Targeting of macrophage galactose-type C-type lectin (MGL) induces DC signaling and activation

European Journal of Immunology

Volumn 42, Issue 4, 2012, Pages 936-945

  Napoletano, Chiara ^a   Zizzari, Ilaria G ^a   Rughetti, Aurelia ^a   Rahimi, Hassan ^a   Irimura, Tatsuro ^b   Clausen, Henrik ^c   Wandall, Hans H ^c   Belleudi, Francesca ^d   Bellati, Filippo ^e   Pierelli, Luca ^a   Frati, Luigi ^a   Nuti, Marianna ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

C type lectins; Dendritic cells; Macrophage galactose type C type lectin (MGL); MUC1; Tn tumor associated antigens

Indexed keywords

DENDRITIC CELL VACCINE; GALACTOSE; GALACTOSE TYPE C LECTIN RECEPTOR; GLYCOPEPTIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LECTIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 3; N ACETYLGALACTOSAMINE; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ARTICLE; CANCER IMMUNOTHERAPY; DENDRITIC CELL; HUMAN; MACROPHAGE; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACETYLGLUCOSAMINE; ANTIGENS, NEOPLASM; CALCIUM; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DENDRITIC CELLS; HUMANS; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUCIN-1; NF-KAPPA B; PHOSPHORYLATION; UP-REGULATION;

EID: 84860247180     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142086     Document Type: Article

References (43)

