Preeclampsia, a disease of the maternal endothelium: The role of antiangiogenic factors and implications for later cardiovascular disease

Circulation

Volumn 123, Issue 24, 2011, Pages 2856-2869

  Powe, Camille E ^a   Levine, Richard J ^b   Karumanchi, S Ananth ^c,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

hypertension; preeclampsia; pregnancy; proteinuria; VEGF

Indexed keywords

CATECHOL METHYLTRANSFERASE; ENDOTHELIAL CELL GROWTH FACTOR; PLACENTAL GROWTH FACTOR; PROTEIN TYROSINE KINASE; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BLOOD VESSEL PERMEABILITY; DISEASE SEVERITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HYPERTENSION; IN VIVO STUDY; MATERNAL DISEASE; NONHUMAN; OXIDATIVE STRESS; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM;

ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; PRE-ECLAMPSIA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS;

EID: 79959507759     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.853127     Document Type: Article

References (191)

1. ACOG Practice Bulletin Committee. Diagnosis and management of preeclampsia and eclampsia. Obstet Gynecol. 2002;99:159-167.
2. Berg CJ, Mackay AP, Qin C, Callaghan WM. Overview of maternal morbidity during hospitalization for labor and delivery in the United States: 1993-1997 and 2001-2005. Obstet Gynecol. 2009;113: 1075-1081.
3. MacKay AP, Berg CJ, Atrash HK. Pregnancy-related mortality from preeclampsia and eclampsia. Obstet Gynecol. 2001;97:533-538.
4. Liu A, Wen SW, Bottomley J, Walker MC, Smith G. Utilization of health care services of pregnant women complicated by preeclampsia in Ontario. Hypertens Pregnancy. 2009;28:76-84.
5. Thadhani R, Ecker JL, Kettyle E, Sandler L, Frigoletto FD. Pulse pressure and risk of preeclampsia: a prospective study. Obstet Gynecol. 2001;97:515-520.
6. Bosio PM, McKenna PJ, Conroy R, O'Herlihy C. Maternal central hemodynamics in hypertensive disorders of pregnancy. Obstet Gynecol. 1999;94:978-984.
7. Lafayette RA, Druzin M, Sibley R, Derby G, Malik T, Huie P, Polhemus C, Deen WM, Myers BD. Nature of glomerular dysfunction in pre-eclampsia. Kidney Int. 1998;54:1240-1249. (Pubitemid 28449911)
8. Stillman IE, Karumanchi SA. The glomerular injury of preeclampsia. J Am Soc Nephrol. 2007;18:2281-2284. (Pubitemid 47203843)
9. Garovic VD, Wagner SJ, Turner ST, Rosenthal DW, Watson WJ, Brost BC, Rose CH, Gavrilova L, Craigo P, Bailey KR, Achenbach J, Schiffer M, Grande JP. Urinary podocyte excretion as a marker for preeclampsia. Am J Obstet Gynecol. 2007;196:320 e321-e327.
10. Rolfes DB, Ishak KG. Liver disease in toxemia of pregnancy. Am J Gastroenterol. 1986;81:1138-1144. (Pubitemid 17216841)
11. Sibai BM, Ramadan MK, Usta I, Salama M, Mercer BM, Friedman SA. Maternal morbidity and mortality in 442 pregnancies with hemolysis, elevated liver enzymes, and low platelets (HELLP syndrome). Am J Obstet Gynecol. 1993;169:1000-1006. (Pubitemid 23317544)
12. Weinstein L. Syndrome of hemolysis, elevated liver enzymes, and low platelet count: a severe consequence of hypertension in pregnancy. Am J Obstet Gynecol. 1982;142:159-167. (Pubitemid 12222094)
13. Isler CM, Rinehart BK, Terrone DA, Martin RW, Magann EF, Martin JN Jr. Maternal mortality associated with HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome. Am J Obstet Gynecol. 1999;181:924-928. (Pubitemid 29503617)
14. Hinchey J, Chaves C, Appignani B, Breen J, Pao L, Wang A, Pessin MS, Lamy C, Mas JL, Caplan LR. A reversible posterior leukoencepha-lopathy syndrome. N Engl J Med. 1996;334:494-500.
15. Sibai BM. Diagnosis, prevention, and management of eclampsia. Obstet Gynecol. 2005;105:402-410. (Pubitemid 40229462)
16. Wolf M, Sandler L, Munoz K, Hsu K, Ecker JL, Thadhani R. First trimester insulin resistance and subsequent preeclampsia: a prospective study. J Clin Endocrinol Metab. 2002;87:1563-1568. (Pubitemid 34615240)
17. Hansen AR, Barnes CM, Folkman J, McElrath TF. Maternal pre-eclampsia predicts the development of bronchopulmonary dysplasia. J Pediatr. 2010;156:532-536.
18. Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet. 2005;365: 785-799. (Pubitemid 40311367)
19. Esplin MS, Fausett MB, Fraser A, Kerber R, Mineau G, Carrillo J, Varner MW. Paternal and maternal components of the predisposition to preeclampsia. N Engl J Med. 2001;344:867-872. (Pubitemid 32224394)
20. Duckitt K, Harrington D. Risk factors for pre-eclampsia at antenatal booking: systematic review of controlled studies. BMJ. 2005;330:565.
