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Semin Thromb Hemost 2010; 36(3): 309-320
DOI: 10.1055/s-0030-1253453
© Thieme Medical PublishersDOI: 10.1055/s-0030-1253453
Placental Vasculature in Health and Disease
Further Information
Publication History
Publication Date:
20 May 2010 (online)
ABSTRACT
Both angiogenesis and vasculogenesis occur during normal placental development. Additionally, the placenta undergoes a process of vascular mimicry (also referred to as pseudo-vasculogenesis) where the placental cytotrophoblasts that invade the spiral arteries convert from an epithelial to an endothelial phenotype during normal pregnancy. Failure of placental angiogenesis and pseudo-vasculogenesis during placental development has been linked to the pathogenesis of preeclampsia and related disorders such as intrauterine growth restriction. This review discusses placental vascular development during health and in disease with a focus on accumulating recent evidence that the maternal clinical syndrome of preeclampsia may be due to the result of excess antiangiogenic factors liberated by the diseased placenta.
KEYWORDS
Angiogenesis - hypertension - vascular endothelial growth factor - placental growth factor - preeclampsia
REFERENCES
- 1 Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol. 1995; 11 73-91
- 2 Risau W. Mechanisms of angiogenesis. Nature. 1997; 386(6626) 671-674
- 3 Demir R, Kaufmann P, Castellucci M, Erbengi T, Kotowski A. Fetal vasculogenesis and angiogenesis in human placental villi. Acta Anat (Basel). 1989; 136(3) 190-203
- 4 Cross J C, Werb Z, Fisher S J. Implantation and the placenta: key pieces of the development puzzle. Science. 1994; 266(5190) 1508-1518
- 5 Genbacev O, Zhou Y, Ludlow J W, Fisher S J. Regulation of human placental development by oxygen tension. Science. 1997; 277(5332) 1669-1672
- 6 Zhou Y, Fisher S J, Janatpour M et al.. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J Clin Invest. 1997; 99(9) 2139-2151
- 7 Jaffe R. First trimester utero-placental circulation: maternal-fetal interaction. J Perinat Med. 1998; 26(3) 168-174
- 8 Roth I, Fisher S J. IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion. Dev Biol. 1999; 205(1) 194-204
- 9 Lim K H, Zhou Y, Janatpour M et al.. Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am J Pathol. 1997; 151(6) 1809-1818
- 10 Brosens I A, Robertson W B, Dixon H G. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu. 1972; 1 177-191
- 11 Hanna J, Goldman-Wohl D, Hamani Y et al.. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med. 2006; 12(9) 1065-1074
- 12 Kohnen G, Kertschanska S, Demir R, Kaufmann P. Placental villous stroma as a model system for myofibroblast differentiation. Histochem Cell Biol. 1996; 105(6) 415-429
- 13 Kaufmann P, Bruns U, Leiser R, Luckhardt M, Winterhager E. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat Embryol (Berl). 1985; 173(2) 203-214
- 14 Kaufmann P, Luckhardt M, Schweikhart G, Cantle S J. Cross-sectional features and three-dimensional structure of human placental villi. Placenta. 1987; 8(3) 235-247
- 15 Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev. 1997; 18(1) 4-25
- 16 Shibuya M. Structure and function of VEGF/VEGF-receptor system involved in angiogenesis. Cell Struct Funct. 2001; 26(1) 25-35
- 17 Persico M G, Vincenti V, DiPalma T. Structure, expression and receptor-binding properties of placenta growth factor (PlGF). Curr Top Microbiol Immunol. 1999; 237 31-40
- 18 Carmeliet P, Moons L, Luttun A et al.. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med. 2001; 7(5) 575-583
- 19 Charnock-Jones D S, Burton G J. Placental vascular morphogenesis. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000; 14(6) 953-968
- 20 Jussila L, Alitalo K. Vascular growth factors and lymphangiogenesis. Physiol Rev. 2002; 82(3) 673-700
- 21 Olofsson B, Jeltsch M, Eriksson U, Alitalo K. Current biology of VEGF-B and VEGF-C. Curr Opin Biotechnol. 1999; 10(6) 528-535
- 22 Kendall R L, Thomas K A. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A. 1993; 90(22) 10705-10709
- 23 He Y, Smith S K, Day K A, Clark D E, Licence D R, Charnock-Jones D S. Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol Endocrinol. 1999; 13(4) 537-545
- 24 Papapetropoulos A, García-Cardeña G, Dengler T J, Maisonpierre P C, Yancopoulos G D, Sessa W C. Direct actions of angiopoietin-1 on human endothelium: evidence for network stabilization, cell survival, and interaction with other angiogenic growth factors. Lab Invest. 1999; 79(2) 213-223
- 25 Koblizek T I, Weiss C, Yancopoulos G D, Deutsch U, Risau W. Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr Biol. 1998; 8(9) 529-532
- 26 Davis S, Aldrich T H, Jones P F et al.. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell. 1996; 87(7) 1161-1169
- 27 Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000; 6(4) 389-395
- 28 Thurston G, Rudge J S, Ioffe E et al.. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med. 2000; 6(4) 460-463
- 29 Thurston G, Suri C, Smith K et al.. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 1999; 286(5449) 2511-2514
- 30 Stratmann A, Acker T, Burger A M, Amann K, Risau W, Plate K H. Differential inhibition of tumor angiogenesis by tie2 and vascular endothelial growth factor receptor-2 dominant-negative receptor mutants. Int J Cancer. 2001; 91(3) 273-282
- 31 Tanaka S, Mori M, Sakamoto Y, Makuuchi M, Sugimachi K, Wands J R. Biologic significance of angiopoietin-2 expression in human hepatocellular carcinoma. J Clin Invest. 1999; 103(3) 341-345
- 32 Maisonpierre P C, Suri C, Jones P F et al.. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 1997; 277(5322) 55-60
- 33 Wulff C, Wilson H, Dickson S E, Wiegand S J, Fraser H M. Hemochorial placentation in the primate: expression of vascular endothelial growth factor, angiopoietins, and their receptors throughout pregnancy. Biol Reprod. 2002; 66(3) 802-812
- 34 Charnock-Jones D S, Sharkey A M, Boocock C A et al.. Vascular endothelial growth factor receptor localization and activation in human trophoblast and choriocarcinoma cells. Biol Reprod. 1994; 51(3) 524-530
- 35 Cooper J C, Sharkey A M, McLaren J, Charnock-Jones D S, Smith S K. Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J Reprod Fertil. 1995; 105(2) 205-213
- 36 Geva E, Ginzinger D G, Zaloudek C J, Moore D H, Byrne A, Jaffe R B. Human placental vascular development: vasculogenic and angiogenic (branching and nonbranching) transformation is regulated by vascular endothelial growth factor-A, angiopoietin-1, and angiopoietin-2. J Clin Endocrinol Metab. 2002; 87(9) 4213-4224
- 37 Clark D E, Smith S K, Sharkey A M, Charnock-Jones D S. Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod. 1996; 11(5) 1090-1098
- 38 Zhou Y, McMaster M, Woo K et al.. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol. 2002; 160(4) 1405-1423
- 39 Hildebrandt V A, Babischkin J S, Koos R D, Pepe G J, Albrecht E D. Developmental regulation of vascular endothelial growth/permeability factor messenger ribonucleic acid levels in and vascularization of the villous placenta during baboon pregnancy. Endocrinology. 2001; 142(5) 2050-2057
- 40 Shalaby F, Rossant J, Yamaguchi T P et al.. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995; 376(6535) 62-66
- 41 Fong G H, Rossant J, Gertsenstein M, Breitman M L. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature. 1995; 376(6535) 66-70
- 42 Ain R, Canham L N, Soares M J. Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol. 2003; 260(1) 176-190
- 43 Zhou Y, Bellingard V, Feng K T, McMaster M, Fisher S J. Human cytotrophoblasts promote endothelial survival and vascular remodeling through secretion of Ang2, PlGF, and VEGF-C. Dev Biol. 2003; 263(1) 114-125
- 44 Rowe A J, Wulff C, Fraser H M. Localization of mRNA for vascular endothelial growth factor (VEGF), angiopoietins and their receptors during the peri-implantation period and early pregnancy in marmosets (Callithrix jacchus). Reproduction. 2003; 126(2) 227-238
- 45 Dunk C, Shams M, Nijjar S et al.. Angiopoietin-1 and angiopoietin-2 activate trophoblast Tie-2 to promote growth and migration during placental development. Am J Pathol. 2000; 156(6) 2185-2199
- 46 Zhang E G, Smith S K, Baker P N, Charnock-Jones D S. The regulation and localization of angiopoietin-1, -2, and their receptor Tie2 in normal and pathologic human placentae. Mol Med. 2001; 7(9) 624-635
- 47 Goldman-Wohl D S, Ariel I, Greenfield C, Lavy Y, Yagel S. Tie-2 and angiopoietin-2 expression at the fetal-maternal interface: a receptor ligand model for vascular remodelling. Mol Hum Reprod. 2000; 6(1) 81-87
- 48 Clark D E, Smith S K, He Y et al.. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod. 1998; 59(6) 1540-1548
- 49 Bdolah Y, Sukhatme V P, Karumanchi S A. Angiogenic imbalance in the pathophysiology of preeclampsia: newer insights. Semin Nephrol. 2004; 24(6) 548-556
- 50 Walker J J. Pre-eclampsia. Lancet. 2000; 356(9237) 1260-1265
- 51 Page E W. The relation between hydatid moles, relative ischemia of the gravid uterus and the placental origin of eclampsia. Am J Obstet Gynecol. 1939; 37 291-293
- 52 Red-Horse K, Zhou Y, Genbacev O et al.. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest. 2004; 114(6) 744-754
- 53 Zhou Y, Damsky C H, Fisher S J. Preeclampsia 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. 1997; 99(9) 2152-2164
- 54 Moldenhauer J S, Stanek J, Warshak C, Khoury J, Sibai B. The frequency and severity of placental findings in women with preeclampsia are gestational age dependent. Am J Obstet Gynecol. 2003; 189(4) 1173-1177
- 55 Harrington K, Cooper D, Lees C, Hecher K, Campbell S. Doppler ultrasound of the uterine arteries: the importance of bilateral notching in the prediction of pre-eclampsia, placental abruption or delivery of a small-for-gestational-age baby. Ultrasound Obstet Gynecol. 1996; 7(3) 182-188
- 56 Makris A, Thornton C, Thompson J et al.. Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int. 2007; 71(10) 977-984
- 57 Roberts J M, Taylor R N, Musci T J, Rodgers G M, Hubel C A, McLaughlin M K. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol. 1989; 161(5) 1200-1204
- 58 Ferris T F. Pregnancy, preeclampsia, and the endothelial cell. N Engl J Med. 1991; 325(20) 1439-1440
- 59 Roberts J M. Endothelial dysfunction in preeclampsia. Semin Reprod Endocrinol. 1998; 16(1) 5-15
- 60 Fisher K A, Luger A, Spargo B H, Lindheimer M D. Hypertension in pregnancy: clinical-pathological correlations and remote prognosis. Medicine (Baltimore). 1981; 60(4) 267-276
- 61 Thorp Jr J M, White II G C, Moake J L, Bowes Jr W A. von Willebrand factor multimeric levels and patterns in patients with severe preeclampsia. Obstet Gynecol. 1990; 75(2) 163-167
- 62 Redman C W, Sacks G P, Sargent I L. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol. 1999; 180(2 Pt 1) 499-506
- 63 Calvin S, Corrigan J, Weinstein L, Jeter M. Factor VIII: von Willebrand factor patterns in the plasma of patients with pre-eclampsia. Am J Perinatol. 1988; 5(1) 29-32
- 64 Lockwood C J, Peters J H. Increased plasma levels of ED1 + cellular fibronectin precede the clinical signs of preeclampsia. Am J Obstet Gynecol. 1990; 162(2) 358-362
- 65 Friedman S A, de Groot C J, Taylor R N, Golditch B D, Roberts J M. Plasma cellular fibronectin as a measure of endothelial involvement in preeclampsia and intrauterine growth retardation. Am J Obstet Gynecol. 1994; 170(3) 838-841
- 66 Taylor R N, Crombleholme W R, Friedman S A, Jones L A, Casal D C, Roberts J M. High plasma cellular fibronectin levels correlate with biochemical and clinical features of preeclampsia but cannot be attributed to hypertension alone. Am J Obstet Gynecol. 1991; 165(4 Pt 1) 895-901
- 67 Minakami H, Takahashi T, Izumi A, Tamada T. Increased levels of plasma thrombomodulin in preeclampsia. Gynecol Obstet Invest. 1993; 36(4) 208-210
- 68 Boffa M C, Valsecchi L, Fausto A et al.. Predictive value of plasma thrombomodulin in preeclampsia and gestational hypertension. Thromb Haemost. 1998; 79(6) 1092-1095
