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Volume 13, Issue 5 (7-2015)
IJRM 2015, 13(5): 251-262 |
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Nikuei P, Malekzadeh K, Rajaei M, Nejatizadeh A, Ghasemi N. The imbalance in expression of angiogenic and anti-angiogenic factors as candidate predictive biomarker in preeclampsia. IJRM 2015; 13 (5) :251-262
URL: http://ijrm.ir/article-1-652-en.html
URL: http://ijrm.ir/article-1-652-en.html
1- Molecular Medicine Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
2- Molecular Medicine Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran ,keyanoosh@gmail.com
3- Fertility and Infertility Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
4- Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
2- Molecular Medicine Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran ,
3- Fertility and Infertility Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
4- Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences, Yazd, Iran
Abstract: (3105 Views)
Preeclampsia is an important pregnancy disorder with serious maternal and fetal complications which its etiology has not been completely understood yet. Early diagnosis and management of disease could reduce its potential side effects. The vascular endothelial growth factor (VEGF) family including VEGF-A is the most potent endothelial growth factor which induces angiogenesis and endothelial cell proliferation and has basic role in vasculogenesis. VEGF and its tyrosine kinase receptors (Flt1 and KDR) are major factors for fetal and placental angiogenic development. Finding mechanisms involved in expression of angiogenic factors may lead to new prognostic and therapeutic points in management of preeclampsia. Recent researches, has shown capability of some anti-angiogenic factors as potential candidate to be used as early predictors for preeclampsia. Soluble fms-like tyrosin kinase-1 (sFlt1) is a truncated splice variant of the membrane-bound VEGF receptor Flt1, that is produced by the placenta and it can bind to angiogenic growth factors and neutraliz, their effects. It is also observed that the ratio of sFlt1 to placental growth factor is valuable as prognostic marker. In this review, VEGF family member’s role in angiogenesis is evaluated as biomarkers to be used for prediction of preeclampsia.
Keywords: Preeclampsia, Angiogenic proteins, Biomarker, Vascular endothelial growth factor (VEGF-A), Vascular endothelial growth factor receptor-1 (VEGFR-1).
Type of Study: Original Article |
References
1. Zhu XM, Han T, Sargent IL, Yin GW, Yao YQ. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am J Obstet Gynecol 2009; 200: 661. [DOI:10.1016/j.ajog.2008.12.045]
2. Wang W, Feng L, Zhang H, Hachy S, Satohisa S, Laurent LC, et al. Preeclampsia up-regulates angiogenesis-associated microRNA (ie., miR-17,-20a, and-20b) that target ephrin-B2 and EPHB4 in human placenta. J Clin Endocrinol Metab 2012; 97: 1051-1059. [DOI:10.1210/jc.2011-3131]
3. Choudhury M, Friedman JE. Epigenetics and microRNAs in preeclampsia. Clin Exp Hypertens 2012; 34: 334-341. [DOI:10.3109/10641963.2011.649931]
4. Duley L. The global impact of pre-eclampsia and eclampsia. Semin Perinatol 2009;33:130-137. [DOI:10.1053/j.semperi.2009.02.010]
5. Nejatizadeh A, Stobdan T, Malhotra N, Pasha MQ. The genetic aspects of pre-eclampsia: achievements and limitations. Biochem Genet 2008; 46: 451-479. [DOI:10.1007/s10528-008-9163-9]
6. Buurma A, Turner R, Driessen J, Mooyaart A, choones J, Bruijn J, et al. Genetic variants in pre-eclampsia: a meta-analysis. Hum Reprod Update 2013; 19: 289-303. [DOI:10.1093/humupd/dms060]
7. Miko E, Meggyes M, Bogar B, Schmitz N, Barakonyi A, Varnagy A, et al. Involvement of Galectin-9/TIM-3 Pathway in the Systemic Inflammatory Response in Early-Onset Preeclampsia. Plos One 2013; 8: e71811. [DOI:10.1371/journal.pone.0071811]
8. Kleinrouweler C, Wiegerinck M, Ris‐Stalpers C, Bossuyt P, van der Post J, Von Dadelszen P, et al. Accuracy of circulating placental growth factor, vascular endothelial growth factor, soluble fms‐like tyrosine kinase 1 and soluble endoglin in the prediction of pre‐eclampsia: a systematic review and meta‐analysis. BJOG 2012; 119: 778-787. [DOI:10.1111/j.1471-0528.2012.03311.x]
9. Lam C, Lim K-H, Karumanchi SA. Circulating Angiogenic Factors in the Pathogenesis and Prediction of Preeclampsia. Hypertension 2005; 46: 1077-1085. [DOI:10.1161/01.HYP.0000187899.34379.b0]
10. Mutter WP, Karumanchi SA. Molecular mechanisms of preeclampsia. Microvasc Res 2008; 75: 1-8. [DOI:10.1016/j.mvr.2007.04.009]
11. Karimi S, Azinfar A, Rajaei M, Azizi KM. Evaluation the frequency of factor v leiden mutation in pregnant women with preeclampsia syndrome in an iranian population. Iran J Reprod Med 2012; 10: 59-66.
