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Evidence-Based Complementary and Alternative Medicine
Volume 2014, Article ID 327294, 9 pages
http://dx.doi.org/10.1155/2014/327294
Research Article

Danggui-Shaoyao-San Improves Learning and Memory in Female SAMP8 via Modulation of Estradiol

Beijing Institute of Pharmacology and Toxicology, Tai Ping Road 27, Beijing 100850, China

Received 24 November 2013; Revised 22 January 2014; Accepted 6 February 2014; Published 16 March 2014

Academic Editor: Jing Yu Yang

Copyright © 2014 Yan Huang 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. J. L. Cummings, “Alzheimer's disease,” The New England Journal of Medicine, vol. 351, no. 1, pp. 56–67, 2004. View at Google Scholar
  2. K. Andersen, L. J. Launer, M. E. Dewey et al., “Gender differences in the incidence of AD and vascular dementia: The EURODEM Studies,” Neurology, vol. 53, no. 9, pp. 1992–1997, 1999. View at Google Scholar · View at Scopus
  3. A. F. Jorm and D. Jolley, “The incidence of dementia: a meta-analysis,” Neurology, vol. 51, no. 3, pp. 728–733, 1998. View at Google Scholar · View at Scopus
  4. A. Ruitenberg, A. Ott, J. C. Van Swieten, A. Hofman, and M. M. B. Breteler, “Incidence of dementia: does gender make a difference?” Neurobiology of Aging, vol. 22, no. 4, pp. 575–580, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. L. L. Barnes, R. S. Wilson, J. L. Bienias, J. A. Schneider, D. A. Evans, and D. A. Bennett, “Sex differences in the clinical manifestations of Alzheimer disease pathology,” Archives of General Psychiatry, vol. 62, no. 6, pp. 685–691, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. E. H. Corder, E. Ghebremedhin, M. G. Taylor, D. R. Thal, T. G. Ohm, and H. Braak, “The biphasic relationship between regional brain senile plaque and neurofibrillary tangle distributions: modification by age, sex, and APOE polymorphism,” Annals of the New York Academy of Sciences, vol. 1019, pp. 24–28, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. D. F. Swaab, W. C. J. Chung, F. P. M. Kruijver, M. A. Hofman, and T. A. Ishunina, “Structural and functional sex differences in the human hypothalamus,” Hormones and Behavior, vol. 40, no. 2, pp. 93–98, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. J. G. Buckwalter, E. Sobel, M. E. Dunn, M. M. Diz, and V. W. Henderson, “Gender differences on a brief measure of cognitive functioning in Alzheimer's disease,” Archives of Neurology, vol. 50, no. 7, pp. 757–760, 1993. View at Google Scholar · View at Scopus
  9. V. W. Henderson and J. G. Buckwalter, “Cognitive deficits of men and women with Alzheimer's disease,” Neurology, vol. 44, no. 1, pp. 90–96, 1994. View at Google Scholar · View at Scopus
  10. E. Sinforiani, A. Citterio, C. Zucchella et al., “Impact of gender differences on the outcome of alzheimer's disease,” Dementia and Geriatric Cognitive Disorders, vol. 30, no. 2, pp. 147–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. J. J. Manly, C. A. Merchant, D. M. Jacobs et al., “Endogenous estrogen levels and Alzheimer's disease among postmenopausal women,” Neurology, vol. 54, no. 4, pp. 833–837, 2000. View at Google Scholar · View at Scopus
  12. E. R. Rosario, L. Chang, E. H. Head, F. Z. Stanczyk, and C. J. Pike, “Brain levels of sex steroid hormones in men and women during normal aging and in Alzheimer's disease,” Neurobiology of Aging, vol. 32, no. 4, pp. 604–613, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. X. Yue, M. Lu, T. Lancaster et al., “Brain estrogen deficiency accelerates Aβ plaque formation in an Alzheimer's disease animal model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 52, pp. 19198–19203, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. J. C. Carroll and C. J. Pike, “Selective estrogen receptor modulators differentially regulate Alzheimer-like changes in female 3xTg-AD mice,” Endocrinology, vol. 149, no. 5, pp. 2607–2611, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. J. A. Levin-Allerhand, C. E. Lominska, J. Wang, and J. D. Smith, “17α-estradiol and 17β-estradiol treatments are effective in lowering cerebral amyloid-β levels in AβPPSWE transgenic mice,” Journal of Alzheimer's Disease, vol. 4, no. 6, pp. 449–457, 2002. View at Google Scholar · View at Scopus
