Skip to main content
SpringerLink
Log in

Trophoblastic invasion and the development of uteroplacental arteries in the macaque: immunohistochemical localization of cytokeratins, desmin, type IV collagen, laminin, and fibronectin

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The processes by which trophoblast cells invade and modify the walls of the uteroplacental arteries of macaques during the course of gestation were examined. Antibodies to cytokeratins were employed to identify trophoblast, anti-desmin antibody to identify smooth muscle, and antibodies to type IV collagen, laminin, and fibronectin to examine changes in extracellular matrix distribution in the arterial wall. During early gestation, endovascular trophoblast adhered to the arterial wall, often in an asymmetrical distribution. As trophoblast cells moved outwardly into the tunica media, the basement membrane underlying the endothelium was lost, as indicated by gaps in the layer when stained for type IV collagen and laminin. Trophoblast cells became sequestered in the vessel wall where they hypertrophied and became surrounded by a capsule containing type IV collagen and laminin. As the trophoblast cells became established in the vessel wall, the muscular layer of the artery became discontinuous. Throughout gestation it was common for trophoblast cells to invade the vessel intimal layer and share the lining of the artery with typical endothelial cells. This general disposition of endovascular and intramural trophoblast persisted into late gestation. In addition, and contrary to the results of earlier studies of macaques, we identified trophoblastic invasion and modification of myometrial segments of the uteroplacental arteries in later gestation. We also found evidence of interstitial trophoblast cells among the stromal cells of the endometrium, especially during early gestation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Autio-Harmainen H, Sandberg M, Pihlajaniemi T, Vuorio E (1991) Synthesis of laminin and type IV collagen by trophoblastic cells and fibroblastic stromal cells in the early human placenta. Lab Invest 64:483–491

    Google Scholar 

  • Barsky SH, Rao NC, Restrepo C, Liotta L (1984) Immunocytochemical enhancement of basement membrane antigens by pepsin: applications in diagnostic pathology. Am J Clin Pathol 82:191–194

    Google Scholar 

  • Bischof P, Friedli E, Martelli M, Campana A (1991) Expression of extracellular matrix-degrading metalloproteinases by cultured human cytotrophoblast cells: effects of cell adhesion and immunopurification. Am J Obstet Gynecol 165:1791–1801

    Google Scholar 

  • Blankenship TN, Enders AC, King BF (1992) Distribution of laminin, type IV collagen, and fibronectin in the cell columns and trophoblastic shell of early macaque placentas. Cell Tissue Res 270:241–248

    Google Scholar 

  • Boyd JD, Hamilton WJ (1970) The human placenta. Heffer, Cambridge

    Google Scholar 

  • Brosens IA (1977) Morphological changes in the utero-placental bed in pregnancy hypertension. Clin Obstet Gynecol 4:573–593

    Google Scholar 

  • Brosens IA (1988) The utero-placental vessels at term-the distribution and extent of physiological changes. Troph Res 3:61–67

    Google Scholar 

  • Brosens IA, Robertson WB, Dixon HG (1967) The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 93:569–579

    Google Scholar 

  • Bulmer JN, Smith J, Morrison L, Wells M (1988) Maternal and fetal relationships in the human placental basal plate. Placenta 9:237–246

    Google Scholar 

  • 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

    Google Scholar 

  • Daya D, Sabet L (1991) The use of cytokeratin as a sensitive and reliable marker for trophoblastic tissue. Am J Clin Pathol 95:137–141

    Google Scholar 

  • De Wolf F, De Wolf-Peters 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

    Google Scholar 

  • Earl U, Estlin C, Bulmer JN (1990) Fibronectin and laminin in the early human placenta. Placenta 11:223–231

    Google Scholar 

  • Emonard H, Christiane Y, Smet M, Grimaud JA, Foidart JM (1990) Type IV and interstitial collagenolytic activities in normal and malignant trophoblastic cells are specifically regulated by the extracellular matrix. Invasion Metastasis 10:170–177

    Google Scholar 

  • Enders AC, King BF (1991) Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon. Am J Anat 192:329–346

    Google Scholar 

  • Falck Larsen J (1980) Human implantation and clinical aspects. Prog Repord Biol 7:284–296

    Google Scholar 

  • Feinberg RF, Kao L-C, Haimowitz JE, Queenan JT, Wun T-C, Strauss III JF, Kliman HJ (1989) Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. Lab Invest 61:20–26

    Google Scholar 

  • Fernandez PL, Merino MJ, Nogales FF, Charonis AS, Stetler-Stevenson W, Liotta L (1992) Immunohistochemical profile of basement membrane proteins and 72 kilodalton type IV collagenase in the implantation placental site. Lab Invest 66:572–579

    Google Scholar 

  • Fisher SJ, Cui T-Y, Zhang L, Hartman L, Grahl K, Gou-Yang Z, Tarpey J, Damsky CH (1989) Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol 109:891–902

    Google Scholar 

  • Gerretsen G, Huisjes HJ, Elema JD (1981) Morphological changes of the spiral arteries in the placental bed in relation to preeclampsia and fetal growth retardation. Br J Obstet Gynaecol 88:876–881

    Google Scholar 

  • Graham CH, Lala PK (1991) Mechanism of control of trophoblast invasion in situ. J Cell Physiol 148:228–234

    Google Scholar 

  • Harris JWS, Ramsey EM (1966) The morphology of human uteroplacental vasculature. Contrib Embryol 38:43–58

    Google Scholar 

  • Khong TY, De Wolf F, Robertson WB, Brosens I (1986a) Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 93:1049–1059

    Google Scholar 

  • Khong TY, Lane EB, Robertson WB (1986b) An immunocytochemical study of fetal cells at the maternal-placental interface using monoclonal antibodies to keratins, vimentin and desmin. Cell Tissue Res 246:189–195

    Google Scholar 

  • Khong TY, Lane EB, Robertson WB (1987) Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol 94:649–655

    Google Scholar 

  • Knoth M, Falck Larsen J (1972) Ultrastructure of a human implantation site. Acta Obstet Gynecol Scand 51:385–393

    Google Scholar 

  • Korhonen M, Ylanne J, Laitinen L, Cooper HM, Quaranta V, Virtanen I (1991) Distribution of the α1-α6 integrin subunits in human developing and term placenta. Lab Invest 65:347–356

    Google Scholar 

  • Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, Grobelny D, Galardy R, Damsky CH, Fisher SJ (1991) 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 113:437–449

    Google Scholar 

  • Liotta LA, Steeg PS, Stetler-Stevenson WG (1991) Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327–336

    Google Scholar 

  • Moll UM, Lane BL (1990) Proteolytic activity of first trimester human placenta: localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 94:555–560

    Google Scholar 

  • Pijnenborg R, Dixon G, Robertson WB, Brosens I (1980) Trophoblast invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1:3–19

    Google Scholar 

  • Pijnenborg R, Bland JM, Robertson WB, Brosens I (1983) Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4:397–414

    Google Scholar 

  • Queenan JT, Kao L-C, Arboleda CE, Ulloa-Aguirre A, Golos TG, Cines DB, Strauss III JF (1987) Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J Biol Chem 262:10903–10906

    Google Scholar 

  • Ramsey EM (1981) Functional anatomy of the primate placenta. In: Wallenburg HCS, van Kreel BK, van Dijk JP (eds) Transfer across the primate and non-primate placenta. Placenta [Suppl 1]:29–42

  • Ramsey EM, Donner MW (1980) Placental vasculature and circulation. Thieme, Stuttgart

    Google Scholar 

  • Ramsey EM, Harris JWS (1966) Comparison of uteroplacental vasculature and circulation in the rhesus monkey and man. Contrib Embryol 38:59–70

    Google Scholar 

  • Ramsey EM, Houston ML, Harris JWS (1976) Interactions of the trophoblast and maternal tissues in three closely related primate species. Am J Obstet Gynecol 124:647–652

    Google Scholar 

  • Robertson WB, Khong TY (1987) Pathology of the uteroplacental bed. In: Sharp F, Symonds EM (eds) Hypertension and pregnancy; reproductive and perinatal medicine, vol 7. Perinatology Press, Ithaca, pp 101–113

    Google Scholar 

  • Robertson WB, Warner B (1974) The ultrastructure of the human placental bed. J Pathol 112:203–211

    Google Scholar 

  • Robertson WB, Brosens IA, Dixon G (1975) Uteroplacental vascular pathology. Eur J Obstet Gynecol Reprod Biol 5:47–65

    Google Scholar 

  • Robertson WB, Brosens IA, Dixon HG (1981) Maternal blood supply in fetal growth retardation. In: Van Assche FA, Robertson WB (es) Fetal growth retardation. Churchill-Livingston, London, pp 126–138

    Google Scholar 

  • Robertson WB, Brosens IA, Landells WN (1985) Abnormal placentation. Obstet Gynecol Ann 14:411–426

    Google Scholar 

  • Sheppard BL, Bonnar J (1974a) Scanning electron microscopy of the human placenta and decidual spiral arteries in normal pregnancy. J Obstet Gynaecol Br Commonw 81:20–29

    Google Scholar 

  • Sheppard BL, Bonnar J (1974b) The ultrastructure of the arterial supply of the human placenta in early and late pregnancy. J Obstet Gynaecol Br Commonw 81:497–511

    Google Scholar 

  • Sheppard BL, Bonnar J (1981) An ultrastructural study of uteroplacental spiral arteries in hypertensive and normotensive pregnancy and fetal growth retardation. Br J Obstet Gynaecol 88:695–705

    Google Scholar 

  • Sheppard BL, Bonnar J (1988) The maternal blood supply to the placenta in pregnancy complicated by intrauterine fetal growth retardation. Troph Res 3:69–81

    Google Scholar 

  • Tarara R, Enders AC, Hendrickx AG, Gulamhusein N, Hodges JK, Hearn JP, Eley RB, Else JG (1987) Early implantation and embryonic development of the baboon: stages 5, 6 and 7. Anat Embryol 176:267–275

    Google Scholar 

  • Yagel S, Parhar RS, Jeffrey JJ, Lala PK (1988) Normal nonmetastatic human trophoblast cells share in vitro invasive properties of malignant cells. J Cell Physiol 136:455–462

    Google Scholar 

  • Yagel S, Kerbel R, Lala P, Eldar-Gera T, Dennis JW (1990) Basement membrane invasion by first trimester human trophoblast: requirement for branched complex-type Asn-linked oligosaccharides. Clin Exp Metastasis 8:305–317

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell Biology and Human Anatomy, School of Medicine, University of California, 95616-8643, Davis, CA, USA

    Thomas N. Blankenship, Allen C. Enders & Barry F. King

Authors
  1. Thomas N. Blankenship
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Allen C. Enders
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barry F. King
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blankenship, T.N., Enders, A.C. & King, B.F. 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 (1993). https://doi.org/10.1007/BF00302728

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00302728

Key words

Search

Navigation