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The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1994 Oct;94(4):1585–1596. doi: 10.1172/JCI117500

B lymphocyte binding to E- and P-selectins is mediated through the de novo expression of carbohydrates on in vitro and in vivo activated human B cells.

A A Postigo 1, M Marazuela 1, F Sánchez-Madrid 1, M O de Landázuri 1
PMCID: PMC295318  PMID: 7523454

Abstract

Cell adhesion to endothelium regulates the trafficking and recruitment of leukocytes towards lymphoid organs and sites of inflammation. This phenomenon is mediated by the expression of a number of adhesion molecules on both the endothelium and circulating cells. Activation of endothelial cells (EC) with different stimuli induces the expression of several adhesion molecules (E- and P-selectins, ICAM-1, VCAM-1), involved in their interaction with circulating cells. In this report, we have studied the binding of nonactivated and activated B cells to purified E- and P-selectins. Activated but not resting B cells were able to interact with both selectins. This binding capacity of activated B cells paralleled the induction of different carbohydrate epitopes (Lewisx, sialyl-Lewisx, CD57 and CDw65) as well as other molecules bearing these or related epitopes in myeloid cells (L-selectin, alpha L beta 2 and alpha X beta 2 integrins, and CD35) involved in the interaction of different cell types with selectins. B cells infiltrating inflamed tissues like in Hashimoto's thyroiditis, also expressed these selectin-binding carbohydrates in parallel with the expression of E-selectin by surrounding follicular dendritic cells. Moreover, the crosslinking of these selectin-binding epitopes resulted in an increased binding of B cells to different integrin ligands. Thus, in addition to the involvement of integrins, E- and P-selectins could play an important role in the interaction of B lymphocytes with the endothelium during B cell extravasation into lymphoid tissues and inflammatory foci as well as in their organization into lymphoid organs.

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Selected References

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  1. 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]
  2. Bast B. J., Zhou L. J., Freeman G. J., Colley K. J., Ernst T. J., Munro J. M., Tedder T. F. The HB-6, CDw75, and CD76 differentiation antigens are unique cell-surface carbohydrate determinants generated by the beta-galactoside alpha 2,6-sialyltransferase. J Cell Biol. 1992 Jan;116(2):423–435. doi: 10.1083/jcb.116.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Berg E. L., Robinson M. K., Mansson O., Butcher E. C., Magnani J. L. A carbohydrate domain common to both sialyl Le(a) and sialyl Le(X) is recognized by the endothelial cell leukocyte adhesion molecule ELAM-1. J Biol Chem. 1991 Aug 15;266(23):14869–14872. [PubMed] [Google Scholar]
  5. Berg E. L., Yoshino T., Rott L. S., Robinson M. K., Warnock R. A., Kishimoto T. K., Picker L. J., Butcher E. C. The cutaneous lymphocyte antigen is a skin lymphocyte homing receptor for the vascular lectin endothelial cell-leukocyte adhesion molecule 1. J Exp Med. 1991 Dec 1;174(6):1461–1466. doi: 10.1084/jem.174.6.1461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bevilacqua M. P., Nelson R. M. Selectins. J Clin Invest. 1993 Feb;91(2):379–387. doi: 10.1172/JCI116210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butcher E. C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991 Dec 20;67(6):1033–1036. doi: 10.1016/0092-8674(91)90279-8. [DOI] [PubMed] [Google Scholar]
  8. Cotran R. S., Gimbrone M. A., Jr, Bevilacqua M. P., Mendrick D. L., Pober J. S. Induction and detection of a human endothelial activation antigen in vivo. J Exp Med. 1986 Aug 1;164(2):661–666. doi: 10.1084/jem.164.2.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Damle N. K., Klussman K., Dietsch M. T., Mohagheghpour N., Aruffo A. GMP-140 (P-selectin/CD62) binds to chronically stimulated but not resting CD4+ T lymphocytes and regulates their production of proinflammatory cytokines. Eur J Immunol. 1992 Jul;22(7):1789–1793. doi: 10.1002/eji.1830220718. [DOI] [PubMed] [Google Scholar]
