Abstract
Interaction of leukocytes in flow with adherent leukocytes may contribute to their accumulation at sites of inflammation. Using L- selectin immobilized in a flow chamber, a model system that mimics presentation of L-selectin by adherent leukocytes, we characterize ligands for L-selectin on leukocytes and show that they mediate tethering and rolling in shear flow. We demonstrate the presence of L- selectin ligands on granulocytes, monocytes, and myeloid and lymphoid cell lines, and not on peripheral blood T lymphocytes. These ligands are calcium dependent, sensitive to protease and neuraminidase, and structurally distinct from previously described ligands for L-selectin on high endothelial venules (HEV). Differential sensitivity to O-sialo- glycoprotease provides evidence for ligand activity on both mucin-like and nonmucin-like structures. Transfection with fucosyltransferase induces expression of functional L-selectin ligands on both a lymphoid cell line and a nonhematopoietic cell line. L-selectin presented on adherent cells is also capable of supporting tethering and rolling interactions in physiologic shear flow. L-selectin ligands on leukocytes may be important in promoting leukocyte-leukocyte and subsequent leukocyte endothelial interactions in vivo, thereby enhancing leukocyte localization at sites of inflammation.
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- Alon R., Fuhlbrigge R. C., Finger E. B., Springer T. A. Interactions through L-selectin between leukocytes and adherent leukocytes nucleate rolling adhesions on selectins and VCAM-1 in shear flow. J Cell Biol. 1996 Nov;135(3):849–865. doi: 10.1083/jcb.135.3.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aruffo A., Kolanus W., Walz G., Fredman P., Seed B. CD62/P-selectin recognition of myeloid and tumor cell sulfatides. Cell. 1991 Oct 4;67(1):35–44. doi: 10.1016/0092-8674(91)90570-o. [DOI] [PubMed] [Google Scholar]
- Aruffo A., Seed B. Molecular cloning of a CD28 cDNA by a high-efficiency COS cell expression system. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8573–8577. doi: 10.1073/pnas.84.23.8573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bargatze R. F., Kurk S., Butcher E. C., Jutila M. A. Neutrophils roll on adherent neutrophils bound to cytokine-induced endothelial cells via L-selectin on the rolling cells. J Exp Med. 1994 Nov 1;180(5):1785–1792. doi: 10.1084/jem.180.5.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baumheter S., Singer M. S., Henzel W., Hemmerich S., Renz M., Rosen S. D., Lasky L. A. Binding of L-selectin to the vascular sialomucin CD34. Science. 1993 Oct 15;262(5132):436–438. doi: 10.1126/science.7692600. [DOI] [PubMed] [Google Scholar]
- Bennett T. A., Schammel C. M., Lynam E. B., Guyer D. A., Mellors A., Edwards B., Rogelj S., Sklar L. A. Evidence for a third component in neutrophil aggregation: potential roles of O-linked glycoproteins as L-selectin counter-structures. J Leukoc Biol. 1995 Nov;58(5):510–518. doi: 10.1002/jlb.58.5.510. [DOI] [PubMed] [Google Scholar]
- Berg E. L., Magnani J., Warnock R. A., Robinson M. K., Butcher E. C. Comparison of L-selectin and E-selectin ligand specificities: the L-selectin can bind the E-selectin ligands sialyl Le(x) and sialyl Le(a). Biochem Biophys Res Commun. 1992 Apr 30;184(2):1048–1055. doi: 10.1016/0006-291x(92)90697-j. [DOI] [PubMed] [Google Scholar]
- Bøyum A. Isolation of human blood monocytes with Nycodenz, a new non-ionic iodinated gradient medium. Scand J Immunol. 1983 May;17(5):429–436. doi: 10.1111/j.1365-3083.1983.tb00809.x. [DOI] [PubMed] [Google Scholar]
- Carlos T., Kovach N., Schwartz B., Rosa M., Newman B., Wayner E., Benjamin C., Osborn L., Lobb R., Harlan J. Human monocytes bind to two cytokine-induced adhesive ligands on cultured human endothelial cells: endothelial-leukocyte adhesion molecule-1 and vascular cell adhesion molecule-1. Blood. 1991 May 15;77(10):2266–2271. [PubMed] [Google Scholar]
- Carr M. W., Roth S. J., Luther E., Rose S. S., Springer T. A. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3652–3656. doi: 10.1073/pnas.91.9.3652. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crommie D., Rosen S. D. Biosynthesis of GlyCAM-1, a mucin-like ligand for L-selectin. J Biol Chem. 1995 Sep 22;270(38):22614–22624. doi: 10.1074/jbc.270.38.22614. [DOI] [PubMed] [Google Scholar]
- Diacovo T. G., Roth S. J., Morita C. T., Rosat J. P., Brenner M. B., Springer T. A. Interactions of human alpha/beta and gamma/delta T lymphocyte subsets in shear flow with E-selectin and P-selectin. J Exp Med. 1996 Mar 1;183(3):1193–1203. doi: 10.1084/jem.183.3.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- English D., Andersen B. R. Single-step separation of red blood cells. Granulocytes and mononuclear leukocytes on discontinuous density gradients of Ficoll-Hypaque. J Immunol Methods. 1974 Aug;5(3):249–252. doi: 10.1016/0022-1759(74)90109-4. [DOI] [PubMed] [Google Scholar]
- Fina L., Molgaard H. V., Robertson D., Bradley N. J., Monaghan P., Delia D., Sutherland D. R., Baker M. A., Greaves M. F. Expression of the CD34 gene in vascular endothelial cells. Blood. 1990 Jun 15;75(12):2417–2426. [PubMed] [Google Scholar]
- Foxall C., Watson S. R., Dowbenko D., Fennie C., Lasky L. A., Kiso M., Hasegawa A., Asa D., Brandley B. K. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J Cell Biol. 1992 May;117(4):895–902. doi: 10.1083/jcb.117.4.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fukushima K., Hirota M., Terasaki P. I., Wakisaka A., Togashi H., Chia D., Suyama N., Fukushi Y., Nudelman E., Hakomori S. Characterization of sialosylated Lewisx as a new tumor-associated antigen. Cancer Res. 1984 Nov;44(11):5279–5285. [PubMed] [Google Scholar]
- Gallatin W. M., Weissman I. L., Butcher E. C. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature. 1983 Jul 7;304(5921):30–34. doi: 10.1038/304030a0. [DOI] [PubMed] [Google Scholar]
- Girard J. P., Springer T. A. Cloning from purified high endothelial venule cells of hevin, a close relative of the antiadhesive extracellular matrix protein SPARC. Immunity. 1995 Jan;2(1):113–123. doi: 10.1016/1074-7613(95)90083-7. [DOI] [PubMed] [Google Scholar]
- Hansel T. T., De Vries I. J., Iff T., Rihs S., Wandzilak M., Betz S., Blaser K., Walker C. An improved immunomagnetic procedure for the isolation of highly purified human blood eosinophils. J Immunol Methods. 1991 Dec 15;145(1-2):105–110. doi: 10.1016/0022-1759(91)90315-7. [DOI] [PubMed] [Google Scholar]
- Hemmerich S., Bertozzi C. R., Leffler H., Rosen S. D. Identification of the sulfated monosaccharides of GlyCAM-1, an endothelial-derived ligand for L-selectin. Biochemistry. 1994 Apr 26;33(16):4820–4829. doi: 10.1021/bi00182a010. [DOI] [PubMed] [Google Scholar]
- Hemmerich S., Butcher E. C., Rosen S. D. Sulfation-dependent recognition of high endothelial venules (HEV)-ligands by L-selectin and MECA 79, and adhesion-blocking monoclonal antibody. J Exp Med. 1994 Dec 1;180(6):2219–2226. doi: 10.1084/jem.180.6.2219. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huber A. R., Kunkel S. L., Todd R. F., 3rd, Weiss S. J. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science. 1991 Oct 4;254(5028):99–102. doi: 10.1126/science.1718038. [DOI] [PubMed] [Google Scholar]
- Imai Y., Lasky L. A., Rosen S. D. Sulphation requirement for GlyCAM-1, an endothelial ligand for L-selectin. Nature. 1993 Feb 11;361(6412):555–557. doi: 10.1038/361555a0. [DOI] [PubMed] [Google Scholar]
- Jutila M. A., Kurk S. Analysis of bovine gamma delta T cell interactions with E-, P-, and L-selectin. Characterization of lymphocyte on lymphocyte rolling and the effects of O-glycoprotease. J Immunol. 1996 Jan 1;156(1):289–296. [PubMed] [Google Scholar]
- Kishimoto T. K., Jutila M. A., Butcher E. C. Identification of a human peripheral lymph node homing receptor: a rapidly down-regulated adhesion molecule. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2244–2248. doi: 10.1073/pnas.87.6.2244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knibbs R. N., Craig R. A., Natsuka S., Chang A., Cameron M., Lowe J. B., Stoolman L. M. The fucosyltransferase FucT-VII regulates E-selectin ligand synthesis in human T cells. J Cell Biol. 1996 May;133(4):911–920. doi: 10.1083/jcb.133.4.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kukowska-Latallo J. F., Larsen R. D., Nair R. P., Lowe J. B. A cloned human cDNA determines expression of a mouse stage-specific embryonic antigen and the Lewis blood group alpha(1,3/1,4)fucosyltransferase. Genes Dev. 1990 Aug;4(8):1288–1303. doi: 10.1101/gad.4.8.1288. [DOI] [PubMed] [Google Scholar]
- Lasky L. A., Singer M. S., Dowbenko D., Imai Y., Henzel W. J., Grimley C., Fennie C., Gillett N., Watson S. R., Rosen S. D. An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell. 1992 Jun 12;69(6):927–938. doi: 10.1016/0092-8674(92)90612-g. [DOI] [PubMed] [Google Scholar]
- Lawrence M. B., Bainton D. F., Springer T. A. Neutrophil tethering to and rolling on E-selectin are separable by requirement for L-selectin. Immunity. 1994 May;1(2):137–145. doi: 10.1016/1074-7613(94)90107-4. [DOI] [PubMed] [Google Scholar]
- Lawrence M. B., Springer T. A. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell. 1991 May 31;65(5):859–873. doi: 10.1016/0092-8674(91)90393-d. [DOI] [PubMed] [Google Scholar]
- Lawrence M. B., Springer T. A. Neutrophils roll on E-selectin. J Immunol. 1993 Dec 1;151(11):6338–6346. [PubMed] [Google Scholar]
- Ley K., Gaehtgens P., Fennie C., Singer M. S., Lasky L. A., Rosen S. D. Lectin-like cell adhesion molecule 1 mediates leukocyte rolling in mesenteric venules in vivo. Blood. 1991 Jun 15;77(12):2553–2555. [PubMed] [Google Scholar]
- Lorant D. E., McEver R. P., McIntyre T. M., Moore K. L., Prescott S. M., Zimmerman G. A. Activation of polymorphonuclear leukocytes reduces their adhesion to P-selectin and causes redistribution of ligands for P-selectin on their surfaces. J Clin Invest. 1995 Jul;96(1):171–182. doi: 10.1172/JCI118018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowe J. B., Kukowska-Latallo J. F., Nair R. P., Larsen R. D., Marks R. M., Macher B. A., Kelly R. J., Ernst L. K. Molecular cloning of a human fucosyltransferase gene that determines expression of the Lewis x and VIM-2 epitopes but not ELAM-1-dependent cell adhesion. J Biol Chem. 1991 Sep 15;266(26):17467–17477. [PubMed] [Google Scholar]
- McEver R. P. Selectins. Curr Opin Immunol. 1994 Feb;6(1):75–84. doi: 10.1016/0952-7915(94)90037-x. [DOI] [PubMed] [Google Scholar]
