Abstract
Fungi characteristically display mannose groups on the surface of their cell wall. These mannose residues are crucial for cell wall integrity and fungal viability. They constitute Pathogen-Associated-Molecular-Patterns (PAMPs) that can be detected by specific recognition receptors expressed by mammalian antigen-presenting cells. Fungal mannosylation, the mammalian membrane receptors that have evolved to detect fungal mannose groups and the immune responses resulting from fungal recognition by these receptors are the topics of this chapter. It consists of four parts. First, we give an introduction into fungal mannosylation to lay the ground for understanding mannose-based fungal recognition receptors. In the second part of the chapter we describe common features of mannose receptors. We then focus on two membranous mannose-receptors for which fungal binding has been demonstrated, the dendritic cell specific ICAM-3 grabbing non-integrin receptor (DC-SIGN) and the classic Mannose Receptor (MR). Finally, we give an outlook into potential therapeutic applications by targeting DC-SIGN and MR to prevent and treat fungal infections
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Cambi, A. and Figdor, C.G. (2003) Dual function of, C-type lectin-like receptors in the immune system. Curr. Opin. Cell. Biol. 15(5), 539–46.
Cambi, A. and Figdor, C.G. (2005) Levels of complexity in pathogen recognition by C-type lectins. Curr. Opin. Immunol. 17(4), 345–51.
Cambi, A., Gijzen, K., de 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 DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33, 532–38.
Cambi, A., de Lange, F., van Maarseveen, N.M., Nijhuis, M., Joosten, B., van Dijk, E.M., de Bakker, B.I., Fransen, J.A., Bovee-Geurts, P.H., van Leeuwen, F.N., Van Hulst, N.F. and Figdor, C.G. (2004) Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells. J. Cell. Biol. 164(1), 145–55.
Cambi, A., Koopman, M. and Figdor, C.G. (2005) How C-type lectins detect pathogens. Cell. Microbiol. 7(4), 481–88.
Chieppa, M., Bianchi, G., Doni, A., Del Prete, A., 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 monocytes-derived dendritic cells activates and anti-inflammatory immunosuppressive program. J. Immunol. 171, 4552–60.
DeFife, K.M., Jenney, C.R., McNally, A.K., Colton, E. and Anderson, J.M. (1997) Interleukin-13 induces human monocytes/macrophage fusion and macrophage mannose receptor expression. J. Immunol. 158, 3385–90.
Doyle, A.G., Herbein, G., Montaner, L.J., Minty, A.J., Caput, D., Ferara, P. and Gordon, S. (1994) Interleukin-13 alters the activation state of murine macrophages in vitro: comparison with interleukin-4 and interferon-gamma. Eur. J. Immunol. 24, 1441–45.
East, L. and Isacke, C.M. (2002) The mannose receptor family. Biochim. Biophys. Acta. 1572(2–3), 364–86.
Engering, A., Geijtenbeek, T.B., van Vliet, S.J., Wijers, M., van Liempt, E., Demaurex, N., Lanzavecchia, A., Fransen, J., Figdor, C.G., Piguet, V. and van Kooyk, Y. (2002) The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J. Immunol. 168(5), 2118–26.
Ernst, J.F. and Prill, SK. (2001) O-glycosylation. Med. Mycol. 39(suppl 1): 67–74.
Ezekowitz, R.A., Williams, D.J, Koziel, H., Armstrong, M.Y., Warner, A., Richards, F.F. and Rose, R.M. (1991) Uptake of Pneumocystis carinii mediated by the macrophage mannose receptor. Nature 351(6322), 155–58.
Feinberg, H., Mitchell, D.A., Drickamer, K., Weis, W.I (2001) Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294, 2163–66.
Feizi, T. and Chai, W. (2004) Oligosaccharide microarrays to decipher the glyco code. Nat. Rev. Mol. Cell. Biol. 5(7), 582–8.
Fiete, D.J., Beranek, M.C., Baenziger, J.U (1998) A cysteine-rich domain of the “mannose” receptor mediates GalNAc-4-SO4 binding. Proc. Natl. Acad. Sci. USA 95(5), 2089–93.
Figdor, C.G., van Kooyk, Y., Adema, G.J (2002) C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2(2), 77–84.
Fraser, I.P., Takahashi, K., Koziel, H., Fardin, B., Harmsen, A. and Ezekowitz, R.A. (2000) Pneumocystis carinii enhances soluble mannose receptor production by macrophages. Microbes. Infect. 2(11), 1305–10.
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(6), 1277–86.