1. van Vliet, S. J., García-Vallejo, J. J. and van Kooyk, Y., Dendritic cells and C-type lectin receptors: coupling innate to adaptive immune responses. Immunol. Cell. Biol. 2008. 86: 580-587.
2. Cummings, R. D. and McEver, R. P., C-type Lectins. In Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W. et al. (Eds.), Essentials of glycobiology, 2nd edition, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2009, Chapter 31.
3. Zelensky, A. N. and Gready, J. E., The C-type lectin-like domain superfamily. FEBS J. 2005. 272: 6179-6217.
4. Geijtenbeek, T. B. and Gringhuis, S. I., Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 2009. 9: 465-479.
5. Raes, G., Brys, L., Dahal, B. K., Brandt, J., Grooten, J., Brombacher, F., Vanham, G. et al., Macrophage galactose-type C-type lectins as novel markers for alternatively activated macrophages elicited by parasitic infections and allergic airway inflammation. J. Leukoc. Biol. 2005. 77: 321-327.
6. van Vliet, S. J., Paessens, L. C., Broks-van den Berg, V. C., Geijtenbeek, T. B. and van Kooyk, Y., The C-type lectin macrophage galactose-type lectin impedes migration of immature APCs. J. Immunol. 2008. 181: 3148-3155.
7. van Vliet, S. J., van Liempt, E., Saeland, E., Aarnoudse, C. A., Appelmelk, B., Irimura, T., Geijtenbeek, T. B. et al., 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. 2005. 17: 661-669.
8. Tsuiji, M., Fujimori, M., Ohashi, Y., Higashi, N., Onami, T. M., Hedrick, S. M. and Irimura, T., Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. J. Biol. Chem. 2002. 277: 28892-28901.
9. Kumamoto, Y., Denda-Nagai, K., Aida, S., Higashi, N. and Irimura, T., MGL2 Dermal dendritic cells are sufficient to initiate contact hypersensitivity in vivo. PLoS One 2009. 4: e5619.
10. Singh, S. K., Streng-Ouwehand, I., Litjens, M., Weelij, D. R., García-Vallejo, J. J., van Vliet, S. J., Saeland, E. et al., Characterization of murine MGL1 and MGL2 C-type lectins: distinct glycan specificities and tumor binding properties. Mol. Immunol. 2009. 46: 1240-1249.
11. van Vliet, S. J., Aarnoudse, C. A., Broks-van den Berg, V. C., Boks, M., Geijtenbeek, T. B. and van Kooyk, Y., MGL-mediated internalization and antigen presentation by dendritic cells: a role for tyrosine-5. Eur. J. Immunol. 2007. 37: 2075-2081.
12. Takada, A., Fujioka, K., Tsuiji, M., Morikawa, A., Higashi, N., Ebihara, H., Kobasa, D. et al., Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine promotes filovirus entry. J. Virol. 2004. 78: 2943-2947.
13. van Liempt, E., van Vliet, S. J., Engering, A., García Vallejo, J. J., Bank, C. M., Sanchez-Hernandez, M., van Kooyk, Y. 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. 2007. 44: 2605-2615.
14. van Sorge, N. M., Bleumink, N. M., van Vliet, S. J., Saeland, E., van der Pol, W. L., van Kooyk, Y. and van Putten, J. P., N-glycosylated proteins and distinct lipooligosaccharide glycoforms of Campylobacter jejuni target the human C-type lectin receptor MGL. Cell. Microbiol. 2009. 11: 1768-1781.
15. van Vliet, S. J., Steeghs, L., Bruijns, S. C., Vaezirad, M. M., Snijders Blok, C., Arenas Busto, J. A., Deken, M. et al., Variation of Neisseria gonorrhoeae lipooligosaccharide directs dendritic cell-induced T helper responses. PLoS Pathog. 2009. 5: e1000625.
16. van Vliet, S. J., Gringhuis, S. I., Geijtenbeek, T. B. and van Kooyk, Y., Regulation of effector T cells by antigen-presenting cells via interaction of the C-type lectin MGL with CD45. Nat. Immunol. 2006. 7: 1200-1208.
17. Saeland, E., van Vliet, S. J., Bäckström, M., van den Berg, V. C., Geijtenbeek, T. B., Meijer, G. A. and van Kooyk, Y., The C-type lectin MGL expressed by dendritic cells detects glycan changes on MUC1 in colon carcinoma. Cancer Immunol. Immunother. 2007. 56: 1225-1236.
18. Napoletano, C., Rughetti, A., Agervig Tarp, M. P., Coleman, J., Bennett, E. P., Picco, G., Sale, P. et al., Tumor-associated Tn-MUC1 glycoform is internalized through the macrophage galactose-type C-type lectin and delivered to the HLA class I and II compartments in dendritic cells. Cancer Res. 2007. 67: 8358-8367.
19. Gendler, S. J., Spicer, A. P., Lalani, E. N., Duhig, T., Peat, N., Burchell, J., Pemberton, L. et al., Structure and biology of a carcinoma-associated mucin, MUC1. Am. Rev. Respir. Dis. 1991. 144: S42-S47.
20. Burchell, J. M., Mungul, A. and Taylor-Papadimitriou, J., O-linked glycosylation in the mammary gland: changes that occur during malignancy. J. Mammary Gland Biol. Neoplasia 2001. 6: 355-364.
21. Kaisho, T. and Tanaka, T., Turning NF-kappaB and IRFs on and off in DC. Trends Immunol. 2008. 29: 329-336.
22. Nishikori, M., Classical and alternative NfkB activation pathways and their roles in lymphoid malignancies. J. Clin. Exp. Hematopathol. 2005. 45: 15-22.
