Endothelial dysfunction in the pathogenesis of pre-eclampsia

Frontiers in Bioscience - Landmark

Volumn 19, Issue 5, 2014, Pages 734-746

  Szpera Gozdziewicz, Agata ^a   Breborowicz, Grzegorz H ^a  

^a POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

Endothelium; Hypertension; Pathogenesis; Pre Eclampsia; Pregnancy; Review

Indexed keywords

ARTICLE; FEMALE; HUMAN; PATHOPHYSIOLOGY; PREECLAMPSIA; PREGNANCY; VASCULAR ENDOTHELIUM;

ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; PRE-ECLAMPSIA; PREGNANCY;

EID: 84904100838     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4240     Document Type: Article

References (111)

1. Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. Am J Obstet Gynecol 183(1), S1-S22 (2000)
2. ACOG Committee on Practice Bulletins- Obstetrics: ACOG practice bulletin: Diagnosis and management of pre-eclampsia and eclampsia. Obstet Gynecol 99, 159 (2002)
3. J.R. Barton, B.M. Sibai: Prediction and prevention of recurrent pre-eclampsia. Obstet Gynecol 112(2 Pt 1), 359-372 (2008)
4. R.E. Harskamp, G.G. Zeeman: Pre-eclampsia: at risk for remote cardiovascular disease. Am J Med Sci 334(4), 291-295 (2007)
5. R. Thadhani, C.G. Solomon: Pre-eclampsia- a glimpse into the future? N Engl J Med 359(8), 858-860 (2008)
6. M. Wolf, C.A. Hubel, C. Lam, M. Sampson, J.L. Ecker, R.B. Ness, A. Rajakumar, A. Daftary, A.S. Shakir, E.W. Seely, J.M. Roberts, V.P. Sukhatme, S.A. Karumanchi, R. Thadhani: Pre-eclampsia and future cardiovascular disease: potential role of altered angiogenesis and insulin resistance. J Clin Endocrinol Metab 89(12), 6239-6243 (2004)
7. C.W. Redman, I.L. Sargent: Latest advances in understanding pre-eclampsia. Science 308(5728), 1592-1594 (2005)
8. P.L. Gross, W.C. Aird: The endothelium and thrombosis. Semin Thromb Hemost 26(5), 463-478 (2000)
9. D.D. Wagner, P.S. Frenette: The vessel wall and its interactions. Blood 111(11), 5271-5281 (2008)
10. K. Matsuo, S. Kooshesh, M. Dinc, C.C. Sun, T. Kimura, A.A. Baschat: Late postpartum eclampsia: report of two cases managed by uterine curettage and review of the literature. Am J Perinatol 24 (4), 257-266 (2007)
11. M.A. Shembrey, A.D. Noble: An instructive case of abdominal pregnancy. Aust N Z J Obstet Gynaecol 35(2), 220-221 (1995)
12. Y. Zhou, C.H. Damsky, S.J. Fisher: Pre-eclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J Clin Invest 99(9), 2152-2164 (1997)
13. J.W. Meekins, R. Pijnenborg, M. Hanssens, I.R. McFadyen, A. van Asshe: A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J ObstetGynaecol 101(8), 669-674 (1994)
14. I. Brosens, R. Pijnenborg, L. Vercruysse, R. Romero: The "Great Obstetrical Syndromes" are associated with disorders of deep placentation. Am J Obstet Gynecol 204(3), 193-201 (2011)
15. Y. Zhou, C.H. Damsky, K. Chiu, J.M. Roberts, S.J. Fisher: Pre-eclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 91(3), 950-60 (1993)
16. K.H. Lim, Y. Zhou, M. Janatpour, M. McMaster, K. Bass, S.H. Chun, S.J. Fisher: Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am J Pathol 151(6), 1809-1818 (1997)
17. S.J. Fisher: The placental problem: linking abnormal cytotrophoblast differentiation to the maternal symptoms of pre-eclampsia. Reprod Biol Endocrinol 2, 53 (2004)
