Placenta-derived angiogenic proteins and their contribution to the pathogenesis of preeclampsia

Angiogenesis

Volumn 18, Issue 2, 2015, Pages 115-123

  Pratt, Anita ^a,b   Da Silva Costa, Fabricio ^a,b   Borg, Anthony J ^a,b   Kalionis, Bill ^a,b   Keogh, Rosemary ^a,b   Murthi, Padma ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ROYAL WOMEN'S HOSPITAL   (Australia)

Author keywords

Placenta; Spiral artery remodelling; Trophoblasts; Vascular endothelial factor

Indexed keywords

ACETYLSALICYLIC ACID; ANGIOGENIC FACTOR; ANGIOGENIC PROTEIN; ANGIOPOIETIN 1; ANGIOPOIETIN 2; ENDOGLIN; GELATINASE B; INTERCELLULAR ADHESION MOLECULE 1; PLACENTA DERIVED ANGIOGENIC PROTEIN; PLACENTAL GROWTH FACTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; SOLUBLE ENDOGLIN; TIE RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; CARDIOVASCULAR DISEASE; CELL DISRUPTION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CEREBROVASCULAR ACCIDENT; CLINICAL FEATURE; DISEASE ASSOCIATION; DISEASE MARKER; DOPPLER ECHOGRAPHY; EARLY DIAGNOSIS; EARLY INTERVENTION; ECLAMPSIA; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX REMODELLING; HIGH RISK POPULATION; HUMAN; INTRAUTERINE GROWTH RETARDATION; MATERNAL RISK FACTOR; MOLECULAR DYNAMICS; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PATIENT MONITORING; PLACENTA DEVELOPMENT; PLACENTAL ANGIOGENESIS; PREDICTIVE VALUE; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; RISK ASSESSMENT; RISK FACTOR; TROPHOBLAST; VASCULAR RESISTANCE; FEMALE; PHYSIOLOGY; PLACENTA; PRE-ECLAMPSIA; PREGNANCY;

ANGIOGENIC PROTEINS; FEMALE; HUMANS; PLACENTA; PRE-ECLAMPSIA; PREGNANCY;

EID: 84925506401     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-014-9452-3     Document Type: Review

References (80)

1. Aaserud M, Lewin S, Innvaer S, Paulsen E, Dahlgren A, Trommald M, Duley L, Zwarenstein M, Oxman A (2005) Translating research into policy and practice in developing countries: a case study of magnesium sulphate for pre-eclampsia. BMC Health Serv Res 5:68
2. Athanassiades A, Hamilton G, Lala P (1998) Vascular endothelial growth factor stimulates proliferation but not migration or invasiveness in human extravillous trophoblast. Biol Reprod 59(3):643–654
3. Austgulen R, Lien E, Vince G, Redman C (1997) Increased maternal plasma levels of soluble adhesion molecules (ICAM-1, VCAM-1, E-selectin) in pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 71(1):53–58
4. Bauer S, Pollheimer J, Hartmann P, Husslein J, Aplin D, Knofler M (2004) Tumor necrosis factor alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first trimester villous explant cultures. J Clin Endocrinol Metab 89:903–8
5. Bellamy L, Casas J, Hingorani A, Williams D (2007) Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ 335(7627):974
6. Brosens I, Robertson WB, Dixon HG (1967) The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 2:569–79
7. Brosens I, Robertson W, Dixon H (1972) The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1:177–191
8. Brown MC, Best KE, Pearce MS, Waugh J, Robson SC, Bell R (2013) Cardiovascular disease risk in women with pre-eclampsia: systematic review and meta-analysis. Eur J Epidemiol 28(1):1–19
9. Bujold E, Morency A, Roberge S, Lacasse Y, Forest J, Gigeure Y (2009) Acetylsalicylic acid for the prevention of preeclampsia and intra-uterine growth restriction in women with abnormal uterine artery Doppler: a systematic review and meta-analysis. J Obstet Gynecol Can 31(9):818–826
10. Chien P, Arnott N, Gordon A, Owen P, Khan K (2000) How useful is uterine artery Doppler flow velocimetry in the prediction of pre-eclampsia, intrauterine growth retardation and perinatal death? An overview. BJOG 107(2):196–208
11. Chaiworapongsa T, Romero R, Savasan ZA, Kusanovic JP, Ogge G, Soto E et al (2011) Maternal plasma concentrations of angiogenic/antiangiogenic 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
12. Cross J, Werb Z, Fisher S (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266(5190):1508–1518
13. Dijke P, Goumans M, Pardali E (2008) Endoglin in angiogenesis and vascular diseases. Angiogenesis 11(1):79–89
14. Duley L (2009) The global impact of pre-eclampsia and eclampsia. Semin Perinatol 33(3):130–137
15. 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
16. Geva E, Jaffe R (2000) Role of vascular endothelial growth factor in ovarian physiology and pathology. Fertil Steril 74(3):429–438
17. Goksu A, Nazli M, Elis Yildiz S (2012) Significance of platelet endothelial cell adhesion molecule-1 (PECAM-1) and intercellular adhesion molecule-1 (ICAM-1) expressions in preeclamptic placentae. Endocrine 42(1):125–131
18. Goldenberg R, Culhane J, Iams J, Romero R (2008) Epidemiology and causes of preterm birth. The Lancet 371(9606):75–84
19. Gude N, Roberts C, Kalionis B, King R (2004) Growth and function of the normal human placenta. Thromb Res 114(5–6):397–407
20. Harrington KF, Campbell S, Bewley S, Bower S (1991) Doppler velocimetry studies of the uterine artery in the early prediction of pre-eclampsia and intra-uterine growth retardation. Eur J Obstet Gynecol Reprod Biol 42(Suppl.):S14–S20
21. Hoeben A, Landuyt B, Highley M, Wildiers H, Van Oosterom A, De Bruijn E (2004) Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 56(4):549–580
22. Irving R, Belton N, Elton R, Walker B (2000) Adult cardiovascular risk factors in premature babies. The Lancet 355(9221):2135–2136
23. Kumasawa K, Ikawa M, Kidoya H, Hasuwa H, Saito-Fujita T, Morioka Y, Takakura N, Kimura T, Okabe M (2011) Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc Natl Acad Sci USA 108(4):1451–1455
24. Kim YM, Hwang S, Kim Y, Pyun B, Kim T, Lee S, Gho Y, Kwon Y (2002) Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J Biol Chem 277(31):27872–27879
25. Laskowska M, Laskowska K, Leszczynsak-Gorzelak B, Oleszczuk J (2002) Maternal and umbilical sTNFR-1 in preeclamptic pregnancies with intrauterine normal and intrauterine growth retarded fetus. Hypertens pregnancy 26(1):13–21
26. Leal A, Poon L, Frivosa V, Veduta A, Nicolaides K (2009) First trimester maternal serum tumour necrosis factor receptor-1 and pre-eclampsia. Ultrasound Obstet Gynecol 33:135–141
27. Levine R, Lam C, Qian C, Yu K, Maynard S, Sachs B, Sibai B, Epstein F, Romero R, Thadhani R, Karumanchi S (2006) Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 355(10):992–1005
28. Linzer D, Fisher S (1999) The placenta and the prolactin family of hormones: regulation of the physiology of pregnancy. Mol Endocrinol 13:837–840
29. Lockwood C, Oner C, Uz Y, Kayisli U, Huang S, Buchwalkder L, Murk W, Funai E, Schatz F (2008) Matrix metalloproteinase 9 (MMP9) expression in pre-eclamptic decidua and MMP9 induction by tumor necrosis factor alpha and interleukin 1 beta in human first trimester decidual cells. Biol Reprod 78(6):1064–1072
30. Lykke JA, Langhoff-Roos J, Sibai BM, Funai EF, Triche EW, Paidas MJ (2009) Hypertensive pregnancy disorders and subsequent cardiovascular morbidity and type 2 diabetes mellitus in the mother. Hypertension 53:944–951
31. Madazli R, Benian A, Ilvan S, Calay Z (2006) Placental apoptosis and adhesion molecules expression in the placenta and the maternal placental bed of pregnancies complicated by fetal growth restriction with and without pre-eclampsia. J Obstet Gynaecol 26(1):5–10
32. Maisonpierre P, Suri C, Jones P, Bartunkova S, Wiegand S, Radziejewski C, Compton D (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277(5322):55–60
33. Maynard S, Epstein F, Karumanchi S (2008) Preeclampsia and angiogenic imbalance. Annu Rev Med 59:61–78
34. Maynard S, Min J, Lim K, Li J, Mondal S, Libermann T, Morgan J, Sellke F, Stillman I, Epstein F, Sukhatme V, Karumanchi S (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111(5):649–658
35. Milner C, Hansen T, Singh H, Brindle N (2009) Roles of the receptor tyrosine kinases Tie-1 and Tie-2 in mediating the effects of angiopoietin-1 on endothelial permeability and apoptosis. Microvasc Res 77:187–191
36. Mutter W, Karumanchi S (2008). Molecular mechanisms of preeclampsia. Microvasc Res 75(1):1–8
37. Nisell H, Lintu H, Lunell N, Mollerstrom G, Pettersson E (1995) Blood pressure and renal function seven years after pregnancy complicated by hypertension. Br J Obstet Gynaecol 102(11):876–881
38. Noori M, Donald AE, Angelakopoulou A, Hingorani AD, Williams DJ (2010) Prospective study of placental angiogenic factors and maternal vascular function before and after preeclampsia and gestational hypertension. Circulation 122(5):478–487
39. Okada Y, Ueshin Y, Isotani A, Saito-Fujita T, Nakashima H, Kimura K, Mizoguchi A, Oh-Hora M, Mori Y, Ogata M, Oshima RG, Okabe M, Ikawa M (2007) Complementation of placental defects and embryonic lethality by trophoblast-specific lentiviral gene transfer. Nat Biotechnol 25(2):233–237
40. Parra M, Rodrigo R, Barja P, Bosco C, Fernández V, Muñoz H, Soto-Chacón E (2005) Screening test for preeclampsia through assessment of uteroplacental blood flow and biochemical markers of oxidative stress and endothelial dysfunction. Am J Obstet Gynecol 193:1486–1491
41. Papageorghiou AT, Yu CK, Cicero S, Bower S, Nicolaides KH (2002) Second-trimester uterine artery Doppler screening in unselected populations: a review. J Matern Fetal Neonatal Med 12:78–88
42. Pijnenborg R, Dixon G, Robertson W, Brosens I (1980) Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1(1):3–19
43. Pollheimer J, Bauer S, Huber A, Husslein P, Aplin J, Knofler M (2004) Expression patterns of collagen XVIII and its cleavage product, the angiogenesis inhibitor endostatin, at the fetal–maternal interface. Placenta 25:770–779
44. Pollheimer J, Haslinger P, Fock V, Prast J, Saleh L, Biadasiewicz K, Jetne-Delmann R, Haraldsen G, Haider S, Hirtenlehner-Ferber K, Knofler M (2011) Endostatin suppresses IGF-II-mediated signaling and invasion of human extravillous trophoblasts. Endocrinology 152(11):4431–4442
45. Poon LC, Kametas NA, Maiz N, Akolekar R, Nicolaides KH (2011) First-trimester prediction of hypertensive disorders in pregnancy. Hypertension 53:812–818
46. Poon IK, Patel KK, Davis DS, Parish CR, Hulett MD (2011). Histidine-rich glycoprotein: the swiss army knife of mammalian plasma. Blood 117(7):2093–101
47. Powe CE, Levine RJ, Karumanchi SA (2011) Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 123(24):2856–2869
48. Qin L, Xiyun Y, Yang L, Ying Z, Xingang Z, Yi S (2003) Pre-eclampsia is associated with the failure of melanoma cell adhesion molecule (MCAM/CD146) expression by intermediate trophoblast. Laboratory Investigation 84(2):221–8
49. Ray JG, Vermeulen MJ, Schull MJ, Redelmeier DA (2005) Cardiovascular Health After Maternal Placental Syndromes (CHAMPS): population-based retrospective cohort study. The Lancet 366:1797–1803
50. Reith A, Booth N, Moore N, Cruickshank D, Bennett B (1993) Plasminogen activator inhibitors (PAI-1 and PAI-2) in normal pregnancies, pre-eclampsia and hyatidiform mole. Br J Obstet Gynaecol 100(4):370–374
51. Roberge S, Demers S, Bujold E (2013) Initiation of aspirin in early gestation for the prevention of pre-eclampsia. BJOG 120(6):773–774
52. Roberts J, Cooper D (2001) Pathogenesis and genetics of pre-eclampsia. The Lancet 357:53–56
53. Roberts J, Taylor R, Musci T, Rodgers G, Hubel C, McLaughlin M (1989) Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 161(5):1200–1204
54. Romero R, Nien J, Espinoza J, Todem D, Fu W, Chung H, Karumanchi S (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. Journal of Maternal-Fetal and Neonatal Medicine 21(1):9–23