  10. Forsyth K. D., Simpson A. C., Levinsky R. J. CD15 antibodies increase neutrophil adhesion to endothelium by an LFA-1-dependent mechanism. Eur J Immunol. 1989 Jul;19(7):1331–1334. doi: 10.1002/eji.1830190727. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Freedman A. S., Munro J. M., Rice G. E., Bevilacqua M. P., Morimoto C., McIntyre B. W., Rhynhart K., Pober J. S., Nadler L. M. Adhesion of human B cells to germinal centers in vitro involves VLA-4 and INCAM-110. Science. 1990 Aug 31;249(4972):1030–1033. doi: 10.1126/science.1697696. [DOI] [PubMed] [Google Scholar]
  13. Goelz S. E., Hession C., Goff D., Griffiths B., Tizard R., Newman B., Chi-Rosso G., Lobb R. ELFT: a gene that directs the expression of an ELAM-1 ligand. Cell. 1990 Dec 21;63(6):1349–1356. doi: 10.1016/0092-8674(90)90430-m. [DOI] [PubMed] [Google Scholar]
  14. Goelz S., Kumar R., Potvin B., Sundaram S., Brickelmaier M., Stanley P. Differential expression of an E-selectin ligand (SLex) by two Chinese hamster ovary cell lines transfected with the same alpha (1,3)-fucosyltransferase gene (ELFT). J Biol Chem. 1994 Jan 14;269(2):1033–1040. [PubMed] [Google Scholar]
  15. Graber N., Gopal T. V., Wilson D., Beall L. D., Polte T., Newman W. T cells bind to cytokine-activated endothelial cells via a novel, inducible sialoglycoprotein and endothelial leukocyte adhesion molecule-1. J Immunol. 1990 Aug 1;145(3):819–830. [PubMed] [Google Scholar]
  16. Handa K., Nudelman E. D., Stroud M. R., Shiozawa T., Hakomori S. Selectin GMP-140 (CD62; PADGEM) binds to sialosyl-Le(a) and sialosyl-Le(x), and sulfated glycans modulate this binding. Biochem Biophys Res Commun. 1991 Dec 31;181(3):1223–1230. doi: 10.1016/0006-291x(91)92069-v. [DOI] [PubMed] [Google Scholar]
  17. Hynes R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. doi: 10.1016/0092-8674(92)90115-s. [DOI] [PubMed] [Google Scholar]
  18. Kishimoto T. K., Warnock R. A., Jutila M. A., Butcher E. C., Lane C., Anderson D. C., Smith C. W. Antibodies against human neutrophil LECAM-1 (LAM-1/Leu-8/DREG-56 antigen) and endothelial cell ELAM-1 inhibit a common CD18-independent adhesion pathway in vitro. Blood. 1991 Aug 1;78(3):805–811. [PubMed] [Google Scholar]
  19. Klaus G. G., Humphrey J. H., Kunkl A., Dongworth D. W. The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol Rev. 1980;53:3–28. doi: 10.1111/j.1600-065x.1980.tb01038.x. [DOI] [PubMed] [Google Scholar]
  20. Koopman G., Parmentier H. K., Schuurman H. J., Newman W., Meijer C. J., Pals S. T. Adhesion of human B cells to follicular dendritic cells involves both the lymphocyte function-associated antigen 1/intercellular adhesion molecule 1 and very late antigen 4/vascular cell adhesion molecule 1 pathways. J Exp Med. 1991 Jun 1;173(6):1297–1304. doi: 10.1084/jem.173.6.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Koszdin K. L., Bowen B. R. The cloning and expression of a human alpha-1,3 fucosyltransferase capable of forming the E-selectin ligand. Biochem Biophys Res Commun. 1992 Aug 31;187(1):152–157. doi: 10.1016/s0006-291x(05)81472-x. [DOI] [PubMed] [Google Scholar]
  22. Kuijpers T. W., Hoogerwerf M., van der Laan L. J., Nagel G., van der Schoot C. E., Grunert F., Roos D. CD66 nonspecific cross-reacting antigens are involved in neutrophil adherence to cytokine-activated endothelial cells. J Cell Biol. 1992 Jul;118(2):457–466. doi: 10.1083/jcb.118.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kuijpers T. W. Terminal glycosyltransferase activity: a selective role in cell adhesion. Blood. 1993 Feb 15;81(4):873–882. [PubMed] [Google Scholar]
  24. 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]
  25. Kumar R., Potvin B., Muller W. A., Stanley P. Cloning of a human alpha(1,3)-fucosyltransferase gene that encodes ELFT but does not confer ELAM-1 recognition on Chinese hamster ovary cell transfectants. J Biol Chem. 1991 Nov 15;266(32):21777–21783. [PubMed] [Google Scholar]
