535
Views
8
CrossRef citations to date
0
Altmetric
Editorial

The role of an ‘anti-angiogenic state’ in complications of pregnancy

, MD, PhD
Pages 3-7 | Published online: 07 Jul 2009

References

  • Li Z, Zhang Y, Ying M J, Kapoun A M, Shao Q, Kerr I, Lam A, O'Young G, Sannajust F, Stathis P, et al. Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 2007; 50: 686–692
  • Folkman J. Angiogenesis inhibitors: A new class of drugs. Cancer Biol Ther 2003; 2: S127–133
  • Folkman J. Antiangiogenesis in cancer therapy—endostatin and its mechanisms of action. Exp Cell Res 2006; 312: 594–607
  • Folkman J. Angiogenesis: An organizing principle for drug discovery?. Nat Rev Drug Discov 2007; 6: 273–286
  • Murray M J, Lessey B A. Embryo implantation and tumor metastasis: Common pathways of invasion and angiogenesis. Semin Reprod Endocrinol 1999; 17: 275–290
  • Charnock-Jones D S, Kaufmann P, Mayhew T M. Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta 2004; 25: 103–113
  • Kaufmann P, Mayhew T M, Charnock-Jones D S. Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 2004; 25: 114–126
  • Mayhew T M, Charnock-Jones D S, Kaufmann P. Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta 2004; 25: 127–139
  • Gale N W, Yancopoulos G D. Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development. Genes Dev 1999; 13: 1055–1066
  • Yancopoulos G D, Davis S, Gale N W, Rudge J S, Wiegand S J, Holash J. Vascular-specific growth factors and blood vessel formation. Nature 2000; 407: 242–248
  • Matsumoto T, Claesson-Welsh L. VEGF receptor signal transduction. Sci STKE 2001; 2001: RE21
  • Ferrara N, Gerber H P, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669–676
  • Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature 2005; 438: 937–945
  • Alitalo K, Tammela T, Petrova T V. Lymphangiogenesis in development and human disease. Nature 2005; 438: 946–953
  • Pereira F A, Qiu Y, Zhou G, Tsai M J, Tsai S Y. The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev 1999; 13: 1037–1049
  • Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005; 438: 932–936
  • Petit F G, Jamin S P, Kurihara I, Behringer R R, DeMayo F J, Tsai M J, Tsai S Y. Deletion of the orphan nuclear receptor COUP-TFII in uterus leads to placental deficiency. Proc Natl Acad Sci U S A 2007; 104: 6293–6298
  • Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380: 435–439
  • Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea K S, Powell-Braxton L, Hillan K J, Moore M W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996; 380: 439–442
  • Clark D E, Smith S K, He Y, Day K A, Licence D R, Corps A N, Lammoglia R, Charnock-Jones D S. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998; 59: 1540–1548
  • Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, Alitalo K, Damsky C, Fisher S J. 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 2002; 160: 1405–1423
  • Reynolds L P, Redmer D A. Utero-placental vascular development and placental function. J Anim Sci 1995; 73: 1839–1851
  • Kendall R L, Wang G, Thomas K A. Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 1996; 226: 324–328
  • Lyall F, Greer I A. The vascular endothelium in normal pregnancy and pre-eclampsia. Rev Reprod 1996; 1: 107–116
  • Cheung C Y. Vascular endothelial growth factor: Possible role in fetal development and placental function. J Soc Gynecol Investig 1997; 4: 169–177
  • Kupferminc M J, Daniel Y, Englender T, Baram A, Many A, Jaffa A J, Gull I, Lessing J B. Vascular endothelial growth factor is increased in patients with preeclampsia. Am J Reprod Immunol 1997; 38: 302–306
