Altered protease expression by periarterial trophoblast cells in severe early-onset preeclampsia with IUGR
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Frank Reister
Abstract
Adaptation of uteroplacental arteries in patients with early-onset preeclampsia combined with IUGR is compromized due to insufficient invasion of extravillous trophoblast cells (EVT) into the spiral artery wall. The underlying molecular mechanisms are widely unknown. We investigated expression and possible mechanisms of regulation of different matrix-metalloproteases (MMPs) by EVT in placental bed biopsies from patients with early onset preeclampsia combined with IUGR and healthy pregnant women. Expression of MMP-3 and MMP-7 by EVT was markedly reduced in preeclamptic patients, especially close to spiral arteries. In contrast to healthy pregnancies these cells strongly expressed the receptor for leukemia inhibitory factor (LIF). LIF is known to suppress MMP-expression and is produced by uterine natural killer (uNK) cells which we found to be present in higher concentrations in the placental bed of preeclamptic patients, and accumulating aside the spiral arteries. We speculate that in preeclampsia a maternal immune cell network accumulating and interfering in the placental bed leads to an altered cytokine environment, resulting in disturbed trophoblast cell function such as impaired MMP expression and reduced invasiveness.
References
1 Bischof P, L Haenggeli, A Campana: Gelatinase and oncofetal fibronectin secretion is dependent on integrin expression of human cytotrophoblasts. Mol Hum Reprod10 (1995) 734Search in Google Scholar
2 Biswas R, H Sawhney, R Dass, RK Saran, K Vasishta: Histopathological study of placental bed biopsy in placenta previa. Acta Obstet Gynecol Scand78 (1999) 173Search in Google Scholar
3 Brosens IA, WB Robertson, HG Dixon: The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol93 (1967) 569Search in Google Scholar
4 Brosens IA, WB Robertson, HG Dixon: The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu1 (1972) 177Search in Google Scholar
5 Brosens IA, HG Dixon, WB Robertson: Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynecol84 (1977) 656Search in Google Scholar
6 Bulmer JN: Immune aspects of pathology of the placental bed contributing to pregnancy pathology. Baill Clin Obstet Gynaecol6 (1992) 46110.1016/S0950-3552(05)80006-9Search in Google Scholar
7 Cawston TE: Proteinases and Inhibitors. Br Med Bull51 (1995) 38510.1093/oxfordjournals.bmb.a072968Search in Google Scholar PubMed
8 Dalbeth N, R Gundle, RJ Davies, YC Lee, AJ McMichael, MF Callan, J: CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. Immunol173 (2004) 6418Search in Google Scholar
9 Feinberg RF, HJ Kliman, CJ Lookwood: Is oncofetal fibronectin a trophoblast glue for human implantation? Am J Pathol138 (1991) 537Search in Google Scholar
10 Graham CH, KR McCrae: Altered expression of gelatinase and surface-associated plasminogen activator activity by trophoblast cells isolated from placentas of preeclamptic patients. Am J Obstet Gynecol175 (1996) 555Search in Google Scholar
11 Herrler A, U von Rango, HM Beier: Embryo-maternal signalling: how the embryo starts talking to its mother to accomplish implantation. Reprod Biomed Online6 (2003) 244Search in Google Scholar
12 Hohenauer L: Intrauterine growth curves for German-speaking countries. Zeitschr Geburtsh Perinat184 (1980) 167Search in Google Scholar
13 Huppertz B, S Kertschanska, AY Demir, H-G Frank, P Kaufmann: Immunohistochemistry of MMP, their substrates, and their inhibitors (TIMP) during trophoblast invasion in the human placenta. Cell Tissue Res291 (1998) 133Search in Google Scholar
14 Huppertz B, HG Frank, F Reister, J Kingdom, H Korr, P Kaufmann: Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest79 (1999) 1687Search in Google Scholar
15 Jokhi PP, A King, AM Sharkey, SK Smith, YW Loke: Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction. J Immunol153 (1994) 4427Search in Google Scholar
16 Kadyrov M, JCP Kingdom, Huppertz: Divergent Trophoblast Invasion and Apoptosis in Placental Bed Spiral Arteries from Pregnancies Complicated by Maternal Anemia and Early-Onset Preeclampsia/IUGR. Am J Obstet Gynecol, in pressSearch in Google Scholar
17 Kamohara H, K Sakamoto, T Ishiko, Y Masuda, T Abe, M Ogawa: Leukemia inhibitory factor induces apoptosis and proliferation of human carcinoma cells through different oncogene pathways. Int J Cancer72 (1997) 687Search in Google Scholar
18 Kaufmann P, S Black, B Huppertz: Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod69 (2003) 1Search in Google Scholar
19 Konan KV, MW Taylor: Treatment of ME180 cells with interferon-gamma causes apoptosis as a result of tryptophan starvation. J Interferon Cytokine Res16 (1996) 751Search in Google Scholar
20 Lyall F, H Simpson, JN Bulmer, A Barber, SC Robson: Transforming growth factor-beta expression in human placenta and placental bed in third trimester normal pregnancy, preeclampsia, and fetal growth restriction. Am J Pathol159 (2001) 1827Search in Google Scholar
21 Marzusch K, F Buchholz, P Ruck, R Handgretinger, A Geiselhart, L Engelmann, J Dietl: Interleukin-12- and interleukin-2-stimulated release of interferon-γ by uterine CD56++ large granular lymphocytes is amplified by decidual macrophages. Hum Reprod12 (1997) 921Search in Google Scholar
22 Meekins JW, R Pijnenborg, M Hanssens, IR McFadyen, A van Asche: A study of placental bed spiral arteries and trophoblast invasion in normal and severe preeclamptic pregnancies. Br J Obstet Gynaecol101 (1994) 669Search in Google Scholar
23 Moll W, A Nienartowicz, H Hees, KH Wrobel, A Lenz: Blood flow regulation in the uteroplacental arteries. Troph Res3 (1988) 83Search in Google Scholar
24 Nachtigall MJ, HJ Kliman, RF Feinberg, DL Olive, O Engin, A Arici: The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. J Clin Endocrinol Metab81 (1996) 801Search in Google Scholar
25 Navrocki B, M Polette, V Marchand, E Maquoi, A Biorchia, J Tournier, JM Foidart, P Birembaut: Membrane-type matrix metalloproteinase-1 expression at the site of human placentation. Placenta17 (1996) 565Search in Google Scholar
26 Pijnenborg R, JM Bland, WB Robertson, HG Dixon: Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta4 (1983) 397Search in Google Scholar
27 Reister F, HG Frank, W Heyl, G Kosanke, B Huppertz, W Schroeder, P Kaufmann, W Rath: The distribution of macrophages in spiral arteries of the placental bed in preeclampsia differs from that in healthy patients. Placenta20 (1999) 229Search in Google Scholar
28 Reister F, HG Frank, JCP Kingdom, W Heyl, P Kaufmann, W Rath, B Huppertz: Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab Invest81 (2001) 1143Search in Google Scholar
29 Sawai K, N Matsuzaki, T Okada, K Shimoya, M Koyama, C Azuma, F Saji, Y Murata: Human decidual cell biosynthesis of leukemia inhibitory factor: regulation by decidual cytokines and steroid hormones. Biol Reprod56 (1997) 1274Search in Google Scholar
30 Schofield G, SJ Kimber: Leukocyte subpopulations in the uteri of leukemia inhibitory factor knockout mice during early pregnancy. Biol Reprod72 (2005) 872Search in Google Scholar
31 Sharkey AM, A King, DE Clark, TD Burrows, PP Jokhi, DS Charnock-Jones, YW Loke, SK Smith: Localization of leucemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol Reprod60 (1999) 355Search in Google Scholar
32 Stallmach T, G Hebisch, P Orban, X Lu: Aberrant positioning of trophoblast and lymphocytes in the feto-maternal interface with preeclampsia. Virchows Arch43 (1999) 207Search in Google Scholar
33 Tarrade A, F Goffin, C Munaut, F Lai-Kuen, V Tricottet, J-M Foidart, M Vidaud, F Frankenne, D Evain-Brion: Effect of Matrigel on human extravillous trophoblasts differentiation: modulation of protease pattern gene expression. Biol Reprod67 (2002) 1628Search in Google Scholar
34 Von Rango U, CA Krusche, S Kertschanska, J Alfer, P Kaufmann, HM Beier: Apoptosis of extravillous trophoblast cells limits the trophoblast invasion in uterine but not in tubal pregnancy during first trimester. Placenta24 (2003) 929Search in Google Scholar
35 Werner-Felmayer G, ER Werner, D Fuchs, A Hausen, D Reibnegger, A Wachter: Tumour necrosis factor-alpha and lipopolysaccharide enhance interpheron-induced tryptophan degradation and pteridine synthesis in human cells. Biol Chem Hoppe Seyler370 (1989) 1063Search in Google Scholar
©2006 by Walter de Gruyter Berlin New York
Articles in the same Issue
- Advances in Perinatal Medicine - 5th Annual meeting of the Italian Society of Perinatal Medicine held in Parma, Italy on June 15th – 17th 2006
- Hemorrhagic shock in obstetrics
- Altered protease expression by periarterial trophoblast cells in severe early-onset preeclampsia with IUGR
- Gestational diabetes mellitus in patients receiving long-term corticosteroid therapy during pregnancy
- Accuracy and influence of ascorbic acid on glucose-test with urine dip sticks in prenatal care
- Protein C, protein S, and thrombomodulin in amniotic fluid. A preliminary study
- Timing of cord clamping revisited
- Intrapartum cardiotocography – the dilemma of interpretational variation
- Maturation of the autonomic nervous system: differences in heart rate variability in premature vs. term infants
- Four chamber view plus three-vessel and trachea view for a complete evaluation of the fetal heart during the second trimester
- Pleural fluid/serum immunoglobulin ratio is a diagnostic marker for congenital chylothorax in utero
- Fetal brain sparing is strongly related to the degree of increased placental vascular impedance
- Outcome of fetuses in women with pregestational diabetes mellitus
- Outcome of fetuses in women with pregestational diabetes mellitus
- Inhaled nitric oxide therapy might reduce the need for hyperventilation therapy in infants with persistent pulmonary hypertension of the newborn
- To drain or not to drain: a single institution experience with neonatal intestinal perforation
- Infective puerperal endocarditis caused by Escherichia coli
- Correlation between plasma and urinary caffeine levels in preterm infants
- Fetal ascites secondary to urinary hydrocolpos
- Congress Calendar
- Suppression of IL-2 and IFN-γ production in women with spontaneous preterm labor
Articles in the same Issue
- Advances in Perinatal Medicine - 5th Annual meeting of the Italian Society of Perinatal Medicine held in Parma, Italy on June 15th – 17th 2006
- Hemorrhagic shock in obstetrics
- Altered protease expression by periarterial trophoblast cells in severe early-onset preeclampsia with IUGR
- Gestational diabetes mellitus in patients receiving long-term corticosteroid therapy during pregnancy
- Accuracy and influence of ascorbic acid on glucose-test with urine dip sticks in prenatal care
- Protein C, protein S, and thrombomodulin in amniotic fluid. A preliminary study
- Timing of cord clamping revisited
- Intrapartum cardiotocography – the dilemma of interpretational variation
- Maturation of the autonomic nervous system: differences in heart rate variability in premature vs. term infants
- Four chamber view plus three-vessel and trachea view for a complete evaluation of the fetal heart during the second trimester
- Pleural fluid/serum immunoglobulin ratio is a diagnostic marker for congenital chylothorax in utero
- Fetal brain sparing is strongly related to the degree of increased placental vascular impedance
- Outcome of fetuses in women with pregestational diabetes mellitus
- Outcome of fetuses in women with pregestational diabetes mellitus
- Inhaled nitric oxide therapy might reduce the need for hyperventilation therapy in infants with persistent pulmonary hypertension of the newborn
- To drain or not to drain: a single institution experience with neonatal intestinal perforation
- Infective puerperal endocarditis caused by Escherichia coli
- Correlation between plasma and urinary caffeine levels in preterm infants
- Fetal ascites secondary to urinary hydrocolpos
- Congress Calendar
- Suppression of IL-2 and IFN-γ production in women with spontaneous preterm labor