Pivotal role of ADP-ribosylation factor 6 in toll-like receptor 9-mediated immune signaling

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4323-4334

  Wu, Jing Yiing ^a,b   Kuo, Cheng Chin ^a,c  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADP-RIBOSYLATION FACTORS; CELLULAR EVENTS; CELLULAR UPTAKE; CONSTITUTIVELY ACTIVES; CPG-ODN; CYTOKINE PRODUCTION; ENDOSOMES; INNATE IMMUNE RESPONSE; OLIGODEOXYNUCLEOTIDES; PHOSPHATIDYLINOSITOL; RATE-LIMITING STEPS; TOLL-LIKE RECEPTOR 9; TOLL-LIKE RECEPTORS;

CYTOLOGY; INTERFERONS; MOLECULAR BIOLOGY; OLIGONUCLEOTIDES;

CELLS;

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BETA INTERFERON; CPG OLIGODEOXYNUCLEOTIDE; INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOSOME; HUMAN; HUMAN CELL; INHIBITION KINETICS; INNATE IMMUNITY; LYSOSOME; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTORS; ANIMALS; CELL LINE; ENZYME ACTIVATION; HUMANS; IMMUNITY, INNATE; MALE; MICE; MICE, INBRED BALB C; MUTATION; OLIGODEOXYRIBONUCLEOTIDES; PHOSPHATIDYLINOSITOL 3-KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 9;

EID: 84863050423     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.295113     Document Type: Article

References (44)

