Formation of tissue factor-bearing leukocytes during and after cardiopulmonary bypass

Aya Shibamiya; Noriyuki Tabuchi; Jihwa Chung; Makoto Sunamori; Takatoshi Koyama

doi:10.1160/TH03-12-0787

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2004; 92(01): 124-131
DOI: 10.1160/TH03-12-0787

Platelets and Blood Cells

Schattauer GmbH

Formation of tissue factor-bearing leukocytes during and after cardiopulmonary bypass

Aya Shibamiya

¹Graduate School of Health Sciences, Tokyo Medical and Dental University, Tokyo, Japan

,

Noriyuki Tabuchi

²Graduate School of Medicine, Division of Thoracic-Cardiovascular Surgery, Tokyo Medical and Dental University, Tokyo, Japan

,

Jihwa Chung

¹Graduate School of Health Sciences, Tokyo Medical and Dental University, Tokyo, Japan

,

Makoto Sunamori

²Graduate School of Medicine, Division of Thoracic-Cardiovascular Surgery, Tokyo Medical and Dental University, Tokyo, Japan

,

Takatoshi Koyama

¹Graduate School of Health Sciences, Tokyo Medical and Dental University, Tokyo, Japan

› Author Affiliations

Abstract

Summary

During cardiopulmonary bypass (CPB), the extrinsic coagulation system initiated by tissue factor (TF) is a major procoagulant stimulus. TF is present in surgical wounds and could be expressed on activated monocytes. However, recent studies have suggested that collagen stimulation rapidly induces TF by leukocyte-platelet complex formation. Therefore, the appearance of TF-bearing leukocytes and their effect on promoting coagulation were investigated in 5 patients undergoing coronary bypass surgery. Neutrophils and monocytes positive for CD41a and TF increased abruptly in circulating blood during CPB. Their increase was most prominent in blood pooled in the pericardial cavity. Monocytes, but not neutrophils positive for TF showed a second peak one day after operation, which accords with the increase in TF mRNA levels in leukocytes. Similarly, an increase in leukocytes positive for TF accords with the activated factor X generation assay using isolated leukocytes, and with an increase in thrombin-antithrombin complex in circulating blood. The second increase in TF-positive monocytes seems to be responsible for these coagulation parameters that remained high one day after operation. After 10 min of blood incubation stimulated by collagen in vitro, simulating activation in the pericardial cavity, significant increases in neutrophils and monocytes positive for TF and platelet were observed. Our present study suggested the involvement of two distinct mechanisms for the appearance of TF-bearing leukocytes responsible for promoting coagulation: the quick appearance being partly explained by the formation of leukocyte-platelet complex that occurs mainly in the pericardial cavity, and the slow appearance via transcriptional activation in monocytes.

Keywords

Tissue factor (TF) - cardiopulmonary bypass (CPB) - leukocytes - platelet

Full Text

References

References
1 Philippou H, Adami A, Davidson SJ. et al. Tissue factor is rapidly elevated in plasma collected from the pericardial cavity during cardiopulmonary bypass. Thromb Haemost 2000; 84: 124-8.
2 Spanier TB, Chen JM, Oz MC. et al. Selective anticoagulation with active site-blocked factor IXA suggests separate roles for intrinsic and extrinsic coagulation pathways in cardiopulmonary bypass. J Thorac Cardiovasc Surg 1998; 116: 860-9.
3 Tabuchi N, de Haan J, Boonstra PW. et al. Activation of fibrinolysis in the pericardial cavity during cardiopulmonary bypass. J Thorac Cardiovasc Surg 1993; 106: 828-33.
4 Ernofsson M, Thelin S, Siegbahn A. Monocyte tissue factor expression, cell activation, and thrombin formation during cardiopulmonary bypass: a clinical study. J Thorac Cardiovasc Surg 1997; 113: 576-84.
5 Engelmann B, Luther T, Müller I. Intravascular tissue factor pathway – a model for rapid initiation of coagulation within the blood vessel. Thromb Haemost 2003; 89: 3-8.
6 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.
7 Scholz T, Temmler U, Krause S. et al. Transfer of tissue factor from platelets to monocytes: role of platelet-derived microvesicles and CD62P. Thromb Haemost 2002; 88: 1033-8.
8 Zillmann A, Luther T, Müller I. et al. Plateletassociated tissue factor contributes to the collagen-triggered activation of blood coagulation. Biochem Biophys Res Commun 2001; 281: 603-9.
9 Koyama T, Shibakura M, Ohsawa M. et al. Anticoagulant effects of 1α,25-dihydroxyvitamin D₃ on human myelogenous leukemia cells and monocytes. Blood 1998; 92: 160-7.
10 Kozek-Langenecker SA, Spiss CK, Michalek-Sauberer A. et al. Effect of prostacyclin on platelets, polymorphonuclear cells, and heterotypic cell aggregation during hemofiltration. Crit Care Med 2003; 31: 864-8.
11 Ogura H, Kawasaki T, Tanaka H. et al. Activated platelets enhance microparticle formation and platelet-leukocyte interaction in severe trauma and sepsis. J Trauma 2001; 50: 801-9.
12 Bunescu A, Widman J, Lenkei R. et al. Increases in circulating levels of monocyteplatelet and neutrophil-platelet complexes following hip arthroplasty. Clin Sci 2002; 102: 279-86.
13 Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC. et al. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 1997; 96: 3534-41.
14 Sturk-Maquelin KN, Nieuwland R, Romijn FP. et al. Pro- and non-coagulant forms of non-cell-bound tissue factor in vivo . J Thromb Haemost 2003; 01: 1920-6.
15 Koyama T, Nishida K, Ohdama S. et al. Determination of plasma tissue factor antigen and its clinical significance. Br J Haematol 1994; 87: 343-7.
16 Misumi K, Ogawa H, Yasue H. et al. Comparison of plasma tissue factor levels in unstable and stable angina pectoris. Am J Cardiol 1998; 81: 22-6.
17 Rauch U, Bonderman D, Bohrmann B. et al. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood 2000; 96: 170-5.
18 Brisset AC, Terrisse AD, Dupouy D. et al. Shedding of active tissue factor by aortic smooth muscle cells (SMCs) undergoing apoptosis. Thromb Haemost 2003; 90: 511-8.
19 Tabuchi N, Shibamiya A, Koyama T. et al. Activated leukocytes adsorbed on the surface of an extracorporeal circuit. Artif Organs 2003; 27: 591-4.
20 Morgan EN, Pohlman TH, Vocelka C. et al. Nuclear factor κB medaiates a procoagulant response in monocytes during extracorporeal circulation. J Thorac Cardiovasc Surg 2003; 125: 165-71.
21 Ohsawa M, Koyama T, Yamamoto K. et al. 1α,25-dihydroxyvitamin D₃ and ist potent synthetic analogs downregulate tissue factor and upregulate thrombomodulin expression in monocytic cells, counteracting the effects of tumor necrosis factor and oxidized LDL. Circulation 2000; 102: 2867-72.
22 Lindmark E, Wallentin L, Siegbahn A. Blood cell activation, coagulation, and inflammation in men and women with coronary artery disease. Thromb Res 2001; 103: 249-59.
23 Arefieva TI, Provatorov SI, Samko AN. et al. Monocyte integrin expression and monocyteplatelet complex formation in humans with coronary restenosis. Clin Exp Pharmacol Physiol 2001; 28: 804-8.
24 Parolari A, Colli S, Mussoni L. et al. Coagulation and fibrinolytic markers in a twomonth follow-up of coronary bypass surgery. J Thorac Cardiovasc Surg 2003; 125: 336-43.