  16. S. S. Petanceska, V. Nagy, D. Frail, and S. Gandy, “Ovariectomy and 17β-estradiol modulate the levels of Alzheimer's amyloid β peptides in brain,” Neurology, vol. 54, no. 12, pp. 2212–2217, 2000. View at Google Scholar · View at Scopus
  17. H. Xu, R. Wang, Y.-W. Zhang, and X. Zhang, “Estrogen, β-amyloid metabolism/trafficking, and Alzheimer's disease,” Annals of the New York Academy of Sciences, vol. 1089, pp. 324–342, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Fujii, “Herbal factors in the treatment of autoimmunity-related habitual abortion,” Vitamins and Hormones, vol. 65, pp. 333–344, 2002. View at Google Scholar · View at Scopus
  19. N. Hagino, “An overview of Kampo medicine: Toki—Shakuyaku—San (TJ—23),” Phytotherapy Research, vol. 7, no. 6, pp. 391–394, 1993. View at Google Scholar
  20. S. Higaki, T. Toyomoto, and M. Morohashi, “Seijo-bofu-to, Jumi-haidoku-to and Toki-shakuyaku-san suppress rashes and incidental symptoms in acne patients,” Drugs under Experimental and Clinical Research, vol. 28, no. 5, pp. 193–196, 2002. View at Google Scholar · View at Scopus
  21. K. Inanaga, “Aging in brain and mind–drug therapy for patients with Behavioral and Psychological Symptoms of Dementia (BPSD),” Seishin Shinkeigaku Zasshi, vol. 109, no. 7, pp. 703–708, 2007. View at Google Scholar · View at Scopus
  22. N. Kotani, T. Oyama, I. Sakai et al., “Analgesic effect of a herbal medicine for treatment of primary dysmenorrhea -A Double-Blind Study,” American Journal of Chinese Medicine, vol. 25, no. 2, pp. 205–212, 1997. View at Google Scholar · View at Scopus
  23. M. H. Chung, S. Suzuki, T. Nishihara, and M. Hattori, “Estrogenic effects of a Kampo formula, Tokishakuyakusan, in parous ovariectomized rats,” Biological and Pharmaceutical Bulletin, vol. 31, no. 6, pp. 1145–1149, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Usuki, “Tokishakuyakusan stimulates progesterone and estradiol-17 beta production by rat granulosa cells and progesterone, testosterone and estradiol-17 beta by the residual portion of the follicle in vitro,” American Journal of Chinese Medicine, vol. 19, no. 2, pp. 155–161, 1991. View at Google Scholar · View at Scopus
  25. N. Mizushima, “Effects of TJ-23 (Toki-shakuyaku-san) on senile dementia,” Japanese Medical and Pharmaceutical Society for WAKAN-YAKU, vol. 6, pp. 456–457, 1989. View at Google Scholar
  26. N. Egashira, K. Iwasaki, Y. Akiyoshi et al., “Protective effect of Toki-shakuyaku-san on amyloid β25-35- induced neuronal damage in cultured rat cortical neurons,” Phytotherapy Research, vol. 19, no. 5, pp. 450–453, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Itoh, S. Michijiri, S. Murai et al., “Regulatory effect of danggui-shaoyao-san on central cholinergic nervous system dysfunction in mice,” American Journal of Chinese Medicine, vol. 24, no. 3-4, pp. 205–217, 1996. View at Google Scholar · View at Scopus
  28. Y. Kitabayashi, K. Shibata, T. Nakamae, J. Narumoto, and K. Fukui, “Effect of traditional Japanese herbal medicine toki-shakuyaku-san for mild cognitive impairment: SPECT Study,” Psychiatry and Clinical Neurosciences, vol. 61, no. 4, pp. 447–448, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. 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
  30. Y. Ueda, M. Komatsu, and M. Hiramatsu, “Free radical scavenging activity of the Japanese herbal medicine Toki-Shakuyaku-San (TJ-23) and its effect on superoxide dismutase activity, lipid peroxides, glutamate, and monoamine metabolites in aged rat brain,” Neurochemical Research, vol. 21, no. 8, pp. 909–914, 1996. View at Google Scholar · View at Scopus
