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PMID: 19337544 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Pathophysiology of placentation abnormalities in pregnancy-induced hypertension.

Vascular health and risk management ·Vol. 4 ·No. 6 ·2008-00-00 ·Pages 1301-13

Furuya M, Ishida J, Aoki I, Fukamizu A

Abstract

During embryogenesis and development, the fetus obtains oxygen and nutrients from the mother through placental microcirculation. The placenta is a distinctive organ that develops and differentiates per se, and that organizes fetal growth and maternal condition in the entire course of gestation. Several life-threatening diseases during pregnancy, such as pregnancy-induced hypertension (PIH) and eclampsia, are closely associated with placental dysfunction. Genetic susceptibilities and poor placentation have been investigated intensively to understand the pathophysiology of PIH. It is currently thought that "poor placentation hypothesis", in which extravillous trophoblasts fail to invade sufficiently the placental bed, explains in part maternal predisposition to this disease. Cumulative studies have suggested that hypoxic micromilieu of fetoplacental site, shear stress of uteroplacental blood flow, and aberrantly secreted proinflammatory substances into maternal circulation synergistically contribute to the progression of PIH. For example, soluble form of vascular endothelial growth factor receptor-1 (sVEGFR-1) and soluble form of CD105 are elevated in circulation of PIH mothers. However, it remains to be poorly understood the pathological events in the placenta during the last half of gestation as maternal systemic disorders get worse. For better understanding and effective therapeutic approaches to PIH, it is important to clarify pathological course of PIH-associated changes in the placenta. In this review, current understanding of placental development and the pathophysiology of PIH placenta are summarized. In addition, recent findings of vasoactive signalings in PIH and rodent PIH models are discussed.

Keywords
intrauterine growth restriction neovascularization placenta preeclampsia pregnancy-induced hypertension renin –angiotensin-system transgenic mice
MeSH Terms
Animals Antihypertensive Agents/therapeutic use Cell Differentiation Disease Models, Animal Embryo Implantation Endothelial Cells/metabolism Female Fetal Growth Retardation/physiopathology Gestational Age Humans Hypertension, Pregnancy-Induced/drug therapy,etiology,metabolism,physiopathology Inflammation/physiopathology Inflammation Mediators/metabolism Neovascularization, Physiologic Placenta/blood supply,metabolism,physiopathology Placental Circulation Placentation Pre-Eclampsia/physiopathology Pregnancy Receptor, Angiotensin, Type 1/metabolism Renin-Angiotensin System Risk Factors Signal Transduction Trophoblasts/metabolism
Chemicals
Antihypertensive Agents Inflammation Mediators Receptor, Angiotensin, Type 1
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Furuya Mitsuko
Department of Pathology, Yokohama City University Graduate School of Medicine, 3-9 Fuku-ura, Kanazawa, Yokohama, Japan. [email protected]
Ishida Junji
Aoki Ichiro
Fukamizu Akiyoshi
References (100)
100 references, click to expand
  1. CD105 is important for angiogenesis: evidence and potential applications.
    FASEB J. 2003 Jun;17(9):984-92 PMID: 12773481
  2. Soluble endoglin contributes to the pathogenesis of preeclampsia.
    Nat Med. 2006 Jun;12(6):642-9 PMID: 16751767
  3. Targeting HIF-1 for cancer therapy.
    Nat Rev Cancer. 2003 Oct;3(10):721-32 PMID: 13130303
  4. Excessive placental secretion of neurokinin B during the third trimester causes pre-eclampsia.
    Nature. 2000 Jun 15;405(6788):797-800 PMID: 10866201
  5. Angiotensinogen T235 expression is elevated in decidual spiral arteries.
    J Clin Invest. 1997 Sep 15;100(6):1406-15 PMID: 9294106
  6. Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility.
