Oligodeoxynucleotides containing CpG motifs induce IL-12, IL-18 and IFN-γ production in cells from allergic individuals and inhibit IgE synthesis in vitro

European Journal of Immunology

Volumn 29, Issue 7, 1999, Pages 2344-2353

  Bohle, Barbara ^a   Jahn Schmid, Beatrice ^b   Maurer, Dieter ^a   Kraft, Dietrich ^a   Ebner, Christof ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

CpG motif; Immunomodulation; Specific immunotherapy; Th1 Th2; Type I allergy

Indexed keywords

ALLERGEN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 12; INTERLEUKIN 18; OLIGODEOXYNUCLEOTIDE; OLIGODEOXYNUCLEOTIDE PHOSPHOROTHIOATE;

ALLERGY; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMEDIATE TYPE HYPERSENSITIVITY; IMMUNOGLOBULIN PRODUCTION; IMMUNOTHERAPY; MONONUCLEAR CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; STAINING;

BASE SEQUENCE; CPG ISLANDS; HUMANS; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-18; KILLER CELLS, NATURAL; OLIGODEOXYRIBONUCLEOTIDES; RHINITIS, ALLERGIC, SEASONAL; RNA, MESSENGER; THIONUCLEOTIDES;

EID: 0345120862     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-4141(199907)29:07<2344::AID-IMMU2344>3.0.CO;2-R     Document Type: Article

References (56)

1. Klinman, D., Yi, A.-K., Beaucage, S. L., Conover, J. and Krieg, A. M., CpG motifs expressed by bacterial DNA rapidly induce lymphocytes to secrete IL-6, IL-12 and IFN. Proc. Natl. Acad. Sci. USA 1996. 93: 2879-2883.
2. Roman, M., Martin-Orozco, E., Goodman, J. S., Nguyen, M.-D., Sato, Y., Ronaghy, A., Kronbluth, R. S., Richman, D. D., Carson, D. A. and Raz, E., Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat. Med. 1997. 3: 849-855.
3. Chu, R. S., Targoni, O. S., Krieg, A. M., Lehmann, P. V. and Harding, C. V., CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J. Exp. Med. 1997. 186: 1623-1631.
4. Carson, D. A. and Raz, E., Oligonucleotide adjuvants for T helper 1 (Th1)-specific vaccination. J. Exp. Med. 1997. 186: 1621-1622.
5. Heeg, K., Sparwasser, T., Lipford, G. B., Häcker, H., Zimmermann, S. and Wagner, H., Bacterial DNA as an evolutionary conserved ligand signalling danger of infection to immune cells. Eur. J. Microbiol. Infect. Dis. 1998. 17: 464-469.
6. Yamamoto, S., Yamamoto, T., Kataoka, T., Kuramoto, E., Yano, O. and Tokunaga, T., Unique palindromic sequences in synthetic oligonucleotides are required to induce INF and augment INF-mediated natural killer activity. J. Immunol. 1992. 148: 4072-4076.
7. Lipford, G. B., Bauer, M., Blank, C., Reiter, R., Wagner, H. and Heeg, K., CpG-containing synthetic oligonucleotides promote B and cytotoxic T cell response to protein antigen: a new class of vaccine adjuvants. Eur. J. Immunol. 1997. 27: 2340-2344.
8. Yi, A.-K., Chace, J. H., Cowdery, J. S. and Krieg, A. M., IFN-γ promotes IL-6 and IgM secretion in response to CpG motifs in bacterial DNA and oligodeoxynucleotides. J. Immunol. 1996. 156: 558-564.
9. Sparwasser, T., Miethke, T., Lipford, G., Erdmann, A., Häcker, H., Heeg, K. and Wagner, H., Macrophages sense pathogens via DNA motifs: induction of tumor necrosis factor-oc-mediated shock. Eur. J. Immunol. 1997. 27: 3420-3426.
10. Stacey, K. J., Sweet, M. J. and Hume, D. A., Macrophages ingest and are activated by bacterial DNA. J. Immunol. 1996. 157: 2116-2122.
11. Ballas, Z. K., Wendy, L. R. and 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.
12. Okamura, H., Tsutsul, H., Komatsu, T., Yutsudo, M., Hakura, A., Tanimoto, T., Torigoe, K., Okura, T., Nukada, Y., Hattori, K., Akita, K., Namba, M., Tanabe, F., Konishi, K., Fukuda, S. and Kurimoto, M., Cloning of a new cytokine that induces IFN-γ production by T cells. Nature 1995. 378: 88-91.
13. Sparwasser, T., Koch, E.-S., Vabulas, R. M., Heeg, K., Lipford, G. B., Ellwart, J. W. and Wagner, H., Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 1998. 28: 2045-2054.
14. Krieg, A. M., Yi, A.-K., Matson, S., Waldschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A. and Klinman, D. M., CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995. 374: 546-549.
15. Liang, H., Nishioka, Y., Reich, C. F., Pisetsky, D. S. and Lipsky, P. E., Activation of human B cells by phosphorothioate oligodeoxynucleotides. J. Clin. Invest. 1996. 98: 1119-1129.
16. Kline, J. N., Waldschmidt, T. J., Busigna, T. R., Lemish, J. E., Weinstock, J. V., Thorne, P. S. and Krieg, A. M., Cutting Edge: Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J. Immunol. 1998. 160: 2555-2559.
17. Goodman, J. S., Van Uden, J. H., Kobayashi, H., Broide, D. and Raz, E., DNA immunotherapeutics: new potential treatment modalities for allergic disease. Int. Arch. Allergy Immunol. 1998. 116: 177-187.
18. + T lymphocytes in atopic patients. J. Immunol. 1990. 144: 4651-4656.
19. Romagnani, S., Regulation of the development of type 2 T-helper cells in allergy. Curr. Opin. Immunol. 1994. 6: 838-846.
20. Wüthrich, B., Schindler, C., Leuenberger, P., Ackermann-Liebrich, U. and the SAPALDIA Team, Prevalence of atopy and pollinosis in the adult population of Switzerland (SAPALDIA Study). Int. Arch. Allergy Immunol. 1995. 106: 149-156.
21. Noon, L., Prophylactic inoculation against hay fever. Lancet 1911. 1: 1572-1573.
22. Varney, V. A., Gaga, M., Frew, A. J., Aber, V. R., Kay, A. B. and Durham, S. R., Usefulness of immunotherapy in patients with severe summer hay fever uncontrolled by antiallergic drugs. Br. Med. J. 1991. 302: 265-269.