21. Tubbergen P, Lachmeijer AM, Althuisius SM, Vlak ME, van Geijn HP, Dekker GA. Change in paternity: a risk factor for preeclampsia in multiparous women? J Reprod Immunol. 1999;45:81-88. (Pubitemid 29486732)
22. Skjaerven R, Wilcox AJ, Lie RT. The interval between pregnancies and the risk of preeclampsia. N Engl J Med. 2002;346:33-38. (Pubitemid 34438917)
23. Klonoff-Cohen HS, Savitz DA, Cefalo RC, McCann MF. An epidemi-ologic study of contraception and preeclampsia. JAMA. 1989;262: 3143-3147.
24. Wang JX, Knottnerus AM, Schuit G, Norman RJ, Chan A, Dekker GA. Surgically obtained sperm, and risk of gestational hypertension and pre-eclampsia. Lancet. 2002;359:673-674. (Pubitemid 34203769)
25. Yogev, Chen, Hod, Coustan, Oats, McIntyre, Metzger, Lowe, Dyer, Dooley, Trimble, McCance, Hadden, Persson, Rogers; Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study Cooperative Research Group. Hyperglycemia and Adverse Pregnancy Outcome (HAPO) study: preeclampsia. Am J Obstet Gynecol. 2010;202:255.e1-255.e7.
26. Wolf M, Kettyle E, Sandler L, Ecker JL, Roberts J, Thadhani R. Obesity and preeclampsia: the potential role of inflammation. Obstet Gynecol. 2001;98:757-762. (Pubitemid 33042541)
27. Conde-Agudelo A, Althabe F, Belizan JM, Kafury-Goeta AC. Cigarette smoking during pregnancy and risk of preeclampsia: a systematic review. Am J Obstet Gynecol. 1999;181:1026-1035. (Pubitemid 29503633)
28. Sibai BM, Stella CL. Diagnosis and management of atypical preeclampsia-eclampsia. Am J Obstet Gynecol. 2009;200: 481.e481-481.e487.
29. Thangaratinam S, Ismail KM, Sharp S, Coomarasamy A, Khan KS. Accuracy of serum uric acid in predicting complications of pre-eclampsia: a systematic review. BJOG. 2006;113:369-378.
30. Lim KH, Friedman SA, Ecker JL, Kao L, Kilpatrick SJ. The clinical utility of serum uric acid measurements in hypertensive diseases of pregnancy. Am J Obstet Gynecol. 1998;178:1067-1071. (Pubitemid 28247188)
31. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003;111:649-658. (Pubitemid 36278583)
32. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D'Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006;12:642-649. (Pubitemid 43865232)
33. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med. 2006;355:992-1005. (Pubitemid 44343543)
34. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004;350:672-683. (Pubitemid 38364626)
35. Noori M, Donald AE, Angelakopoulou A, Hingorani AD, Williams DJ. Prospective study of placental angiogenic factors and maternal vascular function before and after preeclampsia and gestational hypertension. Circulation. 2010;122:478-487.
36. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, Mazor M. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med. 2005;17:3-18. (Pubitemid 40515938)
37. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Goncalves LF, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the patho-physiology of preeclampsia: Young Investigator Award. Am J Obstet Gynecol. 2004;190:1541-1547; discussion 1547-1550.
38. Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res. 2004;95:884-891. (Pubitemid 39435003)
39. Matsuo K, Kooshesh S, Dinc M, Sun CC, Kimura T, Baschat AA. Late postpartum eclampsia: report of two cases managed by uterine curettage and review of the literature. Am J Perinatol. 2007;24:257-266. (Pubitemid 46676708)
40. Soto-Wright V, Bernstein M, Goldstein DP, Berkowitz RS. The changing clinical presentation of complete molar pregnancy. Obstet Gynecol. 1995;86:775-779.
41. Salafia CM, Pezzullo JC, Lopez-Zeno JA, Simmens S, Minior VK, Vintzileos AM. Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol. 1995;173:1097-1105.
42. Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest. 1992;89:210-222.
43. Zhou Y, Damsky CH, Chiu K, Roberts JM, Fisher SJ. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest. 1993;91:950-960. (Pubitemid 23095269)
44. Zhou Y, Damsky CH, Fisher SJ. 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;99:2152-2164. (Pubitemid 27203771)
45. Lam C, Lim KH, Karumanchi SA. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension. 2005;46: 1077-1085. (Pubitemid 41533005)
46. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest. 1996;97:540-550. (Pubitemid 26039422)
47. Palmer SK, Moore LG, Young D, Cregger B, Berman JC, Zamudio S. Altered blood pressure course during normal pregnancy and increased preeclampsia at high altitude (3100 meters) in Colorado. Am J Obstet Gynecol. 1999;180:1161-1168. (Pubitemid 29259011)
48. North RA, Ferrier C, Long D, Townend K, Kincaid-Smith P. Uterine artery Doppler flow velocity waveforms in the second trimester for the prediction of preeclampsia and fetal growth retardation. Obstet Gynecol. 1994;83:378-386. (Pubitemid 24067806)
49. Granger JP, LaMarca BB, Cockrell K, Sedeek M, Balzi C, Chandler D, Bennett W. Reduced uterine perfusion pressure (RUPP) model for studying cardiovascular-renal dysfunction in response to placental ischemia. Methods Mol Med. 2006;122:383-392.
50. Makris A, Thornton C, Thompson J, Thomson S, Martin R, Ogle R, Waugh R, McKenzie P, Kirwan P, Hennessy A. Uteroplacental ischemia results in proteinuric hypertension and elevated sFlt-1. Kidney Int. 2007; 71:977-984. (Pubitemid 46741987)
51. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306-1309. (Pubitemid 20066716)
52. Keck PJ, Hauser SD, Krivi G, Sanzo K, Warren T, Feder J, Connolly DT. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science. 1989;246:1309-1312. (Pubitemid 20066717)
53. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci U S A. 1991;88: 9267-9271. (Pubitemid 21915612)
54. Park JE, Chen HH, Winer J, Houck KA, Ferrara N. Placenta growth factor: potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem. 1994;269:25646-25654.
55. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem. 1994;269: 26988-26995. (Pubitemid 24332901)
56. Keyt BA, Nguyen HV, Berleau LT, Duarte CM, Park J, Chen H, Ferrara N. Identification of vascular endothelial growth factor determinants for binding KDR and Flt-1 receptors: generation of receptor-selective VEGF variants by site-directed mutagenesis. J Biol Chem. 1996;271: 5638-5646.
57. Clauss M, Weich H, Breier G, Knies U, Rockl W, Waltenberger J, Risau W. The vascular endothelial growth factor receptor Flt-1 mediates biological activities: implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem. 1996;271: 17629-17634. (Pubitemid 26250731)
58. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62-66.
59. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angio-genesis in mice. Proc Natl Acad Sci U S A. 1998;95:9349-9354. (Pubitemid 28506234)
60. Chappell JC, Taylor SM, Ferrara N, Bautch VL. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev Cell. 2009;17: 377-386.
61. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439-442. (Pubitemid 26102720)
62. Maharaj AS, Saint-Geniez M, Maldonado AE, D'Amore PA. Vascular endothelial growth factor localization in the adult. Am J Pathol. 2006; 168:639-648. (Pubitemid 43271161)
63. 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;140:947-959. (Pubitemid 28141231)
64. Kamba T, Tam BY, Hashizume H, Haskell A, Sennino B, Mancuso MR, Norberg SM, O'Brien SM, Davis RB, Gowen LC, Anderson KD, Thurston G, Joho S, Springer ML, Kuo CJ, McDonald DM. VEGF-dependent plasticity of fenestrated capillaries in the normal adult micro-vasculature. Am J Physiol. 2006;290:H560-H576.
65. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest. 2003;111:707-716. (Pubitemid 36278589)
66. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N. VEGF is required for growth and survival in neonatal mice. Development. 1999;126:1149-1159. (Pubitemid 29182112)
67. LeCouter J, Moritz DR, Li B, Phillips GL, Liang XH, Gerber HP, Hillan KJ, Ferrara N. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science. 2003;299:890-893. (Pubitemid 36182447)
68. Maharaj AS, Walshe TE, Saint-Geniez M, Venkatesha S, Maldonado AE, Himes NC, Matharu KS, Karumanchi SA, D'Amore PA. VEGF and TGF-beta are required for the maintenance of the choroid plexus and ependyma. J Exp Med. 2008;205:491-501. (Pubitemid 351281612)
69. Ku DD, Zaleski JK, Liu S, Brock TA. Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am J Physiol. 1993;265:H586-H592. (Pubitemid 23273595)
70. He H, Venema VJ, Gu X, Venema RC, Marrero MB, Caldwell RB. 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;274:25130-25135.
71. Wheeler-Jones C, Abu-Ghazaleh R, Cospedal R, Houliston RA, Martin J, Zachary I. Vascular endothelial growth factor stimulates prostacyclin production and activation of cytosolic phospholipase A2 in endothelial cells via p42/p44 mitogen-activated protein kinase. FEBS Lett. 1997; 420:28-32. (Pubitemid 28037194)
72. Facemire CS, Nixon AB, Griffiths R, Hurwitz H, Coffman TM. Vascular endothelial growth factor receptor 2 controls blood pressure by regulating nitric oxide synthase expression. Hypertension. 2009;54: 652-658.
73. Glusker P, Recht L, Lane B. Reversible posterior leukoencephalopathy syndrome and bevacizumab. N Engl J Med. 2006;354:980-982; discussion 980-982.
74. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F. Bevacizumab plus irinotecan, fluo-rouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350:2335-2342. (Pubitemid 38702844)
75. Miller K, Wang M, Gralow J, Dickler M, Cobleigh M, Perez EA, Shenkier T, Cella D, Davidson NE. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med. 2007;357: 2666-2676.
76. Yang JC, Haworth L, Sherry RM, Hwu P, Schwartzentruber DJ, Topalian SL, Steinberg SM, Chen HX, Rosenberg SA. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med. 2003;349:427-434. (Pubitemid 36910021)
77. Patel TV, Morgan JA, Demetri GD, George S, Maki RG, Quigley M, Humphreys BD. 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: 282-284. (Pubitemid 351480534)
78. Eremina V, Jefferson JA, Kowalewska J, Hochster H, Haas M, Weisstuch J, Richardson C, Kopp JB, Kabir MG, Backx PH, Gerber HP, Ferrara N, Barisoni L, Alpers CE, Quaggin SE. VEGF inhibition and renal thrombotic microangiopathy. N Engl J Med. 2008;358:1129-1136. (Pubitemid 351398487)
79. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med. 2001;7:575-583. (Pubitemid 32448325)
80. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P. Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med. 2002;8:831-840.
81. Autiero M, Waltenberger J, Communi D, Kranz A, Moons L, Lambrechts D, Kroll J, Plaisance S, De Mol M, Bono F, Kliche S, Fellbrich G, Ballmer-Hofer K, Maglione D, Mayr-Beyrle U, Dewerchin M, Dombrowski S, Stanimirovic D, Van Hummelen P, Dehio C, Hicklin DJ, Persico G, Herbert JM, Shibuya M, Collen D, Conway EM, Carmeliet P. Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med. 2003;9:936-943. (Pubitemid 36889938)
82. Cao Y, Chen H, Zhou L, Chiang MK, Anand-Apte B, Weatherbee JA, Wang Y, Fang F, Flanagan JG, Tsang ML. Heterodimers of placenta growth factor/vascular endothelial growth factor: endothelial activity, tumor cell expression, and high affinity binding to Flk-1/KDR. J Biol Chem. 1996;271:3154-3162. (Pubitemid 26060529)
83. Oshima M, Oshima H, Taketo MM. TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol. 1996;179:297-302. (Pubitemid 26363265)
84. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J. 2002;21:1743-1753. (Pubitemid 34614630)
85. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, Li E. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci U S A. 2000;97:2626-2631. (Pubitemid 30159221)
86. Lebrin F, Goumans MJ, Jonker L, Carvalho RL, Valdimarsdottir G, Thorikay M, Mummery C, Arthur HM, ten Dijke P. Endoglin promotes endothelial cell proliferation and TGF-beta/alk1 signal transduction. EMBO J. 2004;23:4018-4028. (Pubitemid 39472423)
87. Shao ES, Lin L, Yao Y, Bostrom KI. Expression of vascular endothelial growth factor is coordinately regulated by the activin-like kinase receptors 1 and 5 in endothelial cells. Blood. 2009;114:2197-2206.
88. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Baldwin MA, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet. 1994;8: 345-351.
89. Bourdeau A, Dumont DJ, Letarte M. A murine model of hereditary hemorrhagic telangiectasia. J Clin Invest. 1999;104:1343-1351.
90. Walshe TE, Saint-Geniez M, Maharaj AS, Sekiyama E, Maldonado AE, D'Amore PA. TGF-beta is required for vascular barrier function, endo-thelial survival and homeostasis of the adult microvasculature. PLoS One. 2009;4:e5149.
91. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol. 1989;161:1200-1204. (Pubitemid 20007682)
92. Rodgers GM, Taylor RN, Roberts JM. Preeclampsia is associated with a serum factor cytotoxic to human endothelial cells. Am J Obstet Gynecol. 1988;159:908-914. (Pubitemid 18266621)
93. McCarthy AL, Woolfson RG, Raju SK, Poston L. Abnormal endothelial cell function of resistance arteries from women with preeclampsia. Am J Obstet Gynecol. 1993;168:1323-1330. (Pubitemid 23122189)
94. Ashworth JR, Warren AY, Baker PN, Johnson IR. Loss of endotheli-um-dependent relaxation in myometrial resistance arteries in pre-eclampsia. Br J Obstet Gynaecol. 1997;104:1152-1158. (Pubitemid 27406486)
95. Nova A, Sibai BM, Barton JR, Mercer BM, Mitchell MD. Maternal plasma level of endothelin is increased in preeclampsia. Am J Obstet Gynecol. 1991;165:724-727.
96. Deng L, Bremme K, Hansson LO, Blomback M. Plasma levels of von Willebrand factor and fibronectin as markers of persisting endothelial damage in preeclampsia. Obstet Gynecol. 1994;84:941-945. (Pubitemid 24360252)
97. Taylor RN, Crombleholme WR, Friedman SA, Jones LA, Casal DC, Roberts JM. 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;165:895-901.
98. Stubbs TM, Lazarchick J, Horger EO III. Plasma fibronectin levels in preeclampsia: a possible biochemical marker for vascular endothelial damage. Am J Obstet Gynecol. 1984;150:885-887. (Pubitemid 15237772)
99. Thorp JM Jr, White GC II, Moake JL, Bowes WA Jr. Von Willebrand factor multimeric levels and patterns in patients with severe pre-eclampsia. Obstet Gynecol. 1990;75:163-167. (Pubitemid 20062223)
100. Minakami H, Takahashi T, Izumi A, Tamada T. Increased levels of plasma thrombomodulin in preeclampsia. Gynecol Obstet Invest. 1993; 36:208-210. (Pubitemid 23343698)
101. Hsu CD, Iriye B, Johnson TR, Witter FR, Hong SF, Chan DW. Elevated circulating thrombomodulin in severe preeclampsia. Am J Obstet Gynecol. 1993;169:148-149. (Pubitemid 23223948)
102. Musci TJ, Roberts JM, Rodgers GM, Taylor RN. Mitogenic activity is increased in the sera of preeclamptic women before delivery. Am J Obstet Gynecol. 1988;159:1446-1451. (Pubitemid 19021593)
103. Cackovic M, Buhimschi CS, Zhao G, Funai EF, Norwitz ER, Kuczynski E, Lockwood CJ, Buhimschi IA. Fractional excretion of tumor necrosis factor-alpha in women with severe preeclampsia. Obstet Gynecol. 2008; 112:93-100.
104. Mills JL, DerSimonian R, Raymond E, Morrow JD, Roberts LJ II, Clemens JD, Hauth JC, Catalano P, Sibai B, Curet LB, Levine RJ. Prostacyclin and thromboxane changes predating clinical onset of pre-eclampsia: a multicenter prospective study. JAMA. 1999;282:356-362. (Pubitemid 29350490)
105. Fitzgerald DJ, Entman SS, Mulloy K, FitzGerald GA. Decreased pros-tacyclin biosynthesis preceding the clinical manifestation of pregnancy-induced hypertension. Circulation. 1987;75:956-963. (Pubitemid 17068524)
106. Sandrim VC, Palei AC, Metzger IF, Gomes VA, Cavalli RC, Tanus-Santos JE. Nitric oxide formation is inversely related to serum levels of antiangiogenic factors soluble fms-like tyrosine kinase-1 and soluble endogline in preeclampsia. Hypertension. 2008;52:402-407.
107. Myers J, Mires G, Macleod M, Baker P. In preeclampsia, the circulating factors capable of altering in vitro endothelial function precede clinical disease. Hypertension. 2005;45:258-263. (Pubitemid 40179969)
108. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A. 1993;90:10705-10709. (Pubitemid 23347111)
109. Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor, Flt-1, and its heterodimerization with KDR. Biochem Biophys Res Commun. 1996; 226:324-328. (Pubitemid 26331903)
110. Clark DE, Smith SK, He Y, Day KA, Licence DR, Corps AN, Lammoglia R, Charnock-Jones DS. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod. 1998;59:1540-1548. (Pubitemid 28549874)
111. Thomas CP, Andrews JI, Raikwar NS, Kelley EA, Herse F, Dechend R, Golos TG, Liu KZ. A recently evolved novel trophoblast-enriched secreted form of fms-like tyrosine kinase-1 variant is up-regulated in hypoxia and preeclampsia. J Clin Endocrinol Metab. 2009;94: 2524-2530.
112. Sela S, Itin A, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Yagel S, Keshet E. 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;102:1566-1574.
113. Heydarian M, McCaffrey T, Florea L, Yang Z, Ross MM, Zhou W, Maynard SE. Novel splice variants of sflt1 are upregulated in pre-eclampsia. Placenta. 2009;30:250-255.
114. Gilbert JS, Babcock SA, Granger JP. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension. 2007;50: 1142-1147. (Pubitemid 350172938)
115. Lu F, Longo M, Tamayo E, Maner W, Al-Hendy A, Anderson GD, Hankins GD, Saade GR. The effect of over-expression of sFlt-1 on blood pressure and the occurrence of other manifestations of pre-eclampsia in unrestrained conscious pregnant mice. Am J Obstet Gynecol. 2007;196:396.e391-396.e397; discussion 396.e397.
116. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab. 2003;88:2348-2351. (Pubitemid 36549917)
117. Hertig A, Berkane N, Lefevre G, Toumi K, Marti HP, Capeau J, Uzan S, Rondeau E. Maternal serum sFlt1 concentration is an early and reliable predictive marker of preeclampsia. Clin Chem. 2004;50: 1702-1703. (Pubitemid 39121252)
118. Tsatsaris V, Goffin F, Munaut C, Brichant JF, Pignon MR, Noel A, Schaaps JP, Cabrol D, Frankenne F, Foidart JM. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab. 2003;88:5555-5563. (Pubitemid 37452769)
119. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, Ecker J, Karumanchi SA. First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab. 2004;89:770-775. (Pubitemid 38269892)
120. Levine RJ, Thadhani R, Qian C, Lam C, Lim KH, Yu KF, Blink AL, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Urinary placental growth factor and risk of preeclampsia. JAMA. 2005; 293:77-85. (Pubitemid 40066702)
121. Verlohren S, Galindo A, Schlembach D, Zeisler H, Herraiz I, Moertl MG, Pape J, Dudenhausen JW, Denk B, Stepan H. An automated method for the determination of the sFlt-1/PlGF ratio in the assessment of preeclampsia. Am J Obstet Gynecol. 2010;202:161.e1-161.e11.
122. Buhimschi CS, Norwitz ER, Funai E, Richman S, Guller S, Lockwood CJ, Buhimschi IA. Urinary angiogenic factors cluster hypertensive disorders and identify women with severe preeclampsia. Am J Obstet Gynecol. 2005;192:734-741. (Pubitemid 40311263)
123. Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, Mazaki-Tovi S, Gotsch F, Edwin SS, Gomez R, Yeo L, Conde-Agudelo A, Hassan SS. 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;22:1021-1038.
124. Signore C, Mills JL, Qian C, Yu K, Lam C, Epstein FH, Karumanchi SA, Levine RJ. Circulating angiogenic factors and placental abruption. Obstet Gynecol. 2006;108:338-344. (Pubitemid 44305675)
125. Signore C, Mills JL, Qian C, Yu KF, Rana S, Karumanchi SA, Levine RJ. Circulating soluble endoglin and placental abruption. Prenat Diagn. 2008;28:852-858.
126. Vaisbuch E, Whitty J, Hassan S, Romero R, Kusanovic J, Cotton D, Sorokin Y, Karumanchi SA. Circulating angiogenic and anti-angiogenic factors in women with eclampsia. Am J Obstet Gynecol. 2011:204: 152.e1-152.e9.
127. Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, Kozuma S, Taketani Y. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophys-iology of preeclampsia. Endocrinology. 2004;145:4838-4845. (Pubitemid 39551100)
128. Gerber HP, Condorelli F, Park J, Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes: Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem. 1997;272:23659- 23667. (Pubitemid 27410939)
129. Tal R, Shaish A, Barshack I, Polak-Charcon S, Afek A, Volkov A, Feldman B, Avivi C, Harats D. Effects of hypoxia-inducible factor-1alpha overexpression in pregnant mice: possible implications for pre-eclampsia and intrauterine growth restriction. Am J Pathol. 2010;177: 2950-2962.
130. Rosario GX, Konno T, Soares MJ. Maternal hypoxia activates endo-vascular trophoblast cell invasion. Dev Biol. 2008;314:362-375.
131. Wimalasundera RC, Larbalestier N, Smith JH, de Ruiter A, McG Thom SA, Hughes AD, Poulter N, Regan L, Taylor GP. Pre-eclampsia, anti-retroviral therapy, and immune reconstitution. Lancet. 2002;360: 1152-1154. (Pubitemid 35246493)
132. Huang SJ, Chen CP, Schatz F, Rahman M, Abrahams VM, Lockwood CJ. Pre-eclampsia is associated with dendritic cell recruitment into the uterine decidua. J Pathol. 2008;214:328-336. (Pubitemid 351212388)
133. Lockwood CJ, Matta P, Krikun G, Koopman LA, Masch R, Toti P, Arcuri F, Huang ST, Funai EF, Schatz F. Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-alpha and interleukin-1beta in first trimester human decidual cells: implications for preeclampsia. Am J Pathol. 2006;168:445-452. (Pubitemid 43271143)
134. Hiby SE, Walker JJ, O'Shaughnessy KM, Redman CW, Carrington M, Trowsdale J, Moffett A. Combinations of maternal kir and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med. 2004;200:957-965. (Pubitemid 39431121)
135. Girardi G, Yarilin D, Thurman JM, Holers VM, Salmon JE. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med. 2006;203: 2165-2175. (Pubitemid 44352237)
136. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C,
137. Rinsler MG, Rigby B. Function of aldosterone in the metabolism of sodium and water in pregnancy. BMJ. 1957;2:966-969.
138. Weir RJ, Paintin DB, Robertson JI, Tree M, Fraser R, Young J. Renin, angiotensin and aldosterone relationships in normal pregnancy. Proc R Soc Med. 1970;63:1101-1102.
139. Weir RJ, Brown JJ, Fraser R, Kraszewski A, Lever AF, McIlwaine GM, Morton JJ, Robertson JI, Tree M. Plasma renin, renin substrate, angio-tensin II, and aldosterone in hypertensive disease of pregnancy. Lancet. 1973;1:291-294.
140. Wallukat G, Homuth V, Fischer T, Lindschau C, Horstkamp B, Jupner A, Baur E, Nissen E, Vetter K, Neichel D, Dudenhausen JW, Haller H, Luft FC. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest. 1999;103:945-952. (Pubitemid 29169601)
141. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, Hicks MJ, Ramin SM, Kellems RE, Xia Y. Angiotensin receptor agonistic autoan-tibodies induce pre-eclampsia in pregnant mice. Nat Med. 2008;14: 855-862.
142. Hubel CA, Wallukat G, Wolf M, Herse F, Rajakumar A, Roberts JM, Markovic N, Thadhani R, Luft FC, Dechend R. Agonistic angiotensin II type 1 receptor autoantibodies in postpartum women with a history of preeclampsia. Hypertension. 2007;49:612-617.
143. Zhou A, Carrell RW, Murphy MP, Wei Z, Yan Y, Stanley PL, Stein PE, Broughton Pipkin F, Read RJ. A redox switch in angiotensinogen modulates angiotensin release. Nature. 2010;468:108-111.
144. Kanasaki K, Palmsten K, Sugimoto H, Ahmad S, Hamano Y, Xie L, Parry S, Augustin HG, Gattone VH, Folkman J, Strauss JF, Kalluri R. Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia. Nature. 2008;453:1117-1121. (Pubitemid 351871733)
145. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW, Ahmed A. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxy-genase-1. Circulation. 2007;115:1789-1797. (Pubitemid 46648616)
146. Baum M, Schiff E, Kreiser D, Dennery PA, Stevenson DK, Rosenthal T, Seidman DS. End-tidal carbon monoxide measurements in women with pregnancy-induced hypertension and preeclampsia. Am J Obstet Gynecol. 2000;183:900-903.
147. Karumanchi SA, Levine RJ. How does smoking reduce the risk of preeclampsia? Hypertension. 2010;55:1100-1101.
148. Raijmakers MT, Dechend R, Poston L. Oxidative stress and pre-eclampsia: rationale for antioxidant clinical trials. Hypertension. 2004; 44:374-380. (Pubitemid 39281478)
149. Hubel CA. Oxidative stress in the pathogenesis of preeclampsia. Proc Soc Exp Biol Med. 1999;222:222-235.
150. Roberts JM, Myatt L, Spong CY, Thom EA, Hauth JC, Leveno KJ, Pearson GD, Wapner RJ, Varner MW, Thorp JM Jr, Mercer BM, Peaceman AM, Ramin SM, Carpenter MW, Samuels P, Sciscione A, Harper M, Smith WJ, Saade G, Sorokin Y, Anderson GB. Vitamins C and E to prevent complications of pregnancy-associated hypertension. N Engl J Med. 2010;362:1282-1291.
151. Rumbold AR, Crowther CA, Haslam RR, Dekker GA, Robinson JS. Vitamins C and E and the risks of preeclampsia and perinatal complications. N Engl J Med. 2006;354:1796-1806.
152. Spinnato JA II, Freire S, Pinto ESJL, Cunha Rudge MV, Martins-Costa S, Koch MA, Goco N, Santos Cde B, Cecatti JG, Costa R, Ramos JG, Moss N, Sibai BM. Antioxidant therapy to prevent preeclampsia: a randomized controlled trial. Obstet Gynecol. 2007;110:1311-1318. (Pubitemid 351326075)
153. Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH. Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial. Lancet. 2006;367:1145-1154.
154. Villar J, Purwar M, Merialdi M, Zavaleta N, Thi Nhu Ngoc N, Anthony J, De Greeff A, Poston L, Shennan A. World Health Organisation multicentre randomised trial of supplementation with vitamins C and E among pregnant women at high risk for pre-eclampsia in populations of low nutritional status from developing countries. BJOG. 2009;116: 780-788.
155. Redman CW, Sargent IL. Latest advances in understanding pre-eclampsia. Science. 2005;308:1592-1594.
156. Knight M, Redman CW, Linton EA, Sargent IL. Shedding of syncy-tiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol. 1998;105:632-640. (Pubitemid 28293481)
157. Chua S, Wilkins T, Sargent I, Redman C. Trophoblast deportation in pre-eclamptic pregnancy. Br J Obstet Gynaecol. 1991;98:973-979.
158. Lok CA, Boing AN, Sargent IL, Sooranna SR, van der Post JA, Nieuwland R, Sturk A. Circulating platelet-derived and placenta-derived microparticles expose Flt-1 in preeclampsia. Reprod Sci. 2008;15: 1002-1010.
159. Khankin EV, Royle C, Karumanchi SA. Placental vasculature in health and disease. Semin Thromb Hemost. 2010;36:309-320.
160. Sunderji S, Gaziano E, Wothe D, Rogers LC, Sibai B, Karumanchi SA, Hodges-Savola C. Automated assays for sVEGFR1 and PlGF as an aid in the diagnosis of preterm preeclampsia: a prospective clinical study. Am J Obstet Gynecol. 2010;202:40 e41-e47.
161. Ohkuchi A, Hirashima C, Suzuki H, Takahashi K, Yoshida M, Matsubara S, Suzuki M. Evaluation of a new and automated electrochemi-luminescence immunoassay for plasma sFlt-1 and PlGF levels in women with preeclampsia. Hypertens Res. 2010;33:422-427.
162. Qazi U, Lam C, Karumanchi SA, Petri M. Soluble fms-like tyrosine kinase associated with preeclampsia in pregnancy in systemic lupus erythematosus. J Rheumatol. 2008;35:631-634. (Pubitemid 351500058)
163. Cohen A, Lim KH, Lee Y, Rana S, Karumanchi SA, Brown F. Circulating levels of the antiangiogenic marker soluble fms-like tyrosine kinase 1 are elevated in women with pregestational diabetes and pre-eclampsia: angiogenic markers in preeclampsia and preexisting diabetes. Diabetes Care. 2007;30:375-377. (Pubitemid 46198350)
164. Young B, Levine RJ, Salahuddin S, Qian C, Lim KH, Karumanchi SA, Rana S. The use of angiogenic biomarkers to differentiate non-HELLP related thrombocytopenia from HELLP syndrome. J Matern Fetal Neonatal Med. 2010;23:366-370.
165. Powers RW, Roberts JM, Cooper KM, Gallaher MJ, Frank MP, Harger GF, Ness RB. 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;193:185-191. (Pubitemid 40991843)
166. Levine RJ, Qian C, Maynard SE, Yu KF, Epstein FH, Karumanchi SA. Serum sFlt1 concentration during preeclampsia and mid trimester blood pressure in healthy nulliparous women. Am J Obstet Gynecol. 2006;194: 1034-1041.
167. Li Z, Zhang Y, Ying Ma J, Kapoun AM, Shao Q, Kerr I, Lam A, O'Young G, Sannajust F, Stathis P, Schreiner G, Karumanchi SA, Protter AA, Pollitt NS. Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension. 2007;50:686-692. (Pubitemid 47442732)
168. Bergmann A, Ahmad S, Cudmore M, Gruber AD, Wittschen P, Lindenmaier W, Christofori G, Gross V, Gonzalves A, Grone HJ, Ahmed A, Weich HA. Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a mouse model. J Cell Mol Med. 2010; 14:1857-1867.
169. Gilbert JS, Verzwyvelt J, Colson D, Arany M, Karumanchi SA, Granger JP. Recombinant vascular endothelial growth factor 121 infusion lowers blood pressure and improves renal function in rats with placental ischemia-induced hypertension. Hypertension. 2010;55:380-385.
170. Smith GC, Pell JP, Walsh D. Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet. 2001;357:2002-2006. (Pubitemid 32592386)
171. Wilson BJ, Watson MS, Prescott GJ, Sunderland S, Campbell DM, Hannaford P, Smith WC. Hypertensive diseases of pregnancy and risk of hypertension and stroke in later life: results from cohort study. BMJ. 2003;326:845.
