Transcriptionally active syncytial aggregates in the maternal circulation may contribute to circulating soluble fms-like tyrosine kinase 1 in preeclampsia

Hypertension

Volumn 59, Issue 2, 2012, Pages 256-264

  Rajakumar, Augustine ^a,b   Cerdeira, Ana Sofia ^a,c   Rana, Sarosh ^a   Zsengeller, Zsuzsanna ^a   Edmunds, Lia ^d   Jeyabalan, Arun ^d,e   Hubel, Carl A ^d,e   Stillman, Isaac E ^a   Parikh, Samir M ^a   Ananth Karumanchi, S ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Gulbenkian Programme for Advanced Medical Education   (Portugal)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Microparticles; Preeclampsia; SFlt1; Soluble VEGFR1; Syncytial aggregates; Syncytial knots

Indexed keywords

FMS LIKE TYROSINE KINASE 1; MESSENGER RNA; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FEMALE; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; PLACENTA; PLASMA; PREECLAMPSIA; PRIORITY JOURNAL; SYNCYTIOTROPHOBLAST; THIRD TRIMESTER PREGNANCY;

CELL-DERIVED MICROPARTICLES; CELLS, CULTURED; FEMALE; HUMANS; ORGAN CULTURE TECHNIQUES; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATIONS, HEMATOLOGIC; PREGNANCY PROTEINS; PREGNANCY TRIMESTER, THIRD; RNA, MESSENGER; TROPHOBLASTS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84856304025     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.111.182170     Document Type: Article

References (43)

1. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005;308:1592-1594. (Pubitemid 40807500)
2. Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet. 2005;365:785-799. (Pubitemid 40311367)
3. Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res. 2004;95:884-891. (Pubitemid 39435003)
4. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Goncalves LF, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Am J Obstet Gynecol. 2004;190:1541-1547.
5. 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. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004;350:672-683. (Pubitemid 38364626)
6. 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. 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. (Pubitemid 36278583)
7. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, Mazor M. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med. 2005;17:3-18. (Pubitemid 40515938)
8. Bergmann A, Ahmad S, Cudmore M, Gruber AD, Wittschen P, Lindenmaier W, Christofori G, Gross V, Gonzalves A, Grone HJ, Ahmed A, Weich HA. Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a mouse model. J Cell Mol Med. 2010;14:1857-1867.
9. Lu F, Longo M, Tamayo E, Maner W, Al-Hendy A, Anderson GD, Hankins GD, Saade GR. The effect of over-expression of sFlt-1 on blood pressure and the occurrence of other manifestations of preeclampsia in unrestrained conscious pregnant mice. Am J Obstet Gynecol. 2007;196:396e1-396e7.
10. Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation. 2011;123:2856-2869.
11. Bujold E, Romero R, Chaiworapongsa T, Kim YM, Kim GJ, Kim MR, Espinoza J, Goncalves LF, Edwin S, Mazor M. Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin. J Matern Fetal Neonatal Med. 2005;18:9-16. (Pubitemid 41224357)
12. Holash J, Davis S, Papadopoulos N, Croll SD, Ho L, Russell M, Boland P, Leidich R, Hylton D, Burova E, Ioffe E, Huang T, Radziejewski C, Bailey K, Fandl JP, Daly T, Wiegand SJ, Yancopoulos GD, Rudge JS. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci USA. 2002;99:11393-11398. (Pubitemid 34920936)
13. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci USA. 1993;90:10705-10709. (Pubitemid 23347111)
14. Park M, Lee ST. The fourth immunoglobulin-like loop in the extracellular domain of FLT-1, a VEGF receptor, includes a major heparin-binding site. Biochem Biophys Res Commun. 1999;264:730-734.
15. Sela S, Itin A, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Yagel S, Keshet E. 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. 2008;102:1566-1574.
16. Sela S, Natanson-Yaron S, Zcharia E, Vlodavsky I, Yagel S, Keshet E. Local retention versus systemic release of soluble VEGF receptor-1 are mediated by heparin-binding and regulated by heparanase. Circ Res. 2011;108:1063-1070.
17. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, Zamudio S, Caniggia I. Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1085-R1093. (Pubitemid 44498450)
18. Redman CW, Sargent IL. Circulating microparticles in normal pregnancy and pre-eclampsia. Placenta. 2008;29(suppl A): S73-S77.
19. Askelund KJ, Chamley LW. Trophoblast deportation part I: Review of the evidence demonstrating trophoblast shedding and deportation during human pregnancy. Placenta. 2011;32:716-723.
20. National Institutes of Health. Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. Am J Obstet Gynecol. 2000;183:S1-S22.
21. Silasi M, Rana S, Powe C, Cohen B, Lim KH, Zsengeller ZK, Karumanchi SA, Stillman IE. Placental expression of angiogenic factors in Trisomy 13. Am J Obstet Gynecol. 2011;204:546.
22. Rajakumar A, Michael HM, Rajakumar PA, Shibata E, Hubel CA, Karumanchi SA, Thadhani R, Wolf M, Harger G, Markovic N. 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. 2005;26:563-573. (Pubitemid 40916309)
23. Rajakumar A, Doty K, Daftary A, Harger G, Conrad KP. Impaired oxygen-dependent reduction of HIF-1α and-2α proteins in pre-eclamptic placentae. Placenta. 2003;24:199-208. (Pubitemid 37184716)
24. Abumaree MH, Stone PR, Chamley LW. An in vitro model of human placental trophoblast deportation/shedding. Mol Hum Reprod. 2006;12:687-694. (Pubitemid 44605601)
25. Rajakumar A, Powers RW, Hubel CA, Shibata E, von Versen-Hoynck F, Plymire D, Jeyabalan A. Novel soluble Flt-1 isoforms in plasma and cultured placental explants from normotensive pregnant and preeclamptic women. Placenta. 2009;30:25-34.
26. Kuo CJ, Farnebo F, Yu EY, Christofferson R, Swearingen RA, Carter R, von Recum HA, Yuan J, Kamihara J, Flynn E, D'Amato R, Folkman J, Mulligan RC. Comparative evaluation of the antitumor activity of antiangiogenic proteins delivered by gene transfer. Proc Natl Acad Sci U S A. 2001;98:4605-4610. (Pubitemid 32295023)
27. Redman CW, Sargent IL. Placental debris, oxidative stress and preeclampsia. Placenta. 2000;21:597-602.
28. Aharon A, Brenner B. Microparticles and pregnancy complications. Thromb Res. 2011;127(suppl 3): S67-S71.
29. Germain SJ, Sacks GP, Sooranna SR, Sargent IL, Redman CW. Systemic inflammatory priming in normal pregnancy and preeclampsia: the role of circulating syncytiotrophoblast microparticles. J Immunol. 2007;178:5949-5956. (Pubitemid 46674392)
30. Kumpel B, King MJ, Sooranna S, Jackson D, Eastlake J, Cheng R, Johnson M. Phenotype and mRNA expression of syncytiotrophoblast microparticles isolated from human placenta. Ann N Y Acad Sci. 2008;1137:144-147.
31. Than NG, Abdul Rahman O, Magenheim R, Nagy B, Fule T, Hargitai B, Sammar M, Hupuczi P, Tarca AL, Szabo G, Kovalszky I, Meiri H, Sziller I, Rigo J Jr, Romero R, Papp Z. Placental protein 13 (galectin-13) has decreased placental expression but increased shedding and maternal serum concentrations in patients presenting with preterm pre-eclampsia and HELLP syndrome. Virchows Arch. 2008;453:387-400.
32. van der Post JA, Lok CA, Boer K, Sturk A, Sargent IL, Nieuwland R. The functions of microparticles in pre-eclampsia. Semin Thromb Hemost. 2011;37:146-152.
33. Burton GJ. Deportation of syncytial sprouts from the term human placenta. Placenta. 2011;32:96-98.
34. Chamley LW, Chen Q, Ding J, Stone PR, Abumaree M. Trophoblast deportation: just a waste disposal system or antigen sharing? J Reprod Immunol. 2011;88:99-105.
35. Guller S, Tang Z, Ma YY, Di Santo S, Sager R, Schneider H. Protein composition of microparticles shed from human placenta during placental perfusion: potential role in angiogenesis and fibrinolysis in preeclampsia. Placenta. 2011;32:63-69.
36. Huppertz B. IFPA Award in Placentology Lecture: biology of the placental syncytiotrophoblast-myths and facts. Placenta. 2010;31(suppl): S75-S81.
37. Guller S. Role of the syncytium in placenta-mediated complications of preeclampsia. Thromb Res. 2009;124:389-392.
38. Redman CW, Sargent IL. Pre-eclampsia, the placenta and the maternal systemic inflammatory response: a review. Placenta. 2003;24(suppl A): S21-S27. (Pubitemid 37184731)
39. Attwood HD, Park WW. Embolism to the lungs by trophoblast. J Obstet Gynaecol Br Commonw. 1961;68:611-617.
40. Johansen M, Redman CW, Wilkins T, Sargent IL. Trophoblast deportation in human pregnancy: its relevance for pre-eclampsia. Placenta. 1999;20:531-539. (Pubitemid 29391296)
41. Lapaire O, Holzgreve W, Oosterwijk JC, Brinkhaus R, Bianchi DW. Georg Schmorl on trophoblasts in the maternal circulation. Placenta. 2007;28:1-5. (Pubitemid 44767223)
42. Fox H. The significance of villous syncytial knots in the human placenta. J Obstet Gynaecol Br Commonw. 1965;72:347-355.
43. Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension. 2008;51:970-975. (Pubitemid 351398986)