- Miller L. J., Bainton D. F., Borregaard N., Springer T. A. Stimulated mobilization of monocyte Mac-1 and p150,95 adhesion proteins from an intracellular vesicular compartment to the cell surface. J Clin Invest. 1987 Aug;80(2):535–544. doi: 10.1172/JCI113102. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moore K. L., Patel K. D., Bruehl R. E., Li F., Johnson D. A., Lichenstein H. S., Cummings R. D., Bainton D. F., McEver R. P. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol. 1995 Feb;128(4):661–671. doi: 10.1083/jcb.128.4.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Natsuka S., Gersten K. M., Zenita K., Kannagi R., Lowe J. B. Molecular cloning of a cDNA encoding a novel human leukocyte alpha-1,3-fucosyltransferase capable of synthesizing the sialyl Lewis x determinant. J Biol Chem. 1994 Jun 17;269(24):16789–16794. [PubMed] [Google Scholar]
- Nelson R. M., Cecconi O., Roberts W. G., Aruffo A., Linhardt R. J., Bevilacqua M. P. Heparin oligosaccharides bind L- and P-selectin and inhibit acute inflammation. Blood. 1993 Dec 1;82(11):3253–3258. [PubMed] [Google Scholar]
- Norgard-Sumnicht K. E., Varki N. M., Varki A. Calcium-dependent heparin-like ligands for L-selectin in nonlymphoid endothelial cells. Science. 1993 Jul 23;261(5120):480–483. doi: 10.1126/science.7687382. [DOI] [PubMed] [Google Scholar]
- Oxley S. M., Sackstein R. Detection of an L-selectin ligand on a hematopoietic progenitor cell line. Blood. 1994 Nov 15;84(10):3299–3306. [PubMed] [Google Scholar]
- Picker L. J., Warnock R. A., Burns A. R., Doerschuk C. M., Berg E. L., Butcher E. C. The neutrophil selectin LECAM-1 presents carbohydrate ligands to the vascular selectins ELAM-1 and GMP-140. Cell. 1991 Sep 6;66(5):921–933. doi: 10.1016/0092-8674(91)90438-5. [DOI] [PubMed] [Google Scholar]
- Pouyani T., Seed B. PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell. 1995 Oct 20;83(2):333–343. doi: 10.1016/0092-8674(95)90174-4. [DOI] [PubMed] [Google Scholar]
- Puri K. D., Finger E. B., Gaudernack G., Springer T. A. Sialomucin CD34 is the major L-selectin ligand in human tonsil high endothelial venules. J Cell Biol. 1995 Oct;131(1):261–270. doi: 10.1083/jcb.131.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosen S. D., Bertozzi C. R. The selectins and their ligands. Curr Opin Cell Biol. 1994 Oct;6(5):663–673. doi: 10.1016/0955-0674(94)90092-2. [DOI] [PubMed] [Google Scholar]
- Sako D., Comess K. M., Barone K. M., Camphausen R. T., Cumming D. A., Shaw G. D. A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell. 1995 Oct 20;83(2):323–331. doi: 10.1016/0092-8674(95)90173-6. [DOI] [PubMed] [Google Scholar]
- Simon S. I., Rochon Y. P., Lynam E. B., Smith C. W., Anderson D. C., Sklar L. A. Beta 2-integrin and L-selectin are obligatory receptors in neutrophil aggregation. Blood. 1993 Aug 15;82(4):1097–1106. [PubMed] [Google Scholar]
- Smith C. W., Kishimoto T. K., Abbassi O., Hughes B., Rothlein R., McIntire L. V., Butcher E., Anderson D. C., Abbass O. Chemotactic factors regulate lectin adhesion molecule 1 (LECAM-1)-dependent neutrophil adhesion to cytokine-stimulated endothelial cells in vitro. J Clin Invest. 1991 Feb;87(2):609–618. doi: 10.1172/JCI115037. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spertini O., Luscinskas F. W., Gimbrone M. A., Jr, Tedder T. F. Monocyte attachment to activated human vascular endothelium in vitro is mediated by leukocyte adhesion molecule-1 (L-selectin) under nonstatic conditions. J Exp Med. 1992 Jun 1;175(6):1789–1792. doi: 10.1084/jem.175.6.1789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spertini O., Luscinskas F. W., Kansas G. S., Munro J. M., Griffin J. D., Gimbrone M. A., Jr, Tedder T. F. Leukocyte adhesion molecule-1 (LAM-1, L-selectin) interacts with an inducible endothelial cell ligand to support leukocyte adhesion. J Immunol. 1991 Oct 15;147(8):2565–2573. [PubMed] [Google Scholar]
