Skip to main content
SpringerLink
Log in

Permeability of the foetal capillary endothelium of the guinea-pig placenta to haem proteins of various molecular sizes

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

Summary

Haem proteins of different molecular sizes were perfused into the foetal circulation of the guinea-pig placenta to study the permeability of the foetal endothelium.

The smallest molecules tested, microperoxidase (ae 1.0 nm) and cytochrome C (ae 1.5 nm), readily penetrated the endothelium; tracer-reaction product was found in the subendothelial space of the capillaries. However, there was no uptake of these two tracers into the syncytiotrophoblast layer of the placenta. An intermediate-sized molecule, myoglobin (ae 1.7 nm), produced only a weak reaction product in the subendothelial space even when perfused at high concentration. The largest molecule tested, haemoglobin (ae 2.8 nm), did not penetrate the foetal endothelium at any of the concentrations employed.

The foetal capillary endothelium thus provided a barrier to protein penetration from the foetal circulation, dependent on molecular size. There was evidence that the site of this barrier was located in the lateral intercellular spaces between the endothelial cells.

The syncytiotrophoblast of this haemomonochorial placenta provided an almost absolute barrier to protein penetration from the foetal circulation. As other workers have described maternal-to-foetal transmission of proteins across this layer in the guinea-pig, a working hypothesis of the role of endothelium and syncytiotrophoblast in maternal/foetal protein exchange is discussed.

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

  • Anderson WC (1972) The use of exogenous myoglobin as an ultrastructural tracer. Reabsorption and translocation of protein by the renal tubule. J Histochem Cytochem 20:672–684

    Google Scholar 

  • Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–677

    Google Scholar 

  • Cotran RS, Karnovsky MJ (1967) Vascular leakage induced by horseradish peroxidase in the rat. Proc Soc Exp Biol Med 126:557–561

    Google Scholar 

  • Crone Ch (1979) Permeability of single capillaries compared with results from whole-organ studies. Acta Physiol Scand Suppl 463:75–79

    Google Scholar 

  • Enders AC (1965) A comparative study of the fine structure of the trophoblast of several haemochorial placentas. Am J Anat 116:29–67

    Google Scholar 

  • Firth JA, Farr A (1977) Structural features and quantitative age-dependent changes in the intervascular barrier of the guinea-pig haemochorial placenta. Cell Tissue Res 184:507–516

    Google Scholar 

  • Frokjaer-Jensen J (1980a) Endothelial vesicles as part of permanent invaginations of plasmalemma demonstrated by serial sectioning of endothelial cells. J Physiol 301:70p

    Google Scholar 

  • Frokjaer-Jensen J (1980b) Three-dimensional organisation of plasmalemma vesicle in endothelial cells. An analysis by serial sectioning of frog mesenteric capillaries. J Ultrastruc Res 73:9–20

    Google Scholar 

  • Graham RC, Karnovsky MJ (1966) The early stage of absorption of injected horseradish peroxidase in the proximal tubule of the mouse kidney. Ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302

    Google Scholar 

  • Hedley R, Bradbury MW (1980) Transport of polar non-electrolytes across the intact and perfused guinea-pig placenta. Placenta 1:277–285

    Google Scholar 

  • Heinrich D, Metz J, Raviola E, Forssmann WG (1976) Ultrastructure of perfusion-fixed fetal capillaries in the human placenta. Cell Tissue Res 172:157–169

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A

    Google Scholar 

  • Kaufmann P (1981) Functional anatomy of the non-primate placenta. Placenta (Supplement 1):13–28

  • Kaufmann P, Davidoff M (1977) The guinea-pig placenta. Adv Anat Embryol Cell Biol 53:(2), 1–91

    Google Scholar 

  • Kaufmann P, Schröder H (1980) Protein transfer across the guinea-pig chorioallantoic placenta. XI International Congress of Anatomy, Mexico City 1980

  • King BF, Enders AC (1971) Protein absorption by the guinea-pig chorioallantoic placenta. Am J Anat 130:409–430

    Google Scholar 

  • Mann GE, Smaje LH, Yudilevich DL (1979) Permeability of the fenestrated capillaries in the cat submandibular gland to lipid-insoluble molecules. J Physiol 297:335–354

    Google Scholar 

  • Palade GE, Simionescu M, Simionescu N (1979) Structural aspects of the permeability of the microvascular endothelium. Acta Physiol Scand Suppl 463:11–32

    Google Scholar 

  • Pappenheimer JR, Renkin EM, Borrero LM (1951) Filtration, diffusion, and molecular sieving through peripheral capillary membranes. A contribution to the pore theory of capillary permeability. Am J Physiol 167:13–46

    Google Scholar 

  • Pietra GG, Szidon JP, Leventhal MM (1969) Haemoglobin as a tracer in haemodynamic pulmonary oedema. Sicence 166:1643–1646

    Google Scholar 

  • Pino RM, Essner E (1981) Permeability of rat choriocapillaris to hemeproteins. Restrictions of tracers by a fenestrated endothelium. J Histochem Cytochem 29 (2):281–290

    Google Scholar 

  • Reese TS, Karnovsky MJ (1967) Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Cell Biol 34:207–217

    Article  CAS  PubMed  Google Scholar 

  • Renkin EM (1978) Transport pathways through capillary endothelium. Microvas Res 15:123–135

    Google Scholar 

  • Renkin EM (1979) Relation of capillary morphology to transport of fluid and large molecules: a review. Acta Physiol Scand Suppl 463:81–91

    Google Scholar 

  • Rennke HG, Venkatachalam MA (1977) Structural determinants of glomerular permselectivity. Fed Proc 36:2619–2626

    Google Scholar 

  • Sibley CP, Bauman KF, Firth JA (1981) Ultrastructural study of the permeability of the guinea-pig placenta to horseradish peroxidase. Cell Tissue Res 219:637–647

    Google Scholar 

  • Simionescu N (1979) Enzymatic tracers in the study of vascular permeability. J Histochem Cytochem 27 (8):1120–1130

    Google Scholar 

  • Simionescu N, Simionescu M, Palade GE (1975) Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J Cell Biol 64:586–607

    Google Scholar 

  • Thornburg KL, Faber JJ (1977) Transfer of hydrophilic molecules by placenta and yolk sac of guineapig. Am J Physiol 233 (3):C111-C124

    Google Scholar 

  • Wissig SL (1979) Identification of the small pore in muscle capillaries. Acta Physiol Scand Suppl 463:33–44

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, St. George's Hospital Medical School, London, England

    C. P. Sibley, K. F. Bauman & J. A. Firth

Authors
  1. C. P. Sibley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. F. Bauman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. A. Firth
    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

Sibley, C.P., Bauman, K.F. & Firth, J.A. Permeability of the foetal capillary endothelium of the guinea-pig placenta to haem proteins of various molecular sizes. Cell Tissue Res. 223, 165–178 (1982). https://doi.org/10.1007/BF00221507

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00221507

Key words

Search

Navigation