Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin

References

• Romero R. Prenatal medicine: The child is the father of the man. Prenat Neonat Med 1996;1:8–11.
   Google Scholar
• Roberts JM. Pregnancy related hypertension. In: Creasy RK, Resnik R (editors). Maternal fetal medicine. Philadelphia: WB Saunders; 1998. pp 883–892.
   Google Scholar
• Dekker GA, Sibai BM. Etiology and pathogenesis of preeclampsia: current concepts. Am J Obstet Gynecol 1998;179:1359–1375.
   PubMed Web of Science ®Google Scholar
• Sibai BM. Diagnosis and management of gestational hyper-tension and preeclampsia. Obstet Gynecol 2003;102:181–192
   PubMed Web of Science ®Google Scholar
• Romero R, Lockwood C, Oyarzun E, Hobbins JC. Toxemia: New concepts in an old disease. Semin Perinatol 1988;12:302–323.
   PubMed Web of Science ®Google Scholar
• Brosens IA. Morphological changes in the utero-placental bed in pregnancy hypertension. Clin Obstet Gynaecol 1977;4: 573–593.
   PubMed Web of Science ®Google Scholar
• Conrad KP, Benyo DF. Placental cytokines and the patho-genesis of preeclampsia. Am J Reprod Immunol 1997;37:240–249.
   PubMed Web of Science ®Google Scholar
• Granger JP, Alexander BT, Llinas MT, et al. Pathophysiology of preeclampsia: Linking placental ischemia/hypoxia with microvascular dysfunction. Microcirculation 2002;9:147–160.
   PubMed Web of Science ®Google Scholar
• Myatt L. Role of placenta in preeclampsia. Endocrine 2002;19:103–111.
   PubMed Web of Science ®Google Scholar
• Huppertz B, Kadrov M, Black S, et al. Maternal anemia and preeclampsia display opposite invasive phenotype and reduced apoptosis of interstitial extravillous trophoblast. J Soc Gynecol Investig 2003;10:316A.
   Google Scholar
• Kaufmann P, Black S, Huppertz B. Endovascular trophoblast invasion: Implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 2003;69:1–7.
   Google Scholar
• Genbacev 0, DiFederico E, McMaster M, et al. Invasive cytotrophoblast apoptosis in pre-eclampsia. Hum Reprod 1999;14 (Suppl. 2): 59–66.
   Google Scholar
• Huppertz B, Frank HG, Reister F, et al. Apoptosis cascade progresses during turnover of human trophoblast: Analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest 1999;79:1687–1702.
   PubMed Web of Science ®Google Scholar
• DiFederico E, Genbacev 0, Fisher SJ. Preeclampsia is associated with widespread apoptosis of placental cytotropho-blasts within the uterine wall. Am J Pathol 1999;155:293–301.
   Google Scholar
• Leung DN, Smith SC, To KF, et al. Increased placental apoptosis in pregnancies complicated by preeclampsia. Am J Obstet Gynecol 2001;184:1249–1250.
   PubMed Web of Science ®Google Scholar
• Ishihara N, Matsuo H, Murakoshi H, et al. Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am J Obstet Gynecol 2002;186:158–166.
   PubMed Web of Science ®Google Scholar
• Neale D, Demasio K, Illuzi J, et al. Maternal serum of women with pre-eclampsia reduces trophoblast cell viability: evidence for an increased sensitivity to Fas-mediated apoptosis. J Matern Fetal Neonatal Med 2003;13:39–44.
   PubMedGoogle Scholar
• Huppertz B, Kingdom J, Caniggia I, et al. Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotro-phoblast into the maternal circulation. Placenta 2003;24:181–190
   PubMed Web of Science ®Google Scholar
• Roberts JM, Taylor RN, Musci TJ, et al. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 1989;161: 1200–1204.
   PubMed Web of Science ®Google Scholar
• Clark BA, Halvorson L, Sachs B, et al. Plasma endothelin levels in preeclampsia: elevation and correlation with uric acid levels and renal impairment. Am J Obstet Gynecol 1992; 166:962–968.
   PubMed Web of Science ®Google Scholar
• Taylor RN, de Groot CJ, Cho YK, et al. Circulating factors as markers and mediators of endothelial cell dysfunction in preeclampsia. Semin Reprod Endocrinol 1998;16:17–31.
