Anatomy and Embryology

, Volume 176, Issue 1, pp 87–97 | Cite as

The basement membrane of the persisting maternal blood vessels in the placenta of Callithrix jacchus

  • H. -J. Merker
  • D. Bremer
  • H. -J. Barrach
  • R. Gossrau


Formation and morphology of the thickened basement membrane-like layer around the persisting maternal vessels of the Callithrix jacchus placenta were investigated from day 45 until term (day 142) using light, electron and immunofluorescence microscopy. Thickening occurs with the establishment of contacts between the vessels and the syncytiotrophoblast (day 48). Final thickness is reached at about day 100. The course of the vessels shows wide gaps where the maternal blood flows freely into the intertrabecular spaces. As revealed by electron microscopy, the extracellular sheath around the maternal vessels consists of an inner subendothelial basement membrane (3–6 μm) and an outer fibril-containing layer (2–4 μm). Cell debris is seen between the two layers and in the basement membrane. Plaques of granular and fine-filamentous material are incorporated into the fibril-containing layer. The synthesis of the basement membrane material is localized in the endothelial cells. Immunofluorescence microscopy reveals collagen types IV and V, laminin and heparan sulfate proteoglycan (BM-1) in the sheath around the persisting vessels. Fibronectin occurs only in certain areas or in the form of dots. Collagen types I and III are not seen in the region of the vascular wall. It can, therefore, be assumed that the subendothelial layer represents a genuine basement membrane; the fibrils consist of collagen type V and the plaques contain fibronectin. The existence of the thick perivascular sheath is attributed to the persistence and stability of the maternal vessels.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adachi E, Hayashi T (1985) In vitro formation of fine fibrils with a D-periodic binding pattern from type V collagen. Coll Relat Res 5:225–232Google Scholar
  2. Barrach H-J, Grundmann K, Hinz N, Felies A (1980) Immunofluorescent microscopic investigations of intercellular substances during limb development. In: Merker H-J, Nau H, Neubert D (eds) Teratology of the Limbs. Walter de Gruyter Verlag, Berlin, pp 273–293Google Scholar
  3. Barrach H-J, Grundmann K, Hinz N, Felies A (1981) Comparison of the differentiation of muscle and connective tissue of mouse limb buds in culture and in vivo: A morphological study by indirect immunofluorescence. In: Neubert D, Merker H-J (eds) Culture Techniques. Walter de Gruyter Verlag, Berlin, pp 135–159Google Scholar
  4. Bremer D (1983) Entwicklung und Charakterisierung der Placenta von Callithrix jacchus. Doctoral thesis, Freie Universität BerlinGoogle Scholar
  5. Csato W, Merker H-J (1983) Production and formation of the basement membrane in embryonic tissues of the mouse. Cell Tissue Res 228:85–98Google Scholar
  6. Enders A (1965) A comparative study of the fine structure of the trophoblast in several haemochorial placentas. Am J Anat 116:29–68Google Scholar
  7. Engvall E, Ruoslahti E (1977) Binding of a soluble form of fibroblast surface protein fibronectin to collagen Int J Cancer 20:1–5Google Scholar
  8. Farquhar MG, Courtoy PJ, Lemkin MC, Kanwar YS (1981) Current knowledge of the functional architecture of the glomerular basement membrane. In: Kühn K, Schöne H-J, Timpl R (eds) New Trends in Basement Membrane Research. Raven Press, New York, pp 9–29Google Scholar
  9. Feller B, Merker H-J (1979) Elektronenmikroskopische Untersuchungen zur Wirkung von Colchizin auf Knorpelgewebe aus Organkulturen von Extremitätenknospen. Acta Anat 103:445–460Google Scholar
  10. Furthmayr H (ed) (1982) Immunochemistry of the extracellular matrix. CRC-Press, Boca Raton, Florida, vol I, IIGoogle Scholar
  11. Furthmayr H, Roll FJ, Madri JA, Foellmer H (1981) Composition of basement membranes as viewed with the electron microscope. In: Kühn K, Schöne H-J, Timpl R (eds) New Trends in Basement Membrane Research Raven Press, New York, pp 31–48Google Scholar
  12. Geyer G (1973) Ultrahistochemie. Gustav Fischer Verlag, JenaGoogle Scholar
  13. Gosslau B, Barrach H-J (1979) Enzyme-linked immunosorbent microassay for quantification of specific antibodies to collagen type I, II, III. J Immunol Methods 29:71–77Google Scholar
  14. Gossrau R, Heger W, Merker H-J. Enzyme-histochemical studies of the endothelium of maternal vessels in the placenta of marmosets (Callithrix jacchus), in preparationGoogle Scholar
  15. Hassell JR, Gehron RP, Barrach H-J, Wilszek J, Rennard SJ, Martin GR (1980) Isolation of heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci USA 77:4494–4498Google Scholar
  16. Hedman K, Vaheri A, Wartiovaara J (1978) External fibronectin of cultured human fibroblasts is predominantly a matrix protein. J Cell Biol 76:748–760Google Scholar
  17. Heger W, Neubert D (1983) Timing of ovulation and implantation in the common marmoset Callithrix jacchus, by monitoring of estrogens and 6-hydroxypregnanolone in urine. Arch Toxicol 54:41–52Google Scholar