12. Wang A, Rana S, Karumanchi SA. Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology 2009; 24: 147-158. [DOI:10.1152/physiol.00043.2008]
13. Zygmunt M, Herr F, Münstedt K, Lang U, Liang OD. Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol 2003; 110: S10-S8. [DOI:10.1016/S0301-2115(03)00168-4]
14. Escudero CA, Roberts JM, Myatt L, Feoktistov I. Impaired adenosine-mediated angiogenesis in preeclampsia: potential implications for fetal programming. Cardiovasc Smooth Muscle Pharmacol 2014; 5: 134. [DOI:10.3389/fphar.2014.00134]
15. Shibuya M. Involvement of Flt1 (VEGF receptor-1) in cancer and preeclampsia. Proc Japan Acadm Series B, Physic Biol Sci 2010; 87: 167-178. [DOI:10.2183/pjab.87.167]
16. Cerdeira AS, Karumanchi SA. Angiogenic factors in preeclampsia and related disorders. Cold Spring Harbor Perspect Med 2012; 2: Pii: a006585. [DOI:10.1101/cshperspect.a006585]
17. Harapan H, Andalas M, Mudhakir D, Pedroza NC, Laddha SV, Anand JR. Micro RNA: New aspect in pathobiology of preeclampsia? Egypt J Med Hum Genet 2012; 13: 127-131. [DOI:10.1016/j.ejmhg.2011.09.002]
18. Bdolah Y, Sukhatme VP, Karumanchi SA. Angiogenic imbalance in the pathophysiology of preeclampsia: newer insights. Semin Nephrol 2004; 24:548-556. [DOI:10.1016/j.semnephrol.2004.07.003]
19. Agarwal I, Karumanchi SA. Preeclampsia and the anti-angiogenic state. Pregnancy Hypertension: An Int J Women's Cardiovasc Health 2011; 1: 17-21. [DOI:10.1016/j.preghy.2010.10.007]
20. Carmeliet P, De Smet F, Loges S, Mazzone M. Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way. Nature Rev Clin Oncol 2009; 6: 315-326. [DOI:10.1038/nrclinonc.2009.64]
21. Fu G, Brkić J, Hayder H, Peng C. MicroRNAs in Human Placental Development and Pregnancy Complications. Int J Mol Sci 2013; 14: 5519-5544. [DOI:10.3390/ijms14035519]
22. Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J Clin Invest 1997; 99: 2152. [DOI:10.1172/JCI119388]
23. Naicker T, Khedun SM, Moodley J, Pijnenborg R. Quantitative analysis of trophoblast invasion in preeclampsia. Acta Obstet Gynecol Scand 2003; 82: 722-729. [DOI:10.1034/j.1600-0412.2003.00220.x]
24. Kadyrov M, Kingdom JC, Huppertz B. 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 2006; 194: 557-563. [DOI:10.1016/j.ajog.2005.07.035]
25. Furuya M, Kurasawa K, Nagahama K, Kawachi K, Nozawa A, Takahashi T, et al. Disrupted balance of angiogenic and antiangiogenic signalings in preeclampsia. J Pregnancy 2011; 2011: 123717. [DOI:10.1155/2011/123717]
26. Tsatsaris V, Goffin F, Munaut C, Brichant J-F, Pignon M-R, Noel A, et al. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metabo 2003; 88: 5555-5563. [DOI:10.1210/jc.2003-030528]
27. Ferrara N, Gerber HP. The role of vascular endothelial growth factor in angiogenesis. Acta Haematol 2001; 106: 148-156. [DOI:10.1159/000046610]
