The Biology of P-Selectin Glycoprotein Ligand-1: Its Role as a Selectin Counterreceptor in Leukocyte-Endothelial and Leukocyte-Platelet Interaction

Summary

Cell-cell interactions mediating leukocyte trafficking, thrombogene-sis and inflammation are crucial for the host defense mechanism. The selectin family of integral membrane proteins includes E-selectin, L-selectin and P-selectin. Selectins mediate tethering and rolling of leukocytes to the vessel wall at the site of inflammation. The counter-receptor for P-selectin and possibly the other selectins is P-selectin glycoprotein ligand-1 (PSGL-1). This review focuses on the properties and biology of PSGL-1.

• References

• 1 Celi A, Lorenzet R, Furie BC, Furie B. Platelet-leukocyte-endothelial cell interaction on the blood vessel wall. Semin Hemat 1997; 34: 327-35.
• 2 Palabrica T, Lobb R, Furie BC, Aronovitz M, Benjamin C, Hsu YM, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359: 848-51.
• 3 Foxall C, Watson SR, Dowbenko D, Fennie C, Lasky LA, Kiso M, Hasegawa A, Asa D, Brandley BK. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J Cell Biol 1992; 117: 895-902.
• 4 McEver RP, Moore KL, Cummings RD. Leukocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem 1995; 270: 11025-8.
• 5 Varki A. Selectin ligands: will the real ones please stand up. J Clin Invest 1997; 99: 158-62.
• 6 Larsen E, Celi A, Gilbert GE, Furie BC, Erban JK, Bonfanti R, Wagner DD, Furie B. PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell 1989; 59: 305-12.
• 7 Larsen E, Palabrica T, Sajer S, Gilbert GE, Wagner DD, Furie BC, Furie B. PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNFIII (CD15). Cell 1990; 63: 467-74.
• 8 Moore KL, Stults NL, Diaz S, Smith DF, Cummings RD, Varki A, McEver RP. Identification of a specific glycoprotein ligand for P-selectin (CD62) on myeloid cells. J Cell Biol 1992; 118: 445-56.
• 9 Sako D, Chang XJ, Barone KM, Vachino G, White HM, Shaw G, Veldman GM, Bean KM, Ahern TJ, Furie B, Cumming DA, Larsen GR. Expression cloning of a functional glycoprotein ligand for P-selectin. Cell 1993; 75: 1179-86.
• 10 Moore KL, Patel KD, Bruehl RE, Li F, Johnson DA, Lichenstein HS, Cummings RD, Bainton DF, McEver RP. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol 1995; 128: 661-71.
• 11 Yang J, Galipeau J, Kozak CA, Furie BC, Furie B. Mouse P-selectin glycoprotein ligand- 1: molecular cloning, chromosomal localization, and expression of a functional P-selectin receptor. Blood 1996; 87: 4176-86.
• 12 Borges E, Eytner R, Moll T, Steegmaier M, Campbell MA, Ley K, Mossmann H, Vestweber D. The P-selectin glycoprotein ligand-1 is important for recruitment of neutrophils into inflamed mouse peritoneum. Blood 1997; 90: 1934-42.
• 13 Goetz DJ, Greif DM, Ding H, Camphausen RT, Howes S, Comess KM, Snapp KR, Kansas GS, Luscinskas FW. Isolated P-selectin glycoprotein ligand-1 dynamic adhesion to P- and E-selectin. J Cell Biol 1997; 137: 509-19.
• 14 Ushiyama S, Laue TM, Moore KL, Erickson HP, McEver RP. Structural and functional characterization of monomeric soluble P-selectin and comparison with membrane P-selectin. J Biol Chem 1993; 268: 15229-37.
• 15 Norgard KE, Moore KL, Diaz S, Stults NL, Ushiyama S, McEver RP, Cummings RD, Varki A. Characterization of a specific ligand for P-selection on myeloid cells. A minor glycoprotein with sialylated O-linked oligosaccharides. J Biol Chem 1993; 268: 12764-74.
• 16 Norman KE, Moore KL, McEver RP, Ley K. Leukocyte rolling in vivo is mediated by P-selectin glycoprotein ligand-1. Blood 1995; 86: 4417-21.
• 17 Croce K, Freedman SJ, Furie BC, Furie B. Interaction of soluble P-selectin and soluble PSGL-1. Biochemistry 1998; 37: 16472-80.
• 18 Bruehl RE, Moore KL, Lorant DE, Borregaard N, Zimmerman GA, McEver RP, Bainton DF. Leukocyte activation induces surface redistribution of P-selectin glycoprotein ligand-1. J Leuk Biol 1997; 61: 489-99.
• 19 McEver RP, Cummings RD. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 1997; 100: S97-S103..
• 20 Moore KL, Eaton SF, Lyons DE, Lichenstein HS, Cummings RD, McEver RP. The P-selectin glycoprotein ligand from human neutrophils displays sialylated, fucosylated, O-linked poly-N-acetyllactosamine. J Biol Chem 1994; 269: 23318-27.
• 21 Kumar R, Camphausen RT, Sullivan FX, Cumming DA. Core2 beta-1,6-N-acetylglucosaminyltransferase enzyme activity is critical for P-selectin glycoprotein ligand-1 binding to P-selectin. Blood 1996; 88: 3872-9.
• 22 Li F, Wilkins PP, Crawley S, Weinstein J, Cummings RD, McEver RP. Post-translational modifications of recombinant P-selectin glycoprotein ligand-1 required for binding to P- and E-selectin. J Biol Chem 1996; 271: 3255-64.
• 23 Snapp KR, Wagers AJ, Craig R, Stoolman LM, Kansas GS. P-selectin glycoprotein ligand-1 is essential for adhesion to P-selectin but not E-selectin in stably transfected hematopoietic cell lines. Blood 1997; 89: 896-901.
• 24 Wilkins PP, McEver RP, Cummings RD. Structures of the O-glycans on P-selectin glycoprotein ligand-1 from HL-60 cells. J Biol Chem 1996; 271: 18732-42.
• 25 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; 83: 333-43.
• 26 Sako D, Comess KM, Barone KM, Camphausen RT, Cumming DA, Shaw GD. A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell 1995; 83: 323-31.
• 27 Wilkins PP, Moore KL, McEver RP, Cummings RD. Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J Biol Chem 1995; 270: 22677-80.
• 28 Aigner S, Sthoeger ZM, Fogel M, Weber E, Zarn J, Ruppert M, Zeller Y, Vestweber D, Stahel R, Sammar M, Altevogt P. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 1997; 89: 3385-95.
• 29 Veldman GM, Bean KM, Cumming DA, Eddy RL, Sait SN, Shows TB. Genomic organization and chromosomal localization of the gene encoding human P-selectin glycoprotein ligand. J Biol Chem 1995; 270: 16470-5.
• 30 Vachino G, Chang XJ, Veldman GM, Kumar R, Sako D, Fouser LA, Berndt MC, Cumming DA. P-selectin glycoprotein ligand-1 is the major counter-receptor for P-selectin on stimulated T cells and is widely distributed in non-functional form on many lymphocytic cells. J Biol Chem 1995; 270: 21966-74.
• 31 Fujimoto TT, Noda M, Takafuta T, Shimomura T, Fujimura K, Kuramoto A. Expression and functional characterization of the P-selectin glycoprotein ligand-1 in various cells. Int J Hem 1996; 64: 231-9.
• 32 Li F, Erickson HP, James JA, Moore KL, Cummings RD, McEver RP. Visualization of P-selectin glycoprotein ligand-1 as a highly extended molecule and mapping of protein epitopes for monoclonal antibodies. J Biol Chem 1996; 271: 6342-8.
