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Published in: Archives of Gynecology and Obstetrics 4/2012

01-04-2012 | General Gynecology

Hormone replacement therapy leads to increased plasma levels of platelet derived microparticles in postmenopausal women

Authors: Andreas Rank, Rienk Nieuwland, Katharina Nikolajek, Sabine Rösner, Lisa-Maria Wallwiener, Erhard Hiller, Bettina Toth

Published in: Archives of Gynecology and Obstetrics | Issue 4/2012

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Abstract

Background

Whereas prevention of cardiovascular diseases by hormonal replacement therapy is still part of an ongoing debate, well-defined data are available relating hormonal replacement therapy to an elevated risk of venous thrombosis and embolism. Although it seems that venous thrombosis in patients treated with hormonal replacement therapy is linked to changes in plasmatic coagulation, less is known about the role of platelet-derived microparticles, as well as endothelial cell-derived microparticles.

Patients and methods

In this prospective case–control study, levels of microparticles were investigated in postmenopausal women receiving hormone replacement therapy (n = 15) and compared to age-matched controls (n = 15).

Results

Total count of microparticles and the subgroup of microparticles derived from endothelial cells did not differ in the investigated groups. In contrast, median levels of microparticles derived from platelet/megacaryocyte were higher in women taking hormonal replacement therapy (5,244 × 106/l) than in controls (2,803 × 106/l; p = 0.040). Furthermore, hormonal replacement therapy led to a higher plasma level of microparticles derived from activated platelets, exposing P-selectin (136 × 106/l vs. 58 × 106/l; p = 0.011), or exposing CD63 (171 × 106 vs. 91 × 106/l; p = 0.011) compared to the control group.

