Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1978 Aug 1;78(2):379–389. doi: 10.1083/jcb.78.2.379

Nonrandom distribution of sialic acid over the cell surface of bristle- coated endocytic vesicles of the sinusoidal endothelium cells

PMCID: PMC2110131  PMID: 29050

Abstract

Previous studies with protein tracers have shown that the luminal surface of the vascular endothelium of the bone marrow is endocytic. The endocytosis occurs through the formation of large bristle-coated vesicles (LCV). The anionic charge distribution in this process was examined at the luminal surface of the endothelial cell, At pH 1.8, colloidal iron (CI), native ferritin, and polycationic ferritin (PCF) are bound by the luminal surface of the endothelial cell, but not at the sites of LCV formation. PCF used over a pH range of 1.8--7.2 (CI is unstable at higher pH levels) revealed LCV binding of this agent in increasing manner from pH 3.5 upwards. PCF binding at low pH (1.8) at the endothelial cell surface was markedly reduced by neuraminidase. Neuraminidase did not reduce PCF binding by the endothelial cell surface nor by the LCV at higher pH levels. It is concluded that the luminal surface of the endothelial cell has exposed sialic acid groups which are absent or significantly diminished at endocytic sites. The free surface of the endothelial cells as well as the sites of endocytosis have, in addition, anionic material with a pKa higher than that of sialic acid (pKa 2.6). These anionic materials may be different at the sites of endocytosis as compared to those present at the free cell surface.

Full Text

The Full Text of this article is available as a PDF (3.4 MB).

