Rapid Immune Activation by CpG Motifs in Bacterial DNA: Systemic Induction of IL-6 Transcription Through an Antioxidant-Sensitive Pathway

Journal of Immunology

Volumn 157, Issue 12, 1996, Pages 5394-5402

  Yi, Ae Kyung ^a   Klinman, Dennis M ^b   Martin, Thomas L ^c   Matson, Sara ^c   Krieg, Arthur M ^a,c  

^a UNIVERSITY OF IOWA   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; BACTERIAL DNA; INTERLEUKIN 6; LYMPHOCYTE ANTIGEN RECEPTOR; REACTIVE OXYGEN METABOLITE;

ANIMAL; ARTICLE; B LYMPHOCYTE; BAGG ALBINO MOUSE; C3H MOUSE; DBA MOUSE; GENETIC TRANSCRIPTION; IMMUNOLOGY; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; STRUCTURE ACTIVITY RELATION; TIME; TISSUE DISTRIBUTION;

ANIMALS; ANTIOXIDANTS; B-LYMPHOCYTES; BASE SEQUENCE; DNA, BACTERIAL; INTERLEUKIN-6; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED DBA; REACTIVE OXYGEN SPECIES; RECEPTORS, ANTIGEN, B-CELL; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS; TISSUE DISTRIBUTION; TRANSCRIPTION, GENETIC;

EID: 0030589385     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (44)

1. Messina, J. P., G. S. Gilkeson, and D. S. Pisetsky. 1991. Stimulation of in vitro murine lymphocyte proliferation by bacterial DNA. J. Immunol. 147:1759.
2. Yamamoto, S., T. Yamamoto, S. Shimada, E. Kuramoto, O. Yano, T. Kataoka, and T. Tokunaga. 1992. DNA from bacteria, but not from vertebrates, induces interferons, activates natural killer cells and inhibits tumor growth. Microbiol. Immunol. 36:983.
3. Razin, A., and J. Friedman. 1981. DNA methylation and its possible biological roles. Prog. Nucleic Acid Res. Mol. Biol. 25:33.
4. Krieg, A. M., A.-K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B cell activation. Nature 374:546.
5. L. J. Immunol. In press.
6. Klinman, D. M., A.-K. Yi, S. L. Beaucage, J. Conover, and A. M. Krieg. 1996. CpG motifs present in bacterial DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon g. Proc. Natl. Acad. Sci. USA 93: 2879.
7. Kishimoto, T. 1989. The biology of interleukin-6. Blood 74:1.
8. Le, J., and J. Vilcek. 1989. Biology of disease. Interleukin 6: a multifunctional cytokine regulating immune reactions and the acute phase protein response. Lab. Invest. 61:588.
9. Hirano, T., S. Akira, T. Taga, and T. Kishimoto. 1990. Biological and clinical aspects of interleukin 6. Immunol. Today 11:443.
10. 2-interferon/B-cell differentiation factor BSF-2 gene expression in human fibroblasts by diacylglycerols and the calcium ionophore A23187. Proc. Natl. Acad. Sci. USA 84:3663.
11. Horii, Y., A. Muraguchi, S. Suematsu, T. Matsuda, K. Yoshizaki, T. Hirano, and T. Kishimoto. 1988. Regulation of BSF-2/IL-6 production by human mononuclear cells: macrophage-dependent synthesis of BSF-2/IL-6 by T cells. J. Immunol. 141:1529.
12. Freeman, G. J., A. S. Freedman, S. N. Rabinowe, J. M. Segil, J. Horowitz, K. Rosen, and J. F. Whitman. 1989. Interleukin-6 gene expression in normal and neoplastic B cells. J. Clin. Invest. 83: 1512.
13. Navarro, S., N. Debili, J.-F. Bernaudin, W. Vainchenter, and J. Doly. 1989. Regulation of the expression of IL-6 in human monocytes. J. Immunol. 142:4339.
14. Muraguchi, A., T. Hirano, B. Tang, T. Matsuda, Y. Hori, K. Nakajima, and T. Kishimoto. 1988. The essential role of B cell stimulatory factor 2 (BSF-2/IL-6) for the terminal differentiation of B cells. J. Exp. Med. 167:332.
15. 2), as a B cell hybridoma/plasmacytoma growth factor induced by interleukin 1 and tumor necrosis factor. J. Exp. Med. 165:914.
16. Uyttenhove, C., P. G. Coulie, and J. Van Snick. 1988. T cell growth and differentiation induced by interleukin-HP1/IL-6, the murine hybridoma/plasmacytoma growth factor. J. Exp. Med. 167:1447.
17. Wong, G. G., J. S. Witek-Giannotti, P. A. Temple, R. Kriz, C. Ferenz, R. M. Hewick, S. C. Clark, K. Ikebuchi, and M. Ogawa. 1988. Stimulation of murine hemopoietic colony formation by human IL-6. J. Immunol. 140:3040.
18. Sachs, L., S. Lotem, and Y. Shabo. 1989. The molecular regulators of macrophage and granulocyte development. Role of MGI-2/IL-6. Ann. NY Acad. Sci. 557:417.
19. Heinrich, P. C., J. V. Castell, and T. Andus. 1990. Interleukin-6 and the acute phase response. Biochem. J. 265:621.
20. Kopf, M., H. Baumann, G. Freer, M. Freudenberg, M. Lamers, T. Kishimoto, R. Zinkernagel, H. Bluethmann, and G. Köhler. 1994. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368:339.
21. Bishop, G. A. 1991. Requirements of class II-mediated B cell differentiation for class II cross-linking and cyclic AMP. J. Immunol. 147:1107.
22. Krieg, A. M., W. C. Cause, M. F. Gourley, and A. D. Steinberg. 1989. A role for endogenous retroviral sequences in the regulation of lymphocyte activation. J. Immunol. 143:2448.
23. 1 mice. J. Clin. Invest. 94:585.
24. Montgomery, R. A., and M. J. Dallman. 1991. Analysis of cytokine gene expression during fetal thymic ontogeny using the polymerase chain reaction. J. Immunol. 147:554.
25. Stoye, J. P., W. N. Frankel, and J. M. Coffin. 1991. DNA hybridization in dried gels with fragmented probes: an improvement over blotting techniques. Techniques 3:123.
26. Pottratz, S. T., T. Bellido, H. Mocharia, D. Crabb, and S. C. Manolagas. 1994. 17B-estradiol inhibits expression of human interleukin-6 promoter-reporter constructs by a receptor-dependent mechanism. J. Clin. Invest. 93:944.
27. Seed, B., and J. Y. Sheen. 1988. A simple phase-extraction assay for chloramphenicol acetyltransferase activity. Gene 76:271.
28. Sen, C. K., and L. Packer. 1996. Antioxidant and redox regulation of gene transcription. FASEB J. 709.
29. Weber, C., W. Erl, A. Pietsch, M. Sträbel, H. W. L. Ziegler-Heitbrock, and P. C. Weber. 1994. Antioxidants inhibit monocyte adhesion by suppressing nuclear factor-κB mobilization and induction of vascular cell adhesion molecule-1 in endothelial cells stimulated to generate radicals. Arterioscler. Thromb. 14:1665.
30. Vowells, S. J., S. Sekhsaria, H. L. Malech, M. Shalit, and T. A. Fleisher. 1995. Flow cytometric analysis of the granulocyte respiratory bust: a comparison study of fluorescent probes. J. Immunol. Methods 178:89.
31. Ray, A., S. B. Tatter, L. T. May, and P. B. Sehgal. 1988. Activation of the human "b2-interferon/hepatocyte-stimutating factor/interleukin 6" promoter by cytokines, viruses, and second messenger agonists. Proc. Natl. Acad. Sci. USA 85: 6701.
32. Cayphas, S., J. van Damme, A. Vink, R. J. Richard, J. Simpson, A. Billiau, and J. van Snick. 1987. Identification of an interleukin HP1-like plasmacytoma growth factor produced by L cells in response to viral infection. J. Immunol. 139:2965.
33. Van Damme, J., M. R. Schaafama, W. E. Fibbe, J. H. F. Falkenburg, G. Opdenakker, and A. Billiau. 1989. Simultaneous production of interleukin 6, interferon-β and colony-stimulating activity by fibroblasts after viral and bacterial infection. Eur. J. Immunol. 19:163.
34. Wollenberg, G., L. E. DeForge, G. Bolgos, and D. G. Remick. 1993. Differential expression of tumor necrosis factor and interleukin-6 by peritoneal macrophages in vivo and in culture. Am. J. Pathol. 143:1121.
35. DeForge, L. E., and D. G. Remick. 1991. Kinetics of TNF, IL-6, and IL-8 gene expression in LPS-stimulated human whole blood. Biochem. Biophys. Res. Com. 174:18.
36. Ng, S. B., Y. H. Tan, and G. R. Guy. 1994. Differential induction of the interleukin-6 gene by tumor necrosis factor and interleukin-1. J. Biol. Chem. 269: 19021.
37. Emlen, W., and M. Mannik. 1978. Kinetics and mechanisms for removal of circulating single-stranded DNA in mice. J. Exp. Med. 147:684.
38. Emlen, W., and M. Mannik. 1984. Effect of DNA size and strandedness on the in vivo clearance and organ localization of DNA. Clin. Exp. Immunol. 56:185.
39. Cowdery, J. S., J. H. Chace, A.-K. Yi, and A. M. Krieg. 1996. Bacterial DNA induces NK cells to produce IFN-g in vivo and increases the toxicity of lipopolysaccharides. J. Immunol. 156:4570.
40. Hirano, T., T. Teranishi, B. H. Lin, and K. Onoue. 1984. Human helper T cell factor(s). IV. Demonstration of a human late-acting B cell differentiation factor acting on Staphylococcus aureus Cowan I-stimulated B cells. J. Immunol. 133: 798.
41. Nakagawa, T., N. Nakagawa, H. Goldstein, D. J. Volkman, and A. S. Fauci. 1986. Demonstration that human B cells respond differently to interleukin 2 and B cell differentiation factor based on their stages of maturation. J. Immunol. 137:3175.
42. Muraguchi, A., T. Hirano, B. Tang, T. Matsuda, Y. Horii, K. Nakajima, and T. Kishimoto. 1988. The essential role of B cell stimulatory factor 2 (BSF-2/IL-6) for the terminal differentiation of B cells. J. Exp. Med. 167:332.
43. Van Snick, J. 1990. Interleukin-6: an overview. Annu. Rev. Immunol. 8:253.
44. Lotz, M. 1993. Interleukin-6. Cancer Invest. 11:732.