Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori

Nature Immunology

Volumn 10, Issue 10, 2009, Pages 1081-1088

  Gringhuis, Sonja I ^a,b   den Dunnen, Jeroen ^a,b   Litjens, Manja ^b   van der Vlist, Michiel ^a,b   Geijtenbeek, Teunis B H ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARBOHYDRATE; CD209 ANTIGEN; DECTIN 1; FRUCTOSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; MANNOSE; PROTEIN CNK; PROTEIN KSR1; PROTEIN LSP1; RAF PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCAFFOLD PROTEIN; SIGN SIGNALOSOME; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL IMMUNITY; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISSOCIATION; ENZYME ACTIVATION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOREGULATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VIRUS IMMUNITY;

BLOTTING, WESTERN; CARBOHYDRATES; CELL ADHESION MOLECULES; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FUCOSE; HELICOBACTER PYLORI; HIV-1; HUMANS; LECTINS, C-TYPE; MANNOSE; MICROFILAMENT PROTEINS; MYCOBACTERIUM TUBERCULOSIS; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-RAF; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 70349201241     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1778     Document Type: Article

References (48)

1. Ueno, H. et al. Dendritic cell subsets in health and disease. Immunol. Rev. 219, 118-142 (2007).
2. Medzhitov, R. Recognition of microorganisms and activation of the immune response. Nature 449, 819-826 (2007).
3. Wilson, C.B., Rowell, E. & Sekimata, M. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 9, 91-105 (2009).
4. Kanneganti, T.D., Lamkanfi, M. & Núñez, G. Intracellular NOD-like receptors in host defense and disease. Immunity 27, 549-559 (2007).
5. Meylan, E. & Tschopp, J. Toll-Like Receptors and RNA helicases: Two parallel ways to trigger antiviral responses. Mol. Cell 22, 561-569 (2006).
6. O'Neill, L.A.J. When signaling pathways collide: Positive and negative regulation of Toll-like receptor signal transduction. Immunity 29, 12-20 (2008).
7. Robinson, M.J., Sancho, D., Slack, E.C., LeibundGut-Landmann, S. & Sousa, C.R.E. Myeloid C-type lectins in innate immunity. Nat. Immunol. 7, 1258-1265 (2006).
8. Sansonetti, P.J. The innate signaling of dangers and the dangers of innate signaling. Nat. Immunol. 7, 1237-1242 (2006).
9. Kawai, T. & Akira, S. TLR signaling. Cell Death Differ. 13, 816-825 (2006).
10. O'Neill, L.A.J. & Bowie, A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7 353-364 (2007).
11. Ouaaz, F., Arron, J., Zheng, Y., Choi, Y. & Beg, A.A. Dendritic cell development and survival require distinct NF-κB subunits. Immunity 16, 257-270 (2002).
12. Geijtenbeek, T.B.H. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003).
13. Underhill, D.M. Collaboration between the innate immune receptors dectin-1, TLRs, and Nods. Immunol. Rev. 219, 75-87 (2007).
14. Geijtenbeek, T.B.H. & Gringhuis, S.I. Signalling through C-type lectin receptors: Shaping immune responses. Nat. Rev. Immunol. 9, 465-479 (2009).
15. 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).
16. van Kooyk, Y. & Geijtenbeek, T.B.H. DC-SIGN: Escape mechanism for pathogens. Nat. Rev. Immunol. 3, 697-709 (2003).
17. Feinberg, H., Mitchell, D.A., Drickamer, K. & Weis, W.I. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294, 2163-2166 (2001).
18. 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).
19. Smits, H.H. et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J. Allergy Clin. Immunol. 115, 1260-1267 (2005).
20. Steeghs, L. et al. Neisseria meningitidis expressing lgtB lipopolysaccharide targets DC-SIGN and modulates dendritic cell function. Cell. Microbiol. 8, 316-325 (2006).
21. 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).
22. Gringhuis, S.I. et al. C-type lectin DC-SIGN modulates toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-κB. Immunity 26, 605-616 (2007).