  31. Z.-Y. Hu, G. Liu, X.-R. Cheng et al., “JD-30, an active fraction extracted from Danggui-Shaoyao-San, decreases β-amyloid content and deposition, improves LTP reduction and prevents spatial cognition impairment in SAMP8 mice,” Experimental Gerontology, vol. 47, no. 1, pp. 14–22, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. Z.-Y. Hu, G. Liu, H. Yuan et al., “Danggui-Shaoyao-San and its active fraction JD-30 improve Aβ-induced spatial recognition deficits in mice,” Journal of Ethnopharmacology, vol. 128, no. 2, pp. 365–372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Huang, W. Zhou, and Y. Zhang, “Bright lighting conditions during testing increase thigmotaxis and impair water maze performance in BALB/c mice,” Behavioural Brain Research, vol. 226, no. 1, pp. 26–31, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Marzinzig, A. K. Nussler, J. Stadler et al., “Improved methods to measure end products of nitric oxide in biological fluids: nitrite, nitrate, and S-nitrosothiols,” Nitric Oxide, vol. 1, no. 2, pp. 177–189, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. P. L. Feldman, “The surprising life of nitric oxide,” Chemical and Engineering News, vol. 71, no. 51, pp. 26–38, 1993. View at Google Scholar · View at Scopus
  36. S. Moncada, R. M. J. Palmer, and E. A. Higgs, “Nitric oxide: physiology, pathophysiology, and pharmacology,” Pharmacological Reviews, vol. 43, no. 2, pp. 109–142, 1991. View at Google Scholar · View at Scopus
  37. A. M. Rao, A. Dogan, J. F. Hatcher, and R. J. Dempsey, “Fluorometric assay of nitrite and nitrate in brain tissue after traumatic brain injury and cerebral ischemia,” Brain Research, vol. 793, no. 1-2, pp. 265–270, 1998. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Hashimoto, A. Sawa, and M. Iyo, “Increased levels of glutamate in brains from patients with mood disorders,” Biological Psychiatry, vol. 62, no. 11, pp. 1310–1316, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Nomura and Y. Okuma, “Age-related defects in lifespan and learning ability in SAMP8 mice,” Neurobiology of Aging, vol. 20, no. 2, pp. 111–115, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Nomura, Y. Yamanaka, Y. Kitamura et al., “Senescence-accelerated mouse. Neurochemical studies on aging,” Annals of the New York Academy of Sciences, vol. 786, pp. 410–418, 1996. View at Google Scholar · View at Scopus
  41. G.-H. Chen, Y.-J. Wang, X.-M. Wang, and J.-N. Zhou, “Accelerated senescence prone mouse-8 shows early onset of deficits in spatial learning and memory in the radial six-arm water maze,” Physiology and Behavior, vol. 82, no. 5, pp. 883–890, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Takeda, “Senescence-accelerated mouse (SAM): a biogerontological resource in aging research,” Neurobiology of Aging, vol. 20, no. 2, pp. 105–110, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Miyamoto, “Characteristics of age-related behavioral changes in senescence- accelerated Mouse SAMP8 and SAMP10,” Experimental Gerontology, vol. 32, no. 1-2, pp. 139–148, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Takeda, “Senescence-accelerated mouse (SAM) with special references to neurodegeneration models, SAMP8 and SAMP10 mice,” Neurochemical Research, vol. 34, no. 4, pp. 639–659, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Okuma and Y. Nomura, “Senescence-accelerated mouse (SAM) as an animal model of senile dementia: pharmacological, neurochemical and molecular biological approach,” Japanese Journal of Pharmacology, vol. 78, no. 4, pp. 399–404, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Hardy and D. J. Selkoe, “The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics,” Science, vol. 297, no. 5580, pp. 353–356, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. J. C. Carroll and E. R. Rosario, “The potential use of hormone-based therapeutics for the treatment of Alzheimer's disease,” Current Alzheimer Research, vol. 