18. A. Makris, C. Thornton, J. Thompson, S. Thomson, R. Martin, R. Ogle, R. Waugh, P. McKenzie, P. Kirwan, A. Hennessy: Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int 71(10), 977-984 (2007)
19. J.S. Gilbert, S.A. Babcock, J.P. Granger. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 50(6), 1142-1147 (2007)
20. K. Duckitt, D. Harrington: Risk factors for pre-eclampsia at antenatal booking: systematic review of controlled studies. BMJ 330(7491), 565 (2005)
21. Y. Bdolah, C. Lam, A. Rajakumar, V. Shivalingappa, W. Mutter, B.P. Sachs, K.H. Lim, T. Bdolah-Abram, F.H. Epstein, S.A. Karumanchi: Twin pregnancy and the risk of pre-eclampsia: bigger placenta or relative ischemia? Am J Obstet Gynecol 198(4), 428 e1-6 (2008)
22. K. Koga, Y. Osuga, T. Tajima, Y. Hirota, T. Igarashi, T. Fujii, T. Yano, Y. Taketani: Elevated serum soluble fms-like tyrosine kinase 1 (sFlt1) level in women with hydatidiform mole. Fertil Steril 94(1), 305-308 (2010)
23. B. Sibai, G. Dekker, M. Kupferminc: Pre-eclampsia. Lancet 365(9461), 785-799 (2005)
24. S.K. Palmer, L.G. Moore, D. Young, B. Cregger, J.C. Berman, S. Zamudio: Altered blood pressure course during normal pregnancy and increased pre-eclampsia at high altitude (3100 meters) in Colorado. Am J Obstet Gynecol 180(5), 1161-1168.(1999)
25. F. De Wolf, C. De Wolf-Peeters, I. Brosens, W.B. Robertson: The human placental bed: electron microscopic study of trophoblastic invasion of spiral arteries. Am J Obstet Gynecol 137(1), 58-70 (1980)
26. C.M. Salafia, J.C. Pezzullo, A. Ghidini, J.A. Lopèz-Zeno, S.S. Whittington: Clinical correlations of patterns of placental pathology in preterm pre-eclampsia. Placenta 19(1), 67-72 (1998)
27. G. Gerretsen, H.J. Huisjes, J.D. Elema: Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol 88(9), 876-881 (1981)
28. F. De Wolf, W.B. Robertson, I. Brosens. The ultrastructure of acute atherosis in hypertensive pregnancy. Am J Obstet Gynecol 123(2), 164-174 (1975)
29. W.B. Robertson, I. Brosens, H.G. Dixon: The pathological response of the vessels of the placental bed to hypertensive pregnancy J Pathol Bacteriol 93(2), 581-592 (1967)
30. S.E. Maynard, J.Y. Min, J. Merchan, K.H. Lim, J. Li, S. Mondal, T.A. Libermann, J.P. Morgan, F.W. Sellke, I.E. Stillman, F.H. Epstein, V.P. Sukhatme, S.A. Karumanchi: Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111(5), 649-658 (2003)
31. K. Koga, Y. Osuga, O. Yoshino, Y. Hirota, X. Ruimeng, T. Hirata, S. Takeda, T. Yano, O. Tsutsumi, Y. Taketani: Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with pre=eclampsia. J Clin Endocrinol Metab 88(5), 2348-2351 (2003)
32. S. Venkatesha, M. Toporsian, C. Lam, J. Hanai, T. Mammoto, Y.M. Kim, Y. Bdolah, K.H. Lim, H.T. Yuan, T.A. Libermann, I.E. Stillman, D. Roberts, P.A. D'Amore, F.H. Epstein, F.W. Sellke, R. Romero, V.P. Sukhatme, M. Letarte, S.A. Karumanchi: Soluble endoglin contributes to the pathogenesis of pre-eclampsia. Nat Med 12(6), 642-649 (2006) Erratum in: Nat Med 12(7), 862 (2006)
33. R.J. Levine, S.E. Maynard, C. Qian, K.H. Lim, L.J. England, K.F. Yu, E.F. Schisterman, R. Thadhani, B.P. Sachs, F.H. Epstein, B.M. Sibai, V.P. Sukhatme, S.A. Karumanchi: Circulating angiogenic factors and the risk of pre-eclampsia. N Engl J Med 350(7), 672-683 (2004)
