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Evidence-Based Complementary and Alternative Medicine
Volume 2013 (2013), Article ID 518421, 12 pages
http://dx.doi.org/10.1155/2013/518421
Research Article

The effect of PN-1, a Traditional Chinese Prescription, on the Learning and Memory in a Transgenic Mouse Model of Alzheimer’s Disease

Comparative Medical Center, Institute of Laboratory Animal Science, Peking Union Medical College (PUMC), Chinese Academy of Medical Science (CAMS), Beijing 100021, China

Received 14 October 2012; Revised 13 January 2013; Accepted 15 January 2013

Academic Editor: Wei Jia

Copyright © 2013 Zhi-Gang Yao 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. M. A. Henson, A. C. Roberts, K. Salimi et al., “Developmental regulation of the NMDA receptor subunits, NR3A and NR1, in human prefrontal cortex,” Cerebral Cortex, vol. 18, no. 11, pp. 2560–2573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. S. Ho, K. F. So, and R. C. Chang, “Drug discovery from Chinese medicine against neurodegeneration in Alzheimer's and vascular dementia,” Chinese Medicine, vol. 6, article 15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. Z. Lin, J. Gu, J. Xiu, T. Mi, J. Dong, and J. K. Tiwari, “Traditional Chinese medicine for senile dementia,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 692621, 13 pages, 2012. View at Publisher · View at Google Scholar
  4. H. Yan, L. Li, and X. C. Tang, “Treating senile dementia with traditional Chinese medicine,” Clinical Interventions in Aging, vol. 2, no. 2, pp. 201–208, 2007. View at Scopus
  5. B. Flaws and P. Sionneau, The Treatment of Modern Western Medical Diseases with Chinese Medicine: A Textbook & Clinical Manual, Blue Poppy Press, Boulder, Colo, USA, 2001.
  6. D. A. Evans, H. H. Funkenstein, M. S. Albert et al., “Prevalence of Alzheimer's disease in a community population of older persons. Higher than previously reported,” Journal of the American Medical Association, vol. 262, no. 18, pp. 2551–2556, 1989. View at Scopus
  7. A. M. A. Brands, G. J. Biessels, E. H. F. De Haan, L. J. Kappelle, and R. P. C. Kessels, “The effects of type 1 diabetes on cognitive performance: a meta-analysis,” Diabetes Care, vol. 28, no. 3, pp. 726–735, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. D. J. Selkoe, “Alzheimer's disease: genes, proteins, and therapy,” Physiological Reviews, vol. 81, no. 2, pp. 741–766, 2001. View at Scopus
  9. L. F. Lue, Y. M. Kuo, A. E. Roher et al., “Soluble amyloid β peptide concentration as a predictor of synaptic change in Alzheimer's disease,” American Journal of Pathology, vol. 155, no. 3, pp. 853–862, 1999. View at Scopus
  10. S. Li, M. Jin, T. Koeglsperger, N. E. Shepardson, G. M. Shankar, and D. J. Selkoe, “Soluble a β oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors,” Journal of Neuroscience, vol. 31, no. 18, pp. 6627–6638, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Kamenetz, T. Tomita, H. Hsieh et al., “APP processing and synaptic function,” Neuron, vol. 37, no. 6, pp. 925–937, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. G. M. Shankar and D. M. Walsh, “Alzheimer's disease: synaptic dysfunction and Aβ,” Molecular Neurodegeneration, vol. 4, no. 1, article 48, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. B. J. Cummings and C. W. Cotman, “Image analysis of β-amyloid load in Alzheimer's disease and relation to dementia severity,” Lancet, vol. 346, no. 8989, pp. 1524–1528, 1995. View at Scopus
  14. G. Blessed, B. E. Tomlinson, and M. Roth, “The association between quantitative measures of dementia and of senile change in the cerebral grey matter of elderly subjects,” British Journal of Psychiatry, vol. 114, no. 512, pp. 797–811, 1968. View at Scopus
  15. H. Okano, T. Hirano, and E. Balaban, “Learning and memory,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 23, pp. 12403–12404, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. S. M. Yuan, K. Gao, D. M. Wang et al., “Evodiamine improves congnitive abilities in SAMP8 and APP swe/PS1ΔE9 transgenic mouse models of Alzheimer's disease,” Acta Pharmacologica Sinica, vol. 32, no. 3, pp. 295–302, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. X. Wang, P. Liu, H. Zhu et al., “miR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation,” Brain Research Bulletin, vol. 80, no. 4-5, pp. 268–273, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. State Pharmacopoeia Commission of PRC, Pharmacopoeia of the People’s Republic of China, Beijing, China, 2010.