    Science. 2001 Mar 2;291(5509):1800-3 PMID: 11230698
  7. Antiplatelet drugs for prevention of pre-eclampsia and its consequences: systematic review.
    BMJ. 2001 Feb 10;322(7282):329-33 PMID: 11159655
  8. Preeclampsia: recent insights.
    Hypertension. 2005 Dec;46(6):1243-9 PMID: 16230510
  9. Minireview: overview of the renin-angiotensin system--an endocrine and paracrine system.
    Endocrinology. 2003 Jun;144(6):2179-83 PMID: 12746271
  10. Human spiral artery renin-angiotensin system.
    Hypertension. 1998 Oct;32(4):683-7 PMID: 9774363
  11. Identification of two novel quantitative trait loci for pre-eclampsia susceptibility on chromosomes 5q and 13q using a variance components-based linkage approach.
    Mol Hum Reprod. 2007 Jan;13(1):61-7 PMID: 17085769
  12. Analysis of natural killer cells isolated from human decidua: Evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-cell function.
    Blood. 2006 Dec 15;108(13):4078-85 PMID: 16931625
  13. Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1.
    Circulation. 2007 Apr 3;115(13):1789-97 PMID: 17389265
  14. Control of vascular resistance in the human placenta.
    Placenta. 1992 Jul-Aug;13(4):329-41 PMID: 1438081
  15. Angiotensin-II stimulates estradiol secretion from human placental explants through AT1 receptor activation.
    J Clin Endocrinol Metab. 1995 Apr;80(4):1233-7 PMID: 7714093
  16. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF.
    Nature. 1999 Dec 23-30;402(6764):884-8 PMID: 10622253
  17. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors.
    Curr Opin Cell Biol. 1998 Oct;10(5):660-6 PMID: 9818178
  18. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma.
    Nat Rev Cancer. 2003 Jun;3(6):411-21 PMID: 12778131
  19. Agonist-induced interactions between angiotensin AT1 and epidermal growth factor receptors.
    Mol Pharmacol. 2005 Aug;68(2):356-64 PMID: 15905421
  20. Angiogenesis in the placenta.
    Biol Reprod. 2001 Apr;64(4):1033-40 PMID: 11259247
  21. How Does the maternal immune system contribute to the development of pre-eclampsia?
    Placenta. 2007 Apr;28 Suppl A:S51-6 PMID: 17292469
  22. Tissue levels of active and total renin, angiotensinogen, human chorionic gonadotropin, estradiol, and progesterone in human placentas from different methods of delivery.
    J Clin Endocrinol Metab. 1989 Jul;69(1):31-7 PMID: 2659618
  23. Prostatic tumor cell plasticity involves cooperative interactions of distinct phenotypic subpopulations: role in vasculogenic mimicry.
    Prostate. 2002 Feb 15;50(3):189-201 PMID: 11813211
  24. Pre-eclampsia, the placenta and the maternal systemic inflammatory response--a review.
    Placenta. 2003 Apr;24 Suppl A:S21-7 PMID: 12842410
  25. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta.
    Dev Biol. 2002 Oct 15;250(2):358-73 PMID: 12376109
  26. Animal models of placental angiogenesis.
    Placenta. 2005 Nov;26(10):689-708 PMID: 16226119
  27. Endothelin converting enzyme (ECE) activity in normal pregnancy and preeclampsia.
    Hypertens Pregnancy. 2003;22(3):215-24 PMID: 14572358
  28. The localization and expression of the renin-angiotensin system in the human placenta throughout pregnancy.
    Placenta. 1999 Jul-Aug;20(5-6):467-74 PMID: 10419812
  29. Production of prostacyclin and thromboxane A2 in mononuclear cells from preeclamptic women.
    Am J Obstet Gynecol. 1993 Nov;169(5):1106-11 PMID: 8238168
  30. Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy.
    Am J Obstet Gynecol. 2000 Jul;183(1):S1-S22 PMID: 10920346
  31. Hypoxia and sFlt-1 in preeclampsia: the "chicken-and-egg" question.
    Endocrinology. 2004 Nov;145(11):4835-7 PMID: 15489315
  32. Placental development: lessons from mouse mutants.
    Nat Rev Genet. 2001 Jul;2(7):538-48 PMID: 11433360
  33. G-protein-coupled receptors and cancer.
    Nat Rev Cancer. 2007 Feb;7(2):79-94 PMID: 17251915
  34. Absence of endothelial cells, central necrosis, and fibrosis are associated with aggressive inflammatory breast cancer.
    Cancer Res. 2001 Jan 15;61(2):445-51 PMID: 11212228
  35. Immunology of placentation in eutherian mammals.
    Nat Rev Immunol. 2006 Aug;6(8):584-94 PMID: 16868549
  36. Cell migration activated by platelet-derived growth factor receptor is blocked by an inverse agonist of the sphingosine 1-phosphate receptor-1.
    FASEB J. 2006 Mar;20(3):509-11 PMID: 16319133
  37. Profile of neurokinin B concentrations in maternal and cord blood in normal pregnancy.
    Clin Endocrinol (Oxf). 2003 May;58(5):597-600 PMID: 12699441
  38. An antiangiogenic neurokinin-B/thromboxane A2 regulatory axis.
    J Cell Biol. 2006 Sep 25;174(7):1047-58 PMID: 17000881
  39. Differential roles of renin and angiotensinogen in the feto-maternal interface in the development of complications of pregnancy.
    Mol Endocrinol. 2005 May;19(5):1361-72 PMID: 15695374
  40. Maternal segregation of the Dutch preeclampsia locus at 10q22 with a new member of the winged helix gene family.
    Nat Genet. 2005 May;37(5):514-9 PMID: 15806103
  41. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor.
    J Clin Invest. 1999 Apr;103(7):945-52 PMID: 10194466
  42. Pathophysiology of pregnancy-induced hypertension.
    Am J Hypertens. 2001 Jun;14(6 Pt 2):178S-185S PMID: 11411754
  43. Angiotensin II levels in hypertensive and normotensive pregnancies.
    Br J Obstet Gynaecol. 1991 Feb;98(2):155-61 PMID: 2004051
  44. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success.
    J Exp Med. 2004 Oct 18;200(8):957-65 PMID: 15477349
  45. Prostacyclin and thromboxane changes predating clinical onset of preeclampsia: a multicenter prospective study.
    JAMA. 1999 Jul 28;282(4):356-62 PMID: 10432033
  46. An essential role for angiotensin II type 1a receptor in pregnancy-associated hypertension with intrauterine growth retardation.
    FASEB J. 2004 Feb;18(2):388-90 PMID: 14688210
  47. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry.
    Am J Pathol. 1999 Sep;155(3):739-52 PMID: 10487832
  48. Possible molecular mechanisms involved in the toxicity of angiogenesis inhibition.
    Nat Rev Cancer. 2007 Jun;7(6):475-85 PMID: 17522716
  49. Mechanisms of hypertension associated with BAY 43-9006.
    J Clin Oncol. 2006 Mar 20;24(9):1363-9 PMID: 16446323
  50. Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: role in vasculogenic mimicry.
    Crit Rev Oncol Hematol. 2002 Oct;44(1):17-27 PMID: 12398997
  51. Molecular determinants of ovarian cancer plasticity.
    Am J Pathol. 2001 Apr;158(4):1279-88 PMID: 11290546
  52. Cellular localization of AT1 receptor mRNA and protein in normal placenta and its reduced expression in intrauterine growth restriction. Angiotensin II stimulates the release of vasorelaxants.
    J Clin Invest. 1998 Jan 15;101(2):442-54 PMID: 9435317
  53. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10705-9 PMID: 8248162
  54. Neurokinin B peptide serum levels are higher in normotensive pregnant women than in preeclamptic pregnant women.
    Am J Obstet Gynecol. 2003 Nov;189(5):1418-22 PMID: 14634580
  55. Angiotensin II induces soluble fms-Like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy.
    Circ Res. 2007 Jan 5;100(1):88-95 PMID: 17158338
  56. Dialogue between blastocyst hCG and endometrial LH/hCG receptor: which role in implantation?
    Gynecol Obstet Invest. 2007;64(3):156-60 PMID: 17934312
  57. Surface expression of HLA-C antigen by human extravillous trophoblast.
    Placenta. 2000 May;21(4):376-87 PMID: 10833373
  58. New insights into the biology of preeclampsia.
    Biol Reprod. 2006 May;74(5):772-6 PMID: 16421233
  59. Angiogenesis and vasculogenesis in pregnancy.
    Eur J Obstet Gynecol Reprod Biol. 2003 Sep 22;110 Suppl 1:S10-8 PMID: 12965086
  60. Transforming growth factor-beta expression in human placenta and placental bed in third trimester normal pregnancy, preeclampsia, and fetal growth restriction.
    Am J Pathol. 2001 Nov;159(5):1827-38 PMID: 11696443
  61. Determination of renin, angiotensin converting enzyme and angiotensin II levels in human placenta, chorion and amnion from women with pregnancy induced hypertension.
    Clin Endocrinol (Oxf). 1996 Apr;44(4):429-33 PMID: 8706309
  62. Comparative developmental anatomy of the murine and human definitive placentae.
    Placenta. 2002 Jan;23(1):3-19 PMID: 11869088
  63. Cancer neovascularization and proinflammatory microenvironments.
    Curr Cancer Drug Targets. 2008 Jun;8(4):253-65 PMID: 18537549
  64. Latest advances in understanding preeclampsia.
    Science. 2005 Jun 10;308(5728):1592-4 PMID: 15947178
  65. Endoglin regulates nitric oxide-dependent vasodilatation.
    FASEB J. 2004 Mar;18(3):609-11 PMID: 14734648
  66. Hypertension induced in pregnant mice by placental renin and maternal angiotensinogen.
    Science. 1996 Nov 8;274(5289):995-8 PMID: 8875944
  67. A study of angiotensin II pressor response throughout primigravid pregnancy.
    J Clin Invest. 1973 Nov;52(11):2682-9 PMID: 4355997
  68. Angiotensin II type 1 receptor agonistic antibodies reflect fundamental alterations in the uteroplacental vasculature.
    Hypertension. 2005 Dec;46(6):1275-9 PMID: 16260641
  69. Human uterine decidual macrophages express renin.
    J Clin Endocrinol Metab. 1995 Apr;80(4):1273-7 PMID: 7714100
  70. Cross-sectional and longitudinal evaluation of uterine artery Doppler velocimetry for the prediction of pre-eclampsia in normotensive women with specific risk factors.
    Ultrasound Obstet Gynecol. 2003 Aug;22(2):160-5 PMID: 12905511
  71. Autoantibody from women with preeclampsia induces soluble Fms-like tyrosine kinase-1 production via angiotensin type 1 receptor and calcineurin/nuclear factor of activated T-cells signaling.
    Hypertension. 2008 Apr;51(4):1010-9 PMID: 18259044
  72. Association of a variant of the angiotensinogen gene with pure type of hypertension in pregnancy in the Japanese: implication of a racial difference and significance of an age factor.
    Am J Med Genet. 1999 Sep 17;86(3):232-6 PMID: 10482871
  73. Trophoblastic remodeling in normal and preeclamptic pregnancies: implication of cytokines.
    Clin Biochem. 2003 Jul;36(5):323-31 PMID: 12849862
  74. Predicting the risk of pre-eclampsia and a small-for-gestational-age infant by quantitative assessment of the diastolic notch in uterine artery flow velocity waveforms in unselected women.
    Ultrasound Obstet Gynecol. 2000 Aug;16(2):171-8 PMID: 11117089
  75. The uterine spiral arteries in human pregnancy: facts and controversies.
    Placenta. 2006 Sep-Oct;27(9-10):939-58 PMID: 16490251
  76. Impaired placental neovascularization in mice with pregnancy-associated hypertension.
    Lab Invest. 2008 Apr;88(4):416-29 PMID: 18268474
  77. Current topic: the uteroplacental renin-angiotensin system.
    Placenta. 2000 Jul-Aug;21(5-6):468-77 PMID: 10940196
  78. Priming and remodelling of human placental bed spiral arteries during pregnancy--a review.
    Placenta. 2005 Apr;26 Suppl A:S31-6 PMID: 15837064
  79. Angiotensin II regulation of ovine fetoplacental artery endothelial functions: interactions with nitric oxide.
    J Physiol. 2005 May 15;565(Pt 1):59-69 PMID: 15790666
  80. Targeting sphingosine-1-phosphate: a novel avenue for cancer therapeutics.
    Cancer Cell. 2006 Mar;9(3):148-50 PMID: 16530698
  81. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells.
    Eur J Immunol. 2000 Jun;30(6):1623-31 PMID: 10898498
  82. Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness.
    Nat Med. 2001 Sep;7(9):1003-9 PMID: 11533702
  83. Assessment of fetal compromise by Doppler ultrasound investigation of the fetal circulation. Arterial, intracardiac, and venous blood flow velocity studies.
    Circulation. 1995 Jan 1;91(1):129-38 PMID: 7805194
  84. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia.
    Circ Res. 2004 Oct 29;95(9):884-91 PMID: 15472115
  85. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia.
    N Engl J Med. 2006 Sep 7;355(10):992-1005 PMID: 16957146
  86. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia.
    J Clin Invest. 2003 Mar;111(5):649-58 PMID: 12618519
  87. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?
    J Clin Invest. 1997 May 1;99(9):2139-51 PMID: 9151786
  88. Endoglin increases eNOS expression by modulating Smad2 protein levels and Smad2-dependent TGF-beta signaling.
    J Cell Physiol. 2007 Feb;210(2):456-68 PMID: 17058229
  89. Physiology of local renin-angiotensin systems.
    Physiol Rev. 2006 Jul;86(3):747-803 PMID: 16816138
  90. Expression of kallikrein, bradykinin b2 receptor, and endothelial nitric oxide synthase in placenta in normal gestation, preeclampsia, and placenta accreta.
    Endocrine. 2006 Jun;29(3):491-9 PMID: 16943589
  91. Dysregulation of the circulating and tissue-based renin-angiotensin system in preeclampsia.
    Hypertension. 2007 Mar;49(3):604-11 PMID: 17261642
  92. Rats transgenic for human renin and human angiotensinogen as a model for gestational hypertension.
    J Am Soc Nephrol. 2000 Nov;11(11):2056-2061 PMID: 11053481
  93. Mechanical stress-initiated signal transductions in vascular smooth muscle cells.
    Cell Signal. 2000 Jul;12(7):435-45 PMID: 10989277
  94. 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 Apr;160(4):1405-23 PMID: 11943725
  95. The influence of donated gametes on the incidence of hypertensive disorders of pregnancy.
    Hum Reprod. 1999 Sep;14(9):2268-73 PMID: 10469693
  96. Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-gamma.
    J Immunol. 2006 Dec 15;177(12):8522-30 PMID: 17142750
  97. Pathophysiology of tumor neovascularization.
    Vasc Health Risk Manag. 2005;1(4):277-90 PMID: 17315600
  98. Endovascular trophoblast invasion, spiral artery remodelling and uteroplacental haemodynamics in a transgenic rat model of pre-eclampsia.
    Placenta. 2008 Jul;29(7):614-23 PMID: 18502502
  99. Basement membranes: structure, assembly and role in tumour angiogenesis.
    Nat Rev Cancer. 2003 Jun;3(6):422-33 PMID: 12778132
  100. Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer.
    J Clin Oncol. 2006 Jan 1;24(1):25-35 PMID: 16314617
Article Info
Journal
Vascular health and risk management
Abbr.
Vasc Health Risk Manag
ISSN
1178-2048
Published
2008-00-00
Pages
1301-13
Language
English
Region
New Zealand
NLM ID
101273479
PMCID
PMC2663465
Subset
IM
Analysis Services
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