   PubMedGoogle Scholar
• Sacks GP, Studena K, Sargent K, et al. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998;179:80–86.
   PubMed Web of Science ®Google Scholar
• Redman CW, Sacks GP, Sargent IL. Preeclampsia: An excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999;180:499–506.
   Google Scholar
• Redman CW, Sargent IL. Placental debris, oxidative stress and pre-eclampsia. Placenta 2000;21:597–602.
   PubMed Web of Science ®Google Scholar
• Gervasi MT, Chaiworapongsa T, Pacora P, et al. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001;185:792–797.
   PubMed Web of Science ®Google Scholar
• Redman CW, Sargent IL. The pathogenesis of pre-eclampsia. Gynecol Obstet Fertil 2001;29:518–522.
   PubMedGoogle Scholar
• Chua S, Wilkins T, Sargent I, et al. Trophoblast deportation in pre-eclamptic pregnancy. Br J Obstet Gynaecol 1991;98: 973–979.
   PubMedGoogle Scholar
• Cockell AP, Learmont JG, Smarason AK, et al. Human placental syncytiotrophoblast microvillous membranes impair maternal vascular endothelial function. Br J Obstet Gynaecol 1997;104:235–240.
   PubMedGoogle Scholar
• Johansen M, Redman CW, Wilkins T, et al. Trophoblast deportation in human pregnancy-its relevance for pre-eclampsia. Placenta 1999;20:531–539.
   PubMed Web of Science ®Google Scholar
• Knight M, Redman CW, Linton EA, et al. Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol 1998;105: 632–640.
   PubMedGoogle Scholar
• von Dadelszen P, Hurst G, Redman CW. Supernatants from co-cultured endothelial cells and syncytiotrophoblast micro-villous membranes activate peripheral blood leukocytes in vitro. Hum Reprod 1999;14:919–924.
   Google Scholar
• Williams J. Premature seperation of the normally implanted placenta. Surg Gynecol Obstet 1915;21:541–554.
   Google Scholar
• Elmer DB, Granai CO, Ball HG, et al. Persistence of gestational trophoblastic disease for longer than 1 year following evacuation of hydatidiform mole. Obstet Gynecol 1993;81:888–890.
   PubMed Web of Science ®Google Scholar
• Maynard SE, Min JY, Merchan J, 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.
   PubMed Web of Science ®Google Scholar
• Zhou Y, McMaster M, Woo K, et al. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclamp-sia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol 2002;160:1405–1423.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Bellingard V, Feng KT, et al. Human cytotropho-blasts promote endothelial survival and vascular remodeling through secretion of Ang2, P1GF, and VEGF-C. Dev Biol 2003;263:114–125.
   PubMed Web of Science ®Google Scholar
• Ahmed A, Perkins J. Angiogenesis and intrauterine growth restriction. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:981–998.
   PubMed Web of Science ®Google Scholar
• Charnock-Jones DS, Burton GJ. Placental vascular morpho-genesis. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:953–968.
   PubMed Web of Science ®Google Scholar
• Ong S, Lash G, Baker PN. Angiogenesis and placental growth in normal and compromised pregnancies. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:969–980.
   Google Scholar
• Torry DS, Mukherjea D, Arroyo J, et al. Expression and function of placenta growth factor: implications for abnormal placentation. J Soc Gynecol Investig 2003;10:178–188.
   PubMedGoogle Scholar
• Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669–676.
   Google Scholar
• Gerber HP, McMurtrey A, Kowalski J, et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal trans-duction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 1998;273:30336–3043.
   PubMed Web of Science ®Google Scholar
• Torry DS, Ahn H, Barnes EL, et al. Placenta growth factor: Potential role in pregnancy. Am J Reprod Immunol 1999;41:79–85.
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Romero R, Kim YM, Kin GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, et al. Plasma soluble vascular endothelial growth factor receptor-1 concentraton is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005;17(1):3–18.
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Espinoza J, Bujold E, 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; 190:41–47.
   Web of Science ®Google Scholar
• Koga K, Osuga Y, Yoshino 0, et al. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003;88: 2348–2351.
   Google Scholar
• Tsatsaris V, Goffin F, Munaut C, et al. Overexpression of the soluble vascular endothelial growth factor receptor in pre-eclamptic patients: Pathophysiological consequences. J Clin Endocrinol Metab 2003;88:5555–5563.