Garner, R.E., Rubanowice, K., Sawyer, R.T. and Hudson, J.A. (1994) Secretion of TNF-alpha by alveolar macrophages in response to Candida albicans mannan. J. Leukoc. Biol. 55(2), 161–8.
Geijtenbeek, T.B., Torensma, R., van Vliet, S.J., van Duijnhoven, G.C., Adema, G.J., van Kooyk, Y. and Figdor, C.G. (2000a) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100, 575–85.
Geijtenbeek, T.B., Krooshoop, D.J., Bleijs, D.A., van Vliet, S.J., van Duijnhoven, G.C., Grabovsky, V., Alon, R., Figdor, C.G. and van Kooyk, Y. (2000b) DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat. Immunol. 1(4), 353–57.
Geijtenbeek, T.B., Van Vliet, S.J., Koppel, E.A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C.M., Appelmelk, B. and Van Kooyk, Y. (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197(1), 7–17.
Granelli-Piperno, A., Pritsker, A., Pack, M., Shimeliovich, I., Arrighi, J.F., Park, C.G., Trumpfheller, C., Piguet, V., Moran, T.M. and Steinman, R.M. (2005) Dendritic Cell-Specific Intercellular Adhesion Molecule 3-Grabbing Nonintegrin/CD209 Is Abundant on Macrophages in the Normal Human Lymph Node and Is Not Required for Dendritic Cell Stimulation of the Mixed Leukocyte Reaction. J. Immunol. 175(7), 4265–73.
Guo, Y., Feinberg, H., Conroy, E., Mitchell, D.A., Alvarez, R., Blixt, O., Taylor, M.E., Weis, W.I. and Drickamer, K. (2004) Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat. Struct. Mol. Biol. 11(7), 591–98.
Herscovics, A. and Orlean, P. (1993) Glycoprotein biosynthesis in yeast. FASEB. J. 7, 540–50.
Jordens, R., Thompson, A., Amons, R. and Koning, F. (1999) Human dendritic cells shed a functional, soluble form of the mannose receptor. Int. Immunol. 11(11), 1775–80.
Karbassi, A., Becker, J.M., Foster, J.S. and Moore, R.N. (1987) Enhanced killing of Candida albicans by murine macrophages treated with macrophage colony-stimulating factor: evidence for augmented expression of mannose receptors. J. Immunol. 139(2), 417–21.
Larsen, F., Madsen, H.O., Sim, R.B., Koch, C. and Garred, P. (2004) Disease-associated mutations in human mannose-binding lectin compromise oligomerization and activity of the final protein. J. Biol. Chem. 279(20), 21302–11.
Le Cabec, V., Emorine, L.J., Toesca, I., Cougoule, C. and Maridonneau-Parini, I. (2005) The human macrophage mannose receptor is not a professional phagocytic receptor. J. Leukoc. Biol. 77(6), 934–43.
Lee, R.T., Ichikawa, Y., Fay, M., Drickamer, K., Shao, M.C. and Lee, Y.C. (1991) Ligand-binding characteristics of rat serum-type mannose-binding protein (MBP-A). Homology of binding site architecture with mammalian and chicken hepatic lectins. J. Biol. Chem. 266, 4810–15.
Lee, S.J., Evers, S., Roeder, D., Parlow, A.F., Risteli, J., Risteli, L., Lee, Y.C., Feizi, T., Langen, H. and Nussenzweig, M.C. (2002) Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science 295(5561), 1898–901.
Lee, S.J., Zheng, N.Y., Clavijo, M. and Nussenzweig, M.C. (2003) Normal host defense during systemic candidiasis in mannose receptor-deficient mice. Infect. Immun. 71(1), 437–45.
Limper, A.H., Hoyte, J.S. and Standing, J.E. (1997) The role of alveolar macrophages in Pneumocystis carinii degradation and clearance from the lung. J. Clin. Invest. 99(9), 2110–17.
Mansour, M.K., Schlesinger, L.S. and Levitz, S.M. (2002) Optimal T cell responses to Cryptococcus neoformans mannoprotein are dependent on recognition of conjugated carbohydrates by mannose receptors. J. Immunol. 168(6), 2872–79.
Marodi, L., Korchak, H.M. and Johnston, R.B Jr. (1991) Mechanisms of host defense against Candida species. I. Phagocytosis by monocytes and monocyte-derived macrophages. J. Immunol. 146(8), 2783–9.
Martinez-Pomares, L., Mahoney, J.A., Kaposzta, R., Linehan, S.A., Stahl, P.D. and Gordon, S. (1998) A functional soluble form of the murine mannose receptor is produced by macrophages in vitro and is present in mouse serum. J. Biol. Chem. 273(36), 23376–80.
Martinez-Pomares, L., Reid, D.M., Brown, G.D., Taylor, P.R., Stillion, R.J., Linehan, S.A., Zamze, S., Gordon, S. and Wong, S.Y. (2003) Analysis of mannose receptor regulation by IL-4, IL-10, and proteolytic processing using novel monoclonal antibodies. J. Leukoc. Biol. 73, 604–13.
Masuoka, J. (2004) Surface glycans of Candida albicans and other pathogenic fungi: physiological roles, clinical uses, and experimental challenges. Clin. Microbiol. Rev. 17(2), 281–310.
McGinnis, M.R. and Tyring, S.K. (1996) Introduction to Mycology. In: Baron, S. (ed) Medical Microbiology, 4th edn, online, The University of Texas Medical Branch at Galveston.
Medzhitov, R. and Janeway, C. Jr. (2000) Innate immune recognition: mechanisms and pathways. Immunol. Rev. 173, 89–97.
Mi, Y., Shapiro, S.D. and Baenziger, J.U. (2002) Regulation of lutropin circulatory half-life by the mannose/N-acetylgalactosamine-4-SO4 receptor is critical for implantation in vivo. J. Clin. Invest. 109(2), 269–76.
Mitchell, T.G. and Perfect, J.R. (1995) Cryptococcosis in the era of AIDS–100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev. 8(4), 515–48.
Mitchell, D.A., Fadden, A.J. and Drickamer, K. (2001) A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. J. Biol. Chem. 276, 28939–45.
Mullin, N.P., Hitchen, P.G. and Taylor, M.E. (1997) Mechanism of Ca2+ and monosaccharide binding to a C-type carbohydrate-recognition domain of the macrophage mannose receptor. J. Biol. Chem. 272(9), 5668–81.
Nagaoka, K., Takahara, K., Tanaka, K., Yoshida, H., Steinman, R.M., Saitoh, S., Akashi-Takamura, S., Miyake, K., Kang, Y.S., Park, C.G. and Inaba, K. (2005) Association of SIGNR1 with TLR4-MD-2 enhances signal transduction by recognition of LPS in gram-negative bacteria. Int. Immunol. 17(7), 827–36.
Netea, M.G., Gijzen, K., Coolen, N., Verschueren, I., Figdor, C., Van der Meer, J.W., Torensma, R. and Kullberg, B.J. (2004) Human dendritic cells are less potent at killing Candida albicans than both monocytes and macrophages. Microbes. Infect. 6(11), 985–89.
Newman, S.L. and Holly, A. (2001) Candida albicans is phagocytosed, killed, and processed for antigen presentation by human dendritic cells. Infect. Immun. 69(11), 6813–22.
O’Riordan, D.M., Standing, J.E. and Limper, A.H. (1995) Pneumocystis carinii glycoprotein A binds macrophage mannose receptors. Infect. Immun. 63(3), 779–84.
Pietrella, D., Corbucci, C., Perito, S., Bistoni, G. and Vecchiarelli, A. (2005) Mannoproteins from Cryptococcus neoformans promote dendritic cell maturation and activation. Infect. Immun. 73(2), 820–27.
Romani, L., Bistoni, F. and Puccetti, P. (2002) Fungi, dendritic cells and receptors: a host perspective of fungal virulence. Trends Microbiol. 11, 508–14.
Saville, S.P., Lazzell, A.L., Monteagudo, C., Lopez-Ribot, J.L. (2003) Engineered control of cell morphology in vivo reveals distinctroles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2, 1053–60.
Savolainen, J., Rantala, A., Nermes, M., Lehtonen, L. and Viander, M. (1996) Enhanced IgE response to Candida albicans in postoperative invasive candidiasis. Clin. Exp. Allergy 26(4), 452–60.
Serrano-Gomez, D., Dominguez-Soto, A., Ancochea, J., Jimenez-Heffernan, J.A., Leal, J.A. and Corbi, A.L. (2004) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J. Immunol. 173(9), 5635–43.
Shepherd, V.L., Konish, M.G. and Stahl, P. (1985) Dexamethasone increases expression of mannose receptors and decreases extracellular lysosomal enzyme accumulation in macrophages. J. Biol. Chem. 260, 160–64.
Sheriff, S., Chang, C.Y. and Ezekowitz, R.A. (1994) Human mannose-binding protein carbohydrate recognition domain trimerizes through a triple alpha-helical coiled-coil. Nat. Struct. Biol. 1(11), 789–94.
Soilleux, E.J., Morris, L.S., Leslie, G., Chehimi, J., Luo, Q., Levroney, E., Trowsdale, J., Montaner, L.J., Doms, R.W., Weissman, D., Coleman, N. and Lee, B. (2002) Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J. Leukoc. Biol. 71(3), 445–57.
Spiro, R.G. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12(4), 43R–56R.
Stahl, P.D., Rodman, J.S., Miller, M.J. and Schlesinger, P.H (1978) Evidence for receptor-mediated binding of glycoproteins, glycoconjugates, and lysosomal glycosidases by alveolar macrophages. Proc. Natl. Acad. Sci. U.S.A. 75, 1399–1403.
Stahl, P., Schlesinger, P.H., Sigardson, E., Rodman, J.S. and Lee, Y.C. (1980) Receptor-mediated pinocytosis of mannose glycoconjugates by macrophages: characterization and evidence for receptor recycling. Cell 19(1), 207–15.
Sternberg, S. (1994) The emerging fungal threat. Science 266(5191), 1632–34.
Strahl-Bolsinger, S., Gentsch, M. and Tanner, W. (1999) Protein O-mannosylation. Biochim. Biophys. Acta. 1426, 297–307.
Su, Y., Bakker, T., Harris, J., Tsang, C., Brown, G.D., Wormald, M.R., Gordon, S., Dwek, R.A., Rudd, P.M. and Martinez-Pomares, L. (2005) Glycosylation influences the lectin activities of the macrophage mannose receptor. J. Biol. Chem. 280(38), 32811–20.
Swain, S.D., Lee, S.J., Nussenzweig, M.C. and Harmsen, A.G. (2003) Absence of the macrophage mannose receptor in mice does not increase susceptibility to Pneumocystis carinii infection in vivo. Infect. Immun. 71(11), 6213–21.
Syme, R.M., Spurrell, J.C., Amankwah, E.K., Green, F.H. and Mody, C.H. (2002) Primary dendritic cells phagocytose Cryptococcus neoformans via mannose receptors and Fcgamma receptor II for presentation to T lymphocytes. Infect. Immun. 70(11), 5972–81.
Tacken, P.J., de Vries, I.J., Gijzen, K., Joosten, B., Wu, D., Rother, R.P., Faas, S.J., Punt, C.J., Torensma, R., Adema, G.J. and Figdor, C.G (2005) Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 106(4), 1278–85.
Takeda, K., Kaisho, T. and Akira, S. (2003) Toll-like receptors. Annu. Rev. Immunol. 21, 335–76.
Taylor, M.E., Bezouska, K. and Drickamer, K. (1992) Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. J. Biol. Chem. 267(3), 1719–26.
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(2), 1157–62.
Taylor, P.R., Gordon, S. and Martinez-Pomares, L. (2005) The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol. 26(2), 104–10.
Thomas, C.F., Jr. and Limper, A.H. (2004) Pneumocystis pneumonia. N. Engl. J. Med. 350(24), 2487–98.
van Gisbergen, K.P., Sanchez-Hernandez, M., Geijtenbeek, T.B. and van Kooyk, Y. (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 201(8), 1281–92.
Wallis, R. and Drickamer, K. (1999) Molecular determinants of oligomer formation and complement fixation in mannose-binding proteins. J. Biol. Chem. 274(6), 3580–9.
Wileman, T., Boshans, R.L., Schlesinger, P. and Stahl, P. (1984) Monensin inhibits recycling of macrophage mannose-glycoprotein receptors and ligand delivery to lysosomes. Biochem. J. 220(3), 665–75.
Zhang, L., Ikegami, M., Crouch, E.C., Korfhagen, T.R. and Whitsett, J.A. (2001) Activity of pulmonary surfactant protein-D (SP-D) in vivo is dependent on oligomeric structure. J. Biol. Chem. 276(22), 19214–19.
Zhang, J., Tachado, S.D., Patel, N., Zhu, J., Imrich, A., Manfruelli, P., Cushion, M., Kinane, T.B. and Koziel, H. (2005) Negative regulatory role of mannose receptors on human alveolar maceophage proinflammatory cytokine release in vitro. J. Leukoc. Biol. 78(3), 665–674.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2007 Springer
About this chapter
Cite this chapter
Meyer-Wentrup, F., Cambi, A., Figdor, C., Adema, G. (2007). Detection of Fungi by Mannose-based Recognition Receptors. In: Brown, G.D., Netea, M.G. (eds) Immunology of Fungal Infections. Springer, Dordrecht. https://doi.org/10.1007/1-4020-5492-0_13
Download citation
DOI: https://doi.org/10.1007/1-4020-5492-0_13
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-5491-4
Online ISBN: 978-1-4020-5492-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)