  18. Hill J (1932) On the developmental history of the primates. Croonian Lecture. Philos Trans R Soc Lond [Biol] 221:45–178Google Scholar
  19. Jollie W (1973) Fine structural changes in the placental membrane of the marmosets with increasing gestational age. Anat Rec 176:307–320Google Scholar
  20. Jollie W, Haar JL, Craig SS (1975) Fine structural observations on haematopoiesis in the chorioallantoic placenta of the marmosets. Am J Anat 144:9–38Google Scholar
  21. Kefalides NA (ed) (1978) Biology and chemistry of basement membranes. Academic Press, New YorkGoogle Scholar
  22. Lauri GW, Leblond CP, Martin GR, Silver MH (1982) Intercellular localization of basement membrane precursors in the endodermal cells of the rat parietal yolk sac. J Histochem Cytochem 30:991–998Google Scholar
  23. Luckett W (1974) Comparative development and evolution of the placenta in primates. Contrib Primatol 3:142–234Google Scholar
  24. Luckett W (1975) Ontogeny of the fetal membranes and placentae: Their bearing on primate phylogeny. In: Luckett W, Szalay F (eds) Phylogeny of the Primates. A Multidisciplinary Approach. Plenum Press, New York, pp 157–182Google Scholar
  25. Luckett W, Szalay F (eds) (1975) Phylogeny of the Primates. A multidisciplinary Approach. Plenum Press, New YorkGoogle Scholar
  26. Ludwig K (1981) Vergleichende Anatomie der Plazenta. In: Becker V, Schiebler Th, Kubli F (eds) Die Plazenta des Menschen. Thieme Verlag, Stuttgart pp 1–12Google Scholar
  27. Madri JA, Pratt BM, Yurchenko PD, Furthmayr H (1984) The structural organization and architecture of basement membranes. In: Basement Membranes and Cell Movements. Ciba Foundation Symposium 108, Pitman, London, pp 6–24Google Scholar
  28. Merker H-J, Barrach H-J (1981) The morphology of basement membrane formation. Eur J Cell Biol 26:111–120Google Scholar
  29. Palotie A, Tryggvason K, Peltonen L, Seppä H (1983) Components of subendothelial aorta basement membrane. Immunohistochemical localization and role in cell attachment. Lab Invest 49:362–370Google Scholar
  30. Phillips J, Grist S (1975) The use of transabdominal palpation to determine the course of pregnancy in the marmoset, Callithrix jacchus. J Reprod Fertil 43:103–108Google Scholar
  31. Romeis B (1968) Mikroskopische Technik. Oldenburg Verlag, München WienGoogle Scholar
  32. Sage H, Bornstein P (1979) Characterization of a novel collagen chain in human placenta and its relation to AB collagen. Biochemistry 18:3815–3822Google Scholar
  33. Sage H, Woodbury RG, Bornstein P (1979) Structural studies on human type IV collagen. J Biol Chem 254:9893–9900Google Scholar
  34. Schuppan D, Becker J, Boehm H, Hahn EG (1986) Immunfluorescent localization of type V collagen as a fibrillar component of the interstitial connective tissue of human oval mucosa, aortery and liver. Cell Tissue Res 243:535–543Google Scholar
  35. Smith BD, McKenney KH, Lustberg TJ (1977) Characterization of collagen precursors found in rat skin and rat bone. Biochemistry 16:2980–2985Google Scholar
  36. Starck D (1978) Primaten. In: Vergleichende Anatomie der Wirbeltiere, vol I. Springer Verlag, Heidelberg, pp 189–200Google Scholar
  37. Szalay F, Delson E (1979) Infraorder platyrrhini. In: Evolutionary History of the Primates. Academic Press, New York, pp 275–302Google Scholar
  38. Szarfman A, Hassell J, Rohrbach DH, Stanley J, Martin GR (1981) Components of basement membranes. Their properties, functions and alterations in disease states. In: Kühn K, Schöne H-H, Timpl R (eds) New Trends in Basement Membrane Research. Raven Press, New York, pp 267–278Google Scholar
  39. Timpl R, Rohde H, Geron RP, Rennard SJ, Foidart J-M, Martin GR (1979) Laminin — a glycoprotein from basement membranes. J Biol Chem 254:9933–9937Google Scholar
  40. Trelstad RL, Catanese VM, Rubin DF (1976) Collagen fractionation: Separation of native types I, II and III by differential precipitation. Anal Biochem 71:114–118Google Scholar
  41. Vracko R (1981) The role of basal lamina in maintenance of orderly tissue structure. In: Kühn K, Schöne H-H, Timpl R (eds) New Trends in Basement Membrane Research. Raven Press, New York, pp 1–8Google Scholar
  42. Wislocki G (1929) On the placentation of primates, with a consideration of the phylogeny of the placenta. Contrib Embryol Carneg Inst 111:51–80Google Scholar
  43. Wislocki G (1932) Placentation in the marmoset (Oedipomidas Geoffroyi) with remarks on twinning in monkeys. Anat Rec 52:381–399Google Scholar
  44. Wislocki G (1943) Hemopoiesis in the chorionic villi of the placenta of Platyrrhine monkeys. Anat Rec 85:349–364Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • H. -J. Merker
    • 1
  • D. Bremer
    • 1
  • H. -J. Barrach
    • 1
  • R. Gossrau
    • 1
  1. 1.Institute of Anatomy and Institute of Toxicology and Prenatal PharmacologyFree University of BerlinBerlinGermany

Personalised recommendations