9, no. 1, pp. 18–34, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. C. J. Pike, J. C. Carroll, E. R. Rosario, and A. M. Barron, “Protective actions of sex steroid hormones in Alzheimer's disease,” Frontiers in Neuroendocrinology, vol. 30, no. 2, pp. 239–258, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Amtul, L. Wang, D. Westaway, and R. F. Rozmahel, “Neuroprotective mechanism conferred by 17beta-estradiol on the biochemical basis of Alzheimer's disease,” Neuroscience, vol. 169, no. 2, pp. 781–786, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Desdouits-Magnen, F. Desdouits, S. Takeda et al., “Regulation of secretion of Alzheimer amyloid precursor protein by the mitogen-activated protein kinase cascade,” Journal of Neurochemistry, vol. 70, no. 2, pp. 524–530, 1998. View at Google Scholar · View at Scopus
  51. A. B. Jaffe, C. D. Toran-Allerand, P. Greengard, and S. E. Gandy, “Estrogen regulates metabolism of Alzheimer amyloid β precursor protein,” Journal of Biological Chemistry, vol. 269, no. 18, pp. 13065–13068, 1994. View at Google Scholar · View at Scopus
  52. D. Manthey, S. Heck, S. Engert, and C. Behl, “Estrogen induces a rapid secretion of amyloid β precursor protein via the mitogen-activated protein kinase pathway,” European Journal of Biochemistry, vol. 268, no. 15, pp. 4285–4291, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. M. K. Thakur and S. T. Mani, “Estradiol regulates APP mRNA alternative splicing in the mice brain cortex,” Neuroscience Letters, vol. 381, no. 1-2, pp. 154–157, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. B. M. Cooke and C. S. Woolley, “Gonadal hormone modulation of dendrites in the mammalian CNS,” Journal of Neurobiology, vol. 64, no. 1, pp. 34–46, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. M. R. Foy, M. Baudry, G. K. Akopian, and R. F. Thompson, “Regulation of hippocampal synaptic plasticity by estrogen and progesterone,” Vitamins and Hormones, vol. 82, pp. 219–239, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. R. B. Gibbs, “Estrogen therapy and cognition: a review of the cholinergic hypothesis,” Endocrine Reviews, vol. 31, no. 2, pp. 224–253, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. J. W. Simpkins, K. D. Yi, S.-H. Yang, and J. A. Dykens, “Mitochondrial mechanisms of estrogen neuroprotection,” Biochimica et Biophysica Acta, vol. 1800, no. 10, pp. 1113–1120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Suzuki, C. M. Brown, and P. M. Wise, “Neuroprotective effects of estrogens following ischemic stroke,” Frontiers in Neuroendocrinology, vol. 30, no. 2, pp. 201–211, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. V. W. Henderson, A. Paganini-Hill, C. K. Emanuel, M. E. Dunn, and J. G. Buckwalter, “Estrogen replacement therapy in older women: Comparisons between Alzheimer's disease cases and nondemented control subjects,” Archives of Neurology, vol. 51, no. 9, pp. 896–900, 1994. View at Google Scholar · View at Scopus
  60. E. Hogervorst, M. Boshuisen, W. Riedel, C. Willeken, and J. Jolles, “The effect of hormone replacement therapy on cognitive function in elderly women,” Psychoneuroendocrinology, vol. 24, no. 1, pp. 43–68, 1999. View at Publisher · View at Google Scholar · View at Scopus
  61. E. S. Leblanc, J. Janowsky, B. K. S. Chan, and H. D. Nelson, “Hormone replacement therapy and cognition: systematic review and meta-analysis,” Journal of the American Medical Association, vol. 285, no. 11, pp. 1489–1499, 2001. View at Google Scholar · View at Scopus
  62. A. Paganini-Hill, “Oestrogen replacement therapy and Alzheimer's disease,” British Journal of Obstetrics and Gynaecology, Supplement, vol. 103, no. 13, pp. 80–86, 1996. View at Google Scholar · View at Scopus
