In vivo experiments reveal the good, the bad and the ugly faces of sFlt-1 in Pregnancy

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Szalai, Gabor ^a   Xu, Yi ^a   Romero, Roberto ^a   Chaiworapongsa, Tinnakorn ^a,b   Xu, Zhonghui ^a   Jen Chiang, Po ^a   Ahn, Hyunyoung ^a   Sundell, Birgitta ^a   Plazyo, Olesya ^a   Jiang, Yang ^a   Olive, Mary ^a,b   Wang, Bing ^a   Jacques, Suzanne M ^b   Qureshi, Faisal ^b   Tarca, Adi L ^a,b,c   Erez, Offer ^d   Dong, Zhong ^a   Papp, Zoltan ^e   Hassan, Sonia S ^a,b   Hernandez Andrade, Edgar ^a,b   Than, Nandor Gabor ^a,b,e,f   more..

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

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Wayne State University   (United States)

^d BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^e SEMMELWEIS UNIVERSITY   (Hungary)

^f INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; COMPLEMENTARY DNA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; CREATININE; FLT1 PROTEIN, HUMAN; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; PEPTIDE; PLACENTA PROTEIN;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; CESAREAN SECTION; CHRONIC DISEASE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CREATININE URINE LEVEL; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIAL DYSFUNCTION; FEMALE; FETUS WEIGHT; GENE EXPRESSION PROFILING; GENE TARGETING; GESTATION PERIOD; HISTOPATHOLOGY; IN VIVO STUDY; LITTER SIZE; MALE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; PLACENTA WEIGHT; PREECLAMPSIA; PREGNANCY; PREGNANCY OUTCOME; PROMOTER REGION; PROTEIN EXPRESSION; PUERPERIUM; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; RNA ISOLATION; SURVIVAL RATE; SYMPTOMATOLOGY; TELEMETRY; TISSUE DISTRIBUTION; TRANSGENE; TROPHOBLAST; URINALYSIS; VASCULAR RING; VIRAL GENE DELIVERY SYSTEM; ADENOVIRIDAE; ADMINISTRATION AND DOSAGE; ALBUMINURIA; ANIMAL; ARTERIAL PRESSURE; GENE EXPRESSION; GENE VECTOR; GENETICS; HUMAN; KIDNEY; METABOLISM; MICROVASCULATURE; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA; PROTEINURIA; URINE;

MUS; PRIMATES;

ADENOVIRIDAE; ALBUMINURIA; ANIMALS; ARTERIAL PRESSURE; CREATININE; FEMALE; GENE EXPRESSION; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; KIDNEY; LITTER SIZE; MICE; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDES; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY OUTCOME; PREGNANCY PROTEINS; PROTEIN ISOFORMS; PROTEINURIA; TRANSGENES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84907966941     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110867     Document Type: Article

References (226)

1. Medawar PB (1953) Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp Soc Exp Biol 44: 320-338.
2. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B (1995) T cell awareness of paternal alloantigens during pregnancy. Science 270: 630-633.
3. Moffett A, Loke YW (2004) The immunological paradox of pregnancy: a reappraisal. Placenta 25: 1-8.
4. Aluvihare VR, Kallikourdis M, Betz AG (2004) Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5: 266-271.
5. Trowsdale J, Betz AG (2006) Mother's little helpers: mechanisms of maternalfetal tolerance. Nat Immunol 7: 241-246.
6. Hunt JS (2006) Stranger in a strange land. Immunol Rev 213: 36-47.
7. Zenclussen AC, Gerlof K, Zenclussen ML, Ritschel S, Zambon BA, et al. (2006) Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur J Immunol 36: 82-94.
8. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, et al. (2007) A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 13: 1450-1457.
9. Terness P, Kallikourdis M, Betz AG, Rabinovich GA, Saito S, et al. (2007) Tolerance signaling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells. Am J Reprod Immunol 58: 238-254.
10. Than NG, Romero R, Erez O, Weckle A, Tarca AL, et al. (2008) Emergence of hormonal and redox regulation of galectin-1 in placental mammals: implication in maternal-fetal immune tolerance. Proc Natl Acad Sci USA 105: 15819-15824.
11. Erlebacher A (2010) Immune surveillance of the maternal/fetal interface: controversies and implications. Trends Endocrinol Metab 21: 428-434.
12. Mor G, Cardenas I (2010) The immune system in pregnancy: a unique complexity. Am J Reprod Immunol 63: 425-433.
13. Mor G, Cardenas I, Abrahams V, Guller S (2011) Inflammation and pregnancy: the role of the immune system at the implantation site. Ann N Y Acad Sci 1221: 80-87.
14. Wegmann TG, Lin H, Guilbert L, Mosmann TR (1993) Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today 14: 353-356.
15. Pijnenborg R (2002) Implantation and immunology: maternal inflammatory and immune cellular responses to implantation and trophoblast invasion. Reprod Biomed Online 4 Suppl 3: 14-17.
16. Paulesu L, Bhattacharjee J, Bechi N, Romagnoli R, Jantra S, et al. (2010) Proinflammatory cytokines in animal and human gestation. Curr Pharm Des 16: 3601-3615.
17. Romero R, Parvizi ST, Oyarzun E, Mazor M, Wu YK, et al. (1990) Amniotic fluid interleukin-1 in spontaneous labor at term. J Reprod Med 35: 235-238.
18. Mitchell MD, Chang MC, Chaiworapongsa T, Lan HY, Helliwell RJ, et al. (2005) Identification of 9alpha, 11beta-prostaglandin F2 in human amniotic fluid and characterization of its production by human gestational tissues. J Clin Endocrinol Metab 90: 4244-4248.
19. Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, et al. (2006) Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am J Obstet Gynecol 195: 394e1-24.
20. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, et al. (2006) Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med 11: 317-326.
21. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, et al. (2008) Inflammatory processes in preterm and term parturition. J Reprod Immunol 79: 50-57.
22. Han YM, Romero R, Kim JS, Tarca AL, Kim SK, et al. (2008) Region-specific gene expression profiling: novel evidence for biological heterogeneity of the human amnion. Biol Reprod 79: 954-961.
23. Hassan SS, Romero R, Tarca AL, Nhan-Chang CL, Vaisbuch E, et al. (2009) The transcriptome of cervical ripening in human pregnancy before the onset of labor at term: identification of novel molecular functions involved in this process. J Matern Fetal Neonatal Med 22: 1183-1193.
24. Gomez-Lopez N, Vega-Sanchez R, Castillo-Castrejon M, Romero R, Cubeiro-Arreola K, et al. (2013) Evidence for a role for the adaptive immune response in human term parturition. Am J Reprod Immunol 69: 212-230.
25. Romero R, Wu YK, Brody DT, Oyarzun E, Duff GW, et al. (1989) Human decidua: a source of interleukin-1. Obstet Gynecol 73: 31-34.
26. Sacks GP, Studena K, Sargent K, Redman CW (1998) Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 179: 80-86.
27. Gervasi MT, Chaiworapongsa T, Naccasha N, Blackwell S, Yoon BH, et al. (2001) Phenotypic and metabolic characteristics of maternal monocytes and granulocytes in preterm labor with intact membranes. Am J Obstet Gynecol 185: 1124-1129.
28. Gervasi MT, Chaiworapongsa T, Pacora P, Naccasha N, Yoon BH, et al. (2001) Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 185: 792-797.
29. Naccasha N, Gervasi MT, Chaiworapongsa T, Berman S, Yoon BH, et al. (2001) Phenotypic and metabolic characteristics of monocytes and granulocytes in normal pregnancy and maternal infection. Am J Obstet Gynecol 185: 1118-1123.
30. Gervasi MT, Chaiworapongsa T, Naccasha N, Pacora P, Berman S, et al. (2002) Maternal intravascular inflammation in preterm premature rupture of membranes. J Matern Fetal Neonatal Med 11: 171-175.
31. Blackwell S, Romero R, Chaiworapongsa T, Refuerzo J, Gervasi MT, et al. (2003) Unexplained fetal death is associated with changes in the adaptive limb of the maternal immune response consistent with prior antigenic exposure. J Matern Fetal Neonatal Med 14: 241-246.
32. Richani K, Romero R, Soto E, Espinoza J, Nien JK, et al. (2005) Unexplained intrauterine fetal death is accompanied by activation of complement. J Perinat Med 33: 296-305.
33. Kim YM, Romero R, Chaiworapongsa T, Espinoza J, Mor G, et al. (2006) Dermatitis as a component of the fetal inflammatory response syndrome is associated with activation of Toll-like receptors in epidermal keratinocytes. Histopathology 49: 506-514.
34. Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, et al. (2006) The preterm parturition syndrome. BJOG 113 Suppl 3: 17-42.
35. Gotsch F, Romero R, Kusanovic JP, Mazaki-Tovi S, Pineles BL, et al. (2007) The fetal inflammatory response syndrome. Clin Obstet Gynecol 50: 652-683.
36. Romero R, Gotsch F, Pineles B, Kusanovic JP (2007) Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr Rev 65: S194-202.
37. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel L, et al. (2007) The role of inflammation and infection in preterm birth. Semin Reprod Med 25: 21-39.
38. Erez O, Gotsch F, Mazaki-Tovi S, Vaisbuch E, Kusanovic JP, et al. (2009) Evidence of maternal platelet activation, excessive thrombin generation, and high amniotic fluid tissue factor immunoreactivity and functional activity in patients with fetal death. J Matern Fetal Neonatal Med 22: 672-687.
39. Kim SK, Romero R, Chaiworapongsa T, Kusanovic JP, Mazaki-Tovi S, et al. (2009) Evidence of changes in the immunophenotype and metabolic characteristics (intracellular reactive oxygen radicals) of fetal, but not maternal, monocytes and granulocytes in the fetal inflammatory response syndrome. J Perinat Med 37: 543-552.
40. Kim CJ, Romero R, Kusanovic JP, Yoo W, Dong Z, et al. (2010) The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth. Mod Pathol 23: 1000-1011.
41. Madsen-Bouterse SA, Romero R, Tarca AL, Kusanovic JP, Espinoza J, et al. (2010) The transcriptome of the fetal inflammatory response syndrome. Am J Reprod Immunol 63: 73-92.
42. Ogge G, Romero R, Chaiworapongsa T, Gervasi MT, Pacora P, et al. (2010) Leukocytes of pregnant women with small-for-gestational age neonates have a different phenotypic and metabolic activity from those of women with preeclampsia. J Matern Fetal Neonatal Med 23: 476-487.
43. Lee J, Romero R, Dong Z, Xu Y, Qureshi F, et al. (2011) Unexplained fetal death has a biological signature of maternal anti-fetal rejection: chronic chorioamnionitis and alloimmune anti-human leucocyte antigen antibodies. Histopathology 59: 928-938.