23. Djurup, R., The subclass and nature of the IgG antibody response in patients undergoing allergen specific immunotherapy. Allergy 1985. 40: 469-486.
24. Ebner, C., Siemann, U., Bohle, B., Willheim, M., Wiedermann, U., Schenk, S., Klotz, F., Ebner, H., Kraft, D. and Scheiner, O., Immunological changes during specific immunotherapy of grass pollen allergy: reduced lymphoproliferative responses to allergen and shift from Th2 to Th 1 in T cell clones specific for PhI p 1, a major grass pollen allergen. Clin. Exp. Allergy 1997. 27: 1007-1015.
25. Akdis, C. A., Blesken, T., Akdis, M., Wüthrich, B. and Blaser, K., The role of IL-10 in specific immunotherapy. J. Clin. Invest. 1998. 102: 98-106.
26. + T cells from allergic individuals is modulated by antigen concentration and antigen-presenting cell type. J. Exp. Med. 1995. 181: 1081-1089.
27. + T lymphocytes and eosinophils in the nasal mucosa and increases the number of cells expressing messenger RNA for interferon-γ. J. Allergy Clin. Immunol. 1996. 97: 1356-1365.
28. Jutel, M., Pichler, W. J., Skrbic, D., Urwyler, A., Dahinden, C. and Mueller, U. R., Bee venom immunotherapy results in decrease of IL-4 and IL-5 and increase of IFN-γ secretion in specific allergen-stimulated T cell cultures. J. Immunol. 1995. 154: 4187-4194.
29. + T cells from allergic individuals. J. Exp. Med. 1993. 178: 2123-2130.
30. Ferreira, F., Hirtenlehner, K., Jilek, A., Godnic-Cvar, J., Breiteneder, H., Grimm, R., Hoffmann-Sommergruber, K., Scheiner, O., Kraft, D., Breitenbach, M., Rheinberger, H. J. and Ebner, C., Dissection of IgE and T lymphocyte reactivity of isoforms of the major birch pollen allergen Bet v 1: Potential use of hypoallergenic isoforms for immunotherapy. J. Exp. Med. 1996. 183: 599-609.
31. Ferreira, F., Ebner, C., Kramer, B., Casari, G., Briza, P., Kungl, A., Grimm, R., Jahn-Schmid, B., Breiteneder, H., Kraft, D., Breitenbach, M., Rheinberger, H. J. and Scheiner, O., Modulation of IgE reactivity of allergens by site-directed mutagenesis: potential use of hypoallergenic variants for immunotherapy. FASEB J. 1998. 12: 231-242.
32. Bousquet, J., Becker, W. M., Hejjaoui, I., Chanel, I., Lebel, B., Dhivert, H. and Michel, F. B., Differences in clinical and immunological reactivity of patients allergic to grass pollen and to multiple-pollen species. II. Efficacy of a double blind placebo controlled, specific immunotherapy with standardized extracts. J. Allergy Clin. Immunol. 1991. 88: 43-53.
33. Ishizaka, K., Regulation of IgE synthesis. Annu. Rev. Immunol. 1984. 2: 159-182.
34. Wiedermann, U., Jahn-Schmid, B., Fritsch, R., Bauer, L., Renz, H., Kraft, D. and Ebner, C., Effects of adjuvants on the immune response to allergens in a murine model of allergen inhalation: cholera toxin induces a Th1-like response to Bet v 1, the major birch pollen allergen. Clin. Exp. Immunol. 1998. 111: 144-151.
35. hO phenotype in vitro by induction of IL-12. Int. Immunol. 1997. 9: 1867-1874.
36. Sun, S., Kishimoto, H. and Sprent, J., DNA as an adjuvant: capacity of insect DNA and synthetic oligodeoxynucleotides to augment T cell responses to specific antigen. J. Exp. Med. 1998. 187: 1145-1150.
37. Klinman, D. M., Barnhart, K. M. and Conover, J., CpG motifs as immune adjuvants. Vaccine 1999. 17: 19-25.
38. Bohle, B., Schwihla, H., Hu, H.-Z., Friedl-Hajek, R., Sowka, S., Ferreira, F., Breiteneder, H., Bruijnzeel-Koomen, C. A. F. M., de Weger, R. A., Mudde, G. C., Ebner, C. and Van Reijsen, F. C., Long-lived Th2 clones specific for seasonal and perennial allergens can be detected in blood and skin by their TCR-hypervariable regions. J. Immunol. 1998. 160: 2022-2027.
39. Leonard, C., Tormey, V., Burke, C. and Poulter, L. W., Allergen-induced cytokine production in atopic disease and its relationship to disease severity. Am. J. Respir. Cell Mol. Biol. 1997. 17: 368-375.
40. Jones, K. P., Morris, R. H., Rolf, S., Whatley, J. and Davies, B. H., The assay of interleukin 4 in the serum of normal subjects and atopic patients using a novel immunoassay. Cytokine 1997. 9: 529-534.
