Skip to main content
SpringerLink
Log in

The cell surface of a restrictive fenestrated endothelium

I. Distribution of lectin-receptor monosaccharides on the choriocapillaris

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

Summary

The choriocapillaris is one example of a capillary bed lined by a fenestrated endothelium that is restrictive to exogenous tracers and endogenous plasma proteins. In this study we have examined the distribution of cell-surface monosaccharides utilizing biotinylated lectin-avidin ferritin cytochemistry. Receptors for wheat germ agglutinin were localized to the plasmalemma and diaphragms of some fenestrae, vesicles, and channels at the luminal endothelial front in amounts greater than seen for the other lectins employed. The absence of labeling following inhibition with N-acetylglucosamine and after tissue digestion with N-acetylhexosaminidase, but not after neuraminidase indicated that this lectin marked N-acetylglucosamine residues and not sialic acid. Wheat germ agglutinin receptors were not affected by pronase E or trypsin digestion, but were partially removed by proteinase K. The latter also removed many fenestral diaphragms. Wheat germ agglutinin receptors were cleaved with endoglycosidase D. The combined results indicate that the wheat germ agglutinin receptor is of the low-mannose type and part of a protein with hydrophobic properties. Receptors for concanavalin A (mannose) and Ricinus communis agglutinin (galactose) were also localized to the plasmalemma and endothelial diaphragms. The examination of sections at different tilt angles revealed that these lectins bound to the endothelium in a non-random distribution, encircling diaphragms of fenestrae and channels. Soybean agglutinin (N-acetylgalactosamine) marked endothelial structures sparsely. Following digestion with pronase E or trypsin, receptor sugars for the latter three lectins were completely removed, indicating their presence on protease susceptible glycoproteins. These findings demonstrate that the endothelium of the choriocapillaris bears carbohydrate moieties that are different than those described for permeable fenestrated endothelia.

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

  • Bankston PW, Milici AJ (1983) A survey of the binding of polycationic ferritin in several fenestrated capillary beds: indication of heterogeneity in the luminal glycocalyx of fenestral diaphragms. Microvasc Res 26:36–48

    Google Scholar 

  • Bearer EL, Orci L (1985) Endothelial fenestral diaphragms: a quick-freeze, deep-etch study. J Cell Biol 100:418–428

    Google Scholar 

  • Bignon J, Jaubert F, Jaurand MC (1976) Plasma protein immunocytochemistry and polysaccharide cytochemistry at the surface of alveolar and endothelial cells in the rat lung. J Histochem Cytochem 24:1076–1084

    Google Scholar 

  • Bretton R, Bariety J (1974) Ultrastructural localization of concanavalin A in normal rat kidney glomeruli and arterioles. J Ultrastruct Res 48:396–403

    Google Scholar 

  • Bretton R, Bariety J (1976) A comparative ultrastructural localization of concanavalin A, wheat germ agglutinin and Ricinus communis on glomeruli of normal rat kidney. J Histochem Cytochem 24:1093–1100

    Google Scholar 

  • Clementi F, Palade GE (1969a) Intestinal capillaries. I. Permeability to peroxidase and ferritin. J Cell Biol 41:33–58

    Google Scholar 

  • Clementi F, Palade GE (1969b) Intestinal capillaries. II. Structural effects of EDTA and histamine. J Cell Biol 42:706–714

    Google Scholar 

  • Debray H, Decout D, Strecker G, Spik G, Montreuil J (1981) Specificity of twelve lectins towards oligosaccharides and glyco-peptides related to N-glycosylproteins. Eur J Biochem 117:41–55

    Google Scholar 

  • Ebling W, Hennrich N, Klockow M, Metz H, Orth HD, Lang H (1974) Proteinase K from Tritirachium album limber. Eur J Biochem 47:91–97

    Google Scholar 

  • Essner E, Gordon SR (1983) Observations on the permeability of the choriocapillaris of the eye. Cell Tissue Res 231:571–577

    Google Scholar 

  • Goldstein U, Hayes CE (1978) The lectins: carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem 35:127–340

    Google Scholar 

  • Gordon JA, Staehelin LA, Kuettner CA (1977) Lectin-mediated agglutination of erythrocyte ghost membranes following depletion of membrane protein and intramembrane particles. Exp Cell Res 110:439–448

    Google Scholar 

  • Graham RC, Karnovsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney. Ultrastructural cytochemistry by a new technique. J Histochem Cytochem 15:291–302

    Google Scholar 

  • Green NM (1963) Avidin. I. The use of 14C biotin for kinetic studies and for assay. Biochem J 89:585–591

    Google Scholar 

  • Holthofer H, Virtnen I, Kariniemi A-L, Hormia M, Linder E, Miettinen A (1982) Ulex europaeus I lectin as a marker for vascular endothelium in human tissues. Lab Invest 47:60–66

    Google Scholar 

  • Hurley JV, McCallum NEW (1974) The degree and functional significance of the escape of marker particles from small blood vessels with fenestrated endothelium. J Pathol 113:183–196

    Google Scholar 

  • Koide N, Muramatsu T (1974) End-β-N-acetylglucosaminidase acting on carbohydrate moieties of glycoproteins. Purification and properties of the enzymes from Diplococcus pneumoniae. J Biol Chem 249:4897–4904

    Google Scholar 

  • Kornfeld R, Kornfeld S (1970) The structure of a phytohemagglutinin receptor from human erythrocytes. J Biol Chem 245:2536–2545

    Google Scholar 

  • Linker A, Hovingh P (1972) Heparinase and heparitinase from Flavobacteria. In Ginsberg V (ed) Methods in enzymology, Vol 28. Academic Press, New York, pp 902–911

    Google Scholar 

  • Luft JH (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409–414

    Article  CAS  PubMed  Google Scholar 

  • Monsigny M, Roche A-C, Sene C, Maget-Dana R, Delmotte F (1980) Sugar-lectin interactions: how does wheat-germ agglutinin bind sialoglycoconjugates? Eur J Biochem 104:147–153

    Google Scholar 

  • Morihara K, Tsuzuki H (1975) Specificity of proteinase K from Tritirachium album limber for synthetic peptides. Agr Biol Chem 39:1489–1492

    Google Scholar 

  • Muller LI, Jacks TJ (1975) Rapid chemical dehydration of samples for electron microscopic examinations. J Histochem Cytochem 23:107–110

    Google Scholar 

  • Nicolson GL (1976) Trans-membrane control of the receptors on normal and tumor cells. I. Cytoplasmic influence over cell surface components. Biochim Biophys Acta 457:57–108

    Google Scholar 

  • Novikoff AB, Novikoff PM, Davis C, Quintana N (1972) Diffusion artifacts in 3,3′-diaminobenzidine cytochemistry. J Histochem Cytochem 20:745–749

    Google Scholar 

  • Peters K-R, Milici AJ (1983) High resolution scanning electron microscopy of the luminal surface of a fenestrated capillary endothelium. J Cell Biol 97: 336a

  • Pino RM (1984a) Ultrastructural localization of lectin receptors on the bone-marrow sinusoidal endothelium of the rat. Am J Anat 169:259–272

    Google Scholar 

  • Pino RM (1984b) Ultrastructural localization of lectin receptors on the surface of the rat retinal pigment epithelium. Decreased sensitivity of the avidin-biotin method due to cell surface charge. J Histochem Cytochem 32:862–868

    Google Scholar 

  • Pino RM (1984c) Heparin and heparan sulfate domains on a fenestrated endothelium. Third Intl Symposium on the Biology of the Vascular Endothelial Cell, Cambridge, MA, abstracts: 32

  • Pino RM (1985) Restriction to endogenous plasma proteins by a fenestrated capillary endothelium: an ultrastructural immunocytochemical study of the choriocapillary endothelium. Am J Anat 172:279–289

    Google Scholar 

  • Pino RM (1986) The cell surface of a restrictive fenestrated endothelium. II. Dynamics of cationic ferritin binding and the identification of heparin and heparan sulfate domains on the choriocapillaris. Cell Tissue Res 243:157–164

    Google Scholar 

  • Pino RM, Essner E (1980) Structure and permeability to ferritin of the choriocapillary endothelium of the rat eye. Cell Tissue Res 208:21–27

    Google Scholar 

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

    Google Scholar 

  • Pino RM, Thouron CL (1983) Vascular permeability in the rat eye to endogenous albumin and immunoglobulin G (IgG) examined by immunohistochemical methods. J Histochem Cytochem 31:411–416

    Google Scholar 

  • Pino RM, Essner E, Pino LC (1982a) Permeability of the neonate rat choriocapillaris to hemeproteins and ferritin. Am J Anat 164:333–341

    Google Scholar 

  • Pino RM, Essner E, Pino LC (1982b) Location and chemical composition of anionic sites in Bruch's membrane of the rat. J Histochem Cytochem 30:245–252

    Google Scholar 

  • Rafelson ME, Gold S, Priede I (1966) Neuraminidase (sialidase) from Influenza virus. In Neufeld EF, Ginsberg V (eds) Methods in enzymology, Vol 8. Academic Press, New York, pp 677–680

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 67:638–646

    Google Scholar 

  • Schneeberger EE, Hamelin M (1984) Interaction of serum proteins with lung endothelial glycocalyx: its effect on endothelial permeability. Am J Physiol 247 (Heart Circ Physiol 16):H206-H217

    Google Scholar 

  • Sharon N, Lis H (1982) Glycoproteins. In Neurath H, Hill RL (eds) The proteins, Vol 5. Academic Press, New York, pp 1–144

    Google Scholar 

  • Shimamura T, Morrison AB (1973) Vascular permeability of the medullary vessels in the mouse and rat. Am J Pathol 71:155–166

    Google Scholar 

  • Simionescu M, Simionescu N, Silbert JE, Palade GE (1981) Differentiated microdomains on the luminal surface of the capillary endothelium. II. Partial characterization of their anionic sites. J Cell Biol 90:614–621

    Google Scholar 

  • Simionescu M, Simionescu N, Palade GE (1982) Differentiated microdomains on the luminal surface of capillary endothelium: Distribution of lectin receptors. J Cell Biol 71:218–231

    Google Scholar 

  • Simionescu N, Simionescu M, Palade GE (1972) Permeability of intestinal capillaries. Pathway followed by dextrans and glycogens. J Cell Biol 53:365–392

    Google Scholar 

  • Simionescu N, Lupu F, Simionescu M (1983) Rings of membrane sterols surround the openings of vesicles and fenestrae, in capillary endothelium. J Cell Biol 97:1592–1600

    Google Scholar 

  • Stein O, Chajek T, Stein Y (1976) Ultrastructural localization of concanavalin A in the perfused rat heart. Lab Invest 35:103–110

    Google Scholar 

  • Venkatachalam MA, Karnovsky MJ (1972) Extravascular protein in the kidney. An ultrastructural study of its relation to renal peritubular capillarypermeability using protein tracers. Lab Invest 27:435–444

    Google Scholar 

  • Weber G, Fabbrini P, Resi L (1973) On the presence of concanavalin A reactive coat over the endothelial aortic surface and its modification during early experimental cholesterol atherogenesis in rabbits. Virchows Arch (Pathol Anat) 359:299–307

    Google Scholar 

  • Wolff JR (1977) Ultrastructure of the terminal vascular bed as related to function. In: Kaley G, Altura BM (eds) Microcirculation. University Park Press, Baltimore, pp 95–130

    Google Scholar 

  • Yamamoto K, Tsutomu T, Matsumoto I, Osawa T (1981) Structural requirements for the binding of oligosaccharides and glycopeptides to immobilized wheat germ agglutinin. Biochemistry 20:5894–5899

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Louisiana State University Medical Center, New Orleans, Louisiana, USA

    Richard M. Pino

Authors
  1. Richard M. Pino
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported by NIH EY 03776

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pino, R.M. The cell surface of a restrictive fenestrated endothelium. Cell Tissue Res. 243, 145–155 (1986). https://doi.org/10.1007/BF00221863

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00221863

Key words

Search

Navigation