Endosomal translocation of CpG-oligodeoxynucleotides inhibits DNA-PKcs-dependent IL-10 production in macrophages

Journal of Immunology

Volumn 180, Issue 2, 2008, Pages 809-816

  Yotsumoto, Satoshi ^a   Saegusa, Kazuharu ^a   Aramaki, Yukihiko ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; CHLOROQUINE; CPG OLIGODEOXYNUCLEOTIDE; DNA; INTERLEUKIN 10; INTERLEUKIN 12P70; LIPOSOME; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; SMALL INTERFERING RNA; 1,2 DIOLEOYLOXY 3 (TRIMETHYLAMMONIUM)PROPANE; 1,2-DIOLEOYLOXY-3-(TRIMETHYLAMMONIUM)PROPANE; CPG OLIGONUCLEOTIDE; CPG-OLIGONUCLEOTIDE; DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; INTERLEUKIN 12; MONOUNSATURATED FATTY ACID; NUCLEAR PROTEIN; OLIGODEOXYRIBONUCLEOTIDE; PRKDC PROTEIN, MOUSE; QUATERNARY AMMONIUM DERIVATIVE; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL TRANSPORT; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; DENDRITIC CELL; DNA PROTEIN COMPLEX; ENDOSOME; ENZYME ACTIVATION; IMMUNOTHERAPY; MACROPHAGE; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SCID MOUSE; ANIMAL; BIOSYNTHESIS; CELL LINE; CHEMISTRY; DRUG ANTAGONISM; ENDOCYTOSIS; ENZYMOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PERITONEUM MACROPHAGE;

ANIMALS; CELL LINE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; ENDOCYTOSIS; ENDOSOMES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FATTY ACIDS, MONOUNSATURATED; INTERLEUKIN-10; INTERLEUKIN-12; LIPOSOMES; MACROPHAGES, PERITONEAL; MICE; MICE, SCID; NUCLEAR PROTEINS; OLIGODEOXYRIBONUCLEOTIDES; QUATERNARY AMMONIUM COMPOUNDS; RNA, SMALL INTERFERING;

EID: 40449101333     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.2.809     Document Type: Article

References (53)

1. Krieg, A. M. 2006. Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 5: 471-484.
2. Wilson, H. L., A. Dar, S. K. Napper, A. Marianela Lopez, L. A. Babiuk, and G. K. Mutwiri. 2006. Immune mechanisms and therapeutic potential of CpG oligodeoxynucleotides. Int. Rev. Immunol. 25: 183-213.
3. Akdis, C. A., and K. Blaser. 2001. Mechanisms of interleukin-10-mediated immune suppression. Immunology 103: 131-136.
4. Mocellin, S., F. M. Marincola, and H. A. Young. 2005. Interleukin-10 and the immune response against cancer: a counterpoint. J. Leukocyte Biol. 78: 1043-1051.
5. Duramad, O., K. L. Fearon, J. H. Chan, H. Kanzler, J. D. Marshall, R. L. Coffman, and F. J. Barrat. 2003. IL-10 regulates plasmacytoid dendritic cell response to CpG-containing immunostimulatory sequences. Blood 102: 4487-4492.
6. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
7. Vicari, A. P., C. Chiodoni, C. Vaure, S. Ait-Yahia, C. Dercamp, F. Matsos, O. Reynard, C. Taverne, P. Merle, M. P. Colombo, et al. 2002. Reversal of tumor-induced dendritic cell paralysis by CpG immunostimulatory oligonucleotide and anti-interleukin 10 receptor antibody. J. Exp. Med. 196: 541-549.
8. + regulatory T cells in the inhibition of antitumor CD8 T-cell responses. Cancer Res. 65: 8479-8486.
9. Guiducci, C., A. P. Vicari, S. Sangaletti, G. Trinchieri, and M. P. Colombo. 2005. Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 65: 3437-3446.
10. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
11. Yi, A. K., R. Tuetken, T. Redford, M. Waldschmidt, J. Kirsch, and A. M. Krieg. 1998. CpG motifs in bacterial DNA activate leukocytes through the pH-dependent generation of reactive oxygen species. J. Immunol. 160: 4755-4761.
12. Rutz, M., J. Metzger, T. Gellert, P. Luppa, G. B. Lipford, H. Wagner, and S. Bauer. 2004. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence-and pH-dependent manner. Eur. J. Immunol. 34: 2541-2550.
13. Latz, E., A. Schoenemeyer, A. Visintin, K. A. Fitzgerald, B. G. Monks, C. F. Knetter, E. Lien, N. J. Nilsen, T. Espevik, and D. T. Golenbock. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5: 190-198.
14. Hacker, H., H. Mischak, T. Miethke, S. Liptay, R. Schmid, T. Sparwasser, K. Heeg, G. B. Lipford, and H. Wagner. 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.
15. Yi, A. K., M. Chang, D. W. Peckham, A. M. Krieg, and R. F. Ashman. 1998. CpG oligodeoxyribonucleotides rescue mature spleen B cells from spontaneous apoptosis and promote cell cycle entry. J. Immunol. 160: 5898-5906.
16. Park, Y., S. W. Lee, and Y. C. Sung. 2002. Cutting edge: CpG DNA inhibits dendritic cell apoptosis by up-regulating cellular inhibitor of apoptosis proteins through the phosphatidylinositide-3′-OH kinase pathway. J. Immunol. 168: 5-8.
17. Dragoi, A. M., X. Fu, S. Ivanov, P. Zhang, L. Sheng, D. Wu, G. C. Li, and W. M. Chu. 2005. DNA-PKcs, but not TLR9, is required for activation of Akt by CpG-DNA. EMBO J. 24: 779-789.
18. Smith, G. C., and S. P. Jackson. 1999. The DNA-dependent protein kinase. Genes Dev. 13: 916-934.
19. Dip, R., and H. Naegeli. 2005. More than just strand breaks: the recognition of structural DNA discontinuities by DNA-dependent protein kinase catalytic subunit. FASEB J. 19: 704-715.
20. Carter, T., I. Vancurova, I. Sun, W. Lou, and S. DeLeon. 1990. A DNA-activated protein kinase from HeLa cell nuclei. Mol. Cell. Biol. 10: 6460-6471.
21. Koike, M., T. Awaji, M. Kataoka, G. Tsujimoto, T. Kartasova, A. Koike, and T. Shiomi. 1999. Differential subcellular localization of DNA-dependent protein kinase components Ku and DNA-PKcs during mitosis. J. Cell Sci. 112: 4031-4039.
22. Nilsson, A., F. Sirzen, R. Lewensohn, N. Wang, and S. Skog. 1999. Cell cycle-dependent regulation of the DNA-dependent protein kinase. Cell Prolif. 32: 239-248.
23. Blunt, T., N. J. Finnie, G. E. Taccioli, G. C. Smith, J. Demengeot, T. M. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo, et al. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80: 813-823.
24. Meek, K., L. Kienker, C. Dallas, W. Wang, M. J. Dark, P. J. Venta, M. L. Huie, R. Hirschhorn, and T. Bell. 2001. SCID in Jack Russell terriers: a new animal model of DNA-PKcs deficiency. J. Immunol. 167: 2142-2150.
25. Kashishian, A., H. Douangpanya, D. Clark, S. T. Schlachter, C. T. Eary, J. G. Schiro, H. Huang, L. E. Burgess, E. A. Kesicki, and J. Halbrook. 2003. DNA-dependent protein kinase inhibitors as drug candidates for the treatment of cancer. Mol. Cancer Ther. 2: 1257-1264.
26. Saegusa, K., S. Yotsumoto, S. Kato, and Y. Aramaki. 2007. Phosphatidylinositol 3-kinase-mediated regulation of IL-10 and IL-12 production in macrophages stimulated with CpG oligodeoxynucleotide. Mol. Immunol. 44: 1323-1330.
27. Yasuda, K., P. Yu, C. J. Kirschning, B. Schlatter, F. Schmitz, A. Heit, S. Bauer, H. Hochrein, and H. Wagner. 2005. Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 174: 6129-6136.
28. Honda, K., Y. Ohba, H. Yanai, H. Negishi, T. Mizutani, A. Takaoka, C. Taya, and T. Taniguchi. 2005. Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434: 1035-1040.
29. Litzinger, D. C., and L. Huang. 1992. Phosphatidylethanolamine liposomes: drug delivery, gene transfer, and immunodiagnostic applications. Biochim. Biophys. Acta 1113: 201-227.
30. Felgner, J. H., R. Kumar, C. N. Sridhar, C. J. Wheeler, Y. J. Tsai, R. Border, P. Ramsey, M. Martin, and P. L. Felgner. 1994. Enhanced gene delivery and mechanism studies with a novel series of cationic lipid formulations. J. Biol. Chem. 269: 2550-2561.
31. Farhood, H., N. Serbina, and L. Huang. 1995. The role of dioleoyl phosphatidylethanolamine in cationic liposome mediated gene transfer. Biochim. Biophys. Acta 1235: 289-295.
32. Legendre, J. Y., and F. C. Szoka, Jr. 1992. Delivery of plasmid DNA into mammalian cell lines using pH-sensitive liposomes: comparison with cationic liposomes. Pharm. Res. 9: 1235-1242.
33. Hafez, I. M., and P. R. Cullis. 2001. Roles of lipid polymorphism in intracellular delivery. Adv. Drug Deliv. Rev. 47: 139-148.
34. Hemmi, H., T. Kaisho, K. Takeda, and S. Akira. 2003. The roles of Toll-like receptor 9, MyD88, and DNA-dependent protein kinase catalytic subunit in the effects of two distinct CpG DNAs on dendritic cell subsets. J. Immunol. 170: 3059-3064.
35. Ishii, K. J., F. Takeshita, I. Gursel, M. Gursel, J. Conover, A. Nussenzweig, and D. M. Klinman. 2002. Potential role of phosphatidylinositol 3 kinase, rather than DNA-dependent protein kinase, in CpG DNA-induced immune activation. J. Exp. Med. 196: 269-274.
36. Boonstra, A., R. Rajsbaum, M. Holman, R. Marques, C. Asselin-Paturel, J. P. Pereira, E. E. M. Bates, S. Akira, P. Viera, Y.-J. Liu, et al. 2006. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88- and TRIF-dependent TLR signals, and TLR-independent signals. J. Immunol. 177: 7551-7558.
37. Wingender, G., N. Garbi, B. Schumak, F. Jungerkes, E. Endl, D. von Bubnoff, J. Steitz, J. Striegler, G. Moldenhauer, T. Tuting, et al. 2006. Systemic application of CpG-rich DNA suppresses adaptive T cell immunity via induction of IDO. Eur. J. Immunol. 36: 12-20.
38. 2-M delay. Clin. Cancer Res. 3: 1149-1156.
39. Smith, G. C., N. Divecha, N. D. Lakin, and S. P. Jackson. 1999. DNA-dependent protein kinase and related proteins. Biochem. Soc. Symp. 64: 91-104.
40. Chu, W., X. Gong, Z. Li, K. Takabayashi, H. Ouyang, Y. Chen, A. Lois, D. J. Chen, G. C. Li, M. Karin, and E. Raz. 2000. DNA-PKcs is required for activation of innate immunity by immunostimulatory DNA. Cell 103: 909-918.
41. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363.
42. Sester, D. P., K. Brion, A. Trieu, H. S. Goodridge, T. L. Roberts, J. Dunn, D. A. Hume, K. J. Stacey, and M. J. Sweet. 2006. CpG DNA activates survival in murine macrophages through TLR9 and the phosphatidylinositol 3-kinase-Akt pathway. J. Immunol. 177: 4473-4480.
43. Gursel, I., M. Gursel, K. J. Ishii, and D. M. Klinman. 2001. Sterically stabilized cationic liposomes improve the uptake and immunostimulatory activity of CpG oligonucleotides. J. Immunol. 167: 3324-3328.
44. + T-cell response using CpG oligodeoxynucleotides and HER-2/neu-derived peptide co-encapsulated in liposomes. Vaccine 21: 3319-3329.
45. Suzuki, Y., D. Wakita, K. Chamoto, Y. Narita, T. Tsuji, T. Takeshima, H. Gyobu, Y. Kawarada, S. Kondo, S. Akira, et al. 2004. Liposome-encapsulated CpG oligodeoxynucleotides as a potent adjuvant for inducing type 1 innate immunity. Cancer Res. 64: 8754-8760.
46. Muller, C., G. Christodoulopoulos, B. Salles, and L. Panasci. 1998. DNA-dependent protein kinase activity correlates with clinical and in vitro sensitivity of chronic lymphocytic leukemia lymphocytes to nitrogen mustards. Blood 92: 2213-2219.
47. Xu, W., L. Liu, G. C. Smith, and G. Charles. 2000. Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat. Cell. Biol. 2: 339-345.
48. Sirzen, F., A. Nilsson, B. Zhivotovsky, and R. Lewensohn. 1999. DNA-dependent protein kinase content and activity in lung carcinoma cell lines: correlation with intrinsic radiosensitivity. Eur. J. Cancer 35: 111-116.
49. Shen, H., M. Schultz, G. D. Kruh, and K. D. Tew. 1998. Increased expression of DNA-dependent protein kinase confers resistance to adriamycin. Biochim. Biophys. Acta 1381: 131-138.
50. Frit, P., Y. Canitrot, C. Muller, N. Foray, P. Calsou, E. Marangoni, J. Bourhis, and B. Salles. 1999. Cross-resistance to ionizing radiation in a murine leukemic cell line resistant to cis-dichlorodiammineplatinum(II): role of Ku autoantigen. Mol. Pharmacol. 56: 141-146.
51. Kim, S. H., J. H. Um, B. Dong-Won, B. H. Kwon, D. W. Kim, B. S. Chung, and C. D. Kang. 2000. Potentiation of chemosensitivity in multidrug-resistant human leukemia CEM cells by inhibition of DNA-dependent protein kinase using wort-mannin. Leuk. Res. 24: 917-925.
52. Willmore, E., S. de Caux, N. J. Sunter, M. J. Tilby, G. H. Jackson, C. A. Austin, and B. W. Durkacz. 2004. A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood 103: 4659-4665.
53. Madhusudan, S., and I. D. Hickson. 2005. DNA repair inhibition: a selective tumor targeting strategy. Trends Mol. Med. 11: 503-511.