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9 - Pathogen-recognition receptors as targets for pathogens to modulate immune function of antigen-presenting cells

from IV - Dendritic cells and immune evasion of bacteria in vivo

Published online by Cambridge University Press:  12 August 2009

By
Anneke Engering ,
Sandra J. van Vliet ,
Estella A. Koppel ,
Teunis B. H. Geijtenbeek  and
Yvette van Kooyk
Edited by
Maria Rescigno
Maria Rescigno
Affiliation:
European Institute of Oncology, Milan
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Summary

INTRODUCTION

Antigen-presenting cells (APC), such as dendritic cells (DCs) and macrophages, are located throughout the body to sense and capture invading pathogens and to trigger immune responses to fight such invaders. In addition, in the absence of danger signals, DCs have an active role in the induction of T cell tolerance and the maintenance of homeostasis. The recognition and internalization of pathogens is mediated by so-called pathogen-recognition receptors, germ-line encoded cell surface receptors that include toll-like receptors (TLR) and C-type lectins (CLR). It is becoming increasingly clear that during the long co-evolution with their hosts, pathogens have evolved mechanisms to misuse pathogen-recognition receptors to suppress or evade immune responses and thus to escape clearance. In this chapter, we will review recent examples of how pathogens evade immune activation by targeting recognition receptors on APC and subverting their function.

BACTERIAL RECEPTORS ON ANTIGEN-PRESENTING CELLS

APC interact with invading pathogens via pathogen-recognition receptors that bind conserved patterns of carbohydrates, lipids, proteins and nucleic acids in classes of microbes. This variety of receptors and conserved ligands recognized ensures that most, if not all, microbes can be detected by the immune system, either by a single or by combinations of receptors. Pathogen-recognition receptors include TLR and CLR (Figure 9.1). To date, 11 TLR have been identified (see Chapter 2) that each targets specific pathogenic structures, such as lipopolysaccharide (TLR4), viral dsRNA (TLR3) and bacterial peptidoglycans (TLR2/TLR6).

Type
Chapter
Information
Dendritic Cell Interactions with Bacteria , pp. 173 - 192
Publisher: Cambridge University Press
Print publication year: 2007