1. Messina, J. P., Gilkeson, G. S., and Pisetsky, D. S. (1991) Stimulation of in vitro murine lymphocyte proliferation by bacterial DNA. J. Immunol. 147, 1759-1764
2. Halpern, M. D., Kurlander, R. J., and Pisetsky, D. S. (1996) Bacterial DNA induces murine interferon-γ production by stimulation of interleukin-12 and tumor necrosis factor-α. Cell. Immunol. 167, 72-78 (Pubitemid 26048848)
3. Yi, A. K., and Krieg, A. M. (1998) CpG DNA rescue from anti-IgM-induced WEHI-231 B lymphoma apoptosis via modulation of I&kappaBα and IαBβ and sustained activation of nuclear factor-κB/c-Rel. J. Immunol. 160, 1240-1245
4. Tokunaga, T., Yamamoto, H., Shimada, S., Abe, H., Fukuda, T., Fujisawa, Y., Furutani, Y., Yano, O., Kataoka, T., and Sudo, T. (1984) Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity. J. Natl. Cancer Inst. 72, 955-962 (Pubitemid 14131740)
5. Yamamoto, S., Kuramoto, E., Shimada, S., and Tokunaga, T. (1988) In vitro augmentation of natural killer cell activity and production of interferon- α/β and -γ with deoxyribonucleic acid fraction from Mycobacterium bovis BCG. Jpn. J. Cancer Res. 79, 866-873
6. Stacey, K. J., Sweet, M. J., and Hume, D. A. (1996) Macrophages ingest and are activated by bacterial DNA. J. Immunol. 157, 2116-2122 (Pubitemid 126449689)
7. Yi, A. K., Tuetken, R., Redford, T., Waldschmidt, M., Kirsch, J., and Krieg, A. M. (1998) CpG motifs in bacterial DNA activate leukocytes through the pH-dependent generation of reactive oxygen species. J. Immunol. 160, 4755-4761 (Pubitemid 28215308)
8. Krieg, A. M., Yi, A. K., Matson, S., Waldschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A., and Klinman, D. M. (1995) CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374, 546-549
9. Kline, J. N., Waldschmidt, T. J., Businga, T. R., Lemish, J. E., Weinstock, J. V., Thorne, P. S., and Krieg, A. M. (1998) Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J. Immunol. 160, 2555-2559 (Pubitemid 28136702)
10. Shirota, H., Sano, K., Hirasawa, N., Terui, T., Ohuchi, K., Hattori, T., Shirato, K., and Tamura, G. (2001) Novel roles of CpG oligodeoxynucleotides as a leader for the sampling and presentation of CpG-tagged antigen by dendritic cells. J. Immunol. 167, 66-74 (Pubitemid 32567762)
11. Kumagai, Y., Takeuchi, O., and Akira, S. (2008) TLR9 as a key receptor for the recognition of DNA. Adv. Drug Deliv. Rev. 60, 795-804
12. O'Neill, L. A. (2006) How Toll-like receptors signal. What we know and what we don't know. Curr. Opin. Immunol. 18, 3-9
13. Takeda, K., and Akira, S. (2001) Roles of Toll-like receptors in innate immune responses. Genes Cells 6, 733-742 (Pubitemid 32894068)
14. Krieg, A. M. (2007) Development of TLR9 agonists for cancer therapy. J. Clin. Invest. 117, 1184-1194
15. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745 (Pubitemid 32015992)
16. Bauer, S., Kirschning, C. J., Häcker, H., Redecke, V., Hausmann, S., Akira, S., Wagner, H., and Lipford, G. B. (2001) Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U.S.A. 98, 9237-9242 (Pubitemid 32743900)
17. Lund, J., Sato, A., Akira, S., Medzhitov, R., and Iwasaki, A. (2003) Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198, 513-520 (Pubitemid 36976063)
18. Krug, A., French, A. R., Barchet, W., Fischer, J. A., Dzionek, A., Pingel, J. T., Orihuela, M. M., Akira, S., Yokoyama, W. M., and Colonna, M. (2004) TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21, 107-119 (Pubitemid 38925271)
19. Häcker, H., Mischak, H., Miethke, T., Liptay, S., Schmid, R., Sparwasser, T., Heeg, K., Lipford, G. B., and 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 (Pubitemid 28497796)
20. Akira, S., and Hemmi, H. (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett. 85, 85-95 (Pubitemid 36071561)
21. Häcker, H., Vabulas, R. M., Takeuchi, O., Hoshino, K., Akira, S., and 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 (Pubitemid 30666261)
22. Kobayashi, T., Walsh, M. C., and Choi, Y. (2004) The role of TRAF6 in signal transduction and the immune response. Microbes Infect 6, 1333-1338 (Pubitemid 39539732)
23. Vilaysane, A., and Muruve, D. A. (2009) The innate immune response to DNA. Semin. Immunol. 21, 208-214
24. Krieg, A. M. (2002) CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20, 709-760
25. Kuo, C. C., Liang, S. M., and Liang, C. M. (2006) CpG-B oligodeoxynucleotide promotes cell survival via up-regulation of Hsp70 to increase Bcl-xL and to decrease apoptosis-inducing factor translocation. J. Biol. Chem. 281, 38200-38207
26. Kuo, C. C., Liang, C. M., Lai, C. Y., and Liang, S. M. (2007) Involvement of heat shock protein (Hsp)90β but not Hsp90α in anti-apoptotic effect of CpG-B oligodeoxynucleotide. J. Immunol. 178, 6100-6108
27. Latz, E., Schoenemeyer, A., Visintin, A., Fitzgerald, K. A., Monks, B. G., Knetter, C. F., Lien, E., Nilsen, N. J., Espevik, T., and Golenbock, D. T. (2004) TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5, 190-198 (Pubitemid 38208361)
28. Takeshita, F., Gursel, I., Ishii, K. J., Suzuki, K., Gursel, M., and Klinman, D. M. (2004) Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin. Immunol. 16, 17-22 (Pubitemid 38147429)
29. Kuo, C. C., Lin, W. T., Liang, C. M., and Liang, S. M. (2006) Class I and III phosphatidylinositol 3′-kinase play distinct roles in TLR signaling pathway. J. Immunol. 176, 5943-5949
30. D'Souza-Schorey, C., and Chavrier, P. (2006) ARF proteins. Roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358
31. Inoue, H., and Randazzo, P. A. (2007) Arf GAPs and their interacting proteins. Traffic 8, 1465-1475 (Pubitemid 47591332)
32. Randazzo, P. A., Inoue, H., and Bharti, S. (2007) Arf GAPs as regulators of the actin cytoskeleton. Biol. Cell 99, 583-600 (Pubitemid 47543316)
33. Chockalingam, A., Brooks, J. C., Cameron, J. L., Blum, L. K., and Leifer, C. A. (2009) TLR9 traffics through the Golgi complex to localize to endolysosomes and respond to CpG DNA. Immunol. Cell Biol. 87, 209-217
34. Kawai, T., and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity. Update on Toll-like receptors. Nat. Immunol. 11, 373-384
35. Burns, K., Martinon, F., Esslinger, C., Pahl, H., Schneider, P., Bodmer, J. L., Di Marco, F., French, L., and Tschopp, J. (1998) MyD88, an adapter protein involved in interleukin-1 signaling. J. Biol. Chem. 273, 12203-12209 (Pubitemid 28240584)
36. Ewald, S. E., Lee, B. L., Lau, L., Wickliffe, K. E., Shi, G. P., Chapman, H. A., and Barton, G. M. (2008) The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 456, 658-662
37. Park, B., Brinkmann, M. M., Spooner, E., Lee, C. C., Kim, Y. M., and Ploegh, H. L. (2008) Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 9, 1407-1414
38. Kim, Y. M., Brinkmann, M. M., Paquet, M. E., and Ploegh, H. L. (2008) UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452, 234-238 (Pubitemid 351380247)
39. Stein, M. P., Feng, Y., Cooper, K. L., Welford, A. M., and Wandinger-Ness, A. (2003) Human VPS34 and p150 are Rab7 interacting partners. Traffic 4, 754-771 (Pubitemid 37361856)
40. Kuo, C. C., Kuo, C. W., Liang, C. M., and Liang, S. M. (2005) A transcriptomic and proteomic analysis of the effect of CpG-ODN on human THP-1 monocytic leukemia cells. Proteomics 5, 894-906
41. Gursel, M., Gursel, I., Mostowski, H. S., and Klinman, D. M. (2006) CXCL16 influences the nature and specificity of CpG-induced immune activation. J. Immunol. 177, 1575-1580 (Pubitemid 44092492)
42. Butler, M., Crooke, R. M., Graham, M. J., Lemonidis, K. M., Lougheed, M., Murray, S. F., Witchell, D., Steinbrecher, U., and Bennett, C. F. (2000) Phosphorothioate oligodeoxynucleotides distribute similarly in class A scavenger receptor knockout and wild type mice. J. Pharmacol. Exp. Ther. 292, 489-496 (Pubitemid 30067410)
43. Anderson, R. B., Cianciolo, G. J., Kennedy, M. N., and Pizzo, S. V. (2008) α2-macroglobulin binds CpG oligodeoxynucleotides and enhances their immunostimulatory properties by a receptor-dependent mechanism. J. Leukoc. Biol. 83, 381-392 (Pubitemid 351225619)
44. Sivori, S., Falco, M., Carlomagno, S., Romeo, E., Soldani, C., Bensussan, A., Viola, A., Moretta, L., and Moretta, A. (2010) A novel KIR-associated function. Evidence that CpG DNA uptake and shuttling to early endosomes is mediated by KIR3DL2. Blood 116, 1637-1647