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 Lewisx Types in Addition to the Sulfated N-Glycans of Lutropin

doi:10.1084/jem.191.7.1117

Published online 27 March 2000.

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© The Rockefeller University Press, 0022-1007/2000/4/1117/ $5.00
The Journal of Experimental Medicine, Volume 191, Number 7, April 3, 2000 1117-1126

Original Article

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 Lewis^a and Lewis^x Types in Addition to the Sulfated N-Glycans of Lutropin

Christine Leteux^a, Wengang Chai^a, R. Wendy Loveless^a, Chun-Ting Yuen^b, Lars Uhlin-Hansen^c, Yves Combarnous^d, Mila Jankovic^e, Svetlana C. Maric^e, Ziva Misulovin^e,f, Michel C. Nussenzweig^e,f, and Ten Feizi^a
^a The Glycosciences Laboratory, Imperial College School of Medicine, Northwick Park Hospital, Harrow HA1 3UJ, United Kingdom
^b Laboratory of Molecular Structure, National Institute for Biological Standards and Control, Hertfordshire EN6 3QG, United Kingdom
^c Department of Biochemistry, Institute of Medical Biology, University of Tromsø, N-9037 Tromsø, Norway
^d Institut National de la Recherche Agronomique, Unit 1291, Station Physiologie de la Reproduction des Mammifères Domestiques, 37380 Nouzilly, France
^e Department of Molecular Immunology, The Rockefeller University, New York, New York 10021-6399
^f The Howard Hughes Medical Institute, The Rockefeller University, New York, New York 10021-6399

Correspondence to: Ten Feizi, The Glycosciences Laboratory, Imperial College School of Medicine, Northwick Park Hospital, Watford Road, Harrow, Middlesex HA1 3UJ, UK. Tel:44-20-8869-3460 Fax:44-20-8869-3455 E-mail:t.feizi{at}ic.ac.uk.

The mannose receptor (MR) is an endocytic protein on macrophagesand dendritic cells, as well as on hepatic endothelial, kidneymesangial, tracheal smooth muscle, and retinal pigment epithelialcells. The extracellular portion contains two types of carbohydrate-recognitiondomain (CRD): eight membrane-proximal C-type CRDs and a membrane-distalcysteine-rich domain (Cys-MR). The former bind mannose-, N-acetylglucosamine-,and fucose-terminating oligosaccharides, and may be importantin innate immunity towards microbial pathogens, and in antigentrapping for processing and presentation in adaptive immunity.Cys-MR binds to the sulfated carbohydrate chains of pituitaryhormones and may have a role in hormonal clearance. A secondfeature of Cys-MR is binding to macrophages in marginal zonesof the spleen, and to B cell areas in germinal centers whichmay help direct MR-bearing cells toward germinal centers duringthe immune response. Here we describe two novel classes of carbohydrateligand for Cys-MR: chondroitin-4 sulfate chains of the typefound on proteoglycans produced by cells of the immune system,and sulfated blood group chains. We further demonstrate thatCys-MR interacts with cells in the spleen via the binding sitefor sulfated carbohydrates. Our data suggest that the threeclasses of sulfated carbohydrate ligands may variously regulatethe trafficking and function of MR-bearing cells.

Key Words: chondroitin sulfate, cysteine-rich domain, lutropin (luteinizinghormone), macrophage receptor, sulfo-Lewis^a/x

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