23. Wellbrock, C., Karasarides, M. & Marais, R. The Raf proteins take centre stage. Nat. Rev. Mol. Cell Biol. 5, 875-885 (2004).
24. Geijtenbeek, T.B.H. et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587-597 (2000).
25. Hong, P.W.P. et al. Human immunodeficiency virus envelope (gp120) binding to DC-SIGN and primary dendritic cells is carbohydrate dependent but does not involve 2G12 or cyanovirin binding sites: Implications for structural analyses of gp120-DC-SIGN binding. J. Virol. 76, 12855-12865 (2002).
26. 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).
27. van Gisbergen, K.P.J.M., Sanchez-Hernandez, M., Geijtenbeek, T.B.H. & van Kooyk, Y. Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 201, 1281-1292 (2005).
28. Smith, A.L. et al. Leukocyte-specific protein 1 interacts with DC-SIGN and mediates transport of HIV to the proteasome in dendritic cells. J. Exp. Med. 204, 421-430 (2007).
29. Harrison, R.E., Sikorski, B.A. & Jongstra, J. Leukocyte-specific protein 1 targets the ERK/MAP kinase scaffold protein KSR and MEK1 and ERK2 to the actin cytoskeleton. J. Cell Sci. 117, 2151-2157 (2004).
30. Douziech, M., Sahmi, M., Laberge, G. & Therrien, M.A. KSR/CNK complex mediated by HYP, a novel SAM domain-containing protein, regulates RAS-dependent RAF activation in Drosophila. Genes Dev. 20, 807-819 (2006).
31. Hodges, A. et al. Activation of the lectin DC-SIGN induces an immature dendritic cell phenotype triggering Rho-GTPase activity required for HIV-1 replication. Nat. Immunol. 8, 569-577 (2007).
32. Dhillon, A.S., von, K.A., Grindlay, J. & Kolch, W. Phosphatase and feedback regulation of Raf-1 signaling. Cell Cycle 6, 3-7 (2007).
33. Yadav, M. & Schorey, J.S. The β-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108, 3168-3175 (2006).
34. Appelmelk, B.J. et al. The mannose cap of mycobacterial lipoarabinomannan does not dominate the Mycobacterium-host interaction. Cell. Microbiol. 10, 930-944 (2008).
35. Shaw, A.S. & Filbert, E.L. Scaffold proteins and immune-cell signalling. Nat. Rev. Immunol. 9, 47-56 (2009).
36. Dhanasekaran, D.N., Kashef, K., Lee, C.M., Xu, H. & Reddy, E.P. Scaffold proteins of MAP-kinase modules. Oncogene 26, 3185-3202 (2007).
37. Taya, S. et al. Direct interaction of insulin-like growth factor-1 receptor with leukemia-associated RhoGEF. J. Cell Biol. 155, 809-820 (2001).
38. Jaffe, A.B., Aspenstrom, P. & Hall, A. Human CNK1 acts as a scaffold protein, linking Rho and Ras signal transduction pathways. Mol. Cell. Biol. 24, 1736-1746 (2004).
39. Ziogas, A., Moelling, K. & Radziwill, G. CNK1 is a scaffold protein that regulates Src-mediated Raf-1 activation. J. Biol. Chem. 280, 24205-24211 (2005).
40. Kolch, W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6, 827-837 (2005).
41. Matheny, S.A. et al. Ras regulates assembly of mitogenic signalling complexes through the effector protein IMP. Nature 427, 256-260 (2004).
42. Guo, Y. et al. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat. Struct. Mol. Biol. 11, 591-598 (2004).
43. Madura Larsen, J. et al. BCG stimulated dendritic cells induce an interleukin-10 producing T-cell population with no T helper 1 or T helper 2 bias in vitro. Immunology 121, 276-282 (2007).
44. 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).
45. Uematsu, S. & Akira, S. Toll-Like receptors (TLRs) and their ligands. Handb. Exp. Pharmacol. 183, 1-20 (2008).
46. Hanke, J.H. et al. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701 (1996).
47. Gringhuis, S.I. et al. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-κB activation through Raf-1 and Syk. Nat. Immunol. 10, 203-213 (2009).
48. Remans, P.H.J. et al. Rap1 signaling is required for suppression of Ras-generated reactive oxygen species and protection against oxidative stress in T lymphocytes. J. Immunol. 173, 920-931 (2004).