Thromb Haemost 2002; 87(03): 477-482
DOI: 10.1055/s-0037-1613028
Review Article
Schattauer GmbH

Factor VII Activation, Apolipoprotein A-I and Reverse Cholesterol Transport: Possible Relevance for Postprandial Lipaemia

G. J. Miller
1   MRC Epidemiology and Medical Care Unit, Wolfson Institute of Preventive Medicine, London, UK
,
C. J. Cooke
2   Department of Cardiovascular Biochemistry, St Bartholomew’s and Royal London School of Medicine and Dentistry, London, UK
,
M. N. Nanjee
2   Department of Cardiovascular Biochemistry, St Bartholomew’s and Royal London School of Medicine and Dentistry, London, UK
,
D. J. Howarth
1   MRC Epidemiology and Medical Care Unit, Wolfson Institute of Preventive Medicine, London, UK
,
J. A. Cooper
1   MRC Epidemiology and Medical Care Unit, Wolfson Institute of Preventive Medicine, London, UK
,
I. P. Stepanova
2   Department of Cardiovascular Biochemistry, St Bartholomew’s and Royal London School of Medicine and Dentistry, London, UK
,
J. H. Morrissey
3   Department of Biochemistry, University of Illinois College of Medicine, Urbana, IL, USA
,
N. E. Miller
2   Department of Cardiovascular Biochemistry, St Bartholomew’s and Royal London School of Medicine and Dentistry, London, UK
› Author Affiliations
Further Information

Publication History

Received 24 July 2001

Accepted after resubmission 05 December 2001

Publication Date:
14 December 2017 (online)

Summary

Postprandial lipaemia is associated with activation of factor VII (FVII) and efflux of cholesterol from tissues to nascent plasma high density lipoproteins (HDL) containing apolipoprotein A-I (apo A-I). To determine whether FVII activation and cholesterol efflux occur together in other situations, the responses to intravenous infusion of HDL-like apo A-I/phosphatidylcholine discs were measured in 10 healthy men. Disc infusion (40 mg apo A-I/kg body weight) over 4 h was followed by increases in HDL cholesteryl ester and plasma apo A-I (p <0.0001). Significant activation of FVII was apparent during infusion in fasting subjects (p = 0.03), activated FVII averaging 123% of baseline value by 12 h (p <0.0001). Plasma thrombin-antithrombin (TAT) complex increased to 156% of baseline level by 12 h (p >0.05) but individual responses differed considerably. Peak TAT post-infusion was associated inversely with peak HDL triglyceride concentration (p = 0.004). The coagulation responses to disc-infusion may be due to transfer of phosphatidylserine to cell surfaces during cholesterol efflux.

