Dectin-1 stimulation induces suppressor of cytokine signaling 1, thereby modulating TLR signaling and T cell responses

Journal of Immunology

Volumn 188, Issue 11, 2012, Pages 5644-5654

  Eberle, Mariel E ^a   Dalpke, Alexander H ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DECTIN 1; FOCAL ADHESION KINASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 9; ZYMOSAN;

ANIMAL CELL; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME ACTIVATION; IMMUNOMODULATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TH17 CELL;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; LECTINS, C-TYPE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; T-LYMPHOCYTE SUBSETS; TOLL-LIKE RECEPTORS;

EID: 84862100337     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103068     Document Type: Article

References (54)

1. Alexander, W. S., and D. J. Hilton. 2004. The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu. Rev. Immunol. 22: 503-529. (Pubitemid 38680432)
2. Bode, J. G., A. Nimmesgern, J. Schmitz, F. Schaper, M. Schmitt, W. Frisch, D. Häussinger, P. C. Heinrich, and L. Graeve. 1999. LPS and TNFalpha induce SOCS3 mRNA and inhibit IL-6-induced activation of STAT3 in macrophages. FEBS Lett. 463: 365-370. (Pubitemid 30001952)
3. Crespo, A., M. B. Filla, S. W. Russell, and W. J. Murphy. 2000. Indirect induction of suppressor of cytokine signalling-1 in macrophages stimulated with bacterial lipopolysaccharide: partial role of autocrine/paracrine interferon-alpha/beta. Biochem. J. 349: 99-104. (Pubitemid 30440170)
4. Dalpke, A. H., S. Opper, S. Zimmermann, and K. Heeg. 2001. Suppressors of cytokine signaling (SOCS)-1 and SOCS-3 are induced by CpG-DNA and modulate cytokine responses in APCs. J. Immunol. 166: 7082-7089. (Pubitemid 32525577)
5. Dalpke, A. H., S. Eckerle, M. Frey, and K. Heeg. 2003. Triggering of Toll-like receptors modulates IFN-gamma signaling: involvement of serine 727 STAT1 phosphorylation and suppressors of cytokine signaling. Eur. J. Immunol. 33: 1776-1787. (Pubitemid 37120848)
6. Crespo, A., M. B. Filla, and W. J. Murphy. 2002. Low responsiveness to IFNgamma, after pretreatment of mouse macrophages with lipopolysaccharides, develops via diverse regulatory pathways. Eur. J. Immunol. 32: 710-719. (Pubitemid 34257549)
7. Morita, Y., T. Naka, Y. Kawazoe, M. Fujimoto, M. Narazaki, R. Nakagawa, H. Fukuyama, S. Nagata, and T. Kishimoto. 2000. Signals transducers and activators of transcription (STAT)-induced STAT inhibitor-1 (SSI-1)/suppressor of cytokine signaling-1 (SOCS-1) suppresses tumor necrosis factor alpha-induced cell death in fibroblasts. Proc. Natl. Acad. Sci. USA 97: 5405-5410. (Pubitemid 30313731)
8. Baetz, A., M. Frey, K. Heeg, and A. H. Dalpke. 2004. Suppressor of cytokine signaling (SOCS) proteins indirectly regulate toll-like receptor signaling in innate immune cells. J. Biol. Chem. 279: 54708-54715. (Pubitemid 40053215)
9. Yoshimura, A., H. M. Ohishi, D. Aki, and T. Hanada. 2004. Regulation of TLR signaling and inflammation by SOCS family proteins. J. Leukoc. Biol. 75: 422-427. (Pubitemid 38316372)
10. Creagh, E. M., and L. A. O'Neill. 2006. TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol. 27: 352-357. (Pubitemid 44038661)
11. Janeway, C. A., Jr. 1992. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today 13: 11-16.
12. Brown, G. D., and S. Gordon. 2001. Immune recognition. A new receptor for beta-glucans. Nature 413: 36-37. (Pubitemid 32843478)
13. Brown, G. D. 2006. Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat. Rev. Immunol. 6: 33-43. (Pubitemid 43279751)
14. Drummond, R. A., S. Saijo, Y. Iwakura, and G. D. Brown. 2011. The role of Syk/CARD9 coupled C-type lectins in antifungal immunity. Eur. J. Immunol. 41: 276-281.
