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. 2002 Feb 15;362(Pt 1):155–164. doi: 10.1042/0264-6021:3620155

Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues.

Oliver Politz 1, Alexei Gratchev 1, Peter A G McCourt 1, Kai Schledzewski 1, Pierre Guillot 1, Sophie Johansson 1, Gunbjorg Svineng 1, Peter Franke 1, Christoph Kannicht 1, Julia Kzhyshkowska 1, Paola Longati 1, Florian W Velten 1, Staffan Johansson 1, Sergij Goerdt 1
PMCID: PMC1222372  PMID: 11829752

Abstract

MS-1, a high-molecular-mass protein expressed by non-continuous and angiogenic endothelial cells and by alternatively activated macrophages (Mphi2), and the hepatic sinusoidal endothelial hyaluronan clearance receptor are similar with respect to tissue distribution and biochemical characteristics. In the present study we purified these proteins by immuno- and hyaluronan-affinity chromatography respectively, sequenced tryptic peptides and generated full-length cDNA sequences in both mouse and human. The novel genes, i.e. stabilin-1 and stabilin-2, code for homologous transmembrane proteins featuring seven fasciclin-like adhesion domains, 18-20 epidermal-growth-factor domains, one X-link domain and three to six B-(X(7))-B hyaluronan-binding motifs. Northern-blotting experiments revealed the presence of both stabilins in organs with predominant endothelial sinuses such as liver, spleen and lymph node: stabilin-1 mRNA was also detected in organs with predominant Mphi2 cells, such as placenta, and in interleukin-4/glucocorticoid-stimulated Mphi2 cells in vitro. A polyclonal antibody made against human recombinant stabilin-1 confirmed the expression of stabilin-1 protein in splenic sinus endothelial cells in vivo and in Mphi2 in vitro. On the basis of high similarity at the protein level and the unique domain composition, which differs from that of all other known fasciclin-like proteins and hyaluronan receptors, stabilin-1 and stabilin-2 define a novel family of fasciclin-like hyaluronan receptor homologues that might play a role in cell-cell and cell-matrix interactions in vascular function and inflammatory processes.

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Selected References

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  1. Ades E. W., Candal F. J., Swerlick R. A., George V. G., Summers S., Bosse D. C., Lawley T. J. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol. 1992 Dec;99(6):683–690. doi: 10.1111/1523-1747.ep12613748. [DOI] [PubMed] [Google Scholar]
  2. Dietrich J., Bäckström T., Lauritsen J. P., Kastrup J., Christensen M. D., von Bülow F., Palmer E., Geisler C. The phosphorylation state of CD3gamma influences T cell responsiveness and controls T cell receptor cycling. J Biol Chem. 1998 Sep 11;273(37):24232–24238. doi: 10.1074/jbc.273.37.24232. [DOI] [PubMed] [Google Scholar]
  3. Djemadji-Oudjiel N., Goerdt S., Kodelja V., Schmuth M., Orfanos C. E. Immunohistochemical identification of type II alternatively activated dendritic macrophages (RM 3/1+3, MS-1+/-, 25F9-) in psoriatic dermis. Arch Dermatol Res. 1996 Nov;288(12):757–764. doi: 10.1007/BF02505293. [DOI] [PubMed] [Google Scholar]
  4. Elkins T., Hortsch M., Bieber A. J., Snow P. M., Goodman C. S. Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting. J Cell Biol. 1990 May;110(5):1825–1832. doi: 10.1083/jcb.110.5.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Eriksson S., Fraser J. R., Laurent T. C., Pertoft H., Smedsrød B. Endothelial cells are a site of uptake and degradation of hyaluronic acid in the liver. Exp Cell Res. 1983 Mar;144(1):223–228. doi: 10.1016/0014-4827(83)90458-5. [DOI] [PubMed] [Google Scholar]
  6. Fraser J. R., Kimpton W. G., Laurent T. C., Cahill R. N., Vakakis N. Uptake and degradation of hyaluronan in lymphatic tissue. Biochem J. 1988 Nov 15;256(1):153–158. doi: 10.1042/bj2560153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goerdt S., Bhardwaj R., Sorg C. Inducible expression of MS-1 high-molecular-weight protein by endothelial cells of continuous origin and by dendritic cells/macrophages in vivo and in vitro. Am J Pathol. 1993 May;142(5):1409–1422. [PMC free article] [PubMed] [Google Scholar]
  8. Goerdt S., Kolde G., Bonsmann G., Hamann K., Czarnetzki B., Andreesen R., Luger T., Sorg C. Immunohistochemical comparison of cutaneous histiocytoses and related skin disorders: diagnostic and histogenetic relevance of MS-1 high molecular weight protein expression. J Pathol. 1993 Aug;170(4):421–427. doi: 10.1002/path.1711700404. [DOI] [PubMed] [Google Scholar]
  9. Goerdt S., Orfanos C. E. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity. 1999 Feb;10(2):137–142. doi: 10.1016/s1074-7613(00)80014-x. [DOI] [PubMed] [Google Scholar]
  10. Goerdt S., Walsh L. J., Murphy G. F., Pober J. S. Identification of a novel high molecular weight protein preferentially expressed by sinusoidal endothelial cells in normal human tissues. J Cell Biol. 1991 Jun;113(6):1425–1437. doi: 10.1083/jcb.113.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goerdt S., Walsh L. J., Murphy G. F., Pober J. S. Identification of a novel high molecular weight protein preferentially expressed by sinusoidal endothelial cells in normal human tissues. J Cell Biol. 1991 Jun;113(6):1425–1437. doi: 10.1083/jcb.113.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gratchev A., Guillot P., Hakiy N., Politz O., Orfanos C. E., Schledzewski K., Goerdt S. Alternatively activated macrophages differentially express fibronectin and its splice variants and the extracellular matrix protein betaIG-H3. Scand J Immunol. 2001 Apr;53(4):386–392. doi: 10.1046/j.1365-3083.2001.00885.x. [DOI] [PubMed] [Google Scholar]
  13. Hamann J., Vogel B., van Schijndel G. M., van Lier R. A. The seven-span transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J Exp Med. 1996 Sep 1;184(3):1185–1189. doi: 10.1084/jem.184.3.1185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hirate Y., Tomita K., Yamamoto S., Kobari K., Uemura I., Yamasu K., Suyemitsu T. Association of the sea urchin EGF-related peptide, EGIP-D, with fasciclin I-related ECM proteins from the sea urchin Anthocidaris crassispina. Dev Growth Differ. 1999 Aug;41(4):483–494. doi: 10.1046/j.1440-169x.1999.00446.x. [DOI] [PubMed] [Google Scholar]
  15. Hofmann M., Assmann V., Fieber C., Sleeman J. P., Moll J., Ponta H., Hart I. R., Herrlich P. Problems with RHAMM: a new link between surface adhesion and oncogenesis? Cell. 1998 Nov 25;95(5):591–593. doi: 10.1016/s0092-8674(00)81628-1. [DOI] [PubMed] [Google Scholar]
  16. Horiuchi K., Amizuka N., Takeshita S., Takamatsu H., Katsuura M., Ozawa H., Toyama Y., Bonewald L. F., Kudo A. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res. 1999 Jul;14(7):1239–1249. doi: 10.1359/jbmr.1999.14.7.1239. [DOI] [PubMed] [Google Scholar]
  17. Horton M. R., Burdick M. D., Strieter R. M., Bao C., Noble P. W. Regulation of hyaluronan-induced chemokine gene expression by IL-10 and IFN-gamma in mouse macrophages. J Immunol. 1998 Mar 15;160(6):3023–3030. [PubMed] [Google Scholar]
  18. Horton M. R., McKee C. M., Bao C., Liao F., Farber J. M., Hodge-DuFour J., Puré E., Oliver B. L., Wright T. M., Noble P. W. Hyaluronan fragments synergize with interferon-gamma to induce the C-X-C chemokines mig and interferon-inducible protein-10 in mouse macrophages. J Biol Chem. 1998 Dec 25;273(52):35088–35094. doi: 10.1074/jbc.273.52.35088. [DOI] [PubMed] [Google Scholar]
