Human trophoblast invasion and spiral artery transformation. The role of nitric oxide

American Journal of Pathology

Volumn 154, Issue 4, 1999, Pages 1105-1114

  Lyall, Fiona ^a,c   Bulmer, Judith Nicola ^b   Kelly, Helena ^a   Duffie, Elizabeth ^a   Robson, Stephen Courtenay ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c Medical Genetics   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ARTERY DILATATION; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOTROPHOBLAST; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RETARDATION; PLACENTA; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPONTANEOUS ABORTION; THIRD TRIMESTER PREGNANCY; TROPHOBLAST; UTERINE ARTERY; WESTERN BLOTTING;

EID: 0032903970     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65363-1     Document Type: Article

References (44)

1. Pijnenborg R, Bland JM, Robertson WB, Brosens I: Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983, 4:397-414
2. Brosens I, Robertson WB, Dixon HG: The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 1967, 93:569-579
3. Khong TY, Liddell HS, Robertson WB: Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol 1987, 94:649-655
4. Khong TY: Growth: Fetus and Neonate. Edited by M Hanson, J Spencer, C Rodeck. Cambridge, Cambridge University Press, 1995
5. McFadyen IR, Price AB, Geirsson RT: The relation of birth-weight to histological appearances in vessels of the placental bed. Br J Obstet Gynaecol 1986, 93:476-481
6. Pijnenborg R, Anthony J, Davey DA, Rees A, Tiltman A, Vercruysse L, Van Assche FA: Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991, 98:648-655
7. Sheppard BL, Bonnar J: An ultrastructural study of utero placental arteries in hypertensive and normotensive pregnancy and fetal growth retardation. Br J Obstet Gynaecol 1981, 88:695-705
8. Sheppard BL, Bonnar J: The ultrastructure of the arterial supply of the human placenta in pregnancy complicated by fetal growth retardation. J Obstet Gynaecol Br Commonw 1976, 83:948-959
9. Michel MZ, Khong TY, Clark DA, Beard RW: A morphological and immunological study of human placental bed biopsies in miscarriage. Br J Obstet Gynaecol 1990, 97
10. Hustin J, Jauniaux E, Schaaps JP: Histological study of the maternoembryonic interface in spontaneous abortion. Placenta 1990, 11:477-486
11. Jauniaux E, Zaidi J, Jurkovic D, Campbell S, Hustin J: Comparison of colour Doppler features and pathological findings in complicated early pregnancy. Reprod 1994, 9:2432-2437
12. Knowles RG, Moncada S: Nitric oxide synthases in mammals. Biochem J 1994, 298:249-258
13. Nakaki T, Kato R: Nitric oxide in vascular remodelling. J Invest Surg 1996, 9:431-445
14. Palmer RMJ, Moncada S: A novel citrulline-forming enzyme implicated in the formation of nitric oxide by vascular endothelial cells. Biochem Biophys Res Commun 1989, 59:348-352
15. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH: Cloned and expressed nitric oxide synthase structurally resembles cytochrome p-450 reductase. Nature 1991, 351:714-718
16. Lowenstein CJ, Glatt CS, Bredt DS, Snyder SH: Cloned and expressed macrophage NOS contrast with the brain enzyme. Proc Natl Acad Sci USA 1992, 89:6711-6715
17. Marsden PA, Schapport KT, Chen HS, Flowers M, Sundell CL, Wilcox JN, Lamas S, Michel T: Molecular cloning and characterization of human endothelial NOS. FEBS Lett 1992, 307:287-293
18. Myatt L, Brockman DE, Langdon G, Pollock JS: Constitutive calcium dependent isoform of nitric oxide synthase in the human placental villous vascular tree. Placenta 1993, 14:373-383
19. Myatt L, Brockman DE, Eis ALW, Pollock JS: Immunohistochemical localization of nitric oxide synthase in the human placenta. Placenta 1993, 14:487-495
20. Conrad KD, Davis AK: Nitric oxide synthase activity in placentae from women with pre-eclampsia. Placenta 1995, 16:691-699
21. Conrad KP, Viii M, McGuire PG, Dail WG, Davis AK: Expression of nitric oxide synthase by syncytiotrophoblast in human placental villi. FASEB J 1993, 7:1269-1276
