A Monoclonal Antibody to Platelet Type III Collagen-binding Protein (TIIICBP) Binds to Blood and Vascular Cells, and Inhibits Platelet Vessel-wall Interactions

Emmanuel Monnet; Hilde Depraetere; Chantal Legrand; Hans Deckmyn; Françoise Fauvel-Lafève

doi:10.1055/s-0037-1616106

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2001; 86(02): 694-701
DOI: 10.1055/s-0037-1616106

Review Article

Schattauer GmbH

A Monoclonal Antibody to Platelet Type III Collagen-binding Protein (TIIICBP) Binds to Blood and Vascular Cells, and Inhibits Platelet Vessel-wall Interactions

Emmanuel Monnet

¹U553 INSERM, Hémostase, Endothélium et Angiogénèse, Institut d’Hématologie, Université Paris VII-Denis Diderot, Hôpital Saint-Louis, Paris, France

,

Hilde Depraetere

²Laboratory for Thrombosis Research, IRC, KU Leuven Campus Kortrijk, Kortrijk, Belgium

,

Chantal Legrand

¹U553 INSERM, Hémostase, Endothélium et Angiogénèse, Institut d’Hématologie, Université Paris VII-Denis Diderot, Hôpital Saint-Louis, Paris, France

,

Hans Deckmyn

²Laboratory for Thrombosis Research, IRC, KU Leuven Campus Kortrijk, Kortrijk, Belgium

,

Françoise Fauvel-Lafève

¹U553 INSERM, Hémostase, Endothélium et Angiogénèse, Institut d’Hématologie, Université Paris VII-Denis Diderot, Hôpital Saint-Louis, Paris, France

› Author Affiliations

Abstract

Summary

TIIICBP is a new platelet receptor involved in platelet-type III collagen and platelet-subendothelium interactions. This receptor is composed of a doublet of 72-68 kDa proteins. In this study, the major protein (68 kDa) was purified and used to produce monoclonal antibodies. One of these antibodies, 7F4, binds to platelets as confirmed by flow cytometry. 7F4 inhibited platelet contact, spreading and aggregation induced by type III collagen. Under flow conditions, 7F4 prevented platelet interactions with type III collagen, endothelial cell matrix and the KOGEOGPK type III collagen octapeptide: the specific sequence recognized by TIIICBP. On the other hand, 7F4 had no effect on platelet-type I collagen interactions. TIIICBP was also detected on lymphocytes, granulocytes and monocytes. TIIICBP was expressed on endothelial cells and fibroblasts but not on smooth-muscle cells. These results show that TIIICBP is expressed on several cell types and participates in cell adhesion to the subendothelium.

Keywords

Collagen receptor - platelet adhesion - subendothelium - type III collagen - leukocytes

Full Text

References

References
1 Moroi M, Jung SM. Platelet receptors for collagen. Thromb Haemost 1997; 77: 439-44.
2 Santoro SA. Identification of a 160,000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell 1986; 46: 913-20.
3 Tandon NN, Kralisz U, Jamieson GJ. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion. J Biol Chem 1989; 264: 7576-83.
4 Chiang TM, Rinaldy A, Kang AH. Cloning, characterization, and functional studies of a non-integrin platelet receptor for type I collagen. J Clin Invest 1997; 100: 514-21.
5 Clemetson JM, Polgar J, Magnenat E, Wells TNC, Clemetson KJ. The platelet collagen receptor glycoprotein VI is a member of the immunoglobulin superfamily closely related to FcγR and the natural killer receptors. J Biol Chem 1999; 274: 29019-24.
6 Kehrel B, Wierwille S, Clemetson KJ, Anders O, Steiner M, Knight CG, Farndale RW, Okuma M, Barnes MJ. Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD 36, glycoprotein IIb/IIIa and von Willebrand factor do not. Blood 1998; 91: 491-9.
7 Tsuji M, Ezumi Y, Arai M, Takayama H. A novel association of Fc receptor γ-chain with glycoprotein VI and their co-expression as a collagen receptor in human platelets. J Biol Chem 1997; 272: 23528-31.
8 Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest 1989; 84: 1440-5.
9 Staatz WD, Fok KF, Zutter MM, Adams SP, Rodriguez BA, Santoro SA. Identification of a tetrapeptide recognition sequence for the α₂β₁ integrin in collagen. J Biol Chem 1991; 266: 7363-7.
10 Morton LF, Peachey AR, Zijenah LZ, Goodall AH, Humphries MJ, Barnes MJ. Conformation-dependent platelet adhesion to collagen involving integrin α₂β₁-mediated and other mechanisms: multiple α₂β₁-recognition sites in collagen type I. Biochem J 1994; 299: 791-7.
11 Morton LF, Peachey AR, Knight CG, Farndale RW, Barnes MJ. The platelet reactivity of synthetic peptides based on the collagen III fragment α₁(III)CB4. Am Soc Biochem Mol Biol 1997; 272: 11044-8.
12 Verkleij MW, Ijsseldijk MJW, Heijnen-Snyder GJ, Hulzinga EG, Morton LF, Knight CG, Sixma JJ, de Groot PG, Barnes MJ. Adhesive domains in the collagen III fragment α₁(III)CB4 that support α₂β₁- and von Willebrand factor-mediated platelet adhesion under flow conditions. Thromb Haemost 1999; 82: 1137-44.
13 Monnet E, Sizaret PY, Arbeille B, Fauvel-Lafève F. Different role of platelet glycoprotein GP Ia/IIa in platelet adhesion and activation induced by type I and type III collagens. Thromb Res 2000; 98: 423-33.
14 Asselin J, Gibbins JM, Achison M, Han Lee Y, Morton LF, Farndale RW, Barnes MJ, Watson SP. A collagen-like peptide stimulates tyrosine phosphorylation of syk and phospholipase Cγ2 in platelets independent of the integrin (α₂β₁ . Blood 1997; 89: 1235-42.
15 Jung SM, Moroi M. Signal-transducing mechanisms involved in activation of the platelet collagen receptor integrin α₂β₁ . J Biol Chem 2000; 275: 8016-26.
16 Kehrel B, Kronenberg A, Rauterberg J, Niesing-Bresch D, Niehues U, Kardoeus J, Schwippert B, Tschope D, van de Loo J, Clemetson KJ. Platelets deficient in glycoprotein IIIb aggregate normally to collagens type I and III but not to collagen type V. Blood 1993; 82: 3364-70.
17 Chiang TM, Seyer JM, Kang A. Collagen-platelet interaction: separate receptor sites for types I and III collagen. Thromb Res 1993; 71: 443-56.
18 Monnet E, Fauvel-Lafève F. A new platelet receptor specific to type III collagen. J Biol Chem. 2000; 275: 10912-17.
19 Fauvel F, Legrand YJ, Kuhn K, Bentz H, Fietzek PP, Caen JP. Platelet adhesion to type III collagen: involvement of a sequence of nine aminoacids from α₁(III)CB4 peptide. Thromb Res 1979; 16: 259-65.
20 Fauvel F, Legrand YJ. Inhibition of type III collagen induced platelet aggregation by active α₁(III)CB4 peptide fragments. Thromb Res 1980; 17: 285-7.
21 Karniguian A, Legrand YJ, Lefrancier P, Caen JP. Effect of a collagen derived octapeptide on different steps of platelet-collagen interaction. Thromb Res 1983; 32: 593-604.
22 Karniguian A, Rendu F, Grelac F, Lebret M, Legrand YJ. Effect of a collagen-derived octapeptide on phosphoinositide turnover and 43KD protein phosphorylation in collagen-activated platelets. Biochem Biophys Res Commun 1987; 146: 277-83.
23 Laemmli UK. Cleavage of the structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-5.
24 Kohler G, Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 1975; 256: 495-7.
25 Cauwenberghs N, Meiring M, Vauterin S, van Wyk V, Lamprecht S, Roodts JP, Novak L, Harsfalvi J, Deckmyn H, Kotze HF. Antithrombotic effect of platelet glycoprotein Ib-blocking monoclonal antibody Fab-fragments in nonhuman primates. Arterioscler Thromb Vasc Biol. 2000; 20: 1347-53.
26 Huet C. Purification of Immunoglobulins in Cell Biology: A Laboratory Handbook. San Diego, CA: Academic Press; 1994
27 Shattil SJ, Hoxie JA, Cunningham M, Brass LF. Changes in the platelet membrane glycoprotein IIb/IIIa complex during platelet activation. J Biol Chem 1985; 260: 11107-12.
28 Fauvel-Lafève F, Meric A, Arbeille B, Tabaka V, Legrand YJ. Spectrophotometric evaluation of the adhesion of blood platelets to collagen and microfibrils. Thromb Res 1993; 71: 193-204.
29 Bellavite P, Andrioli G, Guzzo P, Arigliano P, Chirumbolo S, Manzato F, Santonastaso C. A Colorimetric method for the measurement of platelet adhesion in microtiter plates. Anal Biochem 1994; 216: 444-50.
30 Sakariassen KS, Aarts PAMM, de Groot PG, Houdijk WPM, Sixma JJ. A perfusion chamber developed to investigate platelet interaction in flowing blood with human vessel wall cells, their extracellular matrix and purified components. J Lab Clin Med. 1983; 102: 522-35.
31 Fauvel F, Legrand YJ, Kuhn K, Bentz H, Fietzek PP, Caen JP. Platelet-collagen interaction: adhesion of human blood platelets to purified (CB4) peptide from type III collagen. Thromb Res 1978; 12: 841-50.
32 Pischel KD, Hemler ME, Huang C, Bluestein HG, Woods Jr VL. Use of the monoclonal antibody 12F1 to characterize the differentiation epitope VLA-2. J Immunol. 1987; 138: 226-32.
33 Coller BS, Beer JH, Scudder LE, Steinberg MH. Collagen-platelet interactions: evidence for direct interaction of collagen with platelet GPIa/IIa and an indirect interaction with platelet GPIIb/IIIa mediated by adhesive proteins. Blood 1989; 74: 182-92.
34 Kunicki TJ, Orchekowski R, Annis D, Honda Y. Variability of integrin α₂β₁ activity on human platelets. Blood 1993; 82: 2693-703.
35 Peterson DM, Stathopoulos NA, Giorgio TD, Hellums JD, Moake JL. Shear-induced platelet aggregation requires von Willebrand factor and platelet membrane glycoproteins Ib and IIb/IIIa. Blood 1987; 69: 625-8.
36 Fauvel-Lafève F. Microfibrils from the arterial subendothelium. Int Rev Cytol 1999; 188: 1-40.
37 Sixma JJ, van Zanten GH, Banga JD, Nieuwenhuis HK, de Groot PG. Platelet adhesion. Semin Hematol 1995; 32: 1-12.
38 Arencibia I, Sundqvist KG. Collagen receptor on T lymphocytes and the control of lymphocyte motility. Eur J Immunol 1989; 19: 929-34.
39 Roberts AI, Brolin RE, Ebert EC. Integrin alpha1beta1(VLA1) mediates adhesion of activated intraepithelial lymphocytes to collagen. Immunology 1999; 97: 679-85.
40 Goldman R, Harvey J, Hogg N. VLA-2 is the integrin used as a collagen receptor by leukocytes. Eur J Immunol 1992; 22: 1109-14.
41 Miyake S, Sakurai T, Okumura K, Yagita H. Identification of collagen and laminin receptor integrins on murine T lymphocytes. Eur J Immunol 1994; 24: 2000-5.
42 Walzog B, Schuppan D, Heimpel C, Hafezi-Moghadam A, Gaehtgens P, Ley K. The leukocyte integrin Mac-1 (CD11b/CD18) contributes to binding of human granulocytes to collagen. Exp Cell Res 1995; 218: 28-38.
43 Postlethwaite AE, Kang AH. Collagen-and collagen peptide-induced chemotaxis of human blood monocytes. J Exp Med 1976; 143: 1299-1307.
44 Newman SL, Tucci MA. Regulation of human monocyte/macrophage function by extracellular matrix. Adherence of monocytes to collagen matrices enhances phagocytosis of opsonized bacteria by activation of complement receptors and enhancement of Fc receptor function. J Clin Invest 1990; 86: 703-14.
45 Wesley 2nd RB, Meng X, Godin D, Galis ZS. Extracellular matrix modulates macrophage functions characteristic to atheroma: collagen type I enhances acquisition of resident macrophage traits by human peripheral blood monocytes in vitro. Arterioscler Thromb Vasc Biol 1998; 18: 432-40.
46 Bateman JF, Lamandé SR, Ramshaw JAM. Collagen superfamily. In Extracellular Matrix. Vol 2. Comper WD. (ed). Amsterdam: Harwood Academic; 1996: 22-67.
47 Mayne R. Collagenous proteins of blood vessels. Arteriosclerosis 1986; 6: 585-92.