28. Thomas CP, Andrews JI, Liu KZ. Intronic polyadenylation signal sequences and alternate splicing generate human soluble Flt1 variants and regulate the abundance of soluble Flt1 in the placenta. FASEB J 2007; 21: 3885-3895. [DOI:10.1096/fj.07-8809com]
29. Kim JY, Whang JH, Zhou W, Shin J, Noh SM, Song IS, et al. The expression of VEGF receptor genes is concurrently influenced by epigenetic gene silencing of the genes and VEGF activation. Epigenetics 2009; 4: 313-321. [DOI:10.4161/epi.4.5.9160]
30. Geva E, Ginzinger DG, Zaloudek CJ, Moore DH, Byrne A, Jaffe RB. Human placental vascular development: vasculogenic and angiogenic (branching and nonbranching) transformation is regulated by vascular endothelial growth factor-A, angiopoietin-1, and angiopoietin-2. J Clin Endocrinol Metab 2002; 87: 4213-4224. [DOI:10.1210/jc.2002-020195]
31. Demir R, Kayisli U, Seval Y, Celik-Ozenci C, Korgun E, Demir-Weusten A, et al. Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta 2004; 25: 560-572. [DOI:10.1016/j.placenta.2003.11.011]
32. Morbidelli L, Chang C-H, Douglas JG, Granger HJ, Ledda F, Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol Heart Circul Physiol 1996; 270: 411-415. [DOI:10.1152/ajpheart.1996.270.1.H411]
33. He H, Venema VJ, Gu X, Venema RC, Marrero MB, Caldwell RB. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem 1999; 274: 25130-25135. [DOI:10.1074/jbc.274.35.25130]
34. Taylor C, Stevens H, Anthony F, Wheeler T. Influence of hypoxia on vascular endothelial growth factor and chorionic gonadotrophin production in the trophoblast-derived cell lines: JEG, JAr and BeWo. Placenta 1997; 18: 451-458. [DOI:10.1016/S0143-4004(97)80047-1]
35. Kingdom J, Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta 1997; 18: 613-621. [DOI:10.1016/S0143-4004(97)90000-X]
36. Cerdeira AS, Karumanchi SA. Angiogenic factors in preeclampsia and related disorders. Cold Spring Harbor Perspect Med 2012; 2: pii: a006585. [DOI:10.1101/cshperspect.a006585]
37. Zhou CC, Ahmad S, Mi T, Xia L, Abbasi S, Hewett PW, et al. Angiotensin II induces soluble fms-Like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circul Res 2007; 100: 88-95. [DOI:10.1161/01.RES.0000254703.11154.18]
38. Patel TV, Morgan JA, Demetri GD, George S, Maki RG, Quigley M, et al. A preeclampsia-like syndrome characterized by reversible hypertension and proteinuria induced by the multitargeted kinase inhibitors sunitinib and sorafenib. J National Cancer Institute 2008; 100: 282-284. [DOI:10.1093/jnci/djm311]
39. Vatten L, Romundstad P, Trichopoulos D, Skjaerven R. Pre-eclampsia in pregnancy and subsequent risk for breast cancer. Br J Cancer 2002; 87: 971-973. [DOI:10.1038/sj.bjc.6600581]
40. Kuroda M, Oka T, Oka Y, Yamochi T, Ohtsubo K, Mori S, et al. Colocalization of vascular endothelial growth factor (vascular permeability factor) and insulin in pancreatic islet cells. J Clin Endocrinol Metab 1995; 80: 3196-3200.