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References

Taylor, P. R., Martinez-Pomares, L, Stacey, M., Lin, H. H., Brown, G. D., and Gordon, S. (2005). Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23, 901–44CrossRefGoogle ScholarPubMed
Sousa, E. Reis (2004). Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 16, 21–5CrossRefGoogle Scholar
Akira, S., Takeda, K., and Kaisho, T. (2001). Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675–80CrossRefGoogle ScholarPubMed
Figdor, C. G., Kooyk, Y., and Adema, G. J. (2002). C-type lectin receptors on dendritic cells and Langerhans cells. Nature Rev. Immunol. 2, 77–84CrossRefGoogle ScholarPubMed
Underhill, D. M. and Ozinsky, A. (2002). Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14, 103–10CrossRefGoogle ScholarPubMed
McGettrick, A. F. and O'Neill, L. A. (2004). The expanding family of MyD88-like adaptors in Toll-like receptor signal transduction. Mol. Immunol. 41, 577–82CrossRefGoogle ScholarPubMed
Kooyk, Y., Engering, A., Lekkerkerker, A. N., Ludwig, I. S., and Geijtenbeek, T. B. (2004). Pathogens use carbohydrates to escape immunity induced by dendritic cells. Curr. Opin. Immunol. 16, 488–93CrossRefGoogle ScholarPubMed
Geijtenbeek, T. B., Vliet, S. J., Engering, A., Hart, B. A. 't, and Kooyk, Y. (2004). Self- and nonself-recognition by C-type lectins on dendritic cells. Annu. Rev. Immunol. 22, 33–54CrossRefGoogle ScholarPubMed
Drickamer, K. (1999). C-type lectin-like domains. Curr. Opin. Struct. Biol. 9, 585–90CrossRefGoogle ScholarPubMed
Engering, A., Geijtenbeek, T. B., Vliet, S. J., Wijers, M., Liempt, E., Demaurex, N., Lanzavecchia, A., Fransen, J., Figdor, C. G., Piguet, V., and Kooyk, Y. (2002). The dendritic cell-specific adhesion receptor dendritic cell-SIGN internalizes antigen for presentation to T cells. J. Immunol. 168, 2118–26CrossRefGoogle Scholar
Tan, M. C., Mommaas, A. M., Drijfhout, J. W., Jordens, R., Onderwater, J. J., Verwoerd, D., Mulder, A. A., Heiden, A. N., Scheidegger, D., Oomen, L. C., Ottenhoff, T. H., Tulp, A., Neefjes, J. J., and Koning, F. (1997). Mannose receptor-mediated uptake of antigens strongly enhances human leukocyte antigen class II-restricted antigen presentation by cultured dendritic cells. Eur. J. Immunol. 27, 2426–35CrossRefGoogle ScholarPubMed
Engering, A. J., Cella, M., Fluitsma, D., Brockhaus, M., Hoefsmit, E. C., Lanzavecchia, A., and Pieters, J. (1997). The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol. 27, 2417–25CrossRefGoogle ScholarPubMed
Inohara, N., Chamaillard, M., McDonald, C., and Nunez, G. (2005). nucleotide-binding oligomerization domain-leucine-rich repeat proteins: role in host–microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74, 355–83CrossRefGoogle Scholar
Wagner, H. (2004). The immunobiology of the Toll-like receptor9 subfamily. Trends Immunol. 25, 381–6CrossRefGoogle Scholar
McGreal, E. P., Miller, J. L., and Gordon, S. (2005). Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr. Opin. Immunol. 17, 18–24CrossRefGoogle ScholarPubMed
Kokkinopoulos, I., Jordan, W. J., and Ritter, M. A. (2005). Toll-like receptor mRNA expression patterns in human dendritic cells and monocytes. Mol. Immunol. 42, 957–68CrossRefGoogle ScholarPubMed
Portnoy, D. A. (2005). Manipulation of innate immunity by bacterial pathogens. Curr. Opin. Immunol. 17, 25–8CrossRefGoogle ScholarPubMed
Kawasaki, K., Ernst, R. K., and Miller, S. I. (2004). 3-O-deacylation of lipid A by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J. Biol. Chem. 279, 20044–8CrossRefGoogle ScholarPubMed
Darveau, R. P., Pham, T. T., Lemley, K., Reife, R. A., Bainbridge, B. W., Coats, S. R., Howald, W. N., Way, S. S., and Hajjar, A. M. (2004). Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both Toll-like receptors 2 and 4. Infect. Immun. 72, 5041–51CrossRefGoogle ScholarPubMed
Netea, M. G., Meer, J. W., and Kullberg, B. J. (2004). Toll-like receptors as an escape mechanism from the host defense. Trends Microbiol. 12, 484–8CrossRefGoogle ScholarPubMed
