Skip to main content

Biochemical aspects of globoid and metachromatic leukodystrophies

Abstract

Galactosylceramides and sulfogalactosylceramides are characteristic lipids of the myelin sheath. Two genetically determined leukodystrophies are caused by an inability to enzymically hydrolyze these glycolipids. Thus, a deficiency of galactocerebroside β-galactosidase results in globoid cell leukodystrophy, whereas a reduced activity of arylsulfatase A is responsible for metachromatic leukodystrophy. Besides these disorders, deficiencies of arylsulfatases A, B, C, and other sulfatases have been shown in a distinct condition called “multiple sulfatase deficiency”. All of these disorders are fatal and are characterized by marked demyelination and severe mental retardation. The cause of this demyelination is not known. However, cytotoxic galactosylsphingosine and sulfogalactosylsphingosine have been suggested as the agents responsible for this demyelination. Recent immunological studies have also shown that patients with globoid and metachromatic leukodystrophies contain a mutant galactocerebroside β-galactosidase and arylsulfatase A, respectively. The mutant enzymes have different kinetic properties compared to the enzymes from normal subjects. However, the can cross-react with antibodies to these enzymes. Since partially purified preparations of galactocerebroside β-galactosidase and homogeneous arylsulfatase A are now available, the possibility of enzyme replacement therapy in globoid and metachromatic leukodystrophies is discussed.

This is a preview of subscription content, access via your institution.

References

  • Alpers D. J. (1969) Separation and isolation of rat and human intestinal β-galactosidase.J. Biol. Chem. 244, 1237–1242.

    Google Scholar 

  • Aronson N. N. (1972) Degradation of Glycoproteins by Lysosomal Enzymes, inThe Glycoproteins Part B (Gottschalk A., ed.) pp. 1211–1232. Elsevier Publishing Co., Amsterdam.

    Google Scholar 

  • Austin J. H. (1959) Metachromatic sulfatides in cerebral white matter and kidney.Proc. Soc. Exp. Biol. 100, 361–364.

    CAS  PubMed  Google Scholar 

  • Austin J. H., Balasubramanian A. S., Pattabiraman T. N., Saraswathi S., Basu D. K., and Bachhawat B. K. (1963) A controlled study on enzymic activities in three human disorders of glycolipid metabolism.J. Neurochem. 10, 805–816.

    PubMed  CAS  Article  Google Scholar 

  • Austin J., McAfee D., Shearer L., and Ore P. (1965) Metachromatic forms of diffuse cerebral sclerosis.Arch. Neurol. 12, 447–455.

    PubMed  CAS  Google Scholar 

  • Austin J. H. (1967) Some recent findings in leukodystrophies and in gargoylism. inInborn Disorders of Sphingolipid Metabolism (Aronson S. N. and Volk B. W., eds.) pp. 359–387. Pergamon Press, New York.

    Google Scholar 

  • Austin J., Suzuki K., Armstrong D., Brady R., Bachhawat B. K., and Stumpf D. (1970) Studies on globoid (Krabbe) leukodystrophy.Arch. Neurol. 23, 502–512.

    PubMed  CAS  Google Scholar 

  • Austin J. H. (1973) Multiple sulfatase deficiency.Arch. Neurol. 28, 258–264.

    PubMed  CAS  Google Scholar 

  • Avila J. A. and Convit J. (1976) Physiocochemical characteristics of the glycosaminoglycans-lysosomal enzyme interaction in vitro.Biochem. J. 160, 129–135.

    PubMed  CAS  Google Scholar 

  • Bach G., Eisenberg F., Cantz M., and Neufeld E. F. (1973) The defect in the Hunter syndrome: deficiency of sulfoiduronate sulratase.Proc. Natl. Acad. Sci. USA 70, 2134–2138.

    PubMed  CAS  Article  Google Scholar 

  • Bachhawat B. K., Austin J., and Armstrong D. A. (1967) A cerebroside sulfotransferase deficiency in a human disorder of myelin.Biochem. J. 104, 15C-17C.

    CAS  Google Scholar 

  • Balasubramanian K. A. and Bachhawat B. K. (1975) Purification, properties and glycoprotein nature of arylsulfatase A from sheep brain.Biochim. Biophys. Acta 403, 113–121.

    PubMed  CAS  Google Scholar 

  • Barranger J. A., Rapoport S. I., Fredericks W. R., Pentchev P. G., MacDermat K. D., Steusing J. K., and Brady R. O. (1979) Modification of the blood-brain barrier: Increased concentration and fate of enzyme entering the brain.Proc. Natl. Acad. Sci. USA 76, 481–485.

    PubMed  CAS  Article  Google Scholar 

  • Basner R., Von-Figura K., Glossl J., Klein U., Kresse H., and Mlekusch W. L. (1979) Multiple deficiency of mucopolysaccharide sulfatases in mucosulfatidosis.Pediatr. Res. 13, 1316–1318.

    PubMed  CAS  Article  Google Scholar 

  • Benson P. F. (1982) Treatment of the mucopolysaccharidoses by fibroblast or bone marrow transplantation.Prog. Clin. Biol. Res. 103, 597–599.

    PubMed  Google Scholar 

  • Ben-Yoseph Y., Hungerford M., and Nadler H. L. (1978) The nature of mutation in Krabbe disease.Am. J. Hum. Genet. 30, 644–652.

    PubMed  CAS  Google Scholar 

  • Ben-Yoseph Y., Hungerford M., and Nadler H. L. (1979) Galactosylceramide β-galactosidase in Krabbe Disease: Partial purification and characterization of the mutant enzyme.Arch. Biochem. Biophys. 196, 93–101.

    PubMed  CAS  Article  Google Scholar 

  • Ben-Yoseph Y., Hungerford M., and Nadler H. L. (1980) The interrelations between high and low molecular-weight forms of normal and mutant (Krabbe Disease) galactocerebrosidase.Biochem. J. 189, 9–15.

    PubMed  CAS  Google Scholar 

  • Besley G. T. N. and Bain A. D. (1978) Use of a chromogenic substrate for the diagnosis of Krabbe’s disease with special reference to its application in prenatal diagnosis.Clin. Chim. Acta. 88, 229–236.

    PubMed  CAS  Article  Google Scholar 

  • Besley G. T. N. and Gatt S. (1981) Spectrophotometric and fluorimetric assays of galactocerebrosidase activity, their use in the diagnosis of Krabbe’s disease.Clin. Chim. Acta 110, 19–26.

    PubMed  CAS  Article  Google Scholar 

  • Bishayee S., Farooqui A. A., and Bachhawat B. K. (1973) Purification of brain lysosomal arylsulfatases by concanavalin A Sepharose column chromatography.Ind. J. Biochem. Biophys. 10, 1–2.

    CAS  Google Scholar 

  • Bowen D. M. and Radin N. S. (1968) Purification of cerebroside galactosidase from rat brain.Biochim. Biophys. Acta 152, 587–598.

    PubMed  CAS  Google Scholar 

  • Brady R. O. and Barranger J. A. (1982) The therapeutic strategies for lipid storage diseases.Trends Neurosci. 4, 265–267.

    Article  Google Scholar 

  • Brady R. O. (1983) Lysosomal storage diseases.Pharmac. Ther. 19, 327–336.

    CAS  Article  Google Scholar 

  • Breslow J. L. and Sloan H. R. (1972) Purification of arylsulfatase A from human urine.Biochem. Biophys. Res. Commun. 46, 919–925.

    PubMed  CAS  Article  Google Scholar 

  • Bruns G. A. D., Leary A. C., Regina V. M., and Geraid P. S. (1978) Expression of human arylsulfatase A in man-hamster somatic cell hybrid.Cytogenet. Cell. Genet. 22, 182–185.

    PubMed  CAS  Google Scholar 

  • Butterworth J., Broadhead D. M., and Keay A. J. (1978) Low arylsulfatase A activity in a family without metachromatic leukodystrophy.Clin. Genet. 14, 213–218.

    PubMed  CAS  Article  Google Scholar 

  • Chang P. L. and Davidson R. G. (1980) Complementation of arylsulfatase A in somatic hybrids of metachromatic leukodystrophy and multiple sulfatase deficiency disorder fibroblasts.Proc. Natl. Acad. Sci. USA 77, 6166–6170.

    PubMed  CAS  Article  Google Scholar 

  • Chang T. M. S. (1964) Semipermeable microcapsules.Science 146, 524–526.

    PubMed  CAS  Article  Google Scholar 

  • Chang T. M. S. (1973) Immobilization of enzymes, adsorbents or both within semipermeable microcapsules for clinical and experimental treatment of metabolite related disorders, inEnzyme Replacement for Genetic Diseases. (Desnick R. J., Bernlohr K., and Krivit W., eds.), pp. 66–75. Williams and Wilkins, Baltimore.

    Google Scholar 

  • Chwe A. Y. and Leslie S. E. (1983) Enhancement by sulfatide of Na+-independent [3H]GABA binding in mouse brain.Biochem. Biophys. Res. Commun. 112, 827–832.

    Article  Google Scholar 

  • Cho T. M., Cho S. C., and Loh H. H. (1976)3H-cerebroside sulfate redistribution induced by cation, opiate or phosphatidyl serine.Life Sci. 19, 117–124.

    PubMed  CAS  Article  Google Scholar 

  • Colley C. M. and Ryman B. E. (1976) The liposome: from membrane model to the therapeutic agent.Trends Biochem. Sci. 1, 203–205.

    CAS  Google Scholar 

  • Collier J. and Greenfield J. G. (1924) The encephalitis periaxialis of Schilder: A clinical and pathological study with an account of two cases, one of which was diagnosed during life.Brain 47, 489–519.

    Article  Google Scholar 

  • Conzelmann E. and Sandhoff K. (1978) A B variant of infantile GM2 gangliosidosis: Deficiency of a factor necessary for stimulation of hexosaminidase A-catalyzed degradation of ganglioside GM2 and glycolipid GA2.Proc. Natl. Acad. Sci. USA 75, 3979–3983.

    PubMed  CAS  Article  Google Scholar 

  • Conzelmann E., Burg J., Stephan G., and Sandhoff K. (1982) Complexing of glycolipids and their transfer between membranes by the activator protein for degradation of lysosomal ganglioside GM-2.Eur. J. Biochem. 123, 455–464.

    PubMed  CAS  Article  Google Scholar 

  • Crawfurd M. D. A. (1982) Review: Genetics of steroid sulfatase deficiency and X-linked ichthyosis.J. Inher. Metabo. Dis. 5, 153–163.

    CAS  Article  Google Scholar 

  • Cuzner M. L., Davison A. N., and Gregson N. A. (1965) The chemical composition of vertebrate myelin and microsomes.J. Neurochem. 12, 469–481.

    PubMed  CAS  Article  Google Scholar 

  • Dean M. F., Steven, R. L., Muir H., Benson P. F., Button L. R., Anderson R. L., Boylston A., Mowbray J. (1979) Enzyme replacement therapy by fibroblast transplantation: long term biochemical study in three cases of Hunter’s disease.J. Clin. Invest. 63, 138–145.

    PubMed  CAS  Google Scholar 

  • Dean M. F., Muir H., Benson P. F., and Button L. R. (1982) Effectiveness of HLA-compatible fibroblasts for enzyme replacement therapy in mucopolysaccharidoses.Pediatr. Res. 16, 260–261.

    PubMed  CAS  Article  Google Scholar 

  • DeLuca C., Brown J. A., and Shows T. B. (1979) Lysosomal arylsulfatase deficiencies in human: chromosome assignments for arylsulfatases A and B.Proc. Natl. Acad. Sci. USA 76, 1957–1961.

    PubMed  CAS  Article  Google Scholar 

  • Desnick R. J., Thorpe S. R., and Fiddler M. B. (1976) Toward enzyme therapy for lysosomal storage diseases.Physiol. Rev. 56, 57–99.

    PubMed  CAS  Google Scholar 

  • Dickerman, L. H., Kurczynski, T. W., and MacBride, R. G. (1981) The effects of psychosine upon growth of human skin fibroblasts from patients with globoid cell leukodystrophy.J. Neurol. Sci. 50, 181–190.

    PubMed  CAS  Article  Google Scholar 

  • Draper R. K., Fiskum G. M., and Edmond J. (1976) Purification, molecular weight, amino acid and subunit composition of arylsulfatase A from human liver.Arch. Biochem. Biophys. 177, 525–538.

    PubMed  CAS  Article  Google Scholar 

  • Dubois G., Harzer K., and Baumann N. (1977) Very low arylsulfatase and cerebroside sulfatase activities in leukocytes of healthy members of MLD family.Am. J. Genet. 29, 191–194.

    CAS  Google Scholar 

  • Duchen L. W., Eicher E. M., Jacobs J. M., Scardvilli F., and Teixeira F. (1980) Hereditary leukodystrophy in the mouse: The new mutant twitcher.Brain 103, 695–710.

    PubMed  CAS  Article  Google Scholar 

  • Dulaney J. T. and Moser H. W. (1978) Metachromatic Leukodystrophy, inMetabolic Basis of Inherited Diseases (Stanbury J. B., Wyngaarden J. B., and Fredrickson D. S., eds. pp. 770–809. McGraw-Hill, New York.

    Google Scholar 

  • Dunn H. G., Dolman C. L., Farrell D. F., Tischler B., Hasinoff C., and Woolf L. I. (1976) Krabbe’s leukodystrophy without globoid cells.Neurology 26, 1035–1041.

    PubMed  CAS  Google Scholar 

  • Ebadi M. and Chweh A. (1980) Inhibition by arylsulfatase A of Na-independent (3H)-GABA and (3H)-muscimol binding to bovine cerebellar synaptic membranes.Neuropharmacology 19, 1105–1111.

    PubMed  CAS  Article  Google Scholar 

  • Eto Y., Weismann U., and Herschkowitz N. N. (1974a) Sulfogalactosylsphingosine sulfatase. Characteristics of the enzyme and its deficiency in metachromatic leukodystrophy in human cultured skin fibroblasts.J. Biol. Chem. 249, 4955–4960.

    PubMed  CAS  Google Scholar 

  • Eto Y., Rampini S., Weismann U., and Herschkowitz N. N. (1974b) Enzymic studies of sulfatases in tissues of the normal human and in metachromatic leukodystrophy with multiple sulfatase deficiencies.J. Neurochem. 23, 1161–1170.

    PubMed  CAS  Article  Google Scholar 

  • Eto Y., Weismann U. N., Carson J. H., and Herschkowitz N. N. (1974c) Multiple sulfatase deficiencies in cultured skin fibroblasts.Arch. Neurol. 30, 153–156.

    PubMed  CAS  Google Scholar 

  • Eto Y., Tokora T., Handa T., Herschkowitz N. N., and Rennert O. M. (1982) Acid mucopolysaccharide abnormality in multiple sulfatase deficiency: Chemical composition of AMPS in urine and liver.Pediatr. Res. 16, 395–399.

    PubMed  CAS  Article  Google Scholar 

  • Eto Y., Tahara T., Tokoro T., and Malkawa K. (1983) Various sulfatase activities in leukocytes and cultured skin fibroblasts from heterozygotes for the multiple sulfatase deficiency.Pediatr. Res. 17, 97–100.

    PubMed  CAS  Article  Google Scholar 

  • Fankhauser R., Lunginbuhl H., and Hartley W. J. (1963) Leukodystrophie vom Typus Krabbe beim Hund.Schweiz. Arch. Tierheilkd. 105, 198–207.

    Google Scholar 

  • Farooqui A. A. (1976) Purification and properties of human placenta arylsulfatase A.Arch. Int. Physiol. Biochim. 84, 479–492.

    PubMed  CAS  Article  Google Scholar 

  • Farooqui A. A. (1980a) 3-Phosphoadenosine-5′-phosphosulfate metabolism in mammalian tissue.Int. J. Biochem. 12, 529–536.

    PubMed  CAS  Article  Google Scholar 

  • Farooqui A. A. (1980b) Sulfatases, sulfate esters and their metabolic disorders.Clin. Chim. Acta. 100, 285–299.

    PubMed  CAS  Article  Google Scholar 

  • Farooqui A. A. (1980c) Purification of enzymes by heparin-Sepharose chromatography.J. Chromatog. 184, 335–345.

    CAS  Article  Google Scholar 

  • Farooqui A. A. (1981) Metabolism of sulfolipid in mammalian tissues.Adv. Lipid Res. 18, 159–202.

    PubMed  CAS  Google Scholar 

  • Farooqui A. A. and Bachhawat B. K. (1972) Purification and properties of arylsulfatase A from chicken brain.Biochem. J. 126, 1025–1033.

    PubMed  CAS  Google Scholar 

  • Farooqui A. A. and Bachhawat B. K. (1973) Enzymatic desulfation of cerebroside 3-sulfate by chicken brain arylsulfatase A.J. Neurochem. 20, 889–891.

    PubMed  CAS  Article  Google Scholar 

  • Farooqui A. A. and Mandel P. (1977a) Recent developments in the biochemistry of globoid and metachromatic leukodystrophies.Biomedicine 26, 232–236.

    PubMed  CAS  Google Scholar 

  • Farooqui A. A. and Mandel P. (1977b) On properties and role of arylsulfatases A, B and C in mammals.Int. J. Biochem. 8, 685–691.

    CAS  Article  Google Scholar 

  • Farooqui A. A. and Srivastava P. N. (1979) Isolation, characterization and the role of rabbit testicular arylsulfatase A in fertilization.Biochem. J. 181, 331–337.

    PubMed  CAS  Google Scholar 

  • Farooqui A. A., Rebel G., and Mandel P. (1977) Sulfatide metabolism in brain.Life Sci. 20, 569–583.

    PubMed  CAS  Article  Google Scholar 

  • Farooqui A. A. and Horrocks L. A. (1984) Heparin-Sepharose affinity chromatography.Adv. Chromatog. 23, 127–148.

    CAS  Google Scholar 

  • Farrell D. F., MacMartin M. P., and Clark A. F. (1979) Multiple molecular forms of arylsulfatase A in different forms of metachromatic leukodystrophy (MLD).Neurology 29, 16–20.

    PubMed  CAS  Google Scholar 

  • Fischer G. and Jatzkewitz H. (1975) The activator of cerebroside sulphatase. Purification from human liver and identification as a protein.Hoppe-Seyler’s Z. Physiol. Chem. 356, 605–613.

    PubMed  CAS  Google Scholar 

  • Fischer G. and Jatzkewitz H. (1975) The activator of cerebroside sulfatase: A model of the activation.Biochim. Biophys. Acta 528, 69–76.

    Google Scholar 

  • Fletcher T. F., Suzuki K., and Martin F. (1977) Galatocerebrosidase activities in canine globoid leukodystrophy.Neurology 27, 758–767.

    PubMed  CAS  Google Scholar 

  • Fluharty A. L., Stevens R. L., Miller R. T., and Kihara H. (1974) Sulfoglycerogalactolipid from rat testes: A substrate for pure human arylsulfatase A.Biochem. Biophys. Res. Commun. 61, 348–354.

    PubMed  CAS  Article  Google Scholar 

  • Fluharty A. L., Stevens R. L., Miller R. T., Shapiro S. S., and Kihara H. (1976) Ascorbic acid 2-sulfate sulfohydrolase activity of human arylsulphatase A.Biochim. Biophys. Acta 429, 508–516.

    PubMed  CAS  Google Scholar 

  • Fluharty A. L., Stevens R. L., Goldstein E. B., and Kihara H. (1979a) The activity of arylsulfatases A and B on tyrosineO-sulfates.Biochim. Biophys. Acta 566, 321–326.

    PubMed  CAS  Google Scholar 

  • Fluharty A. L., Stevens R. L., Delaflor S. D., Shapiro L. J., and Kihara H. (1979b) Arylsulfatase A modulation with pH in multiple sulfatase deficiency disorder fibroblasts.Am. J. Hum. Genet. 31, 574–580.

    PubMed  CAS  Google Scholar 

  • Fluharty A. L., Stevens R. L., Miller R. T., and Kihara H. (1980) Bile salt activation of cerebroside sulfate sulfohydrolase.Biochem. J. 189, 45–49.

    PubMed  CAS  Google Scholar 

  • Fluharty A. L., Meek W. E., and Kihara H. (1983) Pseudoarylsulfatase deficiency: Evidence for a structurally altered enzyme.Biochem. Biophys. Res. Commun. 112, 191–197.

    PubMed  CAS  Article  Google Scholar 

  • Flynn T. J., Deshmukh D. S., Subba Rao G., and Pieringer R. A. (1975) Sulfogalactosyl diacylglycerol: Occurrence and biosynthesis of a novel lipid in rat brain.Biochem. Biophys. Res. Commun. 65, 122–128.

    PubMed  CAS  Article  Google Scholar 

  • France J. T. and Liggins G. C. (1969) Placental sulfatase deficiency.J. Clin. Endocrinol. 29, 138–141.

    CAS  Google Scholar 

  • France J. T., Seddon R. J., and Ligging G. E. (1973) A study of a pregnancy with low oestrogen production due to placental sulfatase deficiency.J. Clin Endocrinol. 36, 1–9.

    CAS  Google Scholar 

  • Gal A. E., Brady R. O., Pentchev P. G., Furbish F. S., Suzuki K., Tanaka H., and Schneider E. L. (1977) A practical chromogenic procedure for the diagnosis of Krabbe’s disease.Clin. Chim. Acta 77, 53–59.

    PubMed  CAS  Article  Google Scholar 

  • Gartner S. Conzelmann E., and Sandhoff K. (1983) Activator protein for the degradation of globotriaosylceramide by human β-galactosidase.J. Biol. Chem. 258, 12378–12385.

    PubMed  CAS  Google Scholar 

  • Gatt S. (1967) Enzymatic hydrolysis of sphingolipids V. Hydrolysis of monosialoganglioside and hexosylceramides by rat brain β-galactosidase.Biochim. Biophys. Acta 137, 192–194.

    PubMed  CAS  Google Scholar 

  • Greene H. L., Hug G., and Schubert W. K. (1969) Metachromatic leukodystrophy: Treatment with arylsulfatase A.Arch. Neurol. (Chic). 20, 147–153.

    CAS  Google Scholar 

  • Gregoriadis G. (1980) Liposome Drug Carrier Concept: Its Development and Future, inLipsosomes in Biological Systems (Gregoriadis G. and Allison C. A., eds), pp. 25–86. Wiley, New York.

    Google Scholar 

  • Hahn A. F., Gordon B. A., Gilbert J. J., and Hinton G. G. (1981) The AB-variant of metachromatic leukodystrophy (Postulated activator protein deficiency).Acta Neuropathol. 55, 281–287.

    PubMed  CAS  Article  Google Scholar 

  • Hansson C. G., Karlsson K. A., and Samuelsson B. E. (1978) The identification of sulfatides in human erythrocyte membrane and their relation to Na+-K+ dependent ATPase.J. Biochem. (Tokyo) 83, 813–819.

    CAS  Google Scholar 

  • Harben A. M., Krawiecki N., Marcus R., and Hommes F. A. (1982) AK m mutant of arylsulfatase A.Clin. Chim. Acta 125, 351–354.

    PubMed  CAS  Article  Google Scholar 

  • Hechtman P., Gordon B. A., and Kim N. G. Y. (1982) Deficiency of the hexosaminidase A activator protein in a case of GM2-gangliosidosis: Variant AB.Pediatr. Res. 16, 217–222.

    PubMed  CAS  Google Scholar 

  • Helwig J. J., Farooqui A. A., Bollock C., and Mandel P. (1977) Purification and some properties of arylsulfatases A and B from rabbit kidney cortex.Biochem. J. 165, 127–134.

    PubMed  CAS  Google Scholar 

  • Ho M. W. and O’Brien J. S. (1971) Gaucher disease: Deficiency of “acid” β-glucosidase and reconstitution of enzyme activityin vitro.Proc. Natl. Acad. Sci. USA 68, 2810–2813.

    PubMed  CAS  Article  Google Scholar 

  • Hobbs J. R., Hugh-Jones K., Barett A. J., Byrom N., Chambers D., Henry K., James D. C. O., Lucas C. F., Rogers T. R., Benson P. F., Tansley L. R., Mossman J., Young E. P., and Patrick A. D. (1981) Reversal of clinical features of Hurler’s disease and biochemical improvement after treatment by bone-marrow transplantation.Lancet II, 709–712.

    Article  Google Scholar 

  • Hoogeveen A. T., Verheijen F. W., and Galjaard H. (1983) The relation between human lysosomal β-galactosidase and its protective protein.J. Biol. Chem. 258, 12145–12146.

    Google Scholar 

  • Hors-Cayla M. C., Heuertzs S., Van Cong N., Weil D., and Frezal J. (1979) Confirmation of the assignment of the gene for arylsulfatase A to chromosome 22 using somatic cell hybrids.Hum. Genet. 49, 33–40.

    PubMed  CAS  Google Scholar 

  • Horwitz A. L. (1979) Genetic complementation studies of multiple sulfatase deficiency.Proc. Natl. Acad. Sci. USA 76, 6499–6499.

