Fucose-specific DC-SIGN signalling directs T helper cell type-2 responses via IKKε-and CYLD-dependent Bcl3 activation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Gringhuis, Sonja I ^a   Kaptein, Tanja M ^a   Wevers, Brigitte A ^a   Mesman, Annelies W ^a   Geijtenbeek, Teunis B H ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD209 ANTIGEN; CYLD DEUBIQUITINASE; FUCOSE; I KAPPA B KINASE EPSILON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; LSP1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 2; PROTEIN; PROTEIN BCL 3; PROTEIN SERINE THREONINE KINASE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; AUTACOID; CD15 ANTIGEN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; CHEMOKINE; CYLD PROTEIN, HUMAN; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; I KAPPA B KINASE; LECTIN; LIPOPOLYSACCHARIDE; LSP1 PROTEIN, HUMAN; MESSENGER RNA; ONCOPROTEIN; PHOSPHOSERINE; PROTEIN BINDING; PROTO-ONCOGENE PROTEIN BCL-3; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

CARBOHYDRATE; DISEASE CONTROL; ENZYME ACTIVITY; MICROBIAL COMMUNITY; PATHOGEN; SIGNALING;

ADAPTIVE IMMUNITY; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI; SIGNAL TRANSDUCTION; TH1 CELL; TH2 CELL; TRANSCRIPTION INITIATION; ANIMAL; BIOLOGICAL MODEL; CELL POLARITY; DOWN REGULATION; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; UPREGULATION;

ANIMALS; ANTIGENS, CD15; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL POLARITY; CHEMOKINES; DOWN-REGULATION; ENZYME ACTIVATION; FUCOSE; HELICOBACTER PYLORI; HUMANS; I-KAPPA B KINASE; INFLAMMATION MEDIATORS; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; NF-KAPPA B; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RECEPTORS, CELL SURFACE; RNA, MESSENGER; SCHISTOSOMA MANSONI; SIGNAL TRANSDUCTION; TH2 CELLS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84901707773     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4898     Document Type: Article

References (54)

1. Steinman, R. M. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30, 1-22 (2012).
2. Guermonprez, P., Valladeau, J., Zitvogel, L., Théry, C. & Amigorena, S. Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20, 621-667 (2002). (Pubitemid 34293436)
3. Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783-801 (2006). (Pubitemid 43261452)
4. Iwasaki, A. & Medzhitov, R. Regulation of adaptive immunity by the innate immune system. Science 327, 291-295 (2010).
5. Pulendran, B., Tang, H. & Manicassamy, S. Programming dendritic cells to induce TH2 and tolerogenic responses. Nat. Immunol. 11, 647-655 (2010).
6. Zhu, J., Yamane, H. & Paul, W. E. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489 (2010).
7. Nish, S. & Medzhitov, R. Host defense pathways: role of redundancy and compensation in infectious disease phenotypes. Immunity 34, 629-636 (2011).
8. Kawai, T. & Akira, S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650 (2011).
9. Geijtenbeek, T. B. H. & Gringhuis, S. I. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9, 465-479 (2009).
10. Appelmelk, B. J. et al. Carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells. J. Immunol. 170, 1635-1639 (2003). (Pubitemid 36197376)
11. Gringhuis, S. I., den Dunnen, J., Litjens, M., van der Vlist, M. & Geijtenbeek, T. B. H. Carbohydrate-specific signalling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 10, 1081-1088 (2009).
12. Gringhuis, S. I. et al. C-type lectin DC-SIGN modulates toll-like receptor signalling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappa B. Immunity 26, 605-616 (2007). (Pubitemid 46756345)
13. Bergman, M. P. et al. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J. Exp. Med. 200, 979-990 (2004). (Pubitemid 39431123)
14. van Die, I. et al. The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis X. Glycobiology 13, 471-478 (2003).
15. van Liempt, E. et al. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol. Immunol. 44, 2605-2615 (2007).
16. Goriely, S., Neurath, M. F. & Goldman, M. How microorganisms tip the balance between interleukin-12 family members. Nat. Rev. Immunol. 8, 81-86 (2008).
17. Ghosh, S. & Hayden, M. S. New regulators of NF-[kappa]B in inflammation. Nat. Rev. Immunol. 8, 837-848 (2008).
18. Vallabhapurapu, S. & Karin, M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu. Rev. Immunol. 27, 693-733 (2009).
19. Creusot, R. J. NF-[kappa]B in DCs: it takes effort to be immature. Nat. Med. 17, 1554-1556 (2011).
20. Mühlbauer, M., Chilton, P. M., Mitchell, T. C. & Jobin, C. Impaired Bcl3 up-regulation leads to enhanced lipopolysaccharide-induced interleukin (IL)-23p19 gene expression in IL-10-/-Mice. J. Biol. Chem. 283, 14182-14189 (2008).
21. Wessells, J. et al. BCL-3 and NF-kappaB p50 attenuate lipopolysaccharide-induced inflammatory responses in macrophages. J. Biol. Chem. 279, 49995-50003 (2004). (Pubitemid 39577809)
22. Massoumi, R., Chmielarska, K., Hennecke, K., Pfeifer, A. & Fassler, R. Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signalling. Cell 125, 665-677 (2006).
23. Hutti, J. E. et al. Phosphorylation of the tumor suppressor CYLD by the breast cancer oncogene IKKepsilon promotes cell transformation. Mol. Cell 34, 461-472 (2009)
24. Sun, S. C. Deubiquitylation and regulation of the immune response. Nat. Rev. Immunol. 8, 501-511 (2008).
25. Sun, S. C. CYLD: a tumor suppressor deubiquitinase regulating NF-[kappa]B activation and diverse biological processes. Cell Death Differ. 17, 25-34 (2009).
26. Clark, K., Plater, L., Peggie, M. & Cohen, P. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J. Biol. Chem. 284, 14136-14146 (2009).
27. Kishore, N. et al. IKK-i and TBK-1 are enzymatically distinct from the homologous enzyme IKK-2: comparative analysis of recombinant human IKK-i, TBK-1, and IKK-2. J. Biol. Chem. 277, 13840-13847 (2002). (Pubitemid 34967989)
28. Huang, C. K., Zhan, L., Ai, Y. & Jongstra, J. LSP1 is the major substrate for mitogen-activated protein kinase-activated protein kinase 2 in human neutrophils. J. Biol. Chem. 272, 17-19 (1997). (Pubitemid 27021115)
29. Wu, Y. et al. MAPKAPK2-mediated LSP1 phosphorylation and FMLP-induced neutrophil polarization. Biochem. Biophys. Res. Commun. 358, 170-175 (2007). (Pubitemid 46719098)
30. Lukacs, N. W. Role of chemokines in the pathogenesis of asthma. Nat. Rev. Immunol. 1, 108-116 (2001). (Pubitemid 33741964)
31. van Die, I. & Cummings, R. D. Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response? Glycobiology 20, 2-12 (2010).
32. Thomas, P. G. et al. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171, 5837-5841 (2003). (Pubitemid 37467200)
33. van der Kleij, D. et al. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122-48129 (2002).
34. Vanhoutte, F. et al. Toll-like receptor (TLR)2 and TLR3 sensing is required for dendritic cell activation, but dispensable to control Schistosoma mansoni infection and pathology. Microbes Infect. 9, 1606-1613 (2007). (Pubitemid 350225744)
35. Muller, A., Oertli, M. & Arnold, I. C. H. pylori exploits and manipulates innate and adaptive immune cell signalling pathways to establish persistent infection. Cell. Commun. Signal. 9, 25 (2011).
36. de Jong, E. C. et al. 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 (2002). (Pubitemid 34135767)
37. Gringhuis, S. I. et al. HIV-1 exploits innate signalling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 11, 419-426 (2010).
38. Hovius, J. W. et al. Salp15 binding to DC-SIGN inhibits cytokine expression by impairing both nucleosome remodeling and mRNA stabilization. PLoS Pathog. 4, e31 (2008).
39. Menon, S. et al. Binding-site geometry and flexibility in DC-SIGN demonstrated with surface force measurements. Proc. Natl Acad. Sci. USA 106, 11524-11529 (2009).
40. Chau, T. L. et al. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated? Trends Biochem. Sci. 33, 171-180 (2008).
41. Bergman, M., Del Prete, G., van Kooyk, Y. & Appelmelk, B. Helicobacter pylori phase variation, immune modulation and gastric autoimmunity. Nat. Rev. Micro. 4, 151-159 (2006). (Pubitemid 43158158)
42. Chen, F. et al. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 18, 260-266 (2012).
43. Allen, J. E. & Maizels, R. M. Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 11, 375-388 (2011).
44. Everts, B. et al. Schistosome-derived omega-1 drives Th2 polarization by suppressing protein synthesis following internalization by the mannose receptor. J. Exp. Med. 209, 1753-1767 (2012).
45. Korn, T., Bettelli, E., Oukka, M. & Kuchroo, V. K. IL-17 and Th17 cells. Annu. Rev. Immunol. 27, 485-517 (2009).
46. Mbow, M. et al. T-helper 17 cells are associated with pathology in human schistosomiasis. J. Infect. Dis. 207, 186-195 (2013).
47. Larkin, B. et al. Induction and regulation of pathogenic Th17 cell responses in schistosomiasis. Semin. Immunopathol. 34, 873-888 (2012).
48. Kuijk, L. M. et al. Soluble helminth products suppress clinical signs in murine experimental autoimmune encephalomyelitis and differentially modulate human dendritic cell activation. Mol. Immunol. 51, 210-218 (2012).
49. Summers, R. W., Elliott, D. E., Urban, J. F., Thompson, R. & Weinstock, J. V. Trichuris suis therapy in Crohn's disease. Gut 54, 87-90 (2005). (Pubitemid 40007223)
50. Geijtenbeek, T. B. et al. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100, 575-585 (2000).
51. Cuenda, A. et al. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364, 229-233 (1995).
52. Lukas, S. M. et al. Catalysis and function of the p38alpha-MK2a signalling complex. Biochemistry 43, 9950-9960 (2004). (Pubitemid 39030885)
53. Boink, G. J. J. et al. Engineering physiologically controlled pacemaker cells with lentiviral HCN4 gene transfer. J. Gene Med. 10, 487-497 (2008). (Pubitemid 351753518)
54. Arrighi, J.-F. et al. Lentivirus-mediated RNA interference of DC-SIGN expression inhibits human immunodeficiency virus transmission from dendritic cells to T cells. J. Virol. 78, 10848-10855 (2004). (Pubitemid 39299625)