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Review

Placentation abnormalities in the pathophysiology of preeclampsia

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Pages 37-49 | Published online: 09 Jan 2014

References

  • van Lerberghe W; World Health Organization. World health report: make every mother and child count. World Health Organization, Geneva (2005).
  • Marin R, Gorostidi M, Portal CG et al. Long-term prognosis of hypertension in pregnancy. Hypertens. Pregnancy19(2), 199–209 (2000).
  • Duckitt K, Harrington D. Risk factors for preeclampsia at antenatal booking: systemic review of controlled studies. BMJ330(7491), 565–571 (2005).
  • Mazar RM, Srinivas SK, Sammel MD et al. Metabolic score as a novel approach to assessing preeclampsia risk. Am. J. Obstet. Gynecol.197(4), 411 e1–e5 (2007).
  • Loi K, Khoo CK, Tan KH et al. A review of 93 cases of severe preeclampsia in Singapore: are there risk factors for complications? Singapore Med. J.48(9), 808–812 (2007).
  • Silver RK, Wilson RD, Philip J et al. Late first-trimester placental disruption and subsequent gestational hypertension/preeclampsia. Obstet. Gynecol.105(3), 587–592 (2005).
  • Haelterman E, Marcoux S, Croteau A et al. Population-based study on occupational risks for preeclampsia and gestational hypertension. Scand. J. Work Environ. Health33(4), 304–317 (2007).
  • ACOG Committee on Obstetric Practice. Diagnosis and management of preeclampsia and eclampsia. ACOG Practice Bulletin No. 33 American College of Obstetricians and Gynecologists. Obstet. Gynecol.99(1), 159–167 (2002).
  • Sibai BM. Imitators of severe preeclampsia. Obstet. Gynecol.109(4), 956–966 (2007).
  • Sibai BM. Diagnosis and management of gestational hypertension and preeclampsia. Obstet. Gynecol.102(1), 181–192 (2003).
  • Zhou Y, Fisher SJ, Janatpour M et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest.99(9), 2139–2151 (1997).
  • Kaufmann P, Black S, Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod.69(1), 1–7 (2003).
  • Dahlstrom B, Romundstad P, Oian P et al. Placenta weight in pre-eclampsia. Acta Obstet. Gynecol. Scand.87(6), 608–611 (2008).
  • Daayana S, Baker P, Crocker I. An image analysis technique for the investigation of variations in placental morphology in pregnancies complicated by preeclampsia with and without intrauterine growth restriction. J. Soc. Gynecol. Investig.11(6), 545–552 (2004).
  • Kos M, Czernobilsky B, Hlupic L, Kunjko K. Pathological changes in placentas from pregnancies with preeclampsia and eclampsia with emphasis on persistence of endovascular trophoblastic plugs. Croat. Med. J.46(3), 404–409 (2005).
  • Redline RW, Patterson P. Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Hum. Pathol.26(6), 594–600 (1995).
  • Robertson WB, Brosens IA, Dixon HG. Placental bed vessels. Am. J. Obstet Gynecol.117(2), 294–295 (1973).
  • Lain KY, Roberts JM. Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA287(24), 3183–3186 (2002).
  • Redman CWG, Sargent IL. Pre-eclampsia, the placenta and the maternal systemic inflammatory response – a review. Placenta17(Suppl. A), S21–S27 (2003).
  • Stanek J, Weng E. Microscopic chorionic pseudocysts in placental membranes a histologic lesion of in utero hypoxia. Pediatr. Dev. Pathol.10(3), 192–198 (2007).
  • Langbein M, Strick R, Strissel PL et al. Impaired cytotrophoblast cell–cell fusion is associated with reduced syncytin and increased apoptosis in patients with placental dysfunction. Mol. Reprod. Dev.75(1), 175–183 (2008).
  • Richani K, Romero R, Soto E et al. Genetic origin and proportion of basal plate surface-lining cells in normal and abnormal pregnancies. Hum. Pathol.38(2), 269–275 (2007).
  • Smith RK, Ockleford CD, Byrne S, Bosio P, Sanders R. Healthy and pre-eclamptic placental basal plate lining cells: quantitative comparisons based on confocal laser scanning microscopy. Microsc. Res. Tech.64(1), 54–62 (2004).
  • Ockleford CD, Smith RK, Byrne S, Sanders R, Bosio P. Confocal laser scanning microscope study of cytokeratin immunofluorescence differences between villus and extravillous trophoblast: cytokeratin downregulation in preeclampsia. Microsc. Res. Tech.64(1), 43–53 (2004).
  • Resta L, Capobianco C, Marzullo A et al. Confocal laser scanning microscope study of terminal villi vessels in normal term and pre-eclamptic placentas. Placenta27(6–7), 735–739 (2006).
  • Mayhew TM, Charnock-Jones DS, Kaufmann P. Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta25(2–3), 127–139 (2004).
  • Mayhew TM, Wijesekara J, Baker PN, Ong SS. Morphometric evidence that villus development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by preeclampsia. Placenta25(10), 829–833 (2004).
  • Egbor M, Ansari T, Morris N, Green CJ, Sibbons PD. Pre-eclampsia and fetal growth restriction: how morphometrically different is the placenta? Placenta27(6–7), 727–734 (2006).
  • Egbor M, Ansari T, Morris N, Green CJ, Sibbons PD. Morphometric placental villus and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction. BJOG113(5), 580–589 (2006).
  • Vinnars MT, Wijnaendts LC, Westgren M, Bolte AC, Papadogiannakis N, Nasiell J. Severe preeclampsia with and without HELLP differ with regard to placental pathology. Hypertension51(5), 1295–1299 (2008).
  • Reister F, Frank HG, Kingdom JC et al. Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab. Invest.81(8), 1143–1152 (2001).
  • Abrahams VM, Kim YM, Straszewski SL et al. Macrophages and apoptotic cell clearance during pregnancy. Am. J. Reprod. Immnol.51(4), 275–282 (2004).
  • Katabuchi H, Yih S, Ohba T et al. Characterization of macrophages in the decidual atherotic spiral artery with special reference to the cytology of foam cells. Med. Electron Microsc.36(4), 253–262 (2003).
  • Hayashi M, Hoshimoto K, Ohkura T, Inaba N. Increased levels of macrophage colony-stimulating factor in the placenta in the placenta and blood in preeclampsia. Am. J. Reprod. Immunol.47(1), 19–24 (2002).
  • Lockwood CJ, Matta P, Krikun G et al. Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor- and interleukin-1 in first trimester human decidual cells. Am. J. Pathol.168(2), 445–452 (2006).
  • Renaud SJ, Graham CH. The role of macrophages in utero-placental interactions during normal and pathological pregnancy. Immunol. Invest.37(5), 535–564 (2008).
  • Huang SJ, Chen CP, Schatz F, Rahman M, Abrahams VM, Lockwood CJ. Pre-eclampsia is associated with dendritic cell recruitment into the uterine deciduas. J. Pathol.214(3), 328–336 (2008).
  • Hiby SE, Walker JJ, O’shaughnessy KM et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med.200(8), 957–965 (2004).
  • Ballermann BJ. Glomerular endothelial cell differentiation. Kidney Int.67(5), 1668–1671 (2005).
  • Maharaj AS, Saint-Geniez M, Maldonado AE, D’Amore PA. Vascular endothelial growth factor localization in the adult. Am. J. Pathol.168(2), 639–648 (2006).
  • Eremina V, Sood M, Haigh J et al. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J. Clin. Invest.111(5), 707–716 (2003).
  • Sugimoto H, Hamano Y, Charytan D et al. Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt1) induces proteinuria. J. Biol. Chem.278(15), 12605–12608 (2003).
  • Cirpan T, Akercan F, Terek MC et al. Evaluation of VEGF in placental bed biopsies from preeclamptic women by immunohistochemistry. Clin. Exp. Obstet. Gynecol.34(4), 228–231 (2007).
  • Akercan F, Cirpan T, Terek MC et al. The immunohistochemical evaluation of VEGF in placenta biopsies of pregnancies complicated by preeclampsia. Arch. Gynecol. Obstet.277(2), 109–114 (2008).
  • Cobellis L, Mastrogiacomo A, Federico E et al. Distribution of Notch protein members in normal and preeclampsia-complicated placentas. Cell Tissue Res.330(3), 527–534 (2007).
  • Gu Y, Lewis DF, Wang Y. Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1, and placental growth factor in normal and preeclamptic pregnancies. J. Clin. Endocrinol. Metab.93(1), 260–266 (2008).
  • 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.111(5), 649–658 (2003).
  • Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ. Res.95(9), 884–891 (2004).
  • Nagamatsu T, Fujii T, Kusumi M et al. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology145(11), 4838–4845 (2004).
  • Munaut C, Lorquet S, Pequeux C et al. Hypoxia is responsible for soluble vascular endothelial growth factor receptor-1 (VEGFR-1) but nor for soluble endoglin induction in villus trophoblast. Hum. Reprod.23(6), 1407–1415 (2008).
  • Zhou Y, McMaster M, Woo K et al. 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 (2002).
  • Zhou CC, Ahmad S, Mi T et al. Angiotensin II induces soluble fms-like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ. Res.100(1), 88–95 (2007).
  • Li H, Gu B, Zhang Y et al. Hypoxia-induced increase in soluble Flt-1 production correlates with enhanced oxidative stress in trophoblast cells from the human placenta. Placenta26(2–3), 210–217 (2005).
  • Rajakumar A, Brandon HM, Daftary A et al. Evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae. Placenta25(10), 763–769 (2004).
  • Chaouat G, Ledée-Bataille N, Dubanchet S. Immune cells in uteroplacental tissues throughout pregnancy: a brief review. Reprod. Biomed. Online14(2), 256–266 (2007).
  • Bauer S, Pollheimer J, Hartmann J, Husslein P, Aplin JD, Knofler M. Tumor necrosis factor-α inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first trimester villus explants cultures. J. Clin. Endocrinol. Metab.89(2), 812–822 (2004).
  • Hayashi M, Ueda Y, Yamaguchi T et al. Tumor necrosis factor-α in the placenta is not elevated in pre-eclamptic patients despite its elevation in peripheral blood. Am. J. Reprod. Immunol.53(3), 113–119 (2005).
  • Hung TH, Charnock-Jones DS, Skepper JN, Burton GJ. Secretion of tumor necrosis factor- from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation in vitro. Am. J. Pathol.164(3), 1049–1061 (2004).
  • Crocker IP, Cooper S, Ong SC, Baker PN. Differences in apoptotic susceptibility of isolated cytotrophoblasts and syncytiotrophoblasts in pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am. J. Pathol.162(2), 637–643 (2003).
  • Kharfi A, Bureau M, Giguere Y, Moutquin JM, Forest JC. Dissociation between increased apoptosis and expression of the tumor necrosis factor-α system in term placental villi with preeclampsia. Clin. Biochem.39(6), 646–651 (2006).
  • Crocker IP, Tansinda DM, Baker PN. Altered cell kinetics in cultured placental villus explants in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. J. Pathol.204(1), 11–18 (2004).
  • Kwaan HC, Wang J, Boggio L Weiss I, Grobman W. The thrombogenic effect of an inflammatory cytokine on trophoblasts from women with preeclampsia. Am. J. Obstet. Gynecol.191(6), 2142–2147 (2004).
  • Seki H, Matuoka K, Inooku H, Takeda S. TNF-α from monocyte of patients with pre-eclampsia-induced apoptosis in human trophoblast cell line. J. Obstet. Gynaecol. Res.33(4), 408–416 (2007).
  • Huang X, Huang H, Dong M, Yao Q, Wang H. Serum and placental interleukin-18 are elevated in preeclampsia. J. Reprod. Immunol.65(1), 77–87 (2005).
  • Hayashi M, Ueda Y, Ohkura T, Inaba N. Interleukin-6 concentrations in the placenta and blood in normal pregnancies and preeclampsia. Hum. Metab. Res.37(7), 419–424 (2005).
  • Lockwood CJ, Yen CF, Basar M et al. Preeclampsia-related inflammatory cytokines regulate interleukin-6 expression in human decidual cells. Am. J. Pathol.172(6), 1571–1579 (2008).
  • Huang SJ, Schatz F, Masch R et al. Regulation of chemokine production in response to pro-inflammatory cytokines in first trimester decidual cells. J. Reprod. Immunol.72(1,2), 60–73 (2006).
  • Visse R, Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinase: structure, function, and biochemistry. Circ. Res.92(8), 827–839 (2003).
  • Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ. Res.90(3), 251–262 (2002).
  • Jones RL, Findlay JK, Farnworth PG et al. Activin A and inhibin A differentially regulate human uterine matrix metalloproteinases: potential interactions during decidualization and trophoblast invasion. Endocrinology147(2), 724–732 (2006).
  • Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem. Pharmacol.75(2), 346–359 (2007).
  • Sawicki G, Radomski MW, Winkler-Lowen B et al. Polarized release of matrix metalloproteinase-2 and -9 from cultured human placental syncytiotrophoblasts. Bio. Reprod.63(5), 1390–1395 (2000).
  • Staun-Ram E, Goldman S, Gabarin D, Shalev E. Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod. Biol. Endocrinol.2, 59–71 (2004).
  • Narumiya H, Zhang Y, Fernandez-Patron C, Guilbert LJ, Davidge ST. Matrix metalloproteinase-2 is elevated in the plasma of women with preeclampsia. Hypertens. Pregnancy20(2), 185–194 (2001).
  • Isaka K, Usuda S, Ito H et al. Expression and activity of matrix metalloproteinase 2 and 9 in human trophoblasts. Placenta24(1), 53–64 (2003).
  • De Jager CA, Linton EA, Spyropoulou I, Sargent IL, Redman CW. Matrix metalloprotease-9, placental syncytiotrophoblast and the endothelial dysfunction of pre-eclampsia. Placenta24(1), 84–91 (2003).
  • Huisman MA, Timmer A, Zeinstra M et al. Matrix-metalloproteinase activity in first trimester placental bed biopsies in further complicated and uncomplicated pregnancies. Placenta25(4), 253–258 (2004).
  • Falkowski PG, Katz ME, Milligan AJ et al. The rise of oxygen over the past 205 years and the evolution of large placental mammals. Science309(5744), 2202–2204 (2005).
  • Genbacev O, Zhou Y, Ludlow JW et al. Regulation of human placental development by oxygen tension. Science277(5332), 1669–1672 (1997).
  • Lee H, Park H, Kim YJ et al. Expression of lectin-like oxidized low-density lipoprotein receptor-1 (LOX-1) in human preeclamptic placenta: possible implications in the process of trophoblast apoptosis. Placenta26(2–3), 226–233 (2005).
  • Ishioka S, Ezaka Y, Umemura K, Hayashi T, Endo T, Saito T. Proteomic analysis of mechanisms of hypoxia-induced apoptosis in trophoblastic cells. Int. J. Med. Sci.4(1), 36–44 (2007).
  • Rajakumar A, Conrad KP. Expression, ontogeny, and regulation of hypoxia-inducible transcription factors in the human placenta. Biol. Reprod.63(2), 559–569 (2000).
  • Semenza GL. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol.13(2), 167–171 (2001).
  • Caniggia I, Mostachfi H, Winter J et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGF-β(3). J. Clin. Invest.105(5), 577–587 (2000).
  • Hayashi M, Sakata M, Takeda T et al. Induction of glucose transporter 1 expression through hypoxia-inducible factor 1α under hypoxic conditions in trophoblast-derived cells. J. Endocrinol.183(1), 145–154 (2004).
  • Iwagaki S, Yokoyama Y, Tang L, Takahashi Y, Nakagawa Y, Tamaya T. Augmentation of leptin and hypoxia-inducible factor 1 mRNAs in the preeclamptic placenta. Gynecol. Endocrinol.18(5), 263–268 (2004).
  • Rajakumar A, Doty K, Daftary A et al. Impaired oxygen-dependent reduction of HIF-1α and -2α proteins in preeclamptic placentae. Placenta24(2–3), 199–208 (2003).
  • Baumann MU, Zamudio S, Illsley NP. Hypoxic upregulation of glucose transporters in BeWo choriocarcinoma cells is mediated by hypoxia-inducible factor-1. Am. J. Physiol. Cell Physiol.293(1), 477–485 (2007).
  • Biondi C, Pavan B, Lunghi L et al. The role and modulation of the oxidative balance in pregnancy. Curr. Pharm. Des.11(16), 2075–2089 (2005).
  • Pavan L, Tsatsaris V, Hermouet A, Therond P, Evain-Brion D, Fournier T. Oxidized low-density lipoproteins inhibit trophoblastic cell invasion. J. Clin. Endocrinol. Metab.89(4), 1969–1972 (2004).
  • Vanderlelie J, Venardos K, Clifton VL, Gude NM, Clarke FM, Perkins AV. Increased biological oxidation and reduced anti-oxidant enzyme activity in pre-eclamptic placentae. Placenta26(1), 53–58 (2005).
  • Myatt L, Rosenfield RB, Eis AL, Brockman DE, Greer I, Lyall F. Nitrotyrosine residues in placenta: evidence of peroxynitrite formation and action. Hypertension28(3), 488–493 (1996).
  • Chekir C, Nakatsuka M, Noguchi S et al. Accumulation of advanced glycation end products in women with preeclampsia: possible involvement of placental oxidative and nitrative stress. Placenta27(2–3), 225–233 (2006).
  • Takagi Y, Nikaido T, Toki T et al. Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction. Virchows Arch.444(1), 49–55 (2004).
  • Santoso DI, Rogers P, Wallace EM, Manuelpillai U, Walker D, Subakir SB. Localization of indoleamine 2,3-dioxygenase and 4-hydroxynonenal in normal and pre-eclamptic placentae. Placenta23(5), 373–379 (2002).
  • Borrego-Diaz E, Rosales JC, Proverbio T et al. Effect of placental hypoxia on the plasma membrane Ca-ATPase (PMCA) activity and the level of lipid peroxidation of syncytiotrophoblast and red blood cell ghosts. Placenta29(1), 44–50 (2008).
  • Gu Y, Burlison SA, Wang Y. PAF levels and PAF-AH activities in placentas from normal and preeclamptic pregnancies. Placenta27(6–7), 744–749 (2006).
  • Sawicki G, Dakour J, Morrish DW. Functional proteomics of neurokinin B in the placenta indicates a novel role in regulating cytotrophoblast antioxidant defence. Proteomics3(10), 2044–2051 (2003).
  • Cindrova-Davies T, Spasic-Boskovic O, Jauniaux E, Charnock-Jones DS, Burton GJ. Nuclear factor-B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress. Am. J. Pathol.170(5), 1511–1520 (2007).
  • Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH. Vitamins in Pre-eclampsia (VIP) Trial Consortium. Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomized placebo-controlled trial. Lancet367(9517), 1145–1154 (2006).
  • Campbell S, Park JH, Rowe J, Seeho SK, Morris JM, Gallery ED. Chorionic villus sampling as a source of trophoblasts. Placenta28(11–12), 1118–1122 (2007).
  • Kalionis B, Moses E. Advanced molecular techniques in pregnancy research: proteomics and genomics – a workshop report. Placenta17(Suppl. A), S119–S122 (2003).
  • Toft JH, Lian IA, Tarca AL et al. Whole-genome microarray and targeted analysis of angiogenesis-regulating gene expression (ENG, FLT1, VEGF, PlGF) in placentas from pre-eclamptic and small-for-gestational-age pregnancies. J. Matern. Fetal Neontal. Med.21(4), 267–273 (2008).
  • van Dijk M, Mulders J, Poutsma A et al. Maternal segregation of the Dutch preeclampsia locus at 10q22 with a new member of the winged helix gene family. Nat. Genet.37(5), 514–519 (2005).
  • Kivinen K, Peterson H, Hiltunen L et al. Evaluation of STOX1 as a preeclampsia candidate gene in a population-wide sample. Eur. J. Hum. Genet.15(4), 494–497 (2007).
  • Bainbridge SA, Belkacemi L, Dickinson M et al. Carbon monoxide inhibits hypoxia/reoxygenation-induced apoptosis and secondary necrosis in syncytiotrophoblast. Am. J. Pathol.169(3), 774–783 (2006).
  • Belkacemi L, Bainbridge SA, Dickinson MA et al. Glyceryl trinitrate inhibits hypoxia-reoxygenation-induced apoptosis in the syncytiotrophoblast of the human placenta. Am. J. Pathol.170(3), 909–920 (2007).

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