Protective Effect of Soybean-Derived Phosphatidylserine on the Trimethyltin-Induced Learning and Memory Deficits in Rats

  • An, Yong Ho (Acupuncture and Meridian Science Research Center, Kyung Hee University) ;
  • Park, Hyun Jung (Acupuncture and Meridian Science Research Center, Kyung Hee University) ;
  • Shim, Hyun Soo (College of Korean Medical Science Graduate School, Kyung Hee University) ;
  • Choe, Yun Seok (College of Korean Medical Science Graduate School, Kyung Hee University) ;
  • Han, Jeong Jun (Doosan Glonet BU, Doosan Corporation) ;
  • Kim, Jin Su (Molecular Imaging Research Center, Korea Institute of Radiological & Medical Sciences University of Science & Technology) ;
  • Lee, Hye Jung (Acupuncture and Meridian Science Research Center, Kyung Hee University) ;
  • Shim, Insop (Acupuncture and Meridian Science Research Center, Kyung Hee University)
  • Received : 2014.02.14
  • Accepted : 2014.04.14
  • Published : 2014.06.25

Abstract

The present study examined the effects of soybean-derived phosphatidylserine (SB-PS) on the learning and memory function and the neural activity in rats with trimethyltin (TMT)-induced memory deficits. The cognitive improving efficacy of SB-PS on the amnesic rats, which was induced by TMT, was investigated by assessing the Morris water maze test and by performing cholineacetyl transferase (ChAT), acetylcholinesterase (AChE) and cAMP responsive element binding protein (CREB) immunohistochemistry. A positron emission tomography (PET) scanning the rat brain was by performed administer 18F-Fluorodeoxy-glucose (18F-FDG). The rats with TMT injection showed impaired learning and memory of the tasks and treatment with SB-PS produced a significant improvement of the escape latency to find the platform in the Morris water maze at the 2nd day compared to that of the MCT group. In the retention test, the SB-PS group showed increased time spent around the platform compared to that of the MCT group. Consistent with the behavioral data, SB-PS 50 group significantly alleviated the loss of acetyl cholinergic neurons in the hippocampus compared to that of the MCT group. Treatment with SB-PS significantly increased the CREB positive neurons in the hippocampus as compared to that of the MCT group. In addition, SB-PS groups increased the glucose uptake in the hippocampus and SB-PS 50 group increased the glucose uptake in the frontal lobe, as compared to that of the MCT group. These results suggest that SB-PS may be useful for improving the cognitive function via regulation of cholinergic marker enzyme activity and neural activity.

Keywords

References

  1. Stuchbury, G., Mnch, G. Alzheimer's associated inflammation, potential drug targets and future therapies. J. Neural. Transm. 112(3):429-453, 2005. https://doi.org/10.1007/s00702-004-0188-x
  2. Cummings, J.L. Treatment of Alzheimer's disease current and future therapeutic approaches. Rev Neurol Dis. 1: 60-69, 2004.
  3. Nordberg, A., Nyberg, P., Adolfsson, R., Winblad, B. Cholinergic topography in Alzheimer brains a comparison with changes in the monoaminergic profile. J. Neural. Transm. 69: 19-32, 1987. https://doi.org/10.1007/BF01244094
  4. Nordberg, A., Winblad, B. Reduced number of [3H]nicotine and [3H]acetylcholine binding sites in the frontal cortex of Alzheimer brains. Neurosci. Lett. 72: 115-119, 1986. https://doi.org/10.1016/0304-3940(86)90629-4
  5. Wheeler, K.P., Whittam, R. ATPase activity of the sodium pump needs phosphatidylserine. Nature 225: 449-450, 1970. https://doi.org/10.1038/225449a0
  6. Delwaide, P.J., Gyselynck-Mambourg, A.M., Hurlet A., Ylieff, M. Double-blind randomized controlled study of phosphatidylserine in senile demented patients. Acta. Neurol. Scand. 73(2):136-140, 1986. https://doi.org/10.1111/j.1600-0447.1986.tb10550.x
  7. Prusiner, S.B. Molecular biology of prion disease. Science 252(5012):1515-1522, 1991. https://doi.org/10.1126/science.1675487
  8. Kudo, S. Biosurfactants as food additives. Proceedings of the World Conference on Biotechnology for the Fats and Oils Industry. American Oil Chemist's Society. pp 195-201, Hamburg, 1987.
  9. Blokland, A., Hogig, W., Brouns, F., Jolles, J. Cognition-enhancing properties of subchronic phsophatidylserine (PS) treatment in middle-aged rats comparison of bovine cortex PS with egg PS and soybean PS. Nutrition, 15(10):778-783, 1999. https://doi.org/10.1016/S0899-9007(99)00157-4
  10. Jorissen, B.l., Brouns, F., Van Boxtel, M.P., Ponds, R.W., Verhey, F.R., Jolles, J., Riedel, W.J. The influence of soy-derived phosphatdiylserine on cognition in age-associated memory impairment. Nutr. Neurosci. 4(2):121-134, 2001. https://doi.org/10.1080/1028415X.2001.11747356
  11. Sakai, M., Yamatoya, H., Kudo, S. Pharmacological effects of phosphatidylserine enzymatically synthesized from soybean lecithin on brain functions in rodents. J. Nutr. Sci. Vitaminol. 42(1):47-54, 1996. https://doi.org/10.3177/jnsv.42.47
  12. Cannon, R.L., Hoover, D.B., Baisden, R.H., Woodruff, M.L. Effects of trimethyltin (TMT) on choline acetyltransferase activity in the rat hippocampus. Influence of dose and time following exposure. Mol. Chem. Neuropathol. 23(1):27-45, 1994. https://doi.org/10.1007/BF02858505
  13. Cannon, R.L., Hoover, D.B., Baisden, R.H., Woodruff, M.L. The effect of time following exposure to trimethyltin (TMT) on cholinergic muscarinic receptor binding in rat hippocampus. Mol. Chem. Neuropathol. 23(1):47-62, 1994. https://doi.org/10.1007/BF02858506
  14. O'connell, A., Earley, B., Leonard, B.E. The neuroprotective effect of tacrine on trimethyltin induced memory and muscarinic receptor dysfunction in the rat. Neurochem. Int. 25(6):555-566, 1994. https://doi.org/10.1016/0197-0186(94)90154-6
  15. Brabeck, C., Michetti, F., Geloso, M.C., Corvino, V., Goezalan, F., Meyermann, R., Chluesener, H.J. Expression of EMAP-II by activated monocytes/microglia cells in different regions of the rat hippocampus after trimethyltin-induced brain damage. Exp. Neurol. 177(1):341-346, 2002. https://doi.org/10.1006/exnr.2002.7985
  16. Dyer, R.S. Physiological methods for assessment of Trimethyltin exposure. Neurobehav. Toxicol. Teratol. 4(6):659-664, 1982.
  17. Balaban, C.D., O'Callaghan J.P., Billingsley, M.L. Trimethyltin-induced neuronal damage in the rat brain comparative studies using silver degeneration stains, immunocytochemistry and immunoassay for neurotypic and gliotypic proteins. Neuroscience 26(1):337-361, 1988. https://doi.org/10.1016/0306-4522(88)90150-9
  18. Brown, A.W., Aldrige, W.N., Street, B.W. and Verchoyle, R.D. The behavioral and neuropathologic sequelae of intoxication by trimethyltin compounds in the rat. Am. J. Pathol. 97(1):59-82, 1979.
  19. Swartzwelder, H.S., Dyer, R.S., Holahan, W., Myers, R.D. Activity changes in rats following acute trimethyltin exposure. Neurotoxicology 2(3):589-593, 1981.
  20. Woodruff, M.L., Baisden, R.H., Cannon, R.L., Kalbfleisch, J., Freeman, J.N. 3rd. Effects of trimethyltin on acquisition and reversal of a light-dark discrimination by rats. Physiol Behav. 55(6):1055-1061, 1994. https://doi.org/10.1016/0031-9384(94)90387-5
  21. Walsh, T.J., Gallagher, M., Bostock, E., Dyer, R.S. Trimethyltin impairs retention of a passive avoidance task. Neurobahav. Toxicol. Teratol. 4(2):163-167, 1982.
  22. Walsh, T.J., Miller, D.B., Dyer, R.S. Trimethyltin, a selective limbic system neurotoxicant, impairs radical-arm maze performance. Neurobahav. Toxicol. Teratol. 4(2):177-183, 1982.
  23. Earley, B., Burke, M., Leonard, B.E., Gouret, C.J., Junien, J.L. A comparison of the psychopharmacological profiles of phencyclidine, ketamine and (+)SKF 10,047 in the trimethyltin rat model. Neuropharmacology 29(8):695-703, 1990. https://doi.org/10.1016/0028-3908(90)90121-7
  24. Zhao, T.F., Xu, C.X., Li, Z.W., Xie, F., Zhao, Y.T., Wang, S. Q., Luo, C.H., Lu, R.S., Ni, G.L., Ku, Z.Q., Ni, Y.F., Qian, Q., Chen, X.Q. Effect of Tremella fuciformis Berk on acute radiation sickness in dogs. Zhongguo. Yi. Xue. Ke. Xue. Yuan. Xue. Bao. 4(1):20-23, 1982.
  25. Hooge, R., De deyn, P.P. Applications of the Morris water maze in the study of learning and memory. Brain. Res. Rev. 36(1):60-90, 2001. https://doi.org/10.1016/S0165-0173(01)00067-4
  26. Paxinos, G., Watson, C., Pennisi, M., Topple, A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J. Neurosci. Methods 13(2):139-143, 1985. https://doi.org/10.1016/0165-0270(85)90026-3
  27. Fueger, B.J., Czernin, J., Hildebrandt, I., Tran, C., Halpern, B.S., Stout, D., Phelps, M.E., Weber, W.A. Impact of animal handling on the results of 18F-FDG PET studies in mice. J. Nucl. Med. 47(6):999-1006, 2006.
  28. Bao, Q., Newport, D., Chen, M., Stout, D.B., Chatziioannou, A.F. Performance evaluation of the inveon dedicated PET preclinical tomograph based on the NEMA NU-4 standards. J. Nucl. Med. 50(3):401-408, 2009. https://doi.org/10.2967/jnumed.108.056374
  29. Yu, A.R., Kim, J.S., Kim, K.M., Lee, Y.S., Kim, J.G., Woo, S.K., Park, J.A., Kim, H.J., Cheon G.J. Performance Measurement of Siemens Inveon PET Scanner for Small Animal Imaging. Korean J Med Phys. 21: 145-152, 2010.
  30. Kim, J.S., Lee, J.S., Park, M.H., Kang, H., Lee, J.J., Lee, H.J., Im, K.C., Moon, D.H., Lim, S.M., Oh, S.H., Lee, D.S. Assessment of Cerebral Glucose Metabolism in Cat Deafness Model: Strategies for Improving the Voxel-Based Statistical Analysis for Animal PET Studies. Mol. Imaging Biol. 10(3):154-161, 2008. https://doi.org/10.1007/s11307-008-0140-9
  31. Koczyk, D., Skup, M., Zaremba, M., Oderfeld, N.B. Trimethyltin-induced plastic neuronal changes in rat hippocampus are accompanied by astrocytic trophic activity. Acta. Neurobiol. Exp. 56(1):237-241, 1996.
  32. Asano, T., Kato-Kataoka, A., Sakai, M., Tsuji, A., Ebina, R., Nonaka, C., Takamizawa, K. The effect of soybean derived phosphatidylserine on the cognitive function of the elderly. Jpn J. Nutr. Ass. 24(2):165-170, 2005.
  33. Sun, H., Hu, Y., Zhang, J.M., Li S.Y., He W. Effects of one Chinese herbs on improving cognitive function and memory of Alzheimer's disease mouse models. Zhongguo. Zhong. Yao. Za. Zhi. 28(8):751-754, 2003.
  34. Hardinghan, G.E., Bading, H. The Yin and Yang of NMDA receptor signaling. Trends Neurosci. 26(2):81-89, 2003. https://doi.org/10.1016/S0166-2236(02)00040-1
  35. Lonze, B.E., Ginty, D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron. 35(4):371-385, 2002. https://doi.org/10.1016/S0896-6273(02)00742-0
  36. Kim, J.H., Ha, H.C., Lee, M.S., Kang, J.I., Kim, H.S., Lee, S.Y., Pyun, K.H., Shim, I. Effect of Tremella fuciformis on the neurite outgrowth of PC12h cells and the improvement of memory in rats. Biol. Pharm. Bull. 30(4):708-714, 2007. https://doi.org/10.1248/bpb.30.708
  37. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., Silva, A. J. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79(1):59-68, 1994. https://doi.org/10.1016/0092-8674(94)90400-6
  38. Jackson, T., Ramaswami, M. Prospects of memorymodifying drugs that target the CREB pathway. Curr. Opin. Discov. Devel. 6(5):712-719, 2003.
  39. Mirrione, M.M., Schiffer, W.K., Siddiq, M., Dewey, S.L., Tsirka, S.E. PET imaging of glucose metabolism in a mouse model of temporal lobe epilepsy. Synapse. 59(2):119-121, 2006. https://doi.org/10.1002/syn.20216