41. Torry DS, Mukherjea D, Arroyo J, Torry RJ. Expression and function of placenta growth factor: implications for abnormal placentation. J Soc Gynecol Invest 2003; 10: 178-188. [DOI:10.1016/S1071-55760300048-0]
42. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nature Med 2001; 7: 575-583. [DOI:10.1038/87904]
43. Park JE, Chen HH, Winer J, Houck KA, Ferrara N. Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt1 but not to Flk-1/KDR. J Bioll Chem 1994; 269: 25646-25654.
44. Sawano A, Takahashi T, Yamaguchi S, Aonuma M, Shibuya M. Flt1 but not KDR/Flk-1 tyrosine kinase is a receptor for placenta growth factor, which is related to vascular endothelial growth factor. Cell Growth Differ 1996; 7: 213-221.
45. Shibuya M, Claesson-Welsh L. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res 2006; 312: 549-560. [DOI:10.1016/j.yexcr.2005.11.012]
46. Levine RJ, Maynard SE, Qian C, Lim K-H, England LJ, Yu KF, et al. Circulating angiogenic factors and the risk of preeclampsia. New Engl J Med 2004; 350: 672-683. [DOI:10.1056/NEJMoa031884]
47. Madazli R, Kuseyrioglu B, Uzun H, Uludag S, Ocak V. Prediction of preeclampsia with maternal mid-trimester placental growth factor, activin A, fibronectin and uterine artery Doppler velocimetry. Int J Gynecol Obstet 2005; 89: 251-257. [DOI:10.1016/j.ijgo.2005.02.008]
48. Muy-Rivera M, Vadachkoria S, Woelk G, Qiu C, Mahomed K, Williams M. Maternal plasma VEGF, sVEGF-R1, and PIGF concentrations in preeclamptic and normotensive pregnant Zimbabwean women. Physiol Res 2005; 54: 611.
49. Maynard SE, Min J-Y, Merchan J, Lim K-H, Li J, Mondal S, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003; 111: 649-658. [DOI:10.1172/JCI17189]
50. Helske S, Vuorela P, Carpén O, Hornig C, Weich H, Halmesmäki E. Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentas from normal and complicated pregnancies. Mol Hum Reprod 2001; 7: 205-210. [DOI:10.1093/molehr/7.2.205]
51. Savvidou M, Akolekar R, Zaragoza E, Poon L, Nicolaides K. First trimester urinary placental growth factor and development of pre‐eclampsia. BJOG 2009; 116: 643-647. [DOI:10.1111/j.1471-0528.2008.02074.x]
52. Cooper JC, Sharkey AM, Charnock‐Jones DS, Palmer CR, Smith SK. VEGF mRNA levels in placentae from pregnancies complicated by pre‐eclampsia. BJOG 1996; 103: 1191-1196. [DOI:10.1111/j.1471-0528.1996.tb09627.x]
53. Polliotti BM, Fry AG, Saller Jr DN, Mooney RA, Cox C, Miller RK. Second‐trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early‐onset preeclampsia. Obstet Gynecol 2003; 101: 1266-1274.