44. Lee J, Romero R, Xu Y, Kim JS, Topping V, et al. (2011) A signature of maternal anti-fetal rejection in spontaneous preterm birth: chronic chorioamnionitis, anti-human leukocyte antigen antibodies, and C4d. PLoS ONE 6: e16806.
45. Lee J, Romero R, Xu Y, Kim JS, Park JY, et al. (2011) Maternal HLA panelreactive antibodies in early gestation positively correlate with chronic chorioamnionitis: evidence in support of the chronic nature of maternal antifetal rejection. Am J Reprod Immunol 66: 510-526.
46. Girardi G, Prohaszka Z, Bulla R, Tedesco F, Scherjon S (2011) Complement activation in animal and human pregnancies as a model for immunological recognition. Mol Immunol 48: 1621-1630.
47. Romero R, Chaiworapongsa T, Savasan ZA, Hussein Y, Dong Z, et al. (2012) Clinical chorioamnionitis is characterized by changes in the expression of the alarmin HMGB1 and one of its receptors, sRAGE. J Matern Fetal Neonatal Med 25: 558-567.
48. Burton GJ (2009) Oxygen, the Janus gas; its effects on human placental development and function. J Anat 215: 27-35.
49. Rodesch F, Simon P, Donner C, Jauniaux E (1992) Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 80: 283-285.
50. Jauniaux E, Watson A, Ozturk O, Quick D, Burton G (1999) In-vivo measurement of intrauterine gases and acid-base values early in human pregnancy. Hum Reprod 14: 2901-2904.
51. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, et al. (2000) Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 157: 2111-2122.
52. Jauniaux E, Gulbis B, Burton GJ (2003) The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus-A review. Placenta 24 Suppl A: S86-93.
53. Jauniaux E, Hempstock J, Greenwold N, Burton GJ (2003) Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 162: 115-125.
54. Burton GJ, Woods AW, Jauniaux E, Kingdom JC (2009) Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30: 473-482.
55. Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS (2009) Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 30 Suppl A: S43-48.
56. Mole DR, Ratcliffe PJ (2008) Cellular oxygen sensing in health and disease. Pediatr Nephrol 23: 681-694.
57. Kim YW, West XZ, Byzova TV (2013) Inflammation and oxidative stress in angiogenesis and vascular disease. J Mol Med (Berl) 91: 323-328.
58. Scholz CC, Taylor CT (2013) Targeting the HIF pathway in inflammation and immunity. Curr Opin Pharmacol 13: 646-653.
59. Clark DE, Smith SK, He Y, Day KA, Licence DR, et al. (1998) A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 59: 1540-1548.
60. Sherer DM, Abulafia O (2001) Angiogenesis during implantation, and placental and early embryonic development. Placenta 22: 1-13.
61. Wang H, Li Q, Lin H, Yu X, Qian D, et al. (2003) Expression of vascular endothelial growth factor and its receptors in the rhesus monkey (Macaca mulatta) endometrium and placenta during early pregnancy. Mol Reprod Dev 65: 123-131.
62. Charnock-Jones DS, Kaufmann P, Mayhew TM (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 25: 103-113.
63. Erez O, Romero R, Espinoza J, Fu W, Todem D, et al. (2008) The change in concentrations of angiogenic and anti-Angiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age. J Matern Fetal Neonatal Med 21: 279-287.
64. Romero R, Nien JK, Espinoza J, Todem D, Fu W, et al. (2008) 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 21: 9-23.
65. Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, et al. (2009) 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 22: 1021-1038.
66. Romero R, Chaiworapongsa T, Erez O, Tarca AL, Gervasi MT, et al. (2010) An imbalance between angiogenic and anti-Angiogenic factors precedes fetal death in a subset of patients: results of a longitudinal study. J Matern Fetal Neonatal Med 23: 1384-1399.
67. Muttukrishna S, Swer M, Suri S, Jamil A, Calleja-Agius J, et al. (2011) Soluble Flt-1 and PlGF: new markers of early pregnancy loss? PLoS ONE 6: e18041.
68. Kaitu'u-Lino TJ, Whitehead CL, Ngian GL, Permezel M, Tong S (2012) Serum concentrations of soluble Flt-1 are decreased among women with a viable fetus and no symptoms of miscarriage destined for pregnancy loss. PLoS ONE 7: e32509.
69. Fong GH, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66-70.
70. Shibuya M (2001) Structure and function of VEGF/VEGF-receptor system involved in angiogenesis. Cell Struct Funct 26: 25-35.
71. Shibuya M (2011) Involvement of Flt-1 (VEGF receptor-1) in cancer and preeclampsia. Proc Jpn Acad Ser B Phys Biol Sci 87: 167-178.
72. He Y, Smith SK, Day KA, Clark DE, Licence DR, et al. (1999) Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol Endocrinol 13: 537-545.
73. Kendall RL, Wang G, Thomas KA (1996) Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 226: 324-328.
74. Sela S, Itin A, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, et al. (2008) 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 102: 1566-1574.
75. Reuvekamp A, Velsing-Aarts FV, Poulina IE, Capello JJ, Duits AJ (1999) Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre-eclampsia. Br J Obstet Gynaecol 106: 1019-1022.
76. Vuorela P, Helske S, Hornig C, Alitalo K, Weich H, et al. (2000) Amniotic fluid-soluble vascular endothelial growth factor receptor-1 in preeclampsia. Obstet Gynecol 95: 353-357.
77. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, et al. (2003) Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 88: 2348-2351.
78. Maynard SE, Min JY, Merchan J, Lim KH, Li J, et al. (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649-658.
79. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Kim YM, et al. (2004) Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol 190: 1541-1547.
80. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, et al. (2004) Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683.
81. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, et al. (2004) First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 89: 770-775.
82. Hertig A, Berkane N, Lefevre G, Toumi K, Marti HP, et al. (2004) Maternal serum sFlt1 concentration is an early and reliable predictive marker of preeclampsia. Clin Chem 50: 1702-1703.
83. Bdolah Y, Karumanchi SA, Sachs BP (2005) Recent advances in understanding of preeclampsia. Croat Med J 46: 728-736.
84. Bujold E, Romero R, Chaiworapongsa T, Kim YM, Kim GJ, et al. (2005) Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin. J Matern Fetal Neonatal Med 18: 9-16.
85. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, et al. (2005) Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 17: 3-18.
86. Karumanchi SA, Maynard SE, Stillman IE, Epstein FH, Sukhatme VP (2005) Preeclampsia: a renal perspective. Kidney Int 67: 2101-2113.
87. Lam C, Lim KH, Karumanchi SA (2005) Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension 46: 1077-1085.
88. Levine RJ, Karumanchi SA (2005) Circulating angiogenic factors in preeclampsia. Clin Obstet Gynecol 48: 372-386.
89. Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA (2005) Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res 57: 1R-7R.
90. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, et al. (2006) Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 12: 642-649.
91. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, et al. (2006) Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 355: 992-1005.
92. Karumanchi SA, Lindheimer MD (2007) Preeclampsia and the kidney: footprints in the urine. Am J Obstet Gynecol 196: 287-288.
93. Staff AC, Braekke K, Johnsen GM, Karumanchi SA, Harsem NK (2007) Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 197: 176e1-6.
94. Berkane N, Lefevre G, Hertig A (2007) Angiogenic factors in preeclampsia: so complex, so simple? Nephrol Dial Transplant 22: 2753-2756.
95. Vatten LJ, Eskild A, Nilsen TI, Jeansson S, Jenum PA, et al. (2007) Changes in circulating level of angiogenic factors from the first to second trimester as predictors of preeclampsia. Am J Obstet Gynecol 196: 239e1-6.
96. Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, et al. (2008) The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation. J Matern Fetal Neonatal Med 21: 25-40.
97. Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, et al. (2008) Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonatal Med 21: 41-52.
98. Gotsch F, Romero R, Kusanovic JP, Chaiworapongsa T, Dombrowski M, et al. (2008) Preeclampsia and small-for-gestational age are associated with decreased concentrations of a factor involved in angiogenesis: soluble Tie-2. J Matern Fetal Neonatal Med 21: 389-402.
99. Hertig A, Lefevre G, Toumi K, Rondeau E, Capeau J, et al. (2008) Soluble endoglin levels during normotensive and hypertensive pregnancies. Eur J Obstet Gynecol Reprod Biol 140: 138-140.
100. Smith GC, Wear H (2009) The perinatal implications of angiogenic factors. Curr Opin Obstet Gynecol 21: 111-116.
101. Kalkunte S, Lai Z, Norris WE, Pietras LA, Tewari N, et al. (2009) Novel approaches for mechanistic understanding and predicting preeclampsia. J Reprod Immunol 83: 134-138.
102. Wang A, Rana S, Karumanchi SA (2009) Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology (Bethesda) 24: 147-158.
103. Chaiworapongsa T, Romero R, Kusanovic JP, Mittal P, Kim SK, et al. (2010) Plasma soluble endoglin concentration in pre-eclampsia is associated with an increased impedance to flow in the maternal and fetal circulations. Ultrasound Obstet Gynecol 35: 155-162.
104. Chaiworapongsa T, Romero R, Tarca AL, Kusanovic JP, Gotsch F, et al. (2010) A decrease in maternal plasma concentrations of sVEGFR-2 precedes the clinical diagnosis of preeclampsia. Am J Obstet Gynecol 202: 550e1-10.
105. Ogge G, Romero R, Kusanovic JP, Chaiworapongsa T, Dong Z, et al. (2010) Serum and plasma determination of angiogenic and anti-Angiogenic factors yield different results: the need for standardization in clinical practice. J Matern Fetal Neonatal Med 23: 820-827.
106. Powers RW, Jeyabalan A, Clifton RG, Van Dorsten P, Hauth JC, et al. (2010) Soluble fms-Like tyrosine kinase 1 (sFlt1), endoglin and placental growth factor (PlGF) in preeclampsia among high risk pregnancies. PLoS ONE 5: e13263.
107. Sharma S, Norris WE, Kalkunte S (2010) Beyond the threshold: an etiological bridge between hypoxia and immunity in preeclampsia. J Reprod Immunol 85: 112-116.
108. Hertig A, Fort J, Lefevre G, Chabbert-Buffet N, Uzan M, et al. (2010) Soluble endoglin in preeclamptic patients with or without HELLP syndrome. Am J Obstet Gynecol 202: 594e1-4.
109. Chaiworapongsa T, Romero R, Savasan ZA, Kusanovic JP, Ogge G, et al. (2011) Maternal plasma concentrations of angiogenic/anti-Angiogenic factors are of prognostic value in patients presenting to the obstetrical triage area with the suspicion of preeclampsia. J Matern Fetal Neonatal Med 24: 1187-1207.
110. Vaisbuch E, Whitty JE, Hassan SS, Romero R, Kusanovic JP, et al. (2011) Circulating angiogenic and antiangiogenic factors in women with eclampsia. Am J Obstet Gynecol 204: 152e1-9.