  26. Larsen E., Palabrica T., Sajer S., Gilbert G. E., Wagner D. D., Furie B. C., Furie B. PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15). Cell. 1990 Nov 2;63(3):467–474. doi: 10.1016/0092-8674(90)90443-i. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Lo S. K., Lee S., Ramos R. A., Lobb R., Rosa M., Chi-Rosso G., Wright S. D. Endothelial-leukocyte adhesion molecule 1 stimulates the adhesive activity of leukocyte integrin CR3 (CD11b/CD18, Mac-1, alpha m beta 2) on human neutrophils. J Exp Med. 1991 Jun 1;173(6):1493–1500. doi: 10.1084/jem.173.6.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lorant D. E., Topham M. K., Whatley R. E., McEver R. P., McIntyre T. M., Prescott S. M., Zimmerman G. A. Inflammatory roles of P-selectin. J Clin Invest. 1993 Aug;92(2):559–570. doi: 10.1172/JCI116623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Lowe J. B., Stoolman L. M., Nair R. P., Larsen R. D., Berhend T. L., Marks R. M. ELAM-1--dependent cell adhesion to vascular endothelium determined by a transfected human fucosyltransferase cDNA. Cell. 1990 Nov 2;63(3):475–484. doi: 10.1016/0092-8674(90)90444-j. [DOI] [PubMed] [Google Scholar]
  32. Lund-Johansen F., Olweus J., Horejsi V., Skubitz K. M., Thompson J. S., Vilella R., Symington F. W. Activation of human phagocytes through carbohydrate antigens (CD15, sialyl-CD15, CDw17, and CDw65). J Immunol. 1992 May 15;148(10):3221–3229. [PubMed] [Google Scholar]
  33. McEver R. P. Leukocyte-endothelial cell interactions. Curr Opin Cell Biol. 1992 Oct;4(5):840–849. doi: 10.1016/0955-0674(92)90109-p. [DOI] [PubMed] [Google Scholar]
  34. Miyazaki A., Mirakian R., Bottazzo G. F. Adhesion molecule expression in Graves' thyroid glands; potential relevance of granule membrane protein (GMP-140) and intercellular adhesion molecule-1 (ICAM-1) in the homing and antigen presentation processes. Clin Exp Immunol. 1992 Jul;89(1):52–57. doi: 10.1111/j.1365-2249.1992.tb06876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mollicone R., Candelier J. J., Mennesson B., Couillin P., Venot A. P., Oriol R. Five specificity patterns of (1----3)-alpha-L-fucosyltransferase activity defined by use of synthetic oligosaccharide acceptors. Differential expression of the enzymes during human embryonic development and in adult tissues. Carbohydr Res. 1992 Apr 10;228(1):265–276. doi: 10.1016/s0008-6215(00)90564-0. [DOI] [PubMed] [Google Scholar]
  36. Moore K. L., Thompson L. F. P-selectin (CD62) binds to subpopulations of human memory T lymphocytes and natural killer cells. Biochem Biophys Res Commun. 1992 Jul 15;186(1):173–181. doi: 10.1016/s0006-291x(05)80790-9. [DOI] [PubMed] [Google Scholar]
  37. Moore K. L., Varki A., McEver R. P. GMP-140 binds to a glycoprotein receptor on human neutrophils: evidence for a lectin-like interaction. J Cell Biol. 1991 Feb;112(3):491–499. doi: 10.1083/jcb.112.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Munro J. M., Lo S. K., Corless C., Robertson M. J., Lee N. C., Barnhill R. L., Weinberg D. S., Bevilacqua M. P. Expression of sialyl-Lewis X, an E-selectin ligand, in inflammation, immune processes, and lymphoid tissues. Am J Pathol. 1992 Dec;141(6):1397–1408. [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Needham L. K., Schnaar R. L. The HNK-1 reactive sulfoglucuronyl glycolipids are ligands for L-selectin and P-selectin but not E-selectin. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1359–1363. doi: 10.1073/pnas.90.4.1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ohmori K., Yoneda T., Ishihara G., Shigeta K., Hirashima K., Kanai M., Itai S., Sasaoki T., Arii S., Arita H. Sialyl SSEA-1 antigen as a carbohydrate marker of human natural killer cells and immature lymphoid cells. Blood. 1989 Jul;74(1):255–261. [PubMed] [Google Scholar]
  42. Phillips M. L., Nudelman E., Gaeta F. C., Perez M., Singhal A. K., Hakomori S., Paulson J. C. ELAM-1 mediates cell adhesion by recognition of a carbohydrate ligand, sialyl-Lex. Science. 1990 Nov 23;250(4984):1130–1132. doi: 10.1126/science.1701274. [DOI] [PubMed] [Google Scholar]