 
  • References

  • 1 Miller GJ, Martin JC, Mitropoulos KA, Reeves BEA, Thompson RL, Meade TW, Cooper JA, Cruickshank JK. Plasma factor VII is activated by postprandial triglyceridaemia, irrespective of dietary fat composition. Atherosclerosis 1991; 86: 163-71.
  • 2 Marckmann P, Sandstrom B, Jespersen J. Dietary effects on circadian fluctuation in human blood coagulation factor VII and fibrinolysis. Atherosclerosis 1993; 101: 225-34.
  • 3 Mitropoulos KA, Miller GJ, Watts GF, Durrington PN. Lipolysis of triglyceride-rich lipoproteins activates coagulant factor XII: a study in familial lipoprotein-lipase deficiency. Atherosclerosis 1992; 95: 119-25.
  • 4 Miller GJ, Martin JC, Webster J, Wilkes H, Miller NE, Wilkinson WH, Meade TW. Association between dietary fat intake and plasma factor VII activity – a predictor of cardiovascular mortality. Atherosclerosis 1986; 60: 269-77.
  • 5 Marckmann P, Raben A, Astrup A. Ad libitum intake of low-fat diets rich in either starchy foods or sucrose: effects on blood lipids, factor VII coagulant activity, and fibrinogen. Metabolism 2000; 49: 731-6.
  • 6 Ghadder HM, Folsom AR, Aleksic N, Hearne LB, Chambless LE, Morrissey JH, Wu KK. Correlation of factor VIIa values with factor VII gene polymorphism, fasting and postprandial triglyceride levels, and subclinical carotid atherosclerosis. Circulation 1998; 98: 2815-21.
  • 7 Wright D, Poller L, Thomson JM, Gowland E, Burrows GE. The inter-relationship of factor VII and its activity state with plasma lipids in healthy male adults. Br J Haematol 1993; 85: 348-51.
  • 8 Negri M, Arigliano PL, Talamini G, Carlini S, Manzato F, Bonadonna G. Levels of plasma factor VII and factor VII activated forms as a function of plasma triglyceride levels. Atherosclerosis 1993; 99: 55-61.
  • 9 Constantino M, Merskey C, Kudzma DJ, Zucker MB. Increased activity of vitamin K-dependent clotting factors in human hyperlipoproteinaemia – association with cholesterol and triglyceride levels. Thromb Haemost 1977; 38: 465-74.
  • 10 Havel RJ, Kane JP, Kashyap ML. Interchange of apolipoproteins between chylomicrons and high density lipoproteins during alimentary lipemia in man. J Clin Invest 1973; 52: 32-8.
  • 11 Schaefer EJ, Jenkins LL, Brewer B. Human chylomicron apolipoprotein metabolism. Biochem Biophys Res Commun 1978; 80: 405-12.
  • 12 Lasell TS, Guérin M, Auboiron S, Chapman MJ, Guy-Grand B. Preferential cholesteryl ester acceptors among triglyceride-rich lipoproteins during alimentary lipemia in normolipidemic subjects. Arterioscler Thromb Vasc Biol 1998; 18: 65-74.
  • 13 Miller NE. Is cholesterol efflux from tissues regulated by lipolysis of triglyceride-rich lipoproteins?. In: High density lipoproteins and atherosclerosis III. Miller NE, Tall AR; London, Excerpta Medica: 1992: 191-7.
  • 14 Oram JF, Yokoyama S. Apolipoprotein-mediated removal of cellular cholesterol and phospholipids. J Lipid Res 1996; 37: 2473-91.
  • 15 Orso E, Broccardo C, Kaminski WE, Bottcher A, Liebisch G, Drobnik W, Gotz A, Chambenoit O, Diederich W, Langmann T, Spruss T, Luciani MF, Rothe G, Lackner KJ, Chimini G, Schmitz G. Transport of lipids from Golgi to plasma membrane is defective in Tangier disease patients and Abc1-deficient mice. Nat Genet 2000; 24: 192-6.
  • 16 Francis GA, Tsujita M, Terry TL. Apolipoprotein AI efficiently binds to and mediates cholesterol and phospholipid efflux from human but not rat aortic smooth muscle cells. Biochemistry 1999; 38: 16315-22.
  • 17 Bodzioch M, Orso E, Klucken J, Lanmann T, Bottcher A, Diederich W, Drobnik W, Barlage S, Buchler C, Porsch-Ozcurumez M, Kaminski WE, Hahmann HW, Oette K, Rothe G, Aslanidis C, Lackner KJ, Schmitz G. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier Disease. Nat Genet 1999; 22: 347-51.
  • 18 Fielding CJ, Fielding PE. Molecular physiology of reverse cholesterol transport. J Lipid Res 1995; 36: 211-28.
