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Trophoblast function in normal and preeclamptic pregnancy

Published online by Cambridge University Press:  15 January 2010

James C Cross*
Affiliation:
Mount Sinai Hospital and Departments of Obstetrics and Gynaecology and Medical Genetics, University of Toronto, Canada
*
James Cross, Program in Development and Fetal Health, Samuel Lunenfeld Research Institute, Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario, M5G 1X5, Canada.

Extract

Preeclampsia (PE) is a common disease of pregnancy that affects women particularly in their first pregnancies. Current estimates suggest that between 7 and 10% of pregnancies may be complicated by PE. Despite considerable research and medical efforts, the incidence of the disease has not changed substantially in the last century. In severe cases the disease may be life-threatening and is associated with high neonatal mortality and morbidity. Furthermore, therapy is often ineffective and at best treats the disease symptoms rather than the aetiology. One reason for the lack of progress may be that while the disease is generally agreed by most to be due to abnormal implantation and development of the placenta (events which happen in the first trimester) most research efforts have focused on managing and understanding the maternal disease. Since the disease typically appears in the last trimester, many weeks after the likely start of the pathology, it has been difficult to understand the progression of events. However, this picture has improved recently. The purpose here is to review how placental development is affected in PE and describe new insights into the causes. It is hoped that an understanding of the pathogenesis of the placental defects in PE will lead to new efforts towards early diagnosis, before the onset of clinical symptoms, as well as new treatments for these lesions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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References

1Roberts, JM, Taylor, RN, Friedman, SA, Goldfien, A. New developments in preeclampsia. Fetal and maternal medicine review 1990; 2: 125141.CrossRefGoogle Scholar
2 Redman CW. Current topic: preeclampsia and the placenta. Placenta 1991; 12: 301308.Google Scholar
3Roberts, JM, Taylor, RN, Musei, TJ, Rodgers, GM, Hubel, CA, McLaughlin, MK. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 1989; 161: 1200–204.CrossRefGoogle ScholarPubMed
4Cross, JC, Werb, Z, Fisher, SJ. Implantation and the placenta: key pieces of the development puzzle. Science 1994; 266: 1508–518.CrossRefGoogle ScholarPubMed
5Fisher, SJ, Damsky, CH. Human cytotrophoblast invasion. Semin Cell Biol 1993; 4: 183–88.CrossRefGoogle ScholarPubMed
6Fisher, SJ, Cui, T-Y, Zhang, L, Hartman, L, Grahl, K, Zhang, G-Y et al. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 1989; 109: 891902.CrossRefGoogle ScholarPubMed
7Genbacev, O, White, TEK, Gavin, CE, Miller, RK. Human trophoblast cultures: models for implantation and peri-implantation toxicology. Repród Toxicol 1993; 7: 7594.Google Scholar
8Damsky, CH, Fitzgerald, ML, Fisher, SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway in vivo. J Clin Invest 1992; 89: 210–22.Google Scholar
9Damsky, CH, Librach, C, Lim, KH, Fitzgerald, ML, McMaster, MT, Janatpour, M et al. Integrin switching regulates normal trophoblast invasion. Development 1994; 120: 3657–66.CrossRefGoogle ScholarPubMed
10Librach, CL, Werb, Z, Fitzgerald, ML, Chiu, K, Corwin, NM, Esteves, RA et al. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 1991; 113: 437–49.CrossRefGoogle ScholarPubMed
11Pijnenborg, R, Dixon, G, Robertson, WB, Brosens, I. Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980; 1: 319.Google Scholar
12Moore, KL, Persaud, TVN, Shiota, K. Placenta and fetal membranes. Color atlas of clinical embryology. Toronto Canada: WB Saunders Company, 1994: 79104.Google Scholar
13Jaffe, R, Genbacev, O. In vivo assessment of the early uteroplacental circulation. Am J Obstet Gynecol 1993; 169: 1077.Google Scholar
14Jaffe, R, Dorgan, A, Abramowicz, JS. Color Doppler imaging of the uteroplacental circulation in the first trimester: value in predicting pregnancy failure or complication. Am J Roentgenol 1995; 164: 1255–58.CrossRefGoogle ScholarPubMed
15Jauniaux, E, Zaidi, J, Jurkovic, D, Campbell, S, Hustin, J. Comparison of colour Doppler features and pathological findings in complicated early pregnancy. Hum Repród 1994; 9: 2432–37.Google Scholar
16Kurjak, A, Zudenigo, D, Funduk-Kurjak, B, Shalan, H, Predanie, M, Sosie, A. Transvaginal color Doppler in the assessment of the uteroplacental circulation in normal early pregnancy. J Perinat Med 1993; 21: 2534.CrossRefGoogle ScholarPubMed
17Jauniaux, E, Jurkovic, D, Campbell, S, Hustin, J. Doppler ultrasonographic features of the developing placental circulation: correlation with anatomic findings. Am J Obstet Gynecol 1992; 166: 585–87.Google Scholar
18Jurkovic, D, Jauniaux, E, Kurjak, A, Hustin, J, Campbell, S, Nicolaides, KH. Transvaginal color Doppler assessment of the uteroplacental circulation in early pregnancy. Obstet Gynecol 1991; 77: 365–69.Google Scholar
19Thaler, I, Manor, D, Itskovitz, J, Rottem, S, Levit, N, Timor-Tritsch, I et al. Changes in uterine blood flow during human pregnancy. Am J Obstet Gynecol 1990; 162: 121–25.Google Scholar
20Matijevic, R, Meekins, JW, Walkinshaw, SA, Neilson, JP, McFadyen, IR. Spiral artery blood flow in the central and peripheral areas of the placental bed in the second trimester. Obstet Gynecol 1995; 86: 289–92.Google Scholar
21Curran-Everett, D, Morris, KG, Moore, LG. Regional circulatory contributions to increased systemic vascular conductance of pregnancy. Am J Physiol 1991; 261 H184247.Google ScholarPubMed
22Malassine, A, Cronier, L, Mondón, F, Mignot, TM, Ferre, F. Localization and production of immunoreactive endothelin-1 in the trophoblast of human placenta. Cell Tissue Res 1993; 271: 491–97.Google Scholar
23Ferre, F, Mondón, D, Mignot, TM, Cronier, L, Caverò, I, Rostené, W et al. Endothelin-1 binding sites and immunoreactivity in the cultured human placental trophoblast: evidence for an autocrine and paracrine role for endothelin-1. J Cardiovasc Pharmacol 1993; 22 (Suppl. 8): S21418.Google Scholar
24Myatt, L. Current topic: control of vascular resistance in the human placenta. Placenta 1992; 13: 329–41.CrossRefGoogle Scholar
25Magann, EF, Martin, JN. The laboratory evaluation of hypertensive grávidas. Obstet Gynecol Surv 1995; 50: 138–45.Google Scholar
26Redman, CW. Platelets and the beginnings of preeclampsia. N Engl J Med 1990; 323: 478–80.CrossRefGoogle ScholarPubMed
27Friedman, SA, Taylor, RN, Roberts, JM. Pathophysiology of preeclampsia. Clin Perinatol 1991; 18: 661–82.CrossRefGoogle ScholarPubMed
28Brown, MA. The physiology of preeclampsia. Clin Exp Pharmacol Physiol 1995; 22: 781–91.Google Scholar
29Eskenazi, B, Fenster, L, Sidney, S. A multivariate analysis of risk factors for preeclampsia. JAMA 1991; 266: 237–1.CrossRefGoogle ScholarPubMed
30Sibai, BM, Gordon, T, Thorn, E, Caritis, SN, Klebanoff, M, McNellis, D et al. Risk factors for preeclampsia in healthy nulliparous women: a prospective multicenter study. The National Institute of Child Health and Human Development Network of Maternal-Fetal Medicine Units. Am J Obstet Gynecol 1995; 172: 642–48.Google Scholar
31Arngrimsson, R, Bjornsson, H, Geirsson, RT. Analysis of different inheritance patterns in preeclampsia/eclampsia syndrome. Hypertens Pregnancy 1995; 14: 2738.CrossRefGoogle Scholar
32Ward, K, Hata, A, Jeunemaitre, X, Helin, C, Nelson, L, Namikawa, C et al. A molecular variant of angiotensinogen associated with preeclampsia. Nat Genet 1993; 4: 5961.Google Scholar
33Zamudio, S, Droma, T, Norkyel, KY, Acharya, G, Zamudio, JA, Niermeyer, SN et al. Protection from intrauterine growth retardation in Tibetans at high altitude. Am J Phys Anthropol 1993; 91: 215–24.Google Scholar
34Reshetnikova, OS, Burton, GJ, Milovanov, AP. Effects of hypobaric hypoxia on the fetoplacental unit: the morphometric diffusing capacity of the villous membrane at high altitude. Am J Obstet Gynecol 1994; 171: 1560–65.Google Scholar
35Arnholdt, H, Meisel, F, Fandrey, K, Lohrs, U. Proliferation of villous trophoblast of the human placenta in normal and abnormal pregnancies. Virchows Archiv B Cell Pathol incl Mol Pathol 1991; 60: 365–72.Google Scholar
36Genbacev, O, Bass, KE, Joslin, RJ, Fisher, SJ. Maternal smoking inhibits early human cytotrophoblast differentiation. Repród Toxicol 1995; 9: 245–55.CrossRefGoogle ScholarPubMed
37Teasdale, F, Ghislaine, J-J. Morphological changes in the placentas of smoking mothers: a histomorphometric study. Biol Neonate 1989; 55: 251–59.Google Scholar
38Spinillo, A, Capuzzo, E, Egbe, TO, Nicola, S, Piazzi, G, Baltaro, F. Cigarette smoking in pregnancy and risk of pre-eclampsia. J Hum Hyper tens 1994; 8: 771–75.Google Scholar
39Klonoff-Cohen, H, Edelstein, S, Savitz, D. Cigarette smoking and preeclampsia. Obstet Gynecol 1993; 81: 541–44.Google Scholar
40Redman, CW. Immunological aspects of preeclampsia. Baillieres Clin Obstet Gynaecol 1992; 6: 601–15.Google Scholar
41Teasdale, F. Histomorphometry of the human placenta in maternal preeclampsia. Am J Obstet Gynecol 1985; 152: 2531.Google Scholar
42Fox, H. The villous cytotrophoblast as an index of placental ischaemia. J Obstet Gynaecol Br Commonw 1964; 71: 885–93.Google Scholar
43Redline, RW, Patterson, P. Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Hum Pathol 1995; 26: 594600.Google Scholar
44Jones, CJP, Fox, H. An ultrastructural and ultrahistochemical study of the human placenta in maternal pre-eclampsia. Placenta 1980; 1: 6176.CrossRefGoogle ScholarPubMed
45Jackson, MR, Walsh, AJ, Morrow, RJ, Mullen, JB, Lye, SJ, Ritchie, JW. Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms. Am J Obstet Gynecol 1995; 172: 518–25.Google Scholar
46Fuke, Y, Aono, T, Imai, S, Suehara, N, Fujita, T, Nakayama, M. Clinical significance and treatment of massive intervillous fibrin deposition associated with recurrent fetal growth retardation. Gynecol Obstet Invest 1994; 38: 59.CrossRefGoogle ScholarPubMed
47Robertson, WB, Brosens, I, Dixon, G. Uteroplacental vascular pathology. Eur J Obstet Gynecol Repród Biol 1975; 5: 4765.Google Scholar
48Gerretsen, G, Huisjes, HJ, Elema, JD. Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol 1981; 88: 876–81.Google Scholar
49Khong, TY, DeWolf, F, Robertson, WB, Brosens, I. Inadequate maternal vascular response to placentation in pregnancies complicated by preeclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93: 1049–59.Google Scholar
50Brosens, IA, Robertson, WB, Dixon, HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Ann 1972; 1: 177–91.Google Scholar
51Lin, S, Shimizu, I, Suehara, N, Nakayama, M, Aono, T. Uterine artery Doppler velocimetry in relation to trophoblast migration into the myometrium of the placental bed. Obstet Gynecol 1995; 85: 760–65.Google Scholar
52Iwata, M, Matsuzaki, N, Shimizu, I, Mitsuda, N, Nakayama, M, Suehara, N. Prenatal detection of ischemie changes in the placenta of the growth-retarded fetus by Doppler flow velocimetry of the maternal uterine artery. Obstet Gynecol 1993; 82: 494–99.Google Scholar
53Khong, TY, Sawyer, IH, Heryet, AR. An immunohistologic study of endothelialization of uteroplacental vessels in human pregnancy. Evidence that endothelium is focally disrupted by trophoblast in preeclampsia. Am J Obstet Gynecol 1992; 167: 751–56.Google Scholar
54Zhou, Y, Dámsky, CH, Chiù, K, Roberts, JM, Fisher, SJ. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 1993; 91: 950–6O.Google Scholar
55Lim, KH, Dámsky, C, Fisher, SJ. Differentiation of invasive cytotrophoblasts in normal and abnormal pregnancy. Soc Gynecol Invest 1993; abstract no. S166. .Google Scholar
56Roberts, JM, Taylor, RN, Goldfen, A. Clinical and biochemical evidence of endothelial cell dysfunction in the pregnancy syndrome preeclampsia. Am J Hypertens 1991; 4: 700708.Google Scholar
57Zeeman, GG, Dekker, GA. Pathogenesis of preeclampsia: a hypothesis. Clin Obstet Gynecol 1992; 35: 317–37.Google Scholar
58Rodesch, F, Simon, P, Donner, C, Jauniaux, E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992; 80: 283–85.Google ScholarPubMed
59Watson, AL, Palmer, ME, Burton, GJ. Problems associated with oxygen tension in the maintenance of first trimester placental tissue in organ culture. Placenta 1995; 16: A.75.Google Scholar
60Janatpour, MJ, Israel, MA, Fisher, SJ. The transcriptional negative regulator Id-2 can control MMP-9 expression. Mol Biol Cell 1995; Suppl 6: 304a, abstract 1768.Google Scholar
61Tominaga, T, Page, E. Accommodation of the human placenta to hypoxia. Am J Obstet Gynecol 1966; 94: 679–91.Google Scholar
62MacLennan, AH, Sharp, F, Shaw-Dunn, J. The ultrastructure of human trophoblast in spontaneous and induced hypoxia using a system of organ culture: a comparison with ultrastructural changes in pre-eclampsia and placental insufficiency. J Obstet Gynaecol Br Commonw 1912; 79: 113–21.Google Scholar
63Karimu, AL, Burton, GJ. Significance of changes in fetal perfusion pressure to factors controlling angiogenesis in the human term placenta. J Repród Fértil 1994; 102: 447–50.Google Scholar
64Lunell, NO, Nylund, LE, Lewlander, R, Sarby, B. Uteroplacental blood flow in pre-eclampsia. Measurements with indium-113m and a computer-linked gamma camera. Clin Exp Hypertens f Part B] 1982; 1: 105–17.Google Scholar
65Kraayenbrink, AA, Dekker, GA, van Kamp, GJ, van Geijn, HP. Endothelial vasoactive mediators in preeclampsia. Am J Obstet Gynecol 1993; 169: 160–65.Google Scholar
66Vince, GS, Starkey, PM, Austgulen, R, Kwiatkowski, D, Redman, CW. Interleukin-6, tumour necrosis factor and soluble tumour necrosis factor receptors in women with preeclampsia. Br J Obstet Gynaecol 1995; 102: 2025.Google Scholar
67Pahl, HL, Baeuerle, PA. Oxygen and the control of gene expression. Bioessays 1994; 16: 497502.CrossRefGoogle ScholarPubMed
68Endresen, MJ, Lorentzen, B, Henriksen, T. Increased lipolytic activity and high ratio of free fatty acids to albumin in sera from women with preeclampsia leads to triglycéride accumulation in cultured endothelial cells. Am J Obstet Gynecol 1992; 167: 440–47.Google Scholar
69Lorentzen, B, Drevôn, CA, Endresen, MJ, Henriksen, T. Fatty acid pattern of esterified and free fatty acids in sera of women with normal and pre-eclamptic pregnancy: Br J Obstet Gynaecol 1995; 102: 530–37.Google Scholar
70Walsh, SW, Wang, Y. Trophoblast and placental villous core production of lipid peroxides, thromboxane, and prostacyclin in preeclampsia. J Clin Endocrinol Metab 1995; 80: 1888–93.Google ScholarPubMed
71Johnson, MR, Riddle, AF, Grundzinskas, JG, Sharma, V, Collins, WP, Nicolaides, KH. The role of trophoblast dysfunction in the aetiology of miscarriage. Br J Obstet Gynaecol 1993; 100: 353–59.Google Scholar
72Jaffe, R. Investigation of abnormal first-trimester gestations by color Doppler imaging. J Clin Ultrasound 1993; 21: 521–26.Google Scholar
73Kurjak, A, Zudenigo, D, Predanie, M, Kupesic, S, Funduk, B. Assessment of the fetomaternal circulation in threatened abortion by transvaginal color Doppler. Fetal Diagn Ther 1994; 9: 341–47.Google Scholar
74Khong, TY, Liddell, HS, Robertson, WB. Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol 1987; 94: 649–55.CrossRefGoogle ScholarPubMed
75De Wolf, F, Brosens, I, Renaer, M. Fetal growth retardation and the maternal arterial supply of the human placenta in the absence of sustained hypertension. Br J Obstet Gynaecol 1980; 87: 678–85.CrossRefGoogle ScholarPubMed
76Brosens, I, Dixon, HG, Robertson, WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977; 84: 656–63.CrossRefGoogle ScholarPubMed
77Althabe, O, Labarrere, C, Telenta, M. Maternal vascular lesions in placentae of small-for-gestational infants. Placenta 1985; 6: 265–76.Google Scholar
78Jones, CJP, Fox, H. An ultrastructural and ultrahistochemical study of the human placenta in maternal essential hypertension. Placenta 1981; 2: 193204.Google Scholar
79Naeye, RL. Pregnancy hypertension, placental evidences of low uteroplacental blood flow and spontaneous premature delivery. Hum Pathol 1989; 20: 441–44.CrossRefGoogle ScholarPubMed
80Strigini, FA, Lencioni, G, De Luca, G, Lombardo, M, Bianchi, F, Genazzani, AR. Uterine artery velocimetry and spontaneous preterm delivery. Obstet Gynecol 1995; 85: 374–77.Google Scholar
81Nicotra, M, Muttinelli, C, Sbracia, M, Rolfi, G, Passi, S. Blood levels of lipids, lipoperoxides, vitamin E and glutanthione peroxidase in women with habitual abortion. Gynecol Obstet Invest 1994; 38: 223–26.Google Scholar
82Zhou, Y, Chiù, K, Brescia, RJ, Combs, CA, Katz, MA, Kitzmiller, JL et al. Increased depth of trophoblast invasion after chronic constriction of the lower aorta in rhesus monkeys. Am J Obstet Gynecol 1993; 169: 224–29.Google Scholar
83Hoffman, LH, Wooding, FBP. Giant and binucleate trophoblast cells of mammals. J Exp Zool 1993; 266: 559–77.Google Scholar
84McKay, DG, Goldenberg, V, Kaunitz, H, Csavossy, I. Experimental eclampsia: an electron microscope study and review. Arch Path 1967; 84: 557–97.Google Scholar
85Faas, MM, Schuiling, GA, Baller, JFW, Visscher, CA, Bakker, WW. A new animal model for human preeclampsia: ultra-low-dose endotoxin infusion in pregnant rats. Am J Obstet Gynecol 1994; 171: 158–64.CrossRefGoogle ScholarPubMed
86Chari, RS, Friedman, SA, Sibai, BM. Antihypertensive therapy during pregnancy. Fet Mat Med Rev 1995; 7: 6175.Google Scholar
87Brennecke, SP, Brown, MA, Crowther, CA, Hague, WM, King, J, McCowan, L et al. Aspirin and prevention of preeclampsia. Position statement of the use of low-dose aspirin in pregnancy by the Australasian Society for the Study of Hypertension in Pregnancy. Aust N Z J Obstet Gynaecol 1995; 35: 3841.Google Scholar
88Dekker, GA, Sibai, BM. Low-dose aspirin in the prevention of preeclampsia and fetal growth retardation: rationale, mechanisms and clinical trials. Am J Obstet Gynecol 1993; 168: 214–27.Google Scholar
89Uotila, JT, Tuimala, RJ, Aarnio, TM, Pyykko, KA, Ahotupa, MO. Findings on lipid peroxidation and antioxidant function in hypertensive complications of pregnancy. Br J Obstet Gynaecol 1993; 100: 270–76.Google Scholar
90Valsecchi, L, Fausto, A, Grazioli, V. Severe preeclampsia and antioxidant nutrients. Am J Obstet Gynecol 1995; 173: 773–74.CrossRefGoogle ScholarPubMed
91Bower, S, Bewley, S, Campbell, S. Improved prediction of preeclampsia by two-stage screening of uterine arteries using the early diastolic notch and color Doppler imaging. Obstet Gynecol 1993; 82: 7883Google ScholarPubMed