    Article  Google Scholar 

  • Ihler G. M., Glew R. H., and Schnure F. W. (1973) Enzyme loading of erythrocytes.Proc. Natl. Acad. Sci. USA 70, 2663–2666.

    PubMed  CAS  Article  Google Scholar 

  • Igisu H., Takahashi H., Suzuki K., and Suzuki K. (1983) Abnormal accumulation of galactosylceramide in the kidney of twitcher mouse.Biochem. Biophys. Res. Commun. 110, 940–944.

    PubMed  CAS  Google Scholar 

  • Igisu H. and Suzuki K. (1984) Glycolipids of the spinal cord, sciatic nerve and systemic organs of the twitcher mouse.J. Neuropath. Expt. Neurol. 43, 22–26.

    CAS  Google Scholar 

  • Inui K. and Wenger D. A. (1982) Properties of a protein activator of glycosphingolipid hydrolysis isolated from the liver of a patient with GM-1 gangliosidosis type I.Biochem. Biophys. Res. Commun. 105, 745–751.

    PubMed  CAS  Google Scholar 

  • Inui K. and Wenger D. A. (1983) Concentrations of an activator protein for sphingolipid hydrolysis in liver and brain samples from patients with lysosomal storage diseases.J. Clin. Invest. 72, 1622–1625.

    PubMed  CAS  Google Scholar 

  • Inui, K., Emmett, M., and Wenger, D. A. (1983) Immunological evidence for deficiency in an activator protein for sulfatide sulfatase in a variant form of metachromatic leukodystrophy.Proc. Natl. Acad. Sci. USA 80, 3074–3077.

    PubMed  CAS  Article  Google Scholar 

  • Ishibashi T., Maru A., Imai Y., Makita A., and Tsuji I. (1980) A varient form of arylsulfatase A in human urine derived from the renal pelvis.Biochim. Biophys. Acta 616, 218–227.

    PubMed  CAS  Google Scholar 

  • Ishizuka I., Inomata M., Ueeno K., and Yamakawa T. (1978) Sulfated glyceroglycolipid in rat brain. Structure, sulfationin vivo and accumulation in whole brain during development.J. Biol. Chem. 253, 898–907.

    PubMed  CAS  Google Scholar 

  • James G. T. and Austin J. H. (1979) Studies in metachromatic leukodystrophy XIV. Purification and subunit structure of human liver arylsufatase A.Clin. Chim. Acta 98, 103–111.

    PubMed  CAS  Article  Google Scholar 

  • Jatzkewitz H. (1958) Zwei Typen von Cerebrosid-Schwefelsaureestern als sog. Paralipoide and Speichersubstanzen bei der Leukodystrophie, Typ Scholz (Metachromatische Form der diffusen Skelerose).Hoppe-Seylers Z. Physiol. Chem. 311, 279–282.

    PubMed  CAS  Google Scholar 

  • Jatzkewitz H. (1978) Existence localization and some properties of the activators of sphingolipid hydrolases.Adv. Exp. Med. Biol. 101, 561–571.

    PubMed  CAS  Google Scholar 

  • Jerfy A. and Roy A. B. (1973) Comparison of the arylsulfatase and cerebroside sulfatase activities of sulfatase A.Biochim. Biophys. Acta. 293, 178–190.

    PubMed  CAS  Google Scholar 

  • Johnson K. H. (1970) Globoid leukodystrophy in the cat.J. Am. Vet. Med. Assoc. 157, 2057–2064.

    PubMed  CAS  Google Scholar 

  • Kihara H. (1982) Genetic heterogeneity in metachromatic leukodystrophy.Am. J. Hum. Genet. 34, 171–181.

    PubMed  CAS  Google Scholar 

  • Kobayashi T., Yamanaka T., Jacobs J. M., Teixeira F., and Suzuki K. (1980) The Twitcher mouse an emzymatically authentic model of human globoid cell leudodystrophy.Brain Res. 202, 479–483.

    PubMed  CAS  Article  Google Scholar 

  • Kobayashi T. and Suzuki K. (1982) The twitcher mouse: Fate of exogenously administered [3H]galactosylsphingosine.Adv. Expt. Med. Biol. 152, 253–259.

    CAS  Google Scholar 

  • Kolodny E. H. and Moser H. W. (1983) Sulfatide Lipidosis: Metachromatic Leukodystrophy, inThe Metabolic Basis of Inherited Diseases (Stanbury J. B., Wyngaarden J. B., Fredrickson D. S., Goldstein J. L., and Brain M. S. eds.), pp. 881–905. McGraw-Hill, New York.

    Google Scholar 

  • Kosugi M., Maru A., Mitsuhashi K., Koyanagi T., Ishibashi T., and Imai Y. (1983) Clinical significance of a variant form of urinary arylsulfatase A.Jap. J. Exp. Med. 53, 73–76.

    PubMed  CAS  Google Scholar 

  • Kresse H. and Holtfrerich D. (1980) Thiosulfate-mediated increase of arylsulfatase activities in multiple sulfatase deficiency disorder fibroblasts.Biochem. Biophys. Res. Commun. 97, 41–48.

    PubMed  CAS  Article  Google Scholar 

  • Lagenbeck U., Dunker P., Heipertz P., and Pilz H. (1977) Inheritance of metachromatic leukodystrophy.Am. J. Hum. Genet. 29, 639–640.

    Google Scholar 

  • Lee M. B., Sapirstein V. S., Reiss D. S., and Kolodny E. H. (1980) Carbonic anhydrase and 2′,3′ cyclic nucleotide 3′-phosphohydrolase activity in normal human brain and in demyelinating diseases.Neurology 30, 719–727.

    Google Scholar 

  • Li S. C. and Li Y. T. (1976) An activator stimulating the enzymic hydrolysis of sphingoglycolipids.J. Biol. Chem. 251, 1159–1163.

    PubMed  CAS  Google Scholar 

  • Li S. C., Nakamura T., Ogamo A., and Li Y-T. (1979) Evidence for the presence of two separate protein activators for the enzymic hydrolysis of GM-1 and GM-2 ganglioside.J. Biol. Chem. 254, 10592–10595.

    PubMed  CAS  Google Scholar 

  • Li Y. T. and Li S. C. (1983) Activator Proteins for Sphingolipid Hydrolysis, inThe Enzymes (Boyer P. D., ed.), pp. 427–445. Academic Press, New York.

    Google Scholar 

  • Loh H. H., Law P. Y., Ostwald T., Cho T. M., and Way E. L. (1978) Possible involvement of cerebroside sulfate in opiate receptor binding.Fed. Proc. 37, 147–152.

    PubMed  CAS  Google Scholar 

  • Lott I. T., Dulaney J. T., Milunsky A., Hoefnagel D., and Moser H. W. (1976) Apparent biochemical homozygosity in two obligatory heterozygotes of metachromatic leukodystrophy.J. Pediatr. 89, 483–440.

    Article  Google Scholar 

  • Luijten J. A. F. M., Heijden M. C. M. V., Rijksen G., and Staal G. E. J. (1978a) Purification and characterization of arylsulfatase A from human urine.J. Mol. Med. 3, 213–225.

    Google Scholar 

  • Luijten J. A. F. M., Heijden M. C. M. V., Rijksen G., Willemse J., and Staal G. E. J. (1978b) Characterization of arylsulfatase A of three cases of metachromatic leukodystrophy: One of the late infantile, one of the juvenile and one of the adult variant.J. Mol. Med. 3, 227–246.

    Google Scholar 

  • Martensson E. (1963) On the sulfate containing lipids of human kidney.Acta Chem. Scand. 17, 1174–1176.

    CAS  Google Scholar 

  • Martensson E. (1966) Sulfatide of human kidney: Isolation, identification and fatty acid composition.Biochim. Biophys. Acta 116, 521–531.

    PubMed  CAS  Google Scholar 

  • Mehl E. and Jatzkewitz H. (1964) Eine Cerebrosidulfatase aus Schweineniere.Hoppe-Seyler’s Z. Physiol. Chem. 339, 260–276.

    PubMed  CAS  Google Scholar 

  • Mehl E. and Jatzkewitz H. (1968) Cerebroside 3-sulfate as a physiological substrate of arylsulfatase A.Biochim. Biophys. Acta 151, 619–627.

    PubMed  CAS  Google Scholar 

  • Miyatake T. and Suzuki K. (1972) Globoid cell leukodystrophy: Additional deficiency of psychosine galactosidase.Biochem. Biophys. Res. Commun. 48, 538–543.

    CAS  Article  Google Scholar 

  • Miyatake T. and Suzuki K. (1975) Partial purification and characterization of β-galactosidase from rat brain hydrolysing glycosphingolipids.J. Biol. Chem. 250, 585–590.

    PubMed  CAS  Google Scholar 

  • Mohandas T., Shapiro L. J., Sparkes R. S., and Sparkes M. C. (1979) Regional assignment of the steroid sulfatase-X linked ichthyosis locus.Proc. Natl. Acad. Sci. USA 76, 5779–5783.

    PubMed  CAS  Article  Google Scholar 

  • Munnich A., Saudubray J. M., Hors-Cayla M. C., Poenaru L., Ogier H., Strecker G., Aicardi J., Frezal J., and Maroteaux P. (1982) Enzyme replacement therapy by transplantation of HLA-compatible fibroblasts in Sanfilippo syndrome: Another trial.Pediatr. Res. 16, 259–261.

    PubMed  CAS  Article  Google Scholar 

  • Murphy J. V., Wolfe H. J., Balaz E. A., and Moser H. (1971) A patient with deficiency of arylsulfatase A,B,C, and steroid sulphatase associated with storage of sulfatide, cholesterol and glycosaminoglycans inLipid Storage Diseases (Bernsohn J. and Gossman J., eds.), pp. 67–110. Academic Press, New York.

    Google Scholar 

  • Naoi M. and Yagi K. (1980) Incorporation of enzyme through blood-brain barrier into brain by means of liposomes:Biochem. Int. 1, 591–596.

    CAS  Google Scholar 

  • Navari R. M., Buckner C. D., Clift R. A., and Coleman K. M. (1984) Bone Marrow Transplantation,Lab. Med. 15, 245–250.

    Google Scholar 

  • Neuwelt E. A., Barranger J. A., Brady R. O., Pagel M., Furbish F. S., Quirk J. M., Mook G. E., and Frenkel E. (1981) Delivery of hexosaminidase A to the cerebrum after osmotic modification of the blood-brain barrier.Proc. Natl. Acad. Sci. USA 78, 5838–5841.

    PubMed  CAS  Article  Google Scholar 

  • Norton W. T. (1981) Biochemistry of Myelin in Demyelinating Diseases:Basic and Clinical Electrophysiology (Waxman S. G. and Ritchie J. M., eds.) pp. 93–121. Raven Press, New York.

    Google Scholar 

  • Nussbaum J. L. and Mandel P. (1972) Enzymic synthesis of psychosine sulfate.J. Neurochem. 19, 1789–1802.

    PubMed  CAS  Article  Google Scholar 

  • Oakey R. E. (1978) Placental sulfatase deficiency: antepartum differential diagnosis from foetal hypoplasia.Clin. Endocrinol. 9, 81–88.

    CAS  Google Scholar 

  • Oakey R. E., Cawood M., and MacDonald R. R. (1984) Biochemical and clinical observations in a pregnancy with placental sulfatase and other enzyme deficiencies.Clin. Endocrinol. 3, 131–148.

    Google Scholar 

  • O’Brien J. S. and Sampson E. L. (1965) Myelin membrane: A molecular abnormality.Science 150, 1613–1617.

    PubMed  CAS  Article  Google Scholar 

  • Okada S. and O’Brien J. S. (1968) Generalized gangliosidosis: β-Galactosidase deficiency.Science 160, 1002–1004.

    PubMed  CAS  Article  Google Scholar 

  • Okada S., Kato T., Yabuuchi H., Yoshino K., Naoi M., Kiuchi K., and Yagi K. (1984) Use of a fluorescent analogue of galactocerebroside for assay of galactocerebroside β-galactosidase activity in skin fibroblasts from patients with Krabbe’s disease.Clin. Chim. Acta 136, 57–63.

    PubMed  CAS  Article  Google Scholar 

  • Onodera H., Takada G., Tada K., and Desnick R. J. (1983) Microautoradiographic study on the tissue localization of liposome-entrapped or unentrapped3H-labeled β-galactosidase injected into rats.Tohoku J. Exp. Med. 140, 1–13.

    PubMed  CAS  Google Scholar 

  • Poduslo S. E., Tennekoon G., Price D., Miller K., and McKhann G. M. (1976) Fetal metachromatic leukodystrophy: Pathology, biochemistry and a study ofin vitro enzyme replacement in CNS tissue.J. Neuropath. Expt. Neurol. 35, 622–632.

    CAS  Google Scholar 

  • Porter, M. T., Fluharty A. L., Trammell J., and Kihara H. (1971a) A correlation of intracellular cerebroside sulfatase activity in fibroblasts with latency in metachromatic leukodystrophy.Biochem. Biophys. Res., Commun. 44, 660–666.

    CAS  Article  Google Scholar 

  • Porter M. T., Fluharty A. L., and Kihara H. (1971b) Correction of abnormal cerebroside sulfate metabolism in cultured metachromatic leukodystrophy fibroblasts.Science 172, 1263–1265.

    PubMed  CAS  Article  Google Scholar 

  • Porter M. T., Fluharty A. L., DelaFlor, S. D., and Kihara H. (1972) Cerebroside sulfate determination in human fibroblast.Biochim. Biophys. Acta 258, 769–778.

    PubMed  CAS  Google Scholar 

  • Pritchard D. H., Napthine D. V., and Sinclair A. J. (1980) Globoid cell leukodystrophy in polled dorset sheep.Vet. Path. 17, 399–405.

    CAS  Article  Google Scholar 

  • Rattazzi M. C., Lanse S. B., McCullough R. A., Nester J. A., and Jacobs E. A. (1980) Towards enzyme replacement in GM2 gangliosidosis, inEnzyme Therapy in Genetic Disease (Desnick R. J., Paul N. W., and Dickman F., eds.) pp. 179–193. Liss, New York.

    Google Scholar 

  • Rattazzi M. C., Appel, A. M., Baker H. J., and Nester J. (1981) Towards Enzyme Replacement in GM2 Gangliosidosis, inLysosomes and Lysosomal Storage Diseases (Callahan J. W. and Lowden J. A., eds.), pp. 527–537. Raven Press, New York.

    Google Scholar 

  • Rose F. A. (1982) The mammalian sulfatases and placental sulfatase deficiency in man.J. Inher. Metab. Dis. 5, 145–152.

    PubMed  CAS  Article  Google Scholar 

  • Sarafian T. A., Fluharty A. L., Kihara H., Helfand G., and Edmond J. (1982) Large scale purification of pyrogen-free human arylsulfatase A.J. Appl. Biochem. 4, 126–132.

    CAS  Google Scholar 

  • Scaravilli F. and Jacobs J. M. (1981) Peripheral nerve grafts in hereditary leukodystrophic mutant mice (twitcher).Nature 290, 56–58.

    PubMed  CAS  Article  Google Scholar 

  • Scaravilli F. and Jacobs J. M. (1982) Improved myelination in nerve grafts from the leucodystrophic twitcher into trembler mice: Evidence for enzyme replacement.Brain Res. 237, 163–172.

    PubMed  CAS  Article  Google Scholar 

  • Shapira E. and Nadler H. L. (1975a) The nature of the residual arylsulfatase activity in metachromatic leukodystrophy.J. Pediatr. 86, 881–882.

    PubMed  CAS  Article  Google Scholar 

  • Shapira E. and Nadler H. L. (1975b) Purification and some properties of soluble human liver arylsulfatases.Arch. Biochem. Biophys. 170, 179–187.

    PubMed  CAS  Article  Google Scholar 

  • Shapiro L. J., Cousins L., Fluharty A. L., Stevens R. L. and Kihara H. (1977) Steroid sulfatase deficiency.Pediat. Res. 11, 894–897.

    PubMed  CAS  Google Scholar 

  • Shapiro L. J., Weiss R., Buxman M. M., Vidgoff J. Dimond R. L., Roller J. A. and Wells R. S. (1978) Enzymatic basis of typicalX-linked ichthyosis.Lancet 2, 756–757.

    PubMed  CAS  Article  Google Scholar 

  • Shapiro L.J., Aleck K. A., Kaback M. M., Itabashi H., Desnick R. J., Brand N., Stevens R. L., Fluharty A. L., and Kihara H. (1979) Metachromatic leukodystrophy without arylsulfatase A deficiency.Pediatr. Res. 13, 1179–1181.

    PubMed  CAS  Article  Google Scholar 

  • Stevens R. L., Hartman M., Fluharty A. L., and Kihara H. (1973) A second form of arylsulfatase A in human urine.Biochim. Biophys. Acta 302, 338–344.

    PubMed  CAS  Google Scholar 

  • Stevens, R. L., Fluharty A. L., Skokut M. H., and Kihara H. (1975) Purification and properties of arylsulfatase A from human urine.J. Biol. Chem. 250, 2495–2501.

    PubMed  CAS  Google Scholar 

  • Stevens R. L., Fluharty A. L., Killgrove A. R., and Kihara H. (1976) Microheterogeneity of arylsulfatase A from human tissues.Biochim. Biophys. Acta 445, 661–671.

    PubMed  CAS  Google Scholar 

  • Stevens R. L., Fluharty A. L., Kihara H., Kaback M. M., Shapiro L. J., Marsh B., Sandhoff K., and Fischer G. (1981) Cerebroside sulfatase activator deficiency induced metachromatic leukodystrophy.Am. J. Hum. Genet. 33, 900–906.

    PubMed  CAS  Google Scholar 

  • Stoffyn P. and Stoffyn A. (1963) Structure of sulfatide.Biochim. Biophys. Acta 70, 218–220.

    PubMed  CAS  Article  Google Scholar 

  • Stumpf D., Neuwelt E., Austin J., and Kohler P. (1971) Metachromatic leukodystrophy (MLD) X. Immunological studies of the abnormal sulfatase A.Arch. Neurol. Chic. 25, 427–431.

    CAS  Google Scholar 

  • Stumpf D. and Austin J. (1971) Metachromatic leukodystrophy (MLD) IX. Qualitative and quantitative difference in urinary arylsulfatase A in different forms of MLD.Arch. Neurol. 24, 117–124.

    PubMed  CAS  Google Scholar 

  • Subba Rao G., Narcia L. N., Pieringer J., and Pieringer R. A. (1977) The biosynthesis of sulfogalactosyldiacylglycerol of rat brainin vitro.Biochem. J. 166, 429–435.

    Google Scholar 

  • Suzuki Y. and Mizuno Y. (1974) Juvenile metachromatic leukodystrophy: Deficiency of an arylsulfatase A component.J. Pediatr. 85, 824–825.

    Google Scholar 

  • Suzuki Y. and Suzuki K. (1971) Krabbe’s globoid cell leukodystrophy: Deficiency of galactocerebrosidase in serum, leukocytes and fibroblasts.Science 171, 73–75.

    PubMed  CAS  Article  Google Scholar 

  • Suzuki Y. and Suzuki K. (1974) Sphingolipid β-galactosidase: Electrofocusing characterization of the enzymes in human globoid cell leukodystrophy (Krabbe’s disease).J. Biol. Chem. 249, 2105–2108.

    PubMed  CAS  Google Scholar 

  • Suzuki K. and Suzuki Y. (1983) Galactosylceramide Lipidosis: Globoid Cell Leucodystrophy, inMetabolic Basis of Inherited Diseases (Stanbury J. B., Wyngaarden J. B., Fredrickson D. S., Goldstein J. L., and Brown M. S., eds., pp. 857–880. McGraw-Hill, New York.)

    Google Scholar 

  • Suzuki K., Schneider E. L., and Epstein C. J. (1971)In utero diagnosis of globoid cell leukodystrophy (Krabbe’s disease).Biochem. Biophys. Res. Commun. 45, 1363–1366.

    PubMed  CAS  Article  Google Scholar 

  • Svennerholm L. (1963) Some Aspects of the Biological Changes in Leukodystrophy, inBrain Lipids and Lipoproteins and Leukodystrophics, pp. 104–109, Elsevier, Amsterdam.

    Google Scholar 

  • Svennerholm L., Vanier M., and Mansson J. (1980) Krabbe’s disease: a galactosphingosine (psychosine) lipidosis.J. Lipid Res. 21, 53–64.

    PubMed  CAS  Google Scholar 

  • Takada G., Onadera H., and Tada K. (1982) Delivery of fungal α-galactosidase to rat brain by means of liposomes.Tohoku J. Exp. Med. 136, 219–230.

    PubMed  CAS  Google Scholar 

  • Takahashi H., Igisu H., Suzuki K., and Suzuki K. (1983) The twitcher mouse: An ultrastructural study on the oligodendroglia.Acta Neuropath. 59, 159–166.

    PubMed  CAS  Article  Google Scholar 

  • Takahashi H. and Suzuki K. (1984) Demyelination in the spinal cord of murine globoid cell leukodystrophy (The twitcher mouse).Acta Neuropath. 62, 298–308.

    PubMed  CAS  Article  Google Scholar 

  • Taketomi T. and Nishimura K. (1964) Physiological activity of psychosine.Jap. J. Exp. Med. 34, 255–265.

    PubMed  CAS  Google Scholar 

  • Taori G. M., Mammen K. C., Kokrady S., Martin B., Bhaktaviziam A., and Bachawat B. K. (1970) Globoid leukodystrophy (Krabbe’s disease).Ind. J. Med. Res. 58, 993–1001.

    CAS  Google Scholar 

  • Tyrrell D. A., Heath T. D., Colley C. M., and Ryman B. E. (1976) New aspects of liposomes.Biochim. Biophys. Acta 457, 259–302.

    PubMed  CAS  Google Scholar 

  • Uchida T., Egami F., and Roy A. B. (1981) 3′, 5′-cyclic nucleotide phosphodiesterase activity of the sulfatase A of ox liver.Biochim. Biophys. Acta 657, 356–363.

    PubMed  CAS  Google Scholar 

  • Vanier M. T. and Svennerholm L. (1975) Chemical pathology of Krabbe’s disease III. Ceramide and ganglioside of brain.Acta Paediatr. Scand. 64, 641–648.

    PubMed  CAS  Article  Google Scholar 

  • Vanier M. and Svennerholm L. (1976) Chemical pathology of Krabbe’s disease. The occurrence of psychosine and other neutral sphingoglycolipids inCurrent Trends in Sphingolipidoses and Allied Disorders (Volk B. W. and Schneck L., ed.), pp. 115–126, Plenum, New York.

    Google Scholar 

  • Waheed A., Hasilik A., and Von-Figura K. (1982) Enhanced breakdown of arylsulfatase A in multiple sulfatase deficiency.Eur. J. Biochem. 123, 317–321.

    PubMed  CAS  Article  Google Scholar 

  • Waheed A., Steckel F., Hasilik A., and Von-Figura K. (1983) Two allelic forms of human arylsulfatase A with different numbers of asparagin-linked oligosaccharides.Am. J. Hum. Genet. 35, 228–233.

    PubMed  CAS  Google Scholar 

  • Weismann U., Rossi E., Herschkowitz N. (1972) Correction of defective sulfatide degradation in cultured fibroblasts from patients with metachromatic leukodystrophy.Acta. Pediatr. Scand. 61, 296–302.

    Article  Google Scholar 

  • Wenger D. A., Sattler M., and Hiatt W. (1974) Globoid cell leukodystrophy: Deficiency of lactosylceramide β-galactosidase.Proc. Natl. Acad. Sci. USA 71, 854–857.

    PubMed  CAS  Article  Google Scholar 

  • Wenger D. A., Sattler M., and Marley S. P. (1973) Deficiency of monogalactosyl diglyceride in Krabbe’s disease.Biochem. Biophys. Res. Commun. 53, 680–685.

    PubMed  CAS  Article  Google Scholar 

  • Winchester B. (1982) Animal models of human genetic diseases.Trends Biochem. Sci. 7, 71–74.

    Article  Google Scholar 

  • Yamakawa T., Kiso N., Handa S., Makita A., and Yokoyama S. (1962) On the structure of brain cerebroside sulfuric ester and ceramide dihexoside of erythrocyte.J. Biochem. (Tokyo) 52, 266–227.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Farooqui, A.A., Horrocks, L.A. Biochemical aspects of globoid and metachromatic leukodystrophies. Neurochemical Pathology 2, 189–218 (1984). https://doi.org/10.1007/BF02834352

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02834352

Index Entries

  • Biochemistry, of the leukodystrophies
  • leukodystrophies, the biochemistry of, globoid cell leukodystrophy, galactocerebroside β-galactosidase deficiency in
  • leukodystrophy, globoid cell
  • metachromatic leukodystrophy, arylsulfatase A deficiency in
  • galactocerebroside β-galactosidase deficiency, in globoid cell leukodystrophy
  • arylsulfatase A deficiency, in metachromatic leukodystrophy