Syk negatively regulates TLR4-mediated IFNβ and IL-10 production and promotes inflammatory responses in dendritic cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1860, Issue 3, 2016, Pages 588-598

  Yin, Hui ^a   Zhou, Huaxin ^b   Kang, Yi ^a   Zhang, Xiaoju ^a   Duan, Xiaoxian ^b   Alnabhan, Ridab ^b   Liang, Shuang ^b   Scott, David A ^b   Lamont, Richard J ^b   Shang, Jia ^a   Wang, Huizhi ^b  

^a ZHENGZHOU UNIVERSITY   (China)

^b UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

GSK3 ; IL 10; Interferon ; PI3K; Syk; Toll like receptor 4

Indexed keywords

B7 ANTIGEN; BETA INTERFERON; CD86 ANTIGEN; GLYCOGEN SYNTHASE KINASE 3BETA; I KAPPA B KINASE BETA; INTERLEUKIN 10; INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE SYK; STAT1 PROTEIN; STAT3 PROTEIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; GAMMA INTERFERON; GLYCOGEN SYNTHASE KINASE 3; GSK3B PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE; STAT PROTEIN; SYK PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; CELL MATURATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; DENDRITIC CELLS; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INFLAMMATION; INTERFERON-BETA; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; STAT TRANSCRIPTION FACTORS; SYK KINASE; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84953439470     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.12.012     Document Type: Article

References (59)

