The cysteine-rich domain of the macrophage mannose receptor is a multispecific lectin that recognizes chondroitin sulfates A and B and sulfated oligosaccharides of blood group Lewisa and Lewis(x) types in addition to the sulfated N-glycans of lutropin

Journal of Experimental Medicine

Volumn 191, Issue 7, 2000, Pages 1117-1126

  Leteux, Christine ^a   Chai, Wengang ^a   Loveless, R Wendy ^a   Yuen, Chun Ting ^b   Uhlin Hansen, Lars ^c   Combarnous, Yves ^d   Jankovic, Mila ^e   Maric, Svetlana C ^e   Misulovin, Ziva ^e   Nussenzweig, Michel C ^e   Feizi, Ten ^a  

^a NORTHWICK PARK HOSPITAL   (United Kingdom)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^c UNIVERSITY OF TROMSØ   (Norway)

^d CEMAGREF   (France)

^e ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Chondroitin sulfate; Cysteine rich domain; Lutropin (luteinizing hormone); Macrophage receptor; Sulfo Lewis(a x)

Indexed keywords

CHONDROITIN 4 SULFATE; DERMATAN SULFATE; LUTEINIZING HORMONE; MANNOSE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; BLOOD GROUP LEWIS SYSTEM; CONTROLLED STUDY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REACTION ANALYSIS; RECEPTOR AFFINITY; RECEPTOR BINDING; SPLEEN CELL;

ACETYLGALACTOSAMINE; ANIMALS; BINDING SITES; CARBOHYDRATE SEQUENCE; CHONDROITIN SULFATES; CYSTEINE; DERMATAN SULFATE; HUMANS; LECTINS; LECTINS, C-TYPE; LEWIS BLOOD-GROUP SYSTEM; LUTEINIZING HORMONE; MACROPHAGES; MANNOSE-BINDING LECTINS; MICE; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEOGLYCANS; RECEPTORS, CELL SURFACE; SPLEEN; STAINING AND LABELING;

EID: 0034599815     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.7.1117     Document Type: Article

References (48)