55. Romo A, Carceller R, Tobajas J (2009) Intrauterine growth retardation (IUGR): epidemiology and etiology. Pediatr Endocrinol Rev 6(3):332–336
56. Said J, Dekker G (2003) Pre-eclampsia and thrombophilia. Best Pract Res Clin Obstet Gynaecol 17(3):441–458
57. Schlembach D, Wallner W, Sengenberger R, Stiegler E, Mortl M, Beckmann MW, Lang U (2007) Angiogenic growth factor levels in maternal and fetal blood: correlation with Doppler ultrasound parameters in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 29:407–413
58. Shibuya M, Claesson-Welsh L (2006) Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res 312:549–560
59. Shin S, Lee SH, Park S, Kang SM, Chung N, Shim WH, Cho SY, Manabe I, Jang Y (2010) Soluble fms-like tyrosine kinase-1 and the progression of carotid intima-media thickness: 24-month follow-up study. Circ J 74:2211–2215
60. 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(9):809–815
61. Sibai B (2003) Diagnosis and management of gestational hypertension and preeclampsia. Obstet Gynecol 102(1):181–192
62. Sibai B, Dekker G, Kupferminc M (2005) Pre-eclampsia. The Lancet 365(9461):785–799
63. Sibai B, Ewell M, Levine R, Klebanoff M, Exterlitz J, Catalano P, Goldenberg R, Joffe G (1997) Risk factors associated with preeclampsia in healthy nulliparous women. Am J Obstet Gynecol 177(5):1003–1010
64. Smith G, Pell J, Walsh D (2001) Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129 290 births. The Lancet 357(9273):2002–2006
65. Soker S, Takashima S, Miao H, Neufeld G, Klagsbrun M (1998) Neuropillin-1 is expressed by endothelial and tumour cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92:725–745
66. Spencer K, Yu CKH, Savvidou M, Papageorghiou AT, Nicolaides KH (2006) Prediction of pre-eclampsia by uterine artery Doppler ultrasonography and maternal serum pregnancy-associated plasma protein-A, free β-human chorionic gonadotropin, activin A and inhibin A at 22 + 0 to 24 + 6 weeks’ gestation. Ultrasound Obstet Gynecol 27:658–663
67. St-Jacques S, Forte M, Lye S, Letarte M (1994) Localization of endoglin, a transforming growth factor-beta binding protein, and of CD44 and integrins in placenta during the first trimester of pregnancy. Biol Reprod 51(3):405–413
68. Stepan H, Unversucht A, Wessel N, Faber R (2007) Predictive value of maternal angiogenic factors in second trimester pregnancies with abnormal uterine perfusion. Hypertension 49:818–824
69. Stepan H, Geipel A, Schwarz F, Kramer T, Wessel N, Faber R (2008) Circulatory soluble endoglin and its predictive value for preeclampsia in second-trimester pregnancies with abnormal uterine perfusion. Am J Obstet Gynecol 198(175):e1–e6
70. Thadhani R, Kisner T, Hagmann H, Bossung V, Noack S, Schaarschmidt W, Jank A, Kribs A, Cornely OA, Kreyssig C, Hemphill L, Rigby AC, Khedkar S, Lindner TH, Mallmann P, Stepan H, Karumanchi SA, Benzing T (2011) Pilot study of extracorporeal removal of soluble fms-like tyrosine kinase 1 in preeclampsia. Circulation 124(8):940–950
71. Tziotis J, Malamitsi-Puchner A, Vlachos G, Creatsas G, Michalas S (2002) Adhesion molecule expression in the placental bed of pregnancies with pre-eclampsia. BJOG 109(2):197–201
72. Van Wiijk M, Kublickiene K, Boer K, VanBavel E (2000) Vascular function in preeclampsia. Cardiovasc Res 47(1):38–48
73. Venkatesha S, Toporsian M, Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim Y, Bdolah Y, Lim K, Yuan H, Libermann T, Stillman I, Roberts D, D’Amore P, Epstein F, Sellke F, Romero R, Sukhatme V, Letarte M, Karumanchi S (2006) Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 12(6):642–649
74. Verlohren S, Herraiz I, Lapaire O, Schlembach D, Moertl M, Zeisler H et al (2012) The sFlt-1/PlGF ratio in different types of hypertensive pregnancy disorders and its prognostic potential in preeclamptic patients. Am J Obstet Gynecol 206(58):e1–e8
75. Wang Y, Walsh S (1996) TNF alpha concentrations and mRNA expression are increased in preeclamptic placentas. J Reprod Immunol 32:157–169
76. Wathen K, Ylikorkala O, Andersson S, Alfthan H, Stenman U, Vuorela P (2009) Maternal serum endostatin at gestational weeks 16–20 is elevated in subsequent pre-eclampsia but not in intrauterine growth retardation. Acta Obstet Gynecol Scand 88(5):593–598
77. Wilson B, Watson M, Prescott G, Sunderland S, Campbell D, Hannaford P, Smith W (2003) Hypertensive diseases of pregnancy and risk of hypertension and stroke in later life: results from cohort study. BMJ 326(7394):845
78. Zhang J, Zeisler J, Hatch M, Berkowitz G (1997) Epidemiology of pregnancy-induced hypertension. Epidemiol Rev 19(2):218–232
79. Zhou Y, Damsky C, Fischer S (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(9):2152–2164
80. Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, Alitallo K, Damsky C, Fisher S (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(4):1405–1423