Glycosphingolipid depletion in PC12 cells using iminosugars protects neuronal membranes from anti-ganglioside antibody mediated injury

Journal of Neuroimmunology

Volumn 203, Issue 1, 2008, Pages 33-38

  Townson, Kate H ^a   Speak, Anneliese O ^b   Greenshields, Kay N ^a   Goodyear, Carl S ^a   Willison, Hugh J ^a   Platt, Frances M ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Antibody; Ganglioside; Glucosylceramide synthase; Iminosugars; N butyldeoxynojirimycin; Neuropathy

Indexed keywords

CERAMIDE GLUCOSYLTRANSFERASE INHIBITOR; COMPLEMENT; GANGLIOSIDE; GANGLIOSIDE ANTIBODY; GLYCOSPHINGOLIPID; IMINOSUGAR; MEMBRANE ANTIGEN; MIGLUSTAT;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CELL ASSAY; CELL PROTECTION; COMPLEMENT SYSTEM; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; LIPOGENESIS; NERVE CELL LESION; NERVE CELL MEMBRANE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT;

1-DEOXYNOJIRIMYCIN; ANIMALS; ANTIBODIES; CELL MEMBRANE; COMPLEMENT SYSTEM PROTEINS; ENZYME INHIBITORS; GANGLIOSIDES; GLYCOSPHINGOLIPIDS; IMINO SUGARS; NEURITIS, AUTOIMMUNE, EXPERIMENTAL; NEURONS; NEUROPROTECTIVE AGENTS; PC12 CELLS; RATS;

EID: 52949129093     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.06.033     Document Type: Article

References (33)

1. Andersson U., Butters T.D., Dwek R.A., and Platt F.M. N-butyldeoxygalactonojirimycin: a more selective inhibitor of glycosphingolipid biosynthesis than N-butyldeoxynojirimycin, in vitro and in vivo. Biochem. Pharmacol. 59 (2000) 821-829
2. Andersson U., Smith D., Jeyakumar M., Butters T.D., Borja M.C., Dwek R.A., and Platt F.M. Improved outcome of N-butyldeoxygalactonojirimycin-mediated substrate reduction therapy in a mouse model of Sandhoff disease. Neurobiol. Dis. 16 (2004) 506-515
3. Bieberich E., Freischutz B., Suzuki M., and Yu R.K. Differential effects of glycolipid biosynthesis inhibitors on ceramide-induced cell death in neuroblastoma cells. J. Neurochem. 72 (1999) 1040-1049
4. Boffey J., Odaka M., Nicoll D., Wagner E.R., Townson K., Bowes T., Conner J., Furukawa K., and Willison H.J. Characterisation of the immunoglobulin variable region gene usage encoding the murine anti-ganglioside antibody repertoire. J. Neuroimmunol. 165 (2005) 92-103
5. Bullens R.W.M., O'Hanlon G.M., Wagner E., Molenaar P.C., Furukawa K., Furukawa K., Plomp J.J., and Willison H.J. Complex gangliosides at the neuromuscular junction are membrane receptors for autoantibodies and botulinum neurotoxin but redundant for normal synaptic function. J. Neurosci. 22 (2002) 6876-6884
6. Cox T., Lachmann R., Hollak C., Aerts J., van Weely S., Hrebicek M., Platt F., Butters T., Dwek R., Moyses C., Gow I., Elstein D., and Zimran A. Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. The Lancet 355 (2000) 1481-1485
7. Dijkhuis A.J., Klappe K., Kamps W., Sietsma H., and Kok J.W. Gangliosides do not affect ABC transporter function in human neuroblastoma cells. J. Lipid Res. 47 (2006) 1187-1195
8. Elliot-Smith E., Speak A.O., Lloyd-Evans E., Smith D.A., van der Spoel A.C., Jeyakumar M., Butters T.D., Dwek R.A., D'Azzo A., and Platt F.M. Beneficial effects of substrate reduction therapy in a mouse model of GM1 gangliosidosis. Mol. Genet. Metab. 94 (2008) 204-211
9. Fukumoto S., Mutoh T., Hasegawa T., Miyazaki H., Okada M., Goto G., Furukawa K., Urano T., and Furukawa K. GD3 synthase gene expression in PC12 cells results in the continuous activation of TrkA and ERK1/2 and enhanced proliferation. J. Biol. Chem. 275 (2000) 5832-5838
10. Goodfellow J.A., Bowes T., Sheikh K., Odaka M., Halstead S.K., Humphreys P.D., Wagner E.R., Yuki N., Furukawa K., Furukawa K., Plomp J.J., and Willison H.J. Overexpression of GD1a ganglioside sensitizes motor nerve terminals to anti-GD1a antibody-mediated injury in a model of acute motor axonal neuropathy. J. Neurosci. 25 (2005) 1620-1628
11. Guerrera M., and Ladisch S. N-Butyldeoxynojirimycin inhibits murine melanoma cell ganglioside metabolism and delays tumor onset. Cancer Lett. 201 (2003) 31-40
12. Heare T., Alp N.J., Priestman D.A., Kulkarni A.B., Qasba P., Butters T.D., Dwek R.A., Clarke K., Channon K.M., and Platt F.M. Severe endothelial dysfunction in the aorta of a mouse model of Fabry disease; partial prevention by N-butyldeoxynojirimycin treatment. J. Inherit. Metab. Dis. 30 (2007) 79-87
13. Hughes R.A., and Cornblath D.R. Guillain-Barre syndrome. The Lancet 366 (2005) 1653-1666
14. Jeyakumar M., Butters T.D., Cortina-Borja M., Hunnam V., Proia R.L., Perry V.H., Dwek R.A., and Platt F.M. Delayed symptom onset and increased life expectancy in Sandhoff disease mice treated with N-butyldeoxynojirimycin. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6388-6393
15. Lachmann R.H. Miglustat: substrate reduction therapy for glycosphingolipid lysosomal storage disorders. Drugs Today (Barc.). 42 (2006) 29-38
16. Lehmann H.C., Lopez P.H., Zhang G., Ngyuen T., Zhang J., Kieseier B.C., Mori S., and Sheikh K.A. Passive immunization with anti-ganglioside antibodies directly inhibits axon regeneration in an animal model. J. Neurosci. 27 (2007) 27-34
17. Liour S.S., and Yu R.K. Differential effects of three inhibitors of glycosphingolipid biosynthesis on neuronal differentiation of embryonal carcinoma stem cells. Neurochem. Res. 27 (2002) 1507-1512
18. Neville D.C., Coquard V., Priestman D.A., te Vruchte D.J., Sillence D.J., Dwek R.A., Platt F.M., and Butters T.D. Analysis of fluorescently labeled glycosphingolipid-derived oligosaccharides following ceramide glycanase digestion and anthranilic acid labeling. Anal. Biochem. 331 (2004) 275-282
19. Paterson G., Wilson G., Kennedy P.G.E., and Willison H.J. Analysis of anti-GM1 antibodies cloned from motor neuropathy patients demonstrates diverse variable region gene usage with extensive somatic mutation. J. Immunol. 155 (1995) 3049-3059
20. Patterson M.C., Vecchio D., Prady H., Abel L., and Wraith J.E. Miglustat for treatment of Niemann-Pick C disease: a randomised controlled study. Lancet Neurol. 6 (2007) 765-772
21. Platt F.M., and Butters T.D. Inhibition of substrate synthesis: a pharmacological approach for glycosphingolipid storage disease therapy. In: Platt F.M., and Walkley S.U. (Eds). Lysosomal disorders of the brain (2004), Oxford University Press, Oxford 381-408
22. Platt F.M., Neises G.R., Karlsson G.B., Dwek R.A., and Butters T.D. N-butyldeoxygalactonojirimycin inhibits glycolipid biosynthesis but does not affect N-linked oligosaccharide processing. J. Biol. Chem. 269 (1994) 27108-27114
23. 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. Prevention of lysosomal storage in Tay-Sachs mice treated with N-Butyldeoxynojirimycin. Science 276 (1997) 428-431
24. Platt F.M., Reinkensmeier G., Dwek R.A., and Butters T.D. Extensive glycosphingolipid depletion in the liver and lymphoid organs of mice treated with N-Butyldeoxynojirimycin. J. Biol. Chem. 272 (1997) 19365-19372
25. Platt F.M., Jeyakumar M., Andersson U., Dwek R.A., and Butters T.D. New developments in treating glycosphingolipid storage diseases. Adv. Exp. Med. Biol. 564 (2005) 117-126
26. Sonnino S., Mauri L., Chigorno V., and Prinetti A. Gangliosides as components of lipid membrane domains. Glycobiology 17 (2007) 1R-13R
27. Speak A.O., Salio M., Neville D.C., Fontaine J., Priestman D.A., Platt N., Heare T., Butters T.D., Dwek R.A., Trottein F., Exley M.A., Cerundolo V., and Platt F.M. Implications for invariant natural killer T cell ligands due to the restricted presence of isoglobotrihexosylceramide in mammals. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 5971-5976
28. Walton K.M., Sandberg K., Rogers T.B., and Schnaar R.L. Complex ganglioside expression and tetanus toxin binding by PC12 pheochromocytoma cells. J. Biol. Chem. 263 (1988) 2055-2063
29. Watabe K., Ida H., Uehara K., Oyanagi K., Sakamoto T., Tanaka J., Garver W.S., Miyawaki S., Ohno K., and Eto Y. Establishment and characterization of immortalized Schwann cells from murine model of Niemann-Pick disease type C (spm/spm). J. Peripher. Nerv. Syst. 6 (2001) 85-94
30. Willison H.J., and Yuki N. Peripheral neuropathies and anti-glycolipid antibodies. Brain 125 (2002) 2591-2625
31. Willison H.J., O'Hanlon G.M., Paterson G.J., Veitch J., Wilson G., Roberts M., Tang T., and Vincent A. A somatically mutated human anti-ganglioside antibody that induces experimental neuropathy in mice is encoded by the variable region heavy chain gene, V1-18. J. Clin. Invest. 97 (1996) 1155-1164
32. Zervas M., Somers K.L., Thrall M.A., and Walkley S.U. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11 (2001) 1283-1287
33. Zhang G., Lopez P.H.H., Li C.Y., Mehta N.R., Griffin J.W., Schnaar R.L., and Sheikh K.A. Anti-ganglioside antibody-mediated neuronal cytotoxicity and its protection by intravenous immunoglobulin: implications for immune neuropathies. Brain 127 (2004) 1085-1100