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

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Summary

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.

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References

  • Adachi E, Hayashi T (1985) In vitro formation of fine fibrils with a D-periodic binding pattern from type V collagen. Coll Relat Res 5:225–232

    Google Scholar 

  • 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 273–293

    Google Scholar 

  • 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 135–159

    Google Scholar 

  • Bremer D (1983) Entwicklung und Charakterisierung der Placenta von Callithrix jacchus. Doctoral thesis, Freie Universität Berlin

  • Csato W, Merker H-J (1983) Production and formation of the basement membrane in embryonic tissues of the mouse. Cell Tissue Res 228:85–98

    Google Scholar 

  • Enders A (1965) A comparative study of the fine structure of the trophoblast in several haemochorial placentas. Am J Anat 116:29–68

    Google Scholar 

  • Engvall E, Ruoslahti E (1977) Binding of a soluble form of fibroblast surface protein fibronectin to collagen Int J Cancer 20:1–5

    Google Scholar 

  • 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 9–29

    Google Scholar 

  • Feller B, Merker H-J (1979) Elektronenmikroskopische Untersuchungen zur Wirkung von Colchizin auf Knorpelgewebe aus Organkulturen von Extremitätenknospen. Acta Anat 103:445–460

    Google Scholar 

  • Furthmayr H (ed) (1982) Immunochemistry of the extracellular matrix. CRC-Press, Boca Raton, Florida, vol I, II

    Google Scholar 

  • 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 31–48

    Google Scholar 

  • Geyer G (1973) Ultrahistochemie. Gustav Fischer Verlag, Jena

    Google Scholar 

  • Gosslau B, Barrach H-J (1979) Enzyme-linked immunosorbent microassay for quantification of specific antibodies to collagen type I, II, III. J Immunol Methods 29:71–77

    Google Scholar 

  • Gossrau R, Heger W, Merker H-J. Enzyme-histochemical studies of the endothelium of maternal vessels in the placenta of marmosets (Callithrix jacchus), in preparation

  • 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 77:4494–4498

    Google Scholar 

  • Hedman K, Vaheri A, Wartiovaara J (1978) External fibronectin of cultured human fibroblasts is predominantly a matrix protein. J Cell Biol 76:748–760

    Google Scholar 

  • 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 54:41–52

    Google Scholar 

  • Hill J (1932) On the developmental history of the primates. Croonian Lecture. Philos Trans R Soc Lond [Biol] 221:45–178

    Google Scholar 

  • Jollie W (1973) Fine structural changes in the placental membrane of the marmosets with increasing gestational age. Anat Rec 176:307–320

    Google Scholar 

  • Jollie W, Haar JL, Craig SS (1975) Fine structural observations on haematopoiesis in the chorioallantoic placenta of the marmosets. Am J Anat 144:9–38

    Google Scholar 

  • Kefalides NA (ed) (1978) Biology and chemistry of basement membranes. Academic Press, New York

    Google Scholar 

  • 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 30:991–998

    Google Scholar 

  • Luckett W (1974) Comparative development and evolution of the placenta in primates. Contrib Primatol 3:142–234

    Google Scholar 

  • 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 157–182

    Google Scholar 

  • Luckett W, Szalay F (eds) (1975) Phylogeny of the Primates. A multidisciplinary Approach. Plenum Press, New York

    Google Scholar 

  • Ludwig K (1981) Vergleichende Anatomie der Plazenta. In: Becker V, Schiebler Th, Kubli F (eds) Die Plazenta des Menschen. Thieme Verlag, Stuttgart pp 1–12

    Google Scholar 

  • 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 6–24

    Google Scholar 

  • Merker H-J, Barrach H-J (1981) The morphology of basement membrane formation. Eur J Cell Biol 26:111–120

    Google Scholar 

  • Palotie A, Tryggvason K, Peltonen L, Seppä H (1983) Components of subendothelial aorta basement membrane. Immunohistochemical localization and role in cell attachment. Lab Invest 49:362–370

    Google Scholar 

  • Phillips J, Grist S (1975) The use of transabdominal palpation to determine the course of pregnancy in the marmoset, Callithrix jacchus. J Reprod Fertil 43:103–108

    Google Scholar 

  • Romeis B (1968) Mikroskopische Technik. Oldenburg Verlag, München Wien

    Google Scholar 

  • Sage H, Bornstein P (1979) Characterization of a novel collagen chain in human placenta and its relation to AB collagen. Biochemistry 18:3815–3822

    Google Scholar 

  • Sage H, Woodbury RG, Bornstein P (1979) Structural studies on human type IV collagen. J Biol Chem 254:9893–9900

    Google Scholar 

  • 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 243:535–543

    Google Scholar 

  • Smith BD, McKenney KH, Lustberg TJ (1977) Characterization of collagen precursors found in rat skin and rat bone. Biochemistry 16:2980–2985

    Google Scholar 

  • Starck D (1978) Primaten. In: Vergleichende Anatomie der Wirbeltiere, vol I. Springer Verlag, Heidelberg, pp 189–200

    Google Scholar 

  • Szalay F, Delson E (1979) Infraorder platyrrhini. In: Evolutionary History of the Primates. Academic Press, New York, pp 275–302

    Google Scholar 

  • 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 267–278

    Google Scholar 

  • Timpl R, Rohde H, Geron RP, Rennard SJ, Foidart J-M, Martin GR (1979) Laminin — a glycoprotein from basement membranes. J Biol Chem 254:9933–9937

    Google Scholar 

  • Trelstad RL, Catanese VM, Rubin DF (1976) Collagen fractionation: Separation of native types I, II and III by differential precipitation. Anal Biochem 71:114–118

    Google Scholar 

  • 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 1–8

    Google Scholar 

  • Wislocki G (1929) On the placentation of primates, with a consideration of the phylogeny of the placenta. Contrib Embryol Carneg Inst 111:51–80

    Google Scholar 

  • Wislocki G (1932) Placentation in the marmoset (Oedipomidas Geoffroyi) with remarks on twinning in monkeys. Anat Rec 52:381–399

    Google Scholar 

  • Wislocki G (1943) Hemopoiesis in the chorionic villi of the placenta of Platyrrhine monkeys. Anat Rec 85:349–364

    Google Scholar 

Download references

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Merker, H.J., Bremer, D., Barrach, H.J. et al. The basement membrane of the persisting maternal blood vessels in the placenta of Callithrix jacchus. Anat Embryol 176, 87–97 (1987). https://doi.org/10.1007/BF00309756

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