Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1984 May 1;219(3):689–697. doi: 10.1042/bj2190689

Regulation of arylsulphatase A and sulphogalactolipid turnover by cortisol in myelinogenic cultures of cells dissociated from embryonic mouse brain.

J L Stephens, R A Pieringer
PMCID: PMC1153533  PMID: 6146311

Abstract

Myelinogenic cultures of cells dissociated from embryonic mouse brain were used to study the regulation of myelination-associated molecules by cortisol. Cortisol in physiological concentrations (0.03 microM) caused an increased accumulation of myelination-associated sulphogalactolipids. It also stimulated the myelin- and oligodendroglia-specific cyclic nucleotide phosphohydrolase. The increase in sulphogalactolipid content was caused by a cortisol-concentration-dependent inhibition in arylsulphatase A activity and not by an increase in either cerebroside sulphotransferase activity or an increase in availability of adenosine 3'-phosphate 5'-phosphosulphate. Of several steroid hormones tested only the glucocorticoid types brought about these changes. The relationship between net sulphogalactolipid accumulation and arylsulphatase A inhibition induced by cortisol was confirmed by sulphogalactolipid turnover studies. Depending on whether a single-phase or a two-phase decay calculation is used, the turnover of sulphogalactolipid with cortisol present was decreased at 22 days in culture by either 62% or 65% respectively of that without cortisol. This decrease in turnover can be attributed completely to the decrease of arylsulphatase activity by cortisol to 63% of the value for normal cells grown under the same conditions.

Full text

PDF
689

Selected References

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

  1. BAUM H., DODGSON K. S., SPENCER B. The assay of arylsulphatases A and B in human urine. Clin Chim Acta. 1959 May;4(3):453–455. doi: 10.1016/0009-8981(59)90119-6. [DOI] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Bhat N. R., Rao G. S., Pieringer R. A. Investigations on myelination in vitro. Regulation of sulfolipid synthesis by thyroid hormone in cultures of dissociated brain cells from embryonic mice. J Biol Chem. 1981 Feb 10;256(3):1167–1171. [PubMed] [Google Scholar]
  4. Bhat N. R., Sarlieve L. L., Rao G. S., Pieringer R. A. Investigations on myelination in vitro. Regulation by thyroid hormone in cultures of dissociated brain cells from embryonic mice. J Biol Chem. 1979 Oct 10;254(19):9342–9344. [PubMed] [Google Scholar]
  5. Bhat N. R., Shanker G., Pieringer R. A. Cell proliferation in growing cultures of dissociated embryonic mouse brain: macromolecule and ornithine decarboxylase synthesis and regulation by hormones and drugs. J Neurosci Res. 1983;10(2):221–230. doi: 10.1002/jnr.490100210. [DOI] [PubMed] [Google Scholar]
  6. Bhat N. R., Shanker G., Pieringer R. A. Investigations on myelination in vitro: regulation of 2,3'-cyclic nucleotide 3'-phosphohydrolase by thyroid hormone in cultures of dissociated brain cells from embryonic mice. J Neurochem. 1981 Sep;37(3):695–701. doi: 10.1111/j.1471-4159.1982.tb12543.x. [DOI] [PubMed] [Google Scholar]
  7. Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bottenstein J. E., Skaper S. D., Varon S. S., Sato G. H. Selective survival of neurons from chick embryo sensory ganglionic dissociates utilizing serum-free supplemented medium. Exp Cell Res. 1980 Jan;125(1):183–190. doi: 10.1016/0014-4827(80)90202-5. [DOI] [PubMed] [Google Scholar]
  9. Burkart T., Caimi L., Siegrist H. P., Herschkowitz N. N., Wiesmann U. N. Vesicular transport of sulfatide in the myelinating mouse brain. Functional association with lysosomes? J Biol Chem. 1982 Mar 25;257(6):3151–3156. [PubMed] [Google Scholar]
  10. Burkart T., Hofmann K., Siegrist H. P., Herschkowitz N. N., Wiesmann U. N. Quantitative measurement of in vivo sulfatide metabolism during development of the mouse brain: evidence for a large rapidly degradable sulfatide pool. Dev Biol. 1981 Apr 15;83(1):42–48. doi: 10.1016/s0012-1606(81)80006-1. [DOI] [PubMed] [Google Scholar]
  11. Burkart T., Wiesmann U. N., Siegrist H. P., Herschkowitz N. N. Net sulfatide synthesis, galactosylceramide sulfotransferase and arylsulfatase A activity in the developing cerebrum and cerebellum of normal mice and myelin-deficient jimpy mice. Biochim Biophys Acta. 1981 Mar 18;673(3):351–358. doi: 10.1016/0304-4165(81)90466-9. [DOI] [PubMed] [Google Scholar]
  12. Cotterrell M., Balázs R., Johnson A. L. Effects of corticosteroids on the biochemical maturation of rat brain: postnatal cell formation. J Neurochem. 1972 Sep;19(9):2151–2167. doi: 10.1111/j.1471-4159.1972.tb05124.x. [DOI] [PubMed] [Google Scholar]
  13. Davison A. N., Gregson N. A. Metabolism of cellular membrane sulpholipids in the rat brain. Biochem J. 1966 Mar;98(3):915–922. doi: 10.1042/bj0980915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dawson G., Kernes S. M. Mechanism of action of hydrocortisone potentiation of sulfogalactosylceramide synthesis in mouse oligodendroglioma clonal cell lines. J Biol Chem. 1979 Jan 10;254(1):163–167. [PubMed] [Google Scholar]
  15. FIELD E. J. Observations on the development of microglia together with a note on the influence of cortisone. J Anat. 1955 Apr;89(2):201–208. [PMC free article] [PubMed] [Google Scholar]
  16. Farooqui A. A. Metabolism of sulfolipids in mammalian tissues. Adv Lipid Res. 1981;18:159–202. doi: 10.1016/b978-0-12-024918-3.50010-1. [DOI] [PubMed] [Google Scholar]
  17. Fratantoni J. C., Hall C. W., Neufeld E. F. The defect in Hurler's and Hunter's syndromes: faulty degradation of mucopolysaccharide. Proc Natl Acad Sci U S A. 1968 Jun;60(2):699–706. doi: 10.1073/pnas.60.2.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Freysz L., Farooqui A. A., Adamczewska-Goncerzewicz Z., Mandel P. Lysosomal hydrolases in neuronal, astroglial, and olidodendroglial enriched fractions of rabbit and beef brain. J Lipid Res. 1979 May;20(4):503–508. [PubMed] [Google Scholar]
  19. HOWARD E. EFFECTS OF CORTICOSTERONE AND FOOD RESTRICTION ON GROWTH AND ON DNA, RNA AND CHOLESTEROL CONTENTS OF THE BRAIN AND LIVER IN INFANT MICE. J Neurochem. 1965 Mar;12:181–191. doi: 10.1111/j.1471-4159.1965.tb06754.x. [DOI] [PubMed] [Google Scholar]
  20. Herschkowitz N., McKhann G. M., Saxena S., Shooter E. M. Characterization of sulphatide-containing lipoproteins in rat brain. J Neurochem. 1968 Oct;15(10):1181–1188. doi: 10.1111/j.1471-4159.1968.tb06835.x. [DOI] [PubMed] [Google Scholar]
  21. Honegger P., Lenoir D., Favrod P. Growth and differentiation of aggregating fetal brain cells in a serum-free defined medium. Nature. 1979 Nov 15;282(5736):305–308. doi: 10.1038/282305a0. [DOI] [PubMed] [Google Scholar]
  22. Howard E., Benjamins J. A. DNA, ganglioside and sulfatide in brains of rats given corticosterone in infancy, with an estimate of cell loss during development. Brain Res. 1975 Jul 4;92(1):73–87. doi: 10.1016/0006-8993(75)90528-4. [DOI] [PubMed] [Google Scholar]
  23. Jungalwala F. B. Synthesis and turnover of cerebroside sulfate of myelin in adult and developing rat brain. J Lipid Res. 1974 Mar;15(2):114–123. [PubMed] [Google Scholar]
  24. Juurlink B. H., Schousboe A., Jørgensen O. S., Hertz L. Induction by hydrocortisone of glutamine synthetase in mouse primary astrocyte cultures. J Neurochem. 1981 Jan;36(1):136–142. doi: 10.1111/j.1471-4159.1981.tb02388.x. [DOI] [PubMed] [Google Scholar]
  25. KIRK D. L., MOSCONA A. A. SYNTHESIS OF EXPERIMENTALLY INDUCED GLUTAMINE SYNTHETASE (GLUTAMOTRANSFERASE ACTIVITY) IN EMBRYONIC CHICK RETINA IN VITRO. Dev Biol. 1963 Dec;8:341–357. doi: 10.1016/0012-1606(63)90034-4. [DOI] [PubMed] [Google Scholar]
  26. Kim S. U., Pleasure D. Tissue culture analysis of neurogenesis. II. Lipid-free medium retards myelination in mouse spinal cord cultures. Brain Res. 1978 Nov 17;157(1):206–211. doi: 10.1016/0006-8993(78)91016-8. [DOI] [PubMed] [Google Scholar]
  27. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  28. MASTER R. W. POSSIBLE SYNTHESIS OF POLYRIBONUCLEOTIDES OF KNOWN BASE-TRIPLET SEQUENCES. Nature. 1965 Apr 3;206:93–93. doi: 10.1038/206093b0. [DOI] [PubMed] [Google Scholar]
  29. Miller S. L., Benjamins J. A., Morell P. Metabolism of glycerophospholipids of myelin and microsomes in rat brain. Reutilization of precursors. J Biol Chem. 1977 Jun 25;252(12):4025–4037. [PubMed] [Google Scholar]
  30. Miller S. L., Morell P. Turnover of phosphatidylcholine in microsomes and myelin in brains of young and adult rats. J Neurochem. 1978 Oct;31(4):771–777. doi: 10.1111/j.1471-4159.1978.tb00109.x. [DOI] [PubMed] [Google Scholar]
  31. Noguchi T., Sugisaki T., Watanabe M., Kohsaka S., Tsukada Y. Effects of bovine growth hormone on the retarded cerebral development induced by neonatal hydrocortisone intoxication. J Neurochem. 1982 Jan;38(1):246–256. doi: 10.1111/j.1471-4159.1982.tb10877.x. [DOI] [PubMed] [Google Scholar]
  32. Piddington R., Moscona A. A. Precocious induction of retinal glutamine synthetase by hydrocortisone in the embryo and in culture. Age-dependent differences in tissue response. Biochim Biophys Acta. 1967 Jul 25;141(2):429–432. doi: 10.1016/0304-4165(67)90120-1. [DOI] [PubMed] [Google Scholar]
  33. Prohaska J. R., Clark D. A., Wells W. W. Improved rapidity and precision in the determination of brain 2',3'-cyclic nucleotide 3'-phosphohydrolase. Anal Biochem. 1973 Nov;56(1):275–282. doi: 10.1016/0003-2697(73)90189-9. [DOI] [PubMed] [Google Scholar]
  34. Raghavan S. S., Rhoads D. B., Kanfer J. N. Acid hydrolases in neuronal and glial enriched fractions of rat brain. Biochim Biophys Acta. 1972 Jun 16;268(3):755–760. doi: 10.1016/0005-2744(72)90285-9. [DOI] [PubMed] [Google Scholar]
  35. Sarlieve L. L., Rao G. S., Campbell G. L., Pieringer R. A. Investigations on myelination in vitro: biochemical and morphological changes in cultures of dissociated brain cells from embryonic mice. Brain Res. 1980 May 5;189(1):79–90. doi: 10.1016/0006-8993(80)90008-6. [DOI] [PubMed] [Google Scholar]
  36. Shanker G., Bhat N. R., Pieringer R. A. Investigations on myelination in vitro: thyroid hormone receptors in cultures of cells dissociated from embryonic mouse brain. Biosci Rep. 1981 Apr;1(4):289–297. doi: 10.1007/BF01114868. [DOI] [PubMed] [Google Scholar]
  37. Shanker G., Pieringer R. A. Effect of thyroid hormone on the synthesis of sialosyl galactosylceramide (GM4) in myelinogenic cultures of cells dissociated from embryonic mouse brain. Brain Res. 1983 Jan;282(2):169–174. doi: 10.1016/0165-3806(83)90094-9. [DOI] [PubMed] [Google Scholar]
  38. Siegrist H. P., Burkart T., Steck A. J., Wiesmann U., Herschkowitz N. N. Influence of lipids on the activity of cerebroside-sulphotransferase in mouse brain: a comparative study of Jimpty and normal mouse brains. J Neurochem. 1976 Aug;27(2):599–604. doi: 10.1111/j.1471-4159.1976.tb12288.x. [DOI] [PubMed] [Google Scholar]
  39. Siegrist H. P., Burkart T., Wiesmann U. N., Herschkowitz N. N., Spycher M. A. Ceramide-galactosyltransferase and cerebroside-sulphotranserase localisation in Golgi membranes isolated by a continuous sucrose gradient of mouse brain microsomes. J Neurochem. 1979 Aug;33(2):497–504. doi: 10.1111/j.1471-4159.1979.tb05180.x. [DOI] [PubMed] [Google Scholar]
  40. Smith M. E. The turnover of myelin in the adult rat. Biochim Biophys Acta. 1968 Oct 22;164(2):285–293. doi: 10.1016/0005-2760(68)90154-9. [DOI] [PubMed] [Google Scholar]
  41. Volpe J. J., Marasa J. C. Regulation of palmitic acid synthesis in cultured glial cells: effects of glucocorticoid on fatty acid synthetase, acetyl-CoA carboxylase, fatty acid and sterol synthesis. J Neurochem. 1976 Oct;27(4):841–845. doi: 10.1111/j.1471-4159.1976.tb05144.x. [DOI] [PubMed] [Google Scholar]
  42. Volpe J. J., Marasa J. C. Regulation of palmitic acid synthesis in cultured glial cells: effects of lipid on fatty acid synthetase, acetyl-CoA carboxylase, fatty acid and sterol synthesis. J Neurochem. 1975 Sep;25(3):333–340. doi: 10.1111/j.1471-4159.1975.tb06976.x. [DOI] [PubMed] [Google Scholar]
  43. Walravens P., Chase H. P. Influence of thyroid on formation of myelin lipids. J Neurochem. 1969 Oct;16(10):1477–1484. doi: 10.1111/j.1471-4159.1969.tb09900.x. [DOI] [PubMed] [Google Scholar]
  44. Wiesmann U. N., Hofmann K., Burkhart T., Herschkowitz N. Dissociated cultures of newborn mouse brain. I. Metabolism of sulfated lipids and mucopolysaccharides. Neurobiology. 1975 Dec;5(6):305–315. [PubMed] [Google Scholar]
  45. Yavin E., Yavin Z. Attachment and culture of dissociated cells from rat embryo cerebral hemispheres on polylysine-coated surface. J Cell Biol. 1974 Aug;62(2):540–546. doi: 10.1083/jcb.62.2.540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zalc B., Monge M., Dupouey P., Hauw J. J., Baumann N. A. Immunohistochemical localization of galactosyl and sulfogalactosyl ceramide in the brain of the 30-day-old mouse. Brain Res. 1981 May 4;211(2):341–354. doi: 10.1016/0006-8993(81)90706-x. [DOI] [PubMed] [Google Scholar]
  47. Zuppinger K., Wiesmann U., Siegrist H. P., Schäfer T., Sandru L., Schwarz H. P., Herschkowitz N. Effect of glucose deprivation on sulfatide synthesis and oligodendrocytes in cultured brain cells of newborn mice. Pediatr Res. 1981 Apr;15(4 Pt 1):319–325. doi: 10.1203/00006450-198104000-00006. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES