Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Administration of Phytoceramide Enhances Memory and Up-regulates the Expression of pCREB and BDNF in Hippocampus of Mice

  • Lee, Yeonju (Department of Neuroscience and Tissue Injury Defense Research Center, School of Medicine, Ewha Womans University) ;
  • Kim, Jieun (Department of Neuroscience and Tissue Injury Defense Research Center, School of Medicine, Ewha Womans University) ;
  • Jang, Soyong (Department of Neuroscience and Tissue Injury Defense Research Center, School of Medicine, Ewha Womans University) ;
  • Oh, Seikwan (Department of Neuroscience and Tissue Injury Defense Research Center, School of Medicine, Ewha Womans University)
  • Received : 2013.01.03
  • Accepted : 2013.03.27
  • Published : 2013.05.31
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Abstract

This study was aimed at investigating the possible effects of phytoceramide (Pcer) on learning and memory and their underlying mechanisms. Phytoceramide was orally administered to ICR mice for 7 days. Memory performances were assessed using the passive avoidance test and Y-maze task. The expressions of phosphorylated cAMP response element binding protein (pCREB), brain-derived neurotrophic factor (BDNF) were measured with immunoblot. The incorporation of 5-bromo-2-deoxyuridine (BrdU) in hippocampal regions was investigated by using immunohistochemical methods. Treatment of Pcer enhanced cognitive performances in the passive avoidance test and Y-maze task. Immunoblotting studies revealed that the phosphorylated CREB and BDNF were significantly increased on hippocampus in the Pcer-treated mice. Immunohistochemical studies showed that the number of immunopositive cells to BrdU was significantly increased in the hippocampal dentate gyrus regions after Pcer-treatment for 7 days. These results suggest that Pcer contribute to enhancing memory and BDNF expression and it could be secondary to the elevation of neurogenesis.

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References

  1. Ambrogi Lorenzini, C. G., Baldi, E., Bucherelli, C., Sacchetti, B. and Tassoni, G. (1997) Role of ventral hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response memory trace. Brain Res. 768, 242-248. https://doi.org/10.1016/S0006-8993(97)00651-3
  2. Bartus, R. T., Dean, R. L., Beer, B. and Lippa, A. S. (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-414. https://doi.org/10.1126/science.7046051
  3. Bozon, B., Kelly, A., Josselyn, S. A., Silva, A. J., Davis, S., Laroche, S., Bozon, B., Kelly, Á., Josselyn, S. A. and Silva, A. J. (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philol. Trans. R. Soc. Lond. B. Biol. Sci. 358, 805-814. https://doi.org/10.1098/rstb.2002.1224
  4. Cameron, H. A. and McKay, R. D. (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435, 406-417. https://doi.org/10.1002/cne.1040
  5. Christie, B. R. and Cameron, H. A. (2006) Neurogenesis in the adult hippocampus. Hippocampus 16, 199-207. https://doi.org/10.1002/hipo.20151
  6. Duman, R. S. and Monteggia, L. M. (2006) A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116-1127. https://doi.org/10.1016/j.biopsych.2006.02.013
  7. Dupret, D., Revest, J. M., Koehl, M., Ichas, F., De Giorgi, F., Costet, P., Abrous, D. N. and Piazza, P. V. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PloS one 3, e1959. https://doi.org/10.1371/journal.pone.0001959
  8. Durand, G. M., Kovalchuk, Y. and Konnerth, A. (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381, 71-75. https://doi.org/10.1038/381071a0
  9. Ennaceur, A. and Meliani, K. (1992) Effects of physostigmine and scopolamine on rats' performances in object-recognition and radialmaze tests. Psychopharmacology 109, 321-330. https://doi.org/10.1007/BF02245880
  10. Eriksson, P. S., Perfi lieva, E., Björk-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A. and Gage, F. H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. https://doi.org/10.1038/3305
  11. Gage, F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438. https://doi.org/10.1126/science.287.5457.1433
  12. Garcia, J., Shea, J., Alvarez-Vasquez, F., Qureshi, A., Luberto, C., Voit, E. O. and Del Poeta, M. (2008) Mathematical modeling of pathogenicity of Cryptococcus neoformans. Mol. Syst. Biol. 4. 183.
  13. Goldberg, J. L. and Barres, B. A. (2000) The relationship between neuronal survival and regeneration. Annu. Rev. Neurosci. 23, 579-612. https://doi.org/10.1146/annurev.neuro.23.1.579
  14. Gould, E., Beylin, A., Tanapat, P., Reeves, A. and Shors, T. J. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265. https://doi.org/10.1038/6365
  15. Gruest, N., Richer, P. and Hars, B. (2004) Memory consolidation and reconsolidation in the rat pup require protein synthesis. J. Neurosci. 24, 10488-10492. https://doi.org/10.1523/JNEUROSCI.2984-04.2004
  16. Hait, N. C., Oskeritzian, C. A., Paugh, S. W., Milstien, S. and Spiegel, S. (2006) Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim. Biophys. Acta 1758, 2016-2026. https://doi.org/10.1016/j.bbamem.2006.08.007
  17. Hannun, Y. A. and Obeid, L. M. (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150. https://doi.org/10.1038/nrm2329
  18. Jung, J.-C., Lee, Y., Moon, S., Ryu, J. H. and Oh, S. (2011) Phytoceramide shows neuroprotection and ameliorates scopolamineinduced memory impairment. Molecules 16, 9090-9100. https://doi.org/10.3390/molecules16119090
  19. Liao, L., Pilotte, J., Xu, T., Wong, C. C. L., Edelman, G. M., Vanderklish, P. and Yates III, J. R. (2007) BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: an analysis using high-throughput proteomics. J. Proteome Res. 6, 1059-1071. https://doi.org/10.1021/pr060358f
  20. Mao, C., Xu, R., Szulc, Z. M., Bielawska, A., Galadari, S. H. and Obeid, L. M. (2001) Cloning and characterization of a novel human alkaline ceramidase. A mamalian enzyme that hydrolyzes phytoceramide. J. Biol. Chem. 276, 26577-26588. https://doi.org/10.1074/jbc.M102818200
  21. Memberg, S. P. and Hall, A. K. (1995) Proliferation, differentiation, and survival of rat sensory neuron precursors in vitro require specifi c trophic factors. Mol. Cell. Neurosci. 6, 323-335. https://doi.org/10.1006/mcne.1995.1025
  22. Nakagawa, S., Kim, J. E., Lee, R., Malberg, J. E., Chen, J., Steffen, C., Zhang, Y. J., Nestler, E. J. and Duman, R. S. (2002) Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J. Neurosci. 22, 3673-3682.
  23. O'Connell, C., Gallagher, H. C., O'Malley, A., Bourke, M. and Regan, C. M. (2000) CREB phosphorylation coincides with transient synapse formation in the rat hippocampal dentate gyrus following avoidance learning. Neural Plast. 7, 279-289. https://doi.org/10.1155/NP.2000.279
  24. Palmer, T. D., Takahashi, J. and Gage, F. H. (1997) The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci. 8, 389-404. https://doi.org/10.1006/mcne.1996.0595
  25. Patschan, S., Chen, J., Polotskaia, A., Mendelev, N., Cheng, J., Patschan, D. and Goligorsky, M. S. (2008) Lipid mediators of autophagy in stress-induced premature senescence of endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 294, H1119-H1129.
  26. Pittenger, C., Huang, Y. Y., Paletzki, R. F., Bourtchouladze, R., Scanlin, H., Vronskaya, S. and Kandel, E. R. (2002) Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34, 447-462. https://doi.org/10.1016/S0896-6273(02)00684-0
  27. Posse de Chaves, E. I. (2006) Sphingolipids in apoptosis, survival and regeneration in the nervous system. Biochim. Biophys. Acta 1758, 1995-2015. https://doi.org/10.1016/j.bbamem.2006.09.018
  28. Renner, U. D., Oertel, R. and Kirch, W. (2005) Pharmacokinetics and pharmacodynamics in clinical use of scopolamine. Ther. Drug Monit. 27, 655-665. https://doi.org/10.1097/01.ftd.0000168293.48226.57
  29. Sarter, M., Bodewitz, G. and Stephens, D. N. (1988) Attenuation of scopolamine-induced impairment of spontaneous alternation behaviour by antagonist but not inverse agonist and agonist $\beta$-carbolines. Psychopharmacology 94, 491-495. https://doi.org/10.1007/BF00212843
  30. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. and Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376. https://doi.org/10.1038/35066584
  31. Takahashi, J., Palmer, T. D. and Gage, F. H. (1999) Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J. Neurobiol. 38, 65-81. https://doi.org/10.1002/(SICI)1097-4695(199901)38:1<65::AID-NEU5>3.0.CO;2-Q
  32. Taupin, P. (2005) Adult neurogenesis in the mammalian central nervous system: functionality and potential clinical interest. Med. Sci. Monit. 11, RA247-252.
  33. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D. and Gage, F. H. (2002) Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. https://doi.org/10.1038/4151030a
  34. Walton, M., Woodgate, A. M., Muravlev, A., Xu, R., During, M. J. and Dragunow, M. (1999) CREB phosphorylation promotes nerve cell survival. J. Neurochem. 73, 1836-1842.
  35. Weiss, S., Reynolds, B. A., Vescovi, A. L., Morshead, C., Craig, C. G. and der Kooy, D. (1996) Is there a neural stem cell in the mammalian forebrain? Trends Neurosci. 19, 387-393. https://doi.org/10.1016/S0166-2236(96)10035-7
  36. Zhao, C., Deng, W. and Gage, F. H. (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660. https://doi.org/10.1016/j.cell.2008.01.033

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