Paradoxical influence of acid β-galactosidase gene dosage on phenotype of the twitcher mouse (genetic galactosylceramidase deficiency)

Human Molecular Genetics

Volumn 9, Issue 11, 2000, Pages 1699-1707

  Tohyama, Jun ^a,c   Vanier, Marie T ^b   Suzuki, Kinuko ^a   Ezoe, Takanori ^a,d   Matsuda, Junko ^a   Suzuki, Kunihiko ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b INSERM   (France)

^c National Hospital Organization   (Japan)

^d Tokyo Metropol Higashi yamato M   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; GALACTOSYLCERAMIDASE; LACTOSYLCERAMIDE; PSYCHOSINE;

ARTICLE; AUTOSOMAL RECESSIVE INHERITANCE; BIOACCUMULATION; BRAIN LEVEL; CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL FEATURE; DISEASE SEVERITY; ENZYME DEFICIENCY; GENE DOSAGE; GENOTYPE; HIPPOCAMPUS; KNOCKOUT MOUSE; LIFESPAN; NERVE CELL DEGENERATION; PHENOTYPE; PRIORITY JOURNAL; SEIZURE;

ANIMALS; BETA-GALACTOSIDASE; CENTRAL NERVOUS SYSTEM; FEMALE; GALACTOSYLCERAMIDASE; GENOTYPE; GROWTH DISORDERS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NERVE DEGENERATION; PHENOTYPE; SURVIVAL RATE; TIME FACTORS;

EID: 0034234489     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Bowen, D. and Radin, N.S. (1969) Cerebroside galactosidase: a method for determination and a comparison with other lysosomal enzymes in developing rat brain. J. Neurochem., 16, 501-511.
2. Miyatake, T. and Suzuki, K. (1972) Globoid cell leukodystrophy: additional deficiency of psychosine galactosidase. Biochem. Biophys. Res. Commun., 48, 538-543.
3. Wenger, D.A., Sattler, M. and Hiatt, W. (1974) Globoid cell leukodystrophy: deficiency of lactosyl ceramide beta-galactosidase. Proc. Natl Acad. Sci. USA, 71, 854-857.
4. Tanaka, H. and Suzuki, K. (1975) Lactosylceramide β-galactosidase in human sphingolipidoses: evidence for two genetically distinct enzymes. J. Biol. Chem., 250, 2324-2332.
5. Wenger, D.A., Sattler, M. and Markey, J.P. (1973) Deficiency of monogalactosyl diglyceride β-galactosidase activity in Krabbe's disease. Biochem. Biophys. Res. Commun., 53, 680-685.
6. Suzuki, K. and Suzuki, Y. (1970) Globoid cell leucodystrophy (Krabbe's disease): deficiency of galactocerebroside β-galactosidase. Proc. Natl Acad. Sci. USA, 66, 302-309.
7. Suzuki, K., Suzuki, Y. and Suzuki, K. (1995) In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), Metabolic and Molecular Basis of Inherited Disease. McGraw-Hilt, New York, NY, pp. 2671-2692.
8. Vanier, M.-T. and Svennerholm, L. (1976) In Volk, B.W. and Schneck, L. (eds), Current Trends in Sphingolipidoses and Allied Disorders. Plenum Press, New York, NY. Vol. 68, pp. 115-126.
9. Svennerholm, L., Vanier, M.-T. and Månsson, J.-E. (1980) Krabbe disease: a galactosylsphingosine (psychosine) lipidosis. J. Lipid Res., 21, 53-64.
10. Austin, J.H. and Lehfeldt, D. (1965) Studies in globoid (Krabbe) leukodystrophy. III. Significance of experimentally-produced globoid-like elements in rat white matter and spleen. J. Neuropathol. Exp. Neurol., 24, 265-289.
11. Suzuki, K., Tanaka, H. and Suzuki, K. (1976) In Volk, B.W. and Schneck, L. (eds), Current Trends in Sphingolipidoses and Allied Disorders. Plenum Press, New York, NY, pp. 99-113.
12. Kobayashi, T., Yamanaka, T., Jacobs, J.M., Teixeira, F. and Suzuki, K. (1980) The twitcher mouse: an enzymatically authentic model of human globoid cell leukodystrophy (Krabbe disease). Brain Res., 202, 479-483.
13. Sakai, N., Inui, K., Tatsumi, N., Fukushima, H., Nishigaki, T., Taniike, M., Nishimoto, J., Tsukamoto, H., Yanagihara, I., Ozone, K. and Okada, S. (1996) Molecular cloning and expression of cDNA for murine galactocerebrosidase and mutation analysis of the twitcher mouse, a model of Krabbe's disease. J. Neurochem., 66, 1118-1124.
14. Igisu, H. and Suzuki, K. (1984) Progressive accumulation of toxic metabolite in a genetic leukodystrophy. Science, 224, 753-755.
15. Okada, S. and O'Brien, J.S. (1968) Generalized gangliosidosis: beta-galactosidase deficiency. Science, 160, 1002-1004.
16. Tanaka, H. and Suzuki, K. (1977) Sustrate specificities of the two genetically distinct human brain β-galactosidases. Brain Res., 122, 325-335.
17. Suzuki, K. (1968) Cerebral GM1-gangliosidosis: chemical pathology of visceral organs. Science, 159, 1471-1472.
18. Suzuki, Y., Sakuraba, H. and Oshima, A. (1995) In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Basis of Inherited Disease. McGraw-Hill, New York, NY, pp. 2785-2823.
19. Chen, Y.Q., Rafi, M.A., De Gala, G. and Wenger, D.A. (1993) Cloning and expression of cDNA encoding human galactocerebrosidase, the enzyme deficient in globoid cell leukodystrophy. Hum. Mol. Genet., 2, 1841-1845.
20. Oshima, A., Tsuji, A., Nagano, Y., Sakuraba, H. and Suzuki, Y. (1988) Cloning, sequencing and expression of cDNA for human beta-galactosidase. Biochem. Biophys. Res. Commun., 157, 238-244.
21. M1-ganglioside accumulation in mice defective in lysosomal acid β-galactosidase. Hum. Mol. Genet., 6, 205-211.
22. M1-gangliosidosis. Glycoconjugate J., 14, 729-736.
23. Matsuda, J., Suzuki, O., Oshima, A., Ogura, A., Naiki, M. and Suzuki, Y. (1997) Neurological manifestations of knockout mice with β-galactosidase deficiency. Brain Dev., 19, 19-20.
24. Ezeo, T., Vanier, M.T., Oya, Y., Popko, B., Tohyama, J., Matsuda, J., Suzuki, K. and Suzuki, K. (2000) Biochemistry and neuropathology of mice doubly deficient in synthesis and degradation of galactosylceramide. J. Neurosci. Res., 59, 170-178.
25. Igisu, H., Shimomura, K., Kishimoto, Y. and Suzuki, K. (1983) Lipids of developing brain of twitcher mouse - an authentic murine model of human Krabbe disease. Brain, 106, 405-417.
26. Ida, H., Umezawa, F., Kasai, E., Eto, Y. and Maekawa, K. (1982) An accumulation of galactocerebroside in kidney from mouse globoid cell leukodystrophy (twitcher). Biochem. Biophys. Res. Commun., 109, 634-638.
27. 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.
28. Orvisky, E., McKinney, C.E., Krasnewich, D., Eliason, W.K., Tuyebi, N., Martin, B.M., Ginns, E.I. and Sidransky, E. (1997) Glucosylsphingosine accumulation in the brain, liver and spleen of type 2 Gaucher mice. Am. J. Hum. Genet., 61, A258.
29. Ferrari, G., Anderson, B.L., Stephens, R.M., Kaplan, D.R. and Greene, L.A. (1995) Prevention of apoptotic neuronal death by GM1 ganglioside. Involvement of Trk neurotrophin receptors. J. Biol. Chem., 270, 3074-3080.
30. Cavallini, L., Venerando, R., Miotto, G. and Alexandre, A. (1999) Ganglioside GM1 protection from apoptosis of rat heart fibroblasts. Arch. Biochem. Biophys., 370, 156-162.
31. Kobayashi, T., Shinnoh, N., Goto, I. and Kuroiwa, Y. (1985) Hydrolysis of galactosylceramide is catalyzed by two genetically distinct acid beta-galactosidases. J. Biol. Chem., 260, 14982-14987.
32. Warren, K.R., Misra, R.S., Arora, R.C. and Radin, N.S. (1976) Glycosyltransferases of rat brain that make cerebrosides: substrate specificity, inhibitors and abnormal products. J. Neurochem., 26, 1063-1072.
33. Radin, N.S. (1999) Chemotherapy by slowing glucosphingolipid synthesis. Biochem. Pharmacol., 57, 589-595.
34. Platt, F.M., Neises, G.R., Reinkensmeier, G., Townsend, M.J., Perry, V.H., Proia, R.L., Winchester, B., Dwek, R.A. and Butters, T.D. (1997) Prevention of lysosomal storage in Tay-Sachs mice treated with N-butyldeoxynojirimycin. Science, 276, 428-431.
35. Platt, F.M. and Butters, T.D. (1998) New therapeutic prospects for the glycosphingolipid lysosomal storage diseases. Biochem. Pharmacol., 56, 421-430.
36. Jeyakumar, M., Butters, T.D., Cortina-Borja, M., Hunnam, V., Proia, R.L., Perry, V.H., Dwek, R.A. and Platt, F.M. (1999) Delayed symptom onset and increased life expectancy in Sandhoff disease mice treated with N-butyldeoxynojirimycin. Proc. Natl Acad. Sci. USA, 96, 6388-6393.
37. Ezoe, T., Vainer, M.T., Oya, Y., Popko, B., Tohyama, J., Matsuda, J., Suzuki, K. and Suzuki, K. (2000) Twitcher mice with only a single active galactosylceramide synthase gene exhibit clearly detectable but therapeutically minor phenotypic improvements. J. Neurosci. Res., 59, 171-187.
38. Matsushima, G.K., Taniike, M., Glimcher, L.H., Grusby, M.J., Frelinger. J.A., Suzuki, K. and Ting, J.P.Y. (1994) Absence of MHC class II molecules reduces CNS demyelination, microglial macrophage infiltration and twitching in murine globoid cell leukodystrophy. Cell, 78, 645-656.
39. Schmid, C.D., Stienekemeier, M., Oehen, S., Bootz, F., Zielasek, J., Gold, R., Toyka, K.V., Schachner, M. and Martini, R. (2000) Immune deficiency in mouse models for inherited peripheral neuropathies leads to improved myelin maintenance. J. Neurosci., 20, 729-735.
40. Tybulewicz, V.L., Crawford, C.E., Jackson, P.K., Bronson, R.T. and Mulligan, R.C. (1991) Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell. 65, 1153-1163.
41. Suzuki, K. (1987) Enzymatic diagnosis of sphingolipidoses. Methods Enzymol., 138, 727-762.
42. Oya, Y., Nakayasu, H., Fujita, N., Suzuki, K. and Suzuki, K. (1998) Pathological study of mice with total deficiency of sphingolipid activator proteins (SAP knockout mice). Acta Neuropathol., 96, 29-40.
43. Fujita, N., Suzuki, K., Vanier, M.T., Popko, B., Maeda, N., Klein, A., Henseler, M., Sandhoff, K., Nakayasu, H. and Suzuki, K. (1996) Targeted disruption of the mouse sphingolipid activator protein gene: a complex phenotype, including severe leukodystrophy and wide-spread storage of multiple sphingolipids. Hum. Mol. Genet., 5, 711-725.
44. Kyrklund, T. (1987) Two procedures to remove polar contaminants from a crude brain lipid extract by using prepacked reverse-phase columns. Lipids, 22, 274-277.
45. Abramson, M.B., Norton, W.T. and Katzman, R. (1965) Study of ionic structure in phospholipids by infrared spectra. J. Biol. Chem., 240, 2389-2395.
46. Merrill Jr, A.H., Wang, E., Mullins, R.E., Jamison, W.C., Nimkar, S. and Liotta, D.C. (1988) Quantitation of free sphingosine in liver by high-performance liquid chromatography. Anal. Biochem., 171, 373-381.
47. Rodriguez-Lafrasse, C., Rousson, R., Pentchev, P.G., Louisot, P. and Vanier, M.T. (1994) Free sphingoid bases in tissues from patients with type C Niemann-Pick disease and other lysosomal storage disorders. Biochim. Biophys. Acta, 1226, 138-144.
48. Matsumoto, A. Vanier, M.T., Oya, Y., Kelly, D., Popko, B., Wenger, D.A., Suzuki, K. and Suzuki, K. (1997) Minimal increment in galactosylceramidase expression is sufficient for significant phenotypic improvement in twitcher mouse. Dev. Brain Dysfunct., 10, 142-154.
49. Klein, A., Henseler, M., Klein, C., Suzuki, K., Harzer, K. and Sandhoff, K. (1994) Sphingolipid activator protein D (sap-D) stimulates the lysosomal degradation of ceramide in vivo. Biochem. Biophys. Res. Commun., 200, 1440-1448.