  19. Hu S., Sonnenfeld M., Stahl S., Crews S. T. Midline Fasciclin: a Drosophila Fasciclin-I-related membrane protein localized to the CNS midline cells and trachea. J Neurobiol. 1998 Apr;35(1):77–93. doi: 10.1002/(sici)1097-4695(199804)35:1<77::aid-neu7>3.0.co;2-8. [DOI] [PubMed] [Google Scholar]
  20. Huber O., Sumper M. Algal-CAMs: isoforms of a cell adhesion molecule in embryos of the alga Volvox with homology to Drosophila fasciclin I. EMBO J. 1994 Sep 15;13(18):4212–4222. doi: 10.1002/j.1460-2075.1994.tb06741.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kim J. E., Kim S. J., Lee B. H., Park R. W., Kim K. S., Kim I. S. Identification of motifs for cell adhesion within the repeated domains of transforming growth factor-beta-induced gene, betaig-h3. J Biol Chem. 2000 Oct 6;275(40):30907–30915. doi: 10.1074/jbc.M002752200. [DOI] [PubMed] [Google Scholar]
  22. Kodelja V., Müller C., Tenorio S., Schebesch C., Orfanos C. E., Goerdt S. Differences in angiogenic potential of classically vs alternatively activated macrophages. Immunobiology. 1997 Nov;197(5):478–493. doi: 10.1016/S0171-2985(97)80080-0. [DOI] [PubMed] [Google Scholar]
  23. LeBaron R. G., Bezverkov K. I., Zimber M. P., Pavelec R., Skonier J., Purchio A. F. Beta IG-H3, a novel secretory protein inducible by transforming growth factor-beta, is present in normal skin and promotes the adhesion and spreading of dermal fibroblasts in vitro. J Invest Dermatol. 1995 May;104(5):844–849. doi: 10.1111/1523-1747.ep12607024. [DOI] [PubMed] [Google Scholar]
  24. Lee J. Y., Spicer A. P. Hyaluronan: a multifunctional, megaDalton, stealth molecule. Curr Opin Cell Biol. 2000 Oct;12(5):581–586. doi: 10.1016/s0955-0674(00)00135-6. [DOI] [PubMed] [Google Scholar]
  25. Mahoney D. J., Blundell C. D., Day A. J. Mapping the hyaluronan-binding site on the link module from human tumor necrosis factor-stimulated gene-6 by site-directed mutagenesis. J Biol Chem. 2001 Apr 3;276(25):22764–22771. doi: 10.1074/jbc.M100666200. [DOI] [PubMed] [Google Scholar]
  26. McCourt P. A., Gustafson S. On the adsorption of hyaluronan and ICAM-1 to modified hydrophobic resins. Int J Biochem Cell Biol. 1997 Oct;29(10):1179–1189. doi: 10.1016/s1357-2725(97)00058-7. [DOI] [PubMed] [Google Scholar]
  27. McCourt P. A., Smedsrød B. H., Melkko J., Johansson S. Characterization of a hyaluronan receptor on rat sinusoidal liver endothelial cells and its functional relationship to scavenger receptors. Hepatology. 1999 Nov;30(5):1276–1286. doi: 10.1002/hep.510300521. [DOI] [PubMed] [Google Scholar]
  28. Page R. D. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996 Aug;12(4):357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  29. Romancino D. P., Ghersi G., Montana G., Bonura A., Perriera S., Di Carlo M. Characterization of bep1 and bep4 antigens involved in cell interactions during Paracentrotus lividus development. Differentiation. 1992 Jun;50(2):67–74. doi: 10.1111/j.1432-0436.1992.tb00487.x. [DOI] [PubMed] [Google Scholar]
  30. Rosenfeld J., Capdevielle J., Guillemot J. C., Ferrara P. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal Biochem. 1992 May 15;203(1):173–179. doi: 10.1016/0003-2697(92)90061-b. [DOI] [PubMed] [Google Scholar]
  31. Schebesch C., Kodelja V., Müller C., Hakij N., Bisson S., Orfanos C. E., Goerdt S. Alternatively activated macrophages actively inhibit proliferation of peripheral blood lymphocytes and CD4+ T cells in vitro. Immunology. 1997 Dec;92(4):478–486. doi: 10.1046/j.1365-2567.1997.00371.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem. 1996 Mar 1;68(5):850–858. doi: 10.1021/ac950914h. [DOI] [PubMed] [Google Scholar]
  33. Singer I. I. The fibronexus: a transmembrane association of fibronectin-containing fibers and bundles of 5 nm microfilaments in hamster and human fibroblasts. Cell. 1979 Mar;16(3):675–685. doi: 10.1016/0092-8674(79)90040-0. [DOI] [PubMed] [Google Scholar]
  34. Szekanecz Z., Haines G. K., Lin T. R., Harlow L. A., Goerdt S., Rayan G., Koch A. E. Differential distribution of intercellular adhesion molecules (ICAM-1, ICAM-2, and ICAM-3) and the MS-1 antigen in normal and diseased human synovia. Their possible pathogenetic and clinical significance in rheumatoid arthritis. Arthritis Rheum. 1994 Feb;37(2):221–231. doi: 10.1002/art.1780370211. [DOI] [PubMed] [Google Scholar]
  35. Termeer C. C., Hennies J., Voith U., Ahrens T., Weiss J. M., Prehm P., Simon J. C. Oligosaccharides of hyaluronan are potent activators of dendritic cells. J Immunol. 2000 Aug 15;165(4):1863–1870. doi: 10.4049/jimmunol.165.4.1863. [DOI] [PubMed] [Google Scholar]
  36. Teuchert M., Berghöfer S., Klenk H. D., Garten W. Recycling of furin from the plasma membrane. Functional importance of the cytoplasmic tail sorting signals and interaction with the AP-2 adaptor medium chain subunit. J Biol Chem. 1999 Dec 17;274(51):36781–36789. doi: 10.1074/jbc.274.51.36781. [DOI] [PubMed] [Google Scholar]
  37. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Walsh L. J., Goerdt S., Pober J. S., Sueki H., Murphy G. F. MS-1 sinusoidal endothelial antigen is expressed by factor XIIIa+, HLA-DR+ dermal perivascular dendritic cells. Lab Invest. 1991 Dec;65(6):732–741. [PubMed] [Google Scholar]
  39. Yang B., Yang B. L., Savani R. C., Turley E. A. Identification of a common hyaluronan binding motif in the hyaluronan binding proteins RHAMM, CD44 and link protein. EMBO J. 1994 Jan 15;13(2):286–296. doi: 10.1002/j.1460-2075.1994.tb06261.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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