Expression of the largest CD97 and EMR2 isoforms on leukocytes facilitates a specific interaction with chondroitin sulfate on B cells

Journal of Leukocyte Biology

Volumn 77, Issue 1, 2005, Pages 112-119

  Kwakkenbos, Mark J ^a   Pouwels, Walter ^a   Matmati, Mourad ^a   Stacey, Martin ^b   Lin, Hsi Hsien ^b   Gordon, Siamon ^b   Van Lier, René A W ^a   Hamann, Jörg ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

B cell; EGF like domain; Ligand specificity; Multivalent probe; Proteoglycan

Indexed keywords

CD97 ANTIGEN; DECAY ACCELERATING FACTOR; DERMATAN SULFATE; EPIDERMAL GROWTH FACTOR; GLYCOSAMINOGLYCAN; LIGAND; MEMBRANE ANTIGEN; MONOCLONAL ANTIBODY; PROTEIN EMR2; RECEPTOR PROTEIN; RECOMBINANT ANTIGEN; TM7 RECEPTOR; UNCLASSIFIED DRUG; CD97 PROTEIN, HUMAN; CHONDROITIN SULFATE; EMR2 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; ISOPROTEIN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CONTROLLED STUDY; DENDRITIC CELL; FLUORESCENCE; HUMAN; HUMAN CELL; LEUKOCYTE; MACROPHAGE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION; CELL CULTURE; LYMPHOCYTE ACTIVATION; METABOLISM;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD55; B-LYMPHOCYTES; CELLS, CULTURED; CHONDROITIN SULFATES; DENDRITIC CELLS; EPIDERMAL GROWTH FACTOR; HUMANS; LEUKOCYTES; LIGANDS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MYELOID CELLS; PROTEIN ISOFORMS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 14644430368     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0704402     Document Type: Article

References (49)

