Adhesive Interactions of Leukocytes, Platelets, and the Vessel Wall during Hemostasis and Inflammation

 

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Summary

In response to hemorrhage, circulating platelets adhere to exposed subendothelial tissues and then recruit additional platelets into aggregates that function as procoagulant surfaces. In response to inflammatory stimuli, circulating leukocytes roll and then arrest on endothelial cells, and finally migrate into the surrounding tissues where they combat pathogens and repair tissue injury. These traditionally separate cellular adhesive contributions to coagulation and inflammation have become progressively linked. We now know that leukocytes roll and then arrest on activated platelets and that platelets roll on activated endothelial cells. Cell adhesion molecules that were first thought to contribute uniquely to either coagulation or inflammation are now known to contribute to both responses. This review focuses on multicellular adhesive interactions in the vasculature, with particular attention to the dual functions of the adhesion molecules P-selectin, P-selectin glycoprotein ligand-1 (PSGL-1), and glycoprotein Ib (GPIb) in coagulation and inflammation.

• References

• 1 Savage B, SaldÌvar E, Ruggeri ZM. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 1996; 84: 289-97.
  CrossrefPubMedGoogle Scholar
• 2 Yuan Y, Kulkarni S, Ulsemer P, Cranmer SL, Yap CL, Nesbitt WS, Harper I, Mistry N, Dopheide SM, Hughan SC, Williamson D, de la Salle C, Salem HH, Lanza F, Jackson SP. The von Willebrand factor-glycoprotein Ib/V/IX interaction induces actin polymerization and cytoskeletal reorganization in rolling platelets and glycoprotein Ib/V/IX-transfected cells. J Biol Chem 99 274: 36241-51.
  PubMedGoogle Scholar
• 3 Ruggeri ZM. Structure and function of von Willebrand factor. Thromb Haemost 1999; 82: 576-84.
  Article in Thieme ConnectPubMedGoogle Scholar
• 4 Ruggeri ZM. Mechanisms initiating platelet thrombus formation [published erratum appears in Thromb Haemost 1997 Oct; 78 (4):1304] [see comments]. Thromb Haemost 1997; 78: 611-6.
  Article in Thieme ConnectPubMedGoogle Scholar
• 5 Lopez JA. The platelet glycoprotein Ib-IX complex. Blood Coagul Fibrinolysis 1994; 5: 97-119.
  CrossrefPubMedGoogle Scholar
• 6 Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 1998; 67: 395-424.
  CrossrefPubMedGoogle Scholar
• 7 Cruz MA, Diacovo TG, Emsley J, Liddington R, Handin RI. Mapping the glycoprotein Ib-binding site in the von willebrand factor A1 domain. J Biol Chem 2000; 275: 19098-105.
  CrossrefPubMedGoogle Scholar
• 8 Dong J, Hyun W, Lopez JA. Aggregation of mammalian cells expressing the platelet glycoprotein (GP) Ib-IX complex and the requirement for tyrosine sulfation of GPIbα. Blood 1995; 86: 4175-83.
  PubMedGoogle Scholar
• 9 Marchese P, Saldivar E, Ware J, Ruggeri ZM. Adhesive roperties of the isolated amino-termial domain of platelet glycoprotein Ibα in flow field. Proc Natl Acad Sci USA 1999; 96: 7837-42.
  CrossrefPubMedGoogle Scholar
• 10 Dong JF, Schade AJ, Romo GM, Andrews RK, Gao S, McIntire LV, López JA. Novel gain-of-function mutations of platelet glycoprotein Iba by valine mutagenesis in the Cys²⁰⁹-Cys²⁴⁸ disulfide loop. J Biol Chem 2000; 275: 27663-70.
  PubMedGoogle Scholar
• 11 Miura S, Li CQ, Cao Z, Wang H, Wardell MR, Sadler JE. Interaction of von Willebrand factor domain A1 with platelet glycoprotein Ibα-(1-289). Slow intrinsic binding kinetics mediate rapid platelet adhesion. J Biol Chem 200 275: 7539-46.
  PubMedGoogle Scholar
• 12 Kumar RA, Dong J, Lopez JA, McIntire LV. Estimation of the platelet glycoprotien (GP) Ibα-von Willebrand factor (vWf) bond lifetime under hydrodynamic flow. Blood 2000; 96: 624a. (Abstr.)
  PubMedGoogle Scholar
• 13 Coller BS, Peerschke EI, Scudder LE, Sullivan CA. Studies with a murine monoclonal antibody that abolishes ristocetin-induced binding of von Willebrand factor to platelets: Additional evidence in support of GPIb as a platelet receptor for von Willebrand factor. Blood 1983; 61: 99-110.
  PubMedGoogle Scholar
• 14 Savage B, Almus-Jacobs F, Ruggeri ZM. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 1998; 94: 657-66.