54. Kim SC, Park MJ, Joo BS, Joo JK, Suh DS, Lee KS. Decreased expressions of vascular endothelial growth factor and visfatin in the placental bed of pregnancies complicated by preeclampsia. J Obstet Gynaecol Res 2012; 38: 665-673. [DOI:10.1111/j.1447-0756.2011.01773.x]
55. Andraweera PH, Dekker GA, Laurence JA, Roberts CT. Placental expression of VEGF family mRNA in adverse pregnancy outcomes. Placenta 2012; 33: 467-472. [DOI:10.1016/j.placenta.2012.02.013]
56. Lee GSR, Joe YS, Kim SJ, Shin JC. Cytokine-related genes and oxidation-related genes detected in preeclamptic placentas. Arch Gynecol Obstet 2010; 282: 363-369. [DOI:10.1007/s00404-009-1222-x]
57. Chung J-Y, Song Y, Wang Y, Magness RR, Zheng J. Differential expression of vascular endothelial growth factor (VEGF), endocrine gland derived-VEGF, and VEGF receptors in human placentas from normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2004; 89: 2484-2490. [DOI:10.1210/jc.2003-031580]
58. Jarvenpaa J, Vuoristo JT, Savolainen E-R, Ukkola O, Vaskivuo T, Ryynanen M. Altered expression of angiogenesis-related placental genes in pre-eclampsia associated with intrauterine growth restriction. Gynecol Endocrinol 2007; 23: 351-355. [DOI:10.1080/09513590701350291]
59. Ranheim T, Staff AC, Henriksen T. VEGF mRNA is unaltered in decidual and placental tissues in preeclampsia at delivery. Acta Obstet Gynecol Scand 2001; 80: 93-98. [DOI:10.1034/j.1600-0412.2001.080002093.x]
60. Sgambati E, Marini M, Zappoli Thyrion GD, Parretti E, Mello G, Orlando C, et al. VEGF expression in the placenta from pregnancies complicated by hypertensive disorders. BJOG 2004; 111: 564-570. [DOI:10.1111/j.1471-0528.2004.00143.x]
61. Andraweera PH, Dekker GA, Roberts CT. The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum Reprod Update 2012; 18: 436-457. [DOI:10.1093/humupd/dms011]
62. Demir R. 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 2009; 47: 435-445.
63. Marini M, Vichi D, Toscano A, Thyrion GZ, Parretti E, Mello G, et al. Expression of vascular endothelial growth factor receptor types 1, 2 and 3 in placenta from pregnancies complicated by hypertensive disorders. Reprod Fertil Dev 2007; 19: 641-651. [DOI:10.1071/RD06131]
64. Nishizawa H, Ota S, Suzuki M, Kato T, Sekiya T, Kurahashi H, et al. Comparative gene expression profiling of placentas from patients with severe pre-eclampsia and unexplained fetal growth restriction. Reprod Biol Endocrinol 2011; 9: 107. [DOI:10.1186/1477-7827-9-107]
65. Munaut C, Lorquet S, Pequeux C, Coulon C, Le Goarant J, Chantraine F, et al. Differential expression of Vegfr-2 and its soluble form in preeclampsia. Plos One 2012; 7: e33475. [DOI:10.1371/journal.pone.0033475]
66. Tripathi R, Rath G, Jain A, Salhan S. Soluble and membranous vascular endothelial growth factor receptor-1 in pregnancies complicated by pre-eclampsia. Ann Anat 2008; 190: 477-489. [DOI:10.1016/j.aanat.2008.08.002]
67. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Gonçalves LF, et al. 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 2004; 190: 1541-1547. [DOI:10.1016/j.ajog.2004.03.043]
68. Shibata E, Rajakumar A, Powers RW, Larkin RW, Gilmour C, Bodnar LM, et al. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: relationship to circulating placental growth factor. J Clin Endocrinol Metab 2005; 90: 4895-4903. [DOI:10.1210/jc.2004-1955]