Selected References

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

  1. Babaï F., Bernhard W. Détection cytochimique par l'acide phosphotungstique de certains polysaccharides sur coupes á congélation ultrafines. J Ultrastruct Res. 1971 Dec;37(5):601–617. doi: 10.1016/s0022-5320(71)80028-x. [DOI] [PubMed] [Google Scholar]
  2. Becker R. P., De Bruyn P. P. The transmural passage of blood cells into myeloid sinusoids and the entry of platelets into the sinusoidal circulation; a scanning electron microscopic investigation. Am J Anat. 1976 Feb;145(2):183–205. doi: 10.1002/aja.1001450204. [DOI] [PubMed] [Google Scholar]
  3. Bennett K. D., Bondareff W. Age related differences in binding of concanavalin A to plasma membranes of isolated neurons. Am J Anat. 1977 Sep;150(1):175–184. doi: 10.1002/aja.1001500112. [DOI] [PubMed] [Google Scholar]
  4. Blanquet P., Puvion E., Driessens J. Localisation ultrastructurale, avec contrôle microspectrophotométrique, des sialo-glycoconjugués de la membrane plasmique cellulaire par la méthode fondée sur la capture de l'hydroxyde de fer colloïdal. C R Acad Sci Hebd Seances Acad Sci D. 1970 Jul 6;271(1):96–99. [PubMed] [Google Scholar]
  5. Curran R. C., Clark A. E., Lovell D. Acid mucopolysaccharides in electron microscopy. The use of the colloidal iron method. J Anat. 1965 Jul;99(Pt 3):427–434. [PMC free article] [PubMed] [Google Scholar]
  6. Danon D., Goldstein L., Marikovsky Y., Skutelsky E. Use of cationized ferritin as a label of negative charges on cell surfaces. J Ultrastruct Res. 1972 Mar;38(5):500–510. doi: 10.1016/0022-5320(72)90087-1. [DOI] [PubMed] [Google Scholar]
  7. De Bruyn P. P., Breen P. C., Thomas T. B. The microcirculation of the bone marrow. Anat Rec. 1970 Sep;168(1):55–68. doi: 10.1002/ar.1091680105. [DOI] [PubMed] [Google Scholar]
  8. De Bruyn P. P., Michelson S., Becker R. P. Endocytosis, transfer tubules, and lysosomal activity in myeloid sinusoidal endothelium. J Ultrastruct Res. 1975 Nov;53(2):133–151. doi: 10.1016/s0022-5320(75)80131-6. [DOI] [PubMed] [Google Scholar]
  9. De Bruyn P. P., Michelson S., Becker R. P. Phosphotungstic acid as a marker for the endocytic-lysosomal system (vacuolar apparatus) including transfer tubules of the lining cells of the sinusoids in the bone marrow and liver. J Ultrastruct Res. 1977 Jan;58(1):87–95. doi: 10.1016/s0022-5320(77)80010-5. [DOI] [PubMed] [Google Scholar]
  10. De Bruyn P. P., Michelson S., Thomas T. B. The migration of blood cells of the bone marrow through the sinusoidal wall. J Morphol. 1971 Apr;133(4):417–437. doi: 10.1002/jmor.1051330406. [DOI] [PubMed] [Google Scholar]
  11. Friend D. S., Farquhar M. G. Functions of coated vesicles during protein absorption in the rat vas deferens. J Cell Biol. 1967 Nov;35(2):357–376. doi: 10.1083/jcb.35.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gasic G. J., Berwick L., Sorrentino M. Positive and negative colloidal iron as cell surface electron stains. Lab Invest. 1968 Jan;18(1):63–71. [PubMed] [Google Scholar]
  13. Glick D., Scott J. E. Phosphotungstic acid not a stain for polysaccharide. J Histochem Cytochem. 1970 Jun;18(6):455–455. doi: 10.1177/18.6.455. [DOI] [PubMed] [Google Scholar]
  14. Grinnell F., Tobleman M. Q., Hackenbrock C. R. The distribution and mobility of anionic sites on the surfaces of baby hamster kidney cells. J Cell Biol. 1975 Sep;66(3):470–479. doi: 10.1083/jcb.66.3.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HUDSON G., YOFFEY J. M. RETICULO-ENDOTHELIAL CELLS IN THE BONE MARROW OF THE GUINEA-PIG. J Anat. 1963 Jul;97:409–416. [PMC free article] [PubMed] [Google Scholar]
  16. Hardin J. H., Spicer S. S. Ultrastructural localization of dialyzed iron-reactive mucosubstance in rabbit heterophils, basophils, and eosinophils. J Cell Biol. 1971 Feb;48(2):368–386. doi: 10.1083/jcb.48.2.368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Haydon D. A., Seaman G. V. Electrokinetic studies on the ultrastructure of the human erythrocyte. I. Electrophoresis at high ionic strengths--the cell as a polyanion. Arch Biochem Biophys. 1967 Oct;122(1):126–136. doi: 10.1016/0003-9861(67)90131-2. [DOI] [PubMed] [Google Scholar]
  18. Hudson G., Yoffey J. M. Ultrastructure of reticuloendothelial elements in guinea-pig bone marrow. J Anat. 1968 Nov;103(Pt 3):515–525. [PMC free article] [PubMed] [Google Scholar]
  19. Katsuyama T., Spicer S. S. The surface characteristics of the plasma membrane of the exocrine pancreas. Am J Anat. 1977 Apr;148(4):535–554. doi: 10.1002/aja.1001480409. [DOI] [PubMed] [Google Scholar]
  20. Kuettner K. E., Croxen R. L., Eisenstein R., Sorgente N. Proteinase inhibitor activity in connective tissues. Experientia. 1974 Jun 15;30(6):595–597. doi: 10.1007/BF01921492. [DOI] [PubMed] [Google Scholar]
  21. Leduc E. H., Bernhard W. Recent modifications of the glycol methacrylate embedding procedure. J Ultrastruct Res. 1967 Jul;19(1):196–199. doi: 10.1016/s0022-5320(67)80068-6. [DOI] [PubMed] [Google Scholar]
  22. Nagura H., Asai J., Katsumata Y., Kojima K. Role of electric surface charge of cell membrane in phagocytosis. Acta Pathol Jpn. 1973 May;23(2):279–290. doi: 10.1111/j.1440-1827.1973.tb00792.x. [DOI] [PubMed] [Google Scholar]
  23. Nicolson G. L. Anionic sites of human erythrocyte membranes. I. Effects of trypsin, phospholipase C, and pH on the topography of bound positively charged colloidal particles. J Cell Biol. 1973 May;57(2):373–387. doi: 10.1083/jcb.57.2.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Noseworthy J., Jr, Korchak H., Karnovsky M. L. Phagocytosis and the sialic acid of the surface of polymorphonuclear leukocytes. J Cell Physiol. 1972 Feb;79(1):91–96. doi: 10.1002/jcp.1040790110. [DOI] [PubMed] [Google Scholar]
  25. Palladini G., Lauro G., Basile A. Observations sur la spécificité de la coloration aux acides phosphotungstique et phosphomolybdique. Histochemie. 1970;24(4):315–321. [PubMed] [Google Scholar]
  26. Pease D. C. Phosphotungstic acid as a specific electron stain for complex carbohydrates. J Histochem Cytochem. 1970 Jun;18(6):455–458. doi: 10.1177/18.6.455-a. [DOI] [PubMed] [Google Scholar]
  27. Pease D. C. Polysaccharides associated with the exterior surface of epithelial cells: kidney, intestine, brain. J Ultrastruct Res. 1966 Aug;15(5):555–588. doi: 10.1016/s0022-5320(66)80128-4. [DOI] [PubMed] [Google Scholar]
  28. Quintarelli G., Cifonelli J. A., Zito R. On phosphotungstic acid staining. II. J Histochem Cytochem. 1971 Nov;19(11):648–653. doi: 10.1177/19.11.648. [DOI] [PubMed] [Google Scholar]
  29. Quintarelli G., Zito R., Cifonelli J. A. On phosphotungstic acid staining. I. J Histochem Cytochem. 1971 Nov;19(11):641–647. doi: 10.1177/19.11.641. [DOI] [PubMed] [Google Scholar]
  30. Quinton P. M., Philpott C. W. A role for anionic sites in epithelial architecture. Effects of cationic polymers on cell membrane structure. J Cell Biol. 1973 Mar;56(3):787–796. doi: 10.1083/jcb.56.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. RINEHART J. F., ABUL-HAJ S. K. An improved method for histologic demonstration of acid mucopolysaccharides in tissues. AMA Arch Pathol. 1951 Aug;52(2):189–194. [PubMed] [Google Scholar]
  32. Rambourg A. Morphological and histochemical aspects of glycoproteins at the surface of animal cells. Int Rev Cytol. 1971;31:57–114. doi: 10.1016/s0074-7696(08)60057-1. [DOI] [PubMed] [Google Scholar]
  33. Scott J. E., Glick D. The invalidity of "phosphotungstic acid as a specific electron stain for complex carbohydrates". J Histochem Cytochem. 1971 Jan;19(1):63–64. doi: 10.1177/19.1.63. [DOI] [PubMed] [Google Scholar]
  34. Scott J. E. Letter: Phosphotungstic acid. "Schiff-reactive" but not a "glycol reagent". J Histochem Cytochem. 1973 Dec;21(12):1084–1085. doi: 10.1177/21.12.1084. [DOI] [PubMed] [Google Scholar]
  35. Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  36. Skutelsky E., Danon D. Redistribution of surface anionic sites on the luminal front of blood vessel endothelium after interaction with polycationic ligand. J Cell Biol. 1976 Oct;71(1):232–241. doi: 10.1083/jcb.71.1.232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Skutelsky E., Farquhar M. G. Variations in distribution of con A receptor sites and anionic groups during red blood cell differentiation in the rat. J Cell Biol. 1976 Oct;71(1):218–231. doi: 10.1083/jcb.71.1.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weiss L., Mayhew E., Ulrich K. The effect of neuraminidase on the phagocytic process in human monocytes. Lab Invest. 1966 Aug;15(8):1304–1309. [PubMed] [Google Scholar]
  39. Weiss L., Zeigel R. Cell surface negativity and the binding of positively charged particles. J Cell Physiol. 1971 Apr;77(2):179–186. doi: 10.1002/jcp.1040770208. [DOI] [PubMed] [Google Scholar]
  40. Wetzel M. G., Wetzel B. K., Spicer S. S. Ultrastructural localization of acid mucosubstances in the mouse colon with iron-containing stains. J Cell Biol. 1966 Aug;30(2):299–315. doi: 10.1083/jcb.30.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES