Soluble Fms-like Tyrosine Kinase 1 and Endothelial Dysfunction in the Pathogenesis of Preeclampsia

Pediatric Research

Volumn 57, Issue 5, 2005, Pages 1R-7R

  Maynard, Sharon E ^a   Venkatesha, Shivalingappa ^a   Thadhani, Ravi ^a   Karumanchi, S Ananth ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOGENIC FACTOR; PROTEIN TYROSINE KINASE; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ENDOTHELIUM CELL; ENZYME ANALYSIS; FETUS; HUMAN; HYPERTENSION; IATROGENIC DISEASE; MORBIDITY; MORTALITY; PATHOGENESIS; PATHOPHYSIOLOGY; PLACENTA CIRCULATION; PREECLAMPSIA; PREMATURITY; PRIORITY JOURNAL; PROTEINURIA; REVIEW; SYNDROME DELINEATION;

ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PROTEIN STRUCTURE, TERTIARY; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 17844372519     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1203/01.PDR.0000159567.85157.B7     Document Type: Review

References (110)

1. Walker JJ 2000 Pre-eclampsia. Lancet 356:1260-1265
2. Page EW 1939 The relation between hydatid moles, relative ischemia of the gravid uterus and the placental origin of eclampsia. Am J Obstet Gynecol 37:291-293
3. Sibai BM 2003 Diagnosis and management of gestational hypertension and preeclampsia. Obstet Gynecol 102:181-192
4. Sibai BM, Mercer BM, Schiff E, Friedman SA 1994 Aggressive versus expectant management of severe preeclampsia at 28 to 32 weeks’ gestation: a randomized controlled trial. Am J Obstet Gynecol 171:818-822
5. Sibai BM, Taslimi M, Abdella TN, Brooks TF, Spinnato JA, Anderson GD 1985 Maternal and perinatal outcome of conservative management of severe preeclampsia in midtrimester. Am J Obstet Gynecol 152:32-37
6. Friedman SA, Schiff E, Kao L, Sibai BM 1995 Neonatal outcome after preterm delivery for preeclampsia. Am J Obstet Gynecol 172:1785-1788
7. Roelofsen AC, van Pampus MG, Aarnoudse JG 2003 The HELLP-syndrome; maternal-fetal outcome and follow up of infants. J Perinat Med 31:201-208
8. Abramovici D, Friedman SA, Mercer BM, Audibert F, Kao L, Sibai BM 1999 Neonatal outcome in severe preeclampsia at 24 to 36 weeks’ gestation: does the HELLP (hemolysis, elevated liver enzymes, and low platelet count) syndrome matter? Am J Obstet Gynecol 180:221-225
9. Sibai BM, Ewell M, Levine RJ, Klebanoff MA, Esterlitz J, Catalano PM, Goldenberg RL, Joffe G 1997 Risk factors associated with preeclampsia in healthy nulliparous women. The Calcium for Preeclampsia Prevention (CPEP) Study Group. Am J Obstet Gynecol 177:1003-1010
10. Caritis S, Sibai B, Hauth J, Lindheimer M, VanDorsten P, Klebanoff M, Thom E, Landon M, Paul R, Miodovnik M, Meis P, Thurnau G, Dombrowski M, McNellis D, Roberts J 1998 Predictors of pre-eclampsia in women at high risk. National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units. Am J Obstet Gynecol 179:946-951
11. Mostello D, Catlin TK, Roman L, Holcomb WL Jr, Leet T 2002 Preeclampsia in the parous woman: who is at risk? Am J Obstet Gynecol 187:425-429
12. Cunningham FG, Cox SM, Harstad TW, Mason RA, Pritchard JA 1990 Chronic renal disease and pregnancy outcome. Am J Obstet Gynecol 163:453-459
13. Sibai BM 2000 Risk factors, pregnancy complications, and prevention of hypertensive disorders in women with pregravid diabetes mellitus. J Matern Fetal Med 9:62-65
14. Weiss JL, Malone FD, Emig D, Ball RH, Nyberg DA, Comstock CH, Saade G, Eddleman K, Carter SM, Craigo SD, Carr SR, D’Alton ME, FASTER Research Consortium 2004 Obesity, obstetric complications and cesarean delivery rate—a population-based screening study. Am J Obstet Gynecol 190:1091-1097
15. Thadhani R, Stampfer MJ, Hunter DJ, Manson JE, Solomon CG, Curhan GC 1999 High body mass index and hypercholesterolemia: risk of hypertensive disorders of pregnancy. Obstet Gynecol 94:543-550
16. Ness RB, Markovic N, Bass D, Harger G, Roberts JM 2003 Family history of hypertension, heart disease, and stroke among women who develop hypertension in pregnancy. Obstet Gynecol 102:1366-1371
17. Basso O, Christensen K, Olsen J 2001 Higher risk of pre-eclampsia after change of partner. An effect of longer interpregnancy intervals? Epidemiology 12:624-629
18. Shembrey MA, Noble AD 1995 An instructive case of abdominal pregnancy. Aust N Z J Obstet Gynaecol 35:220-221
19. Hertig AT 1945 Vascular pathology in the hypertensive albuminuric toxemias of pregnancy. Clinics 4:602-614
20. Zeek PM, Assali NS 1950 Vascular changes with in the decidua associated eclamptogenic toxemia of pregnancy. Am J Clin Pathol 20:1099-1109
21. Salafia CM, Pezzullo JC, Ghidini A, Lopez-Zeno JA, Whittington SS 1998 Clinical correlations of patterns of placental pathology in preterm pre-eclampsia. Placenta 19:67-72
22. Bower S, Schuchter K, Campbell S 1993 Doppler ultrasound screening as part of routine antenatal scanning: prediction of pre-eclampsia and intrauterine growth retardation. Br J Obstet Gynaecol 100:989-994
23. North RA, Ferrier C, Long D, Townend K, Kincaid-Smith P 1994 Uterine artery Doppler flow velocity waveforms in the second trimester for the prediction of preeclampsia and fetal growth retardation. Obstet Gynecol 83:378-386
24. Aardema MW, Saro MC, Lander M, De Wolf BT, Oosterhof H, Aarnoudse JG 2004 Second trimester Doppler ultrasound screening of the uterine arteries differentiates between subsequent normal and poor outcomes of hypertensive pregnancy: two different pathophysiological entities? Clin Sci (Lond) 106:377-382
25. Cavanagh D, Rao PS, Knuppel RA, Desai U, Balis JU 1985 Pregnancy-induced hypertension: development of a model in the pregnant primate (Papio anubis). Am J Obstet Gynecol 151:987-999
26. Combs CA, Katz MA, Kitzmiller JL, Brescia RJ 1993 Experimental preeclampsia produced by chronic constriction of the lower aorta: validation with longitudinal blood pressure measurements in conscious rhesus monkeys. Am J Obstet Gynecol 169:215-223
27. Llinas MT, Alexander BT, Seedek M, Abram SR, Crell A, Granger JP 2002 Enhanced thromboxane synthesis during chronic reductions in uterine perfusion pressure in pregnant rats. Am J Hypertens 15:793-797
28. Isler CM, Bennett WA, Rinewalt AN, Cockrell KL, Martin JN Jr, Morrison JC, Granger JP 2003 Evaluation of a rat model of preeclampsia for HELLP syndrome characteristics. J Soc Gynecol Investig 10:151-153
29. De Wolf F, De Wolf-Peeters C, Brosens I, Robertson WB 1980 The human placental bed: electron microscopic study of trophoblastic invasion of spiral arteries. Am J Obstet Gynecol 137:58-70
30. Brosens IA, Robertson WB, Dixon HG 1972 The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1:177-191
31. Kumar D 1962 Chronic placental ischemia in relation to toxemias of pregnancy. A preliminary report. Am J Obstet Gynecol 84:1323-1329
32. 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
33. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, van Asshe A 1994 A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 101:669-674
34. Pijnenborg R, Anthony J, Davey DA, Rees A, Tiltman A, Vercruysse L, van Assche A 1991 Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 98:648-655
35. Zhou Y, Damsky CH, Chiu K, Roberts JM, Fisher SJ 1993 Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 91:950-960
36. Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, Damsky CH 1997 Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest 99:2139-2151
37. 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
38. Caniggia I, Grisaru-Gravnosky S, Kuliszewsky M, Post M, Lye SJ 1999 Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J Clin Invest 103:1641-1650
39. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, Post M 2000 Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 105:577-587
40. Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, Alitalo K, Damsky C, Fisher SJ 2002 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 160:1405-1423
41. Zhou Y, Chiu K, Brescia RJ, Combs CA, Katz MA, Kitzmiller JL, Heilbron DC, Fisher SJ 1993 Increased depth of trophoblast invasion after chronic constriction of the lower aorta in rhesus monkeys. Am J Obstet Gynecol 169:224-229
42. Ferris TF 1991 Pregnancy, preeclampsia, and the endothelial cell. N Engl J Med 325:1439-1440
43. Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK 1989 Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 161:1200-1204
44. Calvin S, Corrigan J, Weinstein L, Jeter M 1988 Factor VIII: von Willebrand factor patterns in the plasma of patients with pre-eclampsia. Am J Perinatol 5:29-32
45. Lockwood CJ, Peters JH 1990 Increased plasma levels of ED1+ cellular fibronectin precede the clinical signs of preeclampsia. Am J Obstet Gynecol 162:358-362
46. Nova A, Sibai BM, Barton JR, Mercer BM, Mitchell MD 1991 Maternal plasma level of endothelin is increased in preeclampsia. Am J Obstet Gynecol 165:724-727
47. Davidge ST 1998 Oxidative stress and altered endothelial cell function in preeclampsia. Semin Reprod Endocrinol 16:65-73
48. Hubel CA, McLaughlin MK, Evans RW, Hauth BA, Sims CJ, Roberts JM 1996 Fasting serum triglycerides, free fatty acids, and malondialdehyde are increased in preeclampsia, are positively correlated, and decrease within 48 hours post partum. Am J Obstet Gynecol 174:975-982
49. Kolben M, Lopens A, Blaser J, Huber A, Frank M, Wilhelm O, Wilhelm S, Schneider KT, Ulm K, Tschesche H 1995 Measuring the concentration of various plasma and placenta extract proteolytic and vascular factors in pregnant patients with HELLP syndrome, pre-eclampsia and highly pathologic Doppler flow values. Gynakolo Geburtshilfliche Rundschau 35(suppl 1):126-131
50. Chappell LC, Seed PT, Briley A, Kelly FJ, Hunt BJ, Charnock-Jones DS, Mallet AI, Poston L 2002 A longitudinal study of biochemical variables in women at risk of preeclampsia. Am J Obstet Gynecol 187:127-136
51. Mills JL, DerSimonian R, Raymond E, Morrow JD, Roberts LJ II, Clemens JD, Hauth JC, Catalano P, Sibai B, Curet LB, Levine RJ 1999 Prostacyclin and thromboxane changes predating clinical onset of preeclampsia: a multicenter prospective study. JAMA 282:356-362
52. Gant NF, Daley GL, Chand S, Whalley PJ, McDonald PC 1973 A study of angiotensin II pressor response throughout primigravid pregnancy. J Clin Invest 52:2682-2689
53. Ashworth JR, Warren AY, Baker PN, Johnson IR 1997 Loss of endothelium-dependent relaxation in myometrial resistance arteries in pre-eclampsia. Br J Obstet Gynaecol 104:1152-1158
54. Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS 2001 Association of maternal endothelial dysfunction with preeclampsia. JAMA 285:1607-1612
55. Spargo BH, McCartney C, Winemiller R 1959 Glomerular capillary endotheliosis in toxemia of pregnancy. Arch Pathol 13:593-599
56. Fisher KA, Luger A, Spargo BH, Lindheimer MD 1981 Hypertension in pregnancy: clinical-pathological correlations and remote prognosis. Medicine (Baltimore) 60:267-276
57. Morris RH, Vassaldi PI, Beller FK, McCluskey RT 1964 Immunofluorescent studies of renal biopsies in the diagnosis of toxemia of pregnancy. Obstet Gynecol 24:32-46
58. Strevens H, Wide-Swensson D, Hansen A, Horn T, Ingemarsson I, Larsen S, Willner J, Olsen S 2003 Glomerular endotheliosis in normal pregnancy and pre-eclampsia. BJOG 110:831-836
59. 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
60. Haukkamaa L, Salminen M, Laivuori H, Leinonen H, Hiilesmaa V, Kaaja R 2004 Risk for subsequent coronary artery disease after preeclampsia. Am J Cardiol 93:805-808
61. Smith GC, Pell JP, Walsh D 2001 Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet 357:2002-2006
62. Epstein FH 1964 Late vascular effects of toxemia of pregnancy. N Eng J Med 271:391-395
63. Agatisa PK, Ness RB, Roberts JM, Constantino JP, Kuller LH, McLaughlin MK 2004 Impairment of endothelial function in women with a history of preeclampsia: an indicator of cardiovascular risk. Am J Physiol Heart Circ Physiol 286:1389-1393
64. Polednak AP, Janerich DT 1983 Characteristics of first pregnancy in relation to early breast cancer. A case-control study. J Reprod Med 28:314-318
65. Vatten LJ, Romundstad PR, Trichopoulos D, Skjaerven R 2002 Pre-eclampsia in pregnancy and subsequent risk for breast cancer. Br J Cancer 87:971-973
66. Baker PN, Davidge ST, Roberts JM 1995 Plasma from women with preeclampsia increases endothelial cell nitric oxide production. Hypertension 26:244-248
67. Roberts JM, Edep ME, Goldfien A, Taylor RN 1992 Sera from preeclamptic women specifically activate human umbilical vein endothelial cells in vitro: morphological and biochemical evidence. Am J Reprod Immunol 27:101-108
68. de Groot CJ, Murai JT, Vigne JL, Taylor RN 1998 Eicosanoid secretion by human endothelial cells exposed to normal pregnancy and preeclampsia plasma in vitro. Prostaglandins Leukot Essent Fatty Acids 58:91-97
69. Hayman R, Warren A, Brockelsby J, Johnson I, Baker P 2000 Plasma from women with pre-eclampsia induces an in vitro alteration in the endothelium-dependent behaviour of myometrial resistance arteries. BJOG 107:108-115
70. Roberts JM, Lain KY 2002 Recent Insights into the pathogenesis of pre-eclampsia. Placenta 23:359-372
71. Page NM, Woods RJ, Gardiner SM, Lomthaisong K, Gladwell RT, Butlin DJ, Manyonda IT, Lowry PJ 2000 Excessive placental secretion of neurokinin B during the third trimester causes pre-eclampsia. Nature 405:797-800
72. Schlembach D, Scalera F, Fischer T, Marx SG, Beinder E, Garfield RE 2003 Neurokinin B peptide serum levels are higher in normotensive pregnant women than in preeclamptic pregnant women. Am J Obstet Gynecol 189:1418-1422
73. Wareing M, Bhatti H, O’Hara M, Kenny L, Warren AY, Taggart MJ, Baker PN 2003 Vasoactive effects of neurokinin B on human blood vessels. Am J Obstet Gynecol 188:196-202
74. Smarason AK, Sargent IL, Starkey PM, Redman CW 1993 The effect of placental syncytiotrophoblast microvillous membranes from normal and pre-eclamptic women on the growth of endothelial cells in vitro. BJOG 100:943-949
75. AbdAlla S, Lother H, el Massiery A, Quitterer U 2001 Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med 7:1003-1009
76. Ward K, Hata A, Jeunemaitre X, Helin C, Nelson L, Namikawa C, Farrington PF, Ogasawara M, Suzumori K, Tomoda S 1993 A molecular variant of angiotensinogen associated with preeclampsia. Nat Genet 4:59-61
77. 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 1999 Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest 103:945-952
78. Xia Y, Wen H, Bobst S, Day MC, Kellems RE 2003 Maternal autoantibodies from preeclamptic patients activate angiotensin receptors on human trophoblast cells. J Soc Gynecol Investig 10:82-93
79. Dechend R, Viedt C, Muller DN, Ugele B, Brandes RP, Wallukat G, Park JK, Janke J, Barta P, Theuer J, Fiebeler A, Homuth V, Dietz R, Haller H, Kreuzer J, Luft FC 2003 AT1 receptor agonistic antibodies from preeclamptic patients stimulate NADPH oxidase. Circulation 107:1632-1639
80. 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 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
81. Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y 2003 Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 88:2348-2351
82. Tsatsaris V, Goffin F, Munaut C, Brichant JF, Pignon MR, Noel A, Schaaps JP, Cabrol D, Frankenne F, Foidart JM 2003 Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 88:5555-5563
83. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Goncalves LF, Gomez R, Edwin S 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
84. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA 2003 Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 188:177-182
85. 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 2002 Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 8:831-840
86. 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 2001 Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7:575-583
87. Dvorak HF 2002 Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol 20:4368-4380
88. Kendall RL, Thomas KA 1993 Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 90:10705-10709
89. Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, Kozuma S, Taketani Y 2004 Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 145:4838-4845
