Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1991 Feb 1;112(3):491–499. doi: 10.1083/jcb.112.3.491

GMP-140 binds to a glycoprotein receptor on human neutrophils: evidence for a lectin-like interaction

PMCID: PMC2288839  PMID: 1704009

Abstract

GMP-140 is a rapidly inducible receptor for neutrophils and monocytes expressed on activated platelets and endothelial cells. It is a member of the selectin family of lectin-like cell surface molecules that mediate leukocyte adhesion. We used a radioligand binding assay to characterize the interaction of purified GMP-140 with human neutrophils. Unstimulated neutrophils rapidly bound [125I]GMP-140 at 4 degrees C, reaching equilibrium in 10-15 min. Binding was Ca2+ dependent, reversible, and saturable at 3-6 nM free GMP-140 with half- maximal binding at approximately 1.5 nM. Receptor density and apparent affinity were not altered when neutrophils were stimulated with 4 beta- phorbol 12-myristate 13-acetate. Treatment of neutrophils with proteases abolished specific binding of [125I]GMP-140. Binding was also diminished when neutrophils were treated with neuraminidase from Vibrio cholerae, which cleaves alpha 2-3-, alpha 2-6-, and alpha 2-8-linked sialic acids, or from Newcastle disease virus, which cleaves only alpha 2-3- and alpha 2-8-linked sialic acids. Binding was not inhibited by an mAb to the abundant myeloid oligosaccharide, Lex (CD15), or by the neoglycoproteins Lex-BSA and sialyl-Lex-BSA. We conclude that neutrophils constitutively express a glycoprotein receptor for GMP-140, which contains sialic acid residues that are essential for function. These findings support the concept that GMP-140 interacts with leukocytes by a lectin-like mechanism.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amrein P. C., Stossel T. P. Prevention of degradation of human polymorphonuclear leukocyte proteins by diisopropylfluorophosphate. Blood. 1980 Sep;56(3):442–447. [PubMed] [Google Scholar]
  2. Anderson D. C., Miller L. J., Schmalstieg F. C., Rothlein R., Springer T. A. Contributions of the Mac-1 glycoprotein family to adherence-dependent granulocyte functions: structure-function assessments employing subunit-specific monoclonal antibodies. J Immunol. 1986 Jul 1;137(1):15–27. [PubMed] [Google Scholar]
  3. Berman C. L., Yeo E. L., Wencel-Drake J. D., Furie B. C., Ginsberg M. H., Furie B. A platelet alpha granule membrane protein that is associated with the plasma membrane after activation. Characterization and subcellular localization of platelet activation-dependent granule-external membrane protein. J Clin Invest. 1986 Jul;78(1):130–137. doi: 10.1172/JCI112542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bevilacqua M. P., Pober J. S., Mendrick D. L., Cotran R. S., Gimbrone M. A., Jr Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A. 1987 Dec;84(24):9238–9242. doi: 10.1073/pnas.84.24.9238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bowen B. R., Nguyen T., Lasky L. A. Characterization of a human homologue of the murine peripheral lymph node homing receptor. J Cell Biol. 1989 Jul;109(1):421–427. doi: 10.1083/jcb.109.1.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Camerini D., James S. P., Stamenkovic I., Seed B. Leu-8/TQ1 is the human equivalent of the Mel-14 lymph node homing receptor. Nature. 1989 Nov 2;342(6245):78–82. doi: 10.1038/342078a0. [DOI] [PubMed] [Google Scholar]
  7. Cornil I., Kerbel R. S., Dennis J. W. Tumor cell surface beta 1-4-linked galactose binds to lectin(s) on microvascular endothelial cells and contributes to organ colonization. J Cell Biol. 1990 Aug;111(2):773–781. doi: 10.1083/jcb.111.2.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drickamer K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem. 1988 Jul 15;263(20):9557–9560. [PubMed] [Google Scholar]
  9. Fukuda M. N., Dell A., Oates J. E., Wu P., Klock J. C., Fukuda M. Structures of glycosphingolipids isolated from human granulocytes. The presence of a series of linear poly-N-acetyllactosaminylceramide and its significance in glycolipids of whole blood cells. J Biol Chem. 1985 Jan 25;260(2):1067–1082. [PubMed] [Google Scholar]
  10. Fukuda M. Cell surface glycoconjugates as onco-differentiation markers in hematopoietic cells. Biochim Biophys Acta. 1985;780(2):119–150. doi: 10.1016/0304-419x(84)90002-7. [DOI] [PubMed] [Google Scholar]
  11. Fukuda M., Spooncer E., Oates J. E., Dell A., Klock J. C. Structure of sialylated fucosyl lactosaminoglycan isolated from human granulocytes. J Biol Chem. 1984 Sep 10;259(17):10925–10935. [PubMed] [Google Scholar]
  12. Geng J. G., Bevilacqua M. P., Moore K. L., McIntyre T. M., Prescott S. M., Kim J. M., Bliss G. A., Zimmerman G. A., McEver R. P. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature. 1990 Feb 22;343(6260):757–760. doi: 10.1038/343757a0. [DOI] [PubMed] [Google Scholar]
  13. Hamburger S. A., McEver R. P. GMP-140 mediates adhesion of stimulated platelets to neutrophils. Blood. 1990 Feb 1;75(3):550–554. [PubMed] [Google Scholar]
  14. Harlan J. M. Leukocyte-endothelial interactions. Blood. 1985 Mar;65(3):513–525. [PubMed] [Google Scholar]
  15. Hattori R., Hamilton K. K., Fugate R. D., McEver R. P., Sims P. J. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140. J Biol Chem. 1989 May 15;264(14):7768–7771. [PubMed] [Google Scholar]
  16. Hession C., Osborn L., Goff D., Chi-Rosso G., Vassallo C., Pasek M., Pittack C., Tizard R., Goelz S., McCarthy K. Endothelial leukocyte adhesion molecule 1: direct expression cloning and functional interactions. Proc Natl Acad Sci U S A. 1990 Mar;87(5):1673–1677. doi: 10.1073/pnas.87.5.1673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huang L. C., Civin C. I., Magnani J. L., Shaper J. H., Ginsburg V. My-1, the human myeloid-specific antigen detected by mouse monoclonal antibodies, is a sugar sequence found in lacto-N-fucopentaose III. Blood. 1983 May;61(5):1020–1023. [PubMed] [Google Scholar]
  18. Janowska-Wieczorek A., Mannoni P., Turner A. R., McGann L. E., Shaw A. R., Turc J. M. Monoclonal antibody specific for granulocytic-lineage cells and reactive with human pluripotent and committed haematopoietic progenitor cells. Br J Haematol. 1984 Sep;58(1):159–168. doi: 10.1111/j.1365-2141.1984.tb06070.x. [DOI] [PubMed] [Google Scholar]
  19. Johnston G. I., Cook R. G., McEver R. P. Cloning of GMP-140, a granule membrane protein of platelets and endothelium: sequence similarity to proteins involved in cell adhesion and inflammation. Cell. 1989 Mar 24;56(6):1033–1044. doi: 10.1016/0092-8674(89)90636-3. [DOI] [PubMed] [Google Scholar]
  20. Jung T. M., Dailey M. O. Rapid modulation of homing receptors (gp90MEL-14) induced by activators of protein kinase C. Receptor shedding due to accelerated proteolytic cleavage at the cell surface. J Immunol. 1990 Apr 15;144(8):3130–3136. [PubMed] [Google Scholar]
  21. Jutila M. A., Rott L., Berg E. L., Butcher E. C. Function and regulation of the neutrophil MEL-14 antigen in vivo: comparison with LFA-1 and MAC-1. J Immunol. 1989 Nov 15;143(10):3318–3324. [PubMed] [Google Scholar]
  22. Kansas G. S., Wood G. S., Fishwild D. M., Engleman E. G. Functional characterization of human T lymphocyte subsets distinguished by monoclonal anti-leu-8. J Immunol. 1985 May;134(5):2995–3002. [PubMed] [Google Scholar]
  23. Kishimoto T. K., Jutila M. A., Berg E. L., Butcher E. C. Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science. 1989 Sep 15;245(4923):1238–1241. doi: 10.1126/science.2551036. [DOI] [PubMed] [Google Scholar]
  24. Kishimoto T. K., Larson R. S., Corbi A. L., Dustin M. L., Staunton D. E., Springer T. A. The leukocyte integrins. Adv Immunol. 1989;46:149–182. doi: 10.1016/s0065-2776(08)60653-7. [DOI] [PubMed] [Google Scholar]
  25. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  26. Larsen E., Celi A., Gilbert G. E., Furie B. C., Erban J. K., Bonfanti R., Wagner D. D., Furie B. PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell. 1989 Oct 20;59(2):305–312. doi: 10.1016/0092-8674(89)90292-4. [DOI] [PubMed] [Google Scholar]
  27. Lasky L. A., Singer M. S., Yednock T. A., Dowbenko D., Fennie C., Rodriguez H., Nguyen T., Stachel S., Rosen S. D. Cloning of a lymphocyte homing receptor reveals a lectin domain. Cell. 1989 Mar 24;56(6):1045–1055. doi: 10.1016/0092-8674(89)90637-5. [DOI] [PubMed] [Google Scholar]
  28. Lemieux R. U., Bundle D. R., Baker D. A. The properties of a "synthetic" antigen related to the human blood-group Lewis a. J Am Chem Soc. 1975 Jul 9;97(14):4076–4083. doi: 10.1021/ja00847a035. [DOI] [PubMed] [Google Scholar]
  29. Manzi A. E., Dell A., Azadi P., Varki A. Studies of naturally occurring modifications of sialic acids by fast-atom bombardment-mass spectrometry. Analysis of positional isomers by periodate cleavage. J Biol Chem. 1990 May 15;265(14):8094–8107. [PubMed] [Google Scholar]
  30. Marlin S. D., Springer T. A. Purified intercellular adhesion molecule-1 (ICAM-1) is a ligand for lymphocyte function-associated antigen 1 (LFA-1). Cell. 1987 Dec 4;51(5):813–819. doi: 10.1016/0092-8674(87)90104-8. [DOI] [PubMed] [Google Scholar]
  31. McEver R. P., Beckstead J. H., Moore K. L., Marshall-Carlson L., Bainton D. F. GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest. 1989 Jul;84(1):92–99. doi: 10.1172/JCI114175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. McEver R. P., Martin M. N. A monoclonal antibody to a membrane glycoprotein binds only to activated platelets. J Biol Chem. 1984 Aug 10;259(15):9799–9804. [PubMed] [Google Scholar]
  33. Meindl P., Bodo G., Lindner J., Palese P. Einfluss von 2-Desoxy-2,3-dehydro-N-acetylneuraminsäure auf Myxovirus-Neuraminidasen und die Replikation von Influenza- und Newcastle Disease Virus. Z Naturforsch B. 1971 Aug;26(8):792–797. doi: 10.1515/znb-1971-0812. [DOI] [PubMed] [Google Scholar]
  34. Meindl P., Tuppy H. Uber 2-Desoxy-2.3-dehydro-sialinsäuren, II. Kompetitive Hemmung der Vibrio-cholerae-Neuraminidase durch 2-Desoxy-2.3-dehyro-N-acyl-neuraminsäuren. Hoppe Seylers Z Physiol Chem. 1969 Sep;350(9):1088–1092. [PubMed] [Google Scholar]
  35. Palcic M. M., Venot A. P., Ratcliffe R. M., Hindsgaul O. Enzymic synthesis of oligosaccharides terminating in the tumor-associated sialyl-Lewis-a determinant. Carbohydr Res. 1989 Jul 1;190(1):1–11. doi: 10.1016/0008-6215(89)84141-2. [DOI] [PubMed] [Google Scholar]
  36. Paulson J. C., Sadler J. E., Hill R. L. Restoration of specific myxovirus receptors to asialoerythrocytes by incorporation of sialic acid with pure sialyltransferases. J Biol Chem. 1979 Mar 25;254(6):2120–2124. [PubMed] [Google Scholar]
  37. Paulson J. C., Weinstein J., Dorland L., van Halbeek H., Vliegenthart J. F. Newcastle disease virus contains a linkage-specific glycoprotein sialidase. Application to the localization of sialic acid residues in N-linked oligosaccharides of alpha 1-acid glycoprotein. J Biol Chem. 1982 Nov 10;257(21):12734–12738. [PubMed] [Google Scholar]
  38. Philips M. R., Buyon J. P., Winchester R., Weissmann G., Abramson S. B. Up-regulation of the iC3b receptor (CR3) is neither necessary nor sufficient to promote neutrophil aggregation. J Clin Invest. 1988 Aug;82(2):495–501. doi: 10.1172/JCI113623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rosen S. D., Singer M. S., Yednock T. A., Stoolman L. M. Involvement of sialic acid on endothelial cells in organ-specific lymphocyte recirculation. Science. 1985 May 24;228(4702):1005–1007. doi: 10.1126/science.4001928. [DOI] [PubMed] [Google Scholar]
  40. Rothlein R., Springer T. A. The requirement for lymphocyte function-associated antigen 1 in homotypic leukocyte adhesion stimulated by phorbol ester. J Exp Med. 1986 May 1;163(5):1132–1149. doi: 10.1084/jem.163.5.1132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Samuel J. E., Perera L. P., Ward S., O'Brien A. D., Ginsburg V., Krivan H. C. Comparison of the glycolipid receptor specificities of Shiga-like toxin type II and Shiga-like toxin type II variants. Infect Immun. 1990 Mar;58(3):611–618. doi: 10.1128/iai.58.3.611-618.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schauer R. Chemistry, metabolism, and biological functions of sialic acids. Adv Carbohydr Chem Biochem. 1982;40:131–234. doi: 10.1016/s0065-2318(08)60109-2. [DOI] [PubMed] [Google Scholar]
  43. Scudder P., Hanfland P., Uemura K., Feizi T. Endo-beta-D-galactosidases of Bacteroides fragilis and Escherichia freundii hydrolyze linear but not branched oligosaccharide domains of glycolipids of the neolacto series. J Biol Chem. 1984 May 25;259(10):6586–6592. [PubMed] [Google Scholar]
  44. Scudder P., Uemura K., Dolby J., Fukuda M. N., Feizi T. Isolation and characterization of an endo-beta-galactosidase from Bacteroides fragilis. Biochem J. 1983 Aug 1;213(2):485–494. doi: 10.1042/bj2130485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Siegelman M. H., van de Rijn M., Weissman I. L. Mouse lymph node homing receptor cDNA clone encodes a glycoprotein revealing tandem interaction domains. Science. 1989 Mar 3;243(4895):1165–1172. doi: 10.1126/science.2646713. [DOI] [PubMed] [Google Scholar]
  46. Skubitz K. M., August J. T. Characterization of cell surface glycoproteins recognized by the granulocyte-specific monoclonal antibody, AHN-1. Arch Biochem Biophys. 1985 Apr;238(1):263–271. doi: 10.1016/0003-9861(85)90164-x. [DOI] [PubMed] [Google Scholar]
  47. Slodki M. E., Ward R. M., Boundy J. A. Concanavalin A as a probe of phosphomannan molecular structure. Biochim Biophys Acta. 1973 Apr 28;304(2):449–456. doi: 10.1016/0304-4165(73)90264-x. [DOI] [PubMed] [Google Scholar]
  48. Spitalnik P. F., Spitalnik S. L., Danley J. M., Lopez A. F., Vadas M. A., Civin C. I., Ginsburg V. Carbohydrate-specific monoclonal antibodies bind to human granulocytes and stimulate antibody-dependent cellular cytotoxicity. Arch Biochem Biophys. 1989 May 15;271(1):168–176. doi: 10.1016/0003-9861(89)90267-1. [DOI] [PubMed] [Google Scholar]
  49. Spooncer E., Fukuda M., Klock J. C., Oates J. E., Dell A. Isolation and characterization of polyfucosylated lactosaminoglycan from human granulocytes. J Biol Chem. 1984 Apr 25;259(8):4792–4801. [PubMed] [Google Scholar]
  50. Stein K. E., Schwarting G. A., Marcus D. M. Glycolipid markers of murine lymphocyte subpopulations. J Immunol. 1978 Feb;120(2):676–679. [PubMed] [Google Scholar]
  51. Stenberg P. E., McEver R. P., Shuman M. A., Jacques Y. V., Bainton D. F. A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation. J Cell Biol. 1985 Sep;101(3):880–886. doi: 10.1083/jcb.101.3.880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Stoolman L. M., Yednock T. A., Rosen S. D. Homing receptors on human and rodent lymphocytes--evidence for a conserved carbohydrate-binding specificity. Blood. 1987 Dec;70(6):1842–1850. [PubMed] [Google Scholar]
  53. Strauss L. C., Stuart R. K., Civin C. I. Antigenic analysis of hematopoiesis. I. Expression of the My-1 granulocyte surface antigen on human marrow cells and leukemic cell lines. Blood. 1983 Jun;61(6):1222–1231. [PubMed] [Google Scholar]
  54. Tedder T. F., Isaacs C. M., Ernst T. J., Demetri G. D., Adler D. A., Disteche C. M. Isolation and chromosomal localization of cDNAs encoding a novel human lymphocyte cell surface molecule, LAM-1. Homology with the mouse lymphocyte homing receptor and other human adhesion proteins. J Exp Med. 1989 Jul 1;170(1):123–133. doi: 10.1084/jem.170.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Tedder T. F., Penta A. C., Levine H. B., Freedman A. S. Expression of the human leukocyte adhesion molecule, LAM1. Identity with the TQ1 and Leu-8 differentiation antigens. J Immunol. 1990 Jan 15;144(2):532–540. [PubMed] [Google Scholar]
  56. Tetteroo P. A., Mulder A., Lansdorp P. M., Zola H., Baker D. A., Visser F. J., von dem Borne A. E. Myeloid-associated antigen 3-alpha-fucosyl-N-acetyllactosamine (FAL): location on various granulocyte membrane glycoproteins and masking upon monocytic differentiation. Eur J Immunol. 1984 Dec;14(12):1089–1095. doi: 10.1002/eji.1830141205. [DOI] [PubMed] [Google Scholar]
  57. Varki A., Diaz S. A neuraminidase from Streptococcus sanguis that can release O-acetylated sialic acids. J Biol Chem. 1983 Oct 25;258(20):12465–12471. [PubMed] [Google Scholar]
  58. Vedder N. B., Harlan J. M. Increased surface expression of CD11b/CD18 (Mac-1) is not required for stimulated neutrophil adherence to cultured endothelium. J Clin Invest. 1988 Mar;81(3):676–682. doi: 10.1172/JCI113372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Vedder N. B., Winn R. K., Rice C. L., Chi E. Y., Arfors K. E., Harlan J. M. A monoclonal antibody to the adherence-promoting leukocyte glycoprotein, CD18, reduces organ injury and improves survival from hemorrhagic shock and resuscitation in rabbits. J Clin Invest. 1988 Mar;81(3):939–944. doi: 10.1172/JCI113407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Vedder N. B., Winn R. K., Rice C. L., Chi E. Y., Arfors K. E., Harlan J. M. Inhibition of leukocyte adherence by anti-CD18 monoclonal antibody attenuates reperfusion injury in the rabbit ear. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2643–2646. doi: 10.1073/pnas.87.7.2643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Watanabe K., Hakomori S. I. Status of blood group carbohydrate chains in ontogenesis and in oncogenesis. J Exp Med. 1976 Sep 1;144(3):644–653. doi: 10.1084/jem.144.3.644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Yasaka T., Mantich N. M., Boxer L. A., Baehner R. L. Functions of human monocyte and lymphocyte subsets obtained by countercurrent centrifugal elutriation: differing functional capacities of human monocyte subsets. J Immunol. 1981 Oct;127(4):1515–1518. [PubMed] [Google Scholar]
  63. Yednock T. A., Stoolman L. M., Rosen S. D. Phosphomannosyl-derivatized beads detect a receptor involved in lymphocyte homing. J Cell Biol. 1987 Mar;104(3):713–723. doi: 10.1083/jcb.104.3.713. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES