Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1973 Apr 1;57(1):175–189. doi: 10.1083/jcb.57.1.175

THE ROLE OF THE GOLGI COMPLEX IN SULFATE METABOLISM

Richard W Young 1
PMCID: PMC2108953  PMID: 4691393

Abstract

This investigation was designed to determine if sulfate metabolism is the function of a particular cell organelle, or whether the site of sulfation varies, depending upon the type of cell and the class of sulfated compound. Rats and mice were injected intravenously with inorganic sulfate labeled with 35S (H2 35SO4), and were then killed by vascular perfusion of fixative 5–30 min later. Several tissues were prepared for electron microscope autoradiography. 14 different types of specialized cells which incorporated the labeled sulfate were analyzed. In every case, the sulfate was initially detected in the smooth membranes and vesicles of the Golgi complex. Available evidence indicates that these cells were engaged in the synthesis of several different sulfated compounds, including mucopolysaccharides, glycoproteins, lipids, and steroids. These results lead to the generalization that the enzymes required for the transfer of inorganic sulfate to a variety of acceptor molecules are located in the Golgi complex.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

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

  1. ABOOD L. G., ABUL-HAJ S. K. Histochemistry and characterization of hyaluronic acid in axons of peripheral nerve. J Neurochem. 1956 Dec;1(2):119–125. doi: 10.1111/j.1471-4159.1956.tb12062.x. [DOI] [PubMed] [Google Scholar]
  2. ACKERMAN G. A. Cytochemical properties of the blood basophilic granulocyte. Ann N Y Acad Sci. 1963 Feb 26;103:376–393. doi: 10.1111/j.1749-6632.1963.tb53710.x. [DOI] [PubMed] [Google Scholar]
  3. BELANGER L. F. Autoradiographic visualization of S35 incorporation and turnover by the mucous glands of the gastrointestinal tract and other soft tissues of rat and hamster. Anat Rec. 1954 Apr;118(4):755–771. doi: 10.1002/ar.1091180405. [DOI] [PubMed] [Google Scholar]
  4. BOSTROM H., ODEBLAD E. Autoradiographic observations on the uptake of S35 in the genital organs of the female rat and rabbit after injection of labeled sodium sulfate. Acta Endocrinol (Copenh) 1952 May;10(1):89–96. doi: 10.1530/acta.0.0100089. [DOI] [PubMed] [Google Scholar]
  5. Bainton D. F., Farquhar M. G. Origin of granules in polymorphonuclear leukocytes. Two types derived from opposite faces of the Golgi complex in developing granulocytes. J Cell Biol. 1966 Feb;28(2):277–301. doi: 10.1083/jcb.28.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bainton D. F., Farquhar M. G. Segregation and packaging of granule enzymes in eosinophilic leukocytes. J Cell Biol. 1970 Apr;45(1):54–73. doi: 10.1083/jcb.45.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Berg N. B., Young R. W. Sulfate metabolism in pancreatic acinar cells. J Cell Biol. 1971 Aug;50(2):469–483. doi: 10.1083/jcb.50.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. CLAUSEN J., ANDERSEN V. ACID MUCOPOLYSACCHARIDES IN HUMAN LEUCOCYTES. Clin Chim Acta. 1963 Jul;8:505–512. doi: 10.1016/0009-8981(63)90096-2. [DOI] [PubMed] [Google Scholar]
  9. CURRAN R. C., KENNEDY J. S. Utilization of sulphate ion by fibroblasts in the quartz focus. Nature. 1955 Mar 5;175(4453):435–436. doi: 10.1038/175435b0. [DOI] [PubMed] [Google Scholar]
  10. Chandrasekaran E. V., Bachhawat B. K. Isolation and characterization of glycosaminoglycans in peripheral nerve and spinal cord of monkey. J Neurochem. 1969 Nov;16(11):1529–1532. doi: 10.1111/j.1471-4159.1969.tb09908.x. [DOI] [PubMed] [Google Scholar]
  11. DAVIDSON E., HOFFMAN P., LINKER A., MEYER K. The acid mucopolysaccharides of connective tissue. Biochim Biophys Acta. 1956 Sep;21(3):506–518. doi: 10.1016/0006-3002(56)90188-3. [DOI] [PubMed] [Google Scholar]
  12. Dunn W. B., Spicer S. S. Histochemical demonstration of sulfated mucosubstances and cationic proteins in human granulocytes and platelets. J Histochem Cytochem. 1969 Oct;17(10):668–674. doi: 10.1177/17.10.668. [DOI] [PubMed] [Google Scholar]
  13. GLUCKSMANN A., HOWARD A., PELC S. R. The uptake of radioactive sulphate by cells, fibres and ground-substance of mature and developing connective tissue in the adult mouse. J Anat. 1956 Oct;90(4):478–485. [PMC free article] [PubMed] [Google Scholar]
  14. GODMAN G. C., LANE N. ON THE SITE OF SULFATION IN THE CHONDROCYTE. J Cell Biol. 1964 Jun;21:353–366. doi: 10.1083/jcb.21.3.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. GOLDBERG I. H. The sulfolipids. J Lipid Res. 1961 Apr;2:103–109. [PubMed] [Google Scholar]
  16. GREULICH R. C. Utilization of sulfate ion by eosinophile myelocytes in the rat. Exp Cell Res. 1956 Aug;11(1):225–228. doi: 10.1016/0014-4827(56)90211-7. [DOI] [PubMed] [Google Scholar]
  17. George E., Singh M., Bachhawat B. K. The nature of sulphation of uronic acid-containing glycosaminoglycans catalysed by brain sulphotransferase. J Neurochem. 1970 Feb;17(2):189–200. doi: 10.1111/j.1471-4159.1970.tb02200.x. [DOI] [PubMed] [Google Scholar]
  18. HADEK R. ELECTRON MICROSCOPE STUDY ON PRIMARY LIQUOR FOLLICULI SECRETION IN THE MOUSE OVARY. J Ultrastruct Res. 1963 Dec;52:445–458. doi: 10.1016/s0022-5320(63)80077-5. [DOI] [PubMed] [Google Scholar]
  19. HOLT M. W., WARREN S. Microscopic distribution of radioisotopes in tissues. Lab Invest. 1953 Jul-Aug;2(4):264–279. [PubMed] [Google Scholar]
  20. HORN R. G., SPICER S. S. SULFATED MUCOPOLYSACCHARIDE AND BASIC PROTEIN IN CERTAIN GRANULES OF RABBIT LEUKOCYTES. Lab Invest. 1964 Jan;13:1–15. [PubMed] [Google Scholar]
  21. 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]
  22. Herschkowitz N., McKhann G. M., Saxena S., Shooter E. M., Herndon R. Synthesis of sulphatide-containing lipoproteins in rat brain. J Neurochem. 1969 Jul;16(7):1049–1057. doi: 10.1111/j.1471-4159.1969.tb05949.x. [DOI] [PubMed] [Google Scholar]
  23. Hirosawa K., Young R. W. Autoradiographic analysis of sulfate metabolism in the cerebellum of the mouse. Brain Res. 1971 Jul 23;30(2):295–309. doi: 10.1016/0006-8993(71)90080-1. [DOI] [PubMed] [Google Scholar]
  24. JENSEN C. E., ZACHARIAE F. Studies on the mechanism of ovulation: isolation and analysis of acid mucopolysaccharides in bovine follicular fluid. Acta Endocrinol (Copenh) 1958 Mar;27(3):356–368. [PubMed] [Google Scholar]
  25. JORPES E., ODEBLAD E., BOSTROM H. An autoradiographic study on the uptake of S35-labelled sodium sulphate in the mast cells. Acta Haematol. 1953 May;9(5):273–276. doi: 10.1159/000204294. [DOI] [PubMed] [Google Scholar]
  26. Kobayasi T., Midtgård K., Asboe-Hansen G. Ultrastructure of human mast-cell granules. J Ultrastruct Res. 1968 Apr;23(1):153–165. doi: 10.1016/s0022-5320(68)80039-5. [DOI] [PubMed] [Google Scholar]
  27. LAGUNOFF D., PHILLIPS M. T., ISERI O. A., BENDITT E. P. ISOLATION AND PRELIMINARY CHARACTERIZATION OF RAT MAST CELL GRANULES. Lab Invest. 1964 Nov;13:1331–1344. [PubMed] [Google Scholar]
  28. LANE N., CARO L., OTERO VILARDEBO L. R., GODMAN G. C. ON THE SITE OF SULFATION IN COLONIC GOBLET CELLS. J Cell Biol. 1964 Jun;21:339–351. doi: 10.1083/jcb.21.3.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lettré H., Paweletz N. Probleme der elektronenmikroskopischen Autoradiographie. Naturwissenschaften. 1966 Jun;53(11):268–271. doi: 10.1007/BF00621640. [DOI] [PubMed] [Google Scholar]
  30. Lewis D. A. Androgen sulphate formation in male and female mice. Biochem J. 1969 Nov;115(3):489–493. doi: 10.1042/bj1150489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. MANCINI R. E., VILAR O., STEIN E., FIORINI H. A histochemical and radioautographic study of the participation of fibroblasts in the production of mucopolysaccharides in connective tissue. J Histochem Cytochem. 1961 May;9:278–291. doi: 10.1177/9.3.278. [DOI] [PubMed] [Google Scholar]
  32. Margolis R. K., Margolis R. U. Sulfated glycopeptides from rat brain glycoproteins. Biochemistry. 1970 Oct 27;9(22):4389–4396. doi: 10.1021/bi00824a020. [DOI] [PubMed] [Google Scholar]
  33. Merker H. J., Diaz-Encinas J. Das elektronenmikroskopische Bild des Ovars juveniler Ratten und Kaninchen nach Stimulierung mit PMS und HCG. I. Theka und Stroma (Interstitielle Drüse) Z Zellforsch Mikrosk Anat. 1969;94(4):605–623. [PubMed] [Google Scholar]
  34. Nemoto T., Yosizawa Z. Sulfated glycopeptides and glycosaminoglycan peptides isolated from intestinal mucosae of rabbit. Biochim Biophys Acta. 1969 Oct 7;192(1):37–48. doi: 10.1016/0304-4165(69)90007-5. [DOI] [PubMed] [Google Scholar]
  35. ODEBLAD E., BOSTROM H. A time-picture relation study with autoradiography on the uptake of labelled sulphate in the graafian follicles of the rabbit. Acta radiol. 1953 Feb;39(2):137–140. doi: 10.3109/00016925309136697. [DOI] [PubMed] [Google Scholar]
  36. Olsson I., Gardell S. Isolation and characterization of glycosaminoglycans from human leukocytes and platelets. Biochim Biophys Acta. 1967 Jul 25;141(2):348–357. doi: 10.1016/0304-4165(67)90109-2. [DOI] [PubMed] [Google Scholar]
  37. Olsson I. Subcellular sites for synthesis of glycosaminoglycans (mucopolysaccharides) of rabbit bone marrow cells. Exp Cell Res. 1972 Jan;70(1):173–184. doi: 10.1016/0014-4827(72)90195-4. [DOI] [PubMed] [Google Scholar]
  38. Olsson I. The intracellular transport of glycosaminoglycans (mucopolysaccharides) in human leukocytes. Exp Cell Res. 1969 Mar;54(3):318–325. doi: 10.1016/0014-4827(69)90209-2. [DOI] [PubMed] [Google Scholar]
  39. Spicer S. S., Greene W. B., Hardin J. H. Ultrastructural localization of acid mucosubstance and antimonate-precipitable cation in human and rabbit platelets and megakaryocytes. J Histochem Cytochem. 1969 Dec;17(12):781–792. doi: 10.1177/17.12.781. [DOI] [PubMed] [Google Scholar]
  40. Weiss L. The structure of bone marrow. Functional interrelationships of vascular and hematopoietic compartments in experimental hemolytic anemia: an electron microscopic study. J Morphol. 1965 Nov;117(3):467–537. doi: 10.1002/jmor.1051170308. [DOI] [PubMed] [Google Scholar]

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

RESOURCES