  CrossrefPubMedGoogle Scholar
• 15 Gu M, Xi X, Englund GD, Berndt MC, Du X. Analysis of the roles of 14-3-3 in the platelet glycoprotein Ib-IX-mediated activation of integrin αIIβ3 using a reconstitued mammalian cell expression model. J Cell Biol 99 147: 1085-96.
  PubMedGoogle Scholar
• 16 Yap CL, Hughan SC, Cranmer SL, Nesbitt WS, Rooney MM, Giuliano S, Kulkarni S, Dopheide SM, Yuan Y, Salem HH, Jackson SP. Synergistic adhesive interactions and signaling mechanism operating between platelet glycoprotein Ib/IX and integrin aIIbb3. Studies in human platelets and transfected Chinese hamster overy cells. J Biol Chem 2000; 275: 41377-88.
  CrossrefPubMedGoogle Scholar
• 17 Zaffran Y, Meyer SC, Negrescu E, Redday KB, Fox JE. Signaling across the platelet adhesion receptor glycoprotein Ib-IX induces αIIbβ3 activation both in platelets and a transfected Chinese hamster ovary cell system. J Biol Chem 2000; 275: 16779-87.
  CrossrefPubMedGoogle Scholar
• 18 Ruggeri ZM, Dent JA, Saldivar E. Contribution of distinct adhesive interactions to platelet aggregation in flowing blood. Blood 1999; 94: 172-8.
  PubMedGoogle Scholar
• 19 Springer TA. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 1995; 57: 827-72.
  CrossrefPubMedGoogle Scholar
• 20 McEver RP, Moore KL, Cummings RD. Leukocyte trafficking mediated by selectin-carbohydrate interactions. J Biol Chem 1995; 270: 11025-8.
  CrossrefPubMedGoogle Scholar
• 21 Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 1996; 88: 3259-87.
  PubMedGoogle Scholar
• 22 Vestweber D, Blanks JE. Mechanisms that regulate the function of the selectins and their ligands [published erratum appears in Physiol Rev 2000 Jul; 80 (3): following table of contents]. Physiol Rev 1999; 79: 181-213.
  CrossrefPubMedGoogle Scholar
• 23 Kunkel EJ, Ley K. Distinct phenotype of E-selectin-deficient mice – E-selectin is required for slow leukocyte rolling in vivo. Circ Res 1996; 79: 1196-204.
  CrossrefPubMedGoogle Scholar
• 24 Jung U, Norman KE, Scharffetter-Kochanek K, Beaudet AL, Ley K. Transit time of leukocytes rolling through venules controls cytokine-induced inflammatory cell recruitment in vivo. J Clin Invest 1998; 102: 1526-33.
  CrossrefPubMedGoogle Scholar
• 25 Zimmerman GA, McIntyre TM, Prescott SM. Adhesion and signaling in vascular cell-cell interactions. J Clin Invest 1996; 98: 1699-702.
  CrossrefPubMedGoogle Scholar
• 26 Harris ES, McIntyre TM, Prescott SM, Zimmerman GA. The leukocyte integrins. J Biol Chem 2000; 275: 23409-12.
  CrossrefPubMedGoogle Scholar
• 27 Kunkel EJ, Dunne JL, Ley K. Leukocyte arrest during cytokine-dependent inflammation in vivo. J Immunol 2000; 164: 3301-8.
  CrossrefPubMedGoogle Scholar
• 28 Forlow SB, White EJ, Barlow SC, Feldman SH, Lu H, Bagby GJ, Beaudet AL, Bullard DC, Ley K. Severe inflammatory defect and reduced viability in CD18 and E-selectin double-mutant mice. J Clin Invest 2000; 106: 1457-66.
  CrossrefPubMedGoogle Scholar
• 29 Sigal A, Bleijs DA, Grabovsky V, Van Vliet SJ, Dwir O, Figdor CG, Van Kooyk Y, Alon R. The LFA-1 integrin supports rolling adhesions on ICAM-1 under physiological shear flow in a permissive cellular environment. J Immunol 2000; 165: 442-52.
  CrossrefPubMedGoogle Scholar
• 30 Alon R, Kassner PD, Carr MW, Finger EB, Hemler ME, Springer TA. The integrin VLA-4 supports tethering and rolling in flow on VCAM-1. J Cell Biol 1995; 128: 1243-53.
  CrossrefPubMedGoogle Scholar
• 31 Berlin C, Bargatze RF, Campbell JJ, Von Andrian UH, Szabo MC, Hasslen SR, Nelson RD, Berg EL, Erlandsen SL, Butcher EC. 4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell 1995; 80: 413-22.
  CrossrefPubMedGoogle Scholar
• 32 Taooka Y, Chen J, Yednock T, Sheppard D. The integrin α9β1 mediates adhesion to activated endothelial cells and transendothelial neutrophil migration through interaction with vascular cell adhesion molecule-1. J Cell Biol 1999; 145: 413-20.
  CrossrefPubMedGoogle Scholar
• 33 Varki A. Selectin ligands: will the real ones please stand up?. J Clin Invest 1997; 99: 158-62.
  CrossrefPubMedGoogle Scholar
• 34 Maly P, Thall AD, Petryniak B, Rogers GE, Smith PL, Marks RM, Kelly RJ, Gersten KM, Cheng GY, Saunders TL, Camper SA, Camphausen RT, Sullivan FX, Isogai Y, Hindsgaul O, Von Andrian UH, Lowe JB. The α(1,3)Fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E-, and P-selectin ligand biosynthesis. Cell 1996; 86: 643-53.
  CrossrefPubMedGoogle Scholar
• 35 Etzioni A, Frydman M, Pollack S, Avidor I, Phillips ML, Paulson JC, Gershoni-Baruch R. Brief report: recurrent severe infections caused by a novel leukocyte adhesion deficiency. N Engl J Med 1992; 327: 1789-92.
  CrossrefPubMedGoogle Scholar
• 36 McEver RP, Cummings RD. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 1997; 100: 485-92.
  CrossrefPubMedGoogle Scholar
• 37 Moore KL, Stults NL, Diaz S, Smith DL, 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.
  CrossrefPubMedGoogle Scholar
• 38 Norgard KE, Moore KL, Diaz S, Stults NL, Ushiyama S, McEver RP, Cummings RD, Varki A. Characterization of a specific ligand for P-selectin on myeloid cells. A minor glycoprotein with sialylated O-linked oligosaccharides. J Biol Chem 1993; 268: 12764-74.
  PubMedGoogle Scholar
• 39 Moore KL, Patel KD, Bruehl RE, Fugang L, 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.
  CrossrefPubMedGoogle Scholar
• 40 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.
  PubMedGoogle Scholar
• 41 Borges E, Eytner R, Moll T, Steegmaier M, Campbell MA, Ley K, Moss-man H, Vestweber D. The P-selectin glycoprotein ligand-1 is important for recruitment of neutrophils into inflamed mouse peritoneum. Blood 1997; 90: 1934-42.
  PubMedGoogle Scholar
• 42 Yang J, Hirata T, Croce K, Merrill-Skoloff G, Tchernychev B, Williams E, Flaumenhaft R, Furie BC, Furie B. Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J Exp Med 1999; 190: 1769-82.
  CrossrefPubMedGoogle Scholar
• 43 Walcheck B, Moore KL, McEver RP, Kishimoto TK. Neutrophil-neutro-phil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1: a mechanism that amplifies initial leukocyte accumulation on P-selectin in vitro. J Clin Invest 1996; 98: 1081-7.
  CrossrefPubMedGoogle Scholar
• 44 Kunkel EJ, Chomas JE, Ley K. Role of primary and secondary capture for leukocyte accumulation in vivo. Circ Res 1998; 82: 30-8.
  CrossrefPubMedGoogle Scholar
• 45 Mitchell DJ, Li P, Reinhardt PH, Kubes P. Importance of L-selectin-dependent leukocyte-leukocyte interactions in human whole blood. Blood 2000; 95: 2954-9.
  PubMedGoogle Scholar
• 46 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.
  CrossrefPubMedGoogle Scholar
• 47 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.
  CrossrefPubMedGoogle Scholar
• 48 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.
  CrossrefPubMedGoogle Scholar
• 49 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.
  CrossrefPubMedGoogle Scholar
• 50 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.
  CrossrefPubMedGoogle Scholar
• 51 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.
  CrossrefPubMedGoogle Scholar
• 52 Liu W-J, 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.
  CrossrefPubMedGoogle Scholar
• 53 Ramachandran V, Nollert MU, Qiu H, Liu W, Cummings RD, Zhu C, McEver RP. Tyrosine replacement in P-selectin glycoprotein ligand-1 affects distinct kinetic and mechanical properties of bonds with P- and L-selectin. Proc Natl Acad Sci USA 1999; 96: 13771-6.
  CrossrefPubMedGoogle Scholar
• 54 Leppanen A, Mehta P, Ouyang Y-B, Ju T, Helin J, Moore KL, van Die I, Canfield WM, McEver RP, Cummings RD. A novel glycosulfopeptide binds to P-selectin and inhibits leukocyte adhesion to P-selectin. J Biol Chem 1999; 274: 24838-48.
  CrossrefPubMedGoogle Scholar
• 55 Leppanen A, White SP, Helin J, McEver RP, Cummings RD. Binding of glycosulfopeptides to P-selectin requires stereospecific contributions of individual tyrosine sulfate and sugar residues. J Biol Chem 2000; 275: 39569-78.
  CrossrefPubMedGoogle Scholar
• 56 Somers WS, Tang J, Shaw GD, Camphausen RT. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1 [In Process Citation]. Cell 2000; 103: 467-79.
  CrossrefPubMedGoogle Scholar
• 57 Mehta P, Cummings RD, McEver RP. Affinity and kinetic analysis of P-selectin binding to P-selectin glycoprotein ligand-1. J Biol Chem 1998; 273: 32506-13.
  CrossrefPubMedGoogle Scholar
• 58 Croce K, Freedman SJ, Furie BC, Furie B. Interaction between soluble P-selectin and soluble P-selectin glycoprotein ligand 1: Equilibrium binding analysis. Biochemistry 1998; 37: 16472-80.
  CrossrefPubMedGoogle Scholar
• 59 Poppe L, Brown GS, Philo JS, Nikrad PV, Shah BH. Conformation of sLex tetrasaccharide, free in solution and bound to E-, P-, and L-selectin. J Am Chem Soc 1997; 119: 1727-36.
  CrossrefPubMedGoogle Scholar
• 60 Brandley BK, Kiso M, Abbas S, Nikrad P, Srivasatava O, Foxall C, Oda Y, Hasegawa A. Structure-function studies on selectin carbohydrate ligands. Modifications to fucose, sialic acid and sulphate as a sialic acid replacement. Glycobiology 1993; 3: 633-9.
  CrossrefPubMedGoogle Scholar
• 61 Koenig A, Jain R, Vig R, Norgard-Sumnicht KE, Matta KL, Varki A. Selectin inhibition: Synthesis and evaluation of novel sialylated, sulfated and fucosylated oligosaccharides, including the major capping group of GlyCAM-1. Glycobiology 1997; 7: 79-93.
  CrossrefPubMedGoogle Scholar
• 62 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.
  PubMedGoogle Scholar
• 63 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.
  CrossrefPubMedGoogle Scholar
• 64 Alon R, Hammer DA, Springer TA. Lifetime of the P-selectin: carbohydrate bond and its response to tensile force in hydrodynamic flow. Nature 1995; 374: 539-42.
  CrossrefPubMedGoogle Scholar
• 65 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.
  PubMedGoogle Scholar
• 66 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.
  CrossrefPubMedGoogle Scholar
• 67 Hattori R, Hamilton KK, Fugate RD, McEver RP, Sims PJ. 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; 264: 7768-71.
  PubMedGoogle Scholar
• 68 Von Andrian UH, Hasslen SR, Nelson RD, Erlandsen SL, Butcher EC. A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell 1995; 82: 989-99.
  CrossrefPubMedGoogle Scholar
• 69 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 Leukoc Biol 1997; 61: 489-99.
  CrossrefPubMedGoogle Scholar
• 70 Patel KD, Nollert MU, McEver RP. P-selectin must extend a sufficient length from the plasma membrane to mediate rolling of neutrophils. J Cell Biol 1995; 131: 1893-902.
  CrossrefPubMedGoogle Scholar
• 71 Shao JY, Ting-Beall HP, Hochmuth RM. Static and dynamic lengths of neutrophil microvilli. Proc Natl Acad Sci USA 1998; 95: 6797-802.
  CrossrefPubMedGoogle Scholar
• 72 Schmidtke DW, Diamond SL. Direct observation of membrane tethers formed during neutrophil attachment to platelets or P-selectin under physiological flow. J Cell Biol 2000; 149: 719-29.
  CrossrefPubMedGoogle Scholar
• 73 Setiadi H, Sedgewick G, Erlandsen SL, McEver RP. Interactions of the cytoplasmic domain of P-selectin with clathrin-coated pits enhance leukocyte adhesion under flow. J Cell Biol 1998; 142: 859-71.
  CrossrefPubMedGoogle Scholar
• 74 Epperson TK, Patel KD, McEver RP, Cummings RD. Noncovalent dimerization of P-selectin glycoprotein ligand-1 and minimal determinants for binding to P-selectin. J Biol Chem 2000; 275: 7839-53.
  CrossrefPubMedGoogle Scholar
• 75 Snapp KR, Craig R, Herron M, Nelson RD, Stoolman LM, Kansas GS. Dimerization of P-selectin glycoprotein ligand-1 (PSGL-1) required for optimal recognition of P-selectin. J Cell Biol 1998; 142: 263-70.
  CrossrefPubMedGoogle Scholar
• 76 Barkalow FJ, Barkalow KL, Mayadas TN. Dimerization of P-selectin in platelets and endothelial cells. Blood 2000; 96: 3070-7.
  PubMedGoogle Scholar
• 76a Ramachandran V, Yago T, Epperson TK, Kobzdej MAJ, Nollert MU, Cummings RD, Zhu C, McEver RP. Dimerization of a selectin and its ligand stabilizes cell rolling and enhances tether strength in shear flow. Proc Natl Acad Sci USA. in press.
  PubMedGoogle Scholar
• 77 Chen SQ, Springer TA. An automatic braking system that stabilizes leukocyte rolling by an increase in selectin bond number with shear. J Cell Biol 1999; 144: 185-200.
  CrossrefPubMedGoogle Scholar
• 78 Stenberg PE, McEver RP, Shuman MA, Jacques YV, Bainton DF. A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation. J Cell Biol 1985; 101: 880-6.
  CrossrefPubMedGoogle Scholar
• 79 Berman CL, Yeo EL, Wencel-Drake JD, Furie BC, Ginsberg MH, Furie B. A platelet alpha granule membrane protein that is associated with the plasma membrane after activation. J Clin Invest 1986; 78: 130-7.
  CrossrefPubMedGoogle Scholar
• 80 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.
  CrossrefPubMedGoogle Scholar
• 81 Hamburger SA, McEver RP. GMP-140 mediates adhesion of stimulated platelets to neutrophils. Blood 1990; 75: 550-4.
  PubMedGoogle Scholar
• 82 Buttrum SM, Hatton R, Nash GB. Selectin-mediated rolling of neutrophils on immobilized platelets. Blood 1993; 82: 1165-74.
  PubMedGoogle Scholar
• 83 Yeo EL, Sheppard J-AI, Feuerstein IA. Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiologic shear conditions (an injury vessel wall model). Blood 1994; 83: 2498-507.
  PubMedGoogle Scholar
• 84 Diacovo TG, Roth SJ, Buccola JM, Bainton DF, Springer TA. Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the β2-integrin CD11b/CD18. Blood 1996; 88: 146-57.
  PubMedGoogle Scholar
• 85 Weber C, Springer TA. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to αIIβ3 and stimulated by platelet-activating factor. J Clin Invest 1997; 100: 2085-93.
  CrossrefPubMedGoogle Scholar
• 86 McEver RP, Martin MN. A monoclonal antibody to a membrane glycoprotein binds only to activated platelets. J Biol Chem 1984; 259: 9799-804.
  PubMedGoogle Scholar
• 87 Hsu-Lin S-C, Berman CL, Furie BC, August D, Furie B. A platelet membrane protein expressed during platelet activation and secretion. Studies using a monoclonal antibody specific for thrombin-activated platelets. J Biol Chem 1984; 259: 9121-6.
  PubMedGoogle Scholar
• 88 Hidari KIPJ, Weyrich AS, Zimmerman GA, McEver RP. 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.
  CrossrefPubMedGoogle Scholar
• 89 Blanks JE, Moll T, Eytner R, Vestweber D. Stimulation of P-selectin glycoprotein ligand-1 on mouse neutrophils activates β2-integrin mediated cell attachment to ICAM-1. Eur J Immunol 1998; 28: 433-43.
  CrossrefPubMedGoogle Scholar
• 90 Evangelista V, Manarini S, Sideri R, Rotondo S, Martelli N, Piccoli A, Totani L, Piccardoni P, Vestweber D, de Gaetano G, Cerletti C. Platelet/polymorphonuclear leukocyte interaction: P-selectin triggers protein-tyrosine phosphorylation-dependent CD11b/CD18 adhesion: Role of PSGL-1 as a signaling molecule. Blood 1999; 93: 876-85.
  PubMedGoogle Scholar
• 91 Yago T, Tsukuda M, Minami M. P-selectin binding promotes the adhesion of monocytes to VCAM-1 under flow conditions. J Immunol 1999; 163: 367-73.
  PubMedGoogle Scholar
• 92 Weyrich AS, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA. Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-α secretion. J Clin Invest 1995; 95: 2297-303.
  CrossrefPubMedGoogle Scholar
• 93 Ostrovsky L, King AJ, Bond S, Mitchell D, Lorant DE, Zimmerman GA, Larsen R, Niu XF, Kubes P. A juxtacrine mechanism for neutrophil adhesion on platelets involves platelet-activating factor and a selectin-dependent activation process. Blood 1998; 91: 3028-36.
  PubMedGoogle Scholar
• 94 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 Invest 1996; 97: 1525-34.
  CrossrefPubMedGoogle Scholar
• 95 Diacovo TG, DeFougerolles AR, Bainton DF, Springer TA. A functional integrin ligand on the surface of platelets: Intercellular adhesion molecule-2. J Clin Invest 1994; 94: 1243-51.
  CrossrefPubMedGoogle Scholar
• 96 Simon DI, Chen CP, Xu H, Li CQ, Dong JF, McIntire LV, Ballantyne CM, Zhang L, Furman MI, Berndt MC, López JA. Platelet glycopotein Ibα is a counterreceptor for the leukocyte integrin Mac-1 (CD1 1b/CD18). J Exp Med 2000; 192: 193-204.
  CrossrefPubMedGoogle Scholar
• 97 Frenette PS, Johnson RC, Hynes RO, Wagner DD. Platelets roll on stimulated endothelium in vivo. An interaction mediated by endothelial P-selectin. Proc Natl Acad Sci USA 1995; 92: 7450-4.
  CrossrefPubMedGoogle Scholar
• 98 Frenette PS, Moyna C, Hartwell DW, Lowe JB, Hynes RO, Wagner DD. Platelet-endothelial interactions in inflamed mesenteric venules. Blood 1998; 91: 1318-24.
  PubMedGoogle Scholar
• 99 Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, López JA. The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med 1999; 190: 803-13.
  CrossrefPubMedGoogle Scholar
• 100 Frenette PS, Denis CV, Weiss L, Jurk K, Subbarao S, Kehrel B, Hartwig JH, Vestweber D, Wagner DD. P-selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo. J Exp Med 2000; 191: 1413-22.
  CrossrefPubMedGoogle Scholar
• 101 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.
  PubMedGoogle Scholar
• 102 Gross PL, Merrill-Skoloff G, Aab M, Croce K, Ware J, Ruggeri ZM, Furie BC, Furie B. Glycoprotein Ib and PSGL-1 serve as platelet ligands for platelet-endothelial cell interaction during platelet rolling on stimulated postcapillary venules in vivo. Blood 2000; 96: 812a. (Abstr.)
  PubMedGoogle Scholar
• 103 André P, Denis CV, Ware J, Saffaripour S, Hynes RO, Ruggeri ZM, Wagner DD. Platelets adhere to and translocate on von Willebrand factor presented by endothelium in simulated veins. Blood 2000; 96: 3322-8.
  CrossrefPubMedGoogle Scholar
• 104 Massberg S, Enders G, Leiderer R, Eisenmenger S, Vestweber D, Krombach F, Messmer K. Platelet-endothelial cell interactions during ischemia/reperfusion: The role of P-selectin. Blood 1998; 92: 507-15.
  PubMedGoogle Scholar
• 105 Diacovo TG, Puri KD, Warnock RA, Springer TA, Von Andrian UH. Platelet-mediated lymphocyte delivery to high endothelial venules. Science 1996; 273: 252-5.
  CrossrefPubMedGoogle Scholar
• 106 Rosen SD, Hwang ST, Giblin PA, Singer MS. High-endothelial-venule ligands for L-selectin: identification and functions. Biochem Soc Trans 1997; 25: 428-33.
  CrossrefPubMedGoogle Scholar
• 107 Bombeli T, Schwartz BR, Harlan JM. Adhesion of activated platelets to endothelial cells: Evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), α_vβ₃ integrin, and GPIbα. J Exp Med 1998; 187: 329-39.
  CrossrefPubMedGoogle Scholar
• 108 Parmentier S, McGregor L, Catimel B, Leung LLK, McGregor JL. Inhibition of platelet functions by a monoclonal antibody (LYP20) directed against a granule membrane glycoprotein (GMP-140/PADGEM). Blood 1991; 77: 1734-9.
  PubMedGoogle Scholar
• 109 Merten M, Thiagarajan P. P-selectin expression on platelets determines size and stability of platelet aggregates. Circulation 2000; 102: 1931-6.
  CrossrefPubMedGoogle Scholar
• 110 Merten M, Chow T, Hellums JD, Thiagarajan P. A new role for P-selectin in shear-induced platelet aggregation. Circulation 2000; 102: 2045-50.
  CrossrefPubMedGoogle Scholar
• 111 Smyth SS, Reis ED, Fallon JT, Gordon R, Coller BS. Alterations in platelet thrombus formation, leukocyte recruitment, and intimal hyperplasia in P-selectin-deficient mice after transluminal femoral artery injury. Blood 2000; 96: 813a. (Abstr.)
  PubMedGoogle Scholar
• 112 Ruggeri ZM, Subramanian M, Dent JA, Wagner DD, Saldivar E. P-selectin and the three-dimensional structure of platelet thrombi. Blood 2000; 96: 812a. (Abstr.)
  PubMedGoogle Scholar
• 113 Isenberg WM, McEver RP, Shuman MA, Bainton DF. Topographic distribution of a granule membrane protein (GMP-140) that is expressed on the platelet surface after activation: an immunogold-surface replica study. Blood Cells 1986; 12: 191-204.
  PubMedGoogle Scholar
• 114 Lehr H-A, Olofsson AM, Carew TE, Vajkoczy P, Von Andrian UH, Hübner C, Berndt MC, Steinberg D, Messmer K, Arfors KE. P-selectin mediates the interaction of circulating leukocytes with platelets and microvascular endothelium in response to oxidized lipoprotein in vivo. Lab Invest 1994; 71: 380-6.
  PubMedGoogle Scholar
• 115 Theilmeier G, Lenaerts T, Remacle C, Collen D, Vermylen J, Hoylaerts MF. Circulating activated platelets assist THP-1 monocytoid/endothelial cell interaction under shear stress. Blood 1999; 94: 2725-34.
  PubMedGoogle Scholar
• 116 Kirton CM, Nash GB. Activated platelets adherent to an intact endothelial cell monolayer bind flowing neutrophils and enable them to transfer to the endothelial surface. J Lab Clin Med 2000; 136: 303-13.
  CrossrefPubMedGoogle Scholar
• 117 Chan G, von Andrian UH, Diacovo TG. Leukocyte-mediated platelet deposition at sites of venular inflammation. Blood 1999; 94: 449a. (Abstr.)
  PubMedGoogle Scholar
• 118 Merhi Y, Provost P, Chauvet P, Théorêt JF, Phillips ML, Latour JG. Selectin blockade reduces neutrophil interaction with platelets at the site of deep arterial injury by angioplasty in pigs. Arterioscler Thromb Vasc Biol 1999; 19: 372-7.
  CrossrefPubMedGoogle Scholar
• 119 Forlow SB, McEver RP, Nollert MU. Leukocyte-leukocyte interactions mediated by platelet microparticles under flow. Blood 2000; 95: 1317-23.
  CrossrefPubMedGoogle Scholar
• 120 André P, Hartwell D, Hrachovinov· I, Saffaripour S, Wagner DD. Procoagulant state resulting from high levels of soluble P-selectin in blood. Proc Natl Acad Sci USA 2000; 97: 13835-40.
  CrossrefPubMedGoogle Scholar
• 121 Palabrica T, Lobb R, Furie BC, Aronovitz M, Benjamin C, Hsu Y-M, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992; 359: 848-51.
  CrossrefPubMedGoogle Scholar
• 122 Subramaniam M, Frenette PS, Saffaripour S, Johnson RC, Hynes RO, Wagner DD. Defects in hemostasis in P-selectin-deficient mice. Blood 1996; 87: 1238-42.
  PubMedGoogle Scholar
• 123 Wakefield TW, Strieter RM, Downing LJ, Kadell AM, Wilke CA, Burdick MD, Wrobleski SK, Phillips ML, Paulson JC, Anderson DC, Greenfield LJ. P-selectin and TNF inhibition reduce venous thrombosis inflammation. J Surg Res 1996; 64: 26-31.
  CrossrefPubMedGoogle Scholar
• 124 Downing LJ, Wakefield TW, Strieter RM, Prince MR, Londy FJ, Fowlkes JB, Hulin MS, Kadell AM, Wilke CA, Brown SL, Wrobleski SK, Burdick MD, Anderson DC, Greenfield LJ. Anti-P-selectin antibody decreases inflammation and thrombus formation in venous thrombosis. J Vasc Surg 1997; 25: 816-27.
  CrossrefPubMedGoogle Scholar
• 125 Eppihimer MJ, Schaub RG. P-selectin-dependent inhibition of thrombosis during venous stasis. Arterioscler Thromb Vasc Biol 2000; 20: 2483-8.
  CrossrefPubMedGoogle Scholar
• 126 Toombs CF, DeGraaf CL, Martin JP, Geng JG, Anderson DC, Shebuski RJ. Pretreatment with a blocking monoclonal antibody to P-selectin accelerates pharmacological thrombolysis in a primate model of arterial thrombosis. J Pharmacol Exp Ther 1995; 275: 941-9.
  PubMedGoogle Scholar
• 127 Kumar A, Villani MP, Patel UK, Keith Jr JC, Schaub RG. Recombinant soluble form of PSGL-1 accelerates thrombolysis and prevents reocclusion in a porcine model. Circulation 1999; 99: 1363-9.
  CrossrefPubMedGoogle Scholar
• 128 Ikeda H, Ueyama T, Murahara T, Yasukawa H, Haramaki N, Eguchi H, Katoh A, Takajo Y, Onitsuka I, Ueno T, Tojo SJ, Imaizumi T. Adhesive interaction between P-selectin and sialyl Lewis^x plays an important role in recurrent coronary arterial thrombosis in dogs. Arterioscler Thromb Vasc Biol 1999; 19: 1083-90.
  CrossrefPubMedGoogle Scholar
• 129 Zoldhelyi P, Beck PJ, Bjercke RJ, Ober JC, Hu X, McNatt JM, Akhtar S, Ahmed M, Clubb Jr FJ, Chen ZQ, Dixon RAF, Yeh ETH, Willerson JT. Inhibition of coronary thrombosis and local inflammation by a noncarbohydrate selectin inhibitor. Am J Physiol Heart Circ Physiol 2000; 279: H3065-H3075.
  CrossrefPubMedGoogle Scholar
• 130 Giesen PL, Rauch U, Bohrmann B, Kling D, Roque M, Fallon JT, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 1999; 96: 2311-5.
  CrossrefPubMedGoogle Scholar
• 131 Rauch U, Bonderman D, Bohrmann B, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000; 96: 170-5.
  PubMedGoogle Scholar
• 132 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 Natl Acad Sci USA 1994; 91: 8767-71.
  CrossrefPubMedGoogle Scholar
• 133 Bach R, Rifkin DB. Expression of tissue factor procoagulant activity: regulation by cytosolic calcium. Proc Natl Acad Sci USA 1990; 87: 6995-9.
  CrossrefPubMedGoogle Scholar
• 134 Lindmark E, Tenno T, Siegbahn A. Role of platelet P-selectin and CD40 ligand in the induction of monocytic tissue factor expression. Arterioscler Thromb Vasc Biol 2000; 20: 2322-8.
  CrossrefPubMedGoogle Scholar
• 135 Lorant DE, Patel KD, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA. Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: A juxtacrine system for adhesion and activation of neutrophils. J Cell Biol 1991; 115: 223-34.
  CrossrefPubMedGoogle Scholar
• 136 Hartwell DM, Mayadas TN, Berger G, Frenette PS, Rayburn H, Hynes RO, Wagner DD. Role of P-selectin cytoplasmic domain in granular targeting in vivo and in early inflammatory responses. J Cell Biol 1998; 143: 1129-41.
  CrossrefPubMedGoogle Scholar
• 137 Ishiwata N, Takio K, Katayama M, Watanabe K, Titani K, Ikeda Y, Handa M. Alternatively spliced isoform of P-selectin is present in vivo as a soluble molecule. J Biol Chem 1994; 269: 23708-15.
  PubMedGoogle Scholar
• 138 Michelson AD, Barnard MR, Hechtman HB, MacGregor H, Connolly RJ, Loscalzo J, Valeri CR. In vivo tracking of platelets: circulating degranulated platelets rapidly lose surface P-selectin but continue to circulate and function. Proc Natl Acad Sci USA 1996; 93: 11877-82.
  CrossrefPubMedGoogle Scholar
• 139 Chong BH, Murray B, Berndt MC, Dunlop LC, Brighton T, Chesterman CN. Plasma P-selectin is increased in thrombotic consumptive platelet disorders. Blood 1994; 83: 1535-41.
  PubMedGoogle Scholar
• 140 Blann AD, Lip GY. Cell adhesion molecules in cardiovascular disease and its risk factors – what can soluble levels tell us? [editorial; comment]. J Clin Endocrinol Metab 2000; 85: 1745-7.
  PubMedGoogle Scholar
• 141 Abrams CS, Ellison N, Budzynski AZ, Shattil SJ. Direct detection of activated platelets and platelet-derived microparticles in humans. Blood 1990; 75: 128-38.
  PubMedGoogle Scholar
• 142 Mann KG. Biochemistry and physiology of blood coagulation. Thromb Haemost 1999; 82: 165-74.
  Article in Thieme ConnectPubMedGoogle Scholar
• 143 Ross R. Atherosclerosis – an inflammatory disease [see comments]. N Engl J Med 1999; 340: 115-26.
  CrossrefPubMedGoogle Scholar
• 144 Dong ZM, Chapman SM, Brown AA, Frenette PS, Hynes RO, Wagner DD. Combined role of P- and E-selectins in atherosclerosis. J Clin Invest 1998; 102: 145-52.
  CrossrefPubMedGoogle Scholar
• 145 Dong ZM, Brown AA, Wagner DD. Prominent role of P-selectin in the development of advanced atherosclerosis in apoE-deficient mice. Circulation 2000; 101: 2290-5.
  CrossrefPubMedGoogle Scholar
• 146 Collins RG, Velji R, Guevara NV, Hicks MJ, Chan L, Beaudet AL. P-selectin or intercellular adhesion molecule (ICAM)-1 deficiency substantially protects against atherosclerosis in apolipoprotein E-deficient mice. J Exp Med 2000; 191: 189-94.
  CrossrefPubMedGoogle Scholar
• 147 Manka D, Collins R, Ley K, Beaudet AL, Sarembock IJ. Absence of P-selectin, but not ICAM-1, attenuates neointimal growth after arterial injury in apolipoprotein-E-deficient mice. Circulation 2001; 103: 1000-5.
  CrossrefPubMedGoogle Scholar
• 148 Simon DI, Dhen Z, Seifert P, Edelman ER, Ballantyne CM, Rogers C. Decreased neointimal formation in Mac-1(-/-) mice reveals a role for inflammation in vascular repair after angioplasty. J Clin Invest 2000; 105: 293-300.
  CrossrefPubMedGoogle Scholar