  • 19 Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 1996; 271: 518-20.
  • 20 Schroit AJ, Zwaal RFA. Transbilayer movement of phospholipids in red cell and platelet membranes. Biochim Biophys Acta 1991; 1071: 313-29.
  • 21 Pei G, Powers DD, Lentz BR. Specific contribution of different phospholipid surfaces to the activation of prothrombin by the fully assembled prothrombinase. J Biol Chem 1993; 268: 3226-33.
  • 22 Bach R, Gentry R, Nemerson Y. Factor VII binding to tissue factor in reconstituted phospholipids: induction of cooperativity by phosphatidylserine. Biochemistry 1986; 25: 4007-20.
  • 23 Hamon Y, Broccardo C, Chambenoit O, Luciani M-F, Toti F, Chaslin S, Freyssinet J-M, Devaux PF, McNeish J, Marguet D, Chimini G. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2000; 02: 399-406.
  • 24 Stern D, Nawroth P, Handley D, Kisiel W. An endothelial cell-dependent pathway of coagulation. Proc Natl Acad Sci USA 1985; 82: 2523-7.
  • 25 Xu N, Dahlback B, Ohlin A-K, Nilsson A. Presence of vitamin K-dependent coagulation proteins in isolated triglyceride-rich lipoproteins of human plasma. Prostaglandins, Leukotrienes and Essential Fatty Acids 1997; 57: 395-7.
  • 26 Nelsestuen GL, Kisiel W, Di Scipio RG. Interaction of vitamin K dependent proteins with membranes. Biochemistry 1978; 17: 2134-8.
  • 27 Neuenschwander PF, Fiore MM, Morrissey JH. Factor VII autoactivation proceeds via interaction of distinct protease-cofactor and zymogen-cofactor complexes. J Biol Chem 1993; 268: 21489-92.
  • 28 Kjalke M, Silveira A, Hamsten A, Hedner U, Ezban M. Plasma lipoproteins enhance tissue factor-independent factor VII activation. Arterioscler Thromb Vasc Biol 2000; 20: 1835-41.
  • 29 Van Dieijen G, van Rijn JL, Govers-Riemslag JW, Hemker HC, Rosing J. Assembly of the intrinsic factor X activating complex-interactions between factor IXa, factor VIIIa and phospholipid. Thromb Haemost 1985; 53: 396-400.
  • 30 Gilbert GE, Arena AA. Phosphatidylethanolamine induces high affinity binding sites for factor VIII on membranes containing phosphatidyl-Lserine. J Biol Chem 1995; 270: 18500-5.
  • 31 Neuenschwander PF, Bianco-Fisher E, Rezaie AR, Morrissey JH. Phosphatidylethanolamine augments factor VIIa-tissue factor activity: enhancement of sensitivity to phosphatidylserine. Biochemistry 1995; 34: 13988-93.
  • 32 Falls LA, Furie B, Furie BC. Role of phosphatidylethanolamine in assembly and function of the factor IXa-factor VIIIa complex on membrane surfaces. Biochemistry 2000; 39: 13216-22.
  • 33 Castro GR, Fielding CJ. Effects of postprandial lipemia on plasma cholesterol metabolism. J Clin Invest 1985; 75: 874-82.
  • 34 Miller NE, Nanjee MN. Evidence that reverse cholesterol transport is stimulated by lipolysis of triglyceride-rich lipoproteins. FEBS Letters 1991; 285: 132-4.
  • 35 Seligsohn U, Osterud B, Brown SF, Griffin JH, Rapaport SI. Activation of human factor VII in plasma and purified systems. Roles of activated factor IX, kallikrein, and activated factor VII. J Clin Invest 1979; 64: 1056-65.
  • 36 Miller GJ, Martin JC, Mitropoulos KA, Esnouf MP, Cooper JA, Morrissey JH, Howarth DJ, Tuddenham EGD. Activation of factor VII during alimentary lipemia occurs in healthy adults and patients with congenital factor XII or factor XI deficiency, but not in patients with factor IX deficiency. Blood 1996; 87: 4187-96.
  • 37 Silveira A, Karpe F, Johnsson H, Bauer KA, Hamsten A. In vivo demonstration in humans that large postprandial triglyceride-rich lipoproteins activate coagulation factor VII through the intrinsic coagulation pathway. Arterioscler Thromb Vasc Biol 1996; 16: 1333-9.
  • 38 Masys DR, Bajaj SP, Rapaport SI. Activation of human factor VII by activated factors IX and X. Blood 1982; 60: 1143-50.
  • 39 Lerch PG, Fortsch V, Hodler G, Bolli R. Production and characterization of a reconstituted high density lipoprotein for therapeutic applications. Vox Sang 1996; 71: 155-64.
  • 40 Nanjee MN, Miller NE. Sequential microenzymatic assay of cholesterol, triglycerides, and phospholipids in a single aliquot. Clin Chem 1996; 42: 915-26.
  • 41 Demacker PNM, Hijmans AGM, Vos-Janssen HE, Van’t Laar A, Jansen AP. A study of the use of polyethylene glycol in estimating cholesterol in high-density lipoprotein. Clin Chem 1980; 26: 1775-9.
  • 42 Nanjee MN, Crouse JR, King JM, Hovorka R, Rees SE, Carson ER, Morgenthaler JJ, Lerch P, Miller NE. Effects of intravenous infusion of lipid-free apoA-I in humans. Arterioscler Thromb Vasc Biol 1996; 16: 1203-14.
  • 43 Morrissey JH, Macik BG, Neuenschwander PF, Comp PC. Quantitation of activated factor VII levels in plasma using a tissue factor mutant selectively deficient in promoting factor VII activation. Blood 1993; 81: 734-44.
  • 44 Nanjee MN, Doran JE, Lerch PG, Miller NE. Acute effects of intravenous infusion of apo A1/phosphatidycholine discs on plasma lipoproteins in humans. Arterioscler Thromb Vasc Biol 1999; 19: 979-89.
  • 45 Lerch PG, Moudry R, Doran JE, Hubsch A, Omar A, Morgenthaler JJ, Isliker H, Heiniger HJ. In vitro characteristics of reconstituted HDL for therapy. Proceedings of European Lipoprotein Club. Bruges, Belgium; European Lipoprotein Club: 1992. Abstract.
  • 46 Nanjee MN, Cooke CJ, Garvin R, Lewis G, Olszewski WL, Miller NE. Is plasma high density lipoprotein concentration rate limiting for reverse cholesterol transport in humans in vivo?. Circulation 1999; 100: 1-813 (Abstract).
  • 47 Seligsohn U, Kasper CK, Osterud B, Rapaport SI. Activated factor VII: presence in factor IX concentrates and persistence in the circulation after infusion. Blood 1979; 53: 828-37.
  • 48 Issemann I, Prince RA, Tugwood JD, Green S. The peroxisome proliferator-activated receptor: retinoid X receptor heterodimer is activated by fatty acids and fibrate hypolipidaemic drugs. J Mol Endocrinol 1993; 11: 37-47.
  • 49 Chinetti G, Lestavel S, Bocher V, Remaley AT, Neve B, Torra IP, Teissier E, Minnich A, Jaye M, Duverger N, Brewer HB, Fruchart J-C, Clavey V, Staels B. PPAR-α and PPAR-γ activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat Med 2001; 07: 53-8.
  • 50 Mitropoulos KA, Reeves BEA, Miller GJ. The activation of factor VII in citrated plasma by charged long-chain saturated fatty acids at the interface of large triglyceride-rich lipoproteins. Blood Coag Fibrinol 1993; 04: 943-51.
  • 51 Deguchi H, Fernandez JA, Hackeng TM, Banka CL, Griffin JH. Cardiolipin is a normal component of human plasma lipoproteins. Proc Nat Acad Sci USA 2000; 97: 1743-8.
  • 52 Mariani G, Bernardi F, Bertina R, Garcia VV, Prydz H, Samama M, Sandset PM, Di Nucci GD, Testa MG, Bendz B, Chiarotti F, Ciarla MV, Strom R. Serum phospholipids are the main environmental determinants of activated factor VII in the most common FVII genotype. Haematologica 1999; 84: 620-6.
  • 53 Hunter KA, Crosbie LC, Weir A, Miller GJ, Dutta-Roy AK. The effects of structurally defined triglycerides of differing fatty acid composition on postprandial haemostasis in young healthy men. Atherosclerosis 1999; 142: 151-8.
  • 54 Bladbjerg EM, Munster A-M, Marckmann P, Keller N, Jespersen J. Dietary factor VII activation does not increase plasma concentrations of prothrombin fragment 1+2 in patients with stable angina pectoris and coronary atherosclerosis. Arterioscler Thromb Vasc Biol 2000; 20: 2494-9.
  • 55 Bakker HM, Tans G, Janssen-Claessen T, Thomassen MCLGD, Hemker HC, Griffin JH, Rosing J. The effect of phospholipids, calcium ions and protein S on rate constants of human factor Va inactivation by activated human protein C. Eur J Biochem 1992; 208: 171-8.
  • 56 Horie S, Ishii H, Hara H, Kazama M. Enhancement of thrombin-thrombomodulin-catalysed protein C activation by phosphatidylethanolamine containing unsaturated fatty acids: possible physiological significance of phosphatidylethanolamine in anticoagulant activity of thrombomodulin. Biochem J 1994; 301: 683-91.