MGL signaling augments TLR2-mediated responses for enhanced IL-10 and TNF-α secretion

Journal of Leukocyte Biology

Volumn 94, Issue 2, 2013, Pages 315-323

  van Vliet, Sandra J ^a   Bay, Sylvie ^b,d   Vuist, Ilona M ^a   Kalay, Hakan ^a   García Vallejo, Juan J ^a   Leclerc, Claude ^c,e   van Kooyk, Yvette ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Unité de Chimie des Biomolécules   (France)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

^e INSERM   (France)

Author keywords

C type lectin; Dendritic cells; Macrophage galactose type lectin; Tn antigen

Indexed keywords

ANTIBODY; CARBOHYDRATE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P70; LECTIN; LIGAND; MACROPHAGE GALACTOSE TYPE LECTIN; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL MATURATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PHOSPHORYLATION; PRIORITY JOURNAL; STIMULATION; TH2 CELL;

C-TYPE LECTIN; DENDRITIC CELLS; MACROPHAGE GALACTOSE-TYPE LECTIN; TN ANTIGEN;

ACETYLGALACTOSAMINE; AMINO ACID SEQUENCE; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; ANTIGENS, VIRAL; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DENDRITIC CELLS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INTERLEUKIN-10; LECTINS, C-TYPE; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PEPTIDE FRAGMENTS; PHOSPHORYLATION; POLIOVIRUS; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA STABILITY; TETANUS TOXIN; TOLL-LIKE RECEPTOR 2; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880976282     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1012520     Document Type: Article

References (45)