172. Ray JG, Vermeulen MJ, Schull MJ, Redelmeier DA. Cardiovascular Health After Maternal Placental Syndromes (CHAMPS): population-based retrospective cohort study. Lancet. 2005;366:1797-1803. (Pubitemid 41642644)
173. Lykke JA, Langhoff-Roos J, Sibai BM, Funai EF, Triche EW, Paidas MJ. Hypertensive pregnancy disorders and subsequent cardiovascular morbidity and type 2 diabetes mellitus in the mother. Hypertension. 2009;53:944-951.
174. Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ. 2007;335:974.
175. Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS. Association of maternal endothelial dysfunction with preeclampsia. JAMA. 2001;285:1607-1612. (Pubitemid 32240253)
176. Saxena AR, Karumanchi SA, Brown NJ, Royle CM, McElrath TF, Seely EW. Increased sensitivity to angiotensin II is present postpartum in women with a history of hypertensive pregnancy. Hypertension. 2010; 55:1239-1245.
177. Sattar N, Ramsay J, Crawford L, Cheyne H, Greer IA. Classic and novel risk factor parameters in women with a history of pre-eclampsia. Hypertension. 2003;42:39 - 42. (Pubitemid 36842234)
178. Parretti E, Lapolla A, Dalfra M, Pacini G, Mari A, Cioni R, Marzari C, Scarselli G, Mello G. Preeclampsia in lean normotensive normotolerant pregnant women can be predicted by simple insulin sensitivity indexes. Hypertension. 2006;47:449-453. (Pubitemid 43740289)
179. Wolf M, Hubel CA, Lam C, Sampson M, Ecker JL, Ness RB, Rajakumar A, Daftary A, Shakir AS, Seely EW, Roberts JM, Sukhatme VP, Karumanchi SA, Thadhani R. Preeclampsia and future cardiovascular disease: potential role of altered angiogenesis and insulin resistance. J Clin Endocrinol Metab. 2004;89:6239-6243. (Pubitemid 39628439)
180. Laivuori H, Tikkanen MJ, Ylikorkala O. Hyperinsulinemia 17 years after preeclamptic first pregnancy. J Clin Endocrinol Metab. 1996;81: 2908-2911. (Pubitemid 26323884)
181. Hubel CA, Powers RW, Snaedal S, Gammill HS, Ness RB, Roberts JM, Arngrimsson R. C-reactive protein is elevated 30 years after eclamptic pregnancy. Hypertension. 2008;51:1499-1505.
182. Romundstad PR, Magnussen EB, Smith GD, Vatten LJ. Hypertension in pregnancy and later cardiovascular risk: common antecedents? Circulation. 2010;122:579-584.
183. Sattar N, Greer IA. Pregnancy complications and maternal cardiovascular risk: opportunities for intervention and screening? BMJ. 2002;325: 157-160. (Pubitemid 34800133)
184. Germain AM, Romanik MC, Guerra I, Solari S, Reyes MS, Johnson RJ, Price K, Karumanchi SA, Valdes G. Endothelial dysfunction: a link among preeclampsia, recurrent pregnancy loss, and future cardiovascular events? Hypertension. 2007;49:90-95. (Pubitemid 46360346)
185. Yinon Y, Kingdom JC, Odutayo A, Moineddin R, Drewlo S, Lai V, Cherney DZ, Hladunewich MA. Vascular dysfunction in women with a history of preeclampsia and intrauterine growth restriction: insights into future vascular risk. Circulation. 2010;122:1846-1853.
186. Rajakumar A, Michael HM, Rajakumar PA, Shibata E, Hubel CA, Karumanchi SA, Thadhani R, Wolf M, Harger G, Markovic N. Extra-placental expression of vascular endothelial growth factor receptor-1, (Flt-1) and soluble Flt-1 (sFlt-1), by peripheral blood mononuclear cells (PBMCs) in normotensive and preeclamptic pregnant women. Placenta. 2005;26:563-573. (Pubitemid 40916309)
187. Di Marco GS, Reuter S, Hillebrand U, Amler S, Konig M, Larger E, Oberleithner H, Brand E, Pavenstadt H, Brand M. The soluble VEGF receptor sFlt1 contributes to endothelial dysfunction in CKD. J Am Soc Nephrol. 2009;20:2235-2245.
188. Levine RJ, Vatten LJ, Horowitz GL, Qian C, Romundstad PR, Yu KF, Hollenberg AN, Hellevik AI, Asvold BO, Karumanchi SA. Pre-eclampsia, soluble fms-like tyrosine kinase 1, and the risk of reduced thyroid function: nested case-control and population based study. BMJ. 2009;339:b4336.
189. Khurana R, Simons M, Martin JF, Zachary IC. Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation. 2005;112: 1813-1824. (Pubitemid 41368158)
190. Shin S, Lee SH, Park S, Kang SM, Chung N, Shim WH, Cho SY, Manabe I, Jang Y. Soluble fms-like tyrosine kinase-1 and the progression of carotid intima-media thickness: 24-month follow-up study. Circ J. 2010;74:2211-2215.
191. Jayet PY, Rimoldi SF, Stuber T, Salmon CS, Hutter D, Rexhaj E, Thalmann S, Schwab M, Turini P, Sartori-Cucchia C, Nicod P, Villena M, Allemann Y, Scherrer U, Sartori C. Pulmonary and systemic vascular dysfunction in young offspring of mothers with preeclampsia. Circulation. 2010;122:488-494.