Endovascular trophoblast invasion: Implications for the pathogenesis of intrauterine growth retardation and preeclampsia

Biology of Reproduction

Volumn 69, Issue 1, 2003, Pages 1-7

  Kaufmann, Peter ^a,b   Black, Simon ^a   Huppertz, Berthold ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

Apoptosis; Early development; Placenta; Syncytiotrophoblast; Trophoblast

Indexed keywords

CELL ADHESION MOLECULE; NITRIC OXIDE; SELECTIN;

APOPTOSIS; ARTERY DILATATION; CELL INVASION; ENDOTHELIUM CELL; GENE EXPRESSION; INTRAUTERINE GROWTH RETARDATION; MACROPHAGE ACTIVATION; PATHOGENESIS; PLACENTA; PLACENTA CIRCULATION; PREECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; SHORT SURVEY; TROPHOBLAST; VASCULAR RESISTANCE; VASOMOTOR REFLEX;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; APOPTOSIS; FEMALE; FETAL GROWTH RETARDATION; HUMANS; MACROPHAGE ACTIVATION; MODELS, BIOLOGICAL; NITRIC OXIDE; PLACENTA; PLACENTAL CIRCULATION; PRE-ECLAMPSIA; PREGNANCY; TROPHOBLASTS; UTERUS; VASCULAR RESISTANCE;

ANIMALIA;

EID: 0038113155     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.102.014977     Document Type: Short Survey

References (57)

