Thromb Haemost 2008; 99(05): 909-915
DOI: 10.1160/TH08-01-0030
Blood Coagulation, Fibrinolysis and Cellular Haemostasis
Schattauer GmbH

Microparticle-associated vascular adhesion molecule-1 and tissue factor follow a circadian rhythm in healthy human subjects

Leigh A. Madden
1   Postgraduate Medical Institute, University of Hull, Hull, UK
,
Rebecca V. Vince
1   Postgraduate Medical Institute, University of Hull, Hull, UK
,
Marie E. Sandström
2   Department of Sport, Health and Exercise Science, University of Hull, Hull, UK
,
Lee Taylor
2   Department of Sport, Health and Exercise Science, University of Hull, Hull, UK
,
Lars McNaughton
2   Department of Sport, Health and Exercise Science, University of Hull, Hull, UK
,
Gerard Laden
3   Hyperbaric Unit, Hull and East Riding Hospital, Anlaby, Hull, UK
› Author Affiliations
Further Information

Publication History

Received 14 January 2008

Accepted after major revision 23 March 2008

Publication Date:
30 November 2017 (online)

Summary

An increased risk of death or severe injury due to late-morning thrombotic events is well established. Tissue factor (TF) is the initiator of the coagulation cascade, and endothelial stresses, coupled with production of pro-coagulant microparticles (MP) are also important factors in loss of haemostasis. TF and vascular cell adhesion molecule-1 (VCAM-1) -positive cell microparticles were assessed periodically over a 24-hour (h) period in healthy human subjects to ascertain if they followed a circadian rhythm. Eleven healthy male subjects were assessed in a temperature-controlled environment with dietary intake consistent between subjects. Blood samples were taken every 4 h by venipuncture, and TF and VCAM-1 positive microparticles were quantified by flow cytometry. A significant circadian rhythm was observed in VCAM-1 MP (p=<0.0001), and a trend was shown, although not statistically significant (p=0.065) in TF microparticles. A peak was observed at 9 a.m. for VCAM-1 positive MP, followed by a decrease and subsequent peak at 9 p.m. and a minimum at 5 a.m. TF-positive MP followed a strikingly similar trend in both variation and absolute numbers with a delay. A circadian rhythm was observed in VCAM-1 and less so TF-positive MP. This has significant implications in terms of the well known increased risk of cardiovascular thrombotic events matching this data. To our knowledge this is the first such report of quantified measurements of these MP over a 24-h period and the only measurement of a 24-h variation of in-vivo blood-borne TF.

 
  • References

  • 1 ISIS-2 Collaborative Group.. Randomised trial of intravenous streptokinase, oral aspirin, both or neither among 17 187 cases of suspected acute myocardial infarction. Lancet II. 1988: g349-360.
  • 2 Bridges AB, Fisher TC, Scott N. et al. Circadianrhythm of white blood-cell aggregation and free-radical status in healthy-volunteers. Free Radical Res Comm 1992; 16: 89-97.
  • 3 Bridges AB, McLaren M, Saniabadi A. et al. Circadian variation of endothelial-cell function, red-bloodcell deformability and dehydro-thromboxane-b2 in healthy-volunteers. Blood Coag Fibrinol 1991; 2: 447-452.
  • 4 Muller JE, Stone PH, Turi ZG. et al. circadian variation in the frequency of onset of acute myocardial-infarction. N Engl J Med 1985; 313: 1315-1322.
  • 5 Ridker PM, Manson JE, Buring JE. et al. circadian variation of acute myocardial-infarction and the effect of low-dose aspirin in a randomized trial of physicians. Circulation 1990; 82: 897-902.
  • 6 Hjalmarson A, Gilpin EA, Nicod P. et al. Differing circadian patterns of symptom onset in subgroups of patients with acute myocardial-infarction. Circulation 1989; 80: 267-275.
  • 7 Kapiotis S, Jilma B, Quehenberger P. et al. Morning hypercoagulability and hypofibrinolysis – Diurnal variations in circulating activated factor VII, prothrombin fragment F1+2, and plasmin-plasmin inhibitor complex. Circulation 1997; 96: 19-21.
  • 8 Kloner RA, Poole WK, Perritt RL. When throughout the year is coronary death most likely to occur? A 12-year population-based analysis of more than 220 000 cases. Circulation 1999; 100: 1630-1634.
  • 9 Otto ME, Svatikova A, Barretto RBD, Santos S, Hoffmann M, Khandheria B, Somers V. Early morning attenuation of endothelial function in healthy humans. Circulation. 2004: 2507-2510.
  • 10 Ley K, Huo YQ. VCAM-1 is critical in atherosclerosis. J Clin Invest 2001; 107: 1209-1210.
  • 11 Morel O, Toti F, Hugel B, Bakouboula B, Camoin-Jau L, Dignat-George F, Freyssinet JM. Procoagulant microparticles – Disrupting the vascular homeostasis equation?. Arterioscler Thromb Vasc Biol 2006; 26: 2594-2604.
  • 12 Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol 1967; 13: 269-288.
  • 13 Combes V, Simon AC, Grau GE. et al. In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J Clin Invest 1999; 104: 93-102.
  • 14 Omoto S, Nomura S, Shouzu A, Nishikawa M, Fukuhara S, Iwasaka T. Detection of monocyte-derived microparticles in patients with Type II diabetes mellitus. Diabetologia 2002; 45: 550-555.
  • 15 Pattanapanyasat K, Noulsri E, Fucharoen S. et al. Flow cytometric quantitation of red blood cell vesicles in thalassemia. Clin Cytometry 2004; 57B: 23-31.
  • 16 Horstman LL, Jy W, Jimenez JJ. et al. Endothelial microparticles as markers of endothelial dysfunction. Front Biosci 2004; 9: 1118-1135.
  • 17 Jimenez JJ, Jy W, Mauro LM. et al. Endothelial microparticles (EMP) as vascular disease markers. Adv Clin Chem 2005; 39: 131-157.
  • 18 Osterud B, Bjorklid E. Blood borne tissue factor (including microparticles). ten Cate H, Levi M. Molecular mechanisms of disseminated intravascular coagulation Eurekah.com 2003
  • 19 Semeraro N, Colucci M. Endothelial cell pertubation and disseminated intravascular coagulation. ten Cate H, Levi M. Molecular mechanisms of disseminated intravascular coagulation. Eurekah.com 2003
  • 20 Banner DW, Darcy A, Chene C. et al. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 1996; 380: 41-46.
  • 21 Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human-tissues – implications for disorders of hemostasis and thrombosis. Am J Pathol 1989; 134: 1087-1097.
  • 22 Sabatier F, Roux V, Anfosso F, Camoin L, Sampol J, Dignat-George F. Interaction of endothelial microparticles with monocytic cells in vitro induces tissue factor- dependent procoagulant activity. Blood 2002; 99: 3962-3970.
  • 23 Jimenez JJ, Jy W, Mauro LM, Horstman LL, Soderland C, Ahn YS. Endothelial microparticles released in thrombotic thrombocytopenic purpura express von Willebrand factor and markers of endothelial activation. Br J Haematol 2003; 123: 896-902.
  • 24 R Development Core Team. R: A language and environment for statistical computing.. R Foundation for Statistical Computing; Vienna, Austria.: ISBN 3–900051–07–0. 2007
  • 25 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: 170-175.
  • 26 Nieuwland R, Berckmans RJ, RotteveelEijkman RC. et al. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 1997; 96: 3534-3541.
  • 27 del Conde I, Shrimpton CN, Thiagarajan P. et al. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 2005; 106: 1604-1611.
  • 28 Szotowski B, Antoniak S, Poller W. et al. Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res 2005; 96: 1233-1239.