   PubMed Web of Science ®Google Scholar
• Schlembach D, Beinder E. Angiogenic factors in preeclamp-sia. J Soc Gynecol Investig 2003;10:316A.
   Google Scholar
• Clark DE, Smith SK, Sharkey AM, et al. Localization of VEGF and expression of its receptors tit and KDR in human placenta throughout pregnancy. Hum Reprod 1996;11:1090–1098.
   PubMed Web of Science ®Google Scholar
• Clark DE, Smith SK, He Y, et al. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998;59:1540–1548.
   PubMed Web of Science ®Google Scholar
• Sibai BM, Ewell M, Levine RJ, et al. Risk factors associated with preeclampsia in healthy nulliparous women. The Calcium for Preeclampsia Prevention (CPEP) Study Group. Am J Obstet Gynecol 1997;177:1003–1010.
   PubMed Web of Science ®Google Scholar
• Alexander GR, Himes JH, Kaufman RB, et al. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163–168.
   PubMed Web of Science ®Google Scholar
• Hunter C Jr, Howard WF. A pressor substance (hysterotonin) occurring in toxemia. Am J Obstet Gynecol 1960;79:838–846.
   PubMed Web of Science ®Google Scholar
• Page EW, Cox AJ. Renal chnages following toxaemias of late pregnancy. West J Surg 1983;46:463.
   Google Scholar
• Tatum HJ, Mule JG. The hypertensive action of blood from preeclampsia. Am J Obstet Gynecol 1962;83:1028–1034.
   PubMed Web of Science ®Google Scholar
• Pirani BB, MacGillivray I. The effect of plasma retransfusion on the blood pressure in the puerperium. Am J Obstet Gynecol 1975;121:221–226.
   PubMed Web of Science ®Google Scholar
• Gant NF, Daley GL, Chand S, et al. A study of angiotensin II pressor response throughout primigravid pregnancy. J Clin Invest 1973;52:2682–2689.
   PubMed Web of Science ®Google Scholar
• Gant NF, Chand S, Whalley PJ, et al. The nature of pressor responsiveness to angiotensin II in human pregnancy. Obstet Gynecol 1974;43:854.
   PubMed Web of Science ®Google Scholar
• Gant NF, Chand S, Worley RJ, et al. A clinical test useful for predicting the development of acute hypertension in preg-nancy. Am J Obstet Gynecol 1974;120:1–7.
   PubMed Web of Science ®Google Scholar
• Li C, Ansari R, Yu Z, et al. Definitive molecular evidence of renin-angiotensin system in human uterine decidual cells. Hypertension 2000;36:159–164.
   PubMed Web of Science ®Google Scholar
• Shah DM. Perinatal implications of maternal hypertension. Semin Pediatr Neurol 2001;8:108–119.
   PubMedGoogle Scholar
• Talledo DE, Chesley LC, Zuspan FP. Renin-angiotensin system in normal and toxemic pregnancies.III. Differential sensitivity to angiotensinogen II and norwpineprine in toxemia of pregnancy. Am J Obstet Gynecol 1968;100:218–221.
   Google Scholar
• Zuspan FP. Catecholamines. Their role in pregnancy and the development of pregnancy-induced hypertension. J Reprod Med 1979;23:143–150.
   Google Scholar
• Krege JH, Katz VL. A proposed relationship between vasopressinase altered vasopressin and preeclampsia. Med Hypotheses 1990;31:283–287.
   PubMed Web of Science ®Google Scholar
• McKinney ET, Shouri R, Hunt RS, et al. Plasma, urinary, and salivary 8-epi-prostaglandin f2alpha levels in normoten-sive and preeclamptic pregnancies. Am J Obstet Gynecol 2000;183:874–877.
   PubMed Web of Science ®Google Scholar
• Pedersen EB, Aalkjaer C, Christensen NJ, et al. Renin, angiotensin II, aldosterone, catecholamines, prostaglandins and vasopressin. The importance of pressor and depressor factors for hypertension in pregnancy. Scand J Chin Lab Invest Suppl 1984;169:48–56.
   PubMedGoogle Scholar
• Higgins JR, Walshe JJ, Darling MR, et al. Hemostasis in the uteroplacental and peripheral circulations in normotensive and pre-eclamptic pregnancies. Am J Obstet Gynecol 1998;179:520–526.
   PubMed Web of Science ®Google Scholar
• Higgins JR, Papayianni A, Brady HR, et al. Circulating vascular cell adhesion molecule-1 in pre-eclampsia, gesta-tional hypertension, and normal pregnancy: Evidence of selective dysregulation of vascular cell adhesion molecule-1 homeostasis in pre-eclampsia. Am J Obstet Gynecol 1998;179:464–469.
   PubMed Web of Science ®Google Scholar
• Mellembakken JR, Aukrust P, Olafsen MK, et al. Activation of leukocytes during the uteroplacental passage in preeclamp-sia. Hypertension 2002;39:155–160.
   PubMed Web of Science ®Google Scholar
• Benyo DF, Smarason A, Redman CW, et al. Expression of inflammatory cytokines in placentas from women with preeclampsia. J Chin Endocrinol Metab 2001;86:2505–2512.
   PubMed Web of Science ®Google Scholar
• Norris LA, Higgins JR, Darling MR, et al. Nitric oxide in the uteroplacental, fetoplacental, and peripheral circulations in preeclampsia. Obstet Gynecol 1999;93:958–963.
   PubMed Web of Science ®Google Scholar
• Khaliq A, Dunk C, Jiang J, et al. Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: Molecular evidence for 'placental hyperoxia' in intrauterine growth restriction. Lab Invest 1999;79:151–170.
   PubMed Web of Science ®Google Scholar
• Lash GE, Taylor CM, Trew AJ, et al. Vascular endothelial growth factor and placental growth factor release in cultured trophoblast cells under different oxygen tensions. Growth Factors 2002;20:189–196.
   PubMed Web of Science ®Google Scholar
• Shore VH, Wang TH, Wang CL, et al. Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 1997;18:657–665.
   PubMed Web of Science ®Google Scholar
• Kumazaki K, Nakayama M, Suehara N, et al. Expression of vascular endothelial growth factor, placental growth factor, and their receptors Flt-1 and KDR in human placenta under pathologic conditions. Hum Pathol 2002;33:1069–1077.
   PubMed Web of Science ®Google Scholar
• Ahmed A, Dunk C, Kniss D, et al. Role of VEGF receptor-1 (Flt-1) in mediating calcium-dependent nitric oxide release and limiting DNA synthesis in human trophoblast cells. Lab Invest 1997;76:779–791.
   PubMed Web of Science ®Google Scholar
• Athanassiades A, Lala PK. Role of placenta growth factor (PIGF) in human extravillous trophoblast proliferation, migration and invasiveness. Placenta 1998;19:465–473.
   PubMed Web of Science ®Google Scholar
• Athanassiades A, Hamilton GS, Lala PK. Vascular endothelial growth factor stimulates proliferation but not migration or invasiveness in human extravillous trophoblast. Biol Reprod 1998;59:643–654.
   Google Scholar
• Benirschke K, Kaufmann P. Pathology of the human placenta. New York: Springer-Verlag; 2000.
   Google Scholar
• Desai J, Holt-Shore V, Torry RJ, et al. Signal transduction and biological function of placenta growth factor in primary human trophoblast. Biol Reprod 1999;60:887–892.
   PubMed Web of Science ®Google Scholar
• Kingdom J, Huppertz B, Seaward G, et al. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol 2000;92:35–43.
   PubMed Web of Science ®Google Scholar
• Lash GE, Cartwright JE, Whitley GS, et al. The effects of angiogenic growth factors on extravillous trophoblast invasion and motility. Placenta 1999;20:661–667.
   PubMed Web of Science ®Google Scholar
• Horowitz JR, Rivard A, van der Z R, et al. Vascular endothelial growth factor/vascular permeability factor pro-duces nitric oxide-dependent hypotension. Evidence for a maintenance role in quiescent adult endothelium. Arterioscler Thromb Vasc Biol 1997;17:2793–2800.
   Google Scholar
• He H, Venema VJ, Gu X, et al. 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.
   PubMed Web of Science ®Google Scholar
• Gliki G, Abu-Ghazaleh R, Jezequel S, et al. Vascular endothelial growth factor-induced prostacyclin production is mediated by a protein kinase C (PKC)-dependent activation of extracellular signal-regulated protein kinases 1 and 2 involving PKC-delta and by mobilization of intracellular Ca2 + . Biochem J 2001;353:503–512.
   PubMed Web of Science ®Google Scholar