Conclusion

Higher concentrations of microparticles derived from (activated) platelets/megacaryocytes were present in postmenopausal women taking hormonal replacement therapy. This finding indicates a procoagulant state in these women and might play a role in the development of venous side effects. In contrast, levels of endothelial cell-derived microparticles did not differ.
Literature
1.
go back to reference Hickey M, Davis SR, Sturdee DW (2005) Treatment of menopausal symptoms: what shall we do now? Lancet 366:409–421PubMedCrossRef Hickey M, Davis SR, Sturdee DW (2005) Treatment of menopausal symptoms: what shall we do now? Lancet 366:409–421PubMedCrossRef
2.
go back to reference Bagger YZ, Tanko LB, Alexandersen P, Hansen HB, Mollgaard A, Ravn P, Qvist P, Kanis JA, Christiansen C (2004) Two to three years of hormone replacement treatment in healthy women have long-term preventive effects on bone mass and osteoporotic fractures: the PERF study. Bone 34:728–735PubMedCrossRef Bagger YZ, Tanko LB, Alexandersen P, Hansen HB, Mollgaard A, Ravn P, Qvist P, Kanis JA, Christiansen C (2004) Two to three years of hormone replacement treatment in healthy women have long-term preventive effects on bone mass and osteoporotic fractures: the PERF study. Bone 34:728–735PubMedCrossRef
3.
go back to reference (1997) Collaborative Group on Hormonal Factors in Breast Cancer: breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet 350:1047–1059 (1997) Collaborative Group on Hormonal Factors in Breast Cancer: breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet 350:1047–1059
4.
go back to reference Bath P, Gray LJ (2005) Association between hormone replacement therapy and subsequent stroke: a meta analysis. BMJ 330:342PubMedCrossRef Bath P, Gray LJ (2005) Association between hormone replacement therapy and subsequent stroke: a meta analysis. BMJ 330:342PubMedCrossRef
5.
go back to reference Canonico M, Plu-Bureau G, Lowe GD, Scarabin PY (2008) Hormone replacement therapy and risk for venous thromboembolism in postmenopausal women: systematic review and meta-analysis. BMJ 336(7655):1227–1231PubMedCrossRef Canonico M, Plu-Bureau G, Lowe GD, Scarabin PY (2008) Hormone replacement therapy and risk for venous thromboembolism in postmenopausal women: systematic review and meta-analysis. BMJ 336(7655):1227–1231PubMedCrossRef
6.
go back to reference Sandset PM, Høibraaten E, Eilertsen AL, Dahm A (2009) Mechanisms of thrombosis related to hormone therapy. Thromb Res 123(Suppl 2):S70–S73PubMedCrossRef Sandset PM, Høibraaten E, Eilertsen AL, Dahm A (2009) Mechanisms of thrombosis related to hormone therapy. Thromb Res 123(Suppl 2):S70–S73PubMedCrossRef
7.
go back to reference Scarabin PY, Oger E, Plu-Bureau G, Estrogen and Thromboembolism Risk Study Group (2003) Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk. Lancet 362(9382):428–432PubMedCrossRef Scarabin PY, Oger E, Plu-Bureau G, Estrogen and Thromboembolism Risk Study Group (2003) Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk. Lancet 362(9382):428–432PubMedCrossRef
8.
go back to reference Høibraaten E, Mowinckel MC, de Ronde H, Bertina RM, Sandset PM (2001) Hormone replacement therapy and acquired resistance to activated protein C: results of a randomized, double-blind, placebo-controlled trial. Br J Haematol 115(2):415–420PubMedCrossRef Høibraaten E, Mowinckel MC, de Ronde H, Bertina RM, Sandset PM (2001) Hormone replacement therapy and acquired resistance to activated protein C: results of a randomized, double-blind, placebo-controlled trial. Br J Haematol 115(2):415–420PubMedCrossRef
9.
go back to reference Rosano GM, Vitale C, Fini M (2006) Hormone replacement therapy and cardioprotection: what is good and what is bad for the cardiovascular system? Ann N Y Acad Sci 1092:341–348PubMedCrossRef Rosano GM, Vitale C, Fini M (2006) Hormone replacement therapy and cardioprotection: what is good and what is bad for the cardiovascular system? Ann N Y Acad Sci 1092:341–348PubMedCrossRef
10.
go back to reference Arnal JF, Douin-Echinard V, Tremollières F (2007) Understanding the controversy about hormonal replacement therapy: insights from estrogen effects on experimental and clinical atherosclerosis. Arch Mal Coeur Vaiss 100:554–562PubMed Arnal JF, Douin-Echinard V, Tremollières F (2007) Understanding the controversy about hormonal replacement therapy: insights from estrogen effects on experimental and clinical atherosclerosis. Arch Mal Coeur Vaiss 100:554–562PubMed