111. Maynard SE, Karumanchi SA (2011) Angiogenic factors and preeclampsia. Semin Nephrol 31: 33-46.
112. Eshkoli T, Holcberg G, Bronfenmacher B, Amash A, Huleihel M, et al. (2012) Perfusion with magnesium sulfate increases sFlt-1 secretion only in the fetal side of placenta of women with preeclampsia. J Matern Fetal Neonatal Med 26: 116-122.
113. Moore AG, Young H, Keller JM, Ojo LR, Yan J, et al. (2012) Angiogenic biomarkers for prediction of maternal and neonatal complications in suspected preeclampsia. J Matern Fetal Neonatal Med 25: 2651-2657.
114. Rana S, Powe CE, Salahuddin S, Verlohren S, Perschel FH, et al. (2012) Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia. Circulation 125: 911-919.
115. Reimer T, Rohrmann H, Stubert J, Pecks U, Glocker MO, et al. (2012) Angiogenic factors and acute-phase proteins in serum samples of preeclampsia and HELLP patients: a matched-pair analysis. J Matern Fetal Neonatal Med 26: 263-269.
116. Verlohren S, Stepan H, Dechend R (2012) Angiogenic growth factors in the diagnosis and prediction of pre-eclampsia. Clin Sci (Lond) 122: 43-52.
117. Weed S, Bastek JA, Anton L, Elovitz MA, Parry S, et al. (2012) Examining the correlation between placental and serum placenta growth factor in preeclampsia. Am J Obstet Gynecol 207: 140e1-6.
118. Jebbink J, Keijser R, Veenboer G, van der Post J, Ris-Stalpers C, et al. (2011) Expression of placental FLT1 transcript variants relates to both gestational hypertensive disease and fetal growth. Hypertension 58: 70-76.
119. Whitehead CL, Palmer KR, Nilsson U, Gao Y, Saglam B, et al. (2011) Placental expression of a novel primate-specific splice variant of sFlt-1 is upregulated in pregnancies complicated by severe early onset pre-eclampsia. BJOG 118: 1268-1271.
120. Szalai G, Roberto R, Chaiworapongsa T, Xu Y, Wang B, et al. (2014) Fulllenght human placental sFlt-1-e15a isoform induces distinct maternal phenotypes of preeclampsia in mice. submitted.
121. Kumasawa K, Ikawa M, Kidoya H, Hasuwa H, Saito-Fujita T, et al. (2011) Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc Natl Acad Sci U S A 108: 1451-1455.
122. Li Z, Zhang Y, Ying Ma J, Kapoun AM, Shao Q, et al. (2007) Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 50: 686-692.
123. Lu F, Longo M, Tamayo E, Maner W, Al-Hendy A, et al. (2007) The effect of over-expression of sFlt-1 on blood pressure and the occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am J Obstet Gynecol 196: 396e1-7.
124. Lu F, Bytautiene E, Tamayo E, Gamble P, Anderson GD, et al. (2007) Genderspecific effect of overexpression of sFlt-1 in pregnant mice on fetal programming of blood pressure in the offspring later in life. Am J Obstet Gynecol 197: 418e1-5.
125. Byers BD, Betancourt A, Lu F, Hankins GD, Longo M, et al. (2009) The effect of prepregnancy obesity and sFlt-1-induced preeclampsia-like syndrome on fetal programming of adult vascular function in a mouse model. Am J Obstet Gynecol 200: 432e1-7.
126. Bergmann A, Ahmad S, Cudmore M, Gruber AD, Wittschen P, et al. (2010) Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a mouse model. J Cell Mol Med 14: 1857-1867.
127. Bytautiene E, Lu F, Tamayo EH, Hankins GD, Longo M, et al. (2010) Longterm maternal cardiovascular function in a mouse model of sFlt-1-induced preeclampsia. Am J Physiol Heart Circ Physiol 298: H189-193.
128. Costantine MM, Tamayo E, Lu F, Bytautiene E, Longo M, et al. (2010) Using pravastatin to improve the vascular reactivity in a mouse model of soluble fmslike tyrosine kinase-1-induced preeclampsia. Obstet Gynecol 116: 114-120.
129. Fox KA, Longo M, Tamayo E, Kechichian T, Bytautiene E, et al. (2011) Effects of pravastatin on mediators of vascular function in a mouse model of soluble Fms-like tyrosine kinase-1-induced preeclampsia. Am J Obstet Gynecol 205: 366e1-5.
130. Mateus J, Bytautiene E, Lu F, Tamayo EH, Betancourt A, et al. (2011) Endothelial growth factor therapy improves preeclampsia-like manifestations in a murine model induced by overexpression of sVEGFR-1. Am J Physiol Heart Circ Physiol 301: H1781-1787.
131. Suzuki H, Ohkuchi A, Matsubara S, Takei Y, Murakami M, et al. (2009) Effect of recombinant placental growth factor 2 on hypertension induced by fulllength mouse soluble fms-like tyrosine kinase 1 adenoviral vector in pregnant mice. Hypertension 54: 1129-1135.
132. National Research Council of the National Academies (2011) Guide for the Care and Use of Laboratory Animals Washington, DC: The National Academies Press.
133. Mizuguchi H, Koizumi N, Hosono T, Utoguchi N, Watanabe Y, et al. (2001) A simplified system for constructing recombinant adenoviral vectors containing heterologous peptides in the HI loop of their fiber knob. Gene Ther 8: 730-735.
134. Ahn H, Szalai G, Hernandez-Andrade E, Than NG, King M, et al. (2014) Ultrasound-guided cystocentesis for obtaining urine samples in pregnant mice. in preparation.
135. Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF, 3rd (1986) Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118: 1567-1582.
136. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101: 6062-6067.
137. Katayama K, Furuki R, Yokoyama H, Kaneko M, Tachibana M, et al. (2011) Enhanced in vivo gene transfer into the placenta using RGD fiber-mutant adenovirus vector. Biomaterials 32: 4185-4193.
138. Kamat A, Smith ME, Shelton JM, Richardson JA, Mendelson CR (2005) Genomic regions that mediate placental cell-specific and developmental regulation of human Cyp19 (aromatase) gene expression in transgenic mice. Endocrinology 146: 2481-2488.
139. Kaufmann P, Mayhew TM, Charnock-Jones DS (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 25: 114-126.
140. Mayhew TM, Charnock-Jones DS, Kaufmann P (2004) Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta 25: 127-139.
141. Jackson MR, Carney EW, Lye SJ, Ritchie JW (1994) Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation. Placenta 15: 341-353.
142. Cooper JC, Sharkey AM, Charnock-Jones DS, Palmer CR, Smith SK (1996) VEGF mRNA levels in placentae from pregnancies complicated by preeclampsia. Br J Obstet Gynaecol 103: 1191-1196.
143. Vuckovic M, Ponting J, Terman BI, Niketic V, Seif MW, et al. (1996) Expression of the vascular endothelial growth factor receptor, KDR, in human placenta. J Anat 188 (Pt 2): 361-366.
144. Shiraishi S, Nakagawa K, Kinukawa N, Nakano H, Sueishi K (1996) Immunohistochemical localization of vascular endothelial growth factor in the human placenta. Placenta 17: 111-121.
145. Shibuya M, Yamaguchi S, Yamane A, Ikeda T, Tojo A, et al. (1990) Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5: 519-524.
146. Heydarian M, McCaffrey T, Florea L, Yang Z, Ross MM, et al. (2009) Novel splice variants of sFlt1 are upregulated in preeclampsia. Placenta 30: 250-255.
147. Thomas CP, Andrews JI, Liu KZ (2007) Intronic polyadenylation signal sequences and alternate splicing generate human soluble Flt1 variants and regulate the abundance of soluble Flt1 in the placenta. FASEB J 21: 3885-3895.
148. Thomas CP, Andrews JI, Raikwar NS, Kelley EA, Herse F, et al. (2009) 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 94: 2524-2530.
149. Sharkey AM, Charnock-Jones DS, Boocock CA, Brown KD, Smith SK (1993) Expression of mRNA for vascular endothelial growth factor in human placenta. J Reprod Fertil 99: 609-615.
150. Ahmed A, Li XF, Dunk C, Whittle MJ, Rushton DI, et al. (1995) Colocalisation of vascular endothelial growth factor and its Flt-1 receptor in human placenta. Growth Factors 12: 235-243.
151. Wheeler T, Elcock CL, Anthony FW (1995) Angiogenesis and the placental environment. Placenta 16: 289-296.
152. Shore VH, Wang TH, Wang CL, Torry RJ, Caudle MR, et al. (1997) Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 18: 657-665.
153. Wilting J, Birkenhager R, Eichmann A, Kurz H, Martiny-Baron G, et al. (1996) VEGF121 induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of chorioallantoic membrane. Dev Biol 176: 76-85.
154. De Falco S (2012) The discovery of placenta growth factor and its biological activity. Exp Mol Med 44: 1-9.
155. Fan X, Rai A, Kambham N, Sung JF, Singh N, et al. (2014) Endometrial VEGF induces placental sFLT1 and leads to pregnancy complications. J Clin Invest doi: 10.1172/JCI76864.
156. Yamaguchi S, Iwata K, Shibuya M (2002) Soluble Flt-1 (soluble VEGFR-1), a potent natural antiangiogenic molecule in mammals, is phylogenetically conserved in avians. Biochem Biophys Res Commun 291: 554-559.
157. Rossant J, Cross JC (2001) Placental development: lessons from mouse mutants. Nat Rev Genet 2: 538-548.
158. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, et al. (2002) Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 250: 358-373.
159. Georgiades P, Ferguson-Smith AC, Burton GJ (2002) Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23: 3-19.
160. Carter AM (2007) Animal models of human placentation-A review. Placenta 28 Suppl A: S41-47.
161. Cox B, Kotlyar M, Evangelou AI, Ignatchenko V, Ignatchenko A, et al. (2009) Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol 5: 279.
162. Robertson WB, Brosens I, Dixon HG (1967) The pathological response of the vessels of the placental bed to hypertensive pregnancy. J Pathol Bacteriol 93: 581-592.
163. Brosens IA (1977) Morphological changes in the utero-placental bed in pregnancy hypertension. Clin Obstet Gynaecol 4: 573-593.
164. Gerretsen G, Huisjes HJ, Elema JD (1981) Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol 88: 876-881.
165. Khong TY, De Wolf F, Robertson WB, Brosens I (1986) Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 93: 1049-1059.
166. Zhou Y, Damsky CH, Fisher SJ (1997) 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 99: 2152-2164.
167. Kaufmann P, Black S, Huppertz B (2003) Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69: 1-7.
168. Espinoza J, Romero R, Kim YM, Kusanovic JP, Hassan S, et al. (2006) Normal and abnormal transformation of the spiral arteries during pregnancy. J Perinat Med 34: 447-458.
169. Brosens I, Derwig I, Brosens J, Fusi L, Benagiano G, et al. (2010) The enigmatic uterine junctional zone: the missing link between reproductive disorders and major obstetrical disorders? Hum Reprod 25: 569-574.
170. Brosens I, Pijnenborg R, Vercruysse L, Romero R (2011) The "Great Obstetrical Syndromes" are associated with disorders of deep placentation. Am J Obstet Gynecol 204: 193-201.
171. Webster RP, Roberts VH, Myatt L (2008) Protein nitration in placenta -functional significance. Placenta 29: 985-994.
172. Myatt L, Webster RP (2009) Vascular biology of preeclampsia. J Thromb Haemost 7: 375-384.
173. Young BC, Levine RJ, Karumanchi SA (2010) Pathogenesis of preeclampsia. Annu Rev Pathol 5: 173-192.
174. Redman CW, Sargent IL (2003) Pre-eclampsia, the placenta and the maternal systemic inflammatory response-A review. Placenta 24 Suppl A: S21-27.
175. Sargent IL, Germain SJ, Sacks GP, Kumar S, Redman CW (2003) Trophoblast deportation and the maternal inflammatory response in preeclampsia. J Reprod Immunol 59: 153-160.
176. Redman CW, Sargent IL (2005) Latest advances in understanding preeclampsia. Science 308: 1592-1594.
177. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW (2007) Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J Immunol 178: 5949-5956.
178. Than NG, Abdul Rahman O, Magenheim R, Nagy B, Fule T, et al. (2008) Placental protein 13 (galectin-13) has decreased placental expression but increased shedding and maternal serum concentrations in patients presenting with preterm pre-eclampsia and HELLP syndrome. Virchows Arch 453: 387-400.
179. Redman CW, Sargent IL (2009) Placental stress and pre-eclampsia: a revised view. Placenta 30 Suppl A: S38-42.
180. Singh H, Makino SI, Endo Y, Nie G (2010) Inhibition of HTRA3 stimulates trophoblast invasion during human placental development. Placenta 31: 1085-1092.
181. Balogh A, Pozsgay J, Matko J, Dong Z, Kim CJ, et al. (2011) Placental protein 13 (PP13/galectin-13) undergoes lipid raft-Associated subcellular redistribution in the syncytiotrophoblast in preterm preeclampsia and HELLP syndrome. Am J Obstet Gynecol 205: 156e1-14.
182. Li Y, Puryer M, Lin E, Hale K, Salamonsen LA, et al. (2011) Placental HtrA3 is regulated by oxygen tension and serum levels are altered during early pregnancy in women destined to develop preeclampsia. J Clin Endocrinol Metab 96: 403-411.
183. Dynon K, Heng S, Puryer M, Li Y, Walton K, et al. (2012) HtrA3 as an early marker for preeclampsia: specific monoclonal antibodies and sensitive highthroughput assays for serum screening. PLoS ONE 7: e45956.
184. Redman CW, Sargent IL (2000) Placental debris, oxidative stress and preeclampsia. Placenta 21: 597-602.
185. Chaiworapongsa T, Gervasi MT, Refuerzo J, Espinoza J, Yoshimatsu J, et al. (2002) Maternal lymphocyte subpopulations (CD45RA+ and CD45RO+) in preeclampsia. Am J Obstet Gynecol 187: 889-893.
186. Redman CW, Tannetta DS, Dragovic RA, Gardiner C, Southcombe JH, et al. (2012) Review: Does size matter? Placental debris and the pathophysiology of pre-eclampsia. Placenta 33 Suppl: S48-54.
187. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, et al. (1989) Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 161: 1200-1204.
188. Kraayenbrink AA, Dekker GA, van Kamp GJ, van Geijn HP (1993) Endothelial vasoactive mediators in preeclampsia. Am J Obstet Gynecol 169: 160-165.
189. Higgins JR, Papayianni A, Brady HR, Darling MR, Walshe JJ (1998) Circulating vascular cell adhesion molecule-1 in pre-eclampsia, gestational hypertension, and normal pregnancy: evidence of selective dysregulation of vascular cell adhesion molecule-1 homeostasis in pre-eclampsia. Am J Obstet Gynecol 179: 464-469.
190. Taylor RN, de Groot CJ, Cho YK, Lim KH (1998) Circulating factors as markers and mediators of endothelial cell dysfunction in preeclampsia. Semin Reprod Endocrinol 16: 17-31.
191. Redman CW, Sacks GP, Sargent IL (1999) Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 180: 499-506.
192. Erez O, Romero R, Kim SS, Kim JS, Kim YM, et al. (2008) Over-expression of the thrombin receptor (PAR-1) in the placenta in preeclampsia: a mechanism for the intersection of coagulation and inflammation. J Matern Fetal Neonatal Med 21: 345-355.
193. Erez O, Romero R, Hoppensteadt D, Than NG, Fareed J, et al. (2008) Tissue factor and its natural inhibitor in pre-eclampsia and SGA. J Matern Fetal Neonatal Med 21: 855-869.
194. Erez O, Romero R, Vaisbuch E, Mazaki-Tovi S, Kusanovic JP, et al. (2009) Maternal anti-protein Z antibodies in pregnancies complicated by preeclampsia, SGA and fetal death. J Matern Fetal Neonatal Med 22: 662-671.
195. Roberts JM, Hubel CA (2009) The two stage model of preeclampsia: variations on the theme. Placenta 30 Suppl A: S32-37.
196. Long PA, Abell DA, Beischer NA (1980) Fetal growth retardation and preeclampsia. Br J Obstet Gynaecol 87: 13-18.
197. Ness RB, Roberts JM (1996) Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications. Am J Obstet Gynecol 175: 1365-1370.