1. Montoya, M. C., Sancho, D., Vicente-Manzanares, M., Sanchez-Madrid, F. (2002) Cell adhesion and polarity during immune interactions. Immunol. Rev. 186, 68-82.
2. McKnight, A. J., Gordon, S. (1996) EGF-TM7: a novel subfamily of seven-transmembrane-region leukocyte cell-surface molecules. Immunol. Today 17, 283-287.
3. Kwakkenbos, M. J., Kop, E. N., Stacey, M., Matmati, M., Gordon, S., Lin, H. H., Hamann, J. (2004) The EGF-TM7 family: a postgenomic view. Immunogenetics 55, 655-666.
4. Leemans, J. C., te Velde, A. A., Florquin, S., Bennink, R. J., de Bruin, K., van Lier, R. A., van der Poll, T., Hamann, J. (2004) The epidermal growth factor-seven transmembrane (EGF-TM7) receptor CD97 is required for neutrophil migration and host defense. J. Immunol. 172, 1125-1131.
5. Stacey, M., Lin, H. H., Gordon, S., McKnight, A. J. (2000) LNB-TM7, a group of seven-transmembrane proteins related to family-B G-protein-coupled receptors. Trends Biochem. Sci. 25, 284-289.
6. Fredriksson, R., Lagerstrom, M. C., Lundin, L. G., Schioth, H. B. (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256-1272.
7. Bjarnadottir, T. K., Fredriksson, R., Hoglund, P. J., Gloriam, D. E., Lagerstrom, M. C., Schioth, H. B. (2004) The human and mouse repertoire of the adhesion family of G-protein-coupled receptors. Genomics 84, 23-33.
8. Hamann, J., Eichler, W., Hamann, D., Kerstens, H. M., Poddighe, P. J., Hoovers, J. M., Hartmann, E., Strauss, M., van Lier, R. A. (1995) Expression cloning and chromosomal mapping of the leukocyte activation antigen CD97, a new seven-span transmembrane molecule of the secretion receptor superfamily with an unusual extracellular domain. J. Immunol. 155, 1942-1950.
9. Gray, J. X., Haino, M., Roth, M. J., Maguire, J. E., Jensen, P. N., Yarme, A., Stetler-Stevenson, M. A., Siebenlist, U., Kelly, K. (1996) CD97 is a processed, seven-transmembrane, heterodimeric receptor associated with inflammation. J. Immunol. 157, 5438-5447.
10. Baud, V., Chissoe, S. L., Viegas-Pequignot, E., Diriong, S., N'Guyen, V. C., Roe, B. A., Lipinski, M. (1995) EMR1, an unusual member in the family of hormone receptors with seven transmembrane segments. Genomics 26, 334-344.
11. Lin, H. H., Stacey, M., Hamann, J., Gordon, S., McKnight, A. J. (2000) Human EMR2, a novel EGF-TM7 molecule on chromosome 19pl3.1, is closely related to CD97. Genomics 67, 188-200.
12. Stacey, M., Lin, H. H., Hilyard, K. L., Gordon, S., McKnight, A. J. (2001) Human epidermal growth factor (EGF) module-containing mucin-like hormone receptor 3 is a new member of the EGF-TM7 family that recognizes a ligand on human macrophages and activated neutrophils. J. Biol. Chem. 276, 18863-18870.
13. Hamann, J., Kwakkenbos, M. J., de Jong, E. C., Heus, H., Olsen, A. S., van Lier, R. A. (2003) Inactivation of the EGF-TM7 receptor EMR4 after the Pan-Homo divergence. Eur. J. Immunol. 33, 1365-1371.
14. Eichler, W., Aust, G., Hamann, D. (1994) Characterization of an early activation-dependent antigen on lymphocytes defined by the monoclonal antibody BL-Ac(F2). Scand. J. Immunol. 39, 111-115.
15. Jaspars, L. H., Vos, W., Aust, G., Van Lier, R. A., Hamann, J. (2001) Tissue distribution of the human CD97 EGF-TM7 receptor. Tissue Antigens 57, 325-331.
16. Hamann, J., Vogel, B., van Schijndel, G. M., van Lier, R. A. (1996) The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J. Exp. Med. 184, 1185-1189.
17. Hamann, J., Stortelers, C., Kiss-Toth, E., Vogel, B., Eichler, W., van Lier, R. A. (1998) Characterization of the CD55 (DAF)-binding site on the seven-span transmembrane receptor CD97. Eur. J. Immunol. 28, 1701-1707.
18. Lin, H. H., Stacey, M., Saxby, C., Knott, V., Chaudhry, Y., Evans, D., Gordon, S., McKnight, A. J., Handford, P., Lea, S. (2001) Molecular analysis of the epidermal growth factor-like short consensus repeat domain-mediated protein-protein interactions: dissection of the CD97-CD55 complex. J. Biol. Chem. 276, 24160-24169.
19. Stacey, M., Chang, G. W., Davies, J. Q., Kwakkenbos, M. J., Sanderson, R. D., Hamann, J., Gordon, S., Lin, H. H. (2003) The epidermal growth factor-like domains of the human EMR2 receptor mediate cell attachment through chondroitin sulfate glycosaminoglycans. Blood 102, 2916-2924.
20. Lublin, D. M., Atkinson, J. P. (1989) Decay-accelerating factor: biochemistry, molecular biology, and function. Annu. Rev. Immunol. 7, 35-58.
21. Trowbridge, J. M., Gallo, R. L. (2002) Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology 12, 117R-125R.
22. Sugahara, K., Mikami, T., Uyama, T., Mizuguchi, S., Nomura, K., Kitagawa, H. (2003) Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13, 612-620.
