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Neural Plasticity
Volume 2014, Article ID 196812, 11 pages
http://dx.doi.org/10.1155/2014/196812
Research Article

Blockade of Lysosomal Acid Ceramidase Induces GluN2B-Dependent Tau Phosphorylation in Rat Hippocampal Slices

Département de biologie médicale, Université du Québec à Trois-Rivières, Trois-Rivières, QC, Canada G9A 5H7

Received 15 April 2014; Revised 24 July 2014; Accepted 8 August 2014; Published 8 September 2014

Academic Editor: Zygmunt Galdzicki

Copyright © 2014 Marie-Elaine Laurier-Laurin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Bartke and Y. A. Hannun, “Bioactive sphingolipids: metabolism and function,” Journal of Lipid Research, vol. 50, supplement, pp. S91–S96, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Costantini, R. Weindruch, G. Della Valle, and L. Puglielli, “A TrkA-to-p75NTR molecular switch activates amyloid β-peptide generation during aging,” The Biochemical Journal, vol. 391, no. 1, pp. 59–67, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. R. G. Cutler, J. Kelly, K. Storie et al., “Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 7, pp. 2070–2075, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. R. N. Kolesnick and M. Krönke, “Regulation of ceramide production and apoptosis,” Annual Review of Physiology, vol. 60, pp. 643–645, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Mencarelli and P. Martinez-Martinez, “Ceramide function in the brain: when a slight tilt is enough,” Cellular and Molecular Life Sciences, vol. 70, no. 2, pp. 181–203, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. L. Puglielli, B. C. Ellis, A. J. Saunders, and D. M. Kovacs, “Ceramide stabilizes β-site amyloid precursor protein-cleaving enzyme 1 and promotes amyloid β-peptide biogenesis,” The Journal of Biological Chemistry, vol. 278, no. 22, pp. 19777–19783, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Patil, J. Melrose, and C. Chan, “Involvement of astroglial ceramide in palmitic acid-induced Alzheimer-like changes in primary neurons,” European Journal of Neuroscience, vol. 26, no. 8, pp. 2131–2141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Burek, J. Roth, H.-G. Koch, K. Harzer, M. Los, and K. Schulze-Osthoff, “The role of ceramide in receptor- and stress-induced apoptosis studied in acidic ceramidase-deficient farber disease cells,” Oncogene, vol. 20, no. 45, pp. 6493–6502, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. M. S. Sands, “Farber disease: understanding a fatal childhood disorder and dissecting ceramide biology,” EMBO Molecular Medicine, vol. 5, no. 6, pp. 799–801, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. C. E. Gallegos, M. F. Pediconi, and F. J. Barrantes, “Ceramides modulate cell-surface acetylcholine receptor levels,” Biochimica et Biophysica Acta, vol. 1778, no. 4, pp. 917–930, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Tabatadze, A. Savonenko, H. Song, V. V. R. Bandaru, M. Chu, and N. J. Haughey, “Inhibition of neutral sphingomyelinase-2 perturbs brain sphingolipid balance and spatial memory in mice,” Journal of Neuroscience Research, vol. 88, no. 13, pp. 2940–2951, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Wheeler, E. Knapp, V. V. R. Bandaru et al., “Tumor necrosis factor-α-induced neutral sphingomyelinase-2 modulates synaptic plasticity by controlling the membrane insertion of NMDA receptors,” Journal of Neurochemistry, vol. 109, no. 5, pp. 1237–1249, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Zhou and M. Baudry, “Developmental changes in NMDA neurotoxicity reflect developmental changes in subunit composition of NMDA receptors,” Journal of Neuroscience, vol. 26, no. 11, pp. 2956–2963, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Allyson, E. Dontigny, Y. Auberson, M. Cyr, and G. Massicotte, “Blockade of NR2A-containing NMDA receptors induces tau phosphorylation in rat hippocampal slices,” Neural Plasticity, vol. 2010, Article ID 340168, 10 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Raisova, G. Goltz, M. Bektas et al., “Bcl-2 overexpression prevents apoptosis induced by ceramidase inhibitors in malignant melanoma and HaCaT keratinocytes,” FEBS Letters, vol. 516, no. 1–3, pp. 47–52, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Muller, M. Joly, and G. Lynch, “Contributions of quisqualate and NMDA receptors to the induction and expression of LTP,” Science, vol. 242, no. 4886, pp. 1694–1697, 1988. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Buée, T. Bussière, V. Buée-Scherrer, A. Delacourte, and P. R. Hof, “Tau protein isoforms, phosphorylation and role in neurodegenerative disorders,” Brain Research Reviews, vol. 33, no. 1, pp. 95–130, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. C.-A. Maurage, N. Sergeant, M.-M. Ruchoux, J.-J. Hauw, and A. Delacourte, “Phosphorylated serine 199 of microtubule-associated protein tau is a neuronal epitope abundantly expressed in youth and an early marker of tau pathology,” Acta Neuropathologica, vol. 105, no. 2, pp. 89–97, 2003. View at Google Scholar · View at Scopus
  19. J. Avila, J. J. Lucas, M. Pérez, and F. Hernández, “Role of tau protein in both physiological and pathological conditions,” Physiological Reviews, vol. 84, no. 2, pp. 361–384, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. De Montigny, I. Elhiri, J. Allyson, M. Cyr, and G. Massicotte, “NMDA reduces tau phosphorylation in rat hippocampal slices by targeting NR2A receptors, GSK3β, and PKC activities,” Neural Plasticity, vol. 2013, Article ID 261593, 10 pages, 2013. View at Publisher · View at Google Scholar
  21. P. P. Ruvolo, “Ceramide regulates cellular homeostasis via diverse stress signaling pathways,” Leukemia, vol. 15, no. 8, pp. 1153–1160, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. S. A. F. Morad and M. C. Cabot, “Ceramide-orchestrated signalling in cancer cells,” Nature Reviews Cancer, vol. 13, no. 1, pp. 51–65, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Qin, E. Berdyshev, J. Goya, V. Natarajan, and G. Dawson, “Neurons and oligodendrocytes recycle sphingosine 1-phosphate to ceramide: significance for apoptosis and multiple sclerosis,” The Journal of Biological Chemistry, vol. 285, no. 19, pp. 14134–14143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Levade, H. W. Moser, A. H. Fensom, K. Harzer, A. B. Moser, and R. Salvayre, “Neurodegenerative course in-ceramidase deficiency (Farber disease) correlates with the residual lysosomal ceramide turnover in cultured living patient cells,” Journal of the Neurological Sciences, vol. 134, no. 1-2, pp. 108–114, 1995. View at Publisher · View at Google Scholar · View at Scopus
  25. A. B. A. Shakor, K. Kwiatkowska, and A. Sobota, “Cell surface ceramide generation precedes and controls FcγRII clustering and phosphorylation in rafts,” The Journal of Biological Chemistry, vol. 279, no. 35, pp. 36778–36787, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Grassmé, V. Jendrossek, J. Bock, A. Riehle, and E. Gulbins, “Ceramide-rich membrane rafts mediate CD40 clustering,” Journal of Immunology, vol. 168, no. 1, pp. 298–307, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. S. J. Suchard, V. Hinkovska-Galcheva, P. J. Mansfield, L. A. Boxer, and J. A. Shayman, “Ceramide inhibits IgG-dependent phagocytosis in human polymorphonuclear leukocytes,” Blood, vol. 89, no. 6, pp. 2139–2147, 1997. View at Google Scholar · View at Scopus
  28. C. J. Baier and F. J. Barrantes, “Sphingolipids are necessary for nicotinic acetylcholine receptor export in the early secretory pathway,” Journal of Neurochemistry, vol. 101, no. 4, pp. 1072–1084, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. F. J. Barrantes, “Cholesterol effects on nicotinic acetylcholine receptor,” Journal of Neurochemistry, vol. 103, supplement 1, pp. 72–80, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Dontigny, C. Patenaude, M. Cyr, and G. Massicotte, “Sphingomyelinase selectively reduces M1 muscarinic receptors in rat hippocampal membranes,” Hippocampus, vol. 22, no. 7, pp. 1589–1596, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. B.-S. Chen and K. W. Roche, “Regulation of NMDA receptors by phosphorylation,” Neuropharmacology, vol. 53, no. 3, pp. 362–368, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. H. H. Cheung, L. Teves, M. C. Wallace, and J. W. Gurd, “Increased phosphorylation of the NR1 subunit of the NMDA receptor following cerebral ischemia,” Journal of Neurochemistry, vol. 78, no. 5, pp. 1179–1182, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. C. G. Lau and R. S. Zukin, “NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders,” Nature Reviews Neuroscience, vol. 8, no. 6, pp. 413–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Gulbins, I. Szabo, K. Baltzer, and F. Lang, “Ceramide-induced inhibition of T lymphocyte voltage-gated potassium channel is mediated by tyrosine kinases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 14, pp. 7661–7666, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Abe, S. Matsumura, T. Katano et al., “Fyn kinase-mediated phosphorylation of NMDA receptor NR2B subunit at Tyr1472 is essential for maintenance of neuropathic pain,” The European Journal of Neuroscience, vol. 22, no. 6, pp. 1445–1454, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. S. P. Braithwaite, M. Adkisson, J. Leung et al., “Regulation of NMDA receptor trafficking and function by striatal-enriched tyrosine phosphatase (STEP),” European Journal of Neuroscience, vol. 23, no. 11, pp. 2847–2856, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. K. A. Pelkey, R. Askalan, S. Paul et al., “Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation,” Neuron, vol. 34, no. 1, pp. 127–138, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. R. C. Dickson, “Thematic review series: sphingolipids. New insights into sphingolipid metabolism and function in budding yeast,” Journal of Lipid Research, vol. 49, no. 5, pp. 909–921, 2008. View at Google Scholar
  39. G. F. Nixon, “Sphingolipids in inflammation: pathological implications and potential therapeutic targets,” British Journal of Pharmacology, vol. 158, no. 4, pp. 982–993, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Maalouf and J. M. Rho, “Oxidative impairment of hippocampal long-term potentiation involves activation of protein phosphatase 2A and is prevented by ketone bodies,” Journal of Neuroscience Research, vol. 86, no. 15, pp. 3322–3330, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Allyson, X. Bi, M. Baudry, and G. Massicotte, “Maintenance of synaptic stability requires calcium-independent phospholipase A 2 activity,” Neural Plasticity, vol. 2012, Article ID 569149, 13 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. N. J. Haughey, R. G. Cutler, A. Tamara et al., “Perturbation of sphingolipid metabolism and ceramide production in HIV-dementia,” Annals of Neurology, vol. 55, no. 2, pp. 257–267, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. M. M. Mielke, V. V. R. Bandaru, N. J. Haughey et al., “Serum ceramides increase the risk of Alzheimer disease: the women's health and aging study II,” Neurology, vol. 79, no. 7, pp. 633–641, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. W.-Y. Ong, K. Tanaka, G. S. Dawe, L. M. Ittner, and A. A. Farooqui, “Slow excitotoxicity in Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 35, no. 4, pp. 643–668, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Martin, X. Latypova, C. M. Wilson et al., “Tau protein kinases: involvement in Alzheimer's disease,” Ageing Research Reviews, vol. 12, no. 1, pp. 289–309, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Arboleda, L. C. Morales, B. Benítez, and H. Arboleda, “Regulation of ceramide-induced neuronal death: cell metabolism meets neurodegeneration,” Brain Research Reviews, vol. 59, no. 2, pp. 333–346, 2009. View at Publisher · View at Google Scholar · View at Scopus