CpG-DNA-induced IFN-α production involves p38 MAPK-dependent STAT1 phosphorylation in human plasmacytoid dendritic cell precursors

Journal of Leukocyte Biology

Volumn 72, Issue 5, 2002, Pages 1011-1019

  Takauji, Rumiko ^a   Iho, Sumiko ^a   Takatsuka, Hisakazu ^a   Yamamoto, Saburo ^b   Takahashi, Takayuki ^c   Kitagawa, Harukazu ^d   Iwasaki, Hiromichi ^a   Iida, Reiko ^a   Yokochi, Takashi ^e   Matsuki, Takasumi ^a  

^a UNIVERSITY OF FUKUI   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c KOBE CITY MEDICAL CENTER GENERAL HOSPITAL   (Japan)

^d Chemicals Development Group   (Japan)

^e AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

IRF 7; IRF 9; STAT2; TLR 9

Indexed keywords

ALPHA INTERFERON; CD4 ANTIGEN; DNA; GENE PRODUCT; GLYCOPROTEIN P 15095; INTERFERON REGULATORY FACTOR 7; INTERFERON REGULATORY FACTOR 9; INTERFERON STIMULATED GENE FACTOR 3; MITOGEN ACTIVATED PROTEIN KINASE; OLIGODEOXYRIBONUCLEOTIDE; SERINE PROTEINASE; STAT1 PROTEIN; STAT2 PROTEIN; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL INFECTION; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; CPG ISLAND; DENDRITIC CELL; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INHIBITION KINETICS; INTERFERON PRODUCTION; MOLECULAR MECHANICS; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; STEM CELL; TRANSCRIPTION REGULATION; VIRUS INFECTION;

CELL NUCLEUS; CELLS, CULTURED; DENDRITIC CELLS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; INTERFERON-ALPHA; INTERFERON-STIMULATED GENE FACTOR 3; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; KINETICS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, IMMUNOLOGICAL; OLIGODEOXYRIBONUCLEOTIDES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RNA, MESSENGER; SERINE; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR; STEM CELLS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TYROSINE;

BACTERIA (MICROORGANISMS);

EID: 0036855470     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (43)

1. Medzhitov, R., Janeway Jr., C. A. (1997) Innate immunity: The virtues of a nonclonal system of recognition. Cell 91, 295-298.
2. Banchereau, J., Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252.
3. Kadowaki, N., Antonenko, S., Lau, J. Y-N., Liu, Y-J. (2000) Natural interferon α/β-producing cells link innate and adaptive immunity. J. Exp. Med. 192, 219-225.
4. Sparwasser, T., Koch, E. S., Vabulas, R. M., Heeg, K., Lipford, G. B., Ellwart, J. W., Wagner, H. (1998) Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur. J. Immunol. 28, 2045-2054.
5. Haker, H., Mischak, H., Miethke, T., Liptay, S., Schmid, R., Sparwasser, T., Heeg, K., Lipford, G. B., Wagner H. (1998) CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 17, 6230-6240.
6. Häcker, H., Mischak, H., Häcker, G., Eser, S., Prenzel, N., Ullrich, A., Wagner, H. (1999) Cell type-specific activation of mitogen-activated protein kinases by CpG-DNA controls interleukin-12 release from antigen-presenting cells. EMBO J. 18, 6973-6982.
7. Behboudi, S., Chao, D., Klenerman, P., Austyn J. (2000) The effects of DNA containing CpG motif on dendritic cells. Immunology 99, 361-366.
8. Chu, R. S., Targoni, O. S., Krieg, A. M., Lehmann, P. V., Harding, C. V. (1997) CpG oligodeoxynucleotides act as adjuvants that switch on T helper (Th1) immunity. J. Exp. Med. 186, 1623-1631.
9. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
10. Häcker, H., Vabulas, R. M., Takeuchi, O., Hoshino, K., Akira, S., Wagner, H. (2000) Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF)6. J. Exp. Med. 192, 595-600.
11. 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.
12. Cella, M., Jarrossay, D., Facchetti, F., Alebardi, O., Nakajima, H., Lanzavecchia, A., Colonna, M. (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5, 919-923.
13. Siegal, F. P., Kadowaki, N., Schodell, M., Fitzgerald-Bocarsly, P. A., Shah, K., Ho, S., Antonenko, S., Liu, Y-J. (1999) The nature of the principal type 1 interferon-producing cells in human blood. Science 284, 1835-1837.
14. + dendritic cells to produce type I interferon. J. Immunol. 166, 2291-2295.
15. + dendritic cells. J. Immunol. 166, 5000-5007.
16. 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.
17. Iho, S., Yamamoto, T., Takahashi, T., Yamamoto, S. (1999) Oligodeoxynucleotides containing palindrome sequences with internal 5′-CpG-3′ act directly on human NK and activated T cells to induce IFN-γ production in vitro. J. Immunol. 163, 3642-3652.
18. Kuramoto, E., Yano, O., Kimura, Y., Baba, M., Makino, T., Yamamoto, S., Yamamoto, T., Kataoka, T., Tokunaga, T. (1992) Oligonucleotide sequences required for natural killer cell activation. Jpn. J. Cancer Res. 83, 1128-1131.
19. Hartmann, G., Weeratna, R. D., Ballas, Z. K., Payette, P., Blackwell, S., Suparto, 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.
20. Ballas, Z. K., Rasmussen, W. L., Krieg, A. M. (1996) Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J. Immunol. 157, 1840-1845.
21. Dzionek, A., Fuchs, A., Schmidt, P., Cremer, S., Zysk, M., Miltenyi, S., Buck, D. W., Schmitz. J. (2000) BDCA-2, BDCA-3, and BDCA-4: Three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165, 6037-6046.
22. Kumar, S., Jiang, M. S., Adams, J. L., Lee, J. C. (1999) Pyridinylimidazole compound SB 203580 inhibits the activity but not the activation of p38 mitogen-activated protein kinase. Biochem. Biophys. Res. Commun. 263, 825-831.
23. Karahashi, H., Nagata, K., Ishii, K., Amano, F. (2000) A selective inhibitor of p38 MAP kinase, SB202190, induced apoptotic cell death of a lipopolysaccharide-treated macrophage-like cell line, J774.1. Biochim. Biophys. Acta 1502, 207-223.
24. Yeow, W-S., Au, W-C., Juang, Y-T., Fields, C. D., Dent, C. L., Gewert, D. R., Pitha, P. M. (2000) Reconstitution of virus-mediated expression of interferon α genes in human fibroblast cells by ectopic interferon regulatory factor-7. J. Biol. Chem. 275, 6313-6320.
25. Sato, M., Hata, N., Asagiri, M., Nakaya, T., Taniguchi, T., Tanaka, N. (1998) Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441, 106-110.
26. Sato, M., Suemori, H., Hata, N., Asagiri, M., Ogasawara, K., Nakao, K., Nakaya, T., Katsuki, M., Noguchi, S., Tanaka, N., Taniguchi, T. (2000) Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13, 539-548.
27. Marié, I., Durbin, J. E., Levy, D. E. (1998) Differential viral induction of distinct interferon-α genes by positive feedback through interferon regulatory factor-7. EMBO J. 17, 6660-6669.
28. Nakaya, T., Sato, M., Hata, N., Asagiri, M., Suemori, H., Noguchi, S., Tanaka, N., Taniguchi, T. (2001) Gene induction pathways mediated by distinct IRFs during viral infection. Biochem. Biophys. Res. Commun. 283, 1150-1156.
29. Au, W-C., Moore, P. A., LaFleur, D. W., Tombal, B., Pitha, P. M. (1998) Characterization of the interferon regulatory factor-7 and its potential role in the transcription activation of interferon A genes. J. Biol. Chem. 273, 29210-29217.
30. Hata, N., Sato, M., Takaoka, A., Asagiri, M., Tanaka, N., Taniguchi, T. (2001) Constitutive IFN-α/β signal for efficient IFN-α/β gene induction by virus. Biochem. Biophys. Res. Commun. 285, 518-525.
31. Hiscott, J., Pitha, P., Genin, P., Nguyen, H., Heylbroeck, C., Mamane, Y., Algarte, M., Lin, R. (1999) Triggering the interferon response: The role of IRF-3 transcription factor. J. Interferon Cytokine Res. 19, 1-13.
32. Mamane, Y., Heylbroeck, C., Génin, P., Algarté, M., Servant, M. J., LePage, C., DeLuca, C., Kwon, H., Lin, R., Hiscott, J. (1999) Interferon regulatory factors: the next generation. Gene 237, 1-14.
33. Lin, R., Heylbroeck, C., Pitha, P. M., Hiscott, J. (1998) Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18, 2986-2996.
34. Stark, G. R., Kerr, I. M., Williams, B. R. G., Silverman, R. H., Schreiber, R. D. (1998) How cells respond to interferons. Annu. Rev. Biochem. 67, 227-264.
35. Lu, R., Au, W-C., Yeow, W-S., Hageman, N., Pitha, P. M. (2000) Regulation of the promoter activity of interferon regulatory factor-7 gene. J. Biol. Chem. 275, 31805-31812.
36. Kovarick, P., Stoiber, D., Eyers, P. A., Menghini, R., Neininger, A., Gaestel, M., Cohen, P., Decker, T. (1999) Stress-induced phosphorylation of STAT1 at Ser727 requires p38 mitogen-activated protein kinase whereas IFN-γ uses a different signaling pathway. Proc. Natl. Acad. Sci. USA 96, 13956-13961.
37. Kovarik, P., Mangold, M., Ramsauer, K., Heidari, H., Steinborn, R., Zotter, A., Levy, D. E., Müller, M., Decker, T. (2001) Specificity of signaling by STAT1 depends on SH2 and C-terminal domains that regulate Ser727 phosphorylation, differentially affecting specific target gene expression. EMBO J. 20, 91-100.
38. Gollob, J. A., Schnipper, C. P., Murphy, E. A., Ritz, J., Frank, D. A. (1999) The functional synergy between IL-12 and IL-2 involves p38 mitogenactivated protein kinase and is associated with the augmentation of STAT serine phosphorylation. J. Immunol. 162, 4472-4481.
39. Kadowaki, N., Ho, S., Antonenko, S., Malefyt, R. W. M., Kastelein, R. A., Bazan, F., Liu, Y-J. (2001) Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194, 863-869.
40. 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.
41. Barchet, W., Cella, M., Odermatt, B., Asselin-Paturel, C., Colonna, M., Kalinke, U. (2002) Virus-induced Interferon a production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195, 507-516.
42. Wen, Z., Zhong, Z., Darnell Jr., J. E. (1995) Maximal activation of transcription by Statl and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250.
43. Decker, T., Kovarik, P. (2000) Serine phosphorylation of STATs. Oncogene 19, 2628-2637.