{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T18:18:28Z","timestamp":1791310708961,"version":"4.3.1"},"reference-count":81,"publisher":"Rockefeller University Press","issue":"8","content-domain":{"domain":["rupress.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2000,10,16]]},"abstract":"<jats:p>Recently, biochemical, cell biological, and genetic studies have converged to reveal that integral membrane heparan sulfate proteoglycans (HSPGs) are critical regulators of growth and differentiation of epithelial and connective tissues. As a large number of cytokines involved in lymphoid tissue homeostasis or inflammation contain potential HS-binding domains, HSPGs presumably also play important roles in the regulation of the immune response. In this report, we explored the expression, regulation, and function of HSPGs on B lymphocytes. We demonstrate that activation of the B cell antigen receptor (BCR) and\/or CD40 induces a strong transient expression of HSPGs on human tonsillar B cells. By means of these HSPGs, the activated B cells can bind hepatocyte growth factor (HGF), a cytokine that regulates integrin-mediated B cell adhesion and migration. This interaction with HGF is highly selective since the HSPGs did not bind the chemokine stromal cell\u2013derived factor (SDF)-1\u03b1, even though the affinities of HGF and SDF-1\u03b1 for heparin are similar. On the activated B cells, we observed induction of a specific HSPG isoform of CD44 (CD44-HS), but not of other HSPGs such as syndecans or glypican-1. Interestingly, the expression of CD44-HS on B cells strongly promotes HGF-induced signaling, resulting in an HS-dependent enhanced phosphorylation of Met, the receptor tyrosine kinase for HGF, as well as downstream signaling molecules including Grb2-associated binder 1 (Gab1) and Akt\/protein kinase B (PKB). Our results demonstrate that the BCR and CD40 control the expression of HSPGs, specifically CD44-HS. These HSPGs act as functional coreceptors that selectively promote cytokine signaling in B cells, suggesting a dynamic role for HSPGs in antigen-specific B cell differentiation.<\/jats:p>","DOI":"10.1084\/jem.192.8.1115","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T16:48:33Z","timestamp":1027702113000},"page":"1115-1124","update-policy":"https:\/\/doi.org\/10.1084\/jem.crossmarkpolicy","source":"Crossref","is-referenced-by-count":43,"title":["Regulation of Cytokine Signaling by B Cell Antigen Receptor and Cd40-Controlled Expression of Heparan Sulfate Proteoglycans"],"prefix":"10.1084","volume":"192","author":[{"given":"Robbert","family":"van der Voort","sequence":"first","affiliation":[{"name":"aDepartment of Pathology, Academic Medical Center, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert M.J.","family":"Keehnen","sequence":"additional","affiliation":[{"name":"aDepartment of Pathology, Academic Medical Center, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Esther A.","family":"Beuling","sequence":"additional","affiliation":[{"name":"aDepartment of Pathology, Academic Medical Center, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcel","family":"Spaargaren","sequence":"additional","affiliation":[{"name":"aDepartment of Pathology, Academic Medical Center, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven T.","family":"Pals","sequence":"additional","affiliation":[{"name":"aDepartment of Pathology, Academic Medical Center, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[2000,10,9]]},"reference":[{"key":"2023072509270380800_R1","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1146\/annurev.bi.60.070191.002303","article-title":"Proteoglycansstructures and interactions","volume":"60","author":"Kjellen","year":"1991","journal-title":"Annu. 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Cell Biol."},{"key":"2023072509270380800_R11","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1038\/ng0396-241","article-title":"Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome","volume":"12","author":"Pilia","year":"1996","journal-title":"Nat. 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Biol. Chem."},{"key":"2023072509270380800_R16","doi-asserted-by":"crossref","first-page":"7158","DOI":"10.1073\/pnas.90.15.7158","article-title":"Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8","volume":"90","author":"Webb","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072509270380800_R17","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1038\/332376a0","article-title":"Heparan sulphate bound growth factorsa mechanism for stromal cell mediated haemopoiesis","volume":"332","author":"Roberts","year":"1988","journal-title":"Nature."},{"key":"2023072509270380800_R18","doi-asserted-by":"crossref","first-page":"11216","DOI":"10.1016\/S0021-9258(19)78113-7","article-title":"Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants","volume":"269","author":"Lyon","year":"1994","journal-title":"J. Biol. Chem."},{"key":"2023072509270380800_R19","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1038\/326403a0","article-title":"Compartmentalization of a haematopoietic growth factor (GM-CSF) by glycosaminoglycans in the bone marrow microenvironment","volume":"326","author":"Gordon","year":"1987","journal-title":"Nature."},{"key":"2023072509270380800_R20","doi-asserted-by":"crossref","first-page":"29586","DOI":"10.1074\/jbc.270.49.29586","article-title":"Characterization of heparan sulfate oligosaccharides that bind to hepatocyte growth factor","volume":"270","author":"Ashikari","year":"1995","journal-title":"J. Biol. Chem."},{"key":"2023072509270380800_R21","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1002\/1529-0131(199808)41:8<1365::AID-ART5>3.0.CO;2-W","article-title":"Heparan sulfate proteoglycan on endothelium efficiently induces integrin-mediated T cell adhesion by immobilizing chemokines in patients with rheumatoid synovitis","volume":"41","author":"Tanaka","year":"1998","journal-title":"Arthritis Rheum."},{"key":"2023072509270380800_R22","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1038\/361079a0","article-title":"T-cell adhesion induced by proteoglycan-immobilized cytokine MIP-1 beta","volume":"361","author":"Tanaka","year":"1993","journal-title":"Nature."},{"key":"2023072509270380800_R23","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/0167-5699(92)90039-A","article-title":"Endothelial cell binding of NAP-1\/IL-8role in neutrophil emigration","volume":"13","author":"Rot","year":"1992","journal-title":"Immunol. Today."},{"key":"2023072509270380800_R24","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1146\/annurev.immunol.15.1.675","article-title":"Human chemokinesan update","volume":"15","author":"Baggiolini","year":"1997","journal-title":"Annu. Rev. Immunol."},{"key":"2023072509270380800_R25","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1146\/annurev.iy.12.040194.004313","article-title":"The CD40 antigen and its ligand","volume":"12","author":"Banchereau","year":"1994","journal-title":"Annu. Rev. Immunol."},{"key":"2023072509270380800_R26","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/S0167-5699(97)01160-2","article-title":"Triple check for antigen specificity of B cells during germinal centre reactions","volume":"18","author":"Lindhout","year":"1997","journal-title":"Immunol. 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Med."},{"key":"2023072509270380800_R31","doi-asserted-by":"crossref","first-page":"990","DOI":"10.1182\/blood.V89.3.990","article-title":"Hepatocyte growth factor\/scatter factor promotes adhesion of lymphoma cells to extracellular matrix molecules via alpha 4 beta 1 and alpha 5 beta 1 integrins","volume":"89","author":"Weimar","year":"1997","journal-title":"Blood."},{"key":"2023072509270380800_R32","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1083\/jcb.105.2.983","article-title":"Lymphocyte recognition of high endotheliumantibodies to distinct epitopes of an 85\u201395-kD glycoprotein antigen differentially inhibit lymphocyte binding to lymph node, mucosal, or synovial endothelial cells","volume":"105","author":"Jalkanen","year":"1987","journal-title":"J. Cell Biol."},{"key":"2023072509270380800_R33","doi-asserted-by":"crossref","first-page":"7009","DOI":"10.1016\/S0021-9258(18)83533-5","article-title":"Multiple distinct membrane heparan sulfate proteoglycans in human lung fibroblasts","volume":"264","author":"Lories","year":"1989","journal-title":"J. Biol. Chem."},{"key":"2023072509270380800_R34","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1083\/jcb.118.4.961","article-title":"Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells","volume":"118","author":"David","year":"1992","journal-title":"J. Cell Biol."},{"key":"2023072509270380800_R35","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1042\/bj2470765","article-title":"Identification of a 64 kDa heparan sulphate proteoglycan core protein from human lung fibroblast plasma membranes with a monoclonal antibody","volume":"247","author":"de Boeck","year":"1987","journal-title":"Biochem. J."},{"key":"2023072509270380800_R36","doi-asserted-by":"crossref","first-page":"3760","DOI":"10.4049\/jimmunol.152.8.3760","article-title":"Adhesion through the LFA-1 (CD11a\/CD18)-ICAM-1 (CD54) and the VLA-4 (CD49d)-VCAM-1 (CD106) pathways prevents apoptosis of germinal center B cells","volume":"152","author":"Koopman","year":"1994","journal-title":"J. Immunol."},{"key":"2023072509270380800_R37","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1126\/science.7537388","article-title":"Generation of memory B cells and plasma cells in vitro","volume":"268","author":"Arpin","year":"1995","journal-title":"Science."},{"key":"2023072509270380800_R38","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1006\/bbrc.1995.2267","article-title":"Binding of cell-surface expressed CD44 to hyaluronate is dependent on splicing and cell type","volume":"214","author":"van der Voort","year":"1995","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"2023072509270380800_R39","doi-asserted-by":"crossref","first-page":"6499","DOI":"10.1074\/jbc.274.10.6499","article-title":"Heparan sulfate-modified CD44 promotes hepatocyte growth factor\/scatter factor-induced signal transduction through the receptor tyrosine kinase c-Met","volume":"274","author":"van der Voort","year":"1999","journal-title":"J. Biol. Chem."},{"key":"2023072509270380800_R40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/eji.1830270102","article-title":"Germinal center B cells rescued from apoptosis by CD40 ligation or attachment to follicular dendritic cells, but not by engagement of surface immunoglobulin or adhesion receptors, become resistant to CD95-induced apoptosis","volume":"27","author":"Koopman","year":"1997","journal-title":"Eur. J. Immunol."},{"key":"2023072509270380800_R41","doi-asserted-by":"crossref","first-page":"23916","DOI":"10.1074\/jbc.274.34.23916","article-title":"Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine","volume":"274","author":"Amara","year":"1999","journal-title":"J. Biol. Chem."},{"key":"2023072509270380800_R42","doi-asserted-by":"crossref","first-page":"2378","DOI":"10.1002\/pro.5560031222","article-title":"Molecular evolution and domain structure of plasminogen-related growth factors (HGF\/SF and HGF1\/MSP)","volume":"3","author":"Donate","year":"1994","journal-title":"Protein Sci."},{"key":"2023072509270380800_R43","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1084\/jem.184.3.1101","article-title":"A highly efficacious lymphocyte chemoattractant, stromal cell\u2013derived factor 1 (SDF-1)","volume":"184","author":"Bleul","year":"1996","journal-title":"J. Exp. Med."},{"key":"2023072509270380800_R44","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1083\/jcb.128.4.673","article-title":"Proteoglycan forms of the lymphocyte homing receptor CD44 are alternatively spliced variants containing the v3 exon","volume":"128","author":"Jackson","year":"1995","journal-title":"J. Cell Biol."},{"key":"2023072509270380800_R45","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/384173a0","article-title":"Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis","volume":"384","author":"Weidner","year":"1996","journal-title":"Nature."},{"key":"2023072509270380800_R46","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1016\/0092-8674(94)90031-0","article-title":"Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis","volume":"79","author":"Aviezer","year":"1994","journal-title":"Cell."},{"key":"2023072509270380800_R47","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1038\/31741","article-title":"Structure of a heparin-linked biologically active dimer of fibroblast growth factor","volume":"393","author":"DiGabriele","year":"1998","journal-title":"Nature."},{"key":"2023072509270380800_R48","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1016\/0092-8674(94)90032-9","article-title":"Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation","volume":"79","author":"Spivak-Kroizman","year":"1994","journal-title":"Cell."},{"key":"2023072509270380800_R49","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/S0960-9822(98)70059-4","article-title":"Engineered mutants of HGF\/SF with reduced binding to heparan sulphate proteoglycans, decreased clearance and enhanced activity in vivo","volume":"8","author":"Hartmann","year":"1998","journal-title":"Curr. Biol."},{"key":"2023072509270380800_R50","doi-asserted-by":"crossref","first-page":"6003","DOI":"10.1021\/bi972468t","article-title":"Hepatocyte growth factor\/scatter factor has distinct classes of binding site in heparan sulfate from mammary cells","volume":"37","author":"Rahmoune","year":"1998","journal-title":"Biochemistry."},{"key":"2023072509270380800_R51","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1083\/jcb.142.5.1371","article-title":"ZAP-70 tyrosine kinase is required for LFA-1\u2013dependent T cell migration","volume":"142","author":"Soede","year":"1998","journal-title":"J. Cell Biol."},{"key":"2023072509270380800_R52","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1084\/jem.187.5.753","article-title":"B lymphocyte chemotaxis regulated in association with microanatomic localization, differentiation state, and B cell receptor engagement","volume":"187","author":"Bleul","year":"1998","journal-title":"J. Exp. Med."},{"key":"2023072509270380800_R53","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/S0065-230X(00)79002-6","article-title":"The hepatocyte growth factor-Met pathway in development, tumorigenesis, and B cell differentiation","volume":"79","author":"van der Voort","year":"2000","journal-title":"Adv. Cancer Res."},{"key":"2023072509270380800_R54","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1126\/science.1846706","article-title":"Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product","volume":"251","author":"Bottaro","year":"1991","journal-title":"Science."},{"key":"2023072509270380800_R55","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1016\/0092-8674(91)90363-4","article-title":"Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor","volume":"67","author":"Montesano","year":"1991","journal-title":"Cell."},{"key":"2023072509270380800_R56","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1038\/342440a0","article-title":"Molecular cloning and expression of human hepatocyte growth factor","volume":"342","author":"Nakamura","year":"1989","journal-title":"Nature."},{"key":"2023072509270380800_R57","first-page":"501","article-title":"Hepatocyte growth factor (HGF) stimulates the tyrosine kinase activity of the receptor encoded by the proto-oncogene c-MET","volume":"6","author":"Naldini","year":"1991","journal-title":"Oncogene."},{"key":"2023072509270380800_R58","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/327239a0","article-title":"Scatter factor is a fibroblast-derived modulator of epithelial cell mobility","volume":"327","author":"Stoker","year":"1987","journal-title":"Nature."},{"key":"2023072509270380800_R59","doi-asserted-by":"crossref","first-page":"768","DOI":"10.1038\/376768a0","article-title":"Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud","volume":"376","author":"Bladt","year":"1995","journal-title":"Nature."},{"key":"2023072509270380800_R60","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1038\/373699a0","article-title":"Scatter factor\/hepatocyte growth factor is essential for liver development","volume":"373","author":"Schmidt","year":"1995","journal-title":"Nature."},{"key":"2023072509270380800_R61","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1038\/373702a0","article-title":"Placental defect and embryonic lethality in mice lacking hepatocyte growth factor\/scatter factor","volume":"373","author":"Uehara","year":"1995","journal-title":"Nature."},{"key":"2023072509270380800_R62","doi-asserted-by":"crossref","first-page":"2097","DOI":"10.1083\/jcb.111.5.2097","article-title":"Scatter factormolecular characteristics and effect on the invasiveness of epithelial cells","volume":"111","author":"Weidner","year":"1990","journal-title":"J. Cell Biol."},{"key":"2023072509270380800_R63","doi-asserted-by":"crossref","first-page":"4731","DOI":"10.1073\/pnas.91.11.4731","article-title":"Invasiveness and metastasis of NIH 3T3 cells induced by Met-hepatocyte growth factor\/scatter factor autocrine stimulation","volume":"91","author":"Rong","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072509270380800_R64","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1073\/pnas.90.2.649","article-title":"Transfer of motogenic and invasive response to scatter factor\/hepatocyte growth factor by transfection of human MET protooncogene","volume":"90","author":"Giordano","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072509270380800_R65","doi-asserted-by":"crossref","first-page":"2305","DOI":"10.1073\/pnas.91.6.2305","article-title":"Molecular cloning and structure of a pre-B-cell growth-stimulating factor","volume":"91","author":"Nagasawa","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072509270380800_R66","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1038\/382635a0","article-title":"Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF\/SDF-1","volume":"382","author":"Nagasawa","year":"1996","journal-title":"Nature."},{"key":"2023072509270380800_R67","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1038\/31261","article-title":"The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract","volume":"393","author":"Tachibana","year":"1998","journal-title":"Nature."},{"key":"2023072509270380800_R68","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1038\/31269","article-title":"Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development","volume":"393","author":"Zou","year":"1998","journal-title":"Nature."},{"key":"2023072509270380800_R69","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1084\/jem.185.1.111","article-title":"The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood","volume":"185","author":"Aiuti","year":"1997","journal-title":"J. Exp. Med."},{"key":"2023072509270380800_R70","doi-asserted-by":"crossref","first-page":"1788","DOI":"10.1002\/eji.1830270729","article-title":"The chemokine SDF-1, stromal cell-derived factor 1, attracts early stage B cell precursors via the chemokine receptor CXCR4","volume":"27","author":"D'Apuzzo","year":"1997","journal-title":"Eur. J. Immunol."},{"key":"2023072509270380800_R71","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.1084\/jem.189.9.1461","article-title":"B cell antigen receptor engagement inhibits stromal cell\u2013derived factor (SDF)-1\u03b1 chemotaxis and promotes protein kinase C (PKC)-induced internalization of CXCR4","volume":"189","author":"Guinamard","year":"1999","journal-title":"J. Exp. 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