Elevated sulfatide levels in neurons cause lethal audiogenic seizures in mice

Journal of Neurochemistry

Volumn 112, Issue 1, 2010, Pages 282-295

  Van Zyl, Rebekka ^a   Gieselmann, Volkmar ^a   Eckhardt, Matthias ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Audiogenic seizure; Galactosylceramide; Metachromatic leukodystrophy; Sulfatide; Transgenic mice

Indexed keywords

ADENOSINE 3' PHOSPHO 5' PHOSPHOSULFATE:CEREBROSIDE SULFOTRANSFERASE; GALACTOSYLCERAMIDE; GALACTOSYLTRANSFERASE; SULFATIDE; SULFOTRANSFERASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GALACTOSE:CERAMIDE GALACTOSYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDIOGENIC SEIZURE; AUDITORY STIMULATION; CONTROLLED STUDY; FATTY ACID SYNTHESIS; FEMALE; GENE EXPRESSION; GLIA CELL; LETHALITY; LIFESPAN; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENE; TRANSGENIC MOUSE;

ACOUSTIC STIMULATION; ANIMALS; BRAIN; EPILEPSY, REFLEX; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; SEIZURES; SULFOGLYCOSPHINGOLIPIDS;

MUS; MUS MUSCULUS;

EID: 71649110531     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06458.x     Document Type: Article

References (54)

1. Abe T. Norton W. T. (1974) The characterization of sphingolipids from neurons and astroglia of immature rat brain. J. Neurochem. 23, 1025 1036.
2. + channels. Science 247, 852 854.
3. Becker I., Wang-Eckhardt L., Yaghootfam A., Gieselmann V. Eckhardt M. (2008) Differential expression of (dihydro)ceramide synthases in mouse brain: oligodendrocyte-specific expression of CerS2/Lass2. Histochem. Cell Biol. 129, 233 241.
4. Benjamins J. A., Guarnieri M., Miller K., Sonneborn M. McKhann G. M. (1974) Sulphatide synthesis in isolated oligodendroglial and neuronal cells. J. Neurochem. 23, 751 757.
5. Bligh E. G. Dyer W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911 917.
6. +)-dependent exocytosis in rat pancreatic beta-cells. Diabetes 51, 2514 2521.
7. Calderon R. O., Attema B. DeVries G. H. (1995) Lipid composition of neuronal cell bodies and neurites from cultured dorsal root ganglia. J. Neurochem. 64, 424 429.
8. Carlin R. K., Grab D. J., Cohen R. S. Siekevitz P. (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86, 831 845.
9. Cheng H., Xu J., McKeel D. W. Han X. (2003) Specificity and potential mechanism of sulfatide deficiency in Alzheimer's disease: an electrospray ionization mass spectrometric study. Cell. Mol. Biol. (Noisy-le-grand) 49, 809 818.
10. Chi S. Qi Z. (2006) Regulatory effect of sulphatides on BKCa channels. Br. J. Pharmacol. 149, 1031 1038.
11. Coenen R., Gieselmann V. Lüllmann-Rauch R. (2001) Morphological alterations in the inner ear of the arylsulfatase A-deficient mouse. Acta Neuropathol. 101, 491 498.
12. D'Hooge R., Coenen R., Gieselmann V., Lüllmann-Rauch R. De Deyn P. P. (1999) Decline in brainstem auditory-evoked potentials coincides with loss of spiral ganglion cells in arylsulfatase A-deficient mice. Brain Res. 847, 352 356.
13. DeVries G. H. Zmachinski C. J. (1980) The lipid composition of rat CNS axolemma-enriched fractions. J. Neurochem. 34, 424 430.
14. Eckhardt M., Yaghootfam A., Fewou S. N., Zöller I. Gieselmann V. (2005) A mammalian fatty acid hydroxylase responsible for the formation of α-hydroxylated galactosylceramide in myelin. Biochem. J. 388, 245 254.
15. Eckhardt M. (2008) The role and metabolism of sulfatide in the nervous system. Mol. Neurobiol. 37, 93 103.
16. Eckhardt M., Barth H., Blöcker D. Aktories K. (2000) Binding of Clostridium botulinum C2 toxin to asparagine-linked complex and hybrid carbohydrates. J. Biol. Chem. 275, 2328 2334. (Pubitemid 30081989)
17. Eckhardt M., Hedayati K. K., Pitsch J., Lüllmann-Rauch R., Beck H., Fewou S. N. Gieselmann V. (2007) Sulfatide storage in neurons causes hyperexcitability and axonal degeneration in a mouse model of metachromatic leukodystrophy. J. Neurosci. 27, 9009 9021.
18. Faingold C. L. (2002) Role of GABA abnormalities in the inferior colliculus pathophysiology-audiogenic seizures. Hear. Res. 168, 223 237.
19. Fewou S. N., Büssow H., Schaeren-Wiemers N., Vanier M. T., Macklin W. B., Gieselmann V. Eckhardt M. (2005) Reversal of non-hydroxy:alpha-hydroxy galactosylceramide ratio and unstable myelin in transgenic mice overexpressing UDP-galactose:ceramide galactosyltransferase. J. Neurochem. 94, 469 481.
20. Frank M., van der Haar M. E., Schaeren-Wiemers N. Schwab M. E. (1998) rMAL is a glycosphingolipid-associated protein of myelin and apical membranes of epithelial cells in kidney and stomach. J. Neurosci. 18, 4901 4913.
21. Han X. (2004) The role of apolipoprotein E in lipid metabolism in the central nervous system. Cell. Mol. Life Sci. 61, 1896 1906.
22. Han X., Holtzman D. M., McKeel D. W., Kelley J. Morris J. C. (2002) Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis. J. Neurochem. 82, 809 818.
23. Hermansson M., Käkelä R., Berghäll M., Lehesjoki A. E., Somerharju P. Lahtinen U. (2005) Mass spectrometric analysis reveals changes in phospholipid, neutral sphingolipid and sulfatide molecular species in progressive epilepsy with mental retardation, EPMR, brain: a case study. J. Neurochem. 95, 609 617.
24. Honke K., Tsuda M., Hirahara Y., Ishii A., Makita A. Wada Y. (1997) Molecular cloning and expression of cDNA encoding human 3′- phosphoadenylylsulfate:galactosylceramide 3′-sulfotransferase. J. Biol. Chem. 272, 4864 4868.
25. Honke K., Hirahara Y., Dupree J. et al. (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc. Natl. Acad. Sci. U S A 99, 4227 4232.
26. Honke K., Zhang Y., Cheng X., Kotani N. Taniguchi N. (2004) Biological roles of sulfoglycolipids and pathophysiology of their deficiency. Glycoconj. J. 21, 59 62.
27. Isaac G., Pernber Z., Gieselmann V., Hansson E., Bergquist J. Månsson J. E. (2006) Sulfatide with short fatty acid dominates in astrocytes and neurons. FEBS J. 273, 1782 1790.
28. Ishibashi T., Dupree J. L., Ikenaka K., Hirahara Y., Honke K., Peles E., Popko B., Suzuki K., Nishino H. Baba H. (2002) A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J. Neurosci. 22, 6507 6514.
29. +)ATPase. Arch. Biochem. Biophys. 238, 558 564.
30. Karschin C., Ecke C., Ashcroft F. M. Karschin A. (1997) Overlapping distribution of K(ATP) channel-forming Kir6.2 subunit and the sulfonylurea receptor SUR1 in rodent brain. FEBS Lett. 401, 59 64.
31. Kawai H., Allende M. L., Wada R. et al. (2001) Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures. J. Biol. Chem. 276, 6885 6888.
32. Kohlschütter A. Herschkowitz N. N. (1973) Sulfatide synthesis in neurons: a defect in mice with a hereditary myelination disorder. Brain Res. 50, 379 385.
33. +)-ATPase alpha-subunit in Drosophila melanogaster. EMBO J. 8, 193 202.
34. Lingwood D., Harauz G. Ballantyne J. S. (2005) Regulation of fish gill Na(+)-K(+)-ATPase by selective sulfatide-enriched raft partitioning during seawater adaptation. J. Biol. Chem. 280, 36545 36550.
35. Marcus J., Honigbaum S., Shroff S., Honke K., Rosenbluth J. Dupree J. L. (2006) Sulfatide is essential for the maintenance of CNS myelin and axon structure. Glia 53, 372 381.
36. Molander-Melin M., Pernber Z., Franken S., Gieselmann V., Månsson J. E. Fredman P. (2004) Accumulation of sulfatide in neuronal and glial cells of arylsulfatase A deficient mice. J. Neurocytol. 33, 417 427.
37. Mourre C., Ben Ari Y., Bernardi H., Fosset M. Lazdunski M. (1989) Antidiabetic sulfonylureas: localization of binding sites in the brain and effects on the hyperpolarization induced by anoxia in hippocampal slices. Brain Res. 486, 159 164.
38. Peng L. Suzuki K. (1987) Ultrastructural study of neurons in metachromatic leukodystrophy. Clin. Neuropathol. 6, 224 230.
39. Pernber Z., Molander-Melin M., Berthold C. H., Hansson E. Fredman P. (2002) Expression of the myelin and oligodendrocyte progenitor marker sulfatide in neurons and astrocytes of adult rat brain. J. Neurosci. Res. 69, 86 93.
40. Raghavan S. Kanfer J. N. (1972) Ceramide galactoside of enriched neuronal and glial fractions from rat brain. J. Biol. Chem. 247, 1055 1056.
41. Ramakrishnan H., Hedayati K. K., Lüllmann-Rauch R., Wessig C., Fewou S. N., Maier H., Goebel H. H., Gieselmann V. Eckhardt M. (2007) Increasing sulfatide synthesis in myelin-forming cells of arylsulfatase A-deficient mice causes demyelination and neurological symptoms reminiscent of human metachromatic leukodystrophy. J. Neurosci. 27, 9482 9490.
42. Ramu Y., Xu Y. Lu Z. (2006) Enzymatic activation of voltage-gated potassium channels. Nature 442, 696 699.
43. Ross K. C. Coleman J. R. (2000) Developmental and genetic audiogenic seizure models: behavior and biological substrates. Neurosci. Biobehav. Rev. 24, 639 653.
44. Saravanan K., Schaeren-Wiemers N., Klein D., Sandhoff R., Schwarz A., Yaghootfam A., Gieselmann V. Franken S. (2004) Specific downregulation and mistargeting of the lipid raft-associated protein MAL in a glycolipid storage disorder. Neurobiol. Dis. 16, 396 406.
45. Schaeren-Wiemers N., van der Bijl P. Schwab M. E. (1995) The UDP-galactose:ceramide galactosyltransferase: expression pattern in oligodendrocytes and Schwann cells during myelination and substrate preference for hydroxyceramide. J. Neurochem. 65, 2267 2278.
46. Stroobants S., Leroy T., Eckhardt M., Aerts J. M., Berckmans D. D'Hooge R. (2008) Early signs of neurolipidosis-related behavioural alterations in a murine model of metachromatic leukodystrophy. Behav. Brain Res. 189, 306 316.
47. Vainio S., Bykov I., Hermansson M., Jokitalo E., Somerharju P. Ikonen E. (2005) Defective insulin receptor activation and altered lipid rafts in Niemann-Pick type C disease hepatocytes. Biochem. J. 391, 465 472.
48. Von Figura K., Gieselmann V. Jaeken J. (2001) Metachromatic leukodystrophy, in The Metabolic and Molecular Basis of Inherited Disease (Scriver C. R., Beaudet A. L., Valle D. Sly W. S., eds pp. 3695 3724. McGraw Hill, New York.
49. Williams M. A. McCluer R. H. (1980) The use of Sep-Pak C18 cartridges during the isolation of gangliosides. J. Neurochem. 35, 266 269.
50. Wittke D., Hartmann D., Gieselmann V. Lüllmann-Rauch R. (2004) Lysosomal sulfatide storage in the brain of arylsulfatase A-deficient mice: cellular alterations and topographic distribution. Acta Neuropathol. 108, 261 271.
51. Yaghootfam A., Gieselmann V. Eckhardt M. (2005) Delay of myelin formation in arylsulphatase A-deficient mice. Eur. J. Neurosci. 21, 711 720.
52. Yaghootfam A., Sorkalla T., Häberlein H., Gieselmann V., Kappler J. Eckhardt M. (2007) Cerebroside sulfotransferase forms homodimers in living cells. Biochemistry 46, 9260 6269.
53. Zambrano F. Rojas M. (1987) Sulphatide content in a membrane fraction isolated from rabbit gastric mucosal: its possible role in the enzyme involved in H+ pumping. Arch. Biochem. Biophys. 253, 87 93.
54. Zöller I., Meixner M., Hartmann D., Büssow H., Meyer R., Gieselmann V. Eckhardt M. (2008) Absence of 2-hydroxylated sphingolipids is compatible with normal neural development but causes late-onset axon and myelin sheath degeneration. J. Neurosci. 28, 9741 9754.