Skip to main content
Log in

Developmental changes in the cell columns and trophoblastic shell of the macaque placenta: an immunohistochemical study localizing type IV collagen, laminin, fibronectin and cytokeratins

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

Abstract

Developmental changes in the organization of cells and extracellular matrix in the cell columns and trophoblastic shell of macaque placentas have been examined between 37 days of gestation and term. Between 37 and 53 days a thickened basement membrane developed between the trophoblast cells of the proximal cell columns and the mesenchymal cores of contiguous anchoring villi. This layer stained strongly for type IV collagen and laminin, but weakly for fibronectin. Large “lakes” of extracellular matrix immunoreactive for all 3 of these antigens were present in the distal columns, while smaller amounts were distributed between cells of the proximal columns. During this period the trophoblast cells in the proximal shell reorganized, forming strands of cells that were separated by bands of matrix immunoreactive for type IV collagen, laminin, and fibronectin. Staining for these antigens decreased abruptly at the junction between fetal and maternal tissues. Between 66 and 104 days the thick basement membrane of the proximal columns persisted, but stained only weakly for each of the 3 extracellular matrix antigens. The large lakes of matrix in the distal columns characteristic of earlier stages gradually disappeared. The cell columns became progressively shorter and the tips of the anchoring villi became embedded in the trophoblastic shell. The matrix of the shell decreased in immunostaining intensity except for narrow rims around the trophoblast cells. Gestational ages later than 104 days showed few additional changes in the distribution of the matrix antigens or cell organization of the columns and shell. The thick basement membrane-like layer persisted to term although it continued to stain weakly for the 3 matrix antigens. The distal ends of most anchoring villi were embedded in the trophoblastic shell. The developmental changes in the organization of the columns and shell may be related to changes in placental growth rate.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Armant DR, Kaplan HA, Lennarz WJ (1986) Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts. Dev Biol 116:519–523

    Google Scholar 

  • 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 

  • Benirschke K, Kaufmann P (1990) Pathology of the Human Placenta, 2nd edn. Springer, New York

    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 

  • Carson DD, Tang J-P, Gay S (1988) Collagens support embryo attachment and outgrowth in vitro: effects of the arg-gly-asp sequence. Dev Biol 127:368–375

    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 

  • 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 (1968) Fine structure of anchoring villi of the human placenta. Am J Anat 122:419–452

    Google Scholar 

  • Feinberg RF, Kliman HJ, Lockwood CJ (1991) Is oncofetal fibronectin a trophoblast glue for human implantation? Am J Pathol 138:537–543

    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 H, 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 

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

    Google Scholar 

  • Hamilton WJ, Boyd JD (1960) Development of the human placenta in the first three months of gestation. J Anat 94:297–328

    Google Scholar 

  • Kao L-C, Caltabiano S, Wu S, Strauss III JF, Kliman HJ (1988) The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Dev Biol 130:693–702

    Google Scholar 

  • King BF, Blankenship TN (1993) Development and organization of primate trophoblast cells. In: Soares MJ, Handwerger S, Talamantes F (eds) Trophoblast cells: pathways for metarnal-embryonic communication. Springer (in press)

  • Kisalus LL, Herr JC, Little CD (1987) Immunolocalization of extracellular matrix proteins and collagen synthesis in first-trimester human decidua. Anat Rec 218:402–415

    Google Scholar 

  • Korhonen M, Ylanne J, Laitinen L, Cooper HM, Quaranta V, Virtanen I (1991) Distribution of the α16 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 

  • Loke YW, Gardner L, Burland K, King A (1989) Laminin in human trophoblast-decidua interaction. Human Reprod 4:457–463

    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 

  • Murphy G, Docherty AJP (1992) The matrix metalloproteinases and their inhibitors. Am J Resp Cell Mol Biol 7:120–125

    Google Scholar 

  • Okudaira Y, Hashimoto T, Hamanaka N, Yoshinare S (1971) Electron microscopic study on the trophoblastic cell column of human placenta. J Electron Microse (Tokyo) 20:93–106

    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 

  • Sutherland AE, Calarco PG, Damsky CH (1988) Expression and function of cell surface extracellular matrix receptors in mouse blastocyst attachment and outgrowth. J Cell Biol 106:1331–1348

    Google Scholar 

  • Tarantal AF, Lehrer SB, Lasley BL, Hendrickx AG (1990) Developmental toxicity of temafloxacin hydrochloride in the long-tailed macaque (Macaca fascicularis). Teratology 42:233–242

    Google Scholar 

  • Wewer UM, Faber M, Liotta LA, Albrechtsen R (1985) Immunochemical and ultrastructural assessment of the nature of the pericellular basement membrane of human decidual cells. Lab Invest 53:624–633

    Google Scholar 

  • Wewer UM, Damjanov A, Weiss J, Liotta LA, Damjanov I (1986) Mouse endometrial stromal cells produce basement-membrane components. Differentiation 32:49–58

    Google Scholar 

  • Wewer UM, Taraboletti G, Sobel ME, Albrechtsen R, Liotta LA (1987) Role of laminin receptor in tumor cell migration. Cancer Res 47:5691–5698

    Google Scholar 

  • Wislocki GB, Bennett HS (1943) The histology and cytology of the human and monkey placenta, with special reference to the trophoblast. Am J Anat 73:335–449

    Google Scholar 

  • Wislocki GB, Dempsey EW (1984) The chemical histology of human placenta and decidua with reference to mucoproteins, glycogen, lipids and acid phosphatase. Am J Anat 83:1–41

    Google Scholar 

  • Wislocki GB, Padykula HA (1961) Histochemistry and electron microscopy of the placenta. In: Young WC (ed) Sex and internal secretions, vol. 2, 2rd edn. Williams and Wilkins, Baltimore, pp 883–957

    Google Scholar 

  • Wislocki GB, Streeter GL (1938) On the placentation of the macaque (Macaca mulatta), from the time of implantation until the formation of the definitive placenta. Contrib Embryol 27:1–66

    Google Scholar 

  • Woessner JF (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154

    Google Scholar 

  • Wynn RM (1972) Cytotrophoblastic specialization: an ultrastructural study of the human placenta. Am J Obstet Gynecol 114:339–355

    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 

  • Yamaguchi Y, Isemura M, Yosizawa Z, Kurosawa K, Yoshinaga K, Sato A, Suzuki M (1985) Changes in the distribution of fibronectin in the placenta during normal human pregnancy. Am J Obstet Gynecol 152:715–718

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blankenship, T.N., King, B.F. Developmental changes in the cell columns and trophoblastic shell of the macaque placenta: an immunohistochemical study localizing type IV collagen, laminin, fibronectin and cytokeratins. Cell Tissue Res 274, 457–466 (1993). https://doi.org/10.1007/BF00314542

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00314542

Key words

Navigation