Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 Apr 1;102(4):1304–1311. doi: 10.1083/jcb.102.4.1304

Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis

PMCID: PMC2114181  PMID: 3007533

Abstract

The interaction of homologous and heterologous albumin-gold complex (Alb-Au) with capillary endothelium was investigated in the mouse lung, heart, and diaphragm. Perfusion of the tracer in situ for from 3 to 35 min was followed by washing with phosphate-buffered saline, fixation by perfusion, and processing for electron microscopy. From the earliest time examined, one and sometimes two rows of densely packed particles bound to some restricted plasma membrane microdomains that appeared as uncoated pits, and to plasmalemmal vesicles open on the luminal front. Morphometric analysis, using various albumin-gold concentrations, showed that the binding is saturable at a very low concentration of the ligand and short exposure. After 5 min, tracer-carrying vesicles appeared on the abluminal front, discharging their content into the subendothelial space. As a function of tracer concentration 1-10% of plasmalemmal vesicles contained Alb-Au particles in fluid phase; from 5 min on, multivesicular bodies were labeled by the tracer. Plasma membrane, coated pits, and coated vesicles were not significantly marked at any time interval. Heparin or high ionic strength did not displace the bound Alb-Au from vesicle membrane. No binding was obtained when Alb-Au was competed in situ with albumin or was injected in vivo. Gold complexes with fibrinogen, fibronectin, glucose oxidase, or polyethyleneglycol did not give a labeling comparable to that of albumin. These results suggest that on the capillary endothelia examined, the Alb-Au is adsorbed on specific binding sites restricted to uncoated pits and plasmalemmal vesicles. The tracer is transported in transcytotic vesicles across endothelium by receptor-mediated transcytosis, and to a lesser extent is taken up by pinocytotic vesicles. The existence of albumin receptors on these continuous capillary endothelia may provide a specific mechanism for the transport of albumin and other molecules carried by this protein.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alberti A., Pontisso P., Chemello L., Schiavon E., Realdi G. Virus receptors for polymerized human serum albumin and anti-receptor antibody in hepatitis B virus infection. Prog Clin Biol Res. 1983;143:327–336. [PubMed] [Google Scholar]
  2. Baldwin A. L., Chien S. Endothelial transport of anionized and cationized ferritin in the rabbit thoracic aorta and vasa vasorum. Arteriosclerosis. 1984 Jul-Aug;4(4):372–382. doi: 10.1161/01.atv.4.4.372. [DOI] [PubMed] [Google Scholar]
  3. Bundgaard M., Frøkjaer-Jensen J., Crone C. Endothelial plasmalemmal vesicles as elements in a system of branching invaginations from the cell surface. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6439–6442. doi: 10.1073/pnas.76.12.6439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Corvol P., Bardin C. W. Species distribution of testosterone-binding globulin. Biol Reprod. 1973 Apr;8(3):277–282. doi: 10.1093/biolreprod/8.3.277. [DOI] [PubMed] [Google Scholar]
  5. Curry F. E., Michel C. C. A fiber matrix model of capillary permeability. Microvasc Res. 1980 Jul;20(1):96–99. doi: 10.1016/0026-2862(80)90024-2. [DOI] [PubMed] [Google Scholar]
  6. EVERETT N. B., SIMMONS Measurement and radioautographic localization of albumin in rat tissues after intravenous administration. Circ Res. 1958 May;6(3):307–313. doi: 10.1161/01.res.6.3.307. [DOI] [PubMed] [Google Scholar]
  7. Forker E. L., Luxon B. A. Albumin-mediated transport of rose bengal by perfused rat liver. Kinetics of the reaction at the cell surface. J Clin Invest. 1983 Nov;72(5):1764–1771. doi: 10.1172/JCI111136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frøkjaer-Jensen J. Three-dimensional organization of plasmalemmal vesicles in endothelial cells. An analysis by serial sectioning of frog mesenteric capillaries. J Ultrastruct Res. 1980 Oct;73(1):9–20. doi: 10.1016/0022-5320(80)90111-2. [DOI] [PubMed] [Google Scholar]
  9. Ghitescu L., Fixman A. Surface charge distribution on the endothelial cell of liver sinusoids. J Cell Biol. 1984 Aug;99(2):639–647. doi: 10.1083/jcb.99.2.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hütter J. F., Piper H. M., Spieckermann P. G. Myocardial fatty acid oxidation: evidence for an albumin-receptor-mediated membrane transfer of fatty acids. Basic Res Cardiol. 1984 May-Jun;79(3):274–282. doi: 10.1007/BF01908027. [DOI] [PubMed] [Google Scholar]
  11. Jefferies W. A., Brandon M. R., Hunt S. V., Williams A. F., Gatter K. C., Mason D. Y. Transferrin receptor on endothelium of brain capillaries. Nature. 1984 Nov 8;312(5990):162–163. doi: 10.1038/312162a0. [DOI] [PubMed] [Google Scholar]
  12. King G. L., Johnson S. M. Receptor-mediated transport of insulin across endothelial cells. Science. 1985 Mar 29;227(4694):1583–1586. doi: 10.1126/science.3883490. [DOI] [PubMed] [Google Scholar]
  13. Paaske W. P. Microvascular exchange of albumin. Microvasc Res. 1983 Jan;25(1):101–107. doi: 10.1016/0026-2862(83)90046-8. [DOI] [PubMed] [Google Scholar]
  14. Perl W. Convection and permeation and albumin between plasma and interstitium. Microvasc Res. 1975 Jul;10(1):83–94. doi: 10.1016/0026-2862(75)90022-9. [DOI] [PubMed] [Google Scholar]
  15. Pino R. M., Thouron C. L. Vascular permeability in the rat eye to endogenous albumin and immunoglobulin G (IgG) examined by immunohistochemical methods. J Histochem Cytochem. 1983 Mar;31(3):411–416. doi: 10.1177/31.3.6827079. [DOI] [PubMed] [Google Scholar]
  16. Ramirez C. A., Colton C. K., Smith K. A., Stemerman M. B., Lees R. S. Transport of 125I-albumin across normal and deendothelialized rabbit thoracic aorta in vivo. Arteriosclerosis. 1984 May-Jun;4(3):283–291. doi: 10.1161/01.atv.4.3.283. [DOI] [PubMed] [Google Scholar]
  17. Rhodin J., Nicole P., Zweifach B. 1973 Eugene M. Landis Award presentation to Silvio Baez. Microvasc Res. 1974 Jan;7(1):1–2. doi: 10.1016/0026-2862(74)90031-4. [DOI] [PubMed] [Google Scholar]
  18. Rippe B., Kamiya A., Folkow B. Transcapillary passage of albumin, effects of tissue cooling and of increases in filtration and plasma colloid osmotic pressure. Acta Physiol Scand. 1979 Feb;105(2):171–187. doi: 10.1111/j.1748-1716.1979.tb06329.x. [DOI] [PubMed] [Google Scholar]
  19. Sage H., Johnson C., Bornstein P. Characterization of a novel serum albumin-binding glycoprotein secreted by endothelial cells in culture. J Biol Chem. 1984 Mar 25;259(6):3993–4007. [PubMed] [Google Scholar]
  20. Sharpe R. M. Gonadotrophin-induced accumulation of 'interstitial fluid' in the rat testis. J Reprod Fertil. 1979 Mar;55(2):365–371. doi: 10.1530/jrf.0.0550365. [DOI] [PubMed] [Google Scholar]
  21. Simionescu N. Cellular aspects of transcapillary exchange. Physiol Rev. 1983 Oct;63(4):1536–1579. doi: 10.1152/physrev.1983.63.4.1536. [DOI] [PubMed] [Google Scholar]
  22. Simionescu N., Simionescu M., Palade G. E. Permeability of intestinal capillaries. Pathway followed by dextrans and glycogens. J Cell Biol. 1972 May;53(2):365–392. doi: 10.1083/jcb.53.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Slot J. W., Geuze H. J. Sizing of protein A-colloidal gold probes for immunoelectron microscopy. J Cell Biol. 1981 Aug;90(2):533–536. doi: 10.1083/jcb.90.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Soda R., Tavassoli M. Transendothelial transport (transcytosis) of iron-transferrin complex in the bone marrow. J Ultrastruct Res. 1984 Jul;88(1):18–29. doi: 10.1016/s0022-5320(84)90178-3. [DOI] [PubMed] [Google Scholar]
  25. Spencer P. D. Is convection or permeation the major mechanism of albumin transfer? Microvasc Res. 1983 Nov;26(3):364–366. doi: 10.1016/0026-2862(83)90087-0. [DOI] [PubMed] [Google Scholar]
  26. Vasile E., Simionescu M., Simionescu N. Visualization of the binding, endocytosis, and transcytosis of low-density lipoprotein in the arterial endothelium in situ. J Cell Biol. 1983 Jun;96(6):1677–1689. doi: 10.1083/jcb.96.6.1677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vuento M., Vaheri A. Purification of fibronectin from human plasma by affinity chromatography under non-denaturing conditions. Biochem J. 1979 Nov 1;183(2):331–337. doi: 10.1042/bj1830331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Weisiger R., Gollan J., Ockner R. Receptor for albumin on the liver cell surface may mediate uptake of fatty acids and other albumin-bound substances. Science. 1981 Mar 6;211(4486):1048–1051. doi: 10.1126/science.6258226. [DOI] [PubMed] [Google Scholar]
  29. Widebäck K., Havlícek J., Kronvall G. Demonstration of a receptor for mouse and human serum albumin in Streptococcus pyogenes. Acta Pathol Microbiol Immunol Scand B. 1983 Dec;91(6):373–382. doi: 10.1111/j.1699-0463.1983.tb00063.x. [DOI] [PubMed] [Google Scholar]
  30. Williams S. K., Devenny J. J., Bitensky M. W. Micropinocytic ingestion of glycosylated albumin by isolated microvessels: possible role in pathogenesis of diabetic microangiopathy. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2393–2397. doi: 10.1073/pnas.78.4.2393. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES