Angiogenic factors in preeclampsia and related disorders

Cold Spring Harbor Perspectives in Medicine

Volumn 2, Issue 11, 2012, Pages

  Cerdeira, Ana Sofia ^a,b,c   Karumanchi, S Ananth ^a,b,d  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Howard Hughes Medical Institute ^*

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; ANGIOGENIC PROTEIN; ENDOGLIN; ENDOSTATIN; PROLACTIN; SOMATOMEDIN B; SOMATOMEDIN C RECEPTOR; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; SIGNAL PEPTIDE;

ANGIOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CYTOTROPHOBLAST; ENDOTHELIAL DYSFUNCTION; FETUS CIRCULATION; FETUS DEVELOPMENT; FETUS GROWTH; GAS EXCHANGE; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HYPERTENSION; IMMUNOREACTIVITY; OXYGEN TENSION; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PLACENTA DISORDER; PLACENTA FUNCTION; PREECLAMPSIA; PREGNANCY; PRENATAL GROWTH; PROTEIN EXPRESSION; PROTEINURIA; FEMALE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOPHYSIOLOGY; PLACENTA; REVIEW; VASCULARIZATION;

FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PLACENTA; PRE-ECLAMPSIA; PREGNANCY;

EID: 84886654196     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a006585     Document Type: Article

References (138)

1. Abuzzahab MJ, Schneider A, Goddard A, Grigorescu F, Lautier C, Keller E, KiessW, Klammt J, Kratzsch J, Osgood D, et al. 2003. IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med 349: 2211-2222.
2. Aggarwal PK, Jain V, Sakhuja V, Karumanchi SA, Jha V. 2006. Low urinary placental growth factor is a marker of pre-eclampsia. Kidney Int 69: 621-624.
3. Baker J, Liu JP, Robertson EJ, Efstratiadis A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75: 73-82.
4. Barker DJ. 2003. The developmental origins of adult disease. Eur J Epidemiol 18: 733-736.
5. Baschat AA, Hecher K. 2004. Fetal growth restriction due to placental disease. Semin Perinatol 28: 67-80.
6. Bdolah Y, Sukhatme VP, Karumanchi SA. 2004. Angiogenic imbalance in the pathophysiology of preeclampsia: Newer insights. Semin Nephrol 24: 548-556.
7. Bdolah Y, Palomaki GE, Yaron Y, Bdolah-Abram T, Goldman M, Levine RJ, SachsBP, Haddow JE, Karumanchi SA. 2006. Circulating angiogenic proteins in trisomy 13. Am J Obstet Gynecol 194: 239-245.
8. Bdolah Y, Lam C, Rajakumar A, Shivalingappa V, Mutter W, Sachs BP, Lim KH, Bdolah-Abram T, Epstein FH, Karumanchi SA. 2008. Twin pregnancy and the risk of preeclampsia: Bigger placenta or relative ischemia? Am J Obstet Gynecol 198: 428 e421-e426.
9. Bjorndahl M, Cao R, Eriksson A, Cao Y. 2004. Blockage of VEGF-induced angiogenesis by preventing VEGF secretion. Circ Res 94: 1443-1450.
10. Brosens IA, Robertson WB, Dixon HG. 1972. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1: 177-191.
11. Buhimschi CS, Norwitz ER, Funai E, Richman S, Guller S, Lockwood CJ, Buhimschi IA. 2005. Urinary angiogenic factors cluster hypertensive disorders and identify women with severe preeclampsia. Am J Obstet Gynecol 192: 734-741.
12. Carmeliet P. 2003. Angiogenesis in health and disease. Nat Med 9: 653-660.
13. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, et al. 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.
14. Carmeliet P, De Smet F, Loges S, Mazzone M. 2009. Branching morphogenesis and antiangiogenesis candidates: Tip cells lead the way. Nat Rev Clin Oncol 6: 315-326.
