Thromb Haemost 2002; 88(05): 843-850
DOI: 10.1055/s-0037-1613312
Review Article
Schattauer GmbH

F11-Receptor (F11R/JAM) Mediates Platelet Adhesion to Endothelial Cells: Role in Inflammatory Thrombosis[*]

Anna Babinska
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
,
Mamdouh H. Kedees**
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
,
Humra Athar**
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
,
Tahir Ahmed
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
,
Olcay Batuman
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
,
Yigal H. Ehrlich
1   Program in Neuroscience, Department of Biology, CSI/City University of New York, Staten Island, NY, USA
,
M. Mahmood Hussain
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
,
Elizabeth Kornecki
2   Department of Anatomy/Cell Biology, State University of New York, Downstate Medical Center, Brooklyn, NY, USA
› Author Affiliations
Further Information

Publication History

Received 08 April 2002

Accepted after revision 15 July 2002

Publication Date:
08 December 2017 (online)

Summary

The F11 receptor (F11R) is a cell adhesion molecule (CAM), member of the immunoglobulin superfamily found on the surface of human platelets, and determined to play a role in platelet aggregation, secretion, adhesion and spreading. The same molecule is present also at tight junctions of endothelial cells (EC) where it is known as JAM and acts as a CAM through homophilic interactions. The role of F11R/JAM in the interaction of platelets with endothelial cells was investigated in the current studies. We report here that washed human platelets adhere specifically to a matrix made of immobilized, recombinant sF11R. Furthermore, platelets adhere to cytokine(TNF-α, INF-γ) stimulated human umbilical vein endothelial cells (HUVEC), and approximately 40-60% of the adhesive force is exerted by homophilic interactions between the F11R of platelets and EC. This is evidenced by the inhibition of platelet adhesion to endothelial cells by recombinant soluble form of the F11R, and by two F11R peptides with amino acid sequences of the N-terminal region, and in the 1st Ig fold of the F11R, respectively. This study suggests a role for F11R in the adhesion of platelets to cytokine-inflamed endothelial cells and thus in thrombosis and atherosclerosis induced in non-denuded blood vessels by inflammatory processes. Agents that block the F11R-mediated adhesion of platelets to EC may be of therapeutic value in controlling thrombosis and preventing heart attacks and stroke.

* Part of this work was presented as symposium at the XVIIIth ISTH, July, Paris, France, 2001), and in abstract form (Abstract number: PSY942) in the Supplement to the journal Thrombosis and Haemostasis (see ref. 32)


** M. H. Kedees and H. Athar contributed equally to this work.


 
  • References

  • 1 Karsan A, Harlan JM. The Blood Vessel Wall. In: Hematology: Basic Principles and Practice. 3rd Ed.. Hoffman R, Benz EJ, Shattil SJ, Furie B, Cohen HJ, Silberstein LE, McGlave P. 2000: 1770-82.
  • 2 Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt A-M, Stern DM. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998; 91: 3527-61.
  • 3 May AE, Neumann FJ, Preissner KT. The relevance of blood cell-vessel wall adhesive interactions for vascular thrombotic disease. Thromb Haemost 1999; 82: 962-70.
  • 4 Diquelou A, Dupoy D, Gaspin D, Constans J, Sie P, Boneu B, Sakariassen KS, Cadroy Y. Relationship between endothelial tissue factor and thrombogenesis under blood flow conditions. Thromb Haemost 1995; 74: 778-83.
  • 5 Dardik R, Varon D, Eskaraev R, Tamarin I, Inbal A. Recombinant fragment of von Willebrand factor AR545C inhibits platelet binding to thrombin and platelet adhesion to thrombin-treated endothelial cells. Br J Haematol 2000; 109: 512-8.
  • 6 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 stimulated veins. Blood 2000; 96: 3322-8.
  • 7 Rosenblum WI, Nelson GH, Wornley B, Werner P, Wang J, Shih C. Role of platelet-endothelial cell adhesion molecule (PECAM) in platelet adhesion/aggregation over injured but not denuded endothelium in vivo and ex vivo. Stroke 1995; 27: 709-11.
  • 8 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 I (ICAM-1), αvβ3 integrin, and GPIbα. J Exp Med 1998; 187: 329-39.
  • 9 Verheul HMW, Joma AS, Hoekman K, Broxterman HJ, Gebbink MFBG, Pinedo HM. Vascular endothelial growth factor-stimulated endothelial cells promote adhesion and activation of platelets. Blood 2000; 96: 4216-21.
  • 10 Kornecki E, Walkowiak B, Naik UP, Ehrlich YH. Activation of human platelets by a stimulatory monoclonal antibody. J Biol Chem 1990; 265: 10042-8.
  • 11 Naik UP, Ehrlich YH, Kornecki E. Mechanisms of platelet activation by a stimulatory antibody: cross-linking of a novel platelet receptor for M.Ab.F11 with the FcγRII receptor. Biochem J 1995; 311: 155-62.
  • 12 Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142: 117-27.
  • 13 Kornecki E, Cooper BA, Ehrlich YH. Identification of a unique type of thrombopathy of human platelets: defect in the exposure of active fibrinogen receptors in a patient with Friedreich’s ataxia. J Lab Clin Med 1988; 111: 618-26.
  • 14 Wang F, Naik UP, Ehrlich YH, Osada S-I, Ohno S, Kornecki E. Stimulatory antibody-induced activation and selective translocation of protein kinase C isoenzymes in human platelets. Biochem J 1995; 311: 401-6.
  • 15 Kornecki E, Naik UP, Sobocka M, Ehrlich YH. Mechanisms of stimulation and inhibition of platelet activation by monoclonal antibodies. In: Leu-cocyte VTyping, Schlossman SF. et al Oxford: Oxford University Press; 1995: 1241-3.
  • 16 Sobocka M, Sobocki T, Banerjee P, Kornecki E. Molecular mechanisms of platelet activation by a stimulatory monoclonal antibody, cloning and potential pathophysiological roles for a novel platelet receptor. Blood. 1997 90. No. 10 Supplement 1, Part 2, November 15, 2996a..
  • 17 Sobocka MB. Molecular cloning and characterization of a novel Ig superfamily member from human platelets. PhD Thesis, 1998. SUNY Downstate; Brooklyn, NY: Presented June 10, 1998; published Sept. 15, 1998..
  • 18 Sobocka MB, Sobocki T, Banerjee P, Weiss C, Rushbrook JI, Norin AJ, Hartwig J, Salifu M, Markell MS, Babinska A, Ehrlich YH, Kornecki E. Cloning of the human platelet F11 receptor: a cell adhesion molecule member of the immunoglobulin superfamily involved in platelet aggregation. Blood 2000; 95: 2600-9.
  • 19 Babinska A, Kedees MH, Athar H, Sobocki T, Sobocka MB, Ahmed T, Ehrlich YH, Hussain MM, Kornecki E. Two regions of the human platelet F11-Receptor (F11R) are critical for platelet aggregation, potentiation and adhesion. Throm Haemost 2002; 87: 712-21.
  • 20 Ozaki H, Ishii K, Horiuchi H, Arai H, Kawamoto T, Okawa K, Iwamatsu A, Kita T. Combined treatment of TNF-α and INF-γ causes redistribution of junctional adhesion molecule in human endothelial cells. J Immunol 1999; 163: 553-7.
  • 21 Williams LA, Martin-Padura I, Dejana E, Hogg N, Simmons DL. Identification and characterization of human Junctional Adhesion Molecule (JAM). Mol Immunol 1999; 36: 1175-88.
  • 22 Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Pochet M, Parkos CA. Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Science 2000; 113: 2363-74.
  • 23 Gupta SK, Pillarisetti K, Ohlstein EH. Platelet agonist F11 receptor is a member of the immunoglobulin superfamily and identical with junctional adhesion molecule (JAM): regulation of expression in human endothelial cells and macrophages. IUBMB Life 2000; 50: 51-6.
  • 24 Naik UP, Naik MU, Eckfeld K, Martin-Deleon P, Spychala J. Characterization and chromosomal localization of JAM-1, a platelet receptor for a stimulatory monoclonal antibody. J Cell Sci 2001; 114: 539-47.
  • 25 Sobocka MB, Sobock T, Babinska J, Ehrlich YH, Kornecki E. F11 receptor-mediated potentiation of platelet activation by subthreshold concentrations of physiological agonists. XVIII ISTH Congress, July, 2001; Paris, France: Abs. # P1902. (manuscript in preparation).
  • 26 Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: A laboratory manual. 2nd ed.,. Cold Spring Harbor Laboratory, Cold Spring Harbor; New York: 1989
  • 27 Tuszynski GP, Murphy A. Spectrophotometric quantitation of anchoragedependent cell numbers using the bicinchoninic acid protein assay reagent. Anal Biochem 1990; 184: 189-91.
  • 28 Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. J Clin Invest 1973; 52: 2745-56.
  • 29 Johnson AR. Human pulmonary endothelial cells in culture: activities of cells from arteries and veins. J Clin Invest 65: 841-50.
  • 30 Kostrewa D, Brockhaus M, D’Arcy AD, Dale GE, Nelboeck P, Schmid G, Mueller F, Bazzoni G, Dejana E, Bartfai T, Winkler FK, Hennig M. X-ray structure of junctional adhesion molecule: structural basis for homophilic adhesion via a novel dimerization motif. The EMBO Journal 2001; 20: 4391-8.
  • 31 Sobocki T. Genomic organization of human F11R/JAM and identification of two types of mRNAs regulated by alternative promoters. SUNY Downstate; Brooklyn, NY: PhD Thesis 2001..
  • 32 Kornecki E, Babinska A, Kedees MH, Athar H, Hussain M, Sobocka M, Sobocki T, Rushbrook J, Banerjee P, Hogan MV, Ehrlich YH. F11R: A novel receptor of the immunoglobulin superfamily involved in the adhesion and aggregation of human platelets. Thromb Haemost. 2001 Abs. SY942..
  • 33 Marcus AJ, Broekman MJ, Drosopoulos JHF, Islam N, Alyonyocycheva TN, Safier LB, Hajjar KA, Posnett DN, Schoenborn MA, Schooley KA, Gayle RB, Maliszewski CR. The endothelial cell ecto-ADPase responsible for inhibition of platelet function is CD39. J Clin Invest 1997; 99: 1351-60.
  • 34 Mendelsohn ME, O’Neill S, George D, Loscalzo J. Inhibition of fibrinogen binding to human platelets by S-nitroso-N-acetylcysteine. J Biol Chem 1990; 265: 19028-34.
  • 35 Michelson AD, Benoit SE, Furman MI, Breckwoldt WL, Rohrer MJ, Barnard MR, Loscalzo J. Effects of endothelium-derived relaxin factor/ nitric oxide on platelet surface glycoproteins. Am J Physiol 1996; 39: H1640-8.
  • 36 Frenette PS, Johnson RC, Hynes RO, Wagner DD. Platelets roll on stimulated endothelium in vivo: an interaction mediated by endothelial P-selectin. PNAS 1995; 92: 7450-4.
  • 37 Frenette PS, Moyna C, Hartwell DW, Lowe JB, Hynes RO, Wagner DD. Platelet endothelial interactions in inflamed mesenteric venules. Blood 1998; 91: 1318-23.
  • 38 Frenette PS, Denis CV, Weiss L, Hynes RO, 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.
  • 39 Sun J, Williams J, Yan H-C, Amin KM, Albelda SM, DeLisser HM, Newman PJ. Individually distinct Ig homology domains in PECAM-1 regulate homophilic binding and modulate receptor affinity. J Biol Chem 1996; 271: 11090-8.
  • 40 Gurubhagavatula I, Amrani Y, Practico D, Ruberg L, Albelda SM, Panettieri RA. Engagement of human PECAM-1 (CD31) on human endothelial cells increases intracellular calcium ion concentration and stimulates prostacyclin release. J Clin Invest 1998; 101: 212-22.
  • 41 Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, Lopez JA. The glycoprotein Ib-IX-V complex is a platelet counterpart for P-selectin. J Exp Med 1999; 190: 803-13.
  • 42 Ostermann G, Weber KSC, Zernecke A, Schröder A, Weber C. JAM-1 is a ligand of the β2 integrin LFA-1 involved in transendothelial migration of leukocytes. Nature Immunology 2002; 03: 151-8.
  • 43 Kornecki EH, Ehrlich YH. United States Patent number 5,665,701, issued Sep. 9, 1997.