69. Sitras V, Paulssen R, Grønaas H, Leirvik J, Hanssen T, Vartun A, et al. Differential placental gene expression in severe preeclampsia. Placenta 2009; 30: 424-433. [DOI:10.1016/j.placenta.2009.01.012]
70. Toft JH, Toft JH, Lian IA, Tarca AL, Erez O, Espinoza J, et al. Whole-genome microarray and targeted analysis of angiogenesis-regulating gene expression (ENG, FLT1, VEGF, PlGF) in placentas from pre-eclamptic and small-for-gestational-age pregnancies. J Matern Fetal Neonat Med 2008; 21: 267-273. [DOI:10.1080/14767050801924118]
71. Bdolah Y, Palomaki GE, Yaron Y, Bdolah-Abram T, Goldman M, Levine RJ, et al. Circulating angiogenic proteins in trisomy 13. Am J Obstet Gynecol 2006; 194: 239-245. [DOI:10.1016/j.ajog.2005.06.031]
72. Foyouzi N, Norwitz E, Tsen L, Buhimschi C, Buhimschi I. Placental growth factor in the cerebrospinal fluid of women with preeclampsia. Int J Gynecol Obstet 2006; 92: 32-37. [DOI:10.1016/j.ijgo.2005.09.004]
73. Stepan H, Faber R, Dornhöfer N, Huppertz B, Robitzki A, Walther T. New insights into the biology of preeclampsia. Biol Reprod 2006; 74: 772-776. [DOI:10.1095/biolreprod.105.045997]
74. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308: 1592-1594. [DOI:10.1126/science.1111726]
75. Krysiak O, Bretschneider A, Zhong E, Webb J, Hopp H, Verlohren S, et al. Soluble vascular endothelial growth factor receptor-1 (sFlt1 ) mediates downregulation of FLT1 and prevents activated neutrophils from women with preeclampsia from additional migration by VEGF. Circul Res 2005; 97: 1253-1261. [DOI:10.1161/01.RES.0000194324.29363.82]
76. Karumanchi S, Epstein F. Placental ischemia and soluble fms-like tyrosine kinase 1: cause or consequence of preeclampsia? Kidney Int 2007; 71: 959-961. [DOI:10.1038/sj.ki.5002281]
77. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonat Med 2008; 21: 9-23. [DOI:10.1080/14767050701830480]
78. Haggerty CL, Seifert ME, Tang G, Olsen J, Bass DC, Ananth Karumanchi S, et al. Second trimester anti-angiogenic proteins and preeclampsia. Pregnancy Hypertens 2012; 2: 158-163. [DOI:10.1016/j.preghy.2012.01.005]
79. Staff AC, Braekke K, Harsem NK, Lyberg T, Holthe MR. Circulating concentrations of sFlt1 (soluble fms-like tyrosine kinase 1) in fetal and maternal serum during pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 2005; 122: 33-39. [DOI:10.1016/j.ejogrb.2004.11.015]
80. Huckle WR, Roche RI. Post‐transcriptional control of expression of sFlt‐1, an endogenous inhibitor of vascular endothelial growth factor. J Cell Biochem 2004; 93: 120-132. [DOI:10.1002/jcb.20142]
81. Nevo O, Lee DK, Caniggia I. Attenuation of VEGFR-2 Expression by sFlt1 and Low Oxygen in Human Placenta. Plos One 2013; 8: e81176. [DOI:10.1371/journal.pone.0081176]
82. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Nat Acad Sci 1993; 90: 10705-10709. [DOI:10.1073/pnas.90.22.10705]
83. Kar M. Role of Biomarkers in Early Detection of Preeclampsia. J Clin Diagn Res 2014; 8: BE01-BE04. [DOI:10.7860/JCDR/2014/7969.4261]
84. Verlohren S, Galindo A, Schlembach D, Zeisler H, Herraiz I, Moertl MG, et al. An automated method for the determination of the sFlt1 /PIGF ratio in the assessment of preeclampsia. Am J Obstet Gynecol 2010; 202: 161. [DOI:10.1016/j.ajog.2009.09.016]
85. Groten T, Gebhard N, Kreienberg R, Schleussner E, Reister F, Huppertz B. Differential expression of VE-cadherin and VEGFR-2 in placental syncytiotrophoblast during preeclampsia- New perspectives to explain the pathophysiology. Placenta 2010; 31: 339-343. [DOI:10.1016/j.placenta.2010.01.014]
86. Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, Goncalves L, et al. Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonat Med 2008; 21: 41-52. [DOI:10.1080/14767050701831397]
87. Dommisse J, Tiltman A. Placental bed biopsies in placental abruption. BJOG 1992; 99: 651-654. [DOI:10.1111/j.1471-0528.1992.tb13848.x]
88. Venkatesha S, Toporsian M, Lam C, Hanai J-i, Mammoto T, Kim YM, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nature Med 2006; 12: 642-649. [DOI:10.1038/nm1429]
89. Spencer K, Cowans NJ, Nicolaides KH. Low levels of maternal serum PAPP‐A in the first trimester and the risk of pre‐eclampsia. Prenat Diagn 2008; 28: 7-10. [DOI:10.1002/pd.1890]
90. Marik PE. Hypertensive disorders of pregnancy. Postgrad Med 2009; 121: 69-76. [DOI:10.3810/pgm.2009.03.1978]
91. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. New Engl J Med 2006; 355: 992-1005. [DOI:10.1056/NEJMoa055352]
92. Jauniaux E, Poston L, Burton GJ. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum Reprod Update 2006; 12: 747-755. [DOI:10.1093/humupd/dml016]
93. Hung T-H, Skepper JN, Charnock-Jones DS, Burton GJ. Hypoxia-Reoxygenation A Potent Inducer of Apoptotic Changes in the Human Placenta and Possible Etiological Factor in Preeclampsia. Circul Res 2002; 90: 1274-1281. [DOI:10.1161/01.RES.0000024411.22110.AA]
94. Demir R, Seval Y, Huppertz B. Vasculogenesis and angiogenesis in the early human placenta. Acta Histochem 2007; 109: 257-265. [DOI:10.1016/j.acthis.2007.02.008]
95. Chafetz I, Kuhnreich I, Sammar M, Tal Y, Gibor Y, Meiri H, et al. First-trimester placental protein 13 screening for preeclampsia and intrauterine growth restriction. Am J Obstet Gynecol 2007; 197: 35. [DOI:10.1016/j.ajog.2007.02.025]
96. Barton JR, Sibai BM. Prediction and prevention of recurrent preeclampsia. Obstet Gynecol 2008; 112: 359-372. [DOI:10.1097/AOG.0b013e3181801d56]
97. Tsatsaris V, Goffin F, Munaut C, Brichant J-F, Pignon M-R, Noel A, et al. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 2003; 88: 5555-5563. [DOI:10.1210/jc.2003-030528]
98. Torry DS, Wang H-S, Wang T-H, Caudle MR, Torry RJ. Preeclampsia is associated with reduced serum levels of placenta growth factor. Am J Obstet Gynecol 1998; 179: 1539-1544. [DOI:10.1016/S0002-9378(98)70021-3]
99. Tjoa ML, van Vugt JM, Mulders MA, Schutgens RB, Oudejans C, van Wijk IJ. Plasma placenta growth factor levels in midtrimester pregnancies. Obstet Gynecol 2001; 98: 600-607.
100. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. American journal of obstetrics and gynecology. 2003;188:177-182. [DOI:10.1067/mob.2003.111]
101. Reuvekamp A, Velsing‐Aarts FV, Poulina IE, Capello JJ, Duits AJ. Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre‐eclampsia. BJOG 1999; 106: 1019-1022. [DOI:10.1111/j.1471-0528.1999.tb08107.x]
102. Livingston JC, Haddad B, Gorski LA, Neblett P, Ahokas RA, Ramseya R, et al. Placenta growth factor is not an early marker for the development of severe preeclampsia. Am J Obstet Gynecol 2001; 184: 1218-1220. [DOI:10.1067/mob.2001.113877]
103. Livingston JC, Chin R, Haddad B, McKinney ET, Ahokas R, Sibai BM. Reductions of vascular endothelial growth factor and placental growth factor concentrations in severe preeclampsia. Am J Obstet Gynecol 2000; 183: 1554-1557. [DOI:10.1067/mob.2000.108022]
104. Kim S-Y, Ryu H-M, Yang J-H, Kim M-Y, Han J-Y, Kim J-O, et al. Increased sFlt1 to PlGF ratio in women who subsequently develop preeclampsia. J Korean Med Sci 2007; 22: 873-877. [DOI:10.3346/jkms.2007.22.5.873]
