Skip to main content
Log in

Mucosubstances of rabbit granulocytes studied by means of electron-microscopic radioautography and X-ray microanalysis

  • Published:
Histochemistry Aims and scope Submit manuscript

Summary

Rabbit bone marrow cells have been studied by means of light-and electron-microscopic radioautography and X-ray microanalysis. Carrier free sulfuric acid was used as the radioactive precursor in this experiment. Immature granulocytes showed more active incorporation than mature ones. Silver grains were observed in the Golgi apparatus and granules in three kinds of granulocytes. Electron-microscopically, immature granules showed the incorporation of inorganic sulfate, while mature ones did not. Sulfur was detected in all kinds of granules of the three granulocyte types by X-ray microanalysis. It is concluded that incorporated inorganic sulfur may be utilized for the synthesis of acid glycosaminoglycans and the sulfur detected by X-ray microanalysis may be that contained in the acid glycosaminoglycan. The sulfur detected in the specific granules of the heterophil probably derives from proteins or polypeptides incorporating sulfur containing amino acids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ackerman, G.A.: Cytochemical properties of the blood basophilic granulocyte. Ann. N. Y. Acad. Sci. 103, 376–393 (1963)

    Google Scholar 

  • Avila, J.L., Convit, J.: Inhibition of leucocytic lysosomal enzymes by glycosaminoglycans in vitro. Biochem. J. 152, 57–64 (1975)

    Google Scholar 

  • Avila, J.L., Convit, J.: Physicochemical characteristics of the glycosaminoglycan-lysosomal enzyme interaction in vitro: a model of control of leucocytic lysosomal activity. Biochem. J. 160, 129–136 (1976)

    Google Scholar 

  • Avila, J.L.: The influence of the type of sulphate bond and degree of sulphation of glycosaminoglycans on their interaction with lysosomal enzymes. Biochem. J. 171, 489–491 (1978)

    Google Scholar 

  • Berg, N.B., Young, R.W.: Sulfate metabolism in pancreatic acinar cells. J. Cell Biol. 50, 469–483 (1971)

    Google Scholar 

  • Catini, C., Gheri, G., Miliani, A., Di Guglielmo, R.: Démonstration et caractérisation cytochemique des mucopolysaccharides acides des séries granulocytaires normales. Nouv. Rev. Fr. Hématol. 15, 307–318 (1975)

    Google Scholar 

  • Clausen, J., Anderson, V.: Acid mucopolysaccharides in human leukocytes. Clin. Chim. Acta 8, 505–512 (1963)

    Google Scholar 

  • Dunn, W.B., Spicer, S.S.: Histochemical demonstration of sulfated mucosubstances and cationic proteins in human granulocytes and platelets. J. Histochem. Cytochem. 17, 668–674 (1969)

    Google Scholar 

  • Dziewiatkowski, D.D.: Rate of excretion of radioactive sulfur and its concentration in some tissues of the rat after intraperitoneal administration of labeled sodium sulfate. J. Biol. Chem. 178, 197–202 (1949)

    Google Scholar 

  • Dziewiatkowski, D.D.: Utilization of sulfate sulfur in the rat for the synthesis of cystine. J. Biol. Chem. 207, 181–186 (1954)

    Google Scholar 

  • Ellis, F., Lajtha, L.G., Oliver, R.: Uptake of sulphate 35S by leukaemic human bone marrow in vitro. J. Clin. Pathol. 8, 166–167 (1955)

    Google Scholar 

  • Fedorko, M.E., Morse, S.I.: Isolation, characterization, and distribution of acid mucopolysaccharides in rabbit leukocytes. J. Exp. Med. 121, 39–48 (1965)

    Google Scholar 

  • Godman, G.C., Lane, N.: On the site of sulfation in the chondrocyte. J. Cell Biol. 21, 353–366 (1964)

    Google Scholar 

  • Greulich, R.C.: Utilization of sulfate ion by eosinophile myelocytes in the rat. Exp. Cell Res. 11, 225–228 (1956)

    Google Scholar 

  • Gregory, J.D., Robbins, P.W.: Metabolism of sulfur compounds (sulfate metabolism). Ann. Rev. Biochem. 29, 347–364 (1960)

    Google Scholar 

  • Hardin, J.H., Spicer, S.S.: Ultrastructural localization of dialyzed iron-reactive mucosubstance in rabbit heterophils, basophils and eosinophils. J. Cell Biol. 48, 368–386 (1971)

    Google Scholar 

  • Horn, R.G., Spicer, S.S.: Sulfated mucopolysaccharide and basic protein in certain granules of rabbit leukocytes. Lab. Invest. 13, 1–15 (1964)

    Google Scholar 

  • Jaques, L.B., Mahadoo, J., Riley, J.F.: The mast cell/heparin paradox. Lancet 1977/I, 411–413

  • Lajtha, L.G., Ellis, F., Oliver, R.: Isotope uptake of individual cells: Uptake of S35-sulphate by human bone-marrow cells in vitro. Br. J. Cancer 7, 401–406 (1953)

    Google Scholar 

  • Lane, N., Caro, L., Otero-Vilardebó, L.R.: Godman, G.C.: On the site of sulfation in colonic goblet cells. J. Cell Biol. 21, 339–351 (1964)

    Google Scholar 

  • Lau, P., Cornwell, G.G. III., Williams, W.J.: Mucopolysaccharide synthesis by human bone marrow in short-term suspension culture. J. Lab. Clin. Med. 76, 739–746 (1970)

    Google Scholar 

  • Lettré, H., Paweletz, N.: Problem der elektronenmikroskopischen Autoradiographie. Naturwissenschaften 53, 268–271 (1966)

    Google Scholar 

  • Luft, J.H.: Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol. 9, 401–414 (1961)

    Google Scholar 

  • Monneron, A., Moulé, Y.: Critical evaluation of specificity in electron microscopical radioautography in animal tissues. Exp. Cell Res. 56, 179–193 (1969)

    Google Scholar 

  • Murata, F., Spicer, S.S.: Morphologic and cytochemical studies of rabbit heterophilic leukocytes: evidence for tertiary granules. Lab. Invest. 29, 65–72 (1973)

    Google Scholar 

  • Murata, F., Hardin, J.H., Spicer, S.S.: Coexistence of acid phosphatase and acid mucosubstance in the nucleoid of human blood platelet granules. Histochemie 35, 319–329 (1973)

    Google Scholar 

  • Murata, F., Nagata, T.: Radioautographic studies on the, mucosubstances of the leukocyte. Acta Histochem. Cytochem. 8, 76 (1975a)

    Google Scholar 

  • Murata, F., Nagata, T.: Radioautography of rat bone marrow cells with 35SO4. Acta Anat. Nippon 50, 61–62 (1975b)

    Google Scholar 

  • Murata, F., Spicer, S.S., Nagata, T.: Ultrastructural and cytochemical studies on the basophilic leukocytes. Proc. 10th Int. Cong. Anat. 369 (1975)

  • Murata, F., Momose, Y., Yoshida, K., Nagata, T.: Radioautographic study of the mucosubstances in the rabbit bone marrow cells. Acta Anat. Nippon 52, 44–45 (1977)

    Google Scholar 

  • Murata, F., Yoshida, K., Ohno, S., Nagata, T.: Mucosubstances of the granulocytes studied by means of electron microscopic radioautography and X-ray microanalysis. Proc. 9th Int. Cong. Electron Microscopy 2, 454–455 (1978)

    Google Scholar 

  • Murata, K.: Acidic glycosaminoglycans in human platelets and leukocytes: The isolation and enzymatic characterization of chondroitin 4-sulfate. Clin. Chim. Acta 57, 115–124 (1974)

    Google Scholar 

  • Odell, T.T., Tausche, F.G., Jr., Gude, W.D.: Uptake of radioactive sulfate by elements of the blood and bone marrow of rats. Am. J. Physiol. 180, 491–494 (1955)

    Google Scholar 

  • Olsson, I., Gardell, S.: Isolation and characterization of glycosaminoglycans from human leukocytes and platelets. Biochim. Biophys. Acta 141, 348–357 (1967)

    Google Scholar 

  • Olsson, I., Berg, B., Fransson, L.Å., Norden, Å.: The identify of the metachromatic substance of basophilic leucocytes. Scand. J. Haematol. 7, 440–444 (1970)

    Google Scholar 

  • Olsson, I.: Mucopolysaccharides of rabbit marrow cells. Identification and properties. Exp. Cell Res. 67, 416–426 (1971)

    Google Scholar 

  • Olsson, I.: Subcellular sites for synthesis of glycosaminoglycans (mucopolysaccharides) of rabbit bone marrow cells. Exp. Cell Res. 70, 173–184 (1972)

    Google Scholar 

  • Orenstein, N.S., Galli, S.J., Dvorak, A.M., Silbert, J.E., Dvorak, H.F.: Sulfated glycosaminoglycans of guinea pig basophilic leukocytes. J. Immunol. 121, 586–592 (1978)

    Google Scholar 

  • Payne, D.N., Ackerman, G.A.: Ultrastructural autoradiographic study of the uptake and intracellular localization of 35S-sulfate by developing human neutrophils. Blood 50, 841–856 (1977)

    Google Scholar 

  • Padawer, J.: Identification of mast cells in the scanning electron microscope by means of X-ray spectrometry. J. Cell Biol. 61, 641–646 (1974)

    Google Scholar 

  • Reggio, H., Dagorn, J.C.: Ionic interactions between bovine chymotrypsinogen A and chondroitin sulfate A.B.C.: A possible model for molecular aggregation in zymogen granules. J. Cell Biol. 78, 951–957 (1978)

    Google Scholar 

  • Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)

    Google Scholar 

  • Sabatini, D.D., Bensch, K., Barrnett, R.J.: Cytochemistry and electron microscopy: the preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963)

    Google Scholar 

  • Singher, H.O., Marinelli, L.: Distribution of radioactive sulfur in the rat. Science 101, 414–415 (1945)

    Google Scholar 

  • Spicer, S.S., Hardin, J.H., Setser, M.E.: Ultrastructural visualization of sulphated complex carbohydrates in blood and epithelial cells with the high iron diamine procedure. Histochem. J. 10, 435–452 (1978)

    Google Scholar 

  • Sue, T.K., Jaques, L.B.: Sulfated mucopolysaccharides and basophilic leukocytes in rabbits on a high cholesterol/oil diet. Proc. Soc. Exp. Biol. Med. 146, 1006–1013 (1974)

    Google Scholar 

  • Taniguchi, N., Nanba, I., Koizumi, S.: Characterization of glycosaminoglycans in human leukocytes: Enzymatic subunit assay of isomeric chondroitin sulfates. Biochim. Med. 11, 217–226 (1974)

    Google Scholar 

  • Tarver, H., Schmidt, L.A.: Radioactive sulfur studies. J. Biol. Chem. 146, 69–83 (1942)

    Google Scholar 

  • Vodopick, H.A., Athens, J.W., Warner, H.R., Boggs, D.R., Cartwright, G.E., Wintrobe, M.M.: An evaluation of radiosulfate as a granulocyte label in the dog. J. Clin. Med. 68, 47–56 (1966)

    Google Scholar 

  • Weisberger, A.S., Suhrland, L.G.: Comparative incorporation of S35L-cystine and S35 sodium sulfate by normal and leukemic leukocytes. Blood 10, 458–466 (1955)

    Google Scholar 

  • Young, R.W.: Utilization of S35-sulfate in the formation of azurophil granules in the Golgi complex of developing eosinophilic leucocytes. Anat. Rec. 163, 334 (1969)

    Google Scholar 

  • Young, R.W.: The role of the Golgi complex in sulfate metabolism. J. Cell Biol. 57, 175–189 (1973)

    Google Scholar 

  • Zeya, H.I., Spitznagel, J.K.: Characterization of cationic protein-bearing granules of polymorphonuclear leukocytes. Lab. Invest. 24, 229–236 (1971)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murata, F., Yoshida, K., Ohno, S. et al. Mucosubstances of rabbit granulocytes studied by means of electron-microscopic radioautography and X-ray microanalysis. Histochemistry 61, 139–150 (1979). https://doi.org/10.1007/BF00496526

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00496526

Keywords

Navigation