, J., Hyashi, T., Raz, E. (2001) Systemic administration of immunostimulatory DNA sequences mediates reversible inhibition of Th2 responses in a mouse model of asthma. J. Clin. Immunol. 21, 175-182.
40. Zhu, F. G., Reich, C. F., Piselsky, D. S. (2001) The role of the macrophage scavenger receptor in immune stimulation by bacterial DNA and synthetic oligonucleotides. Immunology 103, 226-234.
41. Hardin, C. C., Henderson, E., Watson, T., Prosser, J. K. (1991) Monovalent cation induced structural transitions in telomeric DNAs: G-DNA folding intermediates. Biochemistry 30, 4460-4472.
42. Marathias, V. M., Bolton, P. H. (1999) Determinants of DNA quadruplex structural type: sequence and potassium binding. Biochemistry 38, 4355-4364.
43. Klinman, D. M., Takeshita, F., Gursel, I., Leifer, C., Ishii, K. J., Verthelyi, D., Gursel, M. (2002) CpG DNA: recognition by and activation of monocytes. Microbes Infect. 4, 897-901.
44. Yamamoto, S., Yamamoto, T., Tokunaga, T. (2000) Oligodeoxyribonucleotides with 5′-ACGT-3′ or 5′-TCGA-3′ sequence induce production of interferons. Curr. Top. Microbiol. Immunol. 247, 23-39.
45. Yamamoto, T., Yamamoto, S., Kataoka, T., Komuro, K., Kohase, M., Tokunaga, T. (1994) Synthetic oligonucleotides with certain palindromes stimulate interferon production of human peripheral blood lymphocytes in vitro. Jpn. J. Cancer Res. 85, 775-779.
46. Kadowaki, N., Antonenko, S., Liu, Y. J. (2001) Distinct CpG DNA and polyinosinic-polycytidylic acid double-stranded RNA, respectively, stimulate CD11c(-) type 2 dendritic cell precursors and CD11c(+) dendritic cells to produce type I IFN. J. Immunol. 166, 2291-2295.
47. Hartmann, G., Weeratna, R. D., Ballas, Z. K., Payette, P., Blackwell, S., Suparlo, I., Rasmussen, W. L., Waldschmidt, M., Sajuthi, D., Purcell, R. H., Davis, H. L., Krieg, A. M. (2000) Delineation of a CpG phosphorothioate oligodeoxynucleotide for activating primate immune responses in vitro and in vivo. J. Immunol. 164, 1617-1624.
48. Krieg, A. M. (1999) Mechanisms and applications of immune stimulatory CpG oligodeoxynucleotides. Biochim. Biophys. Acta 1489, 107-116.
49. Zhao, H., Cheng, S. H., Yew, N. S. (2000) Requirements for effective inhibition of immunostimulatory CpG motifs by neutralizing motifs. Antisense Nucleic Acid Drug Dev. 10, 381-389.
50. Jarrossay, D., Napolitani, G., Colonna, M., Sallusto, F., Lanzavecchia, A. (2001) Specialization and complementarily in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur. J. Immunol. 31, 3388-3393.
51. Krieg, A. M., Wu, T., Weeratna, R., Efler, S. M., Love-Homan, L., Yang, L., Yi, A. K., Short, D., Davis, H. L. (1998) Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs. Proc. Natl. Acad. Sci. USA 95, 12631-12636.
52. Ahmad-Nejad, P., Hacker, H., Rutz, M., Bauer, S., Vabulas, R. M., Wagner, H. (2002) Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur. J. Immunol. 32, 1958-1968.
53. Dalpke, A. H., Zimmermann, S., Albrecht, I., Heeg, K. (2002) Phosphodiester CpG oligonucleotides as adjuvants: polyguanosine runs enhance cellular uptake and improve immunostimulative activity of phosphodiester CpG oligonucleotides in vitro and in vivo. Immunology 106, 102-112.
54. Yu, D., Zhu, F., Bhagat, L., Wang, H., Kandimalla, E., Zhang, R., Agrawal, S. (2002) Potent CpG oligonucleotides containing phosphodiester linkages: in vitro and in vivo immunostimulatory properties. Biochem. Biophys. Res. Commun. 297, 83-90.
55. Hafner, M., Zawatzky, R., Hirtreiter, C., Buurman, W. A., Echtenacher, B., Hehlgans, T., Mannel, D. N. (2001) Antimetastatic effect of CpG DNA mediated by type I IFN. Cancer Res. 61, 5523-5528.
56. Zwaveling, S., Ferreira Mota, S. C., Nouta, J., Johnson, M., Lipford, G. B., Offringa, R., van der Burg, S. H., Melief, C. J. (2002) Established human papillomavirus type 16-expressing tumors are effectively eradicated following vaccination with long peptides. J. Immunol. 169, 350-358.
57. Davis, H. L., Suparto, I. I., Weeratna, R. R., Jumintarto, Iskandriati, D. D., Chamzah, S. S., Ma'ruf, A. A., Nente, C. C., Pawitri, D. D., Krieg, A. M., Heriyanto, Smits, W., Sajuthi, D. D. (2000) CpG DNA overcomes hyporesponsiveness to hepatitis B vaccine in orangutans. Vaccine 18, 1920-1924.
58. Gierynska, M., Kumaraguru, U., Eo, S. K., Lee, S., Krieg, A., Rouse, B. T. (2002) Induction of CD8 T-cell-specific systemic and mucosal immunity against herpes simplex virus with CpG-peptide complexes. J. Virol. 76, 6568-6576.
59. Lipford, G. B., Sparwasser, T., Zimmermann, S., Heeg, K., Wagner, H. (2000) CpG-DNA-mediated transient lymphadenopathy is associated with a state of Th1 predisposition to antigen-driven responses. J. Immunol. 165, 1228-1235.
60. Freidag, B. L., Melton, G. B., Collins, F., Klinman, D. M., Cheever, A., Stobie, L., Suen, W., Seder, R. A. (2000) CpG oligodeoxynucleotides and interleukin-12 improve the efficacy of Mycobacterium bovis BCG vaccination in mice challenged with M. tuberculosis. Infect. Immun. 68, 2948-2953.
61. Dieudonne, F., Vital Durand, D., Eiden, J., Tuck, S., Van Nest, G., Hamilton, R., Creticos, P. S., Andre, C. (2001) ISS linked to Amb a 1 allergen (AIC) stimulates IgG response to Amb a 1 by ragweed-allergic humans. J. Allergy Clin. Immunol. 107, 933.
62. Halperin, S. A., Van Nest, G., Smith, B., Abtahi, S., Whiley, H., Eiden, J. J. (2003) A phase I study of the safety and immunogenicity of recombinant hepatitis B surface antigen co-administered with an immunostimmulatory phosphorothioate oligonucleotide adjuvant. Vaccine, in press.