  63. P. P. Zandi, M. C. Carlson, B. L. Plassman et al., “Hormone replacement therapy and incidence of Alzheimer disease in older women: The Cache County Study,” Journal of the American Medical Association, vol. 288, no. 17, pp. 2123–2129, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. E. M. Schuman and D. V. Madison, “A requirement for the intercellular messenger nitric oxide in long-term potentiation,” Science, vol. 254, no. 5037, pp. 1503–1506, 1991. View at Google Scholar · View at Scopus
  65. B. Jeynes and J. Provias, “Significant negative correlations between capillary expressed eNOS and Alzheimer lesion burden,” Neuroscience Letters, vol. 463, no. 3, pp. 244–248, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Hisamoto and J. R. Bender, “Vascular cell signaling by membrane estrogen receptors,” Steroids, vol. 70, no. 5–7, pp. 382–387, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. Y. Zhao, G. Zhou, J. Wang et al., “Paeoniflorin protects against ANIT-induced cholestasis by ameliorating oxidative stress in rats,” Food and Chemical Toxicology, vol. 58, pp. 242–248, 2013. View at Google Scholar
  68. K. N. Nam, C. G. Yae, J. W. Hong et al., “Paeoniflorin, a monoterpene glycoside, attenuates lipopolysaccharide-induced neuronal injury and brain microglial inflammatory response,” Biotechnology Letters, vol. 35, no. 8, pp. 1183–1189, 2013. View at Google Scholar
  69. R. G. M. Morris, E. Anderson, G. S. Lynch, and M. Baudry, “Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5,” Nature, vol. 319, no. 6056, pp. 774–776, 1986. View at Google Scholar · View at Scopus
  70. J. Z. Tsien, P. T. Huerta, and S. Tonegawa, “The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory,” Cell, vol. 87, no. 7, pp. 1327–1338, 1996. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Yashiro and B. D. Philpot, “Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity,” Neuropharmacology, vol. 55, no. 7, pp. 1081–1094, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Rupsingh, M. Borrie, M. Smith, J. L. Wells, and R. Bartha, “Reduced hippocampal glutamate in Alzheimer disease,” Neurobiology of Aging, vol. 32, no. 5, pp. 802–810, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Hashimoto, T. Fukushima, E. Shimizu et al., “Possible role of D-serine in the pathophysiology of Alzheimer's disease,” Progress in Neuro-Psychopharmacology & Biological Psychiatry, vol. 28, no. 2, pp. 385–388, 2004. View at Google Scholar
  74. S. Yang, H. Qiao, L. Wen, W. Zhou, and Y. Zhang, “D-Serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8,” Neuroscience Letters, vol. 379, no. 1, pp. 7–12, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. Y. Huang, H. Zhang, S. Yang, H. Qiao, W. Zhou, and Y. Zhang, “Liuwei Dihuang decoction facilitates the induction of long-term potentiation (LTP) in senescence accelerated mouse/prone 8 (SAMP8) hippocampal slices by inhibiting voltage-dependent calcium channels (VDCCs) and promoting N-methyl-D-aspartate receptor (NMDA) receptors,” Journal of Ethnopharmacology, vol. 140, no. 2, pp. 384–390, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Harada, K. Nakato, J. Yarimizu et al., “A novel glycine transporter-1 (GlyT1) inhibitor, ASP2535 (4-[3-isopropyl-5-(6-phenyl-3-pyridyl)-4H-1,2,4-triazol-4-yl]-2,1,3-benzoxadiazole), improves cognition in animal models of cognitive impairment in schizophrenia and Alzheimer's disease,” European Journal of Pharmacology, vol. 685, no. 1–3, pp. 59–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Komatsu, Y. Ueda, and M. Hiramatsu, “Different changes in concentrations of monoamines and their metabolites and amino acids in various brain regions by the herbal medicine/Toki- Shakuyaku-San between female and male senescence-accelerated mice (SAMP8),” Neurochemical Research, vol. 24, no. 7, pp. 825–831, 1999. View at Publisher · View at Google Scholar · View at Scopus
  78. G. L. Kobertson, D. D. Hagerman, G. S. Richardson, and C. A. Villee, “Estradiol stimulation of glycine incorporation by human endometrium in tissue culture,” Science, vol. 134, no. 3494, pp. 1986–1987, 1961. View at Google Scholar · View at Scopus