1. C.M. Horvath Weapons of STAT destruction. Interferon evasion by paramyxovirus V protein Eur. J. Biochem. 271 2004 4621 4628
2. A. Takaoka, and H. Yanai Interferon signalling network in innate defence Cell. Microbiol. 8 2006 907 922
3. T. Taniguchi, and A. Takaoka The interferon-alpha/beta system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors Curr. Opin. Immunol. 14 2002 111 116
4. C. Garlanda, D. Di Liberto, A. Vecchi, M.P. La Manna, C. Buracchi, N. Caccamo, A. Salerno, F. Dieli, and A. Mantovani Damping excessive inflammation and tissue damage in Mycobacterium tuberculosis infection by Toll IL-1 receptor 8/single Ig IL-1-related receptor, a negative regulator of IL-1/TLR signaling J. Immunol. 179 2007 3119 3125
5. L.A. O'Neill 'Fine tuning' TLR signaling Nat. Immunol. 9 2008 459 461
6. P.J. Hertzog, and B.R. Williams Fine tuning type I interferon responses Cytokine Growth Factor Rev. 24 2013 217 225
7. T. Horng, G.M. Barton, R.A. Flavell, and R. Medzhitov The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors Nature 420 2002 329 333
8. S. Balachandran, and A.A. Beg Defining emerging roles for NF-kappaB in antivirus responses: revisiting the interferon-beta enhanceosome paradigm PLoS Pathog. 7 2011 e1002165
9. D. Panne, T. Maniatis, and S.C. Harrison An atomic model of the interferon-beta enhanceosome Cell 129 2007 1111 1123
10. D. Thanos, and T. Maniatis Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome Cell 83 1995 1091 1100
11. M. Martin, K. Rehani, R.S. Jope, and S.M. Michalek Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3 Nat. Immunol. 6 2005 777 784
12. H. Wang, J. Brown, C.A. Garcia, Y. Tang, M.R. Benakanakere, T. Greenway, P. Alard, D.F. Kinane, and M. Martin The role of glycogen synthase kinase 3 in regulating IFN-beta-mediated IL-10 production J. Immunol. 186 2011 675 684
13. H. Wang, C.A. Garcia, K. Rehani, C. Cekic, P. Alard, D.F. Kinane, T. Mitchell, and M. Martin IFN-beta production by TLR4-stimulated innate immune cells is negatively regulated by GSK3-beta J. Immunol. 181 2008 6797 6802
14. W. Cao, S. Manicassamy, H. Tang, S.P. Kasturi, A. Pirani, N. Murthy, and B. Pulendran Toll-like receptor-mediated induction of type I interferon in plasmacytoid dendritic cells requires the rapamycin-sensitive PI(3)K-mTOR-p70S6K pathway Nat. Immunol. 9 2008 1157 1164
15. H. Wang, J. Brown, Z. Gu, C.A. Garcia, R. Liang, P. Alard, E. Beurel, R.S. Jope, T. Greenway, and M. Martin Convergence of the mammalian target of rapamycin complex 1- and glycogen synthase kinase 3-beta-signaling pathways regulates the innate inflammatory response J. Immunol. 186 2011 5217 5226
16. A.M. Cheng, B. Rowley, W. Pao, A. Hayday, J.B. Bolen, and T. Pawson Syk tyrosine kinase required for mouse viability and B-cell development Nature 378 1995 303 306
17. M.E. Elder, D. Lin, J. Clever, A.C. Chan, T.J. Hope, A. Weiss, and T.G. Parslow Human severe combined immunodeficiency due to a defect in ZAP-70, a T cell tyrosine kinase Science 264 1994 1596 1599
18. M. Turner, P.J. Mee, P.S. Costello, O. Williams, A.A. Price, L.P. Duddy, M.T. Furlong, R.L. Geahlen, and V.L. Tybulewicz Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk Nature 378 1995 298 302
19. A. Mocsai, J. Ruland, and V.L. Tybulewicz The SYK tyrosine kinase: a crucial player in diverse biological functions Nat. Rev. Immunol. 10 2010 387 402
20. F. Abtahian, N. Bezman, R. Clemens, E. Sebzda, L. Cheng, S.J. Shattil, M.L. Kahn, and G.A. Koretzky Evidence for the requirement of ITAM domains but not SLP-76/Gads interaction for integrin signaling in hematopoietic cells Mol. Cell. Biol. 26 2006 6936 6949
21. D.B. Graham, L.M. Stephenson, S.K. Lam, K. Brim, H.M. Lee, J. Bautista, S. Gilfillan, S. Akilesh, K. Fujikawa, and W. Swat An ITAM-signaling pathway controls cross-presentation of particulate but not soluble antigens in dendritic cells J. Exp. Med. 204 2007 2889 2897
22. A. Chaudhary, T.M. Fresquez, and M.J. Naranjo Tyrosine kinase Syk associates with toll-like receptor 4 and regulates signaling in human monocytic cells Immunol. Cell Biol. 85 2007 249 256
23. T. Yamada, S. Lizhong, N. Takahashi, S. Kubo, N. Narita, D. Suzuki, T. Takabayashi, Y. Kimura, and S. Fujieda Poly(I:C) induces BLyS-expression of airway fibroblasts through phosphatidylinositol 3-kinase Cytokine 50 2010 163 169
24. N.C. Rogers, 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 Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins Immunity 22 2005 507 517
25. G. Weiss, K. Maaetoft-Udsen, S.A. Stifter, P. Hertzog, S. Goriely, A.R. Thomsen, S.R. Paludan, and H. Frokiaer MyD88 drives the IFN-beta response to Lactobacillus acidophilus in dendritic cells through a mechanism involving IRF1, IRF3, and IRF7 J. Immunol. 189 2012 2860 2868
26. P.G. Arndt, N. Suzuki, N.J. Avdi, K.C. Malcolm, and G.S. Worthen Lipopolysaccharide-induced c-Jun NH2-terminal kinase activation in human neutrophils: role of phosphatidylinositol 3-kinase and Syk-mediated pathways J. Biol. Chem. 279 2004 10883 10891
27. Y.C. Lin, D.Y. Huang, C.L. Chu, and W.W. Lin Anti-inflammatory actions of Syk inhibitors in macrophages involve non-specific inhibition of toll-like receptors-mediated JNK signaling pathway Mol. Immunol. 47 2010 1569 1578
28. C. Han, J. Jin, S. Xu, H. Liu, N. Li, and X. Cao Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b Nat. Immunol. 11 2010 734 742
29. Y.C. Lin, D.Y. Huang, C.L. Chu, Y.L. Lin, and W.W. Lin The tyrosine kinase Syk differentially regulates Toll-like receptor signaling downstream of the adaptor molecules TRAF6 and TRAF3 Sci. Signal. 6 2013 ra71
30. K. Singer, D.L. Morris, K.E. Oatmen, T. Wang, J. DelProposto, T. Mergian, K.W. Cho, and C.N. Lumeng Neuropeptide Y is produced by adipose tissue macrophages and regulates obesity-induced inflammation PLoS One 8 2013 e57929
31. M.B. Lutz, N. Kukutsch, A.L. Ogilvie, S. Rossner, F. Koch, N. Romani, and G. Schuler An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow J. Immunol. Methods 223 1999 77 92
32. G. Hajishengallis, P. Ratti, and E. Harokopakis Peptide mapping of bacterial fimbrial epitopes interacting with pattern recognition receptors J. Biol. Chem. 280 2005 38902 38913
33. Z. Liu, C.M. Pelfrey, A. Cotleur, J.C. Lee, and R.A. Rudick Immunomodulatory effects of interferon beta-1a in multiple sclerosis J. Neuroimmunol. 112 2001 153 162
34. A.H. van Boxel-Dezaire, M.R. Rani, and G.R. Stark Complex modulation of cell type-specific signaling in response to type I interferons Immunity 25 2006 361 372
35. H. Wang, J. Brown, S. Gao, S. Liang, R. Jotwani, H. Zhou, J. Suttles, D.A. Scott, and R.J. Lamont The role of JAK-3 in regulating TLR-mediated inflammatory cytokine production in innate immune cells J. Immunol. 191 2013 1164 1174
36. T. Fukao, and S. Koyasu PI3K and negative regulation of TLR signaling Trends Immunol. 24 2003 358 363
37. E.Y. Chang, B. Guo, S.E. Doyle, and G. Cheng Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production J. Immunol. 178 2007 6705 6709
38. H. Kuwata, Y. Watanabe, H. Miyoshi, M. Yamamoto, T. Kaisho, K. Takeda, and S. Akira IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-alpha production in macrophages Blood 102 2003 4123 4129
39. K. Onnureddy, S.K. Ravinder, and D. Onteru Singh, IGF-1 attenuates LPS induced pro-inflammatory cytokines expression in buffalo (Bubalus bubalis) granulosa cells Mol. Immunol. 64 2015 136 143
40. S.R. Schow, and A. Joly N-acetyl-leucinyl-leucinyl-norleucinal inhibits lipopolysaccharide-induced NF-kappaB activation and prevents TNF and IL-6 synthesis in vivo Cell. Immunol. 175 1997 199 202