34. B.M. Polliotti, A.G. Fry, D.N. Saller, R.A. Mooney, C. Cox, R.K. Miller: Second-trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early-onset pre-eclampsia. Obstet Gynecol 101(6), 1266-1274 (2003)
35. R.N. Taylor, J. Grimwood, R.S. Taylor, M.T. McMaster, S.J. Fisher, R.A. North: Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 188(1), 177-182 (2003)
36. J.P. Bridges, J.S. Gilbert, D. Colson, S.A. Gilbert, M.P. Dukes, M.J. Ryan, J.P. Granger: Oxidative stress contributes to soluble fms-like tyrosine kinase-1 induced vascular dysfunction in pregnant rats. Am J Hypertens 22(5), 564-568 (2009)
37. V. Eremina, M. Sood, J. Haigh, A. Nagy, G. Lajoie, N. Ferrara, H.P. Gerber, Y. Kikkawa, J.H. Miner, S.E. Quaggin: Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111(5), 707-716 (2003)
38. B.C. Kuenen, M. Levi, J.C. Meijers, A.K. Kakkar, V.W. van Hinsbergh, P.J. Kostense, H.M. Pinedo, K. Hoekman: Analysis of coagulation cascade and endothelial cell activation during inhibition of vascular endothelial growth factor/vascular endothelial growth factor receptor pathway in cancer patients. Arterioscler Thromb Vasc Biol. 22(9), 1500-1505 (2002)
39. J.C. Yang, L. Haworth L, R.M. Sherry, P. Hwu, D.J. Schwartzentruber, S.L. Topalian, S.M. Steinberg, H.X. Chen, S.A. Rosenberg: A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349(5), 427-434 (2003)
40. E. Shibata, A. Rajakumar, R.W. Powers, R.W. Larkin, C. Gilmour, L.M. Bodnar, W.R. Crombleholme, R.B. Ness, J.M. Roberts, C.A. Hubel: Soluble fms-like tyrosine kinase 1 is increased in pre-eclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab 90(8), 4895-4903 (2005)
41. R.J. Levine, C. Lam, C. Qian, K.F. Yu, S.E. Maynard, B.P. Sachs, B.M. Sibai, F.H. Epstein, R. Romero, R. Thadhani, S.A. Karumanchi, CPEP Study Group: Soluble endoglin and other circulating antiangiogenic factors in pre-eclampsia. N Engl J Med 355(10), 992-1005 (2006) Erratum in: N Engl J Med 355(17), 1840 (2006)
42. R.W. Powers, J.M. Roberts, K.M. Cooper, M.J. Gallaher, M.P. Frank, G.F. Harger, R.B. Ness: Maternal serum soluble fms-like tyrosine kinase 1 concentrations are not increased in early pregnancy and decrease more slowly postpartum in women who develop pre-eclampsia. Am J Obstet Gynecol 193(1), 185-191 (2005)
43. N.O. Lunell, R. Lewander, I. Mamoun, L. Nylund, S. Sarby, S. Thornström: Uteroplacental blood flow in pregnancy induced hypertension. Scand J Clin Lab Invest Suppl 169, 28-35 (1984)
44. J.A. Forsythe, B.H. Jiang, N.V. Iyer, F. Agani, S.W. Leung, R.D. Koos, G.L. Semenza: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16(9), 4604-4613 (1996)
45. H.P. Gerber, F. Condorelli, J. Park, N. Ferrara: Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is upregulated by hypoxia. J Biol Chem 272(38), 23659-23667 (1997)
46. I. Caniggia, H. Mostachfi, J. Winter, M. Gassmann, S.J. Lye, M. Kuliszewski, M. Post: Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta3. J Clin Invest 105(5), 577-587 (2000)
47. A. Rajakumar, K. Doty, A. Daftary, G. Harger, K.P. Conrad: Impaired oxygen-dependent reduction of HIF-1alpha and -2alpha proteins in pre-eclamptic placentae. Placenta 24(2-3), 199-208 (2003) Erratum in: Placenta 24(6), 711 (2003)
48. A. Rajakumar, K.A. Whitelock, L.A. Weissfeld, A.R. Daftary, N. Markovic, K.P. Conrad: Selective overexpression of the hypoxia-inducible transcription factor, HIF-2alpha, in placentas from women with preeclampsia. Biol Reprod 64(2), 499-506 (2001)
49. S. Ahmad, A. Ahmed: Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in pre-eclampsia. Circ Res 95(9), 884-891 (2004)
50. T. Nagamatsu, T. Fujii, M. Kusumi, L. Zou, T. Yamashita, Y. Osuga, M. Momoeda, S. Kozuma, Y. Taketani: Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of pre-eclampsia. Endocrinology 145(11), 4838-4845 (2004)
51. F. Lebrin, M.J. Goumans, L. Jonker, R.L. Carvalho, G. Valdimarsdottir, M. Thorikay, C. Mummery, H.M. Arthur HM, P. ten Dijke: Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 23(20), 4018-4028 (2004)
52. A. Bourdeau, D.J. Dumont, M. Letarte: A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest 104(10), 1343-1351 (1999)
53. H.M. Arthur, J. Ure, A.J. Smith, G. Renforth, D.I. Wilson, E. Torsney, R. Charlton, D.V. Parums, T. Jowett, D.A. Marchuk, J. Burn, A.G. Diamond: Endoglin, an ancillary TGFbeta receptor, is required for extra-embryonic angiogenesis and plays a key role in heart development. Dev Biol 217(1), 42-53 (2000)
54. S. Maynard, F.H. Epstein, S.A. Karumanchi: Pre-eclampsia and angiogenic imbalance. Annu Rev Med 59, 61-78 (2008)
55. V.C. Sandrim, A.C. Palei, I.F. Metzger, V.A. Gomes, R.C. Cavalli, J.E. Tanus-Santos: Nitric oxide formation is inversely related to serum levels of anti-angiogenic factors soluble fms-like tyrosine kinase-1 and soluble endogline in preeclampsia. Hypertension 52(2), 402-407 (2008)
56. A.S. Maharaj, T.E. Walshe, M. Saint-Geniez, S. Venkatesha, A.E. Maldonado, N.C. Himes, K.S. Matharu, S.A. Karumanchi, P.A. D'Amore: VEGF and TGF-beta are required for the maintenance of the choroid plexus and ependyma. J Exp Med 205(2), 491-501 (2008)
57. J.S. Gilbert, S.A. Gilbert, M. Arany, J.P. Granger: Hypertension produced by placental ischemia in pregnant rats is associated with increased soluble endoglin expression. Hypertension 53(2), 399-403 (2009)
58. C.E. Powe, R.J. Levine, S.A. Karumanchi: Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 123(24), 2856-2869 (2011)
59. S. Rana, S.A. Karumanchi, R.J. Levine, S. Venkatesha, J.A. Rauh-Hain, H. Tamez, R. Thadhani: Sequential changes in anti-angiogenic factors in early pregnancy and risk of developing preeclampsia. Hypertension 50(1), 137-142 (2007)
60. C. Signore, J.L. Mills, C. Qian, K. Yu, C. Lam, F.H. Epstein, S.A. Karumanchi, R.J. Levine: Circulating angiogenic factors and placental abruption. Obstet Gynecol 108(2), 338-344 (2006) Erratum in: Obstet Gynecol 108(4), 1035 (2006)
61. C. Signore, J.L. Mills, C. Qian, K.F. Yu, S. Rana, S.A. Karumanchi, R.J. Levine: Circulating soluble endoglin and placental abruption. PrenatDiagn 28(9), 852-858 (2008)
62. M. Noori, A.E. Donald, A. Angelakopoulou, A.D. Hingorani, D.J. Williams: Prospective study of placental angiogenic factors and maternal vascular function before and after preeclampsia and gestational hypertension. Circulation 122(5), 478-487 (2010)
63. A. Leaños-Miranda, I. Campos-Galicia, I. Isordia-Salas, R. Rivera-Leaños, J.F. Romero-Arauz, J.A. Ayala-Méndez, A. Ulloa-Aguirre: Changes in circulating concentrations of soluble fms-like tyrosine kinase-1 and placental growth factor measured by automated electrochemiluminescence immunoassays methods are predictors of preeclampsia. J Hypertens 30(11), 2173-2181 (2012)
64. S. Verlohren, I. Herraiz, O. Lapaire, D. Schlembach, M. Moertl, H. Zeisler, P. Calda, W. Holzgreve, A. Galindo, T. Engels, B. Denk, H. Stepan: The sFlt-1/PlGF ratio in different types of hypertensive pregnancy disorders and its prognostic potential in preeclamptic patients. Am J Obstet Gynecol 206(1), 58 e1-8 (2012)
65. A.C. Staff, K. Braekke, G.M. Johnsen, S.A. Karumanchi, N.K. Harsem: Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in pre-eclampsia. Am J Obstet Gynecol 197(2), 176 e1-6 (2007)
66. F. Dignat-George, J. Sampol: Circulating endothelial cells in vascular disorders: new insights into an old concept. Eur J Haematol 65(4), 215-220 (2000)
67. U. Erdbruegger, M. Haubitz, A. Woywodt: Circulating endothelial cells: a novel marker of endothelial damage. Clin Chim Acta 373(1-2), 17-26 (2006)
68. M. Haubitz, A. Woywodt: Circulating endothelial cells and vasculitis. Intern Med 43(8), 660-667 (2004)
69. F. Dignat-George, J. Sampol, G. Lip, A.D. Blann: Circulating endothelial cells: realities and promises in vascular disorders. Pathophysiol Haemost Thromb 33(5-6), 495-499 (2003/2004)
70. C. Holmén, E. Elsheikh, P. Stenvinkel, A.R. Qureshi, E. Pettersson, S. Jalkanen, S. Sumitran-Holgersson: Circulating inflammatory endothelial cells contribute to endothelial progenitor cell dysfunction in patients with vasculitis and kidney involvement. J Am SocNephrol 16(10), 3110-3120 (2005)
71. A. Woywodt, F. Streiber, K. de Groot, H. Regelsberger, H. Haller, M. Haubitz: Circulating endothelial cells as markers for ANCA-associated small-vessel vasculitis. Lancet 361(9353), 206-210 (2003)
72. B. Canbakan, K. Keven, H. Tutkak, N. Danisman, I. Ergun, G. Nergizoglu: Circulating endothelial cells in pre-eclampsia. J Hum Hypertens 21(7), 558-563 (2007)
73. M. Grundmann, A. Woywodt, T. Kirsch, B. Hollwitz, K. Oehler, U. Erdbruegger, H. Haller, M. Haubitz: Circulating endothelial cells: a marker of vascular damage in patients with pre-eclampsia. Am J Obstet Gynecol 198(3), 317 e1-5 (2008)
74. F. Mehrabian, S.M. Jazi, S.H. Javanmard, M. Kaviani, V. Homayouni: Circulating endothelial cells (CECs) and E-selectin: Predictors of pre-eclampsia. J Res Med Sci 17(1), 15-21 (2012)
75. M.H. Strijbos, C.A. Snijder, J. Kraan, C.H. Lamers, J.W. Gratama, J.J. Duvekot: Levels of circulating endothelial cells in normotensive and severe pre-eclamptic pregnancies. Cytometry B Clin Cytom 78(6), 382-386 (2010)
76. D. Burger, R.M. Touyz: Cellular biomarkers of endothelial health: microparticles, endothelial progenitor cells, and circulating endothelial cells. J Am Soc Hypertens 6(2), 85-99 (2012)
77. S. Rafii: Circulating endothelial precursors: mystery, reality, and promise. J Clin Invest 105(1), 17-19 (2000)
78. M. Gill, S. Dias, K. Hattori, M.L. Rivera, D. Hicklin, L. Witte, L. Girardi, R. Yurt, H. Himel, S. Rafii: Vascular trauma induces rapid but transient mobilization of VEGFR2 (+)AC133 (+) endothelial precursor cells. Circ Res 88(2), 167-174 (2001)
79. P. Carmeliet: Mechanisms of angiogenesis and arteriogenesis. Nat Med 6(4), 389-395 (2000)
80. P. Carmeliet: Angiogenesis in health and disease. Nat Med 9(6), 653-660 (2003)
81. D. Hanahan, J. Folkman: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86(3), 353-364 (1996)
82. J. Folkman: Role of angiogenesis in tumor growth and metastasis. Semin Oncol 29(6 Suppl 16), 15-8 (2002)
83. T. Asahara, H. Masuda, T. Takahashi, C. Kalka, C. Pastore, M. Silver, M. Kearne, M. Magner, J.M. Isner: Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85(3), 221-228 (1999)
84. T. Murayama, O.M. Tepper, M. Silver, H. Ma, D.W. Losordo, J.M. Isner, T. Asahara, C. Kalka: Determination of bone marrow-derived endothelial progenitor cell significance in angiogenic growth factor-induced neovascularization in vivo. ExpHematol 30(8), 967-972 (2002)
85. K. Strehlow, N. Werner, J. Berweiler, A. Link, U. Dirnagl, J. Priller, K. Laufs, L. Ghaeni, M. Milosevic, M. Böhm, G. Nickenig: Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation 107(24), 3059-3065 (2003)
86. A. Iwakura, C. Luedemann, S. Shastry, A. Hanley, M. Kearney, R. Aikawa, J.M. Isner, T. Asahara, D.W. Losordo: Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrow-derived endothelial progenitor cells contributes to re-endothelialization after arterial injury. Circulation 108(25), 3115-3121 (2003)
87. M. Vasa, S. Fichtlscherer, A. Aicher, K. Adler, C. Urbich, H. Martin, A.M. Zeiher, S. Dimmeler: Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89(1), E1-7 (2001)
88. O.M. Tepper, R.D. Galiano, J.M. Capla, C. Kalka, P.J. Gagne, G.R. Jacobowitz, J.P. Levine, G.C. Gurtner: Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106(22), 2781-2786 (2002)
89. A. Aicher, A.M. Zeiher, S. Dimmeler: Mobilizing endothelial progenitor cells. Hypertension 45(3), 321-325 (2005)
90. S. Rafii, S. Avecilla, S. Shmelkov, K. Shido, R. Tejada, M.A. Moore, B. Heissig, K. Hattori: Angiogenic factors reconstitute hematopoiesis by recruiting stem cells from bone marrow microenvironment. Ann N Y Acad Sci 996, 49-60 (2003)
91. A.O. Robb, N.L. Mills, D.E. Newby, F.C. Denison: Endothelial progenitor cells in pregnancy. Reproduction 133(1), 1-9 (2007)
92. J. Sugawara, M. Mitsui-Saito, T. Hoshiai, C. Hayashi, Y. Kimura, K. Okamura: Circulating endothelial progenitor cells during human pregnancy. J Clin Endocrinol Metab 90(3), 1845-1848 (2005)
93. P. Luppi, R.W. Powers, V. Verma, L. Edmunds, D. Plymire, C.A. Hubel: Maternal circulating CD34+VEGFR-2+ and CD133+VEGFR-2+ progenitor cells increase during normal pregnancy but are reduced in women with preeclampsia. Reprod Sci 17(7), 643-652 (2010)
94. K. Matsubara, E. Abe, Y. Matsubara, K. Kameda, M. Ito: Circulating endothelial progenitor cells during normal pregnancy and pre-eclampsia. Am J Reprod Immunol 56(2), 79-85 (2006)
95. J. Sugawara, M. Mitsui-Saito, C. Hayashi, T. Hoshiai, M. Senoo, H. Chisaka, N. Yaegashi, K. Okamura: Decrease and senescence of endothelial progenitor cells in patients with pre-eclampsia. J Clin Endocrinol Metab 90(9), 5329-5332 (2005)
96. C.W. Redman, I.L. Sargent: Circulating microparticles in normal pregnancy and pre-eclampsia. Placenta 29Suppl A, 73-77 (2008)
97. S.J. Germain, G.P. Sacks, S.R. Sooranna, I.L. Sargent, C.W. Redman: Systemic inflammatory priming in normal pregnancy and pre-eclampsia: the role of circulating syncytiotrophoblast microparticles. J Immunol 178(9), 5949-5956 (2007) Erratum in: J Immunol 179(2), 1390 (2007)
98. C. Beyer, D.S. Pisetsky: The role of microparticles in the pathogenesis of rheumatic diseases. Nat Rev Rheumatol 6(1), 21-29 (2010)
99. D. Burger, A.C. Montezano, N. Nishigaki, Y. He, A. Carter, R.M. Touyz: Endothelial microparticle formation by angiotensin II is mediated via Ang II receptor type I/NADPH oxidase/ Rho kinase pathways targeted to lipid rafts. Arterioscler Thromb Vasc Biol 31(8), 1898-1907 (2011)
100. G.N. Chironi, C.M. Boulanger, A. Simon, F. Dignat-George, J.M. Freyssinet, A. Tedgui: Endothelial microparticles in diseases. Cell Tissue Res 335(1), 143-151 (2009)
101. A.S. Leroyer, F. Anfosso, R. Lacroix, F. Sabatier, S. Simoncini, S.M. Njock, N. Jourde, P. Brunet, L. Camoin-Jau, J. Sampol, F. Dignat-George: Endothelial-derived microparticles: Biological conveyors at the crossroad of inflammation, thrombosis and angiogenesis. Thromb Haemost 104(3), 456-463 (2010)
102. J. Alijotas-Reig, C. Palacio-Garcia, I. Farran-Codina, C. Zarzoso, L. Cabero-Roura, M. Vilardell-Tarres: Circulating cell-derived microparticles in women with pregnancy loss. Am J Reprod Immunol 66(3), 199-208 (2011)
103. F. Bretelle, F. Sabatier, D. Desprez, L. Camoin, L. Grunebaum, V. Combes, C. D'Ercole, F. Dignat-George: Circulating microparticles: a marker of procoagulant state in normal pregnancy and pregnancy complicated by pre-eclampsia or intrauterine growth restriction. Thromb Haemost 89(3), 486-492 (2003)
104. V.H. González-Quintero, J.J. Jiménez, W. Jy, L.M. Mauro, L. Hortman, M.J. O'Sullivan, Y. Ahn: Elevated plasma endothelial microparticles in preeclampsia. Am J Obstet Gynecol 189(2), 589-593 (2003)
105. E. Reyna-Villasmil, J. Mejia-Montilla, N. Reyna-Villasmil, D. Torres-Cepeda, E. Peña-Paredes, J. Santos-Bolívar, J. Perozo-Romero: Endothelial microparticles in preeclampsia and eclampsia. Med Clin (Barc) 136(12), 522-526 (2011)
106. V.H. González-Quintero, L.P. Smarkusky, J.J. Jiménez, L.M. Mauro, W. Jy, L.L. Hortsman, M.J. O'Sullivan, Y.S. Ahn: Elevated plasma endothelial microparticles: pre-eclampsia versus gestational hypertension. Am J Obstet Gynecol 191(4), 1418-1424 (2004)
107. J. Alijotas-Reig, C. Palacio-Garcia, I. Farran-Codina, M. Ruiz-Romance, E. Llurba, M. Vilardell-Tarres: Circulating cell-derived microparticles in severe pre-eclampsia and in fetal growth restriction. Am J Reprod Immunol 67(2), 140-151 (2012)
108. C.M. Boulanger, A. Scoazec, T. Ebrahimian, P. Henry, E. Mathieu, A. Tedgui, Z. Mallat: Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation 104(22), 2649-2652 (2001)
109. S. Guller: Role of the syncytium in placenta-mediated complications of pre-eclampsia. Thromb Res 124(4), 389-392 (2009)
110. A.S. Aly, M. Khandelwal, J. Zhao, A.H. Mehmet, M.D. Sammel, S. Parry: Neutrophils are stimulated by syncytiotrophoblast microvillous membranes to generate superoxide radicals in women with pre-eclampsia. Am J Obstet Gynecol 190(1), 252-258 (2004)
111. O. Salomon, B.Z. Katz, R. Dardik, T. Livnat, D.M. Steinberg, R. Achiron, U. Seligsohn: Plasma levels of microparticles at 24 weeks of gestation do not predict subsequent pregnancy complications. Fertil Steril 92(2), 682-687 (2009)