Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T02:44:57.110Z Has data issue: false hasContentIssue false
  • English
  • Français

Erythrocyte–Platelet Interaction in Uncomplicated Pregnancy

Published online by Cambridge University Press:  03 December 2014

Albe C. Swanepoel  and
Etheresia Pretorius
Albe C. Swanepoel
Affiliation:
Department of Physiology, School of Medicine, Faculty of Health Sciences, University of Pretoria, Private Bag x323; Arcadia 0007, South Africa
Etheresia Pretorius*
Affiliation:
Department of Physiology, School of Medicine, Faculty of Health Sciences, University of Pretoria, Private Bag x323; Arcadia 0007, South Africa
*
*Corresponding author. [email protected]
Get access

Abstract

Maternal and fetal requirements during uncomplicated pregnancy are associated with changes in the hematopoietic system. Platelets and erythrocytes [red blood cells (RBCs)], and especially their membranes, are involved in coagulation, and their interactions may provide reasons for the changed hematopoietic system during uncomplicated pregnancy. We review literature regarding RBC and platelet membrane structure and interactions during hypercoagulability and hormonal changes. We then study interactions between RBCs and platelets in uncomplicated pregnancy, as their interactions may be one of the reasons for increased hypercoagulability during uncomplicated pregnancy. Scanning electron microscopy was used to study whole blood smears from 90 pregnant females in different phases of pregnancy. Pregnancy-specific interaction was seen between RBCs and platelets. Typically, one or more platelets interacted through platelet spreading and pseudopodia formation with a single RBC. However, multiple interactions with RBCs were also shown for a single platelet. Specific RBC–platelet interaction seen during uncomplicated pregnancy may be caused by increased estrogen and/or increased fibrinogen concentrations. This interaction may contribute to the hypercoagulable state associated with healthy and uncomplicated pregnancy and may also play a fundamental role in gestational thrombocytopenia.

Keywords

uncomplicated pregnancyerythrocytesplateletsscanning electron microscopy
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 20 , Issue 6 , December 2014 , pp. 1848 - 1860
Copyright
© Microscopy Society of America 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, R., Schachtrup, C., Davalos, D., Tsigelny, I. & Akassoglou, K. (2007). Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: Lessons from multiple sclerosis. Curr Med Chem 14(27), 2925–2936.CrossRefGoogle ScholarPubMed
Aleman, M.M., Walton, B.L., Byrnes, J.R. & Wolberg, A.S. (2014). Fibrinogen and red blood cells in venous thrombosis. Thromb Res 133(Suppl 1), S38–S40.CrossRefGoogle ScholarPubMed
Allen, R.D., Zacharski, L.R., Widirstky, S.T., Rosenstein, R., Zaitlin, L.M. & Burgess, D.R. (1979). Transformation and motility of human platelets: Details of the shape change and release reaction observed by optical and electron microscopy. J Cell Biol 83(1), 126–142.Google Scholar
Angiolillo, D.J., Capodanno, D. & Goto, S. (2009). Platelet thrombin receptor antagonism and atherothrombosis. Eur Heart J 31 17–28.CrossRefGoogle ScholarPubMed
Aslan, J.E. & McCarty, O.J. (2013). Rho GTPases in platelet function. J Thromb Haemost 11(1), 35–46.Google Scholar
Baines, A.J., Bennett, P.M., Carter, E.W. & Terracciano, C. (2009). Protein 4.1 and the control of ion channels. Blood Cells Mol Dis 42(3), 211–215.Google Scholar