- 69 Mills J L, DerSimonian R, Raymond E et al.. Prostacyclin and thromboxane changes predating clinical onset of preeclampsia: a multicenter prospective study. JAMA. 1999; 282(4) 356-362
- 70 Roberts J M, Edep M E, Goldfien A, Taylor R N. Sera from preeclamptic women specifically activate human umbilical vein endothelial cells in vitro: morphological and biochemical evidence. Am J Reprod Immunol. 1992; 27(3–4) 101-108
- 71 Roberts J M. Preeclampsia: what we know and what we do not know. Semin Perinatol. 2000; 24(1) 24-28
- 72 Hasan K M, Manyonda I T, Ng F S, Singer D R, Antonios T F. Skin capillary density changes in normal pregnancy and pre-eclampsia. J Hypertens. 2002; 20(12) 2439-2443
- 73 Jónsdóttir L S, Arngrímsson R, Geirsson R T, Sigvaldason H, Sigfússon N. Death rates from ischemic heart disease in women with a history of hypertension in pregnancy. Acta Obstet Gynecol Scand. 1995; 74(10) 772-776
- 74 Maynard S E, Min J Y, Merchan J et al.. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003; 111(5) 649-658
- 75 Levine R J, Maynard S E, Qian C et al.. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004; 350(7) 672-683
- 76 Polliotti B M, Fry A G, Saller D N, Mooney R A, Cox C, Miller R K. Second-trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early-onset preeclampsia. Obstet Gynecol. 2003; 101(6) 1266-1274
- 77 Tsatsaris V, Goffin F, Munaut C et al.. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab. 2003; 88(11) 5555-5563
- 78 Bujold E, Romero R, Chaiworapongsa T et al.. Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin. J Matern Fetal Neonatal Med. 2005; 18(1) 9-16
- 79 Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res. 2004; 95(9) 884-891
- 80 Levine R J, Thadhani R, Qian C et al.. Urinary placental growth factor and risk of preeclampsia. JAMA. 2005; 293(1) 77-85
- 81 Levine R J, Lam C, Qian C CPEP Study Group et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med. 2006; 355(10) 992-1005
- 82 Venkatesha S, Toporsian M, Lam C et al.. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006; 12(6) 642-649
- 83 Kusanovic J P, Romero R, Chaiworapongsa T et al.. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia. J Matern Fetal Neonatal Med. 2009; 22(11) 1021-1038
- 84 Romero R, Nien J K, Espinoza J et al.. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med. 2008; 21(1) 9-23
- 85 Morbidelli L, Chang C H, Douglas J G, Granger H J, Ledda F, Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol. 1996; 270(1 Pt 2) H411-H415
- 86 He H, Venema V J, Gu X, Venema R C, Marrero M B, Caldwell R B. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem. 1999; 274(35) 25130-25135
- 87 Kim Y G, Suga S I, Kang D H et al.. Vascular endothelial growth factor accelerates renal recovery in experimental thrombotic microangiopathy. Kidney Int. 2000; 58(6) 2390-2399
- 88 Masuda Y, Shimizu A, Mori T et al.. Vascular endothelial growth factor enhances glomerular capillary repair and accelerates resolution of experimentally induced glomerulonephritis. Am J Pathol. 2001; 159(2) 599-608
- 89 Kang D H, Kim Y G, Andoh T F et al.. Post-cyclosporine-mediated hypertension and nephropathy: amelioration by vascular endothelial growth factor. Am J Physiol Renal Physiol. 2001; 280(4) F727-F736
- 90 Yang J C, Haworth L, Sherry R M et al.. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003; 349(5) 427-434
- 91 Eremina V, Jefferson J A, Kowalewska J et al.. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008; 358(11) 1129-1136
- 92 Patel T V, Morgan J A, Demetri G D et al.. A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J Natl Cancer Inst. 2008; 100(4) 282-284
- 93 Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W. Vascular endothelial growth factor induces endothelial fenestrations in vitro. J Cell Biol. 1998; 140(4) 947-959
- 94 Eremina V, Sood M, Haigh J et al.. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003; 111(5) 707-716
- 95
Bergmann A, Ahmad S, Cudmore M et al..
Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a
mouse model.
J Cell Mol Med.
2009;
, June 16 (Epub ahead of print)
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- 96 Gilbert J S, Verzwyvelt J, Colson D et al.. Recombinant vascular endothelial growth factor 121 infusion lowers blood pressure and improves renal function in rats with placental ischemia-induced hypertension. Hypertension. 2010; 55(2) 380-385
- 97 Li Z, Zhang Y, Ying Ma J et al.. Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension. 2007; 50(4) 686-692
- 98 Powers R W, Roberts J M, Cooper K M et al.. Maternal serum soluble fms-like tyrosine kinase 1 concentrations are not increased in early pregnancy and decrease more slowly postpartum in women who develop preeclampsia. Am J Obstet Gynecol. 2005; 193(1) 185-191
- 99 Parikh S M, Karumanchi S A. Putting pressure on pre-eclampsia. Nat Med. 2008; 14(8) 810-812
- 100 Heydarian M, McCaffrey T, Florea L et al.. Novel splice variants of sFlt1 are upregulated in preeclampsia. Placenta. 2009; 30(3) 250-255
- 101 Sela S, Itin A, Natanson-Yaron S et al.. A novel human-specific soluble vascular endothelial growth factor receptor 1: cell-type-specific splicing and implications to vascular endothelial growth factor homeostasis and preeclampsia. Circ Res. 2008; 102(12) 1566-1574
- 102 Thomas C P, Andrews J I, Liu K Z. Intronic polyadenylation signal sequences and alternate splicing generate human soluble Flt1 variants and regulate the abundance of soluble Flt1 in the placenta. FASEB J. 2007; 21(14) 3885-3895
- 103 Karumanchi S A, Maynard S E, Stillman I E, Epstein F H, Sukhatme V P. Preeclampsia: a renal perspective. Kidney Int. 2005; 67(6) 2101-2113
- 104 Wallukat G, Homuth V, Fischer T et al.. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest. 1999; 103(7) 945-952
- 105 Gant N F, Daley G L, Chand S, Whalley P J, MacDonald P C. A study of angiotensin II pressor response throughout primigravid pregnancy. J Clin Invest. 1973; 52(11) 2682-2689
- 106 Dechend R, Homuth V, Wallukat G et al.. AT(1) receptor agonistic antibodies from preeclamptic patients cause vascular cells to express tissue factor. Circulation. 2000; 101(20) 2382-2387
- 107 Zhou C C, Zhang Y, Irani R A et al.. Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med. 2008; 14(8) 855-862
- 108 Zhou C C, Ahmad S, Mi T et al.. Autoantibody from women with preeclampsia induces soluble Fms-like tyrosine kinase-1 production via angiotensin type 1 receptor and calcineurin/nuclear factor of activated T-cells signaling. Hypertension. 2008; 51(4) 1010-1019
- 109 Herse F, Dechend R, Harsem N K et al.. Dysregulation of the circulating and tissue-based renin-angiotensin system in preeclampsia. Hypertension. 2007; 49(3) 604-611
- 110 Dechend R, Müller D N, Wallukat G et al.. AT1 receptor agonistic antibodies, hypertension, and preeclampsia. Semin Nephrol. 2004; 24(6) 571-579
- 111 Dragun D, Müller D N, Bräsen J H et al.. Angiotensin II type 1-receptor activating antibodies in renal-allograft rejection. N Engl J Med. 2005; 352(6) 558-569
- 112 Walther T, Wallukat G, Jank A et al.. Angiotensin II type 1 receptor agonistic antibodies reflect fundamental alterations in the uteroplacental vasculature. Hypertension. 2005; 46(6) 1275-1279
- 113 Baschat A A, Hecher K. Fetal growth restriction due to placental disease. Semin Perinatol. 2004; 28(1) 67-80
- 114 Mayhew T M, Wijesekara J, Baker P N, Ong S S. Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta. 2004; 25(10) 829-833
- 115 Chaddha V, Viero S, Huppertz B, Kingdom J. Developmental biology of the placenta and the origins of placental insufficiency. Semin Fetal Neonatal Med. 2004; 9(5) 357-369
- 116 Pardi G, Marconi A M, Cetin I. Placental-fetal interrelationship in IUGR fetuses—a review. Placenta. 2002; 23(suppl A) S136-141
- 117 DeChiara T M, Efstratiadis A, Robertson E J. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature. 1990; 345(6270) 78-80
- 118 Crossey P A, Pillai C C, Miell J P. Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest. 2002; 110(3) 411-418
- 119 Baker J, Liu J P, Robertson E J, Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell. 1993; 75(1) 73-82
- 120 Abuzzahab M J, Schneider A, Goddard A Intrauterine Growth Retardation (IUGR) Study Group et al. IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med. 2003; 349(23) 2211-2222
- 121 Lopez-Lopez C, LeRoith D, Torres-Aleman I. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci U S A. 2004; 101(26) 9833-9838
- 122 Herr F, Liang O D, Herrero J et al.. Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy. J Clin Endocrinol Metab. 2003; 88(10) 4811-4817
- 123 Rabinovsky E D, Draghia-Akli R. Insulin-like growth factor I plasmid therapy promotes in vivo angiogenesis. Mol Ther. 2004; 9(1) 46-55
- 124 Krantz D, Goetzl L, Simpson J L First Trimester Maternal Serum Biochemistry and Fetal Nuchal Translucency Screening (BUN) Study Group et al. Association of extreme first-trimester free human chorionic gonadotropin-beta, pregnancy-associated plasma protein A, and nuchal translucency with intrauterine growth restriction and other adverse pregnancy outcomes. Am J Obstet Gynecol. 2004; 191(4) 1452-1458
- 125 Smith G C, Stenhouse E J, Crossley J A, Aitken D A, Cameron A D, Connor J M. Early pregnancy levels of pregnancy-associated plasma protein a and the risk of intrauterine growth restriction, premature birth, preeclampsia, and stillbirth. J Clin Endocrinol Metab. 2002; 87(4) 1762-1767
- 126 Shibata E, Rajakumar A, Powers R W et al.. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab. 2005; 90(8) 4895-4903
- 127 Malamitsi-Puchner A, Boutsikou T, Economou E et al.. The role of the anti-angiogenic factor endostatin in intrauterine growth restriction. J Soc Gynecol Investig. 2005; 12(3) 195-197
- 128 Lepercq J, Guerre-Millo M, André J, Caüzac M, Hauguel-de Mouzon S. Leptin: a potential marker of placental insufficiency. Gynecol Obstet Invest. 2003; 55(3) 151-155
- 129 Savvidou M D, Hingorani A D, Tsikas D, Frölich J C, Vallance P, Nicolaides K H. Endothelial dysfunction and raised plasma concentrations of asymmetric dimethylarginine in pregnant women who subsequently develop pre-eclampsia. Lancet. 2003; 361(9368) 1511-1517
- 130 Lachmeijer A M, Dekker G A, Pals G, Aarnoudse J G, ten Kate L P, Arngrímsson R. Searching for preeclampsia genes: the current position. Eur J Obstet Gynecol Reprod Biol. 2002; 105(2) 94-113
- 131 Lam C, Lim K H, Karumanchi S A. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension. 2005; 46(5) 1077-1085
S. Ananth KarumanchiM.D.
Beth Israel Deaconess Medical Center
99 Brookline Avenue, Boston, MA 02215
Email: sananth@bidmc.harvard.edu