105. Levine RJ, Thadhani R, Qian C, Lam C, Lim K-H, Kai FY, et al. Urinary placental growth factor and risk of preeclampsia. JAMA 2005; 293: 77-85. [DOI:10.1001/jama.293.1.77]
106. Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic JP, et al. 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 Neonat Med 2008; 21: 279-287. [DOI:10.1080/14767050802034545]
107. Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, et al. A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia. J Matern Fetal Neonat Med 2009; 22: 1021-1038. [DOI:10.3109/14767050902994754]
108. Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, et al. First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 2004; 89: 770-775. [DOI:10.1210/jc.2003-031244]
109. Lim JH, Kim SY, Park SY, Yang JH, Kim MY, Ryu HM. Effective prediction of preeclampsia by a combined ratio of angiogenesis-related factors. Obstet Gynecol 2008; 111: 1403-1409. [DOI:10.1097/AOG.0b013e3181719b7a]
110. Stepan H, Unversucht A, Wessel N, Faber R. Predictive value of maternal angiogenic factors in second trimester pregnancies with abnormal uterine perfusion. Hypertension 2007; 49: 818-824. [DOI:10.1161/01.HYP.0000258404.21552.a3]
111. Crispi F, Llurba E, Dominguez C, Martín‐Gallán P, Cabero L, Gratacos E. Predictive value of angiogenic factors and uterine artery Doppler for early‐versus late‐onset pre‐eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 2008; 31: 303-309. [DOI:10.1002/uog.5184]
112. Sunderji S, Gaziano E, Wothe D, Rogers LC, Sibai B, Karumanchi SA, et al. Automated assays for sVEGF R1 and PlGF as an aid in the diagnosis of preterm preeclampsia: a prospective clinical study. Am J Obstet Gynecol 2010; 202: 40. [DOI:10.1016/j.ajog.2009.07.025]
113. De Vivo A, Baviera G, Giordano D, Todarello G, Corrado F, D'anna R. Endoglin, PlGF and sFlt‐1 as markers for predicting pre‐eclampsia. Acta Obstet Gynecol Scand 2008; 87: 837-842. [DOI:10.1080/00016340802253759]
114. Ohkuchi A, Hirashima C, Suzuki H, Takahashi K, Yoshida M, Matsubara S, et al. Evaluation of a new and automated electrochemiluminescence immunoassay for plasma sFlt1 and PlGF levels in women with preeclampsia. Hypertens Res 2010; 33: 422-427. [DOI:10.1038/hr.2010.15]
115. Unal ER, Robinson CJ, Johnson DD, Chang EY. Second-trimester angiogenic factors as biomarkers for future-onset preeclampsia. Am J Obstet Gynecol 2007; 197: 211. [DOI:10.1016/j.ajog.2007.05.022]
116. Lehnen H, Mosblech N, Reineke T, Puchooa A, Menke-Möllers I, Zechner U, et al. Prenatal clinical assessment of sFlt1 (soluble fms-like tyrosine kinase-1)/PlGF (placental growth factor) ratio as a diagnostic tool for preeclampsia, pregnancy-induced hypertension, and proteinuria. Geburtshilfe Frauenheilkund 2013; 73: 440. [DOI:10.1055/s-0032-1328601]
117. Lapaire O, Shennan A, Stepan H. The preeclampsia biomarkers soluble fms-like tyrosine kinase-1 and placental growth factor: current knowledge, clinical implications and future application. Eur J Obstet Gynecol Reprod Biol 2010; 151: 122-129. [DOI:10.1016/j.ejogrb.2010.04.009]
118. Diab AE, El-Behery MM, Ebrahiem MA, Shehata AE. Angiogenic factors for the prediction of pre-eclampsia in women with abnormal midtrimester uterine artery Doppler velocimetry. Int J Gynecol Obstet 2008; 102: 146-151. [DOI:10.1016/j.ijgo.2008.02.016]
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