Barkalow, K.L., Italiano, J.E. Jr., Chou, D.E., Matsuoka, Y., Bennett, V. & Hartwig, J.H. (2003). Alpha-adducin dissociates from F-actin and spectrin during platelet activation. J Cell Biol 161(3), 557–570.Google Scholar
Beller, F. (1994). Cardiovascular system: Coagulation, thrombosis, and contraceptive steroids – is there a link. In Pharmacology of the Contraceptive Steroids, JW Goldzieher (Ed.), pp. 309–332. New York, NY: Raven Press.Google Scholar
Bennett, V. & Healy, J. (2009). Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb Perspect Biol 1(6), a003012.Google Scholar
Berliner, A., Shapira, I., Rogowski, O., Sadees, N., Rotstein, R., Fusman, R., Avitzour, D., Cohen, S., Arber, N. & Zeltser, D. (2000). Combined leukocyte and erythrocyte aggregation in the peripheral venous blood during sepsis. An indication of commonly shared adhesive protein(s). Int J Clin Lab Res 30(1), 27–31.Google Scholar
Berndt, M.C., Metharom, P. & Andrews, R.K. (2014). Primary haemostasis: Newer insights. Haemophilia 20(Suppl 4), 15–22.CrossRefGoogle ScholarPubMed
Bleijerveld, O.B., van Holten, T.C., Preisinger, C., van der Smagt, J.J., Farndale, R.W., Kleefstra, T., Willemsen, M.H., Urbanus, R.T., de Groot, P.G., Heck, A.J., Roest, M. & Scholten, A. (2013). Targeted phosphotyrosine profiling of glycoprotein VI signaling implicates oligophrenin-1 in platelet filopodia formation. Arterioscler Thromb Vasc Biol 33(7), 1538–1543.Google Scholar
Bollini, A., Hernández, G., Luna, M.B., Cinara, L. & Rasia, M. (2005). Study of intrinsic flow properties at the normal pregnancy second trimester. Clin Hemorheol Microcirc 33(2), 155–161.Google ScholarPubMed
Burke, N., Flood, K., Murray, A., Cotter, B., Dempsey, M., Fay, L., Dicker, P., Geary, M.P., Kenny, D. & Malone, F.D. (2013). Platelet reactivity changes significantly throughout all trimesters of pregnancy compared with the nonpregnant state: A prospective study. BJOG 120(13), 1599–1604.Google Scholar
Burton, N.M. & Bruce, L.J. (2011). Modelling the structure of the red cell membrane. Biochem Cell Biol 89(2), 200–215.CrossRefGoogle ScholarPubMed
Carquin, M., Pollet, H., Veiga-da-Cunha, M., Cominelli, A., Van Der Smissen, P., N’Kuli, F., Emonard, H., Henriet, P., Mizuno, H., Courtoy, P.J. & Tyteca, D. (2014). Endogenous sphingomyelin segregates into submicrometric domains in the living erythrocyte membrane. J Lipid Res 55(7), 1331–1342.Google Scholar
Carvalho, F.A., Connell, S., Miltenberger-Miltenyi, G., Pereira, S.V., Tavares, A., Ariëns, R.A. & Santos, N.C. (2010). Atomic force microscopy-based molecular recognition of a fibrinogen receptor on human erythrocytes. ACS Nano 4(8), 4609–4620.Google Scholar
Cenni, E., Stea, S., Cervellati, M., Pizzoferrato, A. & Montanaro, L. (2000). Quantitative evaluation by image analysis of platelet morphological modifications after contact with polyvinylacetate. Minerva Cardioangiol 48(1–2), 1–8.Google ScholarPubMed
Chan, W.S., Rey, E., Kent, N.E., Chan, W.S., Kent, N.E., Rey, E., Corbett, T., David, M., Douglas, M.J., Gibson, P.S., Magee, L., Rodger, M. & Smith, R.E. (2014). Venous thromboembolism and antithrombotic therapy in pregnancy. J Obstet Gynaecol Can 36(6), 527–553.CrossRefGoogle ScholarPubMed
Cimmino, G. & Golino, P. (2013). Platelet biology and receptor pathways. J Cardiovasc Transl Res 6(3), 299–309.Google Scholar
Comeglio, P., Fedi, S., Liotta, A.A., Cellai, A.P., Chiarantini, E., Prisco, D., Mecacci, F., Parretti, E., Mello, G. & Abbate, R. (1996). Blood clotting activation during normal pregnancy. Thromb Res 84(3), 199–202.Google Scholar
Cunha, S.R. & Mohler, P.J. (2009). Ankyrin protein networks in membrane formation and stabilization. J Cell Mol Med 13(11–12), 4364–4376.Google Scholar
Czogalla, A. & Sikorski, A.F. (2010). Do we already know how spectrin attracts ankyrin? Cell Mol Life Sci 67(16), 2679–2683.Google Scholar
Davis, L.H., Otto, E. & Bennett, V. (1991). Specific 33-residue repeat(s) of erythrocyte ankyrin associate with the anion exchanger. J Biol Chem 266(17), 11163–11169.Google Scholar
Diz-Kucukkaya, R. & Lopez, J.A. (2013). Inherited disorders of platelets: Membrane glycoprotein disorders. Hematol Oncol Clin North Am 27(3), 613–627.CrossRefGoogle ScholarPubMed
Dyson, J.M., Munday, A.D., Kong, A.M., Huysmans, R.D., Matzaris, M., Layton, M.J., Nandurkar, H.H., Berndt, M.C. & Mitchell, C.A. (2003). SHIP-2 forms a tetrameric complex with filamin, actin, and GPIb-IX-V: Localization of SHIP-2 to the activated platelet actin cytoskeleton. Blood 102(3), 940–948.Google Scholar
Eyre, L. & Gamlin, F. (2010). Haemostasis, blood platelets and coagulation. Anaesth Intensive Care Med 11(6), 244–246.CrossRefGoogle Scholar
Fehily, A.M., Dickerson, J.W., Meade, B.W. & Ellis, F.R. (1982). Plasma and erythrocyte membrane fatty acids in oral contraceptive users. Clin Chim Acta 120(1), 41–47.Google Scholar
Ferru, E., Giger, K., Pantaleo, A., Campanella, E., Grey, J., Ritchie, K., Vono, R., Turrini, F. & Low, P.S. (2011). Regulation of membrane-cytoskeletal interactions by tyrosine phosphorylation of erythrocyte band 3. Blood 117(22), 5998–6006.Google Scholar
Gafarova, M.E., Rykova, S.Y., Khokhlova, M.D., Lubin, E.V., Skryabina, M.V., Fedyanin, A.A. & Sokolova, I.A. (2012). Red blood cell (dis)aggregation: Effect of inhibition of fibrinogen binding. Ser Biomechan 27(3–4), 69–73.Google Scholar
Galambosi, P.J., Ulander, V.M. & Kaaja, R.J. (2014). The incidence and risk factors of recurrent venous thromboembolism during pregnancy. Thromb Res 134(2), 240–245.Google Scholar
Girasole, M., Dinarelli, S. & Boumis, G. (2012). Structure and function in native and pathological erythrocytes: A quantitative view from the nanoscale. Micron 43(12), 1273–1286.Google Scholar
Goel, M.S. & Diamond, S.L. (2002). Adhesion of normal erythrocytes at depressed venous shear rates to activated neutrophils, activated platelets, and fibrin polymerized from plasma. Blood 100(10), 3797–3803.Google Scholar
Golden, G.A., Rubin, R.T. & Mason, R.P. (1998). Steroid hormones partition to distinct sites in a model membrane bilayer: Direct demonstration by small-angle X-ray diffraction. Biochim Biophys Acta 1368(2), 161–166.Google Scholar
Grey, J.L., Kodippili, G.C., Simon, K. & Low, P.S. (2012). Identification of contact sites between ankyrin and band 3 in the human erythrocyte membrane. Biochemistry 51(34), 6838–6846.Google Scholar
Halbhuber, K.J., Stibenz, D. & Baumler, H. (1986). Topo-optical investigations of the conformational change of the erythrocyte glycocalyx in dependence on extracellular pH and presence of dextran. Acta Histochem Suppl 33, 55–60.Google Scholar
Heijnen, H.F., Schiel, A.E., Fijnheer, R., Geuze, H.J. & Sixma, J.J. (1999). Activated platelets release two types of membrane vesicles: Microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94(11), 3791–3799.Google Scholar