90. 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 2004 Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350:672-683
91. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, Ecker J, Karumanchi SA 2004 First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 89:770-775
92. Simon M, Grone HJ, Johren O, Kullmer J, Plate KH, Risau W, Fuchs E 1995 Expression of vascular endothelial growth factor and its receptors in human renal ontogenesis and in adult kidney. Am J Physiol 268:F240-F250
93. Simon M, Rockl W, Hornig C, Grone EF, Theis H, Weich HA, Fuchs E, Yayon A, Grone HJ 1998 Receptors of vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) in fetal and adult human kidney: localization and [125I]VEGF binding sites. J Am Soc Nephrol 9:1032-1044
94. Masuda Y, Shimizu A, Mori T, Ishiwata T, Kitamura H, Ohashi R, Ishizaki M, Asano G, Sugisaki Y, Yamanaka N 2001 Vascular endothelial growth factor enhances glomerular capillary repair and accelerates resolution of experimentally induced glomerulonephritis. Am J Pathol 159:599-608
95. Ostendorf T, Kunter U, Eitner F, Loos A, Regele H, Kerjaschki D, Henninger DD, Janjic N, Floege J 1999 VEGF(165) mediates glomerular endothelial repair. J Clin Invest 104:913-923
96. Kabbinavar F, Hurwitz HI, Fehrenbacher L, Meropol NJ, Novotny WF, Lieberman G, Griffing S, Bergsland E 2003 Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21:60-65
97. Yang JC, Haworth L, Sherry RM, Hwu P, Schwartzentruber DJ, Topalian SL, Steinberg SM, Chen HX, Rosenberg SA 2003 A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349:427-434
98. Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W 1998 Vascular endothelial growth factor induces endothelial fenestrations in vitro. J Cell Biol 140:947-959
99. Lain KY, Wilson JW, Crombleholme WR, Ness RB, Roberts JM 2003 Smoking during pregnancy is associated with alterations in markers of endothelial function. Am J Obstet Gynecol 189:1196-1201
100. Heeschen C, Jang JJ, Weis M, Pathak A, Kaji S, Hu RS, Tsao PS, Johnson FL, Cooke JP 2001 Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 7:833-839
101. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE 2003 Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111:707-716
102. Tuohy JF, James DK 1992 Pre-eclampsia and trisomy 13. Br J Obstet Gynaecol 99:891-894
103. Moses EK, Lade JA, Guo G, Wilton AN, Grehan M, Freed K, Borg A, Terwilliger JD, North R, Cooper DW, Brennecke SP 2000 A genome scan in families from Australia and New Zealand confirms the presence of a maternal susceptibility locus for pre-eclampsia, on chromosome 2. Am J Hum Genet 67:1581-1585
104. Arngrimsson R, Sigurard ttir S, Frigge ML, Bjarnad ttir RI, Jonsson T, Stefansson H, Baldursdottir A, Einarsdottir AS, Palsson B, Snorradottir S, Lachmeijer AM, Nicolae D, Kong A, Bragason BT, Gulcher JR, Geirsson RT, Stefansson K 1999 A genome-wide scan reveals a maternal susceptibility locus for pre-eclampsia on chromosome 2p13. Hum Mol Genet 8:1799-1805
105. Wolf M, Sandler L, Munoz K, Hsu K, Ecker JL, Thadhani R 2002 First trimester insulin resistance and subsequent preeclampsia: a prospective study. J Clin Endocrinol Metab 87:1563-1568
106. Skjaerven R, Wilcox AJ, Lie RT 2002 The interval between pregnancies and the risk of preeclampsia. N Engl J Med 346:33-38
107. Robillard PY, Hulsey TC, Perianin J, Janky E, Miri EH, Papiernik E 1994 Association of pregnancy-induced hypertension with duration of sexual cohabitation before conception. Lancet 344:973-975
108. Thadhani R, Ecker JL, Mutter WP, Wolf M, Smirnakis KV, Sukhatme VP, Levine RJ, Karumanchi SA 2004 Insulin resistance and alterations in angiogenesis: additive insults that may lead to preeclampsia. Hypertension 43:988-992
109. Ahmad S, Ahmed A2004 Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res
110. Karumanchi SA, Lim KH, Sukhatme VP, August P 2004 Pathogenesis of preeclampsia. in Rose BD (ed) UpToDate, Wellesley, MA, UpToDate Inc.