41. Teramoto, T., Fukao, T., Tashita, H., Inoue, R., Kaneko, H., Takemura, M. and Kondo, N., Serum IgE level is negatively correlated with the ability of peripheral blood mononuclear cells to produce interferon gamma (IFNgamma): evidence of reduced expression of IFN-gamma mRNA in atopic patients. Clin. Exp. Allergy 1998. 28: 74-82.
42. Chace, J. H., Hooker, N. A., Mildenstein, K. L., Krieg, A. M. and Cowdery, J. S., Bacterial DNA-induced NK cell IFN-γ production is dependent on macrophage secretion of IL-12. Clin. Immunol. Immunopathol. 1997. 84: 185-193.
43. Geich, G. J., Zimmermann, E. M., Henderson, L. L. and Yunginger, J. W., Effect of immunotherapy on immunoglobulin E and immunoglobulin G antibodies to ragweed antigens: a six-year prospective study. J. Allergy Clin. Immunol. 1982. 70: 261-271.
44. Birkner, T., Rumpold, H., Jarolim, E., Ebner, H., Breitenbach, M., Skvaril, T., Scheiner, O. and Kraft, D., Evaluation of immunotherapy-induced changes in specific IgE, IgG and IgG subclasses in birch pollen allergie patients by means of immunoblotting: correlation with clinical response. Allergy 1990. 45: 418-425.
45. Djurup, R. and Osterballe, O., IgG subclass antibody response in grass pollen-allergic patients undergoing specific immunotherapy. Prognostic value of serum IgG subclass antibody levels early in immunotherapy. Allergy 1984. 39: 433-441.
46. Raz, E., Tighe, H., Sato, Y., Corr, M. P., Dudler, J. A., Roman, M., Swain, S. L., Spiegelberg, H. L. and Carson, C. A., Preferential induction of a Th1 response and inhibition of specific IgE antibody formation by plasmid DNA immunization. Proc. Natl. Acad. Sci. USA 1996. 93: 5141-5145.
47. Slater, J. E., Zhang, Y. J., Arthur-Smith, A. and Colberg-Poley, A., A DNA vaccine inhibits IgE response to the latex allergen Hev b 5 in mice. J. Allergy Clin. Immunol. 1997. 99: 504 (abstract).
48. Hsu, C.-H., Chua, K.-Y., Tao, M.-H., Lai, Y.-L., Wu, H.-D., Huang, S.-K. and Hsieh, K.-H., Immunoprophylaxis of allergen-induced immunoglobulin E synthesis and airway hyperresponsiveness in vivo by genetic immunization. Nat. Med. 1996. 2: 540-544.
49. Hartl, A., Kisslich, J., Weiss, R., Bernhaupt, A., Mostbock, S., Scheiblhofer, S., Ebner, C., Ferreira, F. and Thalhammer, J., Immune responses after immunization with plasmid DNA encoding Bet v 1, the major allergen of birch. J. Allergy Clin. Immunol. 1999. 103: 107-113.
50. Steinberger, P., Bohle, B., di Padova, F., Wrann, M., Liehl, E., Scheiner, O., Kraft, D. and Valenta, R., Allergen-specific IgE production of comitted B cells from allergic patients in vitro. J. Allergy Clin. Immunol. 96: 209-218.
51. Sallusto, F. and Lanzavecchia, A., Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and down-regulated by tumor necrosis factor alpha. J. Exp. Med. 1994. 179: 1109-1118.
52. Romani, N., Gruner, S., Brang, D., Kämpgen, E., Lenz, A., Trockenbacher, B., Konwalinka, G., Fritsch, P. O., Steinman, R. M. and Schuler, G., Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 1994. 180: 83-93.
53. Geissmann, F., Prost, C., Monnet, J. P., Dy, M., Brousse, N. and Hermine, O., Transforming growth factor β1, in the presence of granulocyte/macrophage colony-stimulating factor and interleukin 4, induces differentiation of human peripheral blood monocytes into dendritic Langerhans cells. J. Exp. Med. 1998. 187: 961-966.
54. Chomczynski, P. and Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanatephenol-chloroform extraction. Anal. Biochem. 1987. 162: 156-159.
55. Benjamin, D., Sharma, V, Kubin, M., Klein, J. L., Sartori, A., Holliday, J. and Trinchieri, G., IL-12 expression in AIDS-related lymphoma B cell lines. J. Immunol. 1996. 156: 1626-1637.
56. Jarolim, E., Teijkl, M., Rohac, M., Schlerka, G., Scheiner, O., Kraft, D., Breitenbach, M. and Rumpold, H., Monoclonal antibodies against birch pollen allergens: characterisation by immunoblotting and use for single step affinity purification of the major allergen Bet v I. Int. Arch. Allergy Immunol. 1989. 90: 54-60.