1. Kawai, T., Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384.
2. Medzhitov, R., Janeway C. A., (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296, 298-300.
3. Matzinger, P. (2002) The danger model: a renewed sense of self. Science 296, 301-305.
4. Vabulas, R. M., Ahmad-Nejad, P., Ghose, S., Kirschning, C. J., Issels, R. D., Wagner, H. (2002) HSP70 as endogenous stimulus of the Toll/ interleukin-1 receptor signal pathway. J. Biol. Chem. 277, 15107-15112.
5. Kawai, T., Akira, S. (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650.
6. Van den Berg, L. M., Gringhuis, S. I., Geijtenbeek, T. B. (2012) An evolutionary perspective on C-type lectins in infection and immunity. Ann. N. Y. Acad. Sci. 1253, 149-158.
7. Sancho, D., Reise Sousa, C. (2012) Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 30, 491-529.
8. Varki, A. (2011) Since there are PAMPs and DAMPs, there must be SAMPs? Glycan self-associated molecular patterns dampen innate immunity, but pathogens can mimic them. Glycobiology 21, 1121-1124.
9. Gringhuis, S. I., den Dunnen, J., Litjens, M., van het Hof, B., van Kooyk Y., Geijtenbeek, T. B. (2007) C-Type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kB. Immunity 26, 605-616.
10. Kanazawa, N., Okazaki, T, Nishimura, H., Tashiro, K, Inaba, K, Miyachi, Y. (2002) DCIR acts as an inhibitory receptor depending on its immunoreceptor tyrosine-based inhibitory motif J. Invest. Dermatol. 118, 261-266.
11. Meyer-Wentrup, F., Benitez-Ribas, D., Tacken, P. J., Punt, C. J., Figdor, C. G., de Vries, I. J., Adema, G. J. (2008) Targeting DCIR on human plasmacytoid dendritic cells results in antigen presentation and inhibits IFN-a production. Blood 111, 4245-4253.
12. Li, D., Romain, G., Flamar, A. L., Duluc, D., Dullaers, M., Li, X. H., Zu-rawski, S., Bosquet, N., Palucka, A. K, Le Grand, R., O'Garra, A., Zu-rawski, G., Banchereau, J., Oh, S. (2012) Targeting self-and foreign antigens to dendritic cells via DC-ASGPR generates IL-10-producing suppressive CD4+ T cells.J. Exp. Med. 209, 109-121.
13. Freire, T., Zhang, X., Deriaud, E., Ganneau, C, Vichier-Guerre, S., Az-ria, E., Launay, O., Lo-Man, R., Bay, S., Leclerc, C. (2010) Glycosidic Tn-based vaccines targeting dermal dendritic cells favor germinal center B-cell development and potent antibody response in the absence of adjuvant. Blood 116, 3526-3536.
14. Van Vliet, S. J., van Liempt, E., Geijtenbeek, T. B., van Kooyk, Y. (2006) Differential regulation of C-type lectin expression on tolerogenic dendritic cell subsets. Immunobiology 211, 577-585.
15. Raes, G., Brys, L., Dahal, B. K, Brandt, J., Grooten, J., Brombacher, F., Vanham, G., Noel, W., Bogaert, P., Boonefaes, T., Kindt, A., Van den Bergh, R., Leenen, P. J., De Baetselier, P., Ghassabeh, G. H. (2005) Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J. Leukoc. Biol. 77, 321-327.
16. Van Vliet, S. J., van Liempt, E., Saeland, E., Aarnoudse, C. A., Ap-pelmelk, B., Irimura, T., Geijtenbeek, T. B., Blixt, O., Alvarez, R., van Die, I., van Kooyk, Y (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int. Immunol. 17, 661-669.
17. Van Vliet, S. J., Aarnoudse, C. A., Broks van den Berg, V C, Boks, M., Geijtenbeek, T. B., van Kooyk, Y (2007) MGL-mediated internalization and antigen presentation by dendritic cells: a role for tyrosine-5. Eur. J. Immunol. 37, 2075-2081.
18. Singh, S. K, Streng-Ouwehand, I., Litjens, M., Kalay, H., Saeland, E., van Kooyk, Y. (2011) Tumour-associated glycan modifications of antigen enhance MGL2 dependent uptake and MHC class I restricted CD8 T cell responses. Int. J. Cancer 128, 1371-1383.
19. Holzberg, D., Knight, C. G., Dittrich-Breiholz, O., Schneider, H., Dorrie, A, Hoffmann, E., Resch, K, Kracht, M. (2003) Disruption of the c-JUN-JNK complex by a cell-permeable peptide containing the c-JUN S domain induces apoptosis and affects a distinct set of interleukin-1-induced inflammatory genes. J. Biol. Chem. 278, 40213-40223.
20. Lo-Man, R., Vichier-Guerre, S., Perraut, R., Deriaud, E., Huteau, V., BenMohamed, L., Diop, O. M., Livingston, P. O., Bay, S., Leclerc, C. (2004) A fully synthetic therapeutic vaccine candidate targeting carcinoma-associated Tn carbohydrate antigen induces tumor-specific antibodies in nonhuman primates. Cancer Res. 64, 4987-4994.
21. Latz, E., Visintin, A., Lien, E., Fitzgerald, K A., Monks, B. G., Kurt-Jones, E. A., Golenbock, D. T., Espevik, T. (2002) Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the Toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J. Biol. Chem. 277, 47834-47843.
22. Garcia-Vallejo, J. J., van het Hof, B., Robben, J., van Wijk, J. A, van Die, I., Jozi-asse, D. H., van Dijk, W. (2004) Approach for defining endogenous reference genes in gene expression experiments. Anal. Biochem. 329, 293-299.
23. Appelmelk, B. J., van Die, I., van Vliet, S. J., Vandenbroucke-Grauls, C. M., Geijtenbeek, T. B., van Kooyk, Y (2003) Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grab-bing nonintegrin on dendritic cells. J. Immunol 170, 1635-1639.
24. Napoletano, C., Zizzari, G, Rughetti, A, Rahimi, H., Irimura, T, Clausen, H, Wandall, H H., Belleudi, F., Bellati, F., Pierelli, L., Frati, L., Nuti, M. (2012) Targeting of macrophage galactose-type C-type lectin (MGL) induces DC signaling and activation. Eur. J. Immunol 42, 936-945.
25. MacKenzie, S., Fernandez-Troy, N., Espel, E. (2002) Post-transcriptional regulation of TNF-a during in vitro differentiation of human monocytes/macrophages in primary culture. J. Leukoc. Biol. 71, 1026-1032.
26. Saraiva, M., O'Garra, A. (2010) The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170-181.
27. Wang, S., Villablanca, E. J., De Calisto, J., Gomes, D. C, Nguyen, D. D., Mizo-guchi, E., Kagan, J. C, Reinecker, H. C, Hacohen, N, Nagler, C, Xavier, R. J., Rossi-Bergmann, B., Chen, Y B., Blomhoff, R., Snapper, S. B., Mora, J. R (2011) MyD88-dependent TLR1/2 signals educate dendritic cells with gut-specific imprinting properties. J. Immunol. 187, 141-150.
28. Liu, Y., Shepherd, E. G., Nelin, L. D. (2007) MAPK phosphatases-regulating the immune response. Nat. Rev. Immunol. 7, 202-212.
29. Xing, J., Ginty, D. D., Greenberg, M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
30. Caparros, E., Munoz, P., Sierra-Filardi, E., Serrano-Gomez, D., Puig-Kroger, A., Rodriguez-Fernandez, J. L., Mellado, M., Sancho, J., Zubiaur, M., Corbi, A. L. (2006) DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 107, 3950-3958.
31. Slack, E. C, Robinson, M. J., Hernanz-Falcon, P., Brown, G. D., Williams, D. L., Schweighoffer, E., Tybulewicz, V. L., Reise Sousa, C. (2007) Syk-dependent ERK activation regulates IL-2 and IL-10 production by DC stimulated with zymosan. Eur. J. Immunol, 37, 1600-1612.
32. Gringhuis, S. I., den Dunnen, J., Litjens, M., van der Vlist, M., Geijtenbeek, T. B. (2009) Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori Nat. Immunol. 10, 1081-1088.
33. Alvarez, Y., Municio, C, Alonso, S., Sanchez, C. M., Fernandez, N. (2009) The induction of IL-10 by zymosan in dendritic cells depends on CREB activation by the coactivators CREB-binding protein and TORC2 and autocrine PGE2. J. Immunol. 183, 1471-1479.
34. Rogers, N. C, Slack, E. C, Edwards, A. D., Nolte, M. A., Schulz, O., Schweighoffer, E., Williams, D. L., Gordon, S., Tybulewicz, V. L., Brown, G.D., Reise Sousa, C. (2005) Syk-dependent cytokine induction by Dec-tin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22, 507-517.
35. Kelly, E. K, Wang, L., Ivashkiv, L. B. (2010) Calcium-activated pathways and oxidative burst mediate zymosan-induced signaling and IL-10 production in human macrophages. J. Immunol. 184, 5545-5552.
36. Dennehy, K M., Ferwerda, G, Faro-Trindade, I., Pyz, E., Willment, J. A, Taylor, P. R., Kerrigan, A, Tsoni, S. V, Gordon, S., Meyer-Wentrup, F., Adema, G. J., Kullberg, B.J., Schweighoffer, E., Tybulewicz, V, Mora-Montes, H. M., Gow, N A., Williams, D. L., Netea, M. G., Brown, G D. (2008) Syk kinase is required for collaborative cytokine production induced through Dectin-1 and Toll-like receptors. Eur. J. Immunol. 38, 500-506.
37. Gringhuis, S. I., den Dunnen, J., Litjens, M., van der Vlist, M., Wevers, B., Bruijns, S. C, Geijtenbeek, T. B. (2009) Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kB activation through Raf-1 and Syk. Nat. Immunol. 10, 203-213.
38. Eberle, M. E., Dalpke, A. H. (2012) Dectin-1 stimulation induces suppressor of cytokine signaling 1, thereby modulating TLR signaling and T cell responses. J. Immunol. 188, 5644-5654.
39. Srivastava, V, Manchanda, M., Gupta, S., Singla, R., Behera, D., Das, G., Natarajan, K (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.
40. Mansell, A., Smith, R., Doyle, S. L., Gray, P., Fenner, J. E., Crack, P. J., Nicholson, S. E., Hilton, D. J., O'Neill, L. A., Hertzog, P.J. (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat. Immunol. 7, 148-155.
41. Madonna, S., Scarponi, C, De Pita, O., Albanesi, C. (2008) Suppressor of cytokine signaling 1 inhibits IFN-7 inflammatory signaling in human keratinocytes by sustaining ERK1/2 activation. FASEBJ. 22, 3287-3297.
42. Saeland, E., van Vliet, S. J., Backstrom, M., van den Berg, V. C, Geijtenbeek, T. B., Meijer, G. A., van Kooyk, Y. (2007) The C-type lectin MGL expressed by dendritic cells detects glycan changes on MUC1 in colon carcinoma. Cancer Immunol. Immunother. 56, 1225-1236.
43. Usami, K, Matsuno, K, Igarashi, M., Denda-Nagai, K, Takada, A., Irimura, T. (2011) Involvement of viral envelope GP2 in Ebola virus entry into cells expressing the macrophage galactose-type C-type lectin. Biochem. Biophys. Res. Commun. 407, 74-78.
44. Van Sorge, N. M., Bleumink, N M., van Vliet, S. J., Saeland, E., van der Pol, W. L., van Kooyk, Y, van Putten, J. P. (2009) N-glycosylated proteins and distinct lipooligosaccharide glycoforms of Campylobacter jejuni target the human C-type lectin receptor MGL. Cell Microbiol. 11, 1768-1781.
45. Van Vliet, S. J., Steeghs, L., Bruijns, S. C, Vaezirad, M. M., Snijders, B. C, Renas Busto, J. A., Deken, M., van Putten, J. P., van Kooyk, Y (2009) Variation of Neisseria gonorrhoeae lipooligosaccharide directs dendritic cell-induced T helper responses. PLoS Pathog. 5, e1000625.