  19. World Health Organization, Quality Control Methods for Medicinal Plant Materials, Geneva, Switzerland, 1998.
  20. Z. W. Tan, H. Y. Hu, and X. Chen, “Effect of qingxin kaiqiao recipe saponin on the expressions of Bax, Bcl-2, Abeta, and betaAPP in the cortex and hippocampus of Alzheimer's disease rats,” Zhongguo Zhong Xi Yi Jie He Za Zhi, vol. 32, no. 9, pp. 1258–1263, 2012.
  21. L. Gao, Q. Tang, X. He, and M. Bi, “Effect of icariin on learning and memory abilities and activity of cholinergic system of senescence-accelerated mice SAMP10,” Zhongguo Zhong Yao Za Zhi, vol. 37, no. 14, pp. 2117–2121, 2012.
  22. J. M. Maler, H. Esselmann, J. Wiltfang et al., “Memantine inhibits ethanol-induced NMDA receptor up-regulation in rat hippocampal neurons,” Brain Research, vol. 1052, no. 2, pp. 156–162, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Arqué, V. Fotaki, D. Fernández, M. M. de Lagrán, M. L. Arbonés, and M. Dierssen, “Impaired spatial learning strategies and novel object recognition in mice haploinsufficient for the dual specificity tyrosine-regulated kinase-1A (Dyrk1A),” PLoS ONE, vol. 3, no. 7, Article ID e2575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. G. M. Shankar, S. Li, T. H. Mehta et al., “Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory,” Nature Medicine, vol. 14, no. 8, pp. 837–842, 2008.
  25. S. P. Handattu, D. W. Garber, C. E. Monroe et al., “Oral apolipoprotein A-I mimetic peptide improves cognitive function and reduces amyloid burden in a mouse model of Alzheimer's disease,” Neurobiology of Disease, vol. 34, no. 3, pp. 525–534, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Paris, N. J. Ganey, V. Laporte et al., “Reduction of β-amyloid pathology by celastrol in a transgenic mouse model of Alzheimer's disease,” Journal of Neuroinflammation, vol. 7, article 17, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Schulman, “Protein phosphorylation in neuronal plasticity and gene expression,” Current Opinion in Neurobiology, vol. 5, no. 3, pp. 375–381, 1995. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Mangialasche, A. Solomon, B. Winblad, P. Mecocci, and M. Kivipelto, “Alzheimer's disease: clinical trials and drug development,” The Lancet Neurology, vol. 9, no. 7, pp. 702–716, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Hayashi, Y. Ishida, T. Inoue et al., “Treatment of behavioral and psychological symptoms of Alzheimer-type dementia with Yokukansan in clinical practice,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 34, no. 3, pp. 541–545, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Sekiguchi, T. Yamaguchi, M. Tabuchi, Y. Ikarashi, and Y. Kase, “Effects of yokukansan, a traditional Japanese medicine, on aggressiveness induced by intracerebroventricular injection of amyloid β protein into mice,” Phytotherapy Research, vol. 23, no. 8, pp. 1175–1181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Tateno, W. Ukai, T. Ono, S. Saito, E. Hashimoto, and T. Saito, “Neuroprotective effects of Yi-Gan San against beta amyloid-induced cytotoxicity on rat cortical neurons,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 32, no. 7, pp. 1704–1707, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Ai, W. Yang, M. Ye, W. Lu, L. Yao, and J. H. Luo, “Differential regulation of AMPA receptor GluA1 phosphorylation at serine 831 and 845 associated with activation of NMDA receptor subpopulations,” Neuroscience Letters, vol. 497, no. 2, pp. 94–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Suzuki, S. Futami, Y. Igari et al., “A Chinese herbal medicine, choto-san, improves cognitive function and activities of daily living of patients with dementia: a double-blind, randomized, placebo-controlled study,” Journal of the American Geriatrics Society, vol. 53, no. 12, pp. 2238–2240, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. Q. Zhao, Y. Murakami, M. Tohda, R. Obi, Y. Shimada, and K. Matsumoto, “Chotosan, a Kampo formula, ameliorates chronic cerebral hypoperfusion-induced deficits in object recognition behaviors and central cholinergic systems in mice,” Journal of Pharmacological Sciences, vol. 103, no. 4, pp. 360–373, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Mizushima, S. Kan, S. Yoshida, Y. Irie, and Y. Urata, “Effect of Choto-san, a Kampo medicine, on impairment of passive avoidance performance in senescence accelerated mouse (SAM),” Phytotherapy Research, vol. 17, no. 5, pp. 542–545, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. J. K. Wide, K. Hanratty, J. Ting, and L. A. M. Galea, “High level estradiol impairs and low level estradiol facilitates non-spatial working memory,” Behavioural Brain Research, vol. 155, no. 1, pp. 45–53, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. S. C. Mueller, V. Temple, E. Oh et al., “Early androgen exposure modulates spatial cognition in congenital adrenal hyperplasia (CAH),” Psychoneuroendocrinology, vol. 33, no. 7, pp. 973–980, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. A. C. G. Souza, C. A. Brüning, M. R. Leite, G. Zeni, and C. W. Nogueira, “Diphenyl diselenide improves scopolamine-induced memory impairment in mice,” Behavioural Pharmacology, vol. 21, no. 5-6, pp. 556–562, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. P. Hwang, C. H. Yang, S. J. Tsai, and K. M. Liu, “Behavioural disturbances in psychiatric inpatients with dementia of the Alzheimer's type in Taiwan,” International Journal of Geriatric Psychiatry, vol. 12, no. 9, pp. 902–906, 1997.