11.
go back to reference Stevenson J (2009) HRT and cardiovascular disease. Best Pract Res Clin Obstet Gynaecol 23(1):109–120PubMedCrossRef Stevenson J (2009) HRT and cardiovascular disease. Best Pract Res Clin Obstet Gynaecol 23(1):109–120PubMedCrossRef
12.
go back to reference Gokkusu C, Tata G, Ademoğlu E, Tamer S (2010) The benefits of hormone replacement therapy on plasma and platelet antioxidant status and fatty acid composition in healthy postmenopausal women. Platelets 21(6):439–444PubMedCrossRef Gokkusu C, Tata G, Ademoğlu E, Tamer S (2010) The benefits of hormone replacement therapy on plasma and platelet antioxidant status and fatty acid composition in healthy postmenopausal women. Platelets 21(6):439–444PubMedCrossRef
13.
go back to reference Signorelli SS, Sciacchitano S, Di Pino L, Costa MP, Pennisi G, Caschetto S (2001) Effects of long-term hormone replacement therapy on arterial wall thickness, lipids and lipoproteins, fibrinogen and antithrombin III. Gynecol Endocrinol 15(5):367–372PubMed Signorelli SS, Sciacchitano S, Di Pino L, Costa MP, Pennisi G, Caschetto S (2001) Effects of long-term hormone replacement therapy on arterial wall thickness, lipids and lipoproteins, fibrinogen and antithrombin III. Gynecol Endocrinol 15(5):367–372PubMed
14.
go back to reference Schindler TH, Campisi R, Dorsey D (2009) Effect of hormone replacement therapy on vasomotor function of the coronary microcirculation in post-menopausal women with medically treated cardiovascular risk factors. Eur Heart J 30(8):978–986PubMedCrossRef Schindler TH, Campisi R, Dorsey D (2009) Effect of hormone replacement therapy on vasomotor function of the coronary microcirculation in post-menopausal women with medically treated cardiovascular risk factors. Eur Heart J 30(8):978–986PubMedCrossRef
15.
go back to reference Iwamoto S, Kawasaki T, Kambayashi J, Ariyoshi H, Shinoki N, Sakon M, Ikeda Y, Monden M (1997) The release mechanism of platelet-activating factor during shear-stress induced platelet aggregation. Biochem Biophys Res Commun 239(1):101–105PubMedCrossRef Iwamoto S, Kawasaki T, Kambayashi J, Ariyoshi H, Shinoki N, Sakon M, Ikeda Y, Monden M (1997) The release mechanism of platelet-activating factor during shear-stress induced platelet aggregation. Biochem Biophys Res Commun 239(1):101–105PubMedCrossRef
16.
go back to reference Cramer EM, Norol F, Guichard J, Breton-Gorius J, Vainchenker W, Massé JM, Debili N (1997) Ultrastructure of platelet formation by human megakaryocytes cultured with the Mpl ligand. Blood 89:2336–2346PubMed Cramer EM, Norol F, Guichard J, Breton-Gorius J, Vainchenker W, Massé JM, Debili N (1997) Ultrastructure of platelet formation by human megakaryocytes cultured with the Mpl ligand. Blood 89:2336–2346PubMed
17.
go back to reference Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC, Maquelin KN, Roozendaal KJ, Jansen PG, ten Have K, Eijsman L, Hack CE, Sturk A (1997) Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 96:3534–3541PubMed Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC, Maquelin KN, Roozendaal KJ, Jansen PG, ten Have K, Eijsman L, Hack CE, Sturk A (1997) Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 96:3534–3541PubMed
18.
go back to reference Sims PJ, Faioni EM, Wiedmer T, Shattil SJ (1988) Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 263:18205–18212PubMed Sims PJ, Faioni EM, Wiedmer T, Shattil SJ (1988) Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 263:18205–18212PubMed
19.
go back to reference Biró E, Sturk-Maquelin KN, Vogel GM, Meuleman DG, Smit MJ, Hack CE, Sturk A, Nieuwland R (2003) Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 1(12):2561–2568PubMedCrossRef Biró E, Sturk-Maquelin KN, Vogel GM, Meuleman DG, Smit MJ, Hack CE, Sturk A, Nieuwland R (2003) Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner. J Thromb Haemost 1(12):2561–2568PubMedCrossRef
20.
go back to reference Sinauridze EI, Kireev DA, Popenko NY, Pichugin AV, Panteleev MA, Krymskaya OV, Ataullakhanov FI (2007) Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost 97(3):425–434PubMed Sinauridze EI, Kireev DA, Popenko NY, Pichugin AV, Panteleev MA, Krymskaya OV, Ataullakhanov FI (2007) Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost 97(3):425–434PubMed
21.
