Abstract
The trophoblast invasion of uteroplacental arteries in the guinea pig has been studied by means of electron microscopy and immunohistochemisty. To identify trophoblast cells, smooth muscle cells, and endothelial cells, antibodies against cytokeratins, smooth muscle myosin, desmin, and vimentin were employed. Furthermore, the immunohistochemical expression patterns of nitric oxide synthase isoforms (eNOS, mNOS and bNOS) were studied and were compared with the enzyme histochemical staining for NADPH-diaphorase. Dilation of uteroplacental arteries begins prior to day 30, when trophoblast cells that coexpress endothelial and macrophage nitric oxide synthase can be found in the vicinity of the vessels and replace the surrounding peritoneal mesothelium. Trophoblast invasion of the arterial walls and the subsequent wall destruction are only secondary effects. Starting around day 50, the final steps of pregnancy-dependent vessel modifications involve intraarterial trophoblast adhesion to the endothelium and subsequent replacement of the endothelium by the trophoblast cells. These may centrifugally invade the vessel media eventually forming intraluminal plugs. These findings led us to the conclusion that in the guinea pig pregnancy-induced physiological dilation of the uteroplacental arteries is due to the effect of nitric oxide rather than being caused by trophoblast-induced media destruction.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Benirschke K, Kaufmann P (1995) Pathology of the Human Placenta, 3rd edn. Springer, New York
Blankenship TN, Enders AC, King BF (1993a) 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 272:227–236
Blankenship TN, Enders AC, King BF (1993b) Trophoblastic invasion and modification of uterine veins during placental development in macaques. Cell Tissue Res 274:135–144
Boyd JD, Hamilton WJ (1970) The Human Placenta. Heffer & Sons, Cambridge
Brosens I (1988) The utero-placental vessels at term — the distribution and extent of physiological changes. Trophoblast Res 3:61–68
Brosens I, Robertson WB, Dixon HG (1967) The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 93:569–579
Brosens I, Robertson WB, Dixon HG (1972) The role of the spinal arteries in the pathogenes of pre-eclampsia. Obstet Gynecol Ann 1:177–191
Brosens I, Dixon HG, Robertson WB (1977) Fetal growth retardation and the arteries of the placental bed. Brit J Obstet Gynaecol 84:656–663
Burrows TD, King A, Loke YW (1994) Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: Implications for vascular invasion during implantation. Placenta 15:21–33
Buttery LDK, McCarthy A, Springall DR, Michel T, Sullivan M, Elder MG, Polak JM (1993) Differential immunochemical localization of endothelial nitric oxide synthase in human placenta. Endothelium 1 [Suppl]:109
Carpenter SJ (1982) Trophoblast invasion and alteration of mesometrial arteries in the pregnant hamster: light and electron microscopic observations. Placenta 3:219–242
Chwalisz K, Garfield RE (1994) Role of progesterone during pregnancy: Models of parturition and pre-eclampsia. Z Geburtsh Perinatol 198:170–180
Chwalisz K, Ciesla I, Garfield RE (1994) Inhibition of nitric oxide (NO) synthesis induces preterm parturition and preeclampsia-like conditions in guinea pigs. Society for Gynecologic Investigation, Chicago (III), Abstract no. 036
Damsky CH, Fitzgerald ML, Fisher SJ (1992) 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 89:210–222
DeWolf F, DeWolf-Peeters C, Brosens I (1973) Ultrastructure of the spiral arteries in the human placental bed at the end of normal pregnancy. Am J Obstet Gynecol 117:833–848
DeWolf F, Brosens I, Renaer M (1980) Fetal growth retardation and the maternal arterial supply of the human placenta in the absence of sustained hypertension. Brit J Obstet Gynaecol 87:678–685
Egund N, Carter AM (1974) Uterine and placental circulation in the guinea-pig: an angiographic study. J Reprod Fertil 40.401–410
Fisher SJ, Damsky CH (1993) Human cytotrophoblast invasion. Semin Cell Biol 4:183–188
Frank HG, Malekzadeh F, Kerschanska S, Crescimanno C, Castellucci M, Lang I, Desoye G, Kaufmann P (1994) Immunohistochemistry of two different types of placental fibrinoid. Acta Anat 150:55–68
Fuller EG, Highison GJ, Tibbits DF, Fuller BD (1994) Migration of intravascular trophoblast cells in uterine arteries of the golden hamster: a scanning electron microscopic study. J Morphol 220:307–313
Garfield RE, Yallampalli C, Buhimschi I, Chwalisz K (1994) Reversal of pre-eclampsia symptoms induced in rats by nitric oxide inhibition with L-arginine, steroid hormones and an endothelin antagonist. Society for Gynecologic Investigation, Chicago (III), Abstract no. 384