- Springer T. A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994 Jan 28;76(2):301–314. doi: 10.1016/0092-8674(94)90337-9. [DOI] [PubMed] [Google Scholar]
- Steininger C. N., Eddy C. A., Leimgruber R. M., Mellors A., Welply J. K. The glycoprotease of Pasteurella haemolytica A1 eliminates binding of myeloid cells to P-selectin but not to E-selectin. Biochem Biophys Res Commun. 1992 Oct 30;188(2):760–766. doi: 10.1016/0006-291x(92)91121-6. [DOI] [PubMed] [Google Scholar]
- Streeter P. R., Berg E. L., Rouse B. T., Bargatze R. F., Butcher E. C. A tissue-specific endothelial cell molecule involved in lymphocyte homing. Nature. 1988 Jan 7;331(6151):41–46. doi: 10.1038/331041a0. [DOI] [PubMed] [Google Scholar]
- Streeter P. R., Rouse B. T., Butcher E. C. Immunohistologic and functional characterization of a vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J Cell Biol. 1988 Nov;107(5):1853–1862. doi: 10.1083/jcb.107.5.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutherland D. R., Marsh J. C., Davidson J., Baker M. A., Keating A., Mellors A. Differential sensitivity of CD34 epitopes to cleavage by Pasteurella haemolytica glycoprotease: implications for purification of CD34-positive progenitor cells. Exp Hematol. 1992 Jun;20(5):590–599. [PubMed] [Google Scholar]
- Varki A. Selectin ligands. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7390–7397. doi: 10.1073/pnas.91.16.7390. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watson S. R., Imai Y., Fennie C., Geoffroy J. S., Rosen S. D., Lasky L. A. A homing receptor-IgG chimera as a probe for adhesive ligands of lymph node high endothelial venules. J Cell Biol. 1990 Jun;110(6):2221–2229. doi: 10.1083/jcb.110.6.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weston B. W., Nair R. P., Larsen R. D., Lowe J. B. Isolation of a novel human alpha (1,3)fucosyltransferase gene and molecular comparison to the human Lewis blood group alpha (1,3/1,4)fucosyltransferase gene. Syntenic, homologous, nonallelic genes encoding enzymes with distinct acceptor substrate specificities. J Biol Chem. 1992 Feb 25;267(6):4152–4160. [PubMed] [Google Scholar]
- Weston B. W., Smith P. L., Kelly R. J., Lowe J. B. Molecular cloning of a fourth member of a human alpha (1,3)fucosyltransferase gene family. Multiple homologous sequences that determine expression of the Lewis x, sialyl Lewis x, and difucosyl sialyl Lewis x epitopes. J Biol Chem. 1992 Dec 5;267(34):24575–24584. [PubMed] [Google Scholar]
- Yuen C. T., Lawson A. M., Chai W., Larkin M., Stoll M. S., Stuart A. C., Sullivan F. X., Ahern T. J., Feizi T. 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. 1992 Sep 29;31(38):9126–9131. doi: 10.1021/bi00153a003. [DOI] [PubMed] [Google Scholar]
- von Andrian U. H., Chambers J. D., Berg E. L., Michie S. A., Brown D. A., Karolak D., Ramezani L., Berger E. M., Arfors K. E., Butcher E. C. L-selectin mediates neutrophil rolling in inflamed venules through sialyl LewisX-dependent and -independent recognition pathways. Blood. 1993 Jul 1;82(1):182–191. [PubMed] [Google Scholar]
- von Andrian U. H., Chambers J. D., McEvoy L. M., Bargatze R. F., Arfors K. E., Butcher E. C. Two-step model of leukocyte-endothelial cell interaction in inflammation: distinct roles for LECAM-1 and the leukocyte beta 2 integrins in vivo. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7538–7542. doi: 10.1073/pnas.88.17.7538. [DOI] [PMC free article] [PubMed] [Google Scholar]