15. Castellucci M, Kosanke G, Verdenelli F, Huppertz B, Kaufmann P. 2000. Villous sprouting: Fundamental mechanisms of human placental development. Hum Reprod Update 6: 485-494.
16. Cerdeira AS, Karumanchi SA. 2010. Angiogenic proteins as aid in the diagnosis and prediction of preeclampsia. Scand J Clin Lab Invest Suppl 242: 73-78.
17. Chaddha V, Viero S, Huppertz B, Kingdom J. 2004. Developmental biology of the placenta and the origins of placental insufficiency. Semin Fetal Neonatal Med 9: 357-369.
18. 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; discussion 1547-1550.
19. Chaiworapongsa T, Romero R, Tarca AL, Kusanovic JP, Gotsch F, Mittal P, KimSK, Vaisbuch E, Mazaki-Tovi S, Erez O, et al. 2010. A decrease in maternal plasma concentrations of sVEGFR-2 precedes the clinical diagnosis of preeclampsia. Am J Obstet Gynecol 202: 550. e1-550. e10.
20. Chappell JC, Taylor SM, Ferrara N, Bautch VL. 2009. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev Cell 17: 377-386.
21. Charnock-Jones DS, Sharkey AM, Boocock CA, Ahmed A, Plevin R, Ferrara N, Smith SK. 1994. Vascular endothelial growth factor receptor localization and activation in human trophoblast and choriocarcinoma cells. Biol Reprod 51: 524-530.
22. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M. 1992. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 267: 19027-19030.
23. Clark DE, Smith SK, Sharkey AM, Charnock-Jones DS. 1996. Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum Reprod 11: 1090-1098.
24. Clark DE, Smith SK, Licence D, Evans AL, Charnock-Jones DS. 1998. Comparison of expression patterns for placenta growth factor, vascular endothelial growth factor (VEGF), VEGF-B and VEGF-C in the human placenta throughout gestation. J Endocrinol 159: 459-467.
25. Cooper JC, Sharkey AM, McLaren J, Charnock-Jones DS, Smith SK. 1995. Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J Reprod Fertil 105: 205-213.
26. Cross JC, Werb Z, Fisher SJ. 1994. Implantation and the placenta: Key pieces of the development puzzle. Science 266: 1508-1518.
27. Crossey PA, Pillai CC, Miell JP. 2002. Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest 110: 411-418.
28. Cudmore M, Ahmad S, Al-Ani B, Fujisawa T, Coxall H, Chudasama K, Devey LR, Wigmore SJ, Abbas A, Hewett PW, et al. 2007. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 115: 1789-1797.
29. de Rooij SR, Wouters H, Yonker JE, Painter RC, Roseboom TJ. 2010. Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci 107: 16881-16886.
30. De Wolf F, Wolf-Peeters CDe, 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.
31. DeChiara TM, Efstratiadis A, Robertson EJ. 1990. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345: 78-80.
32. Demir R. 2009. Expression of VEGF receptors VEFGR-1 and VEGFR-2, angiopoietin receptors Tie-1 and Tie-2 in chorionic villi tree during early pregnancy. Folia Histochem Cytobiol 47: 435-445.
33. Demir R, Kaufmann P, Castellucci M, Erbengi T, Kotowski A. 1989. Fetal vasculogenesis and angiogenesis in human placental villi. Acta Anat (Basel) 136: 190-203.
34. Demir R, Kayisli UA, Seval Y, Celik-Ozenci C, Korgun ET, Demir-Weusten AY, Huppertz B. 2004. Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: Differences between placental vasculogenesis and angiogenesis. Placenta 25: 560-572.
35. Duley L. 2009. The global impact of pre-eclampsia and eclampsia. Semin Perinatol 33: 130-137.
36. Dunk C, Shams M, Nijjar S, Rhaman M, Qiu Y, Bussolati B, Ahmed A. 2000. Angiopoietin-1 and angiopoietin-2 activate trophoblast Tie-2 to promote growth and migration during placental development. Am J Pathol 156: 2185-2199.
37. 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.
38. Ebos JM, Bocci G, Man S, Thorpe PE, Hicklin DJ, Zhou D, Jia X, Kerbel RS. 2004. A naturally occurring soluble form of vascular endothelial growth factor receptor 2 detected in mouse and human plasma. Mol Cancer Res 2: 315-326.
39. 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.
40. 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.
41. Ferris TF. 1991. Pregnancy, preeclampsia, and the endothelial cell. N Engl J Med 325: 1439-1440.
42. Fischer C, Mazzone M, Jonckx B, Carmeliet P. 2008. FLT1 and its ligands VEGFB and PlGF: Drug targets for anti-angiogenic therapy? Nat Rev Cancer 8: 942-956.
43. Folkman J, Shing Y. 1992. Angiogenesis. J Biol Chem 267: 10931-10934.
44. Funai EF, Friedlander Y, Paltiel O, Tiram E, Xue X, Deutsch L, Harlap S. 2005. Long-term mortality after preeclampsia. Epidemiology 16: 206-215.
45. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. 1997. Regulation of human placental development by oxygen tension. Science 277: 1669-1672.
46. Geva E, Ginzinger DG, Zaloudek CJ, Moore DH, Byrne A, Jaffe RB. 2002. Human placental vascular development: Vasculogenic and angiogenic (branching and nonbranching) transformation is regulated by vascular endothelial growth factor-A, angiopoietin-1, and angiopoietin-2. J Clin Endocrinol Metab 87: 4213-4224.
47. Goldman-Wohl DS, Ariel I, Greenfield C, Lavy Y, Yagel S. 2000. Tie-2 and angiopoietin-2 expression at the fetal-maternal interface: A receptor ligand model for vascular remodelling. Mol Hum Reprod 6: 81-87.
48. Gougos A, St Jacques S, Greaves A, O'Connell PJ, d'Apice AJ, Buhring HJ, Bernabeu C, Mourik JAvan, Letarte M. 1992. Identification of distinct epitopes of endoglin, an RGD-containing glycoprotein of endothelial cells, leukemic cells, and syncytiotrophoblasts. Int Immunol 4: 83-92.
49. Groten T, Gebhard N, Kreienberg R, Schleussner E, Reister F, Huppertz B. 2010. Differential expression of VE-cadherin and VEGFR2 in placental syncytiotrophoblast during preeclampsia-New perspectives to explain the pathophysiology. Placenta 31: 339-343.
50. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, et al. 2006. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12: 1065-1074.
51. Harrington K, Cooper D, Lees C, Hecher K, Campbell S. 1996. Doppler ultrasound of the uterine arteries: The importance of bilateral notching in the prediction of pre-eclampsia, placental abruption or delivery of a small-for-gestational-age baby. Ultrasound Obstet Gynecol 7: 182-188.
52. Hashizume H, Falcon BL, Kuroda T, Baluk P, Coxon A, Yu D, Bready JV, OlinerJD, McDonald DM. 2010. Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth. Cancer Res 70: 2213-2223.
53. He H, Venema VJ, Gu X, Venema RC, Marrero MB, Caldwell RB. 1999. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem 274: 25130-25135.
54. Helske S, Vuorela P, Carpen O, Hornig C, Weich H, Halmesmaki E. 2001. Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentas from normal and complicated pregnancies. Mol Hum Reprod 7: 205-210.
55. Herr F, Liang OD, Herrero J, Lang U, Preissner KT, Han VK, Zygmunt M. 2003. Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy. J Clin Endocrinol Metab 88: 4811-4817.
56. Holmgren L, Glaser A, Pfeifer-Ohlsson S, Ohlsson R. 1991. Angiogenesis during human extraembryonic development involves the spatiotemporal control of PDGF ligand and receptor gene expression. Development 113: 749-754.
57. Hong KH, Seki T, Oh SP. 2007. Activin receptor-like kinase 1 is essential for placental vascular development in mice. Lab Invest 87: 670-679.
58. Huckle WR, Roche RI. 2004. Post-transcriptional control of expression of sFlt-1, an endogenous inhibitor of vascular endothelial growth factor. J Cell Biochem 93: 120-132.
59. Huppertz B. 2008. The anatomy of the normal placenta. J Clin Pathol 61: 1296-1302.
60. Irgens HU, Reisaeter L, Irgens LM, Lie RT. 2001. Long term mortality of mothers and fathers after pre-eclampsia: Population based cohort study. Br Med J 323: 1213-1217.
61. Irving RJ, Belton NR, Elton RA, Walker BR. 2000. Adult cardiovascular risk factors in premature babies. Lancet 355: 2135-2136.
62. Jain RK. 2003. Molecular regulation of vessel maturation. Nat Med 9: 685-693.
63. James JL, Stone PR, Chamley LW. 2006. The regulation of trophoblast differentiation by oxygen in the first trimester of pregnancy. Hum Reprod Update 12: 137-144.
64. Jirkovska M, Janacek J, Kalab J, Kubinova L. 2008. Three-dimensional arrangement of the capillary bed and its relationship to microrheology in the terminal villi of normal term placenta. Placenta 29: 892-897.
65. Kadyrov M, Kingdom JC, Huppertz B. 2006. Divergent trophoblast invasion and apoptosis in placental bed spiral arteries from pregnancies complicated by maternal anemia and early-onset preeclampsia/intrauterine growth restriction. Am J Obstet Gynecol 194: 557-563.
66. Kanasaki K, Palmsten K, Sugimoto H, Ahmad S, Hamano Y, Xie L, Parry S, Augustin HG, Gattone VH, Folkman J, et al. 2008. Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia. Nature 453: 1117-1121.
67. Kang DH, Kim YG, Andoh TF, Gordon KL, Suga S, Mazzali M, Jefferson JA, Hughes J, Bennett W, Schreiner GF, et al. 2001. Post-cyclosporine-mediated hypertension and nephropathy: Amelioration by vascular endothelial growth factor. Am J Physiol Renal Physiol 280: F727-F736.
68. Kaufmann P, Bruns U, Leiser R, Luckhardt M, Winterhager E. 1985. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat Embryol 173: 203-214.
69. Kaufmann P, Luckhardt M, Schweikhart G, Cantle SJ. 1987. Cross-sectional features and three-dimensional structure of human placental villi. Placenta 8: 235-247.
70. Kaufmann P, Mayhew TM, Charnock-Jones DS. 2004. Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 25: 114-126.
71. Kayisli UA, Cayli S, Seval Y, Tertemiz F, Huppertz B, Demir R. 2006. Spatial and temporal distribution of Tie-1 and Tie-2 during very early development of the human placenta. Placenta 27: 648-659.
72. Kearney JB, Kappas NC, Ellerstrom C, DiPaola FW, Bautch VL. 2004. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood 103: 4527-4535.
73. Kendall RL, Thomas KA. 1993. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci 90: 10705-10709.
74. Khaw A, Kametas NA, Turan OM, Bamfo JE, Nicolaides KH. 2008. Maternal cardiac function and uterine artery Doppler at 11-14 weeks in the prediction of pre-eclampsia in nulliparous women. BJOG 115: 369-376.
75. Koga K, Osuga Y, Tajima T, Hirota Y, Igarashi T, Fujii T, Yano T, Taketani Y. 2010. Elevated serum soluble fms-like tyrosine kinase 1 (sFlt1) level in women with hydatidiform mole. Fertil Steril 94: 305-308.
76. Kohnen G, Kertschanska S, Demir R, Kaufmann P. 1996. Placental villous stroma as a model system for myofibroblast differentiation. Histochem Cell Biol 105: 415-429.
77. Kopcow HD, Karumanchi SA. 2007. Angiogenic factors and natural killer (NK) cells in the pathogenesis of preeclampsia. J Reprod Immunol 76: 23-29.
78. Kumazaki K, Nakayama M, Suehara N, Wada Y. 2002. Expression of vascular endothelial growth factor, placental growth factor, and their receptors Flt-1 and KDR in human placenta under pathologic conditions. Hum Pathol 33: 1069-1077.
79. Lam C, Lim KH, Karumanchi SA. 2005. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension 46: 1077-1085.
80. Larsson J, Goumans MJ, Sjostrand LJ, van Rooijen MA, Ward D, Leveen P, Xu X, ten Dijke P, Mummery CL, Karlsson S. 2001. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J 20: 1663-1673.
81. Lash GE, Naruse K, Innes BA, Robson SC, Searle RF, Bulmer JN. 2010. Secretion of angiogenic growth factors by villous cytotrophoblast and extravillous trophoblast in early human pregnancy. Placenta 31: 545-548.
82. Lepercq J, Guerre-Millo M, Andre J, Cauzac M, Hauguel-de Mouzon S. 2003. Leptin: A potential marker of placental insufficiency. Gynecol Obstet Invest 55: 151-155.
83. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, et al. 2004. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683.
84. Levine RJ, Thadhani R, Qian C, Lam C, Lim KH, Yu KF, Blink AL, Sachs BP, Epstein FH, Sibai BM, et al. 2005. Urinary placental growth factor and risk of preeclampsia. J Am Med Assoc 293: 77-85.
85. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, et al. 2006. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 355: 992-1005.
86. Liang OD, Korff T, Eckhardt J, Rifaat J, Baal N, Herr F, Preissner KT, Zygmunt M. 2004. Oncodevelopmental alpha-fetoprotein acts as a selective proangiogenic factor on endothelial cell from the fetomaternal unit. J Clin Endocrinol Metab 89: 1415-1422.
87. Lin S, Shimizu I, Suehara N, Nakayama M, Aono T. 1995. Uterine artery Doppler velocimetry in relation to trophoblast migration into the myometrium of the placental bed. Obstet Gynecol 85: 760-765.
88. Lok CA, Boing AN, Sargent IL, Sooranna SR, van der Post JA, Nieuwland R, SturkA. 2008. Circulating platelet-derived and placenta-derived microparticles expose Flt-1 in preeclampsia. Reprod Sci 15: 1002-1010.
89. Looman C, Sun T, Yu Y, Zieba A, Ahgren A, Feinstein R, Forsberg H, Hellberg C, Heldin CH, Zhang XQ, et al. 2007. An activating mutation in the PDGF receptor-beta causes abnormal morphology in the mouse placenta. Int J Dev Biol 51: 361-370.
90. Lopez-Lopez C, LeRoith D, Torres-Aleman I. 2004. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci 101: 9833-9838.
91. Macara L, Kingdom JC, Kaufmann P, Kohnen G, Hair J, More IA, Lyall F, Greer IA. 1996. Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta 17: 37-48.
92. Malamitsi-Puchner A, Boutsikou T, Economou E, Makrakis E, Iliodromiti Z, Kouskouni E, Hassiakos D. 2005. The role of the anti-angiogenic factor endostatin in intrauterine growth restriction. J Soc Gynecol Investig 12: 195-197.
93. Mayhew TM, Wijesekara J, Baker PN, Ong SS. 2004. Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta 25: 829-833.
94. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, MorganJP, Sellke FW, Stillman IE, 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.
95. Maynard SE, Simas TAMoore, Solitro MJ, Rajan A, Crawford S, Soderland P, Meyer BA. 2008. Circulating angiogenic factors in singleton vs multiple-gestation pregnancies. Am J Obstet Gynecol 198: 200 e201-e207.
96. Meegdes BH, Ingenhoes R, Peeters LL, Exalto N. 1988. Early pregnancy wastage: Relationship between chorionic vascularization and embryonic development. Fertil Steril 49: 216-220.
97. Mogren I, Stenlund H, Hogberg U. 2001. Long-term impact of reproductive factors on the risk of cervical, endometrial, ovarian and breast cancer. Acta Oncol 40: 849-854.
98. Naicker T, Khedun SM, Moodley J, Pijnenborg R. 2003. Quantitative analysis of trophoblast invasion in preeclampsia. Acta Obstet Gynecol Scand 82: 722-729.
99. Ohlsson R, Falck P, Hellstrom M, Lindahl P, Bostrom H, Franklin G, Ahrlund-Richter L, Pollard J, Soriano P, Betsholtz C. 1999. PDGFB regulates the development of the labyrinthine layer of the mouse fetal placenta. Dev Biol 212: 124-136.
100. Osol G, Mandala M. 2009. Maternal uterine vascular remodeling during pregnancy. Physiology (Bethesda) 24: 58-71.
101. Pardali E, Goumans MJ, ten Dijke P. 2010. Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol 20: 556-567.
102. Patel TV, Morgan JA, Demetri GD, George S, Maki RG, Quigley M, HumphreysBD. 2008. A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J Natl Cancer Inst 100: 282-284.
103. Rabinovsky ED, Draghia-Akli R. 2004. Insulin-like growth factor I plasmid therapy promotes in vivo angiogenesis. Mol Ther 9: 46-55.
104. Rahimi N, Golde TE, Meyer RD. 2009. Identification of ligand-induced proteolytic cleavage and ectodomain shedding of VEGFR-1/FLT1 in leukemic cancer cells. Cancer Res 69: 2607-2614.
105. Rajakumar A, Michael HM, Rajakumar PA, Shibata E, Hubel CA, Karumanchi SA, Thadhani R, Wolf M, Harger G, Markovic N. 2005. 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 26: 563-573.
106. Redman CW, Sargent IL. 2005. Latest advances in understanding preeclampsia. Science 308: 1592-1594.
107. 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.
108. Romundstad PR, Magnussen EB, Smith GD, Vatten LJ. 2010. Hypertension in pregnancy and later cardiovascular risk. Common antecedents? Circulation 122: 579-584.
109. Rossant J, Cross JC. 2001. Placental development: Lessons from mouse mutants. Nat Rev Genet 2: 538-548.
110. Savvidou MD, Hingorani AD, Tsikas D, Frolich JC, Vallance P, Nicolaides KH. 2003. Endothelial dysfunction and raised plasma concentrations of asymmetric dimethylarginine in pregnant women who subsequently develop pre-eclampsia. Lancet 361: 1511-1517.
111. Schulz LC. 2010. The Dutch Hunger Winter and the developmental origins of health and disease. Proc Natl Acad Sci 107: 16757-16758.
112. Sela S, Itin A, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Yagel S, Keshet E. 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.
113. Seval Y, Sati L, Celik-Ozenci C, Taskin O, Demir R. 2008. The distribution of angiopoietin-1, angiopoietin-2 and their receptors tie-1 and tie-2 in the very early human placenta. Placenta 29: 809-815.
114. Shembrey MA, Noble AD. 1995. An instructive case of abdominal pregnancy. Aust NZ J Obstet Gynaecol 35: 220-221.
115. Shibata E, Rajakumar A, Powers RW, Larkin RW, Gilmour C, Bodnar LM, Crombleholme WR, Ness RB, Roberts JM, Hubel CA. 2005. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: Relationship to circulating placental growth factor. J Clin Endocrinol Metab 90: 4895-4903.
116. Sibai B, Dekker G, Kupferminc M. 2005. Pre-eclampsia. Lancet 365: 785-799.
117. Soto-Wright V, Bernstein M, Goldstein DP, Berkowitz RS. 1995. The changing clinical presentation of complete molar pregnancy. Obstet Gynecol 86: 775-779.
118. Tayade C, Hilchie D, He H, Fang Y, Moons L, Carmeliet P, Foster RA, Croy BA. 2007. Genetic deletion of placenta growth factor in mice alters uterine NK cells. J Immunol 178: 4267-4275.
119. 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.
120. Toporsian M, Gros R, Kabir MG, Vera S, Govindaraju K, Eidelman DH, Husain M, Letarte M. 2005. A role for endoglin in coupling eNOS activity and regulating vascular tone revealed in hereditary hemorrhagic telangiectasia. Circ Res 96: 684-692.
121. Tripathi R, Rath G, Ralhan R, Saxena S, Salhan S. 2009. Soluble and membranous vascular endothelial growth factor receptor-2 in pregnancies complicated by pre-eclampsia. Yonsei Med J 50: 656-666.
122. 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.
123. 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.
124. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, et al. 2006. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 12: 642-649.
125. Vuckovic M, Ponting J, Terman BI, Niketic V, Seif MW, Kumar S. 1996. Expression of the vascular endothelial growth factor receptor, KDR, in human placenta. J Anat 188: 361-366.
126. Wang A, Rana S, Karumanchi SA. 2009. Preeclampsia: The role of angiogenic factors in its pathogenesis. Physiology (Bethesda) 24: 147-158.
127. Wolf M, Shah A, Lam C, Martinez A, Smirnakis KV, Epstein FH, Taylor RN, EckerJL, Karumanchi SA, Thadhani R. 2005. Circulating levels of the antiangiogenic marker sFLT-1 are increased in first versus second pregnancies. Am J Obstet Gynecol 193: 16-22.
128. Wulff C, Wilson H, Dickson SE, Wiegand SJ, Fraser HM. 2002. Hemochorial placentation in the primate: Expression of vascular endothelial growth factor, angiopoietins, and their receptors throughout pregnancy. Biol Reprod 66: 802-812.
129. Xuan YH, Choi YL, Shin YK, Ahn GH, Kim KH, Kim WJ, Lee HC, Kim SH. 2007. Expression of TGF-beta signaling proteins in normal placenta and gestational trophoblastic disease. Histol Histopathol 22: 227-234.
130. Zhang EG, Smith SK, Baker PN, Charnock-Jones DS. 2001. The regulation and localization of angiopoietin-1,-2, and their receptor Tie2 in normal and pathologic human placentae. Mol Med 7: 624-635.
131. Zhao H, Wong RJ, Kalish FS, Nayak NR, Stevenson DK. 2009. Effect of heme oxygenase-1 deficiency on placental development. Placenta 30: 861-868.
132. Zhao S, Gu Y, Fan R, Groome LJ, Cooper D, Wang Y. 2010. Proteases and sFlt-1 release in the human placenta. Placenta 31: 512-518.
133. Zhou Y, Damsky CH, Fisher SJ. 1997a. 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.
134. Zhou Y, Fisher SJ, Janatpour M, Genbacev O, Dejana E, Wheelock M, DamskyCH. 1997b. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest 99: 2139-2151.
135. 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.
136. Zhou CC, Ahmad S, Mi T, Xia L, Abbasi S, Hewett PW, Sun C, Ahmed A, KellemsRE, Xia Y. 2007. Angiotensin II induces soluble fms-like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ Res 100: 88-95.
137. Zhu X, Wu S, Dahut WL, Parikh CR. 2007. Risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: Systematic review and meta-analysis. Am J Kidney Dis 49: 186-193.
138. Zygmunt M, Herr F, Keller-Schoenwetter S, Kunzi-Rapp K, Munstedt K, Rao CV, Lang U, Preissner KT. 2002. Characterization of human chorionic gonadotropin as a novel angiogenic factor. J Clin Endocrinol Metab 87: 5290-5296.