15. Underhill, D. M., E. Rossnagle, C. A. Lowell, and R. M. Simmons. 2005. Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 106: 2543-2550. (Pubitemid 41510832)
16. Rogers, N. C., E. C. Slack, A. D. Edwards, M. A. Nolte, O. Schulz, E. Schweighoffer, D. L.Williams, S. Gordon, V. L. Tybulewicz, G. D. Brown, and C. Reis e Sousa. 2005. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22: 507-517.
17. Slack, E. C., M. J. Robinson, P. Hernanz-Falcón, G. D. Brown, D. L. Williams, E. Schweighoffer, V. L. Tybulewicz, and C. Reis e Sousa. 2007. Syk-dependent ERK activation regulates IL-2 and IL-10 production by DC stimulated with zymosan. Eur. J. Immunol. 37: 1600-1612. (Pubitemid 46939495)
18. Bode, K. A., F. Schmitz, L. Vargas, K. Heeg, and A. H. Dalpke. 2009. Kinetic of RelA activation controls magnitude of TLR-mediated IL-12p40 induction. J. Immunol. 182: 2176-2184.
19. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19: 2499.
20. Hertzog, P. J., L. A. O'Neill, and J. A. Hamilton. 2003. The interferon in TLR signaling: more than just antiviral. Trends Immunol. 24: 534-539. (Pubitemid 37205204)
21. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122. (Pubitemid 29359962)
22. Goodridge, H. S., T. Shimada, A. J. Wolf, Y. M. Hsu, C. A. Becker, X. Lin, and D. M. Underhill. 2009. Differential use of CARD9 by dectin-1 in macrophages and dendritic cells. J. Immunol. 182: 1146-1154.
23. Kelly, E. K., L. Wang, and L. B. Ivashkiv. 2010. Calcium-activated pathways and oxidative burst mediate zymosan-induced signaling and IL-10 production in human macrophages. J. Immunol. 184: 5545-5552.
24. Avraham, H., S. Y. Park, K. Schinkmann, and S. Avraham. 2000. RAFTK/Pyk2-mediated cellular signalling. Cell. Signal. 12: 123-133. (Pubitemid 30126029)
25. Hook, S. S., and A. R. Means. 2001. Ca(2+)/CaM-dependent kinases: from activation to function. Annu. Rev. Pharmacol. Toxicol. 41: 471-505.
26. Sasaki, A., H. Yasukawa, A. Suzuki, S. Kamizono, T. Syoda, I. Kinjyo, M. Sasaki, J. A. Johnston, and A. Yoshimura. 1999. Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4: 339-351. (Pubitemid 29359449)
27. Yoshimura, A., T. Naka, and M. Kubo. 2007. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7: 454-465. (Pubitemid 46834848)
28. Goodridge, H. S., R. M. Simmons, and D. M. Underhill. 2007. Dectin-1 stimulation by Candida albicans yeast or zymosan triggers NFAT activation in macrophages and dendritic cells. J. Immunol. 178: 3107-3115. (Pubitemid 46333192)
29. Goodridge, H. S., and D. M. Underhill. 2008. Fungal recognition by TLR2 and Dectin-1. Handb. Exp. Pharmacol. 87-109.
30. Geijtenbeek, T. B., and S. I. Gringhuis. 2009. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9: 465-479.
31. Saccani, S., I. Marazzi, A. A. Beg, and G. Natoli. 2004. Degradation of promoter-bound p65/RelA is essential for the prompt termination of the nuclear factor kappaB response. J. Exp. Med. 200: 107-113. (Pubitemid 38924733)
32. Strebovsky, J., P. Walker, R. Lang, and A. H. Dalpke. 2011. Suppressor of cytokine signaling 1 (SOCS1) limits NFkappaB signaling by decreasing p65 stability within the cell nucleus. FASEB J. 25: 863-874.
33. van de Veerdonk, F. L., L. A. Joosten, P. J. Shaw, S. P. Smeekens, R. K. Malireddi, J. W. van der Meer, B. J. Kullberg, M. G. Netea, and T. D. Kanneganti. 2011. The inflammasome drives protective Th1 and Th17 cellular responses in disseminated candidiasis. Eur. J. Immunol. 41: 2260-2268.
34. Rivera, A., T. M. Hohl, N. Collins, I. Leiner, A. Gallegos, S. Saijo, J. W. Coward, Y. Iwakura, and E. G. Pamer. 2011. Dectin-1 diversifies Aspergillus fumigatus-specific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation. J. Exp. Med. 208: 369-381.