Hellgren, M. (2003). Hemostasis during normal pregnancy and puerperium. Semin Thromb Hemost 29(2), 125–130.Google Scholar
Huisman, A., Aarnoudse, J., Krans, M., Huisjes, H., Fidler, V. & Zijlstra, W. (1988). Red cell aggregation during normal pregnancy. Br J Haematol 68(1), 121–124.Google Scholar
Janes, S.L. & Goodall, A.H. (1994). Flow cytometric detection of circulating activated platelets and platelet hyper-responsiveness in pre-eclampsia and pregnancy. Clin Sci 86(6), 731–740.CrossRefGoogle ScholarPubMed
Jarvis, G.E., Bihan, D., Hamaia, S., Pugh, N., Ghevaert, C.J., Pearce, A.C., Hughes, C.E., Watson, S.P., Ware, J., Rudd, C.E. & Farndale, R.W. (2012). A role for adhesion and degranulation-promoting adapter protein in collagen-induced platelet activation mediated via integrin alpha(2) beta(1). J Thromb Haemost 10(2), 268–277.Google Scholar
Joly, B., Barbay, V., Borg, J.Y. & Le Cam-Duchez, V. (2013). Comparison of markers of coagulation activation and thrombin generation test in uncomplicated pregnancies. Thromb Res 132(3), 386–391.Google Scholar
Jurk, K. & Kehrel, B.E. (2005). Platelets: Physiology and biochemistry. Semin Thromb Hemost 31(4), 381–392.Google Scholar
Kahn, M.L., Nakanishi-Matsui, M., Shapiro, M.J., Ishihara, H. & Coughlin, S.R. (1999). Protease-activated receptors 1 and 4 mediate activation of human platelets by thrombin. J Clin Invest 103(6), 879–887.Google Scholar
Kamath, S. & Lip, G. (2003). Fibrinogen: Biochemistry, epidemiology and determinants. QJM 96(10), 711–729.CrossRefGoogle ScholarPubMed
Kanaji, T., Ware, J., Okamura, T. & Newman, P.J. (2012). GPIbalpha regulates platelet size by controlling the subcellular localization of filamin. Blood 119(12), 2906–2913.Google Scholar
Kemkes-Matthes, B. (2000). Changes in the blood coagulation system in pregnancy. Z Kardiol 90, 45–48.Google Scholar
Kilby, M.D., Broughton Pipkin, F. & Symonds, E.M. (1993). Changes in platelet intracellular free calcium in normal pregnancy. Br J Obstet Gynaecol 100(4), 375–379.CrossRefGoogle ScholarPubMed
Kim, Y.K., Kim, K. & Park, K. (2012). Measurement techniques for red blood cell deformability: Recent advances. In Blood Cell–An Overview of Studies in Hematology, Terry E. Moschandreou (Ed.), pp. 167–195. Croatia: InTech.Google Scholar
Knijff, S. & Goorissen, E. (2000). Summary of Contraindications to Oral Contraceptives . Nashville: Parthenon Publishing Group.Google Scholar
Kozlova, E.K., Chernysh, A.M., Moroz, V.V. & Kuzovlev, A.N. (2012). Analysis of nanostructure of red blood cells membranes by space Fourier transform of AFM images. Micron.Google Scholar
Kraus, M.J., Strasser, E.F. & Eckstein, R. (2010). A new method for measuring the dynamic shape change of platelets. Transfus Med Hemother 37(5), 306–310.Google Scholar
Laurens, N., Koolwijk, P. & De Maat, M. (2006). Fibrin structure and wound healing. J Thromb Haemost 4(5), 932–939.Google Scholar
Lee, D., Fong, K.P., King, M.R., Brass, L.F. & Hammer, D.A. (2012). Differential dynamics of platelet contact and spreading. Biophys J 102(3), 472–482.CrossRefGoogle ScholarPubMed
Letcher, R.L., Chien, S., Pickering, T.G. & Laragh, J.H. (1983). Elevated blood viscosity in patients with borderline essential hypertension. Hypertension 5(5), 757–762.Google Scholar
Lhermusier, T., Chap, H. & Payrastre, B. (2011). Platelet membrane phospholipid asymmetry: From the characterization of a scramblase activity to the identification of an essential protein mutated in Scott syndrome. J Thromb Haemost 9(10), 1883–1891.CrossRefGoogle Scholar