198. von Dadelszen P, Magee LA, Roberts JM (2003) Subclassification of preeclampsia. Hypertens Pregnancy 22: 143-148.
199. Sibai B, Dekker G, Kupferminc M (2005) Pre-eclampsia. Lancet 365: 785-799.
200. Than NG, Vaisbuch E, Kim CJ, Mazaki-Tovi S, Erez O, et al. (2012) Early-Onset Preeclampsia and HELLP Syndrome: An Overview. In: Preedy VR, editor. Handbook of growth and growth monitoring in health and disease. Heidelberg: Springer. pp. 1867-1891.
201. Moldenhauer JS, Stanek J, Warshak C, Khoury J, Sibai B (2003) The frequency and severity of placental findings in women with preeclampsia are gestational age dependent. Am J Obstet Gynecol 189: 1173-1177.
202. Sebire NJ, Goldin RD, Regan L (2005) Term preeclampsia is associated with minimal histopathological placental features regardless of clinical severity. J Obstet Gynaecol 25: 117-118.
203. Ogge G, Chaiworapongsa T, Romero R, Hussein Y, Kusanovic JP, et al. (2011) Placental lesions associated with maternal underperfusion are more frequent in early-onset than in late-onset preeclampsia. J Perinat Med 39: 641-652.
204. Xiong X, Demianczuk NN, Saunders LD, Wang FL, Fraser WD (2002) Impact of preeclampsia and gestational hypertension on birth weight by gestational age. Am J Epidemiol 155: 203-209.
205. Rasmussen S, Irgens LM (2003) Fetal growth and body proportion in preeclampsia. Obstet Gynecol 101: 575-583.
206. Raymond D, Peterson E (2011) A critical review of early-onset and late-onset preeclampsia. Obstet Gynecol Surv 66: 497-506.
207. Redman CW, Sargent IL, Staff AC (2014) IFPA Senior Award Lecture: making sense of pre-eclampsia -two placental causes of preeclampsia? Placenta 35 Suppl: S20-25.
208. Page EW (1948) Placental dysfunction in eclamptogenic toxemias. Obstet Gynecol Surv 3: 615-628.
209. Page EW (1949) The physiologic basis of symptoms in eclampsia. Calif Med 70: 1-4.
210. Redman CW (1991) Current topic: pre-eclampsia and the placenta. Placenta 12: 301-308.
211. Silasi M, Cohen B, Karumanchi SA, Rana S (2010) Abnormal placentation, angiogenic factors, and the pathogenesis of preeclampsia. Obstet Gynecol Clin North Am 37: 239-253.
212. Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg R (2010) Pre-eclampsia. Lancet 376: 631-644.
213. Eastabrook G, Brown M, Sargent I (2011) The origins and end-organ consequence of pre-eclampsia. Best Pract Res Clin Obstet Gynaecol 25: 435-447.
214. Maynard S, Epstein FH, Karumanchi SA (2008) Preeclampsia and angiogenic imbalance. Annu Rev Med 59: 61-78.
215. Wilson JM (1996) Adenoviruses as gene-delivery vehicles. N Engl J Med 334: 1185-1187.
216. Xing A, Boileau P, Cauzac M, Challier JC, Girard J, et al. (2000) Comparative in vivo approaches for selective adenovirus-mediated gene delivery to the placenta. Hum Gene Ther 11: 167-177.
217. Renaud SJ, Karim Rumi MA, Soares MJ (2011) Review: Genetic manipulation of the rodent placenta. Placenta 32 Suppl 2: S130-135.
218. Kondo K, Hiratsuka S, Subbalakshmi E, Matsushime H, Shibuya M (1998) Genomic organization of the flt-1 gene encoding for vascular endothelial growth factor (VEGF) receptor-1 suggests an intimate evolutionary relationship between the 7-Ig and the 5-Ig tyrosine kinase receptors. Gene 208: 297-305.
219. Katz AB, Keswani SG, Habli M, Lim FY, Zoltick PW, et al. (2009) Placental gene transfer: transgene screening in mice for trophic effects on the placenta. Am J Obstet Gynecol 201: 499e1-8.
220. Thadhani R, Kisner T, Hagmann H, Bossung V, Noack S, et al. (2011) Pilot study of extracorporeal removal of soluble fms-like tyrosine kinase 1 in preeclampsia. Circulation 124: 940-950.
221. Irgens HU, Reisaeter L, Irgens LM, Lie RT (2001) Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. BMJ 323: 1213-1217.
222. Ananth CV, Peltier MR, Kinzler WL, Smulian JC, Vintzileos AM (2007) Chronic hypertension and risk of placental abruption: is the association modified by ischemic placental disease? Am J Obstet Gynecol 197: 273e1-7.
223. Ananth CV, Peltier MR, Chavez MR, Kirby RS, Getahun D, et al. (2007) Recurrence of ischemic placental disease. Obstet Gynecol 110: 128-133.
224. Baumwell S, Karumanchi SA (2007) Pre-eclampsia: clinical manifestations and molecular mechanisms. Nephron Clin Pract 106: c72-81.
225. Drost JT, Maas AH, van Eyck J, van der Schouw YT (2010) Preeclampsia as a female-specific risk factor for chronic hypertension. Maturitas 67: 321-326.
226. Bytautiene E, Bulayeva N, Bhat G, Li L, Rosenblatt KP, et al. (2013) Longterm alterations in maternal plasma proteome after sFlt1-induced preeclampsia in mice. Am J Obstet Gynecol 208: 388e1-8.