1. Taylor, M.E., J.T. Conary, M.R. Lennartz, P.D. Stahl, and K. Drickamer. 1990. Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains. J. Biol. Chem. 265:12156-12162.
2. Ezekowitz, R.A., K. Sastry, P. Bailly, and A. Warner. 1990. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeast in Cos-1 cells. J. Exp. Med. 172:1785-1794.
3. Stahl, P.D., and R.A.B. Ezekowitz. 1998. The mannose receptor is a pattern recognition receptor involved in host defence. Curr. Opin. Immumol. 10:50-55.
4. Taylor, M.E., and K. Drickamer. 1993. Structural requirements for high affinity binding of complex ligands by the macrophage mannose receptor. J. Biol. Chem. 268:399-404.
5. Sallusto, F., M. Cella, C. Danieli, and A. Lanzavecchia. 1995. 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. 182:389-400.
6. 4-4-GalNAcβ1,4GlcNAcβ1,2Manα that mediates rapid clearance of lutropin. Cell. 67:1103-1110.
7. 4-4-GalNAcβ1,4GlcNAcβ or Man at independent sites. Proc. Natl. Acad. Sci. USA. 94:11256-11261.
8. 4-4-GalNAcβ1,4GlcNAcβ1,2Manα-specific receptor from rat liver. J. Biol. Chem. 272:14629-14637.
9. 4 binding. Proc. Natl. Acad. Sci. USA. 95:2089-2093.
10. Weisshaar, G., J. Hiyama, A.G.C. Renwick, and M. Nimtz. 1991. NMR investigations ot the N-linked oligosaccharides at individual glycosylation sites of human lutropin. Eur. J. Biochem. 195:257-268.
11. 4-4-GalNAc and Siaα2,3Gal, respectively. J. Biol. Chem. 268:795-802.
12. Simpson, D.Z., P.G. Hitchen, E.L. Elmhirst, and M.E. Taylor. 1999. Multiple interactions between pituitary hormones and the mannose receptor. Biochem. J. 343:403-411.
13. Martínez-Pomares, L., M. Kosco-Vilbois, E. Darley, P. Tree, S. Herren, J.-Y. Bonnefoy, and S. Gordon. 1996. Fc chimeric protein containing the cysteine-rich domain of the murine mannose receptor binds to macrophages from splenic marginal zone and lymph node subcapsular sinus and to germinal centers. J. Exp. Med. 184:1927-1937.
14. Martínez-Pomares, L., J.A. Mahoney, R. Káposzta, S.A. Linehan, P.D. Stahl, and S. Gordon. 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. 273:23376-23380.
15. Jiang, W., W.J. Swiggard, C. Heufler, M. Peng, A. Mirza, R.M. Steinman, and M.C. Nussenzweig. 1995. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature. 375:151-155.
16. Hennen, G., Z. Pruzik, and G. Maghuin-Rogister. 1971. Porcine lutropin and its subunits. Isolation and characterization. Eur. J. Biochem. 18:376-383.
17. Øynebråten, I., B. Hansen, B. Smedsrod, and L. Uhlin-Hansen. 2000. Serglycin secreted by leukocytes is efficiently eliminated from the circulation by sinusoidal scavanger endothehal cells in the liver. J. Leukoc. Biol. 67:183-188.
18. Lammi, M., and M. Tammi. 1988. Densitometric assay of nanogram quantities of proteoglycans precipitated on nitrocellulose membrane with safranin O. Anal. Biochem. 168: 352-357.
19. Takasaki, S., T. Mizuochi, and A. Kobata. 1982. Hydrazinolysis of asparagine-linked sugar chains to produce free oligosaccharides. Methods Enzymol. 83:263-268.
20. Chai, W., H. Kogelberg, and A.M. Lawson. 1996. Generation and structural characterization of a range of unmodified chondroitin sulfate oligosaccharide fragments. Anal. Biochem. 237:88-102.
21. Ludwigs, U., A. Elgavish, J.D. Esko, E. Meezan, and L. Rodén. 1987. Reaction of unsaturated uronic acid residues with mercuric salts. Cleavage of the hyaluronic acid disaccharide 2-acetamido-2-deoxy-3-O-(β-D-gluco-4-enepyrano-syluronic acid)-D-glucose. Biochem. J. 245:795-804.
22. Bitter, T., and H.M. Muir. 1962. A modified uronic acid carbazole reaction. Anal. Biochem. 4:330-334.
23. Chai, W., A.M. Lawson, M.J. Gradwell, and H. Kogelberg. 1998. Structural characterisation of two hexasaccharides and an octasaccharide from chondroitin sulfate C containing the unusual sequence (4-sulfo)-N-acetylgalactosamine-β1-4-(2-sulfo)-glucuronic acid-β-1-3-(6-sulfo)-N-acetylgalactosamine. Eur. J. Biochem. 251:114-121.
24. Hasegawa, A., T. Ando, A. Kameyama, and M. Kiso. 1992. Synthetic studies on sialoglycoconjugates. 40. Stereocontrolled synthesis of sialyl Lewis X epitope and its ceramide derivative. J. Carbohydr. Chem. 11:645-658.
25. x analogues. In Carbohydrate Mimics: Concepts and Methods. Y. Chapleur, editor. Verlag Chemie, Weinheim, Germany. 365-383.