23. Ouaaz, F., Arron, J., Zheng, Y., Choi, Y. and Beg, A. A., Dendritic cell development and survival require distinct NF-kappaB subunits. Immunity 2002. 16: 257-270.
24. Nakahara, T., Moroi, Y., Uchi, H. and Furue, M., Differential role of MAPK signaling in human dendritic cell maturation and Th1/Th2 engagement. J. Dermatol. Sci. 2006. 42: 1-11.
25. Sallusto, F., Cella, M., Danieli, C. and Lanzavecchia, A., Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 1995. 182: 389-400.
26. Scott, K., Manunta, M., Germain, C., Smith, P., Jones, M., Mitchell, P., Dessi, D. et al., Qualitatively distinct patterns of cytokines are released by human dendritic cells in response to different pathogens. Immunology 2005. 116: 245-254.
27. Simon, T., Fonteneau, J. F. and Grégoire, M., Dendritic cell preparation for immunotherapeutic interventions. Immunotherapy 2009. 1: 289-302.
28. Unger, W. W. and van Kooyk, Y., "Dressed for success" C-type lectin receptors for the delivery of glyco-vaccines to dendritic cells. Curr. Opin. Immunol. 2011. 23: 131-137.
29. Freire, T., Zhang, X., Dériaud, E., Ganneau, C., Vichier-Guerre, S., Azria, E., Launay, O. et al., Glycosidic Tn-based vaccines targeting dermal dendritic cells favor germinal center B-cell development and potent antibody response in the absence of adjuvant. Blood 2010. 116: 3526-3536.
30. Singh, S. K., Streng-Ouwehand, I., Litjens, M., Kalay, H., Saeland, E. and van Kooyk, Y., Tumour-associated glycan modifications of antigen enhance MGL2 dependent uptake and MHC class I restricted CD8 T cell responses. Int. J. Cancer 2011. 128: 1371-1383.
31. Denda-Nagai, K., Aida, S., Saba, K., Suzuki, K., Moriyama, S., Oo-Puthinan, S., Tsuiji, M. et al., Distribution and function of macrophage galactose-type C-type lectin 2 (MGL2/CD301b): efficient uptake and presentation of glycosylated antigens by dendritic cells. J. Biol. Chem. 2010. 285: 19193-19204.
32. Ni, L., Gayet, I., Zurawski, S., Duluc, D., Flamar, A. L., Li, X. H., O'Bar, A. et al., Concomitant activation and antigen uptake via human dectin-1 results in potent antigen-specific CD8+ T cell responses. J. Immunol. 2010. 185: 3504-3513.
33. Caparrós, E., Munoz, P., Sierra-Filardi, E., Serrano-Gómez, D., Puig-Kröger, A., Rodríguez-Fernández, J. L., Mellado, M. et al., DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 2006. 107: 3950-3958.
34. Singh, S. K., Streng-Ouwehand, I., Litjens, M., Kalay, H., Burgdorf, S., Saeland, E., Kurts, C. et al., Design of neo-glycoconjugates that target the mannose receptor and enhance TLR-independent cross-presentation and Th1 polarization. Eur. J. Immunol. 2011. 41: 916-925.
35. Sartorius, R., Bettua, C., D'Apice, L., Caivano, A., Trovato, M., Russo, D., Zanoni, I. et al., Vaccination with filamentous bacteriophages targeting DEC-205 induces DC maturation and potent anti-tumor T-cell responses in the absence of adjuvants. Eur. J. Immunol. 2011. 41: 2573-2584.
36. Idoyaga, J., Cheong, C., Suda, K., Suda, N., Kim, J. Y., Lee, H., Park, C. G. et al., Cutting edge: langerin/CD207 receptor on dendritic cells mediates efficient antigen presentation on MHC I and II products in vivo. J. Immunol. 2008. 180: 3647-3650.
37. Flacher, V., Tripp, C. H., Stoitzner, P., Haid, B., Ebner, S., Del Frari, B., Koch, F. et al., Epidermal Langerhans cells rapidly capture and present antigens from C-type lectin-targeting antibodies deposited in the dermis. J. Invest. Dermatol. 2010. 130: 755-762.
38. Caux, C., Vanbervliet, B., Massacrier, C., Azuma, M., Okumura, K., Lanier, L. L. and Banchereau, J., B70/B7-2 Is Identical to CD86 and Is the Major Functional Ligand for CD28 Expressed on Human Dendritic Cells. J. Exp. Med. 1996. 180: 1841-1847.
39. Puig-Kröger, A., Relloso, M., Fernández-Capetillo, O., Zubiaga, A., Silva, A., Bernabéu, C. and Corbi', A.L., Extracellular signal-regulated protein kinase signaling pathway negatively regulates the phenotypic and functional maturation of monocyte-derived human dendritic cells. Blood 2001. 98: 2175-2182.
40. Ardeshna, K. M., Pizzey, A. R., Devereux, S. and Khwaja, A., The PI3 kinase, p38 SAP kinase, and NF-kappaB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood 2000. 96: 1039-1046.
41. Palucka, K., Ueno, H. and Banchereau, J., Recent developments in cancer vaccines. J. Immunol. 2001. 186: 1325-1331.
42. Fontenot, J. D., Finn, O. J., Dales, N., Andrews, P. C. and Montelaro, R. C., Synthesis of large multideterminant peptide immunogens using a poly-proline beta-turn helix motif. Pept. Res. 1993. 6: 330-336.
43. Wandall, H. H., Hassan, H., Mirgorodskaya, E., Kristensen, A. K., Roepstorff, P., Bennett, E. P., Nielsen, P. A. et al., Substrate specificities of three members of the human UDP-N-acetyl-alpha-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase family, GalNAc-T1, -T2, and -T3. J. Biol. Chem. 1997. 272: 23503-23514.