22. Buttery LDK, McCarthy A, Springall DR, Sullivan MHF, Elder MG, Michel T, Pollock JM: Endothelial nitric oxide synthase in the human placenta: regional distribution and proposed regulatory role at the feto-maternal interface. Placenta 1994, 15:257-265
23. Eis ALW, Brockman DE, Pollock JS, Myatt L: Immunohistochemical localization of endothelial nitric oxide synthase in human villous and extravillous trophoblast populations and expression during syncytiotrophoblast formation in vitro. Placenta 1995, 16:113-126
24. Lyall F, Jablonka-Shariff A, Johnson RD, Olson LM, Nelson DM: Gene expression of nitric oxide synthase in cultured human term placental trophoblast during in vitro differentiation. Placenta 1998, 17:253-260
25. Myatt L, Brewer A, Langdon G, Brockman DE: Attenuation of the vasoconstrictor effects of thromboxane and endothelin by nitric oxide in the human fetal-placental circulation. Am J Obstet Gynecol 1992, 166:224-230
26. Myatt L, Brewer AS, Brickman DE: The action of nitric oxide on the perfused fetal-placental circulation. Am J Obstet Gynecol 1991, 164: 687-692
27. Boura ALA, Walters WAW, Read MA, Leitch IM: Autocoids and control of human placental blood flow. Clin Exp Pharmacol Physiol 1994, 21:737-748
28. Gude NM, King RG, Brennecke SP: Role of endothelium-derived nitric oxide in maintenance of low fetal vascular resistance in placenta. Lancet 1990, 336:1589-1590
29. Pijnenborg R, Dixon G, Robertson WB, Brosens I: Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980, 1:3-19
30. De Wolf F, De Wolf-Peeters C, Brosens I: Ultrastructure of the spiral arteries in human placental bed at the end of normal pregnancy. Am J Obstet Gynecol 1973, 117:833-848
31. Khong TY, De Wolf F, Robertson WB, Brosens I: Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986, 93:1049-1059
32. Blankenship TN, Enders AC, B.F. K: Trophoblastic invasion and modification of uterine veins during placental development macaques. Cell Tissue Res 1993, 274:135-244
33. Craven CM, Morgan T, Ward K: Decidal spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta 1998, 19:241-252
34. 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 of extravillous trophoblast. Cell Tissue Res 1995, 282:407-421
35. Nicholson S, Bonecinialmeida MDG, Silva JRLE, Nathan C, Xie QW, Mumford R, Weider JR, Calaycay J, Geng J, Boechat N, Linhares C, Rom W, Ho J: Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med 1996, 183: 2293-2302
36. McInnes IB, Leung BP, Field M, Wei XQ, Huang F-P, Sturrock RD, Kinninmonth A, Weider J, Mumford R, Liew FY: Production of nitric oxide in the synovial membrane of rheumatoid and osteoarthritis patients. J Exp Med 1996, 184:1519-1524
37. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. Biol Chem 1951, 193:265-275
38. 4. Nature 1970, 227:680-685
39. Zarlingo TJ, Eis ALW, Brockman DE, Kossenjans W, Myatt L: Comparative localization of endothelial and inducible nitric oxide synthase isoforms in haemochorial and epitheliochorial placenta. Placenta 1997, 18:511-520
40. Ilana A, Hochberg A, Shochina M: Endothelial nitric oxide synthase immunoreactivity in early gestation and in trophoblastic disease J Clin Pathol 1998, 51:427-431
41. Campa JS, Poston R, Poston L: Nitric oxide synthase (eNOS) is localized to the vascular endothelium of myometrium from pregnant women at term. J Physiol 1998, 507:69P
42. Farmer DR, Nelson DM: A fibrin matrix modulates the proliferation, hormone secretion and morphologic differentiation of cultured human placental trophoblast. Placenta 1992, 13:163-177
43. Ahmed A, Dunk C, Kniss D, Wilkes M: Role of VEGF receptor (Flt-1) in mediating calcium-dependent nitric oxide release and limiting DNA synthesis in human trophoblast cells. Lab Invest 1997, 76:779-791
44. Diss EM, Moore J, Gabbe SG, Kniss DA: Study of thromboxane and prostacyclin metabolism in an in vitro model of first-trimester human trophoblasts. Am J Obstet Gynecol 1992, 167:1046-1052