  43. Picker L. J., Kishimoto T. K., Smith C. W., Warnock R. A., Butcher E. C. ELAM-1 is an adhesion molecule for skin-homing T cells. Nature. 1991 Feb 28;349(6312):796–799. doi: 10.1038/349796a0. [DOI] [PubMed] [Google Scholar]
  44. Picker L. J., Michie S. A., Rott L. S., Butcher E. C. A unique phenotype of skin-associated lymphocytes in humans. Preferential expression of the HECA-452 epitope by benign and malignant T cells at cutaneous sites. Am J Pathol. 1990 May;136(5):1053–1068. [PMC free article] [PubMed] [Google Scholar]
  45. Picker L. J., Treer J. R., Ferguson-Darnell B., Collins P. A., Bergstresser P. R., Terstappen L. W. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J Immunol. 1993 Feb 1;150(3):1122–1136. [PubMed] [Google Scholar]
  46. 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]
  47. Pinola M., Renkonen R., Majuri M. L., Tiisala S., Saksela E. Characterization of the E-selectin ligand on NK cells. J Immunol. 1994 Apr 1;152(7):3586–3594. [PubMed] [Google Scholar]
  48. Polley M. J., Phillips M. L., Wayner E., Nudelman E., Singhal A. K., Hakomori S., Paulson J. C. CD62 and endothelial cell-leukocyte adhesion molecule 1 (ELAM-1) recognize the same carbohydrate ligand, sialyl-Lewis x. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6224–6228. doi: 10.1073/pnas.88.14.6224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Postigo A. A., Corbí A. L., Sánchez-Madrid F., de Landázuri M. O. Regulated expression and function of CD11c/CD18 integrin on human B lymphocytes. Relation between attachment to fibrinogen and triggering of proliferation through CD11c/CD18. J Exp Med. 1991 Dec 1;174(6):1313–1322. doi: 10.1084/jem.174.6.1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Postigo A. A., Garcia-Vicuña R., Diaz-Gonzalez F., Arroyo A. G., De Landázuri M. O., Chi-Rosso G., Lobb R. R., Laffon A., Sánchez-Madrid F. Increased binding of synovial T lymphocytes from rheumatoid arthritis to endothelial-leukocyte adhesion molecule-1 (ELAM-1) and vascular cell adhesion molecule-1 (VCAM-1). J Clin Invest. 1992 May;89(5):1445–1452. doi: 10.1172/JCI115734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Postigo A. A., Pulido R., Campanero M. R., Acevedo A., García-Pardo A., Corbi A. L., Sanchez-Madrid F., De Landazuri M. O. Differential expression of VLA-4 integrin by resident and peripheral blood B lymphocytes. Acquisition of functionally active alpha 4 beta 1-fibronectin receptors upon B cell activation. Eur J Immunol. 1991 Oct;21(10):2437–2445. doi: 10.1002/eji.1830211021. [DOI] [PubMed] [Google Scholar]
  52. Postigo A. A., Sánchez-Mateos P., Lazarovits A. I., Sánchez-Madrid F., de Landázuri M. O. Alpha 4 beta 7 integrin mediates B cell binding to fibronectin and vascular cell adhesion molecule-1. Expression and function of alpha 4 integrins on human B lymphocytes. J Immunol. 1993 Sep 1;151(5):2471–2483. [PubMed] [Google Scholar]
  53. Rossiter H., van Reijsen F., Mudde G. C., Kalthoff F., Bruijnzeel-Koomen C. A., Picker L. J., Kupper T. S. Skin disease-related T cells bind to endothelial selectins: expression of cutaneous lymphocyte antigen (CLA) predicts E-selectin but not P-selectin binding. Eur J Immunol. 1994 Jan;24(1):205–210. doi: 10.1002/eji.1830240132. [DOI] [PubMed] [Google Scholar]
  54. Ruco L. P., Gearing A. J., Pigott R., Pomponi D., Burgio V. L., Cafolla A., Baiocchini A., Baroni C. D. Expression of ICAM-1, VCAM-1 and ELAM-1 in angiofollicular lymph node hyperplasia (Castleman's disease): evidence for dysplasia of follicular dendritic reticulum cells. Histopathology. 1991 Dec;19(6):523–528. doi: 10.1111/j.1365-2559.1991.tb01500.x. [DOI] [PubMed] [Google Scholar]
  55. Sasaki K., Kurata K., Funayama K., Nagata M., Watanabe E., Ohta S., Hanai N., Nishi T. Expression cloning of a novel alpha 1,3-fucosyltransferase that is involved in biosynthesis of the sialyl Lewis x carbohydrate determinants in leukocytes. J Biol Chem. 1994 May 20;269(20):14730–14737. [PubMed] [Google Scholar]
  56. Sgroi D., Varki A., Braesch-Andersen S., Stamenkovic I. CD22, a B cell-specific immunoglobulin superfamily member, is a sialic acid-binding lectin. J Biol Chem. 1993 Apr 5;268(10):7011–7018. [PubMed] [Google Scholar]
  57. Shimizu Y., Newman W., Tanaka Y., Shaw S. Lymphocyte interactions with endothelial cells. Immunol Today. 1992 Mar;13(3):106–112. doi: 10.1016/0167-5699(92)90151-V. [DOI] [PubMed] [Google Scholar]
  58. Shimizu Y., Shaw S., Graber N., Gopal T. V., Horgan K. J., Van Seventer G. A., Newman W. Activation-independent binding of human memory T cells to adhesion molecule ELAM-1. Nature. 1991 Feb 28;349(6312):799–802. doi: 10.1038/349799a0. [DOI] [PubMed] [Google Scholar]
  59. Skinner M. P., Lucas C. M., Burns G. F., Chesterman C. N., Berndt M. C. GMP-140 binding to neutrophils is inhibited by sulfated glycans. J Biol Chem. 1991 Mar 25;266(9):5371–5374. [PubMed] [Google Scholar]
  60. Skubitz K. M., Snook R. W., 2nd Monoclonal antibodies that recognize lacto-N-fucopentaose III (CD15) react with the adhesion-promoting glycoprotein family (LFA-1/HMac-1/gp 150,95) and CR1 on human neutrophils. J Immunol. 1987 Sep 1;139(5):1631–1639. [PubMed] [Google Scholar]
  61. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  62. Stevens S. K., Weissman I. L., Butcher E. C. Differences in the migration of B and T lymphocytes: organ-selective localization in vivo and the role of lymphocyte-endothelial cell recognition. J Immunol. 1982 Feb;128(2):844–851. [PubMed] [Google Scholar]
  63. Stone J. P., Wagner D. D. P-selectin mediates adhesion of platelets to neuroblastoma and small cell lung cancer. J Clin Invest. 1993 Aug;92(2):804–813. doi: 10.1172/JCI116654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Tiemeyer M., Swiedler S. J., Ishihara M., Moreland M., Schweingruber H., Hirtzer P., Brandley B. K. Carbohydrate ligands for endothelial-leukocyte adhesion molecule 1. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1138–1142. doi: 10.1073/pnas.88.4.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Tohma S., Ramberg J. E., Lipsky P. E. Expression and distribution of CD11a/CD18 and CD54 during human T cell-B cell interactions. J Leukoc Biol. 1992 Jul;52(1):97–103. doi: 10.1002/jlb.52.1.97. [DOI] [PubMed] [Google Scholar]
  66. Tyrrell D., James P., Rao N., Foxall C., Abbas S., Dasgupta F., Nashed M., Hasegawa A., Kiso M., Asa D. Structural requirements for the carbohydrate ligand of E-selectin. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10372–10376. doi: 10.1073/pnas.88.22.10372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Walcheck B., Watts G., Jutila M. A. Bovine gamma/delta T cells bind E-selectin via a novel glycoprotein receptor: first characterization of a lymphocyte/E-selectin interaction in an animal model. J Exp Med. 1993 Sep 1;178(3):853–863. doi: 10.1084/jem.178.3.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Walz G., Aruffo A., Kolanus W., Bevilacqua M., Seed B. Recognition by ELAM-1 of the sialyl-Lex determinant on myeloid and tumor cells. Science. 1990 Nov 23;250(4984):1132–1135. doi: 10.1126/science.1701275. [DOI] [PubMed] [Google Scholar]
  69. 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]
  70. 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]
  71. Wong C. S., Gamble J. R., Skinner M. P., Lucas C. M., Berndt M. C., Vadas M. A. Adhesion protein GMP140 inhibits superoxide anion release by human neutrophils. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2397–2401. doi: 10.1073/pnas.88.6.2397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zhou Q., Moore K. L., Smith D. F., Varki A., McEver R. P., Cummings R. D. The selectin GMP-140 binds to sialylated, fucosylated lactosaminoglycans on both myeloid and nonmyeloid cells. J Cell Biol. 1991 Oct;115(2):557–564. doi: 10.1083/jcb.115.2.557. [DOI] [PMC free article] [PubMed] [Google Scholar]

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