Kleij, D., Latz, E., Brouwers, J. F., Kruize, Y. C., Schmitz, M., Kurt-Jones, E. A., Espevik, T., Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., Tielens, A. G., and Yazdanbakhsh, M. (2002). A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277, 48122–9CrossRefGoogle ScholarPubMed
Sing, A., Rost, D., Tvardovskaia, N., Roggenkamp, A., Wiedemann, A., Kirschning, C. J., Aepfelbacher, M., and Heesemann, J. (2002). Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196, 1017–24CrossRefGoogle ScholarPubMed
Geijtenbeek, T. B. H., Torensma, R., Vliet, S. J., Duijnhoven, G. C. F., Adema, G. J., Kooyk, Y., and Figdor, C. G. (2000). Identification of dendritic cell-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100, 575–85CrossRefGoogle Scholar
Geijtenbeek, T. B., Krooshoop, D. J., Bleijs, D. A., Vliet, S. J., Duijnhoven, G. C., Grabovsky, V., Alon, R., Figdor, C. G., and Kooyk, Y. (2000). dendritic cell-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat. Immunol. 1, 353–7CrossRefGoogle ScholarPubMed
Ariizumi, K., Shen, G. L., Shikano, S., Xu, S., Ritter, R., Kumamoto, T., Edelbaum, D., Morita, A., Bergstresser, P. R., and Takashima, A. (2000). Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J. Biol. Chem. 275, 20157–67CrossRefGoogle ScholarPubMed
Irjala, H., Johansson, E. L., Grenman, R., Alanen, K., Salmi, M., and Jalkanen, S. (2001). Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium. J. Exp. Med. 194, 1033–42CrossRefGoogle ScholarPubMed
Stahl, P. D. (1992). The mannose receptor and other macrophage lectins. Curr. Opin. Immunol. 4, 49–52CrossRefGoogle ScholarPubMed
Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V., Steinman, R. M., and Nussenzweig, M. C. (2001). Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194, 769–79CrossRefGoogle ScholarPubMed
Chieppa, M., Bianchi, G., Doni, A., Prete, A. Del, Sironi, M., Laskarin, G., Monti, P., Piemonti, L., Biondi, A., Mantovani, A., Introna, M., and Allavena, P. (2003). Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J. Immunol. 171, 4552–60CrossRefGoogle ScholarPubMed
Kwon, D. S., Gregorio, G., Bitton, N., Hendrickson, W. A., and Littman, D. R. (2002). dendritic cell-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16, 135–44CrossRefGoogle ScholarPubMed
Ludwig, I. S., Lekkerkerker, A. N., Depla, E., Bosman, F., Musters, R. J., Depraetere, S., Kooyk, Y., and Geijtenbeek, T. B. (2004). Hepatitis C virus targets dendritic cell-SIGN and L-SIGN to escape lysosomal degradation. J. Virol. 78, 8322–32CrossRefGoogle Scholar
Geijtenbeek, T. B. H., Kwon, D. S., Torensma, R., Vliet, S. J., Duijnhoven, G. C. F., Middel, J., Cornelissen, I. L., Nottet, H. S., KewalRamani, V. N., Littman, D. R., Figdor, C. G., and Kooyk, Y. (2000). dendritic cell-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587–97CrossRefGoogle Scholar
Lozach, P. Y., Amara, A., Bartosch, B., Virelizier, J. L., Arenzana-Seisdedos, F., Cosset, F. L., and Altmeyer, R. (2004). C-type lectins L-SIGN and dendritic cell-SIGN capture and transmit infectious hepatitis C virus pseudotype particles. J. Biol. Chem. 279, 32035–45CrossRefGoogle Scholar
Alvarez, C. P., Lasala, F., Carrillo, J., Muniz, O., Corbi, A. L., and Delgado, R. (2002). C-type lectins dendritic cell-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J. Virol. 76, 6841–4CrossRefGoogle Scholar
Halary, F., Amara, A., Lortat-Jacob, H., Messerle, M., Delaunay, T., Houles, C., Fieschi, F., Arenzana-Seisdedos, F., Moreau, J. F., and Dechanet-Merville, J. (2002). Human cytomegalovirus binding to dendritic cell-SIGN is required for dendritic cell infection and target cell trans-infection. Immunity 17, 653–64CrossRefGoogle Scholar
Tassaneetrithep, B., Burgess, T. H., Granelli-Piperno, A., Trumpfheller, C., Finke, J., Sun, W., Eller, M. A., Pattanapanyasat, K., Sarasombath, S., Birx, D. L., Steinman, R. M., Schlesinger, S., and Marovich, M. A. (2003). dendritic cell-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197, 823–9CrossRefGoogle Scholar
Appelmelk, B. J., van Die, I., Vliet, S. J., Vandenbroucke-Grauls, C. M., Geijtenbeek, T. B., and Kooyk, Y. (2003). Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells. J. Immunol. 170, 1635–9CrossRefGoogle ScholarPubMed
Die, I., Vliet, S. J., Kwame Nyame, A., Cummings, R. D., Bank, C. M., Appelmelk, B., Geijtenbeek, T. B., and Kooyk, Y. (2003). The dendritic cell specific C-type lectin dendritic cell-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis-x. Glycobiology 13, 471–8Google Scholar
Cambi, A., Gijzen, K., Vries, J. M., Torensma, R., Joosten, B., Adema, G. J., Netea, M. G., Kullberg, B. J., Romani, L., and Figdor, C. G. (2003). The C-type lectin dendritic cell-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33, 532–8CrossRefGoogle Scholar
Geijtenbeek, T. B., Vliet, S. J., Koppel, E. A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C. M., Appelmelk, B., and Kooyk, Y. (2003). Mycobacteria target dendritic cell-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7–17CrossRefGoogle Scholar
Tailleux, L., Schwartz, O., Herrmann, J. L., Pivert, E., Jackson, M., Amara, A., Legres, L., Dreher, D., Nicod, L. P., Gluckman, J. C., Lagrange, P. H., Gicquel, B., and Neyrolles, O. (2003). dendritic cell-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197, 121–7CrossRefGoogle Scholar
Baldari, C. T., Lanzavecchia, A., and Telford, J. L. (2005). Immune subversion by Helicobacter pylori. Trends Immunol. 26, 199–207CrossRefGoogle ScholarPubMed
Bergman, M. P., Engering, A., Smits, H. H., Vliet, S. J., Bodegraven, A. A., Wirth, H. P., Kapsenberg, M. L., Vandenbroucke-Grauls, C. M., Kooyk, Y., and Appelmelk, B. J. (2004). Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and dendritic cell-SIGN. J. Exp. Med. 200, 979–90CrossRefGoogle Scholar
Appelmelk, B. J., Monteiro, M. A., Martin, S. L., Moran, A. P., and Vandenbroucke-Grauls, C. M. (2000). Why Helicobacter pylori has Lewis antigens. Trends Microbiol. 8, 565–70CrossRefGoogle ScholarPubMed
Smits, H. H., Engering, A., Kleij, D., Jong, E. C., Schipper, K., Capel, T., Zaat, B., Yazdanbakhsh, M., Wierenga, E. A., Kooyk, Y., and Kapsenberg, M. L. (2005). Selective probiotic bacteria induce regulatory T cells by modulating dendritic cell function via dendritic cell-SIGN in vitro. J. Allergy and Clin. Immunol. 115, 1260–7CrossRefGoogle Scholar
Geijtenbeek, T. B., Groot, P. C., Nolte, M. A., Vliet, S. J., Gangaram-Panday, S. T., Duijnhoven, G. C., Kraal, G., Oosterhout, A. J., and Kooyk, Y. (2002). Marginal zone macrophages express a murine homologue of dendritic cell-SIGN that captures blood-borne antigens in vivo. Blood 100, 2908–16CrossRefGoogle Scholar
Baribaud, F., Pohlmann, S., and Doms, R. W. (2001). The role of dendritic cell-SIGN and dendritic cell-SIGNR in HIV and SIV attachment, infection, and transmission. Virology 286, 1–6CrossRefGoogle Scholar
Taylor, P. R., Brown, G. D., Herre, J., Williams, D. L., Willment, J. A., and Gordon, S. (2004). The role of SIGNR1 and the beta-glucan receptor (dectin-1) in the nonopsonic recognition of yeast by specific macrophages. J. Immunol. 172, 1157–62CrossRefGoogle ScholarPubMed
Kang, Y. S., Kim, J. Y., Bruening, S. A., Pack, M., Charalambous, A., Pritsker, A., Moran, T. M., Loeffler, J. M., Steinman, R. M., and Park, C. G. (2004). The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen. Proc. Natl Acad. Sci. USA 101, 215–20CrossRefGoogle ScholarPubMed
Takahara, K., Yashima, Y., Omatsu, Y., Yoshida, H., Kimura, Y., Kang, Y. S., Steinman, R. M., Park, C. G., and Inaba, K. (2004). Functional comparison of the mouse dendritic cell-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins. Int. Immunol. 16, 819–29CrossRefGoogle Scholar
Lanoue, A., Clatworthy, M. R., Smith, P., Green, S., Townsend, M. J., Jolin, H. E., Smith, K. G., Fallon, P. G., and McKenzie, A. N. (2004). SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J. Exp. Med. 200, 1383–93CrossRefGoogle ScholarPubMed
Nagaoka, K., Takahara, K., Tanaka, K., Yoshida, H., Steinman, R. M., Saitoh, S. I., Akashi-Takamura, S., Miyake, K., Kang, Y. S., Park, C. G., and Inaba, K. (2005). Association of SIGNR1 with Toll-like receptor4-MD-2 enhances signal transduction by recognition of lipopolysaccharide in Gram-negative bacteria. Int. Immunol. 17, 827–36CrossRefGoogle ScholarPubMed
Brown, G. D. and Gordon, S. (2001). Immune recognition. A new receptor for beta-glucans. Nature 413, 36–7CrossRefGoogle ScholarPubMed
Underhill, D. M., Ozinsky, A., Hajjar, A. M., Stevens, A., Wilson, C. B., Bassetti, M., and Aderem, A. (1999). The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401, 811–15Google ScholarPubMed
Brown, G. D., Herre, J., Williams, D. L., Willment, J. A., Marshall, A. S., and Gordon, S. (2003). Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 197, 1119–24CrossRefGoogle ScholarPubMed
Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S., and Underhill, D. M. (2003). Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197, 1107–17CrossRefGoogle ScholarPubMed
Herre, J., Marshall, A. S., Caron, E., Edwards, A. D., Williams, D. L., Schweighoffer, E., Tybulewicz, V., Sousa, Reis E, Gordon, S., and Brown, G. D. (2004). Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104, 4038–45CrossRefGoogle ScholarPubMed
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., and Sousa, Reis E (2005). Syk-dependent cytokine induction by dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22, 507–17CrossRefGoogle ScholarPubMed
Gantner, B. N., Simmons, R. M., and Underhill, D. M. (2005). Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24, 1277–86CrossRefGoogle Scholar
d'Ostiani, C. F., Del Sero, G., Bacci, A., Montagnoli, C., Spreca, A., Mencacci, A., Ricciardi-Castagnoli, P., and Romani, L. (2000). Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191, 1661–74CrossRefGoogle ScholarPubMed
Romani, L., Montagnoli, C., Bozza, S., Perruccio, K., Spreca, A., Allavena, P., Verbeek, S., Calderone, R. A., Bistoni, F., and Puccetti, P. (2004). The exploitation of distinct recognition receptors in dendritic cells determines the full range of host immune relationships with Candida albicans. Int. Immunol. 16, 149–61CrossRefGoogle ScholarPubMed
Huang, Q., Liu, D., Majewski, P., Schulte, L. C., Korn, J. M., Young, R. A., Lander, E. S., and Hacohen, N. (2001). The plasticity of dendritic cell responses to pathogens and their components. Science 294, 870–5CrossRefGoogle ScholarPubMed
Jeannin, P., Bottazzi, B., Sironi, M., Doni, A., Rusnati, M., Presta, M., Maina, V., Magistrelli, G., Haeuw, J. F., Hoeffel, G., Thieblemont, N., Corvaia, N., Garlanda, C., Delneste, Y., and Mantovani, A. (2005). Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 22, 551–60CrossRefGoogle ScholarPubMed
Pinhal-Enfield, G., Ramanathan, M., Hasko, G., Vogel, S. N., Salzman, A. L., Boons, G. J., and Leibovich, S. J. (2003). An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A(2A) receptors. Am. J. Pathol. 163, 711–21CrossRefGoogle ScholarPubMed
Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. (2002). Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549–55CrossRefGoogle ScholarPubMed
Mosser, D. M. (2003). The many faces of macrophage activation. J. Leukoc. Biol. 73, 209–12CrossRefGoogle ScholarPubMed
Raes, G., Brys, L., Dahal, B. K., Brandt, J., Grooten, J., Brombacher, F., Vanham, G., Noel, W., Bogaert, P., Boonefaes, T., Kindt, A., , B. R., Leenen, P. J., Baetselier, P., and 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, 321–7CrossRefGoogle ScholarPubMed
Higashi, N., Fujioka, K., Denda-Nagai, K., Hashimoto, S., Nagai, S., Sato, T., Fujita, Y., Morikawa, A., Tsuiji, M., Miyata-Takeuchi, M., Sano, Y., Suzuki, N., Yamamoto, K., Matsushima, K., and Irimura, T. (2002). The macrophage C-type lectin specific for galactose/N-acetylgalactosamine is an endocytic receptor expressed on monocyte-derived immature dendritic cells. J. Biol. Chem. 277, 20686–93CrossRefGoogle ScholarPubMed
Vliet, S. J., Liempt, E., Saeland, E., Aarnoudse, C. A., Appelmelk, B., Irimura, T., Geijtenbeek, T. B., Blixt, O., Alvarez, R., Die, I., and 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, 661–9CrossRefGoogle ScholarPubMed

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