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. 1964 Jun 1;21(3):353–366. doi: 10.1083/jcb.21.3.353

ON THE SITE OF SULFATION IN THE CHONDROCYTE

Gabriel C Godman 1, Nathan Lane 1
PMCID: PMC2106381  PMID: 14189910

Abstract

As observed autoradiographically in the cartilage of embryonic rats, radiosulfate is bound and concentrated only in vesicles of the juxtanuclear Golgi apparatus of secreting chondrocytes within 3 minutes of its presentation. From this area, vacuoles migrate peripherally and lodge in the subcortex; their sulfated contents are thence discharged via stomata to the extracellular matrix. The label, apparently often associated with microvesicles at 10 and 20 minutes, is subsequently localized in the dense contents of the larger vacuoles. Bound radiosulfate is not detectable in other organelles. It is concluded that the vesicular component of the Golgi apparatus is the actual site of sulfation. Intracellular hyaluronidase-sensitive metachromatic granules are found chiefly at the cell periphery or mantle, rarely juxtanuclear in the main Golgi zone.

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Selected References

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  1. ADAMS J. B., RIENITS K. G. The biosynthesis of chondroitin sulphates. Influence of nucleotides and hexosamines on sulphate incorporation. Biochim Biophys Acta. 1961 Aug 19;51:567–578. doi: 10.1016/0006-3002(61)90615-1. [DOI] [PubMed] [Google Scholar]
  2. AMPRINO R. On the incorporation of radiosulfate in the cartilage. Experientia. 1955 Feb 15;11(2):65–67. doi: 10.1007/BF02179030. [DOI] [PubMed] [Google Scholar]
  3. BOSTROM H., MANSSON B. On the enzymatic exchange of the sulfate group of chondroitinsulfuric acid in slices of cartilage. J Biol Chem. 1952 May;196(2):483–488. [PubMed] [Google Scholar]
  4. CAMPO R. D., DZIEWIATKOWSKI D. D. A consideration of the permeability of cartilage to inorganic sulfate. J Biophys Biochem Cytol. 1961 Feb;9:401–408. doi: 10.1083/jcb.9.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CAMPO R. D., DZIEWIATKOWSKI D. D. Intracellular synthesis of protein-polysaccharides by slices of bovine costal cartilage. J Biol Chem. 1962 Sep;237:2729–2735. [PubMed] [Google Scholar]
  6. CARO L. G., VAN TUBERGEN R. P., KOLB J. A. High-resolution autoradiography. I. Methods. J Cell Biol. 1962 Nov;15:173–188. doi: 10.1083/jcb.15.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. CONKLIN J. L. Staining reactions of mucopolysaccharides after formalin-containing fixatives. Stain Technol. 1963 Jan;38:56–59. [PubMed] [Google Scholar]
  8. CURRAN R. C., KENNEDY J. S. The distribution of the sulphated mucopolysaccharides in the mouse. J Pathol Bacteriol. 1955 Oct;70(2):449–457. doi: 10.1002/path.1700700223. [DOI] [PubMed] [Google Scholar]
  9. D'ABRAMO F., LIPMANN F. The formation of adenosine-3'-phosphate-5'-phosphosulfate in extracts of chick embryo cartilage and its conversion into chondroitin sulfate. Biochim Biophys Acta. 1957 Jul;25(1):211–213. doi: 10.1016/0006-3002(57)90452-3. [DOI] [PubMed] [Google Scholar]
  10. DAVIES D. V., YOUNG L. The distribution of radioactive sulfur (35S) in the fibrous tissues, cartilages and bones of the rat following its administration in the form of inorganic sulphate. J Anat. 1954 Apr;88(2):174–183. [PMC free article] [PubMed] [Google Scholar]
  11. DZIEWIATKOWSKI D. D. Intracellular synthesis of chondroitin sulfate. J Cell Biol. 1962 Jun;13:359–364. doi: 10.1083/jcb.13.3.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DZIEWIATKOWSKI D. D. Radioautographic visualization of sulfur-35 disposition in the articular cartilage and bone of suckling rats following injection of labeled sodium sulfate. J Exp Med. 1951 May;93(5):451–458. doi: 10.1084/jem.93.5.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GODMAN G. C., PORTER K. R. Chondrogenesis, studied with the electron microscope. J Biophys Biochem Cytol. 1960 Dec;8:719–760. doi: 10.1083/jcb.8.3.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. GROSSFELD H., MEYER K., GODMAN G., LINKER A. Mucopolysaccharides produced in tissue culture. J Biophys Biochem Cytol. 1957 May 25;3(3):391–396. doi: 10.1083/jcb.3.3.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GROSS J. I., MATHEWS M. B., DORFMAN A. Sodium chondroitin sulfate-protein complexes of cartilage. II. Metabolism. J Biol Chem. 1960 Oct;235:2889–2892. [PubMed] [Google Scholar]
  16. JACKSON D. S., WILLIAMS G. Two organic fixatives for acid mucopolysaccharides. Stain Technol. 1956 Sep;31(5):189–191. doi: 10.3109/10520295609113802. [DOI] [PubMed] [Google Scholar]
  17. KARNOVSKY M. J. Simple methods for "staining with lead" at high pH in electron microscopy. J Biophys Biochem Cytol. 1961 Dec;11:729–732. doi: 10.1083/jcb.11.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. KAWIAK J. PRESENCE OF CHONDROITIN SULPHATE IN CHONDROCYTES. I. HISTOCHEMICAL AND AUTORADIOGRAPHIC OBSERVATIONS. Acta Histochem. 1963 Apr 30;15:153–160. [PubMed] [Google Scholar]
  19. LAYTON L. L., FRANKEL D. R., SCAPA S. Maternal sulfate utilized by mammalian embryos and suckling young. Arch Biochem. 1950 Aug;28(1):142–144. [PubMed] [Google Scholar]
  20. LIPMANN F. Biological sulfate activation and transfer. Science. 1958 Sep 12;128(3324):575–580. doi: 10.1126/science.128.3324.575. [DOI] [PubMed] [Google Scholar]
  21. PARTRIDGE S. M., DAVIS H. F., ADAIR G. S. The chemistry of connective tissues. 6. The constitution of the chondroitin sulphate-protein complex in cartilage. Biochem J. 1961 Apr;79:15–26. doi: 10.1042/bj0790015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. PELC S. R., COOMBES J. D., BUDD G. C. On the adaptation of autoradiographic techniques for use with the electron microscope. Exp Cell Res. 1961 Jun;24:192–195. doi: 10.1016/0014-4827(61)90272-5. [DOI] [PubMed] [Google Scholar]
  23. PELC S. R., GLUCKSMANN A. Sulphate metabolism in the cartilage of the trachea, pinna and xiphoid process of the adult mouse as indicated by autoradiographs. Exp Cell Res. 1955 Apr;8(2):336–344. doi: 10.1016/0014-4827(55)90145-2. [DOI] [PubMed] [Google Scholar]
  24. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. SCHILLER S., MATHEWS M. B., CIFONELLI J. A., DORFMAN A. The metabolism of mucopolysaccharides in animals. III. Further studies on skin utilizing C14-glucose, C14-acetate, and S35-sodium sulfate. J Biol Chem. 1956 Jan;218(1):139–145. [PubMed] [Google Scholar]
  26. SUZUKI S., STROMINGER J. L. Enzymatic sulfation of mucopolysaccharides in hen oviduct. I. Transfer of sulfate from 3'-phosphoadenosine 5'-phosphosulfate to mucopolysaccharides. J Biol Chem. 1960 Feb;235:257–266. [PubMed] [Google Scholar]
  27. SUZUKI S., STROMINGER J. L. Enzymatic sulfation of mucopolysaccharides in hen oviduct. II. Mechanism of the reaction studied with oligosaccharides and monosaccharides as acceptors. J Biol Chem. 1960 Feb;235:267–273. [PubMed] [Google Scholar]
  28. SUZUKI S., STROMINGER J. L. Enzymatic sulfation of mucopolysaccharides in hen oviduct. III. Mechanism of sulfation of chondrotin and chondrotin sulfate A. J Biol Chem. 1960 Feb;235:274–276. [PubMed] [Google Scholar]
  29. WARSHAWSKY H., LEBLOND C. P., DROZ B. Synthesis and migration of proteins in the cells of the exocrine pancreas as revealed by specific activity determination from radioautographs. J Cell Biol. 1963 Jan;16:1–24. doi: 10.1083/jcb.16.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. WHITEHOUSE M. W., BOSTROM H. Studies on the action of some anti-inflammatory agents in inhibiting the biosynthesis of mucopolysaccharide sulphates. Biochem Pharmacol. 1961 Jul;7:135–150. doi: 10.1016/0006-2952(61)90150-2. [DOI] [PubMed] [Google Scholar]

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