  40. M. Harciarek and A. Kertesz, “The prevalence of misidentification syndromes in neurodegenerative diseases,” Alzheimer Disease and Associated Disorders, vol. 22, no. 2, pp. 163–169, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. E. K. Perry, B. E. Tomlinson, and G. Blessed, “Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia,” British Medical Journal, vol. 2, no. 6150, pp. 1457–1459, 1978. View at Scopus
  42. M. Rak, M. R. Del Bigio, S. Mai, D. Westaway, and K. M. Gough, “Dense-core and diffuse Aβ plaques in TgCRND8 mice studied with synchrotron FTIR microspectroscopy,” Biopolymers, vol. 87, no. 4, pp. 207–217, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Bussière, F. Bard, R. Barbour et al., “Morphological characterization of Thioflavin-S-positive amyloid plaques in transgenic Alzheimer mice and effect of passive Aβ immunotherapy on their clearance,” American Journal of Pathology, vol. 165, no. 3, pp. 987–995, 2004. View at Scopus
  44. J. M. Mc Donald, G. M. Savva, C. Brayne et al., “The presence of sodium dodecyl sulphate-stable Aβ dimers is strongly associated with Alzheimer-type dementia,” Brain, vol. 133, no. 5, pp. 1328–1341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. T. E. Golde, “The pathogenesis of Alzheimer's disease and the role of Abeta42,” CNS Spectrums, vol. 12, no. 1, supplement1, pp. 4–6, 2007. View at Scopus
  46. E. McGowan, F. Pickford, J. Kim et al., “Aβ42 is essential for parenchymal and vascular amyloid deposition in mice,” Neuron, vol. 47, no. 2, pp. 191–199, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. S. A. Gravina, L. Ho, C. B. Eckman et al., “Amyloid β protein (Aβ) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at Aβ40 or Aβ42(43),” Journal of Biological Chemistry, vol. 270, no. 13, pp. 7013–7016, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Iijima, H. P. Liu, A. S. Chiang, S. A. Hearn, M. Konsolaki, and Y. Zhong, “Dissecting the pathological effects of human Aβ40 and Aβ42 in Drosophila: a potential model for Alzheimer's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 17, pp. 6623–6628, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Bussière, P. D. Friend, N. Sadeghi et al., “Stereologic assessment of the total cortical volume occupied by amyloid deposits and its relationship with cognitive status in aging and Alzheimer's disease,” Neuroscience, vol. 112, no. 1, pp. 75–91, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. A. W. Bero, P. Yan, J. H. Roh et al., “Neuronal activity regulates the regional vulnerability to amyloid-β 2 deposition,” Nature Neuroscience, vol. 14, no. 6, pp. 750–756, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Sano, T. Nakaya, S. Pedrini et al., “Physiological mouse brain Aβ levels are not related to the phosphorylation state of threonine-668 of Alzheimer's APP,” PLoS ONE, vol. 1, no. 1, article e51, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. G. A. Wayman, Y. S. Lee, H. Tokumitsu, A. Silva, and T. R. Soderling, “Calmodulin-kinases: modulators of neuronal development and plasticity,” Neuron, vol. 59, no. 6, pp. 914–931, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. O. S. Rosenberg, S. Deindl, R. J. Sung, A. C. Nairn, and J. Kuriyan, “Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme,” Cell, vol. 123, no. 5, pp. 849–860, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. K. Fukunaga, D. Muller, and E. Miyamoto, “CaM kinase II in long-term potentiation,” Neurochemistry International, vol. 28, no. 4, pp. 343–358, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Sheng, M. A. Thompson, and M. E. Greenberg, “CREB: a Ca2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases,” Science, vol. 252, no. 5011, pp. 1427–1430, 1991. View at Scopus
  56. A. J. Shaywitz and M. E. Greenberg, “CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals,” Annual Review of Biochemistry, vol. 68, pp. 821–861, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. M. R. Montminy, G. A. Gonzalez, and K. K. Yamamoto, “Regulation of cAMP-inducible genes by CREB,” Trends in Neurosciences, vol. 13, no. 5, pp. 184–188, 1990. View at Scopus
  58. T. E. Meyer and J. F. Habener, “Cyclic adenosine 3,5-monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins,” Endocrine Reviews, vol. 14, no. 3, pp. 269–290, 1993. View at Publisher · View at Google Scholar · View at Scopus
  59. D. D. Ginty, A. Bonni, and M. E. Greenberg, “Nerve growth factor activates a ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB,” Cell, vol. 77, no. 5, pp. 713–726, 1994. View at Scopus
  60. F. Gómez-Pinilla, J. R. Huie, Z. Ying et al., “BDNF and learning: evidence that instrumental training promotes learning within the spinal cord by up-regulating BDNF expression,” Neuroscience, vol. 148, no. 4, pp. 893–906, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Xu, Z. P. Pang, O. H. Shin, and T. C. Südhof, “Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release,” Nature Neuroscience, vol. 12, no. 6, pp. 759–766, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. G. Van Den Bogaart, S. Thutupalli, J. H. Risselada et al., “Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation,” Nature Structural and Molecular Biology, vol. 18, no. 7, pp. 805–812, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. T. Manabe, A. Aiba, A. Yamada et al., “Regulation of long-term potentiation by H-Ras through NMDA receptor phosphorylation,” Journal of Neuroscience, vol. 20, no. 7, pp. 2504–2511, 2000. View at Scopus
  64. H. K. Lee, K. Takamiya, J. S. Han et al., “Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory,” Cell, vol. 112, no. 5, pp. 631–643, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. H. Lin, R. Huganir, and D. Liao, “Temporal dynamics of NMDA receptor-induced changes in spine morphology and AMPA receptor recruitment to spines,” Biochemical and Biophysical Research Communications, vol. 316, no. 2, pp. 501–511, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. B. A. Clark and S. G. Cull-Candy, “Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse,” Journal of Neuroscience, vol. 22, no. 11, pp. 4428–4436, 2002. View at Scopus
  67. S. Y. Yu, H. T. OuYang, J. Y. Yang et al., “Subchronic toxicity studies of Radix astragali extract in rats and dogs,” Journal of Ethnopharmacology, vol. 110, no. 2, pp. 352–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. W. Lin and B. H. Chiang, “Anti-tumor activity of the fermentation broth of Cordyceps militaris cultured in the medium of Radix astragali,” Process Biochemistry, vol. 43, no. 3, pp. 244–250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. L. Zhong, Z. F. Wang, and B. J. Xiao, “Research on the antioxidant effect of Enshi banqiao radix codonopsis on brain ischemia/reperfusion (I/R)injury,” Zhongguo Ying Yong Sheng Li Xue Za Zhi, vol. 28, no. 4, pp. 314–316, 2012.
  70. Q. Gao, Z. H. Ji, Y. Yang, R. Cheng, and X. Y. Yu, “Neuroprotective effect of Rhizoma Atractylodis macrocephalae against excitotoxicity-induced apoptosis in cultured cerebral cortical neurons,” Phytotherapy Research, 2012. View at Publisher · View at Google Scholar
  71. I. H. Jung, S. E. Jang, E. H. Joh, J. Chung, M. J. Han, and D. H. Kim, “Lancemaside A isolated from Codonopsis lanceolata and its metabolite echinocystic acid ameliorate scopolamine-induced memory and learning deficits in mice,” Phytomedicine, vol. 20, no. 1, pp. 84–88, 2012.
  72. Z. Lin, Y. Yan, D. Zhu, B. Yu, and Q. Wang, “Protective effects of FBD—an experimental Chinese traditional medicinal formula on memory dysfunction in mice induced by cerebral ischemia-reperfusion,” Journal of Ethnopharmacology, vol. 97, no. 3, pp. 477–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. Z. Li, L. Zhu, H. Zhang et al., “Protective effect of a polysaccharide from stem of Codonopsis pilosula against renal ischemia/reperfusion injury in rats,” Carbohydrate Polymers, vol. 90, no. 4, pp. 1739–1743, 2012.
  74. J. G. Choi, M. Moon, H. U. Jeong, M. C. Kim, S. Y. Kim, and M. S. Oh, “Cistanches Herba enhances learning and memory by inducing nerve growth factor,” Behavioural Brain Research, vol. 216, no. 2, pp. 652–658, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. B. S. Koo, Y. K. Kim, K. S. Park, K. H. Chung, and C. H. Kim, “Attenuating effect of a traditional Korean formulation, Paeng-Jo-Yeon-Nyeon-Baek-Ja-In-Hwan (PJBH), on hydrogen peroxide-induced injury in PC12 cells,” Phytotherapy Research, vol. 18, no. 6, pp. 488–493, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. S. W. Kim, S. H. Yoo, H. J. Lee et al., “Cistanches herba induces testis cytotoxicity in male mice,” Bulletin of Environmental Contamination and Toxicology, vol. 88, no. 1, pp. 112–117, 2012.