Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists

Journal of Immunology

Volumn 181, Issue 7, 2008, Pages 5120-5127

  Roses, Robert E ^a   Xu, Shuwen ^a   Xu, Min ^a   Koldovsky, Ursula ^a   Koski, Gary ^b   Czerniecki, Brian J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; RESIQUIMOD; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR AGONIST; IMIDAZOLE DERIVATIVE; LIGAND; TEICHOIC ACID; TOLL LIKE RECEPTOR;

ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME INDUCTION; HUMAN; HUMAN CELL; MEMORY CELL; MEMORY T LYMPHOCYTE; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TH1 CELL; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; COCULTURE; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; GENETICS; IMMUNOLOGY; METABOLISM; SECRETION;

CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; HUMANS; IMIDAZOLES; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKIN-17; INTERLEUKIN-23; LIGANDS; LIPOPOLYSACCHARIDES; MYELOID CELLS; TEICHOIC ACIDS; TOLL-LIKE RECEPTORS;

EID: 58149288675     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.7.5120     Document Type: Article

References (43)

1. Trinchieri, G., S. Pflanz, and R. A. Kastelein. 2003. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 19: 641-644. (Pubitemid 37490789)
2. Hunter, C. A. 2005. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5: 521-531.
3. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146. (Pubitemid 37328691)
4. Colombo, M. P., and G. Trinchieri. 2002. Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev. 13: 155-168.
5. Heufler, C., F. Koch, U. Stanzl, G. Topar, M. Wysocka, G. Trinchieri, A. Enk, R. M. Steinman, N. Romani, and G. Schuler. 1996. Interleukin-12 is produced by dendritic cells and mediates T helper 1 development as well as interferon-γ production by T helper 1 cells. Eur. J. Immunol. 26: 659-668. (Pubitemid 26091397)
6. Steinman, R. M., and H. Hemmi. 2006. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 311: 17-58. (Pubitemid 47413194)
7. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189. (Pubitemid 43214587)
8. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin- 12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
9. McKenzie, B. S., R. A. Kastelein, and D. J. Cua. 2006. Understanding the IL- 23-IL-17 immune pathway. Trends Immunol. 27: 17-23.
10. Happel, K. I., P. J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L. J. Quinton, A. R. Odden, J. E. Shellito, G. J. Bagby, S. Nelson, and J. K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202: 761-769.
11. Malley, R., A. Srivastava, M. Lipsitch, C. M. Thompson, C. Watkins, A. Tzianabos, and P. W. Anderson. 2006. Antibody-independent, interleukin- 17A-mediated, cross-serotype immunity to pneumococci in mice immunized intranasally with the cell wall polysaccharide. Infect. Immun. 74: 2187-2195.
12. Lieberman, L. A., F. Cardillo, A. M. Owyang, D. M. Rennick, D. J. Cua, R. A. Kastelein, and C. A. Hunter. 2004. IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J. Immunol. 173: 1887-1893.
13. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
14. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
15. Hue, S., P. Ahern, S. Buonocore, M. C. Kullberg, D. J. Cua, B. S. McKenzie, F. Powrie, and K. J. Maloy. 2006. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203: 2473-2483. (Pubitemid 44664617)
16. Hu, J., X. Yuan, M. L. Belladonna, J. M. Ong, S. Wachsmann-Hogiu, D. L. Farkas, K. L. Black, and J. S. Yu. 2006. Induction of potent antitumor immunity by intratumoral injection of interleukin 23-transduced dendritic cells. Cancer Res. 66: 8887-8896.
17. Kaiga, T., M. Sato, H. Kaneda, Y. Iwakura, T. Takayama, and H. Tahara. 2007. Systemic administration of IL-23 induces potent antitumor immunity primarily mediated through Th1-type response in association with the endogenously expressed IL-12. J. Immunol. 178: 7571-7580. (Pubitemid 46898026)
18. Langowski, J. L., X. Zhang, L. Wu, J. D. Mattson, T. Chen, K. Smith, B. Basham, T. McClanahan, R. A. Kastelein, and M. Oft. 2006. IL-23 promotes tumour incidence and growth. Nature 442: 461-465.
19. Langowski, J. L., R. A. Kastelein, and M. Oft. 2007. Swords into plowshares: IL-23 repurposes tumor immune surveillance. Trends Immunol. 28: 207-212.
20. de Jong, E. C., P. L. Vieira, P. Kalinski, J. H. Schuitemaker, Y. Tanaka, E. A. Wierenga, M. Yazdanbakhsh, and M. L. Kapsenberg. 2002. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse Th cell-polarizing signals. J. Immunol. 168: 1704-1709.
21. Macagno, A., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Duration, combination and timing: the signal integration model of dendritic cell activation. Trends Immunol. 28: 227-233. (Pubitemid 46654873)
22. Tsuji, S., M. Matsumoto, O. Takeuchi, S. Akira, I. Azuma, A. Hayashi, K. Toyoshima, and T. Seya. 2000. Maturation of human dendritic cells by cell wall skeleton of Mycobacterium bovis bacillus Calmette-Guerin: involvement of toll-like receptors. Infect. Immun. 68: 6883-6890. (Pubitemid 32463398)
23. Napolitani, G., A. Rinaldi, F. Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6: 769-776. (Pubitemid 43090462)
24. Xu, S., U. Koldovsky, M. Xu, D. Wang, E. Fitzpatrick, G. Son, G. Koski, and B. J. Czerniecki. 2006. High-avidity antitumor T-cell generation by toll receptor 8-primed, myeloid-derived dendritic cells is mediated by IL-12 production. Surgery 140: 170-178. (Pubitemid 44176060)
25. Snijders, A., P. Kalinski, C. M. Hilkens, and M. L. Kapsenberg. 1998. High-level IL-12 production by human dendritic cells requires two signals. Int. Immunol. 10: 1593-1598. (Pubitemid 28502373)
26. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949.
27. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8: 950-957. (Pubitemid 47300009)
28. Czerniecki, B. J., C. Carter, L. Rivoltini, G. K. Koski, H. I. Kim, D. E. Weng, J. G. Roros, Y. M. Hijazi, S. Xu, S. A. Rosenberg, and P. A. Cohen. 1997. Calcium ionophore-treated peripheral blood monocytes and dendritic cells rapidly display characteristics of activated dendritic cells. J. Immunol. 159: 3823-3837.
29. Koski, G. K., K. Kariko, S. Xu, D. Weissman, P. A. Cohen, and B. J. Czerniecki. 2004. Cutting edge: innate immune system discriminates between RNA containing bacterial versus eukaryotic structural features that prime for high-level IL-12 secretion by dendritic cells. J. Immunol. 172: 3989-3993.
30. Jonuleit, H., J. Knop, and A. H. Enk. 1996. Cytokines and their effects on maturation, differentiation and migration of dendritic cells. Arch Dermatol. Res. 289: 1-8. (Pubitemid 27011060)
31. Vieira, P. L., E. C. de Jong, E. A. Wierenga, M. L. Kapsenberg, and P. Kalinski. 2000. Development of Th1-inducing capacity in myeloid dendritic cells requires environmental instruction. J. Immunol. 164: 4507-4512.
32. Rieser, C., G. Bock, H. Klocker, G. Bartsch, and M. Thurnher. 1997. Prostaglandin E2 and tumor necrosis factor α cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J. Exp. Med. 186: 1603-1608. (Pubitemid 27479821)
33. Liao, J. J., M. C. Huang, and E. J. Goetzl. 2007. Cutting edge: alternative signaling of Th17 cell development by sphingosine 1-phosphate. J. Immunol. 178: 5425-5428.
34. Bettelli, E., M. Oukka, and V. K. Kuchroo. 2007. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8: 345-350.
35. Kryczek, I., S. Wei, L. Zou, S. Altuwaijri, W. Szeliga, J. Kolls, A. Chang, and W. Zou. 2007. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J. Immunol. 178: 6730-6733. (Pubitemid 46847396)
36. + IL-17-producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J. Immunol. 177: 6852-6858.
37. + T cells to tumor antigens by dendritic cells leads to enhanced functional avidity and direct tumor recognition through an IL-12-dependent mechanism. J. Immunol. 171: 2251-2261.
38. + T cell responses in vitro. J. Immunother. 30: 75-82.
39. Sheibanie, A. F., T. Khayrullina, F. F. Safadi, and D. Ganea. 2007. Prostaglandin E2 exacerbates collagen-induced arthritis in mice through the inflammatory interleukin- 23/interleukin-17 axis. Arthritis Rheum. 56: 2608-2619.
40. Van Beelen, A. J., Z. Zelinkova, E. W. Taanman-Kueter, F. J. Muller, D. W. Hommes, S. A. Zaat, M. L. Kapsenberg, and E. C. de Jong. 2007. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity 27: 660-669.
41. Goriely, S., M. F. Neurath, and M. Goldman. 2008. How microorganisms tip the balance between interleukin-12 family members. Nat. Rev. Immunol. 8: 81-86.
42. Kryczek, I., S. Wei, L. Zou, S. Altuwaijri, W. Szeliga, J. Kolls, A. Chang, and W. Zou. 2007. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J. Immunol. 178: 6730-6733. (Pubitemid 46847396)
43. Czerniecki, B. J., G. K. Koski, U. Koldovsky, S. Xu, P. A. Cohen, R. Mick, H. Nisenbaum, T. Pasha, M. Xu, K. R. Fox, et al. 2007. Targeting HER-2/neu in early breast cancer development using dendritic cells with staged interleukin-12 burst secretion. Cancer Res. 67: 1842-1852. (Pubitemid 46383411)