  • Lyall F, Greer I A, Boswell F, Fleming R. Suppression of serum vascular endothelial growth factor immunoreactivity in normal pregnancy and in pre-eclampsia. Br J Obstet Gynaecol 1997; 104: 223–228
  • Vuorela P, Hatva E, Lymboussaki A, Kaipainen A, Joukov V, Persico M G, Alitalo K, Halmesmäki E. Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol Reprod 1997; 56: 489–494
  • Athanassiades A, Lala P K. Role of placenta growth factor (PIGF) in human extravillous trophoblast proliferation, migration and invasiveness. Placenta 1998; 19: 465–473
  • Taylor R N, de Groot C J, Cho Y K, Lim K H. Circulating factors as markers and mediators of endothelial cell dysfunction in preeclampsia. Semin Reprod Endocrinol 1998; 16: 17–31
  • Torry D S, Wang H S, Wang T H, Caudle M R, Torry R J. Preeclampsia is associated with reduced serum levels of placenta growth factor. Am J Obstet Gynecol 1998; 179: 1539–1544
  • Desai J, Holt-Shore V, Torry R J, Caudle M R, Torry D S. Signal transduction and biological function of placenta growth factor in primary human trophoblast. Biol Reprod 1999; 60: 887–892
  • Hayman R, Brockelsby J, Kenny L, Baker P. Preeclampsia: The endothelium, circulating factor(s) and vascular endothelial growth factor. J Soc Gynecol Investig 1999; 6: 3–10
  • Lash G E, Cartwright J E, Whitley G S, Trew A J, Baker P N. The effects of angiogenic growth factors on extravillous trophoblast invasion and motility. Placenta 1999; 20: 661–667
  • Reuvekamp A, Velsing-Aarts F V, Poulina I E, Capello J J, Duits A J. Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre-eclampsia. Br J Obstet Gynaecol 1999; 106: 1019–1022
  • Torry D S, Ahn H, Barnes E L, Torry R J. Placenta growth factor: Potential role in pregnancy. Am J Reprod Immunol 1999; 41: 79–85
  • Ahmed A, Perkins J. Angiogenesis and intrauterine growth restriction. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14: 981–998
  • Charnock-Jones D S, Burton G J. Placental vascular morphogenesis. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14: 953–968
  • Hornig C, Barleon B, Ahmad S, Vuorela P, Ahmed A, Weich H A. Release and complex formation of soluble VEGFR-1 from endothelial cells and biological fluids. Lab Invest 2000; 80: 443–454
  • Ong S, Lash G, Baker P N. Angiogenesis and placental growth in normal and compromised pregnancies. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14: 969–980
  • Tidwell S C, Ho H N, Chiu W H, Torry R J, Torry D S. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001; 184: 1267–1272
  • Maulik D, Frances E J, Ragolia L. Fetal Growth Restriction: Pathogenic Mechanisms. Clin Obstet Gynecol 2006; 49(2)219–227
  • Torry D S, Mukherjea D, Arroyo J, Torry R J. Expression and function of placenta growth factor: Implications for abnormal placentation. J Soc Gynecol Investig 2003; 10: 178–188
  • Tsatsaris V, Goffin F, Munaut C, Brichant J F, Pignon M R, Noel A, Schaaps J P, Cabrol D, Frankenne F, Foidart J M. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: Pathophysiological consequences. J Clin Endocrinol Metab 2003; 88: 5555–5563
  • Maynard S, Epstein F H, Karumanchi S A. Preeclampsia and angiogenic imbalance. Annu Rev Med Oct 15, 2007, [Epub ahead of print]
  • Maynard S E, Min J Y, Merchan J, Lim K H, Li J, Mondal S, Libermann T A, Morgan J P, Sellke F W, Stillman I E, 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
  • Levine R J, Maynard S E, Qian C, Lim K H, England L J, Yu K F, Schisterman E F, Thadhani R, Sachs B P, Epstein F H, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350: 672–683
  • Chaiworapongsa T, Romero R, Kim Y M, Kim G J, Kim M R, Espinoza J, Bujold E, Gonçalves L, Gomez R, Edwin S, et al. 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
  • Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee K Y, Gonçalves L F, Gomez R, Edwin S. 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
  • Levine R J, Lam C, Qian C, Yu K F, Maynard S E, Sachs B P, Sibai B M, Epstein F H, Romero R, Thadhani R, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006; 355: 992–1005
  • Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim Y M, Bdolah Y, Lim K H, Yuan H T, Libermann T A, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12: 642–649
  • Robinson C J, Johnson D D. Soluble endoglin as a second-trimester marker for preeclampsia. Am J Obstet Gynecol 2007; 197: 174–175
  • Staff A C, Braekke K, Johnsen G M, Karumanchi S A, Harsem N K. Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 2007; 197: 176
  • Romero R, Nien J K, Espinoza J, Todem D, Fu W, Chung H, Kusanovic J P, Gotsch F, Erez O, Mazaki-tovi S, 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 Neonatal Med 2008; 21: 9–23
  • Chaiworapongsa T, Espinoza J, Gotsch F, Kim Y M, Kim G J, Goncalves L F, Edwin S, Kusanovic J P, Erez O, Than N G, et al. The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation. J Matern Fetal Neonatal Med 2008; 21: 25–40
  • Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic J P, Gotsch F, Edwin S, Nien J K, Chaiworapongsa T, 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 SGA. J Matern Fetal Neonatal Med 2008
  • Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003; 88: 2348–2351
  • McKeeman G C, Ardill J E, Caldwell C M, Hunter A J, McClure N. Soluble vascular endothelial growth factor receptor-1 (sFlt-1) is increased throughout gestation in patients who have preeclampsia develop. Am J Obstet Gynecol 2004; 191: 1240–1246
  • Krauss T, Pauer H U, Augustin H G. Prospective analysis of placenta growth factor (PlGF) concentrations in the plasma of women with normal pregnancy and pregnancies complicated by preeclampsia. Hypertens Pregnancy 2004; 23: 101–111
  • Thadhani R, Mutter W P, Wolf M, Levine R J, Taylor R N, Sukhatme V P, Ecker J, Karumanchi S A. First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 2004; 89: 770–775
  • Maynard S E, Venkatesha S, Thadhani R, Karumanchi S A. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res 2005; 57: 1R–7R
  • Chaiworapongsa T, Romero R, Kim Y M, Kim G J, Kim M R, Espinoza J, Bujold E, Gonçalves L, Gomez R, Edwin S, et al. 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
  • Redman C W, Sargent I L. Latest advances in understanding preeclampsia. Science 2005; 308: 1592–1594
  • Bdolah Y, Karumanchi S A, Sachs B P. Recent advances in understanding of preeclampsia. Croat Med J 2005; 46: 728–736
  • Levine R J, Thadhani R, Qian C, Lam C, Lim K H, Yu K F, Blink A L, Sachs B P, Epstein F H, Sibai B M, et al. Urinary placental growth factor and risk of preeclampsia. JAMA 2005; 293: 77–85
  • Rajakumar A, Michael H M, Rajakumar P A, Shibata E, Hubel C A, Karumanchi S A, 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
  • Levine R J, Karumanchi S A. Circulating angiogenic factors in preeclampsia. Clin Obstet Gynecol 2005; 48: 372–386
  • Shibata E, Rajakumar A, Powers R W, Larkin R W, Gilmour C, Bodnar L M, Crombleholme W R, Ness R B, Roberts J M, Hubel C A. 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
  • Staff A C, Braekke K, Harsem N K, Lyberg T, Holthe M R. 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
  • Espinoza J, Nien J K, Kusanovic J P, Goncalves L F, Medina L H, Gomez R, Romero R. The combined use of uterine artery Doppler and maternal plasma placental growth factor concentrations identifies patients at risk for early onset and/or severe preeclampsia. Ultrasound Obstet Gynecol 2006; 28: 387–388
  • Robinson C J, Johnson D D, Chang E Y, Armstrong D M, Wang W. Evaluation of placenta growth factor and soluble Fms-like tyrosine kinase 1 receptor levels in mild and severe preeclampsia. Am J Obstet Gynecol 2006; 195: 255–259
  • Aggarwal P K, Jain V, Sakhuja V, Karumanchi S A, Jha V. Low urinary placental growth factor is a marker of pre-eclampsia. Kidney Int 2006; 69: 621–624
  • Levine R J, Qian C, Maynard S E, Yu K F, Epstein F H, Karumanchi S A. Serum sFlt1 concentration during preeclampsia and mid trimester blood pressure in healthy nulliparous women. Am J Obstet Gynecol 2006; 194: 1034–1041
  • Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 2006; 195: 201–207
  • Stepan H, Faber R. Elevated sFlt1 level and preeclampsia with parvovirus-induced hydrops. N Engl J Med 2006; 354: 1857–1858
  • Salahuddin S, Lee Y, Vadnais M, Sachs B P, Karumanchi S A, Lim K H. Diagnostic utility of soluble fms-like tyrosine kinase 1 and soluble endoglin in hypertensive diseases of pregnancy. Am J Obstet Gynecol 2007; 197: 28.e1–6
  • Malamitsi-Puchner A, Boutsikou T, Economou E, Sarandakou A, Makrakis E, Hassiakos D, Creatsas G. Vascular endothelial growth factor and placenta growth factor in intrauterine growth-restricted fetuses and neonates. Mediators Inflamm 2005; 2005: 293–297
  • Boutsikou T, Malamitsi-Puchner A, Economou E, Boutsikou M, Puchner K P, Hassiakos D. Soluble vascular endothelial growth factor receptor-1 in intrauterine growth restricted fetuses and neonates. Early Hum Dev 2006; 82: 235–239
  • Girardi G, Yarilin D, Thurman J M, Holers V M, Salmon J E. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006; 203: 2165–2175
  • Padavala S, Pope N, Baker P, Crocker I. An imbalance between vascular endothelial growth factor and its soluble receptor in placental villous explants of intrauterine growth-restricted pregnancies. J Soc Gynecol Investig 2006; 13: 40–47
  • Wallner W, Sengenberger R, Strick R, Strissel P L, Meurer B, Beckmann M W, Schlembach D. Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clin Sci (Lond) 2007; 112: 51–57
  • Espinoza J, Nien J K, Kusanovic J P, Richani K, Gomez R, Kim C J, Mittal P, Chaiworapongsa T, Romero R. A role of the anti-angiogenic factor sVEGFR-1 in the ‘mirror syndrome’ (Ballantyne's syndrome). Am J Obstet Gynecol 2005; 193: S134
  • Espinoza J, Romero R, Nien J K, Kusanovic J P, Richani K, Gomez R, Kim C J, Mittal P, Gotsh F, Erez O, et al. A role of the anti-angiogenic factor sVEGFR-1 in the ‘mirror syndrome’ (Ballantyne's syndrome). J Matern Fetal Neonatal Med 2006; 19: 607–613
  • Rana S, Venkatesha S, DePaepe M, Chien E K, Paglia M, Karumanchi S A. Cytomegalovirus-induced mirror syndrome associated with elevated levels of circulating antiangiogenic factors. Obstet Gynecol 2007; 109: 549–552
  • Signore C, Mills J L, Qian C, Yu K, Lam C, Epstein F H, Karumanchi S A, Levine R J. Circulating angiogenic factors and placental abruption. Obstet Gynecol 2006; 108: 338–344
  • Kumazaki K, Nakayama M, Suehara N, Wada Y. 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
  • Espinoza J, Chaiworapongsa T, Romero R, Kim Y M, Kim G J, Nien J K, Kusanovic J P, Erez O, Bujold E, Gonçalves L F, et al. Unexplained fetal death: Another anti-angiogenic state. J Matern Fetal Neonatal Med 2007; 20: 495–507
  • Espinoza J, Romero R, Nien J K, Gomez R, Kusanovic J P, Gonçalves L F, Medina L, Edwin S, Hassan S, Carstens M, et al. Identification of patients at risk for early onset and/or severe preeclampsia with the use of uterine artery Doppler velocimetry and placental growth factor. Am J Obstet Gynecol 2007; 196: 326–313

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.