go back to reference Gemmell CH, Sefton MV, Yeo EL (1993) Platelet-derived microparticle formation involves glycoprotein IIb–IIIa. Inhibition by RGDS and a Glanzmann’s thrombasthenia defect. J Biol Chem atherothrombotic disease. J Biol Chem 268(20):14586–14589PubMed Gemmell CH, Sefton MV, Yeo EL (1993) Platelet-derived microparticle formation involves glycoprotein IIb–IIIa. Inhibition by RGDS and a Glanzmann’s thrombasthenia defect. J Biol Chem atherothrombotic disease. J Biol Chem 268(20):14586–14589PubMed
22.
go back to reference Sims PJ, Wiedmer T, Esmon CT, Weiss HJ, Shattil SJ (1988) Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J Biol Chem 264(29):17049–17057 Sims PJ, Wiedmer T, Esmon CT, Weiss HJ, Shattil SJ (1988) Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J Biol Chem 264(29):17049–17057
23.
go back to reference Kuriyama N, Nagakane Y, Hosomi A, Ohara T, Kasai T, Harada S, Takeda K, Yamada K, Ozasa K, Tokuda T, Watanabe Y, Mizuno T, Nakagawa M (2010) Evaluation of factors associated with elevated levels of platelet-derived microparticles in the acute phase of cerebral infarction. Clin Appl Thromb Hemost 16(1):26–32PubMedCrossRef Kuriyama N, Nagakane Y, Hosomi A, Ohara T, Kasai T, Harada S, Takeda K, Yamada K, Ozasa K, Tokuda T, Watanabe Y, Mizuno T, Nakagawa M (2010) Evaluation of factors associated with elevated levels of platelet-derived microparticles in the acute phase of cerebral infarction. Clin Appl Thromb Hemost 16(1):26–32PubMedCrossRef
24.
go back to reference Li X, Cong H (2009) Platelet-derived microparticles and the potential of glycoprotein IIb/IIIa antagonists in treating acute coronary syndrome. Tex Heart Inst J 36(2):134–139PubMed Li X, Cong H (2009) Platelet-derived microparticles and the potential of glycoprotein IIb/IIIa antagonists in treating acute coronary syndrome. Tex Heart Inst J 36(2):134–139PubMed
25.
go back to reference Joop K, Berckmans RJ, Nieuwland R, Berkhout J, Romijn FP, Hack CE, Sturk A (2001) Microparticles from patients with multiple organ dysfunction syndrome and sepsis support coagulation through multiple mechanisms. Thromb Haemost 85(5):810–820PubMed Joop K, Berckmans RJ, Nieuwland R, Berkhout J, Romijn FP, Hack CE, Sturk A (2001) Microparticles from patients with multiple organ dysfunction syndrome and sepsis support coagulation through multiple mechanisms. Thromb Haemost 85(5):810–820PubMed
26.
27.
go back to reference Myers DD, Hawley AE, Farris DM, Wrobleski SK, Thanaporn P, Schaub RG, Wagner DD, Kumar A, Wakefield TW (2003) P-selectin and leukocyte microparticles are associated with venous thrombogenesis. J Vasc Surg 38(5):1075–1089PubMedCrossRef Myers DD, Hawley AE, Farris DM, Wrobleski SK, Thanaporn P, Schaub RG, Wagner DD, Kumar A, Wakefield TW (2003) P-selectin and leukocyte microparticles are associated with venous thrombogenesis. J Vasc Surg 38(5):1075–1089PubMedCrossRef
28.
go back to reference Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS (2003) Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res 109(4):175–180PubMedCrossRef Jimenez JJ, Jy W, Mauro LM, Soderland C, Horstman LL, Ahn YS (2003) Endothelial cells release phenotypically and quantitatively distinct microparticles in activation and apoptosis. Thromb Res 109(4):175–180PubMedCrossRef
29.
go back to reference Abid Hussein MN, Meesters EW, Osmanovic N, Romijn FP, Nieuwland R, Sturk A (2003) Antigenic characterization of endothelial cell-derived microparticles and their detection ex vivo. J Thromb Haemost 1(11):2434–2443PubMedCrossRef Abid Hussein MN, Meesters EW, Osmanovic N, Romijn FP, Nieuwland R, Sturk A (2003) Antigenic characterization of endothelial cell-derived microparticles and their detection ex vivo. J Thromb Haemost 1(11):2434–2443PubMedCrossRef
30.
go back to reference Berckmans RJ, Nieuwland R, Böing AN, Romijn FP, Hack CE, Sturk A (2001) Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 83:639–646 Berckmans RJ, Nieuwland R, Böing AN, Romijn FP, Hack CE, Sturk A (2001) Cell-derived microparticles circulate in healthy humans and support low grade thrombin generation. Thromb Haemost 83:639–646
31.
go back to reference Bal L, Ederhy S, Di Angelantonio E, Toti F, Zobairi F, Dufaitre G, Meuleman C, Mallat Z, Boccara F, Tedgui A, Freyssinet JM, Cohen A (2010) Factors influencing the level of circulating procoagulant microparticles in acute pulmonary embolism. Arch Cardiovasc Dis 103(6–7):394–403PubMedCrossRef Bal L, Ederhy S, Di Angelantonio E, Toti F, Zobairi F, Dufaitre G, Meuleman C, Mallat Z, Boccara F, Tedgui A, Freyssinet JM, Cohen A (2010) Factors influencing the level of circulating procoagulant microparticles in acute pulmonary embolism. Arch Cardiovasc Dis 103(6–7):394–403PubMedCrossRef
32.
go back to reference Rectenwald JE, Myers DD Jr, Hawley AE, Longo C, Henke PK, Guire KE, Schmaier AH, Wakefield TW (2005) D-dimer, P-selectin, and microparticles: novel markers to predict deep venous thrombosis. A pilot study. Thromb Haemost 94(6):1312–1317PubMed Rectenwald JE, Myers DD Jr, Hawley AE, Longo C, Henke PK, Guire KE, Schmaier AH, Wakefield TW (2005) D-dimer, P-selectin, and microparticles: novel markers to predict deep venous thrombosis. A pilot study. Thromb Haemost 94(6):1312–1317PubMed
33.
go back to reference Ramacciotti E, Hawley AE, Farris DM, Ballard NE, Wrobleski SK, Myers DD Jr, Henke PK, Wakefield TW (2009) Leukocyte- and platelet-derived microparticles correlate with thrombus weight and tissue factor activity in an experimental mouse model of venous thrombosis. Thromb Haemost 101(4):748–754PubMed Ramacciotti E, Hawley AE, Farris DM, Ballard NE, Wrobleski SK, Myers DD Jr, Henke PK, Wakefield TW (2009) Leukocyte- and platelet-derived microparticles correlate with thrombus weight and tissue factor activity in an experimental mouse model of venous thrombosis. Thromb Haemost 101(4):748–754PubMed
34.
go back to reference Rank A, Nieuwland R, Crispin A, Gr Tzner S, Iberer M, Toth B, Pihusch R (2011) Clearance of platelet microparticles in vivo. Platelets 22(2):111–116PubMedCrossRef Rank A, Nieuwland R, Crispin A, Gr Tzner S, Iberer M, Toth B, Pihusch R (2011) Clearance of platelet microparticles in vivo. Platelets 22(2):111–116PubMedCrossRef
35.
go back to reference Warren BA, Vales O (1972) The release of vesicles from platelets following adhesion to vessel walls in vitro. Br J Exp Pathol 53:206–215PubMed Warren BA, Vales O (1972) The release of vesicles from platelets following adhesion to vessel walls in vitro. Br J Exp Pathol 53:206–215PubMed
36.
go back to reference Miyazaki Y, Nomura S, Miyake T, Kagawa H, Kitada C, Taniguchi H, Komiyama Y, Fujimura Y, Ikeda Y, Fukuhara S (1996) High shear stress can initiate both platelet aggregation and shedding of procoagulant containing microparticles. Blood 88:3456–3464PubMed Miyazaki Y, Nomura S, Miyake T, Kagawa H, Kitada C, Taniguchi H, Komiyama Y, Fujimura Y, Ikeda Y, Fukuhara S (1996) High shear stress can initiate both platelet aggregation and shedding of procoagulant containing microparticles. Blood 88:3456–3464PubMed
37.
go back to reference Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ (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 94:3791–3799PubMed Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ (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 94:3791–3799PubMed
38.
go back to reference van der Zee PM, Biró E, Ko Y, de Winter RJ, Hack CE, Sturk A, Nieuwland R (2006) P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin Chem 52(4):657–664PubMedCrossRef van der Zee PM, Biró E, Ko Y, de Winter RJ, Hack CE, Sturk A, Nieuwland R (2006) P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin Chem 52(4):657–664PubMedCrossRef
39.
go back to reference Tan KT, Tayebjee MH, Lynd C, Blann AD, Lip GY (2005) Platelet microparticles and soluble P selectin in peripheral artery disease: relationship to extent of disease and platelet activation markers. Ann Med 37(1):61–66PubMedCrossRef Tan KT, Tayebjee MH, Lynd C, Blann AD, Lip GY (2005) Platelet microparticles and soluble P selectin in peripheral artery disease: relationship to extent of disease and platelet activation markers. Ann Med 37(1):61–66PubMedCrossRef
40.
go back to reference Travlos GS (2006) Normal structure, function, and histology of the bone marrow. Toxicol Pathol 34:548–565PubMedCrossRef Travlos GS (2006) Normal structure, function, and histology of the bone marrow. Toxicol Pathol 34:548–565PubMedCrossRef
41.
go back to reference Flaumenhaft R, Dilks JR, Richardson J, Alden E, Patel-Hett SR, Battinelli E, Klement GL, Sola-Visner M, Italiano JE Jr (2009) Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles. Blood 113:1112–1121PubMedCrossRef Flaumenhaft R, Dilks JR, Richardson J, Alden E, Patel-Hett SR, Battinelli E, Klement GL, Sola-Visner M, Italiano JE Jr (2009) Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles. Blood 113:1112–1121PubMedCrossRef
42.
go back to reference Rank A, Nieuwland R, Delker R, Köhler A, Toth B, Pihusch V, Wilkowski R, Pihusch R (2010) Cellular origin of platelet-derived microparticles in vivo. Thromb Res 126(4):255–259CrossRef Rank A, Nieuwland R, Delker R, Köhler A, Toth B, Pihusch V, Wilkowski R, Pihusch R (2010) Cellular origin of platelet-derived microparticles in vivo. Thromb Res 126(4):255–259CrossRef
43.
go back to reference Tarantino MD, Kunicki TJ, Nugent DJ (1994) The estrogen receptor is present in human megakaryocytes. Ann N Y Acad Sci 714:293–296PubMedCrossRef Tarantino MD, Kunicki TJ, Nugent DJ (1994) The estrogen receptor is present in human megakaryocytes. Ann N Y Acad Sci 714:293–296PubMedCrossRef
44.
go back to reference Nagata Y, Yoshikawa J, Hashimoto A, Yamamoto M, Payne AH, Todokoro K (2003) Proplatelet formation of megakaryocytes is triggered by autocrine-synthesized estradiol. Genes Dev 17(23):2864–2869PubMedCrossRef Nagata Y, Yoshikawa J, Hashimoto A, Yamamoto M, Payne AH, Todokoro K (2003) Proplatelet formation of megakaryocytes is triggered by autocrine-synthesized estradiol. Genes Dev 17(23):2864–2869PubMedCrossRef
45.
go back to reference Stevens RF, Alexander MK (1977) A sex difference in the platelet count. Br J Haematol 37(2):295–300PubMedCrossRef Stevens RF, Alexander MK (1977) A sex difference in the platelet count. Br J Haematol 37(2):295–300PubMedCrossRef
46.
go back to reference Toth B, Nikolajek K, Rank A, Nieuwland R, Lohse P, Pihusch V, Friese K, Thaler CJ (2007) Gender-specific and menstrual cycle dependent differences in circulating microparticles. Platelets 18(7):515–521PubMedCrossRef Toth B, Nikolajek K, Rank A, Nieuwland R, Lohse P, Pihusch V, Friese K, Thaler CJ (2007) Gender-specific and menstrual cycle dependent differences in circulating microparticles. Platelets 18(7):515–521PubMedCrossRef
47.
go back to reference Corada M, Liao F, Lindgren M, Lampugnani MG, Breviario F, Frank R, Muller WA, Hicklin DJ, Bohlen P, Dejana E (2001) Monoclonal antibodies directed to different regions of vascular endothelial cadherin extracellular domain affect adhesion and clustering of the protein and modulate endothelial permeability. Blood 97(6):1679–1684PubMedCrossRef Corada M, Liao F, Lindgren M, Lampugnani MG, Breviario F, Frank R, Muller WA, Hicklin DJ, Bohlen P, Dejana E (2001) Monoclonal antibodies directed to different regions of vascular endothelial cadherin extracellular domain affect adhesion and clustering of the protein and modulate endothelial permeability. Blood 97(6):1679–1684PubMedCrossRef
48.
go back to reference Simak J, Holada K, Risitano AM, Zivny JH, Young NS, Vostal JG (2004) Elevated circulating endothelial membrane microparticles in paroxysmal nocturnal haemoglobinuria. Brit J Haematol 125(6):804–813CrossRef Simak J, Holada K, Risitano AM, Zivny JH, Young NS, Vostal JG (2004) Elevated circulating endothelial membrane microparticles in paroxysmal nocturnal haemoglobinuria. Brit J Haematol 125(6):804–813CrossRef
49.
go back to reference Koga H, Sugiyama S, Kugiyama K, Watanabe K, Fukushima H, Tanaka T, Sakamoto T, Yoshimura M, Jinnouchi H, Ogawa H (2005) Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 45:1622–1630PubMedCrossRef Koga H, Sugiyama S, Kugiyama K, Watanabe K, Fukushima H, Tanaka T, Sakamoto T, Yoshimura M, Jinnouchi H, Ogawa H (2005) Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 45:1622–1630PubMedCrossRef
50.
go back to reference Wakefield TW, Henke PK (2005) The role of inflammation in early and late venous thrombosis: are there clinical implications? Semin Vasc Surg 18(3):118–129PubMedCrossRef Wakefield TW, Henke PK (2005) The role of inflammation in early and late venous thrombosis: are there clinical implications? Semin Vasc Surg 18(3):118–129PubMedCrossRef
Metadata
Title
Hormone replacement therapy leads to increased plasma levels of platelet derived microparticles in postmenopausal women
Authors
Andreas Rank
Rienk Nieuwland
Katharina Nikolajek
Sabine Rösner
Lisa-Maria Wallwiener
Erhard Hiller
Bettina Toth
Publication date
01-04-2012
Publisher
Springer-Verlag
Published in
Archives of Gynecology and Obstetrics / Issue 4/2012
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-011-2098-0

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