23. Stacey, M., Chang, G. W., Sanos, S. L., Chittenden, L. R., Stubbs, L., Gordon, S., Lin, H. H. (2002) EMR4, a novel epidermal growth factor (EGF)-TM7 molecule up-regulated in activated mouse macrophages, binds to a putative cellular ligand on B lymphoma cell line A20. J. Biol. Chem. 277, 29283-29293.
24. Bende, R. J., Jochems, G. J., Frame, T. H., Klein, M. R., van Eijk, R. V., van Lier, R. A., Zeijlemaker, W. P. (1992) Effects of IL-4, IL-5, and IL-6 on growth and immunoglobulin production of Epstein-Barr virus-infected human B cells. Cell. Immunol. 143, 310-323.
25. Kwakkenbos, M. J., van Lier, R. A. W., Hamann, J. (2002) Characterization of EGF-TM7 family members by novol monoclonal antibodies. In Leukocyte Typing VII (D. Mason, ed.), Oxford, UK, Oxford University Press, 381-383.
26. Kwakkenbos, M. J., Chang, G. W., Lin, H. H., Pouwels, W., de Jong, E. C., van Lier, R. A., Gordon, S., Hamann, J. (2002) The human EGF-TM7 family member EMR2 is a heterodimeric receptor expressed on myeloid cells. J. Leukoc. Biol. 71, 854-862.
27. Brown, M. H., Preston, S., Barclay, A. N. (1995) A sensitive assay for detecting low-affinity interactions at the cell surface reveals no additional ligands for the adhesion pair rat CD2 and CD48. Eur. J. Immunol. 25, 3222-3228.
28. + subpopulation. Immunol. Today 17, 424-428.
29. ++ cells derived in vitro from peripheral blood monocytes exhibit phenotypic and functional dendritic cell-like characteristics. Eur. J. Immunol. 30, 1872-1883.
30. Randolph, G. J., Sanchez-Schmitz, G., Liebman, R. M., Schakel, K. (2002) The CD16(+) (FcγRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J. Exp. Med. 196, 517-527.
31. Geissmann, F., Jung, S., Littman, D. R. (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71-82.
32. Prydz, K., Dalen, K. T. (2000) Synthesis and sorting of proteoglycans. J. Cell Sci. 113, 193-205.
33. Carey, D. J. (1997) Syndecans: multifunctional cell-surface co-receptors. Biochem. J. 327, 1-16.
34. Yamashita, Y., Oritani, K., Miyoshi, E. K., Wall, R., Bernfield, M., Kincade, P. W. (1999) Syndecan-4 is expressed by B lineage lymphocytes and can transmit a signal for formation of dendritic processes. J. Immunol. 162, 5940-5948.
35. van Kooyk, Y., Geijtenbeek, T. B. (2003) DC-SIGN: escape mechanism for pathogens. Nat. Rev. Immunol. 3, 697-709.
36. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N., Kosco-Vilbois, M. H. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl. Acad. Sci. USA 100, 1885-1890.
37. Middleton, J., Patterson, A. M., Gardner, L., Schmutz, C., Ashton, B. A. (2002) Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 100, 3853-3860.
38. Li, Q., Park, P. W., Wilson, C. L., Parks, W. C. (2002) Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111, 635-646.
39. Berger, M., Medof, M. E. (1987) Increased expression of complement decay-accelerating factor during activation of human neutrophils. J. Clin. Invest. 79, 214-220.
40. Stevens, C. R., Mapp, P. I., Revell, P. A. (1990) A monoclonal antibody (Mab 67) marks type B synoviocytes. Rheumatol. Int. 10, 103-106.
41. Li, L., Spendlove, I., Morgan, J., Durrant, L. G. (2001) CD55 is overexpressed in the tumour environment. Br. J. Cancer 84, 80-86.
42. Hindmarsh, E. J., Marks, R. M. (1998) Decay-accelerating factor is a component of subendothelial extracellular matrix in vitro, and is augmented by activation of endothelial protein kinase C. Eur. J. Immunol. 28, 1052-1062.
43. Steinert, M., Wobus, M., Boltze, C., Schutz, A., Wahlbuhl, M., Hamann, J., Aust, G. (2002) Expression and regulation of CD97 in colorectal carcinoma cell lines and tumor tissues. Am. J. Pathol. 161, 1657-1667.
44. Eichler, W. (2000) CD97 isoform expression in leukocytes. J. Leukoc. Biol. 68, 561-567.
45. MacLennan, I. C. (1994) Germinal centers. Annu. Rev. Immunol. 12, 117-139.
46. Groeneveld, P. H., Erich, T., Kraal, G. (1986) The differential effects of bacterial lipopolysaccharide (LPS) on splenic non-lymphoid cells demonstrated by monoclonal antibodies. Immunology 58, 285-290.
47. Berney, C., Herren, S., Power, C. A., Gordon, S., Martinez-Pomares, L., Kosco-Vilbois, M. H. (1999) A member of the dendritic cell family that enters B cell follicles and stimulates primary antibody responses identified by a mannose receptor fusion protein. J. Exp. Med. 190, 851-860.
48. Sims-Mourtada, J. C., Guzman-Rojas, L., Rangel, R., Nghiem, D. X., Ullrich, S. E., Guret, C., Cain, K., Martinez-Valdez, H. (2003) In vivo expression of interleukin-8, and regulated on activation, normal, T-cell expressed, and secreted, by human germinal centre B lymphocytes. Immunology 110, 296-303.
49. Krzysiek, R., Lefevre, E. A., Zou, W., Foussat, A., Bernard, J., Portier, A., Galanaud, P., Richard, Y. (1999) Antigen receptor engagement selectively induces macrophage inflammatory protein-1 α (MIP-1 α) and MIP-1 β chemokine production in human B cells. J. Immunol. 162, 4455-4463.