35. Smeekens, S. P., F. L. van de Veerdonk, J. W. van der Meer, B. J. Kullberg, L. A. Joosten, and M. G. Netea. 2010. The Candida Th17 response is dependent on mannan- and beta-glucan-induced prostaglandin E2. Int. Immunol. 22: 889-895.
36. Osorio, F., S. LeibundGut-Landmann, M. Lochner, K. Lahl, T. Sparwasser, G. Eberl, and C. Reis e Sousa. 2008. DC activated via dectin-1 convert Treg into IL-17 producers. Eur. J. Immunol. 38: 3274-3281.
37. Stoiber, D., P. Kovarik, S. Cohney, J. A. Johnston, P. Steinlein, and T. Decker. 1999. Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J. Immunol. 163: 2640-2647. (Pubitemid 29399188)
38. Charoenthongtrakul, S., Q. Zhou, N. Shembade, N. S. Harhaj, and E. W. Harhaj. 2011. Human T cell leukemia virus type 1 Tax inhibits innate antiviral signaling via NF-kappaB-dependent induction of SOCS1. J. Virol. 85: 6955-6962.
39. Pothlichet, J., M. Chignard, and M. Si-Tahar. 2008. Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway. J. Immunol. 180: 2034-2038.
40. Srivastava, V., M. Manchanda, S. Gupta, R. Singla, D. Behera, G. Das, and K. Natarajan. 2009. Toll-like receptor 2 and DC-SIGNR1 differentially regulate suppressors of cytokine signaling 1 in dendritic cells during Mycobacterium tuberculosis infection. J. Biol. Chem. 284: 25532-25541.
41. Mostecki, J., B. M. Showalter, and P. B. Rothman. 2005. Early growth response-1 regulates lipopolysaccharide-induced suppressor of cytokine signaling-1 transcription. J. Biol. Chem. 280: 2596-2605. (Pubitemid 40189362)
42. Ostergaard, H. L., and T. L. Lysechko. 2005. Focal adhesion kinase-related protein tyrosine kinase Pyk2 in T-cell activation and function. Immunol. Res. 31: 267-282.
43. Dalpke, A., K. Heeg, H. Bartz, and A. Baetz. 2008. Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology 213: 225-235. (Pubitemid 351479858)
44. Dikic, I., G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383: 547-550. (Pubitemid 26346184)
45. Eliopoulos, A. G., S. Das, and P. N. Tsichlis. 2006. The tyrosine kinase Syk regulates TPL2 activation signals. J. Biol. Chem. 281: 1371-1380.
46. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc. Natl. Acad. Sci. USA 97: 13766-13771.
47. Underhill, D. M., A. Ozinsky, A. M. Hajjar, A. Stevens, C. B.Wilson, M. Bassetti, and A. Aderem. 1999. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401: 811-815.
48. Cao, S., X. Zhang, J. P. Edwards, and D. M. Mosser. 2006. NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J. Biol. Chem. 281: 26041-26050. (Pubitemid 44401810)
49. Sanjabi, S., A. Hoffmann, H. C. Liou, D. Baltimore, and S. T. Smale. 2000. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. USA 97: 12705-12710.
50. Gringhuis, S. I., J. den Dunnen, M. Litjens, M. van der Vlist, B. Wevers, S. C. Bruijns, and T. B. Geijtenbeek. 2009. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat. Immunol. 10: 203-213.
51. Hayden, M. S., and S. Ghosh. 2008. Shared principles in NF-kappaB signaling. Cell 132: 344-362.
52. Choi, H., R. H. Lee, N. Bazhanov, J. Y. Oh, and D. J. Prockop. 2011. Antiinflammatory protein TSG-6 secreted by activated MSCs attenuates zymosaninduced mouse peritonitis by decreasing TLR2/NF-κB signaling in resident macrophages. Blood 118: 330-338.
53. Srivastava, V., M. Vashishta, S. Gupta, R. Singla, N. Singla, D. Behera, and K. Natarajan. 2011. Suppressors of cytokine signaling inhibit effector T cell responses during Mycobacterium tuberculosis infection. Immunol. Cell Biol. 89: 786-791.
54. Zelante, T., A. De Luca, P. Bonifazi, C. Montagnoli, S. Bozza, S. Moretti, M. L. Belladonna, C. Vacca, C. Conte, P. Mosci, et al. 2007. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur. J. Immunol. 37: 2695-2706. (Pubitemid 47578289)