Genbacev O, White TEK, Gavin CE, Miller RK (1993) Human trophoblast cultures: models for implantation and peri-implantation toxicology. Reproduct Toxicol 7:75–94
Harris JWS, Ramsey EM (1966) The morphology of human uteroplacental vasculature. Carnegie Inst Contrib Embryol 38:43–58
Hees H, Moll W, Wrobel K-H, Hees I (1987) Pregnancy-induced structural changes and trophoblastic invasion in the segmental mesometrial arteries of the guinea pig (Cavia porcellus L.). Placenta 8:609–626
Hustin J, Schaaps J-P (1987) Echocardiographic and anatomic studies of the maternotrophoblastic border during the first trimester of pregnancy. Am J Obstet Gynecol 157:162–168
Hustin J, Schaaps J-P, Lambotte R (1988) Anatomical studies of the utero-placental vascularization in the first trimester of pregnancy. Trophoblast Res 3:49–60
Kaufmann P, Davidoff M (1977) The guinea-pig placenta. Adv Anat Embryol Cell Biol 53:1–91
Khong TY, DeWolf F, Robertson WB, Brosens I (1986) Inadequate maternal vascular response to placentation in preeclampsia and intrauterine fetal growth retardation. Brit J Obstet Gynaecol 93:1049–1059
King A, Loke YW (1988) Differential expression of blood-group-related carbohydrate antigens by trophoblast subpopulations. Placenta 9.513–521
Moll W, Espach A, Wrobel K-H (1983) Growth of mesometrial arteries in guinea pigs during pregnancy. Placenta 4:111–124
Moll W, Nienartowicz A, Hees H, Wrobel K-H, Lenz A (1988) Blood flow regulation in the uteroplacental arteries. Trophoblast Res 3:83–96
Myatt L, Brockman DE, Eis ALW, Pollock JS (1993) Immunohistochemical localization of nitric oxide synthase in the human placenta. Placenta 14:487–495
Nanaev AK, Milovanov AP, Domogatsky SP (1993) Immunohistochemical localization of extracellular matrix in perivillous fibrinoid of normal human term placenta. Histochemistry 100:341–346
Pijnenborg R, Robertson WB, Brosens I (1974) The arterial migration of trophoblast in the uterus of the golden hamster, Mesocricetus auratus. J Reprod Fertil 40:269–280
Pijnenborg R, Dixon G, Robertson WB, Brosens I (1980) Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1:3–19
Pijnenborg R, Robertson WB, Brosens I, Dixon G (1981) Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 2:71–92
Ramsey EM, Harris JWS (1966) Comparison of uteroplacental vasculature and circulation in the rhesus monkey and man. Contrib Embryol Carnegie Inst 38:59–70
Schaaps JP, Hustin J (1988) In vivo aspect of the maternal-trophoblastic border during the first trimester of gestation. Trophoblast Res 39–48
Sheppard BL, Bonnar J (1974a) Scanning electron microscopy of the human placenta and decidual spiral arteries in normal pregnancy. J Obstet Gynaecol Brit Commonw 81:17–20
Sheppard BL, Bonnar J (1974b) The ultrastructure of the arterial supply of the human placenta in early and late pregnancy. J Obstet Gynaecol Brit Commonw 81:497–511
Sheppard BL, Bonnar J (1976) The ultrastructure of the arterial supply of the human placenta in prgnancy complicated by fetal growth retardation. Brit J Obstet Gynaecol 83:948–959
Sheppard BL, Bonnar J (1988) The maternal blood supply to the placenta in pregnancy complicated by intrauterine fetal growth retardation. Trophoblast Res 3:69–82
Spessert R, Wohlgemuth C, Reuss S, Layes E (1994) NADPH-diaphorase activity of nitric oxide synthase in the olfactory bulb: co-factor specificity and characterization regarding the interrelation of NO formation. J Histochem Cytochem 42:569–575
Thrower S, Bulmer JN, Griffin NR, Wells M (1991) Further studies of lectin binding by villous and extravillous trophoblast in normal and pathological pregnancy. Int J Gynecol Pathol 10:238–251
Vincent SR, Staines WA, Fibiger HC (1983) Histochemical demonstration of separate population of somatostatin and cholinergic neurons in the rat striatum. Neurosci Lett 35:111–114
Yallampalli C, Byam-Smith M, Nelson SO, Garfield RE (1994) Steroid hormones modulate the production of nitric oxide and cGMP in the rat uterus. Endocrinology 134:1971–1993
Author information
Authors and Affiliations
Additional information
Parts of this study were supported by Grant Ka 36017-2 from the Deutsche Forschungsgemeinschaft.
Rights and permissions
About this article
Cite this article
Nanaev, A., Chwalisz, K., Frank, HG. et al. Physiological dilation of uteroplacental arteries in the guinea pig depends on nitric oxide synthase activity of extravillous trophoblast. Cell Tissue Res 282, 407–421 (1995). https://doi.org/10.1007/BF00318873
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00318873