• 33 Patel KD, Moore KL, Nollert MU, McEver RP. Neutrophils use both shared and distinct mechanisms to adhere to selectins under static and flow conditions. J Clin Invest 1995; 96: 1887-96.
• 34 Steegmaier M, Blanks JE, Borges E, Vestweber D. P-selectin glycoprotein ligand-1 mediates rolling of mouse bone marrow-derived mast cells on P-selectin but not efficiently on E-selectin. Eur J Immunol 1997; 27: 1339-45.
• 35 Liu W, Ramachandran V, Kang J, Kishimoto TK, Cummings RD, McEver RP. Identification of N-terminal residues on P-selectin glycoprotein ligand-1 required for binding to P-selectin. J Biol Chem 1998; 273: 7078-87.
• 36 Snapp KR, Ding H, Atkins K, Warnke R, Luscinskas FW, Kansas GS. A novel P- selectin glycoprotein ligand-1 monoclonal antibody recognizes an epitope within the tyrosine sulfate motif of human PSGL-1 and blocks recognition of both P- and L-selectin. Blood 1998; 91: 154-64.
• 37 Symon FA, Lawrence MB, Williamson ML, Walsh GM, Watson SR, Wardlaw AJ. Functional and structural characterization of the eosinophil P-selectin ligand. J Immunol 157: 1711-9.
• 38 Maemura K, Fukuda M. Poly-N-acetyllactosaminyl O-glycans attached to leukosialin. The presence of sialyl Le(x) structures in O-glycans. J Biol Chem 1992; 267: 24379-86.
• 39 Laszik Z, Jansen PJ, Cummings RD, Tedder TF, McEver RP, Moore KL. P-selectin glycoprotein ligand-1 is broadly expressed in cells of myeloid, lymphoid, and dendritic lineage and in some nonhematopoietic cells. Blood 1996; 88: 3010-21.
• 40 Palomba ML, Yang J, Vestweber D, Furie BC, Furie B. P-selectin glyco-protein ligand-1 is expressed on vascular smooth muscle cells but is not a P-selectin ligand. Blood 1996; 88 (Suppl. 01) Suppl 512a.
• 41 Moore KL, Thompson LF. P-selectin (CD62) binds to subpopulations of human memory T lymphocytes and natural killer cells. Biochem Biophys Res Comm 1992; 186: 173-81.
• 42 Diacovo TG, Roth SJ, Morita CT, Rosat JP, Brenner MB, Springer TA. Interactions of human alpha/beta and gamma/delta T lymphocyte subsets in shear flow with E-selectin and P-selectin. J Exp Med 1996; 183: 1193-203.
• 43 Borges E, Pendl G, Eytner R, Steegmaier M, Zollner O, Vestweber D. The binding of T cell-expressed P-selectin glycoprotein ligand-1 to E-selectin and P-selectin is differentially regulated. J Biol Chem 1997; 272: 28786-92.
• 44 Borges E, Tietz W, Steegmaier M, Moll T, Hallmann R, Hamann A Vestweber. P-selectin glycoprotein ligand-1 (PSGL-1) on T helper 1 but not on T helper 2 cells binds to P-selectin and supports migration into inflamed skin. J Exp Med 1997; 185: 573-8.
• 45 Zannettino AC, Berndt MC, Butcher C, Butcher EC, Vadas MA, Simmons PJ. Primitive human hematopoietic progenitors adhere to P-selectin (CD62P). Blood 1995; 85: 3466-77.
• 46 Tracey JB, Rinder HM. Characterization of the P-selectin ligand on human hematopoietic progenitors. Exp Hematol 1996; 24: 1494-500.
• 47 Geng JG, Raub TJ, Baker CA, Sawada GA, Ma L, Elhammer AP. Expression of a P- selectin ligand in zona pellucida of porcine oocytes and P-selectin on acrosomal membrane of porcine sperm cells. Potential implications for their involvement in sperm-egg interactions. J Cell Biol 1997; 137: 743-54.
• 48 Hirata T, Yang J, Merrill-Skoloff GM, Croce K, Tchernychev B, Flaumen-haft R, Furie BC, Furie B. Blood. 1998; 92 (Suppl. 01) Suppl 498a.
• 49 Lawrence MB, Springer TA. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 1991; 65: 859-73.
• 50 Lorant DE, McEver RP, McIntyre TM, Moore KL, Prescott SM, Zimmer-man GA. Activation of polymorphonuclear leukocytes reduces their adhesion to P-selectin and causes redistribution of ligands for P-selectin on their surfaces. J Clin Inves 1995; 96: 171-82.
• 51 Rinder HM, Tracey JL, Rinder CS, Leitenberg D, Smith BR. Neutrophil but not monocyte activation inhibits P-selectin-mediated platelet adhesion. Thromb Haemost 1994; 72: 750-6.
• 52 Dore M, Burns AR, Hughes BJ, Entman ML, Smith CW. Chemoattractant-induced changes in surface expression and redistribution of a functional ligand for P-selectin on neutrophils. Blood 1996; 87: 2029-37.
• 53 Alon R, Fuhlbrigge RC, Finger EB, Springer TA. Interactions through L-selectin between leukocytes and adherent leukocytes nucleate rolling adhesions on selectins and VCAM-1 in shear flow. J Cell Biol 1996; 135: 849-65.
• 54 Fuhlbrigge RC, Alon R, Puri KD, Lowe JB, Springer TA. Sialylated, fucosylated ligands for L-selectin expressed on leukocytes mediate tethering and rolling adhesions in physiologic flow conditions. J Cell Biol 1996; 135: 837-48.
• 55 Guyer DA, Moore KL, Lynam EB, Schammel CM, Rogelj S, McEver RP, Sklar LA. P-selectin glycoprotein ligand-1 (PSGL-1) is a ligand for L-selectin in neutrophil aggregation. Blood 1996; 88: 2415-21.
• 56 Spertini O, Cordey AS, Monai N, Giuffre L, Schapira M. P-selectin glyco-protein ligand 1 is a ligand for L-selectin on neutrophils, monocytes, and CD34+ hematopoietic progenitor cells. J Cell Biol 1996; 135: 523-31.
• 57 Tu L, Chen A, Delahunty MD, Moore KL, Watson SR, McEver RP, Tedder TF. L-selectin binds to P-selectin glycoprotein ligand-1 on leukocytes: interactions between the lectin, epidermal growth factor, and consensus repeat domains of the selectins determine ligand binding specificity. J Immunol 1996; 157: 3995-4004.
• 58 Walcheck B, Moore KL, McEver RP, Kishimoto TK. Neutrophil-neutrophil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1. A mechanism that amplifies initial leukocyte accumulation of P-selectin in vitro. J Clin Invest 1996; 98: 1081-7.
• 59 Ramos CL, Smith MJ, Snapp KR, Kansas GS, Stickney GW, Ley K, Lawrence MB. Functional characterization of L-selectin ligands on human neutrophils and leukemia cell lines: evidence for mucinlike ligand activity distinct from P-selectin glycoprotein ligand-1. Blood 1998; 91: 1067-75.
• 60 Fuhlbrigge RC, Kieffer JD, Armerding D, Kupper T. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature 1997; 389: 1978-81.
• 61 Larsen GR, Sako D, Ahern TJ, Shaffer M, Erban J, Sajer SA, Gibson RM, Wagner DD, Furie BC, Furie B. P-selectin and E-selectin. Distinct but overlapping leukocyte ligand specificities. J Biol Chem 1992; 267: 11104-10.
• 62 Tamatani T, Suematsu M, Tezuka K, Hanzawa N, Tsuji T, Ishimura Y, Kannagi R, Toyoshima S, Homma M. Recognition of consensus CHO structure in ligands for selectins by novel antibody against sialyl Lewis X. Amer J Physiol 269: 1282-7.
• 63 Asa D, Raycroft L, Ma L, Aeed PA, Kaytes PS, Elhammer AP, Geng JG. The P-selectin glycoprotein ligand functions as a common human leukocyte ligand for P- and E-selectins. J Biol Chem 1995; 270: 11662-70.
• 64 Blanks JE, Moll T, Eytner R, Vestweber D. Stimulation of P-selectin glycoprotein ligand-1 on mouse neutrophils activates beta 2-integrin mediated cell attachment to ICAM-1. Eur J Immunol 1998; 28: 433-43.
• 65 Celi A, Pellegrini G, Lorenzet R, De Blasi A, Ready N, Furie BC, Furie B. P-selectin induces the expression of tissue factor on monocytes. Proc Nat Acad Sci 1994; 91: 8767-71.
• 66 Weyrich AS, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA. Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-alpha secretion. Signal integration and NF-kappa B translocation. J Clin Invest 1995; 95: 2297-303.
• 67 Weyrich AS, Elstad MR, McEver RP, McIntyre TM, Moore KL, Morrissey JH, Prescott SM, Zimmerman GA. Activated platelets signal chemokine synthesis by human monocytes. J Clin Inves 1996; 97: 1525-34.
• 68 Haller H, Kunzendorf U, Sacherer K, Lindschau C, Walz G, Distler A, Luft FC. T cell adhesion to P-selectin induces tyrosine phosphorylation of pp125 focal adhesion kinase and other substrates. J Immunol 1997; 158: 1061-7.
• 69 Hidari K, Weyrich A, Zimmerman G, McEver R. Engagement of P-selectin glycoprotein ligand-1 enhances tyrosine phosphorylation and activates mitogen-activated protein kinases in human neutrophils. J Biol Chem 1997; 272: 28750-6.
• 70 Takada M, Nadeau KC, Shaw GD, Marquette KA, Tilney NL. The cyto-kine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney. Inhibition by a soluble P-selectin ligand. J Clin Invest 1997; 99: 2682-90.
• 71 Albert L, Erickson J, Mason L, Ferranti T, Patel U, Donnelly LH, Keith JC, Schaub RG. Recombinant human soluble P-selectin Glycoprotein Ligand-1 decreases adjuvant-induced arthritis in Lewis rats. Arth. Rheumat 1997; 40: 261.
• 72 Tang T, Frenette PS, Hynes RO, Wagner DD, Mayadas TN. Cytokine-induced meningitis is dramatically attenuated in mice deficient in endothelial selectins. J Clin Invest 1996; 97: 2485-90.
• 73 Johnson RC, Chapman SM, Dong ZM, Ordovas JM, Mayadas TN, Herz J, Hynes RO, Schaefer EJ, Wagner DD. Absence of P-selectin delays fatty streak formation in mice. J Clin Invest 1997; 99: 1037-43.
• 74 Mulligan MS, Polley MJ, Bayer RJ, Nunn MF, Paulson JC, Ward PA. Neutrophil-dependent acute lung injury. Requirement for P-selectin (GMP-140). J Clin Invest 1992; 90: 1600-7.
• 75 Mulligan MS, Watson SR, Fennie C, Ward PA. Protective effects of selectin chimeras in neutrophil-mediated lung injury. J Immunol 1993; 151: 6410-7.
• 76 Coughlan AF, Hau H, Dunlop LC, Berndt MC, Hancock WW. P-selectin and platelet- activating factor mediate initial endotoxin-induced neutropenia. J Exp Med 1994; 179: 329-34.
• 77 Stone JP, Wagner DD. P-selectin mediates adhesion of platelets to neuroblastoma and small cell lung cancer. J Clin Invest 1993; 92: 804-13.