1. Brosens IA, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 1967; 93:569-579.
2. Moll W, Nienartowicz A, Hees H, Wrobel K-H, Lenz A. Blood flow regulation in the uteroplacental arteries. Trophoblast Res 1988; 3:83-96.
3. Benirschke K, Kaufmann P. Pathology of the Human Placenta, 4th ed. New York: Springer; 2000.
4. Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972; 1: 177-191.
5. Brosens IA, Dixon HG, Robertson WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977; 84:656-663.
6. Craven CM, Morgan T, Ward K. Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta 1998; 19:241-252.
7. Hees H, Moll W, Wrobel KH, Hees I. Pregnancy-induced structural changes and trophoblastic invasion in the segmental mesometrial arteries of the guinea pig (Cavia porcellus L). Placenta 1987; 8:609-626.
8. Nanaev AK, Chwalisz K, Frank HG, Kohnen G, Hegele-Hartung C, Kaufmann P. Physiological dilation of uteroplacental arteries in the guinea pig depends on nitric oxide synthase activity of extravillous trophoblast. Cell Tissue Res 1995; 282:407-421.
9. Hirano H, Imai Y, Ito H. Spiral artery of placenta: development and pathology: immunohistochemical, microscopical, and electron-microscopic study. Kobe J Med Sci 2002; 48:13-23.
10. Robertson WB. Uteroplacental vasculature. J Clin Pathol 1976; 29(suppl):9-17.
11. Robertson WB, Manning PJ. Elastic tissue in uterine blood vessels. J Pathol 1974; 112:237-243.
12. Tuttle SE, O'Toole RV, O'Shaughnessy RW, Zuspan FP. Immunohistochemical evaluation of human placental implantation: an initial study. Am J Obstet Gynecol 1985; 153:239-244.
13. Brosens IA. The uteroplacental vessels at term: the distribution and extent of physiological changes. Trophoblast Res 1988; 3:61-68.
14. Blankenship TN, Enders AC, King BF. Trophoblastic invasion and the development of uteroplacental arteries in the macaque: immunohistochemical localization of cytokeratins, desmin, type IV collagen, laminin, and fibronectin. Cell Tissue Res 1993; 272:227-236.
15. Pijnenborg R, Bland JM, Robertson WB, Brosens IA. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983; 4:397-413.
16. Damsky 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; 89:210-222.
17. Fisher SJ, Damsky CH. Human cytotrophoblast invasion. Semin Cell Biol 1993; 4:183-188.
18. Kam EPY, Gardner L, Loke YW, King A. The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod 1999; 14:2131-2138.
19. Craven CM, Zhao L, Ward K. Lateral placental growth occurs by trophoblast cell invasion of decidual veins. Placenta 2000; 21:160-169.
20. King BF, Blankenship TN. Expression of proliferating cell nuclear antigen (PCNA) in developing macaque placentas. Placenta 1993; 14: A36.
21. Bravo R, Macdonald-Bravo H. Existence of two populations of cyclin/ proliferating cell nuclear antigen during the cell cycle: associated with DANN replication sites. J Cel Biol 1987; 105:1549-1554.
22. Kaufmann P, Castellucci M. Extravillous trophoblast in the human placenta. Trophoblast Res 1997; 10:21-65.
23. Vicovac L, Aplin JD. Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat 1996; 156:202-216.
24. Merviel P, Challier JC, Carbillon L, Foidart JM, Uzan S. The role of integrins in human embryo implantation. Fetal Diagn Ther 2001; 16: 364-371.
25. Zhou Y, Fisher SJ, Janatpour MJ, Genbacev O, Dejana E, Wheelock M, Damsky CH. Human cytotrophoblasts adopt a vascular phenotype as they differentiate: a strategy for successful endovascular invasion? J Clin Invest 1997; 99:2139-2151.
26. Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype: one cause of defective endovascular invasion in this syndrome? J Clin Invest 1997; 99:2152-2164.
27. Lyall F, Bulmer JN, Duffie E, Cousins F, Theriault A, Robson SC. Human trophoblast invasion and spiral artery transformation: the role of PECAM-1 in normal pregnancy, preeclampsia, and fetal growth restriction. Am J Pathol 2001; 158:1713-1721.
28. Divers MJ, Bulmer JN, Miller D, Lilford RF. Beta 1 integrins in third trimester human placentae: no differential expression in pathological pregnancy. Placenta 1995; 16:245-260.
29. Floridon C, Nielsen O, Holund B, Sunde L, Westergaard JG, Thomsen SG, Teisner B. Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy. Mol Hum Reprod 2000; 6:943-950.
30. King A, Loke YW. Differential expression of blood-group-related carbohydrate antigens by trophoblast subpopulations. Placenta 1988; 9: 513-521.
31. Burrows TD, King A, Loke YW. Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: implications for vascular invasion during implantation. Placenta 1994; 15:21-33.
32. Takada A, Ohmori K, Yoneda T, Tsuyuoka K, Hasegawa A, Kiso M, Kannagi R. Contribution of carbohydrate antigens sialyl Lewis A and sialyl Lewis X to adhesion of human cancer cells to vascular endothelium. Cancer Res 1993; 53:354-361.
33. Pijnenborg R, Dixon GH, Robertson WB, Brosens IA. Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980; 1:3-19.
34. Nanaev AK, Kosanke G, Reister F, Kemp B, Frank HG, Kaufmann P. Pregnancy-induced de-differentiation of media smooth muscle cells in uteroplacental arteries of the guinea pig is reversible after delivery. Placenta 2000; 21:306-312.
35. Lyall F, Bulmer JN, Kelly H, Duffie E, Robson SC. Human trophoblast invasion and spiral artery transformation: the role of nitric oxide. Am J Pathol 1999; 154:1105-1114.
36. Martin D, Conrad KP. Expression of endothelial nitric oxide synthase by extravillous trophoblast cells in the human placenta. Placenta 2000; 21:23-31.
37. Cartwright JE, Holden DP, Whitley GS. Hepatocyte growth factor regulates human trophoblast motility and invasion: a role for nitric oxide. Br J Pharmacol 1999; 128:181-189.
38. Chwalisz K, Ciesla I, Garfield RE. Inhibition of nitric oxide (NO) synthesis induces preterm parturition and preeclampsia-like conditions in guinea pigs. In: Program of the 41st Meeting of the Society of Gynecologic Investigation; 1994; Chicago, IL. Abstract O 36.
39. Garfield RE, Yallampalli C, Buhimschi IA, Chwalisz K. Reversal of preeclampsia symptoms induced in rats by nitric oxide inhibition with L-arginine, steroid hormones and an endothelin antagonist. In: Program of the 41st Meeting of the Society of Gynecologic Investigation; 1994; Chicago, IL. Abstract P 384.
40. Bulmer JN, Johnson PM. Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 1984; 57:393-403.
41. Reister F, Frank HG, Heyl W, Kosanke G, Huppertz B, Schroder W, Kaufmann P, Rath W. The distribution of macrophages in spiral arteries of the placental bed in pre-eclampsia differs from that in healthy patients. Placenta 1999; 20:229-233.
42. Loke YW, King A. Human Implantation-Cell Biology and Immunology. Cambridge: Cambridge University Press; 1995.
43. Hunt JS. The role of macrophages in the uterine response to pregnancy. Placenta 1990; 11:467-475.
44. Hunt JS. Macrophages in human uteroplacental tissues: a review. Am J Reprod Immunol 1989; 21:119-122.
45. Yui J, Hemmings D, Garcia Lloret MI, Guilbert LJ. Expression of the human p55 and p75 tumor necrosis factor receptors in primary villous trophoblasts and their role in cytotoxic signal transduction. Biol Reprod 1996; 55:400-409.
46. Yui J, Garcia-Lloret MI, Wegmann TG, Guilbert LJ. Cytotoxicity of tumour necrosis factor-alpha and gamma-interferon against primary human placental trophoblasts. Placenta 1994; 15:819-835.
47. Reister F, Frank HG, Kingdom JCP, Heyl W, Kaufmann P, Rath W, Huppertz B. Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab Invest 2001; 81:1143-1152.
48. Miller L, Alley EW, Murphy WJ, Russell SW, Hunt JS. Progesterone inhibits inducible nitric oxide synthase gene expression and nitric oxide production in murine macrophages. J Leukocyte Biol 1996; 59: 442-450.
49. Zhou Y, Genbacev O, Damsky CH, Fisher SJ. Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. J Reprod Immunol 1998; 39:197-213.
50. Caniggia I, Grisaru-Gravnosky S, Kuliszewsky M, Post M, Lye SJ. Inhibition of TGF-beta (3) restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J Clin Invest 1999; 103:1641-1650.
51. Caniggia I, Winter J, Lye SJ, Post M. Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta 2000; 21:S25-S30.
52. Kadyrov M, Schmitz C, Black S, Kaufmann P, Huppertz B. Pre-eclampsia and maternal anemia display reduced apoptosis and opposite invasive phenotypes of extravillous trophoblast. Placenta; (in press).
53. DiFederico E, Genbacev O, Fisher SJ. Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall. Am J Pathol 1999; 155:293-301.
54. Aplin JD. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991; 99:681-692.
55. Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 2002; 187:1416-1423.
56. Ashkar AA, Di Santo JP, Croy BA. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 2000; 192:259-270.
57. Cartwright JE, Kenny LC, Dash PR, Crocker IP, Aplin JD, Baker PN, Whitley GS. Trophoblast invasion of spiral arteries: a novel in vitro model. Placenta 2002; 23:232-235.