  • 29 Jafri SM, Vanrollins M, Ozawa T. et al. Circadian Variation in platelet-function in healthy-volunteers. Am J Cardiol 1992; 69: 951-954.
  • 30 Soulban G, Labrecque G, Barbeau G. Time-dependent variations in the coagulation-factor-II, coagulation- factor-VII, coagulation-factor-IX, and coagulation- factor-X in young and elderly volunteers. Chronobiol Int 1995; 12: 206-213.
  • 31 Pinotti M, Bertolucci C, Portaluppi F. et al. Daily and circadian rhythms of tissue factor pathway inhibitor and factor VII activity. Arterioscler Thromb Vasc Biol 2005; 25: 646-649.
  • 32 Elherik K, Khan F, McLaren M. et al. Circadian variation in vascular tone and endothelial cell function in normal males. Clin Sci 2002; 102: 547-552.
  • 33 Morel O, Hugel B, Jesel L. et al. Circulating procoagulant microparticles and soluble GPV in myocardial infarction treated by primary percutaneous transluminal coronary angioplasty. A possible role for GPIIb-IIIa antagonists. J Thromb Haem 2004; 2: 1118-1126.
  • 34 Preston RA, Jy W, Jimenez JJ. et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003; 41: 211-217.
  • 35 Millarcraig MW, Bishop CN, Raftery EB. Circadian variation of blood-pressure. Lancet 1978; 1: 795-797.
  • 36 Maple C, Kirk G, McLaren M. et al. A circadian variation exists for soluble levels of intercellular adhesion molecule-1 and E-selectin in healthy volunteers. Clin Sci 1998; 94: 537-540.
  • 37 Mosevold KA, Bruserud O. Circadian variations do not have a major impact on serum levels of soluble (s) L-selectin (CD63L), s-intercellular adhesion molecule 1 (sICAM-1/CD54) and thrombopoietin in healthy individuals. Scand J Clin Lab Invest 2002; 62: 75-79.
  • 38 Hwang SJ, Ballantyne CM, Sharrett AR. et al. Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases – The atherosclerosis risk in communities (ARIC) study. Circulation 1997; 96: 4219-4225.
  • 39 Menown IBA, Mathew TP, Gracey HM. et al. Prediction of recurrent events by D-dimer and inflammatory markers in patients with normal cardiac troponin I (PREDICT) study. Am Heart J 2003; 145: 986-992.
  • 40 Pradhan AD, Rifai N, Ridker PM. Soluble intercellular adhesion molecule-1, soluble vascular adhesion molecule-1, and the development of symptomatic peripheral arterial disease in men. Circulation 2002; 106: 820-825.
  • 41 Stenvinkel P, Lindholm B, Heimburger M. et al. Elevated serum levels of soluble adhesion molecules predict death in pre-dialysis patients: association, vith malnutrition, inflammation, and cardiovascular disease. Nephrol Dial Trans 2000; 15: 1624-1630.
  • 42 Ridker PM, Hennekens CH, Roitman-Johnson B. et al. Plasma concentration of soluble intercellular adhesion molecule 1 and risks of future myocardial infarction in apparently healthy men. Lancet 1998; 351: 88-92.
  • 43 Distler JHW, Huber LC, Hueber AJ, Reich CF, Gay S, Distler O, Pisetsky DS. The release of microparticles by apoptotic cells and their effects on macrophages. Apoptosis 2005; 10: 731-741.
  • 44 Jy WC, Mao WW, Horstman LL. et al. Platelet microparticles bind, activate and aggregate neutrophils in vitro. Blood Cells Molecules Dis 1995; 21: 217-231.
  • 45 Semaan HB, Gurbel PA, Anderson JL, Muhlestein JB, Carlquist JF, Horne BD, Serebruany VL. Soluble VCAM-1 and E-selectin, but not ICAM-1 discriminate endothelial injury in patients with documented coronary artery disease. Cardiology 2000; 93: 7-10.
  • 46 Jy W, Hortsman LL, Jiminez JJ. et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1842-1843.
  • 47 Biro E, Nieuwland R, Sturk A. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1843-1844.
  • 48 Dignat-George F, Sabatier F, Camoin-Jau L. et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1844-1845.
  • 49 Hugel B, Zobari F, Freyssinet J-M. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1846-1847.
  • 50 Nomura S. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1847-1848.
  • 51 Shet AS, Key NS, Hebbel RP. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1848-1850.
  • 52 Jiminez JJ, Jy W, Hortsman LL. et al. Measuring circulating cell-derived microparticles. J Thromb Haemost 2004; 2: 1850-1851.
  • 53 Shah MD, Bergeron A, Dong J. et al. Measuring microparticles: Pitfalls and modifications. J Thromb Haemost 2007; 5 (Suppl. 02) P-M-443.
  • 54 Shermata WA, Jy W, Delgado S. et al. Interferon- β1a reduces plasma CD31+ endothelial microparticles (CD31+EMP) in multiple sclerosis. J Neuroinflam 2006; 3: 23-27.
  • 55 Ungvari Z, Wolin MS, Csiszar A. Mechanosensitive production of reactive oxygen species in endothelial and smooth muscle cells: role in microvascular remodeling?. Antiox Redox Signal 2006; 8: 1121-1129.
  • 56 Lehoux S, Castier Y, Tedgui A. Molecular mechanisms of the vascular response to haemodynamic forces. J Internal Med 2006; 259: 381-392.