Li, Z., Delaney, M.K., O’Brien, K.A. & Du, X. (2010). Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 30(12), 2341–2349.Google Scholar
Lominadze, D. & Dean, W.L. (2002). Involvement of fibrinogen specific binding in erythrocyte aggregation. FEBS Lett 517(1–3), 41–44.Google Scholar
Louden, K., Pipkin, F.B., Heptinstall, S., Fox, S., Mitchell, J. & Symonds, E. (1990). A longitudinal study of platelet behaviour and thromboxane production in whole blood in normal pregnancy and the puerperium. BJOG 97(12), 1108–1114.Google Scholar
Lukačín, Š., Rychnavský, J., Mojžiš, J., Mirossay, L., Jurčová, E. & Nicak, A. (1996). Changes of erythrocyte microrheology during normal pregnancy and after delivery. Eur J Obstet Gynecol Reprod Biol 66(2), 125–128.Google Scholar
Lüthje, J. (1989). Extracellular adenine compounds, red blood cells and haemostasis: Facts and hypotheses. Blut 59(4), 367–374.Google Scholar
Mackman, N. (2008). Triggers, targets and treatments for thrombosis. Nature 451(7181), 914–918.Google Scholar
Maeda, N., Seike, M., Kume, S., Takaku, T. & Shiga, T. (1987). Fibrinogen-induced erythrocyte aggregation: Erythrocyte-binding site in the fibrinogen molecule. Biochim Biophys Acta-Biomembr 904(1), 81–91.CrossRefGoogle ScholarPubMed
Mandelli, B., Polatti, F. & Bolis, P. (1984). Study of erythrocyte deformability in physiological pregnancy. Clin Exp Obstet Gynecol 12(1–2), 16–20.Google Scholar
Marcus, A. & Safier, L. (1993). Thromboregulation: Multicellular modulation of platelet reactivity in hemostasis and thrombosis. FASEB J 7(6), 516–522.CrossRefGoogle ScholarPubMed
Marcus, A., Safier, L., Broekman, M., Islam, N., Fliessbach, J., Hajjar, K., Kaminski, W., Jendraschak, E., Silverstein, R. & von Schacky, C. (1995). Thrombosis and inflammation as multicellular processes: Significance of cell-cell interactions. Thromb Haemost 74(1), 213–217.Google Scholar
Marra, C.A., Mangionil, J.O., Tavella, M., del Alaniz, M.J., Ortiz, D. & Sala, C. (1998). Hormonal-induced changes on the lipid composition and DPH fluorescence anisotropy of erythrocyte ghost from pre- and postmenopausal women. Acta Physiol Pharmacol Ther Latinoam 48(1), 8–17.Google Scholar
Matsuoka, Y., Nishikawa, M., Toyoda, H., Hirokawa, Y., Ando, S., Yano, T., Tanabe, K. & Yatani, R. (1994). Mediation of the physiological response of platelets by interactions of spectrin and protein 4.1 with the cytoskeleton. Biochem Biophys Res Commun 198(1), 111–119.CrossRefGoogle ScholarPubMed
McCrae, K.R. (2010). Thrombocytopenia in pregnancy. ASH Educ Program Book 2010(1), 397–402.Google ScholarPubMed
McCrae, K.R., Samuels, P. & Schreiber, A.D. (1992). Pregnancy-associated thrombocytopenia: Pathogenesis and management. Blood 80(11), 2697–2714.Google Scholar
McLintock, C. (2014). Thromboembolism in pregnancy: Challenges and controversies in the prevention of pregnancy-associated venous thromboembolism and management of anticoagulation in women with mechanical prosthetic heart valves. Best Pract Res Clin Obstet Gynaecol 28(4), 519–536.Google Scholar
Min, S.H. & Abrams, C.S. (2013). Regulation of platelet plug formation by phosphoinositide metabolism. Blood 122(8), 1358–1365.Google Scholar
Moro, L., Reineri, S., Piranda, D., Pietrapiana, D., Lova, P., Bertoni, A., Graziani, A., Defilippi, P., Canobbio, I. & Torti, M. (2005). Nongenomic effects of 17β-estradiol in human platelets: Potentiation of thrombin-induced aggregation through estrogen receptor β and Src kinase. Blood 105(1), 115–121.Google Scholar
Moroi, M. & Jung, S.M. (1998). Integrin-mediated platelet adhesion. Front Biosci 3, d719–d728.CrossRefGoogle ScholarPubMed
Morrison, R., Crawford, J., MacPherson, M. & Heptinstall, S. (1985). Platelet behaviour in normal pregnancy, pregnancy complicated by essential hypertension and pregnancy-induced hypertension. Thromb Haemost 54(3), 607–611.Google Scholar
Nieswandt, B. & Watson, S.P. (2003). Platelet-collagen interaction: Is GPVI the central receptor? Blood 102(2), 449–461.Google Scholar
O’Brien, K.A., Gartner, T.K., Hay, N. & Du, X. (2012). ADP-stimulated activation of Akt during integrin outside-in signaling promotes platelet spreading by inhibiting glycogen synthase kinase-3β. Arterioscler Thromb Vasc Biol 32(9), 2232–2240.Google Scholar
Oberleithner, H. (2013). Vascular endothelium leaves fingerprints on the surface of erythrocytes. Pflugers Arch 465(10), 1451–1458.Google Scholar
Ohvo-Rekila, H., Ramstedt, B., Leppimaki, P. & Slotte, J.P. (2002). Cholesterol interactions with phospholipids in membranes. Prog Lipid Res 41(1), 66–97.Google Scholar
Peck, T.M. & Arias, F. (1979). Hematologic changes associated with pregnancy. Clin Obstet Gynecol 22(4), 785–798.Google Scholar
Perez, E. & Wolfe, J. (1988). Oestradiol changes the dielectric structure of bilayer membranes. Eur Biophys J 16(1), 23–29.Google Scholar
Posch, S., Neundlinger, I., Leitner, M., Siostrzonek, P., Panzer, S., Hinterdorfer, P. & Ebner, A. (2013). Activation induced morphological changes and integrin alphaIIbbeta3 activity of living platelets. Methods 60(2), 179–185.Google Scholar
Rampling, M. (1980). The binding of fibrinogen and fibrinogen degradation products to the erythrocyte membrane and its relationship to haemorheology. Acta Biol Med Ger 40(4–5), 373–378.Google Scholar
Robb, A.O., Din, J.N., Mills, N.L., Smith, I.B.J., Blomberg, A., Zikry, M.N.L., Raftis, J.B., Newby, D.E. & Denison, F.C. (2010). The influence of the menstrual cycle, normal pregnancy and pre-eclampsia on platelet activation. Thromb Haemost 103(2), 372–378.Google Scholar
Rosenkranz, A., Hiden, M., Leschnik, B., Weiss, E.C., Schlembach, D., Lang, U., Gallistl, S. & Muntean, W. (2008). Calibrated automated thrombin generation in normal uncomplicated pregnancy. Thromb Haemost 99(2), 331–337.Google Scholar
Rosenstein, R., Zacharski, L.R. & Allen, R.D. (1981). Quantitation of human platelet transformation on siliconized glass: Comparison of “normal” and “abnormal” platelets. Thromb Haemost 46(2), 521–524.Google Scholar
Salnlo, S., Kekomäki, R., Rllkonen, S. & Teramo, K. (2000). Maternal thrombocytopenia at term: A population-based study. Acta Obstet Gynecol Scand 79(9), 744–749.Google Scholar
Santos, M., Valles, J., Aznar, J. & Perez-Requejo, J. (1986). Role of red blood cells in the early stages of platelet activation by collagen. Thromb Haemost 56(3), 376–381.Google Scholar
Santos, M., Valles, J., Marcus, A., Safier, L., Broekman, M., Islam, N., Ullman, H., Eiroa, A. & Aznar, J. (1991). Enhancement of platelet reactivity and modulation of eicosanoid production by intact erythrocytes. A new approach to platelet activation and recruitment. J Clin Invest 87(2), 571–580.Google Scholar
Sathi, A., Viswanad, V., Aneesh, T.P. & Kumar, B.A. (2014). Pros and cons of phospholipid asymmetry in erythrocytes. J Pharm Bioallied Sci 6(2), 81–85.Google Scholar
Senis, Y. & Garcia, A. (2012). Platelet proteomics: State of the art and future perspective. Methods Mol Biol 788, 367–399.Google Scholar
Sheu, J., Hsiao, G., Shen, M., Lin, W. & Tzeng, C. (2002). The hyperaggregability of platelets from normal pregnancy is mediated through thromboxane A2 and cyclic AMP pathways. Clin Lab Haematol 24(2), 121–129.Google Scholar
Soulet, C., Hechler, B., Gratacap, M.P., Plantavid, M., Offermanns, S., Gachet, C. & Payrastre, B. (2005). A differential role of the platelet ADP receptors P2Y1 and P2Y12 in Rac activation. J Thromb Haemost 3(10), 2296–2306.Google Scholar
Speroff, L. & Fritz, M.A. (2005). Clinical Gynecologic Endocrinology and Infertility. Philadelphia: Lippincott Williams & Wilkins.Google Scholar
Standeven, K.F., Ariëns, R.A. & Grant, P.J. (2005). The molecular physiology and pathology of fibrin structure/function. Blood Rev 19(5), 275–288.CrossRefGoogle ScholarPubMed
Straat, M., van Bruggen, R., de Korte, D. & Juffermans, N.P. (2012). Red blood cell clearance in inflammation. Transfus Med Hemother 39(5), 353–361.Google Scholar
Suwalsky, M., Belmar, J., Villena, F., Gallardo, M.J., Jemiola-Rzeminska, M. & Strzalka, K. (2013). Acetylsalicylic acid (aspirin) and salicylic acid interaction with the human erythrocyte membrane bilayer induce in vitro changes in the morphology of erythrocytes. Arch Biochem Biophys 539(1), 9–19.Google Scholar
Swanepoel, A.C., Lindeque, B.G., Swart, P.J., Abdool, Z. & Pretorius, E. (2014). Part 2: Ultrastructural changes of fibrin networks during three phases of pregnancy: A qualitative investigation. Microsc Res Tech 77(8), 602–608.Google Scholar
Swanepoel, A.C. & Pretorius, E. (2014). Ultrastructural analysis of platelets during three phases of pregnancy: A qualitative and quantitative investigation. Hematology [Epub ahead of print].Google Scholar
Swieringa, F., Kuijpers, M.J., Heemskerk, J.W. & van der Meijden, P.E. (2014 a). Targeting platelet receptor function in thrombus formation: The risk of bleeding. Blood Rev 28(1), 9–21.Google Scholar
Swieringa, F., Kuijpers, M.J., Heemskerk, J.W. & van der Meijden, P.E. (2014 b). Targeting platelet receptor function in thrombus formation: The risk of bleeding. Blood Rev 28(1), 9–21.Google Scholar
Thevenin, B.J. & Low, P.S. (1990). Kinetics and regulation of the ankyrin-band 3 interaction of the human red blood cell membrane. J Biol Chem 265(27), 16166–16172.Google Scholar
Thon, J.N. & Italiano, J.E. (2012). Platelets: Production, morphology and ultrastructure. Handb Exp Pharmacol 210, 3–22.Google Scholar
Torres, P.J., Escolar, G., Palacio, M., Gratacós, E., Alonso, P.L. & Ordinas, A. (1996). Platelet sensitivity to prostaglandin E1 inhibition is reduced in pre‐eclampsia but not in nonproteinuric gestational hypertension. BJOG 103(1), 19–24.Google Scholar
Townsley, D.M. (2013). Hematologic complications of pregnancy. Semin Hematol 50(3), 222–231.Google Scholar
Traenka, J., Hauck, C.R., Lewandrowski, U., Sickmann, A., Gambaryan, S., Thalheimer, P. & Butt, E. (2009). Integrin-dependent translocation of LASP-1 to the cytoskeleton of activated platelets correlates with LASP-1 phosphorylation at tyrosine 171 by Src-kinase. Thromb Haemost 102(3), 520–528.Google Scholar
Turitto, V. & Weiss, H. (1980). Red blood cells: Their dual role in thrombus formation. Science 207(4430), 541–543.Google Scholar
Uchikova, E.H. & Ledjev, I.I. (2005). Changes in haemostasis during normal pregnancy. Eur J Obstet Gynecol Reprod Biol 119(2), 185–188.Google Scholar
Valera, M.-C., Parant, O., Vayssiere, C., Arnal, J.-F. & Payrastre, B. (2010). Physiologic and pathologic changes of platelets in pregnancy. Platelets 21(8), 587–595.Google Scholar
Valles, J., Santos, M.T., Aznar, J., Marcus, A.J., Martinez-Sales, V., Portoles, M., Broekman, M.J. & Safier, L.B. (1991). Erythrocytes metabolically enhance collagen-induced platelet responsiveness via increased thromboxane production, adenosine diphosphate release, and recruitment. Blood 78(1), 154–162.Google Scholar
Vallés, J., Santos, M.T., Aznar, J., Martı́nez, M., Moscardó, A., Piñón, M., Broekman, M.J. & Marcus, A.J. (2002). Platelet-erythrocyte interactions enhance αIIbβ3 integrin receptor activation and P-selectin expression during platelet recruitment: Down-regulation by aspirin ex vivo. Blood 99(11), 3978–3984.Google Scholar
van den Akker, E., Satchwell, T.J., Williamson, R.C. & Toye, A.M. (2010). Band 3 multiprotein complexes in the red cell membrane; of mice and men. Blood Cells Mol Dis 45(1), 1–8.Google Scholar
van Meer, G. & Holthuis, J.C. (2000). Sphingolipid transport in eukaryotic cells. Biochim Biophys Acta 1486(1), 145–170.Google Scholar
van Meer, G., Voelker, D.R. & Feigenson, G.W. (2008). Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol 9(2), 112–124.CrossRefGoogle ScholarPubMed
van Zwieten, R., Bochem, A.E., Hilarius, P.M., van Bruggen, R., Bergkamp, F., Hovingh, G.K. & Verhoeven, A.J. (2012). The cholesterol content of the erythrocyte membrane is an important determinant of phosphatidylserine exposure. Biochim Biophys Acta 1821(12), 1493–1500.Google Scholar
Versteeg, H.H., Heemskerk, J.W., Levi, M. & Reitsma, P.H. (2013). New fundamentals in hemostasis. Physiol Rev 93(1), 327–358.Google Scholar
Virkus, R.A., Lokkegaard, E., Lidegaard, O., Langhoff-Roos, J., Nielsen, A.K., Rothman, K.J. & Bergholt, T. (2014). Risk factors for venous thromboembolism in 1.3 million pregnancies: A nationwide prospective cohort. PLoS One 9(5), e96495.Google Scholar
Wang, M., Lu, S., Li, S. & Shen, F. (2013). Reference intervals of D-dimer during the pregnancy and puerperium period on the STA-R evolution coagulation analyzer. Clin Chim Acta 425, 176–180.Google Scholar
Warren, B. (1970). The ultrastructure of platelet pseudopodia and the adhesion of homologous platelets to tumour cells. Br J Exp Pathol 51(6), 570–580.Google Scholar
Warren, B. & Vales, O. (1972). The adhesive dendritic pseudopodium of the platelet and the release reaction. Microvasc Res 4(2), 159–178.Google Scholar
Wei, A.H., Schoenwaelder, S.M., Andrews, R.K. & Jackson, S.P. (2009). New insights into the haemostatic function of platelets. Br J Haematol 147(4), 415–430.Google Scholar
Weng, X., Cloutier, G., Beaulieu, R. & Roederer, G.O. (1996). Influence of acute-phase proteins on erythrocyte aggregation. Am J Physiol 271(6 Pt 2), H2346–H2352.Google Scholar
Whiting, K.P., Brain, P.F. & Restall, C.J. (1995). Steroid hormone induced effects on membrane fluidity. Biochem Soc Trans 23(3), 438S.Google Scholar
Whiting, K.P., Restall, C.J. & Brain, P.F. (2000). Steroid hormone-induced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci 67(7), 743–757.Google Scholar
Yamazaki, H., Motomiya, T., Sonoda, M. & Miyagawa, N. (1979). Changes in platelet aggregability after ovariectomy. Thromb Haemost 42(4), 1332–1339.Google Scholar