41. S. Xie, B. Liu, S. Fu, W. Wang, Y. Yin, N. Li, W. Chen, J. Liu, and D. Liu GLP-2 suppresses LPS-induced inflammation in macrophages by inhibiting ERK phosphorylation and NF-kappaB activation Cell. Physiol. Biochem. 34 2014 590 602
42. K. Jiang, B. Zhong, D.L. Gilvary, B.C. Corliss, E. Vivier, E. Hong-Geller, S. Wei, and J.Y. Djeu Syk regulation of phosphoinositide 3-kinase-dependent NK cell function J. Immunol. 168 2002 3155 3164
43. M.H. Laird, S.H. Rhee, D.J. Perkins, A.E. Medvedev, W. Piao, M.J. Fenton, and S.N. Vogel TLR4/MyD88/PI3K interactions regulate TLR4 signaling J. Leukoc. Biol. 85 2009 966 977
44. C.A. Lowell Src-family and Syk kinases in activating and inhibitory pathways in innate immune cells: signaling cross talk Cold Spring Harb. Perspect. Biol. 3 2011
45. K. Sada, T. Takano, S. Yanagi, and H. Yamamura Structure and function of Syk protein-tyrosine kinase J. Biochem. 130 2001 177 186
46. K.M. Brumbaugh, B.A. Binstadt, D.D. Billadeau, R.A. Schoon, C.J. Dick, R.M. Ten, and P.J. Leibson Functional role for Syk tyrosine kinase in natural killer cell-mediated natural cytotoxicity J. Exp. Med. 186 1997 1965 1974
47. M.A. Beaven, and R.A. Baumgartner Downstream signals initiated in mast cells by Fc epsilon RI and other receptors Curr. Opin. Immunol. 8 1996 766 772
48. N. Blanco-Menendez, C. Del Fresno, S. Fernandes, E. Calvo, R. Conde-Garrosa, W.G. Kerr, and D. Sancho SHIP-1 couples to the Dectin-1 hemITAM and selectively modulates reactive oxygen species production in dendritic cells in response to Candida albicans J. Immunol. 2015
49. G.D. Brown Dectin-1: a signalling non-TLR pattern-recognition receptor Nat. Rev. Immunol. 6 2006 33 43
50. T. Kurosaki, and S. Tsukada BLNK: connecting Syk and Btk to calcium signals Immunity 12 2000 1 5
51. K. Suzuki-Inoue Essential in vivo roles of the platelet activation receptor CLEC-2 in tumour metastasis, lymphangiogenesis and thrombus formation J. Biochem. 150 2011 127 132
52. A. Mocsai, M.B. Humphrey, J.A. Van Ziffle, Y. Hu, A. Burghardt, S.C. Spusta, S. Majumdar, L.L. Lanier, C.A. Lowell, and M.C. Nakamura The immunomodulatory adapter proteins DAP12 and Fc receptor gamma-chain (FcRgamma) regulate development of functional osteoclasts through the Syk tyrosine kinase Proc. Natl. Acad. Sci. U. S. A. 101 2004 6158 6163
53. P.J. Coopman, and S.C. Mueller The Syk tyrosine kinase: a new negative regulator in tumor growth and progression Cancer Lett. 241 2006 159 173
54. H. Wang, A. Kumar, R.J. Lamont, and D.A. Scott GSK3beta and the control of infectious bacterial diseases Trends Microbiol. 22 2014 208 217
55. E. Harokopakis, M.H. Albzreh, M.H. Martin, and G. Hajishengallis TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae J. Immunol. 176 2006 7645 7656
56. J. Brown, H. Wang, J. Suttles, D.T. Graves, and M. Martin Mammalian target of rapamycin complex 2 (mTORC2) negatively regulates Toll-like receptor 4-mediated inflammatory response via FoxO1 J. Biol. Chem. 286 2011 44295 44305
57. H.G. Kim, B. Shrestha, S.Y. Lim, D.H. Yoon, W.C. Chang, D.J. Shin, S.K. Han, S.M. Park, J.H. Park, H.I. Park, J.M. Sung, Y. Jang, N. Chung, K.C. Hwang, and T.W. Kim Cordycepin inhibits lipopolysaccharide-induced inflammation by the suppression of NF-kappaB through Akt and p38 inhibition in RAW 264.7 macrophage cells Eur. J. Pharmacol. 545 2006 192 199
58. E. Shen, J. Fan, and T. Peng Glycogen synthase kinase-3beta suppresses tumor necrosis factor-alpha expression in cardiomyocytes during lipopolysaccharide stimulation J. Cell. Biochem. 104 2008 329 338
59. E. Rodionova, M. Conzelmann, E. Maraskovsky, M. Hess, M. Kirsch, T. Giese, A.D. Ho, M. Zoller, P. Dreger, and T. Luft GSK-3 mediates differentiation and activation of proinflammatory dendritic cells Blood 109 2007 1584 1592