26. a pentasaccharide, the most potent human E-selectin ligand so far. Bioorg. Med. Chem. 2:1143-1151.
27. Yuen, C.-T., A.M. Lawson, W. Chai, M. Larkin, M.S. Stoll, A.C. Stuart, F.X. Sullivan, T.J. Ahern, and T. Feizi. 1992. Novel sulfated ligands for the cell adhesion molecule E-selectin revealed by the neoglycolipid technology among O-linked oligosaccharides on an ovarian cystadenoma glycoprotein. Biochemistry. 31:9126-9131.
28. Feizi, T., M.S. Stoll, C.-T. Yuen, W. Chai, and A.M. Lawson. 1994. Neoglycolipids: probes of oligosaccharide structure, antigenicity, and function. Methods Enzymol. 230:484-519.
29. Stoll, M.S., and T. Feizi. 1997. Preparation of neoglycolipids for structure and function assignments of oligosaccharides. In A Laboratory Guide to Glycoconjugate Analysis. P. Jackson and J.T. Gallagher, editors. Birkhäuser Verlag, Basel. 329-348.
30. Leteux, C., R.A. Childs, W. Chai, M.S. Stoll, H. Kogelberg, and T. Feizi. 1998. Biotinyl-L-3-(2-naphthyl)-alanine hydrazide derivatives of N-glycans: versatile solid-phase probes for carbohydrate-recognition studies. Glycobiology. 8:227-236.
31. Leteux, C., M.S. Stoll, R.A. Childs, W. Chai, M. Vorozhaikina, and T. Feizi. 1999. Influence of oligosaccharide presentation on the interactions of carbohydrate sequence-specific antibodies and the selectins. Observations with biotinylated oligosaccharides. J. Immunol. Methods. 227: 109-119.
32. Chai, W., G.C. Cashmore, R.A. Carruthers, M.S. Stoll, and A.M. Lawson. 1991. Optimal procedure for combined high performance thin-layer chromatography/high sensitivity liquid secondary ion mass spectrometry. Biol. Mass Spectrom. 20: 169-178.
33. x types: relevance to anti-adhesion therapeutics. Biochemistry. 36:5260-5266.
34. Kolset, S.O., and J.T. Gallagher. 1990. Proteoglycans in haemopoietic cells. Biochim. Biophys. Acta. 1032:191-211.
35. Kresse, H., H. Hausser, and E. Schönherr. 1993. Small proteoglycans. Experientia. 49:403-116.
36. Kulseth, M.A., S.L. Mustorp, L. Uhlin-Hansen, F. Öberg, and S.O. Kolset. 1998. Serglycin expression during monocytic differentiation of U937-1 cells. Glycobiology. 8:747-753.
37. Toyama-Sorimachi, N., F. Kitamura, H. Habuchi, Y. Tobita, K. Kimata, and M. Miyasaka. 1997. Widespread expression of chondroitin sulfate-type serglycins with CD44 binding ability in hematopoietic cells. J. Biol. Chem. 272:26714-26719.
38. Liu, Y., A.J. Chirino, C. Leteux, T. Feizi, Z. Misulovin, M.C. Nussenzweig, and P. Bjorkman. 2000. Crystal structure of the cysteine-rich domain of mannose receptor complexed with a sulfated carbohydrate ligand. J. Exp. Med. 191:1105-1115.
39. Kittlick, P.D., and D. Engelmann. 1992. The glycosaminoglycans in cultures of stimulated rat peritoneal macrophages. 1. Pattern and biosynthesis of glycosaminoglycans. Exp. Toxicol. Pathol. 44:407-413.
40. Piepkorn, M., P. Hovingh, K.L. Bennett, A. Aruffo, and A. Linker. 1997. Chondroitin sulphate composition and structure in alternatively spliced CD44 fusion proteins. Biochem. J. 327:499-506.
41. Naujokas, M.F., M. Morin, M.S. Anderson, M. Peterson, and J. Miller. 1993. The chondroitin sulfate form of invariant chain can enhance stimulation of T cell responses through interaction with CD44. Cell. 74:257-268.
42. Prigozy, T.I., P.A. Sterling, D. Clemens, P.L. Stewart, S.M. Behar, S.A. Porcelli, M.B. Brenner, R.L. Modlin, and M. Kronenberg. 1997. The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity. 6:187-197.
43. Ruoslahti, E. 1989. Proteoglycans in cell regulation. J. Biol. Chem. 264:13369-13372.
44. Feizi, T. 1985. Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are onco-developmental antigens. Nature. 314:53-57.
45. a tetrasaccharide sequence. Glycobiology. 8:1237-1242.
46. Feizi, T. 1993. Oligosaccharides that mediate mammalian cell-cell adhesion. Curr. Opin. Struct. Biol. 3:701-710.
47. Martínez-Pomares, L., and S. Gordon. 1999. Potential role of the mannose receptor in antigen transport. Immunol. Lett. 65: 9-13.
48. Martínez-Pomares, L., P.R. Crocker, R. Da Silva, N. Holmes, C. Colominas, P. Rudd, R. Dwek, and S. Gordon. 1999. Cell-specific glycoforms of sialoadhesin and CD45 are counter-receptors